Members of the genus Neisseria include pathogens causing important human diseases such as meningitis, septicaemia, gonorrhoea and pelvic inflammatory disease syndrome. Neisseriae are found on the exposed epithelia of the upper respiratory tract and the urogenital tract. Colonisation of these exposed epithelia is dependent on a repertoire of diverse bacterial molecules, extending not only from the surface of the bacteria but also found within the outer membrane. During invasive disease, pathogenic Neisseriae also interact with immune effector cells, vascular endothelia and the meninges. Neisseria adhesion involves the interplay of these multiple surface factors and in this review we discuss the structure and function of these important molecules and the nature of the host cell receptors and mechanisms involved in their recognition. We also describe the current status for recently identified Neisseria adhesins. Understanding the biology of Neisseria adhesins has an impact not only on the development of new vaccines but also in revealing fundamental knowledge about human biology.
References
[1]
Weichselbaum, A. Ueber die Aetiologie der akuten meningitis cerebro-spinalis. Fortschr. Med. 1887, 5, 573–583; 620–626.
[2]
Marchiafava, E.; Celli, A. Spra i micrococchi della meningite cerebrospinale epidemica. Gazzetta Osp. 1884, 5, 59.
[3]
Heubner, J.O.L. Beobachtungen und versuche über den meningokokkus intracellularis (Weichselbaum-Jaeger). Jb Kinderheilk 1896, 43, 1–22.
[4]
Kiefer, F. Zur differentialdiagnose des erregers der epidemischen cerebrospinal-meningitis und der gonorrhoe. Berl. Klin. Wochenschr. 1896, 33, 628–630.
[5]
Goodwin, M.E.; von Sholly, A.I. The frequent occurrence of meningococci in the nasal cavities of meningitis patients and of those in direct contact with them. Public Health Pap. Rep. 1905, 31, 21–34.
Jung, J.J.; Vu, D.M.; Clark, B.; Keller, F.G.; Spearman, P. Neisseria sicca/subflava bacteremia presenting as cutaneous nodules in an immunocompromised host. Pediatr. Infect. Dis. J. 2009, 28, 661–663, doi:10.1097/INF.0b013e318196bd48.
[8]
Hsiao, J.F.; Lee, M.H.; Chia, J.H.; Ho, W.J.; Chu, J.J.; Chu, P.H. Neisseria elongata endocarditis complicated by brain embolism and abscess. J. Med. Microbiol. 2008, 57, 376–381, doi:10.1099/jmm.0.47493-0.
[9]
Vandamme, P.; Holmes, B.; Bercovier, H.; Coenye, T. Classification of centers for disease control group eugonic fermenter (EF)-4a and EF-4b as Neisseria animaloris sp. nov. and Neisseria zoodegmatis sp . nov., respectively. Int. J. Syst. Evol. Microbiol. 2006, 56, 1801–1805, doi:10.1099/ijs.0.64142-0.
[10]
Han, X.Y.; Hong, T.; Falsen, E. Neisseria bacilliformis sp. nov. isolated from human infections. J. Clin. Microbiol. 2006, 44, 474–479, doi:10.1128/JCM.44.2.474-479.2006.
[11]
Masliah-Planchon, J.; Breton, G.; Jarlier, V.; Simon, A.; Benveniste, O.; Herson, S.; Drieux, L. Endocarditis due to Neisseria bacilliformis in a patient with a bicuspid aortic valve. J. Clin. Microbiol. 2009, 47, 1973–1975, doi:10.1128/JCM.00026-09.
[12]
Abandeh, F.I.; Balada-Llasat, J.M.; Pancholi, P.; Risaliti, C.M.; Maher, W.E.; Bazan, J.A. A rare case of Neisseria bacilliformis native valve endocarditis. Diagn. Microbiol. Infect. Dis. 2012, 73, 378–379, doi:10.1016/j.diagmicrobio.2012.05.006.
[13]
Lee, M.Y.; Park, E.G.; Choi, J.Y.; Cheong, H.S.; Chung, D.R.; Peck, K.R.; Song, J.H.; Ko, K.S. “Neisseria skkuensis” sp. nov., isolated from the blood of a diabetic patient with a foot ulcer. J. Med. Microbiol. 2010, 59, 856–859, doi:10.1099/jmm.0.018150-0.
Wolfgang, W.J.; Passaretti, T.V.; Jose, R.; Cole, J.; Coorevits, A.; Carpenter, A.N.; Jose, S.; van Landschoot, A.; Izard, J.; Kohlerschmidt, D.J.; et al. Neisseria oralis sp. nov. isolated from healthy gingival plaque and clinical samples. Int. J. Syst. Evol. Microbiol. 2013, 63, 1323–1328, doi:10.1099/ijs.0.041731-0.
[16]
Veron, M.; Lenvoise-Furet, A.; Coustere, C.; Ged, C.; Grimont, F. Relatedness of three species of “false Neisseriae,” Neisseria caviae, Neisseria cuniculi, and Neisseria ovis, by DNA-DNA hybridizations and fatty acid analysis. Int. J. Syst. Bacteriol. 1993, 43, 210–220, doi:10.1099/00207713-43-2-210.
[17]
Initiative for Vaccine Research (IVR). Bacterial Infections—Meningococcal Disease. Available online: http://www.who.int/vaccine_research/diseases/soa_bacterial/en/index1.html/ (accessed on 1 July 2013).
Vieusseux, M. Memoire sur la maladie qui a regne a Geneve au printemps de 1805. J. Med. Chir. Pharmacol. 1805, 11, 163–182.
[20]
Wolf, R.E.; Birbara, C.A. Meningococcal infections at an army training center. Am. J. Med. 1968, 44, 243–255, doi:10.1016/0002-9343(68)90156-3.
[21]
Apicella, M.A. Neisseriameningitidis. In Mandell, Douglas, and Bennett’s Principles and Practice of Infectious Diseases, 7th ed.; Mandell, G.L., Douglas, R.G., Bennett, J.E., Dolin, R., Eds.; Elsevier/Churchill Livingstone: Philadelphia, PA, USA, 2010. Chapter 211; pp. 2737–2752.
[22]
Brandtzaeg, P.; van Deuren, M. Classification and Pathogenesis of Meningococcal Infections. In Neisseria meningitidis: Advanced Methods and Protocols; Christodoulides, M., Ed.; Humana Press: New York, NY, USA, 2012. Chapter 4; pp. 21–35.
[23]
Stephens, D.S.; Greenwood, B.; Brandtzaeg, P. Epidemic meningitis, meningococcaemia, and Neisseria meningitidis. Lancet 2007, 369, 2196–2210, doi:10.1016/S0140-6736(07)61016-2.
[24]
Rosenstein, N.E.; Perkins, B.A.; Stephens, D.S.; Popovic, T.; Hughes, J.M. Meningococcal disease. N. Engl. J. Med. 2001, 344, 1378–1388, doi:10.1056/NEJM200105033441807.
[25]
Brasier, A.R.; Macklis, J.D.; Vaughan, D.; Warner, L.; Kirshenbaum, J.M. Myopericarditis as an initial presentation of meningococcemia. Unusual manifestation of infection with serotype W135. Am. J. Med. 1987, 82, 641–644, doi:10.1016/0002-9343(87)90115-X.
[26]
Varon, J.; Chen, K.; Sternbach, G.L. Rupert waterhouse and carl friderichsen: Adrenal apoplexy. J. Emerg. Med. 1998, 16, 643–647, doi:10.1016/S0736-4679(98)00061-4.
[27]
Girard, M.P.; Preziosi, M.P.; Aguado, M.T.; Kieny, M.P. A review of vaccine research and development: Meningococcal disease. Vaccine 2006, 24, 4692–4700, doi:10.1016/j.vaccine.2006.03.034.
Koomen, I.; van Furth, A.M.; Kraak, M.A.; Grobbee, D.E.; Roord, J.J.; Jennekens-Schinkel, A. Neuropsychology of academic and behavioural limitations in school-age survivors of bacterial meningitis. Dev. Med. Child. Neurol. 2004, 46, 724–732.
[30]
Initiative for Vaccine Research (IVR). Sexually Transmitted Diseases—Gonorrhoea. Available online: http://www.who.int/vaccine_research/diseases/soa_std/en/index2.html/ (accessed on 1 July 2013).
[31]
Marrazzo, J.M.; Handsfield, H.H.; Sparling, F.P. Neisseriagonorrhoeae. In Mandell, Douglas, and Bennett’s Principles and Practice of Infectious Diseases, 7th ed.; Mandell, G.L., Douglas, R.G., Bennett, J.E., Dolin, R., Eds.; Elsevier/Churchill Livingstone: Philadelphia, PA, USA, 2010. Chapter 212; pp. 2753–2769.
[32]
Miller, W.C.; Ford, C.A.; Morris, M.; Handcock, M.S.; Schmitz, J.L.; Hobbs, M.M.; Cohen, M.S.; Harris, K.M.; Udry, J.R. Prevalence of chlamydial and gonococcal infections among young adults in the United States. JAMA 2004, 291, 2229–2236, doi:10.1001/jama.291.18.2229.
[33]
Kahn, R.H.; Mosure, D.J.; Blank, S.; Kent, C.K.; Chow, J.M.; Boudov, M.R.; Brock, J.; Tulloch, S. Chlamydia trachomatis and Neisseria gonorrhoeae prevalence and coinfection in adolescents entering selected US juvenile detention centers, 1997–2002. Sex. Transm. Dis. 2005, 32, 255–259, doi:10.1097/01.olq.0000158496.00315.04.
[34]
Fleming, D.T.; Wasserheit, J.N. From epidemiological synergy to public health policy and practice: The contribution of other sexually transmitted diseases to sexual transmission of HIV infection. Sex. Transm. Infect. 1999, 75, 3–17, doi:10.1136/sti.75.1.3.
[35]
CDC. Update to CDC’s Sexually transmitted diseases treatment guidelines, 2010: Oral cephalosporins no longer a recommended treatment for gonococcal infections. MMWR Morb. Mortal. Wkly. Rep. 2012, 61, 590–594.
[36]
Campos-Outcalt, D. CDC update on gonorrhea: Expand treatment to limit resistance. J. Fam. Pract. 2011, 60, 736–740.
[37]
Strom, M.S.; Lory, S. Structure-function and biogenesis of the type IV pili. Annu. Rev. Microbiol. 1993, 47, 565–596, doi:10.1146/annurev.mi.47.100193.003025.
[38]
Merz, A.J.; So, M.; Sheetz, M.P. Pilus retraction powers bacterial twitching motility. Nature 2000, 407, 98–102, doi:10.1038/35024105.
[39]
Fussenegger, M.; Rudel, T.; Barten, R.; Ryll, R.; Meyer, T.F. Transformation competence and type-4 pilus biogenesis in Neisseria gonorrhoeae—A review. Gene 1997, 192, 125–134, doi:10.1016/S0378-1119(97)00038-3.
[40]
Virji, M.; Heckels, J.E. Antigenic cross-reactivity of Neisseria pili: Investigations with type- and species-specific monoclonal antibodies. J. Gen. Microbiol. 1983, 129, 2761–2768.
[41]
Perry, A.C.; Nicolson, I.J.; Saunders, J.R. Neisseria meningitidis C114 contains silent, truncated pilin genes that are homologous to Neisseria gonorrhoeae pil sequences. J. Bacteriol. 1988, 170, 1691–1697.
Virji, M.; Heckels, J.E.; Potts, W.J.; Hart, C.A.; Saunders, J.R. Identification of epitopes recognized by monoclonal antibodies SM1 and SM2 which react with all pili of Neisseria gonorrhoeae but which differentiate between two structural classes of pili expressed by Neisseria meningitidis and the distribution of their encoding sequences in the genomes of Neisseria spp. J. Gen. Microbiol. 1989, 135, 3239–3251.
[44]
Aho, E.L.; Keating, A.M.; McGillivray, S.M. A comparative analysis of pilin genes from pathogenic and nonpathogenic Neisseria species. Microb. Pathog. 2000, 28, 81–88, doi:10.1006/mpat.1999.0325.
Higashi, D.L.; Biais, N.; Weyand, N.J.; Agellon, A.; Sisko, J.L.; Brown, L.M.; So, M. N. elongata produces type IV pili that mediate interspecies gene transfer with N. gonorrhoeae. PLoS One 2011, 6, e21373:1–e21373:7.
[47]
Hagblom, P.; Segal, E.; Billyard, E.; So, M. Intragenic recombination leads to pilus antigenic variation in Neisseria gonorrhoeae. Nature 1985, 315, 156–158, doi:10.1038/315156a0.
[48]
Haas, R.; Meyer, T.F. The repertoire of silent pilus genes in Neisseria gonorrhoeae: Evidence for gene conversion. Cell 1986, 44, 107–115, doi:10.1016/0092-8674(86)90489-7.
[49]
Segal, E.; Hagblom, P.; Seifert, H.S.; So, M. Antigenic variation of gonococcal pilus involves assembly of separated silent gene segments. Proc. Natl. Acad. Sci. USA 1986, 83, 2177–2181, doi:10.1073/pnas.83.7.2177.
[50]
Perry, A.C.; Hart, C.A.; Nicolson, I.J.; Heckels, J.E.; Saunders, J.R. Inter-strain homology of pilin gene sequences in Neisseria meningitidis isolates that express markedly different antigenic pilus types. J. Gen. Microbiol. 1987, 133, 1409–1418.
[51]
Carbonnelle, E.; Hill, D.J.; Morand, P.; Griffiths, N.J.; Bourdoulous, S.; Murillo, I.; Nassif, X.; Virji, M. Meningococcal interactions with the host. Vaccine 2009, 27, B78–B89, doi:10.1016/j.vaccine.2009.04.069.
[52]
Tinsley, C.R.; Heckels, J.E. Variation in the expression of pili and outer membrane protein by Neisseria meningitidis during the course of meningococcal infection. J. Gen. Microbiol. 1986, 132, 2483–2490.
[53]
Criss, A.K.; Kline, K.A.; Seifert, H.S. The frequency and rate of pilin antigenic variation in Neisseria gonorrhoeae. Mol. Microbiol. 2005, 58, 510–519, doi:10.1111/j.1365-2958.2005.04838.x.
