Glycosylation of viral envelope proteins is important for infectivity and interaction with host immunity, however, our current knowledge of the functions of glycosylation is largely limited to N-glycosylation because it is difficult to predict and identify site-specific O-glycosylation. Here, we present a novel proteome-wide discovery strategy for O-glycosylation sites on viral envelope proteins using herpes simplex virus type 1 (HSV-1) as a model. We identified 74 O-linked glycosylation sites on 8 out of the 12 HSV-1 envelope proteins. Two of the identified glycosites found in glycoprotein B were previously implicated in virus attachment to immune cells. We show that HSV-1 infection distorts the secretory pathway and that infected cells accumulate glycoproteins with truncated O-glycans, nonetheless retaining the ability to elongate most of the surface glycans. With the use of precise gene editing, we further demonstrate that elongated O-glycans are essential for HSV-1 in human HaCaT keratinocytes, where HSV-1 produced markedly lower viral titers in HaCaT with abrogated O-glycans compared to the isogenic counterpart with normal O-glycans. The roles of O-linked glycosylation for viral entry, formation, secretion, and immune recognition are poorly understood, and the O-glycoproteomics strategy presented here now opens for unbiased discovery on all enveloped viruses.
References
[1]
White JM, Delos SE, Brecher M, Schornberg K. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Critical reviews in biochemistry and molecular biology. 2008;43(3):189–219. doi: 10.1080/10409230802058320. pmid:18568847
[2]
Braakman I, van Anken E. Folding of viral envelope glycoproteins in the endoplasmic reticulum. Traffic. 2000;1(7):533–9. pmid:11208140 doi: 10.1034/j.1600-0854.2000.010702.x
[3]
Serafini-Cessi F, Dall'Olio F, Scannavini M, Campadelli-Fiume G. Processing of herpes simplex virus-1 glycans in cells defective in glycosyl transferases of the Golgi system: relationship to cell fusion and virion egress. Virology. 1983;131(1):59–70. pmid:6316656 doi: 10.1016/0042-6822(83)90533-0
[4]
Wang J, Fan Q, Satoh T, Arii J, Lanier LL, Spear PG, et al. Binding of herpes simplex virus glycoprotein B (gB) to paired