全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用：99美元
投递稿件

查看量下载量

相关文章

更多...

Scabies Mite Peritrophins Are Potential Targets of Human Host Innate Immunity

DOI: 10.1371/journal.pntd.0001331

Full-Text   Cite this paper   Add to My Lib

Abstract:

Background Pruritic scabies lesions caused by Sarcoptes scabiei burrowing in the stratum corneum of human skin facilitate opportunistic bacterial infections. Emerging resistance to current therapeutics emphasizes the need to identify novel targets for protective intervention. We have characterized several protein families located in the mite gut as crucial factors for host-parasite interactions. Among these multiple proteins inhibit human complement, presumably to avoid complement-mediated damage of gut epithelial cells. Peritrophins are major components of the peritrophic matrix often found in the gut of arthropods. We hypothesized that a peritrophin, if abundant in the scabies mite gut, could be an activator of complement. Methodology/Principal Findings A novel full length scabies mite peritrophin (SsPTP1) was identified in a cDNA library from scabies mites. The amino acid sequence revealed four putative chitin binding domains (CBD). Recombinant expression of one CBD of the highly repetitive SsPTP1 sequence as TSP-hexaHis-fusion protein resulted in soluble protein, which demonstrated chitin binding activity in affinity chromatography assays. Antibodies against a recombinant SsPTP1 fragment were used to immunohistochemically localize native SsPTP1 in the mite gut and in fecal pellets within the upper epidermis, co-localizing with serum components such as host IgG and complement. Enzymatic deglycosylation confirmed strong N- and O-glycosylation of the native peritrophin. Serum incubation followed by immunoblotting with a monoclonal antibody against mannan binding lectin (MBL), the recognition molecule of the lectin pathway of human complement activation, indicated that MBL may specifically bind to glycosylated SsPTP1. Conclusions/Significance This study adds a new aspect to the accumulating evidence that complement plays a major role in scabies mite biology. It identifies a novel peritrophin localized in the mite gut as a potential target of the lectin pathway of the complement cascade. These initial findings indicate a novel role of scabies mite peritrophins in triggering a host innate immune response within the mite gut.