[54]
Helm, R.A.; Seifert, H.S. Frequency and rate of pilin antigenic variation of Neisseria meningitidis. J. Bacteriol. 2010, 192, 3822–3823, doi:10.1128/JB.00280-10.
[55]
Nassif, X.; Beretti, J.L.; Lowy, J.; Stenberg, P.; Ogaora, P.; Pfeifer, J.; Normark, S.; So, M. Roles of pilin and PilC in adhesion of Neisseria-meningitidis to human epithelial and endothelial cells. Proc. Natl. Acad. Sci. USA 1994, 91, 3769–3773.
[56]
Parge, H.E.; McRee, D.E.; Capozza, M.A.; Bernstein, S.L.; Getzoff, E.D.; Tainer, J.A. Three dimensional structure of bacterial pili. Antonie Van Leeuwenhoek 1987, 53, 447–453, doi:10.1007/BF00415501.
[57]
Parge, H.E.; Bernstein, S.L.; Deal, C.D.; McRee, D.E.; Christensen, D.; Capozza, M.A.; Kays, B.W.; Fieser, T.M.; Draper, D.; So, M. Biochemical purification and crystallographic characterization of the fiber-forming protein pilin from Neisseria gonorrhoeae. J. Biol. Chem. 1990, 265, 2278–2285.
[58]
Parge, H.E.; Forest, K.T.; Hickey, M.J.; Christensen, D.A.; Getzoff, E.D.; Tainer, J.A. Structure of the fibre-forming protein pilin at 2.6 A resolution. Nature 1995, 378, 32–38, doi:10.1038/378032a0.
[59]
Forest, K.T.; Dunham, S.A.; Koomey, M.; Tainer, J.A. Crystallographic structure reveals phosphorylated pilin from Neisseria: Phosphoserine sites modify type IV pilus surface chemistry and fibre morphology. Mol. Microbiol. 1999, 31, 743–752, doi:10.1046/j.1365-2958.1999.01184.x.
[60]
Craig, L.; Volkmann, N.; Arvai, A.S.; Pique, M.E.; Yeager, M.; Egelman, E.H.; Tainer, J.A. Type IV pilus structure by cryo-electron microscopy and crystallography: Implications for pilus assembly and functions. Mol. Cell. 2006, 23, 651–662, doi:10.1016/j.molcel.2006.07.004.
[61]
Carbonnelle, E.; Helaine, S.; Nassif, X.; Pelicic, V. A systematic genetic analysis in Neisseria meningitidis defines the Pil proteins required for assembly, functionality, stabilization and export of type IV pili. Mol. Microbiol. 2006, 61, 1510–1522, doi:10.1111/j.1365-2958.2006.05341.x.
[62]
Brown, D.R.; Helaine, S.; Carbonnelle, E.; Pelicic, V. Systematic functional analysis reveals that a set of seven genes is involved in fine-tuning of the multiple functions mediated by type IV pili in Neisseria meningitidis. Infect. Immun. 2010, 78, 3053–3063, doi:10.1128/IAI.00099-10.
[63]
Georgiadou, M.; Castagnini, M.; Karimova, G.; Ladant, D.; Pelicic, V. Large-scale study of the interactions between proteins involved in type IV pilus biology in Neisseria meningitidis: Characterization of a subcomplex involved in pilus assembly. Mol. Microbiol. 2012, 84, 857–873, doi:10.1111/j.1365-2958.2012.08062.x.
[64]
Morand, P.C.; Bille, E.; Morelle, S.; Eugene, E.; Beretti, J.L.; Wolfgang, M.; Meyer, T.F.; Koomey, M.; Nassif, X. Type IV pilus retraction in pathogenic Neisseria is regulated by the PilC proteins. EMBO J. 2004, 23, 2009–2017, doi:10.1038/sj.emboj.7600200.
[65]
Tonjum, T.; Freitag, N.E.; Namork, E.; Koomey, M. Identification and characterization of pilG, a highly conserved pilus-assembly gene in pathogenic Neisseria. Mol. Microbiol. 1995, 16, 451–464, doi:10.1111/j.1365-2958.1995.tb02410.x.
[66]
Drake, S.L.; Koomey, M. The product of the pilQ gene is essential for the biogenesis of type IV pili in Neisseria gonorrhoeae. Mol. Microbiol. 1995, 18, 975–986.
[67]
Carbonnelle, E.; Helaine, S.; Prouvensier, L.; Nassif, X.; Pelicic, V. Type IV pilus biogenesis in Neisseria meningitidis: PilW is involved in a step occurring after pilus assembly, essential for fibre stability and function. Mol. Microbiol. 2005, 55, 54–64.
[68]
Helaine, S.; Carbonnelle, E.; Prouvensier, L.; Beretti, J.L.; Nassif, X.; Pelicic, V. PilX, a pilus-associated protein essential for bacterial aggregation, is a key to pilus-facilitated attachment of Neisseria meningitidis to human cells. Mol. Microbiol. 2005, 55, 65–77.
[69]
Cehovin, A.; Simpson, P.J.; McDowell, M.A.; Brown, D.R.; Noschese, R.; Pallett, M.; Brady, J.; Baldwin, G.S.; Lea, S.M.; Matthews, S.J.; et al. Specific DNA recognition mediated by a type IV pilin. Proc. Natl. Acad. Sci. USA 2013, 110, 3065–3070, doi:10.1073/pnas.1218832110.
[70]
Collins, R.F.; Ford, R.C.; Kitmitto, A.; Olsen, R.O.; Tonjum, T.; Derrick, J.P. Three-dimensional structure of the Neisseria meningitidis secretin PilQ determined from negative-stain transmission electron microscopy. J. Bacteriol. 2003, 185, 2611–2617, doi:10.1128/JB.185.8.2611-2617.2003.
[71]
Collins, R.F.; Davidsen, L.; Derrick, J.P.; Ford, R.C.; Tonjum, T. Analysis of the PilQ secretin from Neisseria meningitidis by transmission electron microscopy reveals a dodecameric quaternary structure. J. Bacteriol. 2001, 183, 3825–3832.
[72]
Collins, R.F.; Frye, S.A.; Kitmitto, A.; Ford, R.C.; Tonjum, T.; Derrick, J.P. Structure of the Neisseria meningitidis outer membrane PilQ secretin complex at 12 A resolution. J. Biol. Chem. 2004, 279, 39750–39756.
[73]
Jain, S.; Moscicka, K.B.; Bos, M.P.; Pachulec, E.; Stuart, M.C.; Keegstra, W.; Boekema, E.J.; van der Does, C. Structural characterization of outer membrane components of the type IV pili system in pathogenic Neisseria. PLoS One 2011, 6, e16624:1–e16624:11.
[74]
Berry, J.L.; Phelan, M.M.; Collins, R.F.; Adomavicius, T.; Tonjum, T.; Frye, S.A.; Bird, L.; Owens, R.; Ford, R.C.; Lian, L.Y.; et al. Structure and assembly of a trans-periplasmic channel for type IV pili in Neisseria meningitidis. PLoS Pathog. 2012, 8, e1002923:1–e1002923:15.
[75]
Balasingham, S.V.; Collins, R.F.; Assalkhou, R.; Homberset, H.; Frye, S.A.; Derrick, J.P.; Tonjum, T. Interactions between the lipoprotein PilP and the secretin PilQ in Neisseria meningitidis. J. Bacteriol. 2007, 189, 5716–5727, doi:10.1128/JB.00060-07.
[76]
Golovanov, A.P.; Balasingham, S.; Tzitzilonis, C.; Goult, B.T.; Lian, L.Y.; Homberset, H.; Tonjum, T.; Derrick, J.P. The solution structure of a domain from the Neisseria meningitidis lipoprotein PilP reveals a new beta-sandwich fold. J. Mol. Biol. 2006, 364, 186–195, doi:10.1016/j.jmb.2006.08.078.
[77]
Trindade, M.B.; Job, V.; Contreras-Martel, C.; Pelicic, V.; Dessen, A. Structure of a widely conserved type IV pilus biogenesis factor that affects the stability of secretin multimers. J. Mol. Biol. 2008, 378, 1031–1039, doi:10.1016/j.jmb.2008.03.028.
[78]
Collins, R.F.; Saleem, M.; Derrick, J.P. Purification and three-dimensional electron microscopy structure of the Neisseria meningitidis type IV pilus biogenesis protein PilG. J. Bacteriol. 2007, 189, 6389–6396, doi:10.1128/JB.00648-07.
[79]
Helaine, S.; Dyer, D.H.; Nassif, X.; Pelicic, V.; Forest, K.T. 3D structure/function analysis of PilX reveals how minor pilins can modulate the virulence properties of type IV pili. Proc. Natl. Acad. Sci. USA 2007, 104, 15888–15893, doi:10.1073/pnas.0707581104.
[80]
Forest, K.T.; Satyshur, K.A.; Worzalla, G.A.; Hansen, J.K.; Herdendorf, T.J. The pilus-retraction protein PilT: Ultrastructure of the biological assembly. Acta Crystallogr. D Biol. Crystallogr. 2004, 60, 978–982, doi:10.1107/S0907444904006055.
[81]
Swanson, J. Studies on gonococcus infection. XIV. Cell wall protein differences among color/opacity colony variants of Neisseria gonorrhoeae. Infect. Immun. 1978, 21, 292–302.
[82]
Parkhill, J.; Achtman, M.; James, K.D.; Bentley, S.D.; Churcher, C.; Klee, S.R.; Morelli, G.; Basham, D.; Brown, D.; Chillingworth, T.; et al. Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491. Nature 2000, 404, 502–506, doi:10.1038/35006655.
Bhat, K.S.; Gibbs, C.P.; Barrera, O.; Morrison, S.G.; Jahnig, F.; Stern, A.; Kupsch, E.M.; Meyer, T.F.; Swanson, J. The opacity proteins of Neisseria gonorrhoeae strain MS11 are encoded by a family of 11 complete genes. Mol. Microbiol. 1991, 5, 1889–1901, doi:10.1111/j.1365-2958.1991.tb00813.x.
[85]
Stern, A.; Meyer, T.F. Common mechanism controlling phase and antigenic variation in pathogenic Neisseriae. Mol. Microbiol. 1987, 1, 5–12, doi:10.1111/j.1365-2958.1987.tb00520.x.
[86]
Wolff, K.; Stern, A. Identification and characterization of specific sequences encoding pathogenicity associated proteins in the genome of commensal Neisseria species. FEMS Microbiol. Lett. 1995, 125, 255–263, doi:10.1111/j.1574-6968.1995.tb07366.x.
[87]
Toleman, M.; Aho, E.; Virji, M. Expression of pathogen-like Opa adhesins in commensal Neisseria: Genetic and functional analysis. Cell Microbiol. 2001, 3, 33–44, doi:10.1046/j.1462-5822.2001.00089.x.
[88]
Malorny, B.; Morelli, G.; Kusecek, B.; Kolberg, J.; Achtman, M. Sequence diversity, predicted two-dimensional protein structure, and epitope mapping of neisserial Opa proteins. J. Bacteriol. 1998, 180, 1323–1330.
[89]
De Jonge, M.I.; Bos, M.P.; Hamstra, H.J.; Jiskoot, W.; van Ulsen, P.; Tommassen, J.; van, A.L.; van der Ley, P. Conformational analysis of opacity proteins from Neisseria meningitidis. Eur. J. Biochem. 2002, 269, 5215–5223, doi:10.1046/j.1432-1033.2002.03228.x.
[90]
Vandeputte-Rutten, L.; Bos, M.P.; Tommassen, J.; Gros, P. Crystal structure of Neisserial surface protein A (NspA), a conserved outer membrane protein with vaccine potential. J. Biol. Chem. 2003, 278, 24825–24830, doi:10.1074/jbc.M302803200.
[91]
Hobbs, M.M.; Malorny, B.; Prasad, P.; Morelli, G.; Kusecek, B.; Heckels, J.E.; Cannon, J.G.; Achtman, M. Recombinational reassortment among opa genes from ET-37 complex Neisseria meningitidis isolates of diverse geographical origins. Microbiology 1998, 144, 157–166, doi:10.1099/00221287-144-1-157.
[92]
Bilek, N.; Ison, C.A.; Spratt, B.G. Relative contributions of recombination and mutation to the diversification of the opa gene repertoire of Neisseria gonorrhoeae. J. Bacteriol. 2009, 191, 1878–1890, doi:10.1128/JB.01518-08.
[93]
Stern, A.; Brown, M.; Nickel, P.; Meyer, T.F. Opacity genes in Neisseria gonorrhoeae: Control of phase and antigenic variation. Cell 1986, 47, 61–71, doi:10.1016/0092-8674(86)90366-1.
[94]
Belland, R.J.; Morrison, S.G.; van der Ley, P.; Swanson, J. Expression and phase variation of gonococcal P.II genes in Escherichia coli involves ribosomal frameshifting and slipped-strand mispairing. Mol. Microbiol. 1989, 3, 777–786, doi:10.1111/j.1365-2958.1989.tb00226.x.
[95]
Mayer, L.W. Rates in vitro changes of gonococcal colony opacity phenotypes. Infect. Immun. 1982, 37, 481–485.
Callaghan, M.J.; Buckee, C.; McCarthy, N.D.; Ibarz Pavon, A.B.; Jolley, K.A.; Faust, S.; Gray, S.J.; Kaczmarski, E.B.; Levin, M.; Kroll, J.S.; et al. Opa protein repertoires of disease-causing and carried meningococci. J. Clin. Microbiol. 2008, 46, 3033–3041, doi:10.1128/JCM.00005-08.
[99]
Zhu, P.; Morelli, G.; Achtman, M. The opcA and (psi)opcB regions in Neisseria: Genes, pseudogenes, deletions, insertion elements and DNA islands. Mol. Microbiol. 1999, 33, 635–650, doi:10.1046/j.1365-2958.1999.01514.x.