 References

[1]  Hengge UR, Currie BJ, J？ger G, Lupi O, Schwartz RA (2006) Scabies: a ubiquitous neglected skin disease. The Lancet Infectious Diseases 6: 769–779. doi: 10.1016/S1473-3099(06)70654-5
[2]  Arlian LG (1989) Biology, host relations and epidemiology of Sarcoptes scabiei. Annual Review of Entomology 34: 139–161. doi: 10.1146/annurev.ento.34.1.139
[3]  Mellanby K (1944) The development of symptoms, parasitic infection and immunity in human scabies. Parasitology 35: 197–206. doi: 10.1017/s0031182000021612
[4]  Walton SF, Holt DC, Currie BJ, Kemp DJ, Baker , et al. (2004) Scabies: New Future for a Neglected Disease. Advances in Parasitology: Academic Press. pp. 309–376.
[5]  Currie BJ, Carapetis JR (2000) Skin infections and infestations in Aboriginal communities in northern Australia. Australas J Dermatol 41: 139–143; quiz 144–135. doi: 10.1046/j.1440-0960.2000.00417.x
[6]  Clucas DB, Carville KS, Connors C, Currie BJ, Carapetis JR, et al. (2008) Disease burden and health-care clinic attendances for young children in remote aboriginal communities of northern Australia. Bull World Health Organ 86: 275–281. doi: 10.2471/BLT.07.043034
[7]  McDonald M, Currie BJ, Carapetis JR (2004) Acute rheumatic fever: a chink in the chain that links the heart to the throat? Lancet Infect Dis 4: 240–245. doi: 10.1016/S1473-3099(04)00975-2
[8]  Mounsey K, Holt D, McCarthy J, Currie B, Walton S (2008) Scabies: molecular perspectives and therapeutic implications in the face of emerging drug resistance. Future Microbiol 3: 57–66. doi: 10.2217/17460913.3.1.57
[9]  Fischer K, Holt DC, Harumal P, Currie BJ, Walton SF, et al. (2003) Generation and characterization of cDNA clones from Sarcoptes scabiei var. hominis for an expressed sequence tag library: identification of homologues of house dust mite allergens. American Journal of Tropical Medicine and Hygiene 68: 61–64.
[10]  Fischer K, Holt DC, Wilson P, Davis J, Hewitt V, et al. (2003) Normalization of a cDNA library cloned in lambda ZAP by a long PCR and cDNA reassociation procedure. BioTechniques 34: 250–252, 254.
[11]  Harumal P, Morgan M, Walton SF, Holt DC, Rode J, et al. (2003) Identification of a homologue of a house dust mite allergen in a cDNA library from Sarcoptes scabiei var. hominis and evaluation of its vaccine potential in a rabbit/S. scabiei var. canis model. American Journal of Tropical Medicine and Hygiene 68: 54–60.
[12]  Holt DC, Fischer K, Allen GE, Wilson D, Wilson P, et al. (2003) Mechanisms for a novel immune evasion strategy in the scabies mite Sarcoptes scabiei: a multigene family of inactivated serine proteases. J Invest Dermatol 121: 1419–1424. doi: 10.1046/j.1523-1747.2003.12621.x
[13]  Holt DC, Fischer K, Pizzutto SJ, Currie BJ, Walton SF, et al. (2004) A multigene family of inactivated cysteine proteases in Sarcoptes scabiei. J Invest Dermatol 123: 240–241. doi: 10.1111/j.0022-202X.2004.22716.x
[14]  Dougall A, Holt DC, Fischer K, Currie BJ, Kemp DJ, et al. (2005) Identification and characterization of Sarcoptes scabiei and Dermatophagoides pteronyssinus glutathione S-transferases: implication as a potential major allergen in crusted scabies. American Journal of Tropical Medicine and Hygiene 73: 977–984.
[15]  Mounsey KE, Holt DC, McCarthy J, Walton SF (2006) Identification of ABC transporters in Sarcoptes scabiei. Parasitology 132: 883–892. doi: 10.1017/S0031182005009716
[16]  Kemp DH, Pearson RD, Gough JM, Willadsen P (1989) Vaccination against Boophilus microplus: localization of antigens on tick gut cells and their interaction with the host immune system. Exp Appl Acarol 7: 43–58. doi: 10.1007/BF01200452
[17]  Blom AM, Hallstrom T, Riesbeck K (2009) Complement evasion strategies of pathogens-acquisition of inhibitors and beyond. Mol Immunol 46: 2808–2817. doi: 10.1016/j.molimm.2009.04.025
[18]  Botto M, Kirschfink M, Macor P, Pickering MC, Wurzner R, et al. (2009) Complement in human diseases: Lessons from complement deficiencies. Mol Immunol 46: 2774–2783. doi: 10.1016/j.molimm.2009.04.029
[19]  Lambris JD, Ricklin D, Geisbrecht BV (2008) Complement evasion by human pathogens. Nat Rev Microbiol 6: 132–142. doi: 10.1038/nrmicro1824
[20]  Zipfel PF, Wurzner R, Skerka C (2007) Complement evasion of pathogens: common strategies are shared by diverse organisms. Mol Immunol 44: 3850–3857. doi: 10.1016/j.molimm.2007.06.149
[21]  Nunn MA, Sharma A, Paesen GC, Adamson S, Lissina O, et al. (2005) Complement Inhibitor of C5 Activation from the Soft Tick Ornithodoros moubata. J Immunol 174: 2084–2091.
[22]  Ribeiro JC (1987) Ixodes dammini: Salivary anti-complement activity. Experimental Parasitology 64: 347–353. doi: 10.1016/0014-4894(87)90046-4
[23]  Tyson KR, Elkins C, de Silva AM (2008) A novel mechanism of complement inhibition unmasked by a tick salivary protein that binds to properdin. J Immunol 180: 3964–3968.
[24]  Willis C, Fischer K, Walton SF, Currie BJ, Kemp DJ (2006) Scabies mite inactivated serine protease paralogues are present both internally in the mite gut and externally in feces. Am J Trop Med Hyg 75: 683–687.
[25]  Fischer K, Langendorf CG, Irving JA, Reynolds S, Willis C, et al. (2009) Structural mechanisms of inactivation in scabies mite serine protease paralogues. J Mol Biol 390: 635–645. doi: 10.1016/j.jmb.2009.04.082
[26]  Bergstrom FC, Reynolds S, Johnstone M, Pike RN, Buckle AM, et al. (2009) Scabies mite inactivated serine protease paralogs inhibit the human complement system. J Immunol 182: 7809–7817. doi: 10.4049/jimmunol.0804205
[27]  Hegedus D, Erlandson M, Gillott C, Toprak U (2009) New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol 54: 285–302. doi: 10.1146/annurev.ento.54.110807.090559
[28]  Tellam RL, Wijffels G, Willadsen P (1999) Peritrophic matrix proteins. Insect Biochem Mol Biol 29: 87–101. doi: 10.1016/S0965-1748(98)00123-4
[29]  Australian Government NHMRC (2004) Australian code of practice for the care and use of animals for scientific purposes. 7th edition ed. pp. 1–84.
[30]  Pearson MS, Pickering DA, Tribolet L, Cooper L, Mulvenna J, et al. (2010) Neutralizing antibodies to the hookworm hemoglobinase Na-APR-1: implications for a multivalent vaccine against hookworm infection and schistosomiasis. J Infect Dis 201: 1561–1569. doi: 10.1086/651953
[31]  Bradford MM (1976) Rapid and Sensitive Method for Quantitation of Microgram Quantities of Protein Utilizing Principle of Protein-Dye Binding. Analytical Biochemistry 72: 248–254. doi: 10.1016/0003-2697(76)90527-3
[32]  Mounsey K, Ho MF, Kelly A, Willis C, Pasay C, et al. (2010) A tractable experimental model for study of human and animal scabies. PLoS Negl Trop Dis 4: e756. doi: 10.1371/journal.pntd.0000756
[33]  Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410. doi: 10.1016/S0022-2836(05)80360-2
[34]  Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680. doi: 10.1093/nar/22.22.4673
[35]  Jensen LJ, Gupta R, Blom N, Devos D, Tamames J, et al. (2002) Prediction of Human Protein Function from Post-translational Modifications and Localization Features. Journal of Molecular Biology 319: 1257–1265. doi: 10.1016/S0022-2836(02)00379-0
[36]  Julenius K, Molgaard A, Gupta R, Brunak S (2005) Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 15: 153–164. doi: 10.1093/glycob/cwh151