[100]
Zhu, P.; Klutch, M.J.; Derrick, J.P.; Prince, S.M.; Tsang, R.S.; Tsai, C.M. Identification of opcA gene in Neisseria polysaccharea: Interspecies diversity of Opc protein family. Gene 2003, 307, 31–40, doi:10.1016/S0378-1119(02)01208-8.
[101]
Sarkari, J.; Pandit, N.; Moxon, E.R.; Achtman, M. Variable expression of the Opc outer membrane protein in Neisseria meningitidis is caused by size variation of a promoter containing poly-cytidine. Mol. Microbiol. 1994, 13, 207–217, doi:10.1111/j.1365-2958.1994.tb00416.x.
[102]
Prince, S.M.; Achtman, M.; Derrick, J.P. Crystal structure of the OpcA integral membrane adhesin from Neisseria meningitidis. Proc. Natl. Acad. Sci. USA 2002, 99, 3417–3421, doi:10.1073/pnas.062630899.
[103]
Luan, B.; Caffrey, M.; Aksimentiev, A. Structure refinement of the OpcA adhesin using molecular dynamics. Biophys. J. 2007, 93, 3058–3069, doi:10.1529/biophysj.107.106724.
[104]
Cherezov, V.; Liu, W.; Derrick, J.P.; Luan, B.; Aksimentiev, A.; Katritch, V.; Caffrey, M. In meso crystal structure and docking simulations suggest an alternative proteoglycan binding site in the OpcA outer membrane adhesin. Proteins 2008, 71, 24–34, doi:10.1002/prot.21841.
[105]
Hadi, H.A.; Wooldridge, K.G.; Robinson, K.; Ala’Aldeen, D.A. Identification and characterization of App: An immunogenic autotransporter protein of Neisseria meningitidis. Mol. Microbiol. 2001, 41, 611–623, doi:10.1046/j.1365-2958.2001.02516.x.
[106]
Serruto, D.; Adu-Bobie, J.; Scarselli, M.; Veggi, D.; Pizza, M.; Rappuoli, R.; Arico, B. Neisseria meningitidis App, a new adhesin with autocatalytic serine protease activity. Mol. Microbiol. 2003, 48, 323–334, doi:10.1046/j.1365-2958.2003.03420.x.
[107]
Turner, D.P.; Marietou, A.G.; Johnston, L.; Ho, K.K.; Rogers, A.J.; Wooldridge, K.G.; Ala'Aldeen, D.A. Characterization of MspA, an immunogenic autotransporter protein that mediates adhesion to epithelial and endothelial cells in Neisseria meningitidis. Infect. Immun. 2006, 74, 2957–2964, doi:10.1128/IAI.74.5.2957-2964.2006.
[108]
Pohlner, J.; Halter, R.; Beyreuther, K.; Meyer, T.F. Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 1987, 325, 458–462, doi:10.1038/325458a0.
[109]
Van Ulsen, P. Protein Folding in Bacterial Adhesion: Secretion and Folding of Classical Monomeric Autotransporters. In Bacterial Adhesion: Chemistry, Biology and Physics; Linke, D., Goldman, A., Eds.; Springer: Dordrecht, Germany, 2011. Chapter 8; pp. 125–142.
[110]
Meng, G.; Spahich, N.; Kenjale, R.; Waksman, G.; St. Geme, J.W. Crystal structure of the Haemophilus influenzae Hap adhesin reveals an intercellular oligomerization mechanism for bacterial aggregation. EMBO J. 2011, 30, 3864–3874, doi:10.1038/emboj.2011.279.
[111]
Cotter, S.E.; Surana, N.K.; St. Geme, J.W. Trimeric autotransporters: A distinct subfamily of autotransporter proteins. Trends Microbiol. 2005, 13, 199–205, doi:10.1016/j.tim.2005.03.004.
[112]
Cotter, S.E.; Surana, N.K.; Grass, S.; St. Geme, J.W. Trimeric autotransporters require trimerization of the passenger domain for stability and adhesive activity. J. Bacteriol. 2006, 188, 5400–5407, doi:10.1128/JB.00164-06.
[113]
Lyskowski, A.; Leo, J.C.; Goldman, A. Structure and biology of trimeric autotransporter adhesins. In Bacterial Adhesion: Chemistry, Biology and Physics; Linke, D., Goldman, A., Eds.; Springer: Dordrecht, Germany, 2011. Chapter 9; pp. 143–158.
[114]
El Tahir, Y.; Skurnik, M. YadA, the multifaceted Yersinia adhesin. Int. J. Med. Microbiol. 2001, 291, 209–218, doi:10.1078/1438-4221-00119.
[115]
Koretke, K.K.; Szczesny, P.; Gruber, M.; Lupas, A.N. Model structure of the prototypical non-fimbrial adhesin YadA of Yersinia enterocolitica. J. Struct. Biol. 2006, 155, 154–161, doi:10.1016/j.jsb.2006.03.012.
[116]
St. Geme, J.W.; Cutter, D. The Haemophilus influenzae Hia adhesin is an autotransporter protein that remains uncleaved at the C terminus and fully cell associated. J. Bacteriol. 2000, 182, 6005–6013, doi:10.1128/JB.182.21.6005-6013.2000.
[117]
Cotter, S.E.; Yeo, H.J.; Juehne, T.; St. Geme, J.W. Architecture and adhesive activity of the Haemophilus influenzae Hsf adhesin. J. Bacteriol. 2005, 187, 4656–4664, doi:10.1128/JB.187.13.4656-4664.2005.
[118]
Comanducci, M.; Bambini, S.; Brunelli, B.; du-Bobie, J.; Arico, B.; Capecchi, B.; Giuliani, M.M.; Masignani, V.; Santini, L.; Savino, S.; et al. NadA, a novel vaccine candidate of Neisseria meningitidis. J. Exp. Med. 2002, 195, 1445–1454, doi:10.1084/jem.20020407.
[119]
Tavano, R.; Capecchi, B.; Montanari, P.; Franzoso, S.; Marin, O.; Sztukowska, M.; Cecchini, P.; Segat, D.; Scarselli, M.; Arico, B.; et al. Mapping of the Neisseria meningitidis NadA cell-binding site: Relevance of predicted {alpha}-helices in the NH2-terminal and dimeric coiled-coil regions. J. Bacteriol. 2011, 193, 107–115, doi:10.1128/JB.00430-10.
[120]
Comanducci, M.; Bambini, S.; Caugant, D.A.; Mora, M.; Brunelli, B.; Capecchi, B.; Ciucchi, L.; Rappuoli, R.; Pizza, M. NadA diversity and carriage in Neisseria meningitidis. Infect. Immun. 2004, 72, 4217–4223, doi:10.1128/IAI.72.7.4217-4223.2004.
[121]
Peak, I.R.; Srikhanta, Y.; Dieckelmann, M.; Moxon, E.R.; Jennings, M.P. Identification and characterisation of a novel conserved outer membrane protein from Neisseria meningitidis. FEMS Immunol. Med. Microbiol. 2000, 28, 329–334, doi:10.1111/j.1574-695X.2000.tb01494.x.
[122]
Scarselli, M.; Serruto, D.; Montanari, P.; Capecchi, B.; Adu-Bobie, J.; Veggi, D.; Rappuoli, R.; Pizza, M.; Arico, B. Neisseria meningitidis NhhA is a multifunctional trimeric autotransporter adhesin. Mol. Microbiol. 2006, 61, 631–644, doi:10.1111/j.1365-2958.2006.05261.x.
[123]
Griffiths, N.J.; Hill, D.J.; Borodina, E.; Sessions, R.B.; Devos, N.I.; Feron, C.M.; Poolman, J.T.; Virji, M. Meningococcal surface fibril (Msf) binds to activated vitronectin and inhibits the terminal complement pathway to increase serum resistance. Mol. Microbiol. 2011, 82, 1129–1149, doi:10.1111/j.1365-2958.2011.07876.x.
[124]
Hodak, H.; Jacob-Dubuisson, F. Current challenges in autotransport and two-partner protein secretion pathways. Res. Microbiol. 2007, 158, 631–637, doi:10.1016/j.resmic.2007.08.001.
[125]
Hodak, H.; Clantin, B.; Willery, E.; Villeret, V.; Locht, C.; Jacob-Dubuisson, F. Secretion signal of the filamentous haemagglutinin, a model two-partner secretion substrate. Mol. Microbiol. 2006, 61, 368–382, doi:10.1111/j.1365-2958.2006.05242.x.
[126]
Jacob-Dubuisson, F.; Fernandez, R.; Coutte, L. Protein secretion through autotransporter and two-partner pathways. Biochim. Biophys. Acta 2004, 1694, 235–257, doi:10.1016/j.bbamcr.2004.03.008.
[127]
Jacob-Dubuisson, F.; Locht, C.; Antoine, R. Two-partner secretion in Gram-negative bacteria: A thrifty, specific pathway for large virulence proteins. Mol. Microbiol. 2001, 40, 306–313, doi:10.1046/j.1365-2958.2001.02278.x.
[128]
Clantin, B.; Hodak, H.; Willery, E.; Locht, C.; Jacob-Dubuisson, F.; Villeret, V. The crystal structure of filamentous hemagglutinin secretion domain and its implications for the two-partner secretion pathway. Proc. Natl. Acad. Sci. USA 2004, 101, 6194–6199.
[129]
Schmitt, C.; Turner, D.; Boesl, M.; Abele, M.; Frosch, M.; Kurzai, O. A functional two-partner secretion system contributes to adhesion of Neisseria meningitidis to epithelial cells. J. Bacteriol. 2007, 189, 7968–7976, doi:10.1128/JB.00851-07.
[130]
Snyder, L.A.; Saunders, N.J. The majority of genes in the pathogenic Neisseria species are present in non-pathogenic Neisseria lactamica, including those designated as “virulence genes”. BMC Genomics 2006, 7, 128:1–128:11.
[131]
Van Ulsen, P.; Rutten, L.; Feller, M.; Tommassen, J.; van der Ende, A. Two-partner secretion systems of Neisseria meningitidis associated with invasive clonal complexes. Infect. Immun. 2008, 76, 4649–4658, doi:10.1128/IAI.00393-08.
[132]
Ur Rahman, S.; van Ulsen, P. System specificity of the TpsB transporters of coexpressed two-partner secretion systems of Neisseria meningitidis. J. Bacteriol. 2013, 195, 788–797, doi:10.1128/JB.01355-12.
[133]
Kizil, G.; Todd, I.; Atta, M.; Borriello, S.P.; Ait-Tahar, K.; Ala’aldeen, D.A. Identification and characterization of TspA, a major CD4(+) T-cell- and B-cell-stimulating Neisseria-specific antigen. Infect. Immun. 1999, 67, 3533–3541.
[134]
Oldfield, N.J.; Bland, S.J.; Taraktsoglou, M.; Dos Ramos, F.J.; Robinson, K.; Wooldridge, K.G.; Ala'aldeen, D.A. T-cell stimulating protein A (TspA) of Neisseria meningitidis is required for optimal adhesion to human cells. Cell Microbiol. 2007, 9, 463–478, doi:10.1111/j.1462-5822.2006.00803.x.
[135]
Semmler, A.B.; Whitchurch, C.B.; Leech, A.J.; Mattick, J.S. Identification of a novel gene, fimV, involved in twitching motility in Pseudomonas aeruginosa. Microbiology 2000, 146, 1321–1332.
[136]
Tunio, S.A.; Oldfield, N.J.; Berry, A.; Ala’Aldeen, D.A.; Wooldridge, K.G.; Turner, D.P. The moonlighting protein fructose-1, 6-bisphosphate aldolase of Neisseria meningitidis: Surface localization and role in host cell adhesion. Mol. Microbiol. 2010, 76, 605–615, doi:10.1111/j.1365-2958.2010.07098.x.
[137]
Tunio, S.A.; Oldfield, N.J.; Ala’Aldeen, D.A.; Wooldridge, K.G.; Turner, D.P. The role of glyceraldehyde 3-phosphate dehydrogenase (GapA-1) in Neisseria meningitidis adherence to human cells. BMC Microbiol. 2010, 10, 280:1–280:10.
[138]
Li, M.S.; Chow, N.Y.; Sinha, S.; Halliwell, D.; Finney, M.; Gorringe, A.R.; Watson, M.W.; Kroll, J.S.; Langford, P.R.; Webb, S.A. A Neisseria meningitidis NMB1966 mutant is impaired for invasion of respiratory epithelial cells, survival in human blood and for virulence in vivo. Med. Microbiol. Immunol. 2009, 198, 57–67, doi:10.1007/s00430-008-0105-2.
[139]
Serino, L.; Nesta, B.; Leuzzi, R.; Fontana, M.R.; Monaci, E.; Mocca, B.T.; Cartocci, E.; Masignani, V.; Jerse, A.E.; Rappuoli, R.; et al. Identification of a new OmpA-like protein in Neisseria gonorrhoeae involved in the binding to human epithelial cells and in vivo colonization. Mol. Microbiol. 2007, 64, 1391–1403, doi:10.1111/j.1365-2958.2007.05745.x.
[140]
Grizot, S.; Buchanan, S.K. Structure of the OmpA-like domain of RmpM from Neisseria meningitidis. Mol. Microbiol. 2004, 51, 1027–1037, doi:10.1111/j.1365-2958.2003.03903.x.
[141]
Danoff, E.J.; Fleming, K.G. The soluble, periplasmic domain of OmpA folds as an independent unit and displays chaperone activity by reducing the self-association propensity of the unfolded OmpA transmembrane beta-barrel. Biophys. Chem. 2011, 159, 194–204, doi:10.1016/j.bpc.2011.06.013.
[142]
Hung, M.C.; Heckels, J.E.; Christodoulides, M. The Adhesin Complex Protein (ACP) of Neisseria meningitidis is a new adhesin with vaccine potential. mBio 2013, 4, e00041:1–e00041:13.
[143]
Jolley, K.A.; Maiden, M.C. BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinf. 2010, 11, 595:1–595:11.
[144]
Schoen, C.; Blom, J.; Claus, H.; Schramm-Gluck, A.; Brandt, P.; Muller, T.; Goesmann, A.; Joseph, B.; Konietzny, S.; Kurzai, O.; et al. Whole-genome comparison of disease and carriage strains provides insights into virulence evolution in Neisseria meningitidis. Proc. Natl. Acad. Sci. USA 2008, 105, 3473–3478, doi:10.1073/pnas.0800151105.
[145]
Swain, C.L.; Martin, D.R. Survival of meningococci outside of the host: Implications for acquisition. Epidemiol. Infect. 2007, 135, 315–320, doi:10.1017/S0950268806006789.
[146]
Claus, H.; Maiden, M.C.; Maag, R.; Frosch, M.; Vogel, U. Many carried meningococci lack the genes required for capsule synthesis and transport. Microbiology 2002, 148, 1813–1819.
[147]
Frosch, M.; Vogel, U. Structure and Genetics of the Meningococcal Capsule. In Handbook of Meningococcal Disease: Infection Biology, Vaccination, Clinical Management; Frosch, M., Maiden, M.C.J., Eds.; Wiley-VCH: Weinheim, Germany, 2006. Chapter 8; pp. 145–162.
[148]
Harrison, O.B.; Claus, H.; Jiang, Y.; Bennett, J.S.; Bratcher, H.B.; Jolley, K.A.; Corton, C.; Care, R.; Poolman, J.T.; Zollinger, W.D.; et al. Description and nomenclature of Neisseria meningitidis capsule locus. Emerg. Infect. Dis. 2013, 19, 566–573, doi:10.3201/eid1904.111799.
[149]
Swartley, J.S.; Marfin, A.A.; Edupuganti, S.; Liu, L.J.; Cieslak, P.; Perkins, B.; Wenger, J.D.; Stephens, D.S. Capsule switching of Neisseria meningitidis. Proc. Natl. Acad. Sci. USA 1997, 94, 271–276, doi:10.1073/pnas.94.1.271.
[150]
Finne, J.; Leinonen, M.; Makela, P.H. Antigenic similarities between brain components and bacteria causing meningitis. Implications for vaccine development and pathogenesis. Lancet 1983, 2, 355–357, doi:10.1016/S0140-6736(83)90340-9.
[151]
Finne, J.; Finne, U.; Deagostini-Bazin, H.; Goridis, C. Occurrence of alpha 2–8 linked polysialosyl units in a neural cell adhesion molecule. Biochem. Biophys. Res. Commun. 1983, 112, 482–487.
[152]
Yamasaki, R.; Bacon, B. Three-dimensional structural analysis of the group B polysaccharide of Neisseria meningitidis 6275 by two-dimensional NMR: The polysaccharide is suggested to exist in helical conformations in solution. Biochemistry 1991, 30, 851–857, doi:10.1021/bi00217a039.
[153]
Lemercinier, X.; Jones, C. Full 1H NMR assignment and detailed O-acetylation patterns of capsular polysaccharides from Neisseria meningitidis used in vaccine production. Carbohydr. Res. 1996, 296, 83–96, doi:10.1016/S0008-6215(96)00253-4.
[154]
Gudlavalleti, S.K.; Szymanski, C.M.; Jarrell, H.C.; Stephens, D.S. In vivo determination of Neisseria meningitidis serogroup A capsular polysaccharide by whole cell high-resolution magic angle spinning NMR spectroscopy. Carbohydr. Res. 2006, 341, 557–562, doi:10.1016/j.carres.2005.11.036.
[155]
Xie, O.; Bolgiano, B.; Gao, F.; Lockyer, K.; Swann, C.; Jones, C.; Delrieu, I.; Njanpop-Lafourcade, B.M.; Tamekloe, T.A.; Pollard, A.J.; et al. Characterization of size, structure and purity of serogroup X Neisseria meningitidis polysaccharide, and development of an assay for quantification of human antibodies. Vaccine 2012, 30, 5812–5823, doi:10.1016/j.vaccine.2012.07.032.
[156]
Garrido, R.; Puyada, A.; Fernandez, A.; Gonzalez, M.; Ramirez, U.; Cardoso, F.; Valdes, Y.; Gonzalez, D.; Fernandez, V.; Verez, V.; et al. Quantitative proton nuclear magnetic resonance evaluation and total assignment of the capsular polysaccharide Neisseria meningitidis serogroup X. J. Pharm. Biomed. Anal. 2012, 70, 295–300, doi:10.1016/j.jpba.2012.07.014.
[157]
Kahler, C.M.; Stephens, D.S. Genetic basis for biosynthesis, structure, and function of meningococcal lipooligosaccharide (endotoxin). Crit. Rev. Microbiol. 1998, 24, 281–334.
[158]
Arking, D.; Tong, Y.; Stein, D.C. Analysis of lipooligosaccharide biosynthesis in the Neisseriaceae. J. Bacteriol. 2001, 183, 934–941, doi:10.1128/JB.183.3.934-941.2001.
[159]
Zhu, P.; Klutch, M.J.; Bash, M.C.; Tsang, R.S.; Ng, L.K.; Tsai, C.M. Genetic diversity of three lgt loci for biosynthesis of lipooligosaccharide (LOS) in Neisseria species. Microbiology 2002, 148, 1833–1844.
[160]
Jennings, M.P.; Srikhanta, Y.N.; Moxon, E.R.; Kramer, M.; Poolman, J.T.; Kuipers, B.; van der Ley, P. The genetic basis of the phase variation repertoire of lipopolysaccharide immunotypes in Neisseria meningitidis. Microbiology 1999, 145, 3013–3021.
[161]
Mandrell, R.E.; Griffiss, J.M.; Macher, B.A. Lipooligosaccharides (LOS) of Neisseria gonorrhoeae and Neisseria meningitidis have components that are immunochemically similar to precursors of human blood group antigens. Carbohydrate sequence specificity of the mouse monoclonal antibodies that recognize crossreacting antigens on LOS and human erythrocytes. J. Exp. Med. 1988, 168, 107–126, doi:10.1084/jem.168.1.107.
[162]
Vogel, U.; Hammerschmidt, S.; Rosch, M. Sialic acids of both the capsule and the sialylated lipooligosaccharide of Neisseria meningitis serogroup B are prerequisites for virulence of meningococci in the infant rat. Med. Microbiol. Immunol. 1996, 185, 81–87, doi:10.1007/s004300050018.
[163]
Hill, D.J.; Griffiths, N.J.; Borodina, E.; Virji, M. Cellular and molecular biology of Neisseria meningitidis colonization and invasive disease. Clin. Sci. (Lond.) 2010, 118, 547–564.
[164]
Takayama, K.; Qureshi, N.; Hyver, K.; Honovich, J.; Cotter, R.J.; Mascagni, P.; Schneider, H. Characterization of a structural series of lipid A obtained from the lipopolysaccharides of Neisseria gonorrhoeae. Combined laser desorption and fast atom bombardment mass spectral analysis of high performance liquid chromatography-purified dimethyl derivatives. J. Biol. Chem. 1986, 261, 10624–10631.
[165]
Michon, F.; Beurret, M.; Gamian, A.; Brisson, J.R.; Jennings, H.J. Structure of the L5 lipopolysaccharide core oligosaccharides of Neisseria meningitidis. J. Biol. Chem. 1990, 265, 7243–7247.
[166]
Yamasaki, R.; Bacon, B.E.; Nasholds, W.; Schneider, H.; Griffiss, J.M. Structural determination of oligosaccharides derived from lipooligosaccharide of Neisseria gonorrhoeae F62 by chemical, enzymatic, and two-dimensional NMR methods. Biochemistry 1991, 30, 10566–10575, doi:10.1021/bi00107a028.
[167]
Gamian, A.; Beurret, M.; Michon, F.; Brisson, J.R.; Jennings, H.J. Structure of the L2 lipopolysaccharide core oligosaccharides of Neisseria meningitidis. J. Biol. Chem. 1992, 267, 922–925.
[168]
Kulshin, V.A.; Zahringer, U.; Lindner, B.; Frasch, C.E.; Tsai, C.M.; Dmitriev, B.A.; Rietschel, E.T. Structural characterization of the lipid A component of pathogenic Neisseria meningitidis. J. Bacteriol. 1992, 174, 1793–1800.
[169]
Wakarchuk, W.W.; Gilbert, M.; Martin, A.; Wu, Y.; Brisson, J.R.; Thibault, P.; Richards, J.C. Structure of an alpha-2,6-sialylated lipooligosaccharide from Neisseria meningitidis immunotype L1. Eur. J. Biochem. 1998, 254, 626–633.
[170]
Cox, A.D.; Li, J.; Brisson, J.R.; Moxon, E.R.; Richards, J.C. Structural analysis of the lipopolysaccharide from Neisseria meningitidis strain BZ157 galE: Localisation of two phosphoethanolamine residues in the inner core oligosaccharide. Carbohydr. Res. 2002, 337, 1435–1444, doi:10.1016/S0008-6215(02)00161-1.
[171]
Leavell, M.D.; Leary, J.A.; Yamasaki, R. Mass spectrometric strategy for the characterization of lipooligosaccharides from Neisseria gonorrhoeae 302 using FTICR. J. Am. Soc. Mass Spectrom. 2002, 13, 571–576, doi:10.1016/S1044-0305(02)00360-4.
[172]
Cox, A.D.; Wright, J.C.; Gidney, M.A.; Lacelle, S.; Plested, J.S.; Martin, A.; Moxon, E.R.; Richards, J.C. Identification of a novel inner-core oligosaccharide structure in Neisseria meningitidis lipopolysaccharide. Eur. J. Biochem. 2003, 270, 1759–1766, doi:10.1046/j.1432-1033.2003.03535.x.
[173]
Swanson, K.V.; Griffiss, J.M. Separation and identification of neisserial lipooligosaccharide oligosaccharides using high-performance anion-exchange chromatography with pulsed amperometric detection. Carbohydr. Res. 2006, 341, 388–396, doi:10.1016/j.carres.2005.11.017.
[174]
Choudhury, B.; Kahler, C.M.; Datta, A.; Stephens, D.S.; Carlson, R.W. The structure of the L9 immunotype lipooligosaccharide from Neisseria meningitidis NMA Z2491. Carbohydr. Res. 2008, 343, 2971–2979, doi:10.1016/j.carres.2008.08.026.
[175]
Kahler, C.M.; Datta, A.; Tzeng, Y.L.; Carlson, R.W.; Stephens, D.S. Inner core assembly and structure of the lipooligosaccharide of Neisseria meningitidis: Capacity of strain NMB to express all known immunotype epitopes. Glycobiology 2005, 15, 409–419.
[176]
Jennings, H.J.; Beurret, M.; Gamian, A.; Michon, F. Structure and immunochemistry of meningococcal lipopolysaccharides. Antonie Van Leeuwenhoek 1987, 53, 519–522, doi:10.1007/BF00415511.
[177]
Pavliak, V.; Brisson, J.R.; Michon, F.; Uhrin, D.; Jennings, H.J. Structure of the sialylated L3 lipopolysaccharide of Neisseria meningitidis. J. Biol. Chem. 1993, 268, 14146–14152.
[178]
Phillips, N.J.; John, C.M.; Reinders, L.G.; Gibson, B.W.; Apicella, M.A.; Griffiss, J.M. Structural models for the cell surface lipooligosaccharides of Neisseria gonorrhoeae and Haemophilus influenzae. Biomed. Environ. Mass Spectrom. 1990, 19, 731–745, doi:10.1002/bms.1200191112.
[179]
Kerwood, D.E.; Schneider, H.; Yamasaki, R. Structural analysis of lipooligosaccharide produced by Neisseria gonorrhoeae, strain MS11mk (variant A): A precursor for a gonococcal lipooligosaccharide associated with virulence. Biochemistry 1992, 31, 12760–12768, doi:10.1021/bi00166a008.
[180]
Johnson, K.G.; Perry, M.B.; McDonald, I.J.; Russel, R.R. Cellular and free lipopolysaccharides of some species of Neisseria. Can. J. Microbiol. 1975, 21, 1969–1980, doi:10.1139/m75-285.
[181]
Johnson, K.G.; Perry, M.B.; McDonald, I.J. Studies of the cellular and free lipopolysaccharides form Neisseria canis and N. subflava. Can. J. Microbiol. 1976, 22, 189–196, doi:10.1139/m76-026.
[182]
Tong, Y.; Reinhold, V.; Reinhold, B.; Brandt, B.; Stein, D.C. Structural and immunochemical characterization of the lipooligosaccharides expressed by Neisseria subflava 44. J. Bacteriol. 2001, 183, 942–950, doi:10.1128/JB.183.3.942-950.2001.
[183]
Tommassen, J.; Vermeij, P.; Struyve, M.; Benz, R.; Poolman, J.T. Isolation of Neisseria meningitidis mutants deficient in class 1 (porA) and class 3 (porB) outer membrane proteins. Infect. Immun. 1990, 58, 1355–1359.
[184]
Kattner, C.; Zaucha, J.; Jaenecke, F.; Zachariae, U.; Tanabe, M. Identification of a cation transport pathway in Neisseria meningitidis porb. Proteins 2013, 81, 830–840, doi:10.1002/prot.24241.
[185]
Cannon, J.G.; Buchanan, T.M.; Sparling, P.F. Confirmation of association of protein I serotype of Neisseria gonorrhoeae with ability to cause disseminated infection. Infect. Immun. 1983, 40, 816–819.
[186]
Feavers, I.M.; Maiden, M.C. A gonococcal porA pseudogene: Implications for understanding the evolution and pathogenicity of Neisseria gonorrhoeae. Mol. Microbiol. 1998, 30, 647–656, doi:10.1046/j.1365-2958.1998.01101.x.
[187]
Derrick, J.P.; Urwin, R.; Suker, J.; Feavers, I.M.; Maiden, M.C. Structural and evolutionary inference from molecular variation in Neisseria porins. Infect. Immun. 1999, 67, 2406–2413.
[188]
Bennett, J.S.; Callaghan, M.J.; Derrick, J.P.; Maiden, M.C. Variation in the Neisseria lactamica porin, and its relationship to meningococcal PorB. Microbiology 2008, 154, 1525–1534, doi:10.1099/mic.0.2007/015479-0.