[37]  Rapp CM, Morgan MS, Arlian LG (2006) Presence of host immunoglobulin in the gut of Sarcoptes scabiei (Acari: Sarcoptidae). J Med Entomol 43: 539–542. doi: 10.1603/0022-2585(2006)43[539:POHIIT]2.0.CO;2
[38]  Shi X, Chamankhah M, Visal-Shah S, Hemmingsen SM, Erlandson M, et al. (2004) Modeling the structure of the type I peritrophic matrix: characterization of a Mamestra configurata intestinal mucin and a novel peritrophin containing 19 chitin binding domains. Insect Biochem Mol Biol 34: 1101–1115. doi: 10.1016/j.ibmb.2004.06.015
[39]  Shen Z, Jacobs-Lorena M (1998) A type I peritrophic matrix protein from the malaria vector Anopheles gambiae binds to chitin. Cloning, expression, and characterization. J Biol Chem 273: 17665–17670. doi: 10.1074/jbc.273.28.17665
[40]  Shen Z, Jacobs-Lorena M (1999) Evolution of chitin-binding proteins in invertebrates. J Mol Evol 48: 341–347. doi: 10.1007/PL00006478
[41]  Elvin CM, Vuocolo T, Pearson RD, East IJ, Riding GA, et al. (1996) Characterization of a major peritrophic membrane protein, peritrophin-44, from the larvae of Lucilia cuprina. cDNA and deduced amino acid sequences. J Biol Chem 271: 8925–8935. doi: 10.1074/jbc.271.15.8925
[42]  Kawabata S, Nagayama R, Hirata M, Shigenaga T, Agarwala KL, et al. (1996) Tachycitin, a small granular component in horseshoe crab hemocytes, is an antimicrobial protein with chitin-binding activity. J Biochem 120: 1253–1260. doi: 10.1093/oxfordjournals.jbchem.a021549
[43]  Wang P, Li G, Granados RR (2004) Identification of two new peritrophic membrane proteins from larval Trichoplusia ni: structural characteristics and their functions in the protease rich insect gut. Insect Biochem Mol Biol 34: 215–227. doi: 10.1016/j.ibmb.2003.10.001
[44]  Schorderet S, Pearson RD, Vuocolo T, Eisemann C, Riding GA, et al. (1998) cDNA and deduced amino acid sequences of a peritrophic membrane glycoprotein, ‘peritrophin-48’, from the larvae of Lucilia cuprina. Insect Biochem Mol Biol 28: 99–111. doi: 10.1016/S0965-1748(97)00103-3
[45]  Wang P, Granados RR (2001) Molecular structure of the peritrophic membrane (PM): identification of potential PM target sites for insect control. Arch Insect Biochem Physiol 47: 110–118. doi: 10.1002/arch.1041
[46]  Wijffels G, Eisemann C, Riding G, Pearson R, Jones A, et al. (2001) A novel family of chitin-binding proteins from insect type 2 peritrophic matrix. cDNA sequences, chitin binding activity, and cellular localization. J Biol Chem 276: 15527–15536. doi: 10.1074/jbc.M009393200
[47]  Du XJ, Wang JX, Liu N, Zhao XF, Li FH, et al. (2006) Identification and molecular characterization of a peritrophin-like protein from fleshy prawn (Fenneropenaeus chinensis). Mol Immunol 43: 1633–1644. doi: 10.1016/j.molimm.2005.09.018
[48]  Gaines PJ, Walmsley SJ, Wisnewski N (2003) Cloning and characterization of five cDNAs encoding peritrophin-A domains from the cat flea, Ctenocephalides felis. Insect Biochem Mol Biol 33: 1061–1073. doi: 10.1016/S0965-1748(03)00096-1
[49]  Peters W (1992) Peritrophic Membranes. Berlin: Springer.
[50]  Lehane MJ (1997) Peritrophic matrix structure and function. Annu Rev Entomol 42: 525–550. doi: 10.1146/annurev.ento.42.1.525
[51]  Baines DM (1978) Observations on peritrophic membrane of locusta-migratoria-migratoriodes (R and F) nymphs. Acrida 7: 11–21.
[52]  Ramos A, Mahowald A, Jacobslorena M (1994) Peritrophic matrix of the black fly simulium- vittatum- formation, structure, and analysis of its protein- components. Journal of Experimental Zoology 268: 269–281. doi: 10.1002/jez.1402680403
[53]  Desch CE, Andrews JRH, Arlian LG, editors. (1991) The digestive system of Sarcoptes scabiei (L.): Light and Electron Microscope Study. Prague: SPB Academic Publishing bv, The Hague. pp. 271–279.