[189]
Minetti, C.A.; Tai, J.Y.; Blake, M.S.; Pullen, J.K.; Liang, S.M.; Remeta, D.P. Structural and functional characterization of a recombinant PorB class 2 protein from Neisseria meningitidis. Conformational stability and porin activity. J. Biol. Chem. 1997, 272, 10710–10720.
[190]
Tanabe, M.; Iverson, T.M. Expression, purification and preliminary X-ray analysis of the Neisseria meningitidis outer membrane protein PorB. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2009, 65, 996–1000, doi:10.1107/S1744309109032333.
[191]
Tanabe, M.; Nimigean, C.M.; Iverson, T.M. Structural basis for solute transport, nucleotide regulation, and immunological recognition of Neisseria meningitidis PorB. Proc. Natl. Acad. Sci. USA 2010, 107, 6811–6816.
[192]
Zeth, K.; Kozjak-Pavlovic, V.; Faulstich, M.; Fraunholz, M.; Hurwitz, R.; Kepp, O.; Rudel, T. Structure and function of the PorB porin from disseminating Neisseria gonorrhoeae. Biochem. J. 2013, 449, 631–642, doi:10.1042/BJ20121025.
[193]
Derrick, J.P.; Maiden, M.C.; Feavers, I.M. Crystal structure of an Fab fragment in complex with a meningococcal serosubtype antigen and a protein G domain. J. Mol. Biol. 1999, 293, 81–91, doi:10.1006/jmbi.1999.3144.
[194]
Tzitzilonis, C.; Prince, S.M.; Collins, R.F.; Achtman, M.; Feavers, I.M.; Maiden, M.C.; Derrick, J.P. Structural variation and immune recognition of the P1.2 subtype meningococcal antigen. Proteins 2006, 62, 947–955.
[195]
Bartley, S.N.; Tzeng, Y.L.; Heel, K.; Lee, C.W.; Mowlaboccus, S.; Seemann, T.; Lu, W.; Lin, Y.H.; Ryan, C.S.; Peacock, C.; et al. Attachment and invasion of Neisseria meningitidis to host cells is related to surface hydrophobicity, bacterial cell size and capsule. PLoS One 2013, 8, e55798:1–e55798:15.
[196]
Deghmane, A.E.; Giorgini, D.; Larribe, M.; Alonso, J.M.; Taha, M.K. Down-regulation of pili and capsule of Neisseria meningitidis upon contact with epithelial cells is mediated by CrgA regulatory protein. Mol. Microbiol. 2002, 43, 1555–1564, doi:10.1046/j.1365-2958.2002.02838.x.
[197]
Virji, M.; Saunders, J.R.; Sims, G.; Makepeace, K.; Maskell, D.; Ferguson, D.J. Pilus-facilitated adherence of Neisseria meningitidis to human epithelial and endothelial cells: Modulation of adherence phenotype occurs concurrently with changes in primary amino acid sequence and the glycosylation status of pilin. Mol. Microbiol. 1993, 10, 1013–1028, doi:10.1111/j.1365-2958.1993.tb00972.x.
[198]
Nassif, X.; Pujol, C.; Morand, P.; Eugene, E. Interactions of pathogenic Neisseria with host cells. Is it possible to assemble the puzzle? Mol. Microbiol. 1999, 32, 1124–1132, doi:10.1046/j.1365-2958.1999.01416.x.
[199]
Rudel, T.; Scheurerpflug, I.; Meyer, T.F. Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature 1995, 373, 357–359, doi:10.1038/373357a0.
[200]
Wolfgang, M.; Lauer, P.; Park, H.S.; Brossay, L.; Hebert, J.; Koomey, M. PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae. Mol. Microbiol. 1998, 29, 321–330, doi:10.1046/j.1365-2958.1998.00935.x.
[201]
Wolfgang, M.; Park, H.S.; Hayes, S.F.; van Putten, J.P.; Koomey, M. Suppression of an absolute defect in type IV pilus biogenesis by loss-of-function mutations in pilT, a twitching motility gene in Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. USA 1998, 95, 14973–14978.
[202]
Pujol, C.; Eugene, E.; Marceau, M.; Nassif, X. The meningococcal PilT protein is required for induction of intimate attachment to epithelial cells following pilus-mediated adhesion. Proc. Natl. Acad. Sci. USA 1999, 96, 4017–4022, doi:10.1073/pnas.96.7.4017.
[203]
Kallstrom, H.; Liszewski, M.K.; Atkinson, J.P.; Jonsson, A.B. Membrane cofactor protein (MCP or CD46) is a cellular pilus receptor for pathogenic Neisseria. Mol. Microbiol. 1997, 25, 639–647, doi:10.1046/j.1365-2958.1997.4841857.x.
Tobiason, D.M.; Seifert, H.S. Inverse relationship between pilus-mediated gonococcal adherence and surface expression of the pilus receptor, CD46. Microbiology 2001, 147, 2333–2340.
[206]
Kirchner, M.; Heuer, D.; Meyer, T.F. CD46-independent binding of neisserial type IV pili and the major pilus adhesin, PilC, to human epithelial cells. Infect. Immun. 2005, 73, 3072–3082, doi:10.1128/IAI.73.5.3072-3082.2005.
[207]
Capecchi, B.; du-Bobie, J.; di Marcello, F.; Ciucchi, L.; Masignani, V.; Taddei, A.; Rappuoli, R.; Pizza, M.; Arico, B. Neisseria meningitidis NadA is a new invasin which promotes bacterial adhesion to and penetration into human epithelial cells. Mol. Microbiol. 2005, 55, 687–698.
[208]
Nagele, V.; Heesemann, J.; Schielke, S.; Jimenez-Soto, L.F.; Kurzai, O.; Ackermann, N. Neisseria meningitidis adhesin NadA targets beta1 integrins: Functional similarity to Yersinia invasin. J. Biol. Chem. 2011, 286, 20536–20546.
[209]
Knaust, A.; Weber, M.V.; Hammerschmidt, S.; Bergmann, S.; Frosch, M.; Kurzai, O. Cytosolic proteins contribute to surface plasminogen recruitment of Neisseria meningitidis. J. Bacteriol. 2007, 189, 3246–3255, doi:10.1128/JB.01966-06.
[210]
Morelle, S.; Carbonnelle, E.; Nassif, X. The REP2 repeats of the genome of Neisseria meningitidis are associated with genes coordinately regulated during bacterial cell interaction. J. Bacteriol. 2003, 185, 2618–2627, doi:10.1128/JB.185.8.2618-2627.2003.
[211]
Ieva, R.; Alaimo, C.; Delany, I.; Spohn, G.; Rappuoli, R.; Scarlato, V. CrgA is an inducible LysR-type regulator of Neisseria meningitidis, acting both as a repressor and as an activator of gene transcription. J. Bacteriol. 2005, 187, 3421–3430, doi:10.1128/JB.187.10.3421-3430.2005.
[212]
Virji, M.; Makepeace, K.; Ferguson, D.J.P.; Achtman, M.; Moxon, E.R. Meningococcal Opa and Opc proteins: Their role in colonization and invasion of human epithelial and endothelial cells. Mol. Microbiol. 1993, 10, 499–510, doi:10.1111/j.1365-2958.1993.tb00922.x.
[213]
Chen, T.; Belland, R.J.; Wilson, J.; Swanson, J. Adherence of pilus- Opa+ gonococci to epithelial cells in vitro involves heparan sulfate. J. Exp. Med. 1995, 182, 511–517, doi:10.1084/jem.182.2.511.
[214]
Van Putten, J.P.; Paul, S.M. Binding of syndecan-like cell surface proteoglycan receptors is required for Neisseria gonorrhoeae entry into human mucosal cells. EMBO J. 1995, 14, 2144–2154.
[215]
Gomez-Duarte, O.G.; Dehio, M.; Guzman, C.A.; Chhatwal, G.S.; Dehio, C.; Meyer, T.F. Binding of vitronectin to opa-expressing Neisseria gonorrhoeae mediates invasion of HeLa cells. Infect. Immun. 1997, 65, 3857–3866.
[216]
Duensing, T.D.; Putten, J.P. Vitronectin binds to the gonococcal adhesin OpaA through a glycosaminoglycan molecular bridge. Biochem. J. 1998, 334, 133–139.
[217]
Moore, J.; Bailey, S.E.; Benmechernene, Z.; Tzitzilonis, C.; Griffiths, N.J.; Virji, M.; Derrick, J.P. Recognition of saccharides by the OpcA, OpaD, and OpaB outer membrane proteins from Neisseria meningitidis. J. Biol. Chem. 2005, 280, 31489–31497, doi:10.1074/jbc.M506354200.
[218]
Gray-Owen, S.D.; Blumberg, R.S. CEACAM1: Contact-dependent control of immunity. Nat. Rev. Immunol. 2006, 6, 433–446, doi:10.1038/nri1864.
[219]
Gold, P.; Freedman, S.O. Demonstration of tumor-specific antigens in human colonic carcinomata by immunological tolerance and absorption techniques. J. Exp. Med. 1965, 121, 439–462, doi:10.1084/jem.121.3.439.
[220]
Chen, T.; Gotschlich, E.C. CGM1a antigen of neutrophils, a receptor of gonococcal opacity proteins. Proc. Natl. Acad. Sci. USA 1996, 93, 14851–14856, doi:10.1073/pnas.93.25.14851.
[221]
Virji, M.; Makepeace, K.; Ferguson, D.J.; Watt, S.M. Carcinoembryonic antigens (CD66) on epithelial cells and neutrophils are receptors for Opa proteins of pathogenic Neisseriae. Mol. Microbiol. 1996, 22, 941–950.
[222]
Virji, M.; Watt, S.M.; Barker, S.; Makepeace, K.; Doyonnas, R. The N-domain of the human CD66a adhesion molecule is a target for Opa proteins of Neisseria meningitidis and Neisseria gonorrhoeae. Mol. Microbiol. 1996, 22, 929–939.
[223]
Bos, M.P.; Grunert, F.; Belland, R.J. Differential recognition of members of the carcinoembryonic antigen family by Opa variants of Neisseria gonorrhoeae. Infect. Immun. 1997, 65, 2353–2361.
[224]
Chen, T.; Grunert, F.; Medina-Marino, A.; Gotschlich, E.C. Several carcinoembryonic antigens (CD66) serve as receptors for gonococcal opacity proteins. J. Exp. Med. 1997, 185, 1557–1564, doi:10.1084/jem.185.9.1557.
[225]
Gray-Owen, S.D.; Dehio, C.; Haude, A.; Grunert, F.; Meyer, T.F. CD66 carcinoembryonic antigens mediate interactions between Opa-expressing Neisseria gonorrhoeae and human polymorphonuclear phagocytes. EMBO J. 1997, 16, 3435–3445, doi:10.1093/emboj/16.12.3435.
[226]
Gray-Owen, S.D.; Lorenzen, D.R.; Haude, A.; Meyer, T.F.; Dehio, C. Differential Opa specificities for CD66 receptors influence tissue interactions and cellular response to Neisseria gonorrhoeae. Mol. Microbiol. 1997, 26, 971–980, doi:10.1046/j.1365-2958.1997.6342006.x.
[227]
Popp, A.; Dehio, C.; Grunert, F.; Meyer, T.F.; Gray-Owen, S.D. Molecular analysis of neisserial Opa protein interactions with the CEA family of receptors: Identification of determinants contributing to the differential specificities of binding. Cell Microbiol. 1999, 1, 169–181, doi:10.1046/j.1462-5822.1999.00017.x.
[228]
Muenzner, P.; Dehio, C.; Fujiwara, T.; Achtman, M.; Meyer, T.F.; Gray-Owen, S.D. Carcinoembryonic antigen family receptor specificity of Neisseria meningitidis Opa variants influences adherence to and invasion of proinflammatory cytokine-activated endothelial cells. Infect. Immun. 2000, 68, 3601–3607, doi:10.1128/IAI.68.6.3601-3607.2000.
[229]
Rowe, H.A.; Griffiths, N.J.; Hill, D.J.; Virji, M. Co-ordinate action of bacterial adhesins and human carcinoembryonic antigen receptors in enhanced cellular invasion by capsulate serum resistant Neisseria meningitidis. Cell Microbiol. 2007, 9, 154–168, doi:10.1111/j.1462-5822.2006.00775.x.
[230]
Griffiths, N.J.; Bradley, C.J.; Heyderman, R.S.; Virji, M. IFN-gamma amplifies NFkappaB-dependent Neisseria meningitidis invasion of epithelial cells via specific upregulation of CEA-related cell adhesion molecule 1. Cell Microbiol. 2007, 9, 2968–2983, doi:10.1111/j.1462-5822.2007.01038.x.
Bos, M.P.; Kuroki, M.; Krop-Watorek, A.; Hogan, D.; Belland, R.J. CD66 receptor specificity exhibited by neisserial Opa variants is controlled by protein determinants in CD66 N-domains. Proc. Natl. Acad. Sci. USA 1998, 95, 9584–9589, doi:10.1073/pnas.95.16.9584.
[233]
Virji, M.; Evans, D.; Hadfield, A.; Grunert, F.; Teixeira, A.M.; Watt, S.M. Critical determinants of host receptor targeting by Neisseria meningitidis and Neisseria gonorrhoeae: Identification of Opa adhesiotopes on the N-domain of CD66 molecules. Mol. Microbiol. 1999, 34, 538–551, doi:10.1046/j.1365-2958.1999.01620.x.
[234]
Bos, M.P.; Kao, D.; Hogan, D.M.; Grant, C.C.; Belland, R.J. Carcinoembryonic antigen family receptor recognition by gonococcal Opa proteins requires distinct combinations of hypervariable Opa protein domains. Infect. Immun. 2002, 70, 1715–1723, doi:10.1128/IAI.70.4.1715-1723.2002.
[235]
De Jonge, M.I.; Hamstra, H.J.; van Alphen, L.; Dankert, J.; van der Ley, P. Mapping the binding domains on meningococcal Opa proteins for CEACAM1 and CEA receptors. Mol. Microbiol. 2003, 50, 1005–1015, doi:10.1046/j.1365-2958.2003.03749.x.
[236]
Virji, M.; Makepeace, K.; Ferguson, D.J.; Achtman, M.; Sarkari, J.; Moxon, E.R. Expression of the Opc protein correlates with invasion of epithelial and endothelial cells by Neisseria meningitidis. Mol. Microbiol. 1992, 6, 2785–2795, doi:10.1111/j.1365-2958.1992.tb01458.x.
[237]
De Vries, F.P.; Cole, R.; Dankert, J.; Frosch, M.; van Putten, J.P. Neisseria meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol. Microbiol. 1998, 27, 1203–1212, doi:10.1046/j.1365-2958.1998.00763.x.
[238]
Virji, M.; Makepeace, K.; Moxon, R. Distinct mechanisms of interactions of Opc-expressing meningococci at apical and basolateral surfaces of human endothelial cells; the role of integrins in apical interactions. Mol. Microbiol. 1994, 14, 173–184, doi:10.1111/j.1365-2958.1994.tb01277.x.
[239]
Unkmeir, A.; Latsch, K.; Dietrich, G.; Wintermeyer, E.; Schinke, B.; Schwender, S.; Kim, K.S.; Eigenthaler, M.; Frosch, M. Fibronectin mediates Opc-dependent internalization of Neisseria meningitidis in human brain microvascular endothelial cells. Mol. Microbiol. 2002, 46, 933–946, doi:10.1046/j.1365-2958.2002.03222.x.
[240]
Sa Cunha, C.E.; Griffiths, N.J.; Murillo, I.; Virji, M. Neisseria meningitidis Opc invasin binds to the cytoskeletal protein alpha-actinin. Cell Microbiol. 2009, 11, 389–405, doi:10.1111/j.1462-5822.2008.01262.x.
[241]
De Vries, F.P.; van der Ende, A.; van Putten, J.P.; Dankert, J. Invasion of primary nasopharyngeal epithelial cells by Neisseria meningitidis is controlled by phase variation of multiple surface antigens. Infect. Immun. 1996, 64, 2998–3006.
[242]
Merz, A.J.; Enns, C.A.; So, M. Type IV pili of pathogenic Neisseriae elicit cortical plaque formation in epithelial cells. Mol. Microbiol. 1999, 32, 1316–1332, doi:10.1046/j.1365-2958.1999.01459.x.
[243]
Chamot-Rooke, J.; Mikaty, G.; Malosse, C.; Soyer, M.; Dumont, A.; Gault, J.; Imhaus, A.F.; Martin, P.; Trellet, M.; Clary, G.; et al. Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science 2011, 331, 778–782, doi:10.1126/science.1200729.
[244]
Ayala, B.P.; Vasquez, B.; Clary, S.; Tainer, J.A.; Rodland, K.; So, M. The pilus-induced Ca2+ flux triggers lysosome exocytosis and increases the amount of Lamp1 accessible to Neisseria IgA1 protease. Cell Microbiol. 2001, 3, 265–275, doi:10.1046/j.1462-5822.2001.00112.x.
[245]
Ayala, P.; Vasquez, B.; Wetzler, L.; So, M. Neisseria gonorrhoeae porin P1.B induces endosome exocytosis and a redistribution of Lamp1 to the plasma membrane. Infect. Immun. 2002, 70, 5965–5971, doi:10.1128/IAI.70.11.5965-5971.2002.
[246]
Greenfield, S.; Sheehe, P.R.; Feldman, H.A. Meningococcal carriage in a population of “normal” families. J. Infect. Dis. 1971, 123, 67–73, doi:10.1093/infdis/123.1.67.
[247]
Hall-Stoodley, L.; Costerton, J.W.; Stoodley, P. Bacterial biofilms: From the natural environment to infectious diseases. Nat. Rev. Microbiol. 2004, 2, 95–108, doi:10.1038/nrmicro821.
[248]
Apicella, M.A.; Shao, J.; Neil, R.B. Methods for Studying Neisseria meningitidis Biofilms. In Neisseria meningitidis: Advanced Methods and Protocols; Christodoulides, M., Ed.; Humana Press: New York, NY, USA, 2012. Chapter 11; pp. 169–184.
[249]
Neil, R.B.; Apicella, M.A. Clinical and laboratory evidence for Neisseria meningitidis biofilms. Future. Microbiol. 2009, 4, 555–563, doi:10.2217/fmb.09.27.
Lappann, M.; Haagensen, J.A.; Claus, H.; Vogel, U.; Molin, S. Meningococcal biofilm formation: Structure, development and phenotypes in a standardized continuous flow system. Mol. Microbiol. 2006, 62, 1292–1309, doi:10.1111/j.1365-2958.2006.05448.x.
[252]
Neil, R.B.; Shao, J.Q.; Apicella, M.A. Biofilm formation on human airway epithelia by encapsulated Neisseria meningitidis serogroup B. Microbes. Infect. 2009, 11, 281–287, doi:10.1016/j.micinf.2008.12.001.
[253]
Lappann, M.; Vogel, U. Biofilm formation by the human pathogen Neisseria meningitidis. Med. Microbiol. Immunol. 2010, 199, 173–183, doi:10.1007/s00430-010-0149-y.
[254]
Neil, R.B.; Apicella, M.A. Role of HrpA in biofilm formation of Neisseria meningitidis and regulation of the hrpBAS transcripts. Infect. Immun. 2009, 77, 2285–2293, doi:10.1128/IAI.01502-08.
[255]
Lappann, M.; Claus, H.; van Alen, T.; Harmsen, M.; Elias, J.; Molin, S.; Vogel, U. A dual role of extracellular DNA during biofilm formation of Neisseria meningitidis. Mol. Microbiol. 2010, 75, 1355–1371, doi:10.1111/j.1365-2958.2010.07054.x.
[256]
Edwards, J.L.; Apicella, M.A. I-domain-containing integrins serve as pilus receptors for Neisseria gonorrhoeae adherence to human epithelial cells. Cell Microbiol. 2005, 7, 1197–1211, doi:10.1111/j.1462-5822.2005.00547.x.
[257]
Harvey, H.A.; Swords, W.E.; Apicella, M.A. The mimicry of human glycolipids and glycosphingolipids by the lipooligosaccharides of pathogenic Neisseria and Haemophilus. J. Autoimmun. 2001, 16, 257–262, doi:10.1006/jaut.2000.0477.
[258]
James-Holmquest, A.N.; Swanson, J.; Buchanan, T.M.; Wende, R.D.; Williams, R.P. Differential attachment by piliated and nonpiliated Neisseria gonorrhoeae to human sperm. Infect. Immun. 1974, 9, 897–902.
[259]
Harvey, H.A.; Porat, N.; Campbell, C.A.; Jennings, M.; Gibson, B.W.; Phillips, N.J.; Apicella, M.A.; Blake, M.S. Gonococcal lipooligosaccharide is a ligand for the asialoglycoprotein receptor on human sperm. Mol. Microbiol. 2000, 36, 1059–1070, doi:10.1046/j.1365-2958.2000.01938.x.
[260]
Liu, J.H.; Li, H.Y.; Cao, Z.G.; Duan, Y.F.; Li, Y.; Ye, Z.Q. Influence of several uropathogenic microorganisms on human sperm motility parameters in vitro. Asian J. Androl. 2002, 4, 179–182.
[261]
Edwards, J.L.; Butler, E.K. The pathobiology of Neisseria gonorrhoeae lower female genital tract infection. Front. Microbiol. 2011, 2, 102:1–102:12.
[262]
Jarvis, G.A. Analysis of C3 deposition and degradation on Neisseria meningitidis and Neisseria gonorrhoeae. Infect. Immun. 1994, 62, 1755–1760.
[263]
Edwards, J.L.; Brown, E.J.; Ault, K.A.; Apicella, M.A. The role of complement receptor 3 (CR3) in Neisseria gonorrhoeae infection of human cervical epithelia. Cell Microbiol. 2001, 3, 611–622, doi:10.1046/j.1462-5822.2001.00140.x.
[264]
Edwards, J.L.; Brown, E.J.; Uk-Nham, S.; Cannon, J.G.; Blake, M.S.; Apicella, M.A. A co-operative interaction between Neisseria gonorrhoeae and complement receptor 3 mediates infection of primary cervical epithelial cells. Cell Microbiol. 2002, 4, 571–584, doi:10.1046/j.1462-5822.2002.t01-1-00215.x.
Van Putten, J.P.; Duensing, T.D.; Carlson, J. Gonococcal invasion of epithelial cells driven by P.IA, a bacterial ion channel with GTP binding properties. J. Exp. Med. 1998, 188, 941–952, doi:10.1084/jem.188.5.941.
[267]
Agarwal, S.; Ram, S.; Ngampasutadol, J.; Gulati, S.; Zipfel, P.F.; Rice, P.A. Factor H facilitates adherence of Neisseria gonorrhoeae to complement receptor 3 on eukaryotic cells. J. Immunol. 2010, 185, 4344–4353, doi:10.4049/jimmunol.0904191.
[268]
Harvey, H.A.; Jennings, M.P.; Campbell, C.A.; Williams, R.; Apicella, M.A. Receptor-mediated endocytosis of Neisseria gonorrhoeae into primary human urethral epithelial cells: The role of the asialoglycoprotein receptor. Mol. Microbiol. 2001, 42, 659–672.
[269]
Swanson, K.V.; Jarvis, G.A.; Brooks, G.F.; Barham, B.J.; Cooper, M.D.; Griffiss, J.M. CEACAM is not necessary for Neisseria gonorrhoeae to adhere to and invade female genital epithelial cells. Cell Microbiol. 2001, 3, 681–691, doi:10.1046/j.1462-5822.2001.00147.x.
[270]
Minor, S.Y.; Banerjee, A.; Gotschlich, E.C. Effect of alpha-oligosaccharide phenotype of Neisseria gonorrhoeae strain MS11 on invasion of Chang conjunctival, HEC-1-B endometrial, and ME-180 cervical cells. Infect. Immun. 2000, 68, 6526–6534, doi:10.1128/IAI.68.12.6526-6534.2000.
[271]
Bessen, D.; Gotschlich, E.C. Interactions of gonococci with HeLa cells: Attachment, detachment, replication, penetration, and the role of protein II. Infect. Immun. 1986, 54, 154–160.
Pruthi, V.; Al-Janabi, A.; Pereira, B.M. Characterization of biofilm formed on intrauterine devices. Indian J. Med. Microbiol. 2003, 21, 161–165.
[276]
Steichen, C.T.; Shao, J.Q.; Ketterer, M.R.; Apicella, M.A. Gonococcal cervicitis: A role for biofilm in pathogenesis. J. Infect. Dis. 2008, 198, 1856–1861, doi:10.1086/593336.
[277]
Falsetta, M.L.; Steichen, C.T.; McEwan, A.G.; Cho, C.; Ketterer, M.; Shao, J.; Hunt, J.; Jennings, M.P.; Apicella, M.A. The composition and metabolic phenotype of Neisseria gonorrhoeae biofilms. Front. Microbiol. 2011, 2, 75:1–75:11.
[278]
Shaw, J.H.; Falkow, S. Model for invasion of human tissue culture cells by Neisseria gonorrhoeae. Infect. Immun. 1988, 56, 1625–1632.
[279]
Christodoulides, M.; Everson, J.S.; Liu, B.L.; Lambden, P.R.; Watt, P.J.; Thomas, E.J.; Heckels, J.E. Interaction of primary human endometrial cells with Neisseria gonorrhoeae expressing green fluorescent protein. Mol. Microbiol. 2000, 35, 32–43, doi:10.1046/j.1365-2958.2000.01694.x.
Griffiss, J.M.; Lammel, C.J.; Wang, J.; Dekker, N.P.; Brooks, G.F. Neisseria gonorrhoeae coordinately uses Pili and Opa to activate HEC-1-B cell microvilli, which causes engulfment of the gonococci. Infect. Immun. 1999, 67, 3469–3480.
[283]
Timmerman, M.M.; Shao, J.Q.; Apicella, M.A. Ultrastructural analysis of the pathogenesis of Neisseria gonorrhoeae endometrial infection. Cell Microbiol. 2005, 7, 627–636, doi:10.1111/j.1462-5822.2005.00491.x.
[284]
McCormack, W.M. Pelvic inflammatory disease. N. Engl. J. Med. 1994, 330, 115–119, doi:10.1056/NEJM199401133300207.
[285]
Ward, M.E.; Watt, P.J.; Robertson, J.N. The human fallopian tube: A laboratory model for gonococcal infection. J. Infect. Dis. 1974, 129, 650–659, doi:10.1093/infdis/129.6.650.
Gorby, G.L.; Schaefer, G.B. Effect of attachment factors (pili plus Opa) on Neisseria gonorrhoeae invasion of human fallopian tube tissue in vitro: Quantitation by computerized image analysis. Microb. Pathog. 1992, 13, 93–108, doi:10.1016/0882-4010(92)90070-5.
[288]
Velasquez, L.; Garcia, K.; Morales, F.; Heckels, J.E.; Orihuela, P.; Rodas, P.I.; Christodoulides, M.; Cardenas, H. Neisseria gonorrhoeae pilus attenuates cytokine response of human fallopian tube explants. J. Biomed. Biotechnol. 2012, 2012, 491298: 1–491298:7.
[289]
Dekker, N.P.; Lammel, C.J.; Mandrell, R.E.; Brooks, G.F. Opa (protein II) influences gonococcal organization in colonies, surface appearance, size and attachment to human fallopian tube tissues. Microb. Pathog. 1990, 9, 19–31, doi:10.1016/0882-4010(90)90037-Q.
[290]
Quan, D.N.; Cooper, M.D.; Potter, J.L.; Roberts, M.H.; Cheng, H.; Jarvis, G.A. TREM-2 binds to lipooligosaccharides of Neisseria gonorrhoeae and is expressed on reproductive tract epithelial cells. Mucosal. Immunol. 2008, 1, 229–238, doi:10.1038/mi.2008.1.