[54]  Billingsley PF, Rudin W (1992) The Role of the Mosquito Peritrophic Membrane in Bloodmeal Digestion and Infectivity of Plasmodium Species. Journal of Parasitology 78: 430–440. doi: 10.2307/3283640
[55]  Ricklin D, Hajishengallis G, Yang K, Lambris JD (2010) Complement: a key system for immune surveillance and homeostasis. Nat Immunol 11: 785–797. doi: 10.1038/ni.1923
[56]  Favoreel HW, Van de Walle GR, Nauwynck HJ, Pensaert MB (2003) Virus complement evasion strategies. J Gen Virol 84: 1–15. doi: 10.1099/vir.0.18709-0
[57]  ？wierzko A, Madaliński K, Cedzyński M (2003) The lectin pathway of complement activation. The role of complement in pathological processes and possible strategies of its activity modulation in therapy of some diseases. Central European Journal of Immunology 28: 67–73.
[58]  Turner MW (1996) Mannose-binding lectin: the pluripotent molecule of the innate immune system. Immunol Today 17: 532–540. doi: 10.1016/0167-5699(96)10062-1
[59]  Holmskov U, Malhotra R, Sim RB, Jensenius JC (1994) Collectins: collagenous C-type lectins of the innate immune defense system. Immunol Today 15: 67–74. doi: 10.1016/0167-5699(94)90136-8
[60]  Anders RF, Coppel RL, Brown GV, Kemp DJ (1988) Antigens with repeated amino acid sequences from the asexual blood stages of Plasmodium falciparum. Prog Allergy 41: 148–172. doi: 10.1159/000318618
[61]  Stahl HD, Kemp DJ, Crewther PE, Scanlon DB, Woodrow G, et al. (1985) Sequence of a cDNA encoding a small polymorphic histidine- and alanine-rich protein from Plasmodium falciparum. Nucleic Acids Res 13: 7837–7846. doi: 10.1093/nar/13.21.7837
[62]  Dame JB, Williams JL, McCutchan TF, Weber JL, Wirtz RA, et al. (1984) Structure of the gene encoding the immunodominant surface antigen on the sporozoite of the human malaria parasite Plasmodium falciparum. Science 225: 593–599. doi: 10.1126/science.6204383
[63]  Allen A, Flemstrom G, Garner A, Kivilaakso E (1993) Gastroduodenal Mucosal Protection. Physiological Reviews 73: 823–857.
[64]  Shao L, Devenport M, Fujioka H, Ghosh A, Jacobs-Lorena M (2005) Identification and characterization of a novel peritrophic matrix protein, Ae-Aper50, and the microvillar membrane protein, AEG12, from the mosquito, Aedes aegypti. Insect Biochemistry and Molecular Biology 35: 947–959. doi: 10.1016/j.ibmb.2005.03.012
[65]  Van den Steen P, Rudd PM, Dwek RA, Opdenakker G (1998) Concepts and principles of O-linked glycosylation. Critical Reviews in Biochemistry and Molecular Biology 33: 151–208. doi: 10.1080/10409239891204198
[66]  Arnold JN, Dwek RA, Rudd PM, Sim RB (2006) Mannan binding lectin and its interaction with immunoglobulins in health and in disease. Immunol Lett 106: 103–110. doi: 10.1016/j.imlet.2006.05.007
[67]  Tellam RL, Eisemann CH, Vuocolo T, Casu R, Jarmey J, et al. (2001) Role of oligosaccharides in the immune response of sheep vaccinated with Lucilia cuprina larval glycoprotein, peritrophin-95. Int J Parasitol 31: 798–809. doi: 10.1016/S0020-7519(01)00195-3
[68]  Willadsen P (2006) Vaccination against ectoparasites. Parasitology 133: SupplS9–S25. doi: 10.1017/S0031182006001788
[69]  Manzano-Roman R, Encinas-Grandes A, Perez-Sanchez R (2006) Antigens from the midgut membranes of Ornithodoros erraticus induce lethal anti-tick immune responses in pigs and mice. Vet Parasitol 135: 65–79. doi: 10.1016/j.vetpar.2005.08.004
[70]  Barros VC, Assump？？o JG, Cadete AM, Santos VC, Cavalcante RR, et al. (2009) The Role of Salivary and Intestinal Complement System Inhibitors in the Midgut Protection of Triatomines and Mosquitoes. PLoS ONE 4: e6047. doi: 10.1371/journal.pone.0006047

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133