Morales, P.; Reyes, P.; Vargas, M.; Rios, M.; Imarai, M.; Cardenas, H.; Croxatto, H.; Orihuela, P.; Vargas, R.; Fuhrer, J.; et al. Infection of human fallopian tube epithelial cells with Neisseria gonorrhoeae protects cells from tumor necrosis factor alpha-induced apoptosis. Infect. Immun. 2006, 74, 3643–3650, doi:10.1128/IAI.00012-06.
[293]
Britigan, B.E.; Cohen, M.S.; Sparling, P.F. Gonococcal infection: A model of molecular pathogenesis. N. Engl. J. Med. 1985, 312, 1683–1694, doi:10.1056/NEJM198506273122606.
[294]
Morello, J.A.; Bohnhoff, M. Serovars and serum resistance of Neisseria gonorrhoeae from disseminated and uncomplicated infections. J. Infect. Dis. 1989, 160, 1012–1017, doi:10.1093/infdis/160.6.1012.
[295]
Rechner, C.; Kuhlewein, C.; Muller, A.; Schild, H.; Rudel, T. Host glycoprotein Gp96 and scavenger receptor SREC interact with PorB of disseminating Neisseria gonorrhoeae in an epithelial invasion pathway. Cell Host. Microbe 2007, 2, 393–403, doi:10.1016/j.chom.2007.11.002.
[296]
Van Deuren, M.; Brandtzaeg, P.; van der Meer, J. Update on meningococcal disease with emphasis on pathogenesis and clinical management. Clin. Microbiol. Rev. 2000, 13, 144–166, doi:10.1128/CMR.13.1.144-166.2000.
[297]
Schneider, M.C.; Exley, R.M.; Ram, S.; Sim, R.B.; Tang, C.M. Interactions between Neisseria meningitidis and the complement system. Trends Microbiol. 2007, 15, 233–240, doi:10.1016/j.tim.2007.03.005.
[298]
Kugelberg, E.; Gollan, B.; Tang, C.M. Mechanisms in Neisseria meningitidis for resistance against complement-mediated killing. Vaccine 2008, 26, I34–I39.
[299]
Stephens, D.S.; Edwards, K.M.; Morris, F.M.G. Pili and outer membrane appendages on Neisseria meningitidis in the cerebrospinal fluid of an infant. J. Infect. Dis. 1982, 146, 568, doi:10.1093/infdis/146.4.568.
[300]
Devoe, I.W. The meningococcus and mechanisms of pathogenicity. Microbiol. Rev. 1982, 46, 162–190.
[301]
Brandtzaeg, P.; van Deuren, M. Current concepts in the role of the host response in Neisseria meningitidis septic shock. Curr. Opin. Infect. Dis. 2002, 15, 247–252, doi:10.1097/00001432-200206000-00006.
[302]
Jarva, H.; Ram, S.; Vogel, U.; Blom, A.M.; Meri, S. Binding of the complement inhibitor C4bp to serogroup B Neisseria meningitidis. J. Immunol. 2005, 174, 6299–6307.
[303]
Madico, G.; Welsch, J.A.; Lewis, L.A.; McNaughton, A.; Perlman, D.H.; Costello, C.E.; Ngampasutadol, J.; Vogel, U.; Granoff, D.M.; Ram, S. The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance. J. Immunol. 2006, 177, 501–510.
[304]
Lewis, L.A.; Ngampasutadol, J.; Wallace, R.; Reid, J.E.; Vogel, U.; Ram, S. The meningococcal vaccine candidate neisserial surface protein A (NspA) binds to factor H and enhances meningococcal resistance to complement. PLoS Pathog 2010, 6, e1001027:1–e1001027:20.
[305]
Ram, S.; McQuillen, D.P.; Gulati, S.; Elkins, C.; Pangburn, M.K.; Rice, P.A. Binding of complement factor H to loop 5 of porin protein 1A: A molecular mechanism of serum resistance of nonsialylated Neisseria gonorrhoeae. J. Exp. Med. 1998, 188, 671–680.
[306]
Ram, S.; Sharma, A.K.; Simpson, S.D.; Gulati, S.; McQuillen, D.P.; Pangburn, M.K.; Rice, P.A. A novel sialic acid binding site on factor H mediates serum resistance of sialylated Neisseria gonorrhoeae. J. Exp. Med. 1998, 187, 743–752, doi:10.1084/jem.187.5.743.
[307]
Ram, S.; Cullinane, M.; Blom, A.M.; Gulati, S.; McQuillen, D.P.; Monks, B.G.; O’Connell, C.; Boden, R.; Elkins, C.; Pangburn, M.K.; et al. Binding of C4b-binding protein to porin: A molecular mechanism of serum resistance of Neisseria gonorrhoeae. J. Exp. Med. 2001, 193, 281–295, doi:10.1084/jem.193.3.281.
[308]
Sjolinder, H.; Eriksson, J.; Maudsdotter, L.; Aro, H.; Jonsson, A.B. Meningococcal outer membrane protein NhhA is essential for colonization and disease by preventing phagocytosis and complement attack. Infect. Immun. 2008, 76, 5412–5420, doi:10.1128/IAI.00478-08.
[309]
Estabrook, M.M.; Jack, D.L.; Klein, N.J.; Jarvis, G.A. Mannose-binding lectin binds to two major outer membrane proteins, opacity protein and porin, of Neisseria meningitidis. J. Immunol. 2004, 172, 3784–3792.
[310]
Devyatyarova-Johnson, M.; Rees, I.H.; Robertson, B.D.; Turner, M.W.; Klein, N.J.; Jack, D.L. The lipopolysaccharide structures of Salmonella enterica serovar Typhimurium and Neisseria gonorrhoeae determine the attachment of human mannose-binding lectin to intact organisms. Infect. Immun. 2000, 68, 3894–3899.
[311]
Melican, K.; Michea, V.P.; Martin, T.; Bruneval, P.; Dumenil, G. Adhesion of Neisseria meningitidis to dermal vessels leads to local vascular damage and purpura in a humanized mouse model. PLoS Pathog. 2013, 9, e1003139:1–e1003139:11.
[312]
Sa E Cunha, C.; Griffiths, N.J.; Virji, M. Neisseria meningitidis Opc invasin binds to the sulphated tyrosines of activated vitronectin to attach to and invade human brain endothelial cells. PLoS Pathog. 2010, 6, e1000911:1–e1000911:18.
[313]
Muenzner, P.; Naumann, M.; Meyer, T.F.; Gray-Owen, S.D. Pathogenic Neisseria trigger expression of their carcinoembryonic antigen-related cellular adhesion molecule 1 (CEACAM1; previously CD66a) receptor on primary endothelial cells by activating the immediate early response transcription factor, nuclear factor-kappaB. J. Biol. Chem. 2001, 276, 24331–24340.
[314]
Soyer, M.; Dumenil, G. A laminar-Flow Chamber Assay for Measuring Bacterial Adhesion under Shear Stress. In Neisseria meningitidis: Advanced Methods and Protocols; Christodoulides, M., Ed.; Humana Press: New York, NY, USA, 2012. Chapter 12; pp. 185–195.
Coureuil, M.; Lecuyer, H.; Scott, M.G.; Boularan, C.; Enslen, H.; Soyer, M.; Mikaty, G.; Bourdoulous, S.; Nassif, X.; Marullo, S. Meningococcus Hijacks a beta2-adrenoceptor/beta-Arrestin pathway to cross brain microvasculature endothelium. Cell 2010, 143, 1149–1160.
[317]
Lecuyer, H.; Nassif, X.; Coureuil, M. Two strikingly different signaling pathways are induced by meningococcal type IV pili on endothelial and epithelial cells. Infect. Immun. 2012, 80, 175–186, doi:10.1128/IAI.05837-11.
[318]
Brissac, T.; Mikaty, G.; Dumenil, G.; Coureuil, M.; Nassif, X. The meningococcal minor pilin PilX is responsible for type IV pilus conformational changes associated with signaling to endothelial cells. Infect. Immun. 2012, 80, 3297–3306, doi:10.1128/IAI.00369-12.
[319]
Virji, M.; Kayhty, H.; Ferguson, D.J.; Alexandrescu, C.; Heckels, J.E.; Moxon, E.R. The role of pili in the interactions of pathogenic Neisseria with cultured human endothelial cells. Mol. Microbiol. 1991, 5, 1831–1841, doi:10.1111/j.1365-2958.1991.tb00807.x.
[320]
Scheuerpflug, I.; Rudel, T.; Ryll, R.; Pandit, J.; Meyer, T.F. Roles of PilC and PilE proteins in pilus-mediated adherence of Neisseria gonorrhoeae and Neisseria meningitidis to human erythrocytes and endothelial and epithelial cells. Infect. Immun. 1999, 67, 834–843.
[321]
Kupsch, E.M.; Knepper, B.; Kuroki, T.; Heuer, I.; Meyer, T.F. Variable opacity (Opa) outer membrane proteins account for the cell tropisms displayed by Neisseria gonorrhoeae for human leukocytes and epithelial cells. EMBO J. 1993, 12, 641–650.
[322]
McNeil, G.; Virji, M. Phenotypic variants of meningococci and their potential in phagocytic interactions: The influence of opacity proteins, pili, PilC and surface sialic acids. Microb. Pathog. 1997, 22, 295–304, doi:10.1006/mpat.1996.0126.
[323]
Swanson, J.; Sparks, E.; Young, D.; King, G. Young, D.; King, G. Studies on Gonococcus infection. X. Pili and leukocyte association factor as mediators of interactions between gonococci and eukaryotic cells in vitro. Infect. Immun. 1975, 11, 1352–1361.
[324]
Soderholm, N.; Vielfort, K.; Hultenby, K.; Aro, H. Pathogenic Neisseria hitchhike on the uropod of human neutrophils. PLoS One 2011, 6, e24353:1–e24353:12.
[325]
Johnson, M.B.; Criss, A.K. Resistance of Neisseria gonorrhoeae to neutrophils. Front. Microbiol. 2011, 2, 77:1–77:12.
[326]
Sadarangani, M.; Pollard, A.J.; Gray-Owen, S.D. Opa proteins and CEACAMs: Pathways of immune engagement for pathogenic Neisseria. FEMS Microbiol. Rev. 2011, 35, 498–514, doi:10.1111/j.1574-6976.2010.00260.x.
[327]
Criss, A.K.; Seifert, H.S. A bacterial siren song: Intimate interactions between Neisseria and neutrophils. Nat. Rev. Microbiol. 2012, 10, 178–190, doi:10.1038/nrmicro2713.
[328]
Wiertz, E.J.; Delvig, A.; Donders, E.M.; Brugghe, H.F.; van Unen, L.M.; Timmermans, H.A.; Achtman, M.; Hoogerhout, P.; Poolman, J.T. T-cell responses to outer membrane proteins of Neisseria meningitidis: Comparative study of the Opa, Opc, and PorA proteins. Infect. Immun. 1996, 64, 298–304.
Boulton, I.C.; Gray-Owen, S.D. Neisserial binding to CEACAM1 arrests the activation and proliferation of CD4+ T lymphocytes. Nat. Immunol. 2002, 3, 229–236, doi:10.1038/ni769.
[331]
Mandrell, R.E.; Zollinger, W.D. Human immune response to meningococcal outer membrane protein epitopes after natural infection or vaccination. Infect. Immun. 1989, 57, 1590–1598.
[332]
Pantelic, M.; Kim, Y.J.; Bolland, S.; Chen, I.; Shively, J.; Chen, T. Neisseria gonorrhoeae kills carcinoembryonic antigen-related cellular adhesion molecule 1 (CD66a)-expressing human B cells and inhibits antibody production. Infect. Immun. 2005, 73, 4171–4179.
[333]
Al-Bader, T.; Jolley, K.A.; Humphries, H.E.; Holloway, J.; Heckels, J.E.; Semper, A.E.; Friedmann, P.S.; Christodoulides, M. Activation of human dendritic cells by the PorA protein of Neisseria meningitidis. Cell Microbiol. 2004, 6, 651–662, doi:10.1111/j.1462-5822.2004.00392.x.
[334]
Franzoso, S.; Mazzon, C.; Sztukowska, M.; Cecchini, P.; Kasic, T.; Capecchi, B.; Tavano, R.; Papini, E. Human monocytes/macrophages are a target of Neisseria meningitidis Adhesin A (NadA). J. Leukoc. Biol. 2008, 83, 1100–1110, doi:10.1189/jlb.1207810.
[335]
Sjolinder, M.; Altenbacher, G.; Hagner, M.; Sun, W.; Schedin-Weiss, S.; Sjolinder, H. Meningococcal outer membrane protein NhhA triggers apoptosis in macrophages. PLoS One 2012, 7, e29586:1–e29586:8.
Jones, C.; Virji, M.; Crocker, P.R. Recognition of sialylated meningococcal lipopolysaccharide by siglecs expressed on myeloid cells leads to enhanced bacterial uptake. Mol. Microbiol. 2003, 49, 1213–1225, doi:10.1046/j.1365-2958.2003.03634.x.
[338]
Peiser, L.; Makepeace, K.; Pluddemann, A.; Savino, S.; Wright, J.C.; Pizza, M.; Rappuoli, R.; Moxon, E.R.; Gordon, S. Identification of Neisseria meningitidis nonlipopolysaccharide ligands for class A macrophage scavenger receptor by using a novel assay. Infect. Immun. 2006, 74, 5191–5199, doi:10.1128/IAI.00124-06.
[339]
Casey, R.; Newcombe, J.; McFadden, J.; Bodman-Smith, K.B. The acute-phase reactant C-reactive protein binds to phosphorylcholine-expressing Neisseria meningitidis and increases uptake by human phagocytes. Infect. Immun. 2008, 76, 1298–1304.
Zimmer, S.M.; Zughaier, S.M.; Tzeng, Y.L.; Stephens, D.S. Human MD-2 discrimination of meningococcal lipid A structures and activation of TLR4. Glycobiology 2007, 17, 847–856, doi:10.1093/glycob/cwm057.
[342]
DeMarco, M.L.; Woods, R.J. From agonist to antagonist: Structure and dynamics of innate immune glycoprotein MD-2 upon recognition of variably acylated bacterial endotoxins. Mol. Immunol. 2011, 49, 124–133, doi:10.1016/j.molimm.2011.08.003.
[343]
Lu, R.; Pan, H.; Shively, J.E. CEACAM1 negatively regulates IL-1beta production in LPS activated neutrophils by recruiting SHP-1 to a SYK-TLR4-CEACAM1 complex. PLoS Pathog. 2012, 8, e1002597:1–e1002597:15.
[344]
Massari, P.; Visintin, A.; Gunawardana, J.; Halmen, K.A.; King, C.A.; Golenbock, D.T.; Wetzler, L.M. Meningococcal porin PorB binds to TLR2 and requires TLR1 for signaling. J. Immunol. 2006, 176, 2373–2380.
[345]
Wetzler, L.M. Innate immune function of the neisserial porins and the relationship to vaccine adjuvant activity. Fut. Microbiol. 2010, 5, 749–758, doi:10.2217/fmb.10.41.
[346]
Macleod, H.; Bhasin, N.; Wetzler, L.M. Role of protein tyrosine kinase and Erk1/2 activities in the Toll-like receptor 2-induced cellular activation of murine B cells by neisserial porin. Clin. Vaccine Immunol. 2008, 15, 630–637, doi:10.1128/CVI.00435-07.
[347]
Singleton, T.E.; Massari, P.; Wetzler, L.M. Neisserial porin-induced dendritic cell activation is MyD88 and TLR2 dependent. J. Immunol. 2005, 174, 3545–3550.
[348]
Sjolinder, M.; Altenbacher, G.; Wang, X.; Gao, Y.; Hansson, C.; Sjolinder, H. The meningococcal adhesin NhhA provokes proinflammatory responses in macrophages via toll-like receptor 4-dependent and -independent pathways. Infect. Immun. 2012, 80, 4027–4033.
[349]
Chu, C.L.; Yu, Y.L.; Kung, Y.C.; Liao, P.Y.; Liu, K.J.; Tseng, Y.T.; Lin, Y.C.; Hsieh, S.S.; Chong, P.C.; Yang, C.Y. The immunomodulatory activity of meningococcal lipoprotein Ag473 depends on the conformation made up of the lipid and protein moieties. PLoS One 2012, 7, e40873:1–e40873:11.
[350]
Hill, M.; Deghmane, A.E.; Segovia, M.; Zarantonelli, M.L.; Tilly, G.; Blancou, P.; Beriou, G.; Josien, R.; Anegon, I.; Hong, E.; et al. Penicillin binding proteins as danger signals: Meningococcal penicillin binding protein 2 activates dendritic cells through Toll-like receptor 4. PLoS One 2011, 6, e23995:1–e23995:11.
[351]
Cecchini, P.; Tavano, R.; Polverino de, L.P.; Franzoso, S.; Mazzon, C.; Montanari, P.; Papini, E. The soluble recombinant Neisseria meningitidis adhesin NadA(Delta351–405) stimulates human monocytes by binding to extracellular Hsp90. PLoS One 2011, 6, e25089:1–e25089:13.
[352]
Zughaier, S.M. Neisseria meningitidis capsular polysaccharides induce inflammatory responses via TLR2 and TLR4-MD-2. J. Leukoc. Biol. 2011, 89, 469–480, doi:10.1189/jlb.0610369.
[353]
Ingalls, R.R.; Lien, E.; Golenbock, D.T. Membrane-associated proteins of a lipopolysaccharide-deficient mutant of Neisseria meningitidis activate the inflammatory response through toll-like receptor 2. Infect. Immun. 2001, 69, 2230–2236, doi:10.1128/IAI.69.4.2230-2236.2001.
[354]
Pridmore, A.C.; Wyllie, D.H.; Abdillahi, F.; Steeghs, L.; van der Ley, P.; Dower, S.K.; Read, R.C. A lipopolysaccharide-deficient mutant of Neisseria meningitidis elicits attenuated cytokine release by human macrophages and signals via toll-like receptor (TLR) 2 but not via TLR4/MD2. J. Infect. Dis. 2001, 183, 89–96, doi:10.1086/317647.
[355]
Fisette, P.L.; Ram, S.; Andersen, J.M.; Guo, W.; Ingalls, R.R. The Lip lipoprotein from Neisseria gonorrhoeae stimulates cytokine release and NF-kappaB activation in epithelial cells in a Toll-like receptor 2-dependent manner. J. Biol. Chem. 2003, 278, 46252–46260.
[356]
Liu, X.; Wetzler, L.M.; Nascimento, L.O.; Massari, P. Human airway epithelial cell responses to Neisseria lactamica and purified porin via Toll-like receptor 2-dependent signaling. Infect. Immun. 2010, 78, 5314–5323, doi:10.1128/IAI.00681-10.
[357]
Toussi, D.N.; Carraway, M.; Wetzler, L.M.; Lewis, L.A.; Liu, X.; Massari, P. The amino acid sequence of Neisseria lactamica PorB surface-exposed loops influences Toll-like receptor 2-dependent cell activation. Infect. Immun. 2012, 80, 3417–3428, doi:10.1128/IAI.00683-12.
[358]
Pron, B.; Taha, M.K.; Rambaud, C.; Fournet, J.C.; Pattey, N.; Monnet, J.P.; Musilek, M.; Beretti, J.L.; Nassif, X. Interaction of Neisseria maningitidis with the components of the blood-brain barrier correlates with an increased expression of PilC. J. Infect. Dis. 1997, 176, 1285–1292.
[359]
Sjolinder, H.; Jonsson, A.B. Olfactory nerve—A novel invasion route of Neisseria meningitidis to reach the meninges. PLoS One 2010, 5, e14034:1–e14034:10.
[360]
Christodoulides, M.; Heckels, J.E.; Weller, R.O. The Role of the Leptomeninges in Meningococcal Meningitis. In Emerging Strategies in the Fight against Meningitis; Ferreiros, C., Criado, M.T., Vazquez, J., Eds.; Horizon Press: Norfolk, UK, 2002; pp. 1–37.
Feurer, D.J.; Weller, R.O. Barrier functions of the leptomeninges: A study of normal meninges and meningiomas in tissue culture. Neuropathol. Appl. Neurobiol. 1991, 17, 391–405, doi:10.1111/j.1365-2990.1991.tb00739.x.
[364]
Alcolado, R.; Weller, R.O.; Parrish, E.P.; Garrod, D. The cranial arachnoid and pia mater in man: Anatomical and ultrastructural observations. Neuropathol. Appl. Neurobiol. 1988, 14, 1–17, doi:10.1111/j.1365-2990.1988.tb00862.x.
[365]
Kleihues, P.; Cavenee, W.K. Pathology and Genetics of Tumours of the Nervous System; IARC press: Lyon, France, 1997.
[366]
Hardy, S.J.; Christodoulides, M.; Weller, R.O.; Heckels, J.E. Interactions of Neisseria meningitidis with cells of the human meninges. Mol. Microbiol. 2000, 36, 817–829, doi:10.1046/j.1365-2958.2000.01923.x.
[367]
Fowler, M.I.; Yin, K.Y.; Humphries, H.E.; Heckels, J.E.; Christodoulides, M. Comparison of the inflammatory responses of human meningeal cells following challenge withNeisseria lactamica and with Neisseria meningitidis. Infect. Immun. 2006, 74, 6467–6478, doi:10.1128/IAI.00644-06.
Del Rio, C.; Stephens, D.S.; Knapp, J.S.; Rice, R.J.; Schalla, W.O. Comparison of isolates of Neisseria gonorrhoeae causing meningitis and report of gonococcal meningitis in a patient with C8 deficiency. J. Clin. Microbiol. 1989, 27, 1045–1049.
[370]
Virji, M.; Alexandrescu, C.; Ferguson, D.J.; Saunders, J.R.; Moxon, E.R. Variations in the expression of pili: The effect on adherence of Neisseria meningitidis to human epithelial and endothelial cells. Mol. Microbiol. 1992, 6, 1271–1279, doi:10.1111/j.1365-2958.1992.tb00848.x.
[371]
Nassif, X.; Lowy, J.; Stenberg, P.; O’Gaora, P.; Ganji, A.; So, M. Antigenic variation of pilin regulates adhesion of Neisseria meningitidis to human epithelial cells. Mol. Microbiol. 1993, 8, 719–725, doi:10.1111/j.1365-2958.1993.tb01615.x.
[372]
Virji, M.; Stimson, E.; Makepeace, K.; Dell, A.; Morris, H.R.; Payne, G.; Saunders, J.R.; Moxon, E.R. Posttranslational modifications of meningococcal pili. Identification of a common trisaccharide substitution on variant pilins of strain C311. Ann. N. Y. Acad. Sci. 1996, 797, 53–64.
[373]
Weiser, J.N.; Goldberg, J.B.; Pan, N.; Wilson, L.; Virji, M. The phosphorylcholine epitope undergoes phase variation on a 43-kilodalton protein in Pseudomonas aeruginosa and on pili of Neisseria meningitidis and Neisseria gonorrhoeae. Infect. Immun. 1998, 66, 4263–4267.
[374]
Marceau, M.; Beretti, J.L.; Nassif, X. High adhesiveness of encapsulated Neisseria meningitidis to epithelial cells is associated with the formation of bundles of pili. Mol. Microbiol. 1995, 17, 855–863.
[375]
Humphries, H.E.; Triantafilou, M.; Makepeace, B.L.; Heckels, J.E.; Triantafilou, K.; Christodoulides, M. Activation of human meningeal cells is modulated by lipopolysaccharide (LPS) and non-LPS components of Neisseria meningitidis and is independent of Toll-like receptor (TLR)4 and TLR2 signalling. Cell Microbiol. 2005, 7, 415–430, doi:10.1111/j.1462-5822.2004.00471.x.
[376]
Dietrich, G.; Kurz, S.; Hubner, C.; Aepinus, C.; Theiss, S.; Guckenberger, M.; Panzner, U.; Weber, J.; Frosch, M. Transcriptome analysis of Neisseria meningitidis during infection. J. Bacteriol. 2003, 185, 155–164, doi:10.1128/JB.185.1.155-164.2003.
[377]
Schubert-Unkmeir, A.; Sokolova, O.; Panzner, U.; Eigenthaler, M.; Frosch, M. Gene expression pattern in human brain endothelial cells in response to Neisseria meningitidis. Infect. Immun. 2007, 75, 899–914, doi:10.1128/IAI.01508-06.
[378]
Schubert-Unkmeir, A.; Slanina, H.; Frosch, M. Mammalian cell transcriptome in response to meningitis-causing pathogens. Expert Rev. Mol. Diagn. 2009, 9, 833–842, doi:10.1586/erm.09.68.
[379]
Echenique-Rivera, H.; Muzzi, A.; Del Tordello, E.; Seib, K.L.; Francois, P.; Rappuoli, R.; Pizza, M.; Serruto, D. Transcriptome analysis of Neisseria meningitidis in human whole blood and mutagenesis studies identify virulence factors involved in blood survival. PLoS Pathog. 2011, 7, e10002027:1–e10002027:18.
[380]
Del, T.E.; Serruto, D. Functional genomics studies of the human pathogen Neisseria meningitidis. Brief. Funct. Genomics 2013, doi:10.1093/bfgp/elt018.
[381]
Merz, A.J.; So, M. Interactions of pathogenic Neisseriae with epithelial cell membranes. Annu. Rev. Cell. Dev. Biol. 2000, 16, 423–457.
[382]
Pujol, C.; Eugene, E.; Morand, P.; Nassif, X. Do pathogenic Neisseriae need several ways to modify the host cell cytoskeleton? Microbes Infect. 2000, 2, 821–827, doi:10.1016/S1286-4579(00)90367-8.
[383]
Virji, M. Pathogenic Neisseriae: Surface modulation, pathogenesis and infection control. Nat. Rev. Microbiol. 2009, 7, 274–286, doi:10.1038/nrmicro2097.
Hill, D.J.; Virji, M. Meningococcal ligands and molecular targets of the host. In Neisseria meningitidis: Advanced Methods and Protocols; Christodoulides, M., Ed.; Humana Press: New York, NY, USA, 2012. Chapter 9; pp. 143–152.
[386]
Miller, F.; Lecuyer, H.; Join-Lambert, O.; Bourdoulous, S.; Marullo, S.; Nassif, X.; Coureuil, M. Neisseria meningitidis colonization of the brain endothelium and cerebrospinal fluid invasion. Cell Microbiol. 2013, 15, 512–519, doi:10.1111/cmi.12082.
[387]
Serruto, D.; Bottomley, M.J.; Ram, S.; Giuliani, M.M.; Rappuoli, R. The new multicomponent vaccine against meningococcal serogroup B, 4CMenB: Immunological, functional and structural characterization of the antigens. Vaccine 2012, 30, B87–B97, doi:10.1016/j.vaccine.2012.01.033.
[388]
Mcneil, L.K.; Zagursky, R.J.; Lin, S.L.; Murphy, E.; Zlotnick, G.W.; Hoiseth, S.K.; Jansen, K.U.; Anderson, A.S. Role of Factor H binding protein in Neisseria meningitidis virulence and its potential as a vaccine candidate to broadly protect against meningococcal disease. Microbiol. Mol. Biol. Rev. 2013, 77, 234–252.
[389]
Marri, P.R.; Paniscus, M.; Weyand, N.J.; Rendon, M.A.; Calton, C.M.; Hernandez, D.R.; Higashi, D.L.; Sodergren, E.; Weinstock, G.M.; Rounsley, S.D.; et al. Genome sequencing reveals widespread virulence gene exchange among human Neisseria species. PLoS One 2010, 5, e11835:1–e11835:9.
[390]
Deasy, A.; Dale, A.; Evans, C.; Guccione, E.; Andrews, N.; Gorringe, A.; Read, R. Induced Nasopharyngeal Colonisation with Neisseria lactamica Protects against Carriage of Neisseria meningitidis in Healthy Adult Volunteers. In Proceedings of the XVIIIth International Pathogenic Neisseria Conference (IPNC), Wurzberg, Germany, 9–14th September 2012; p. 100.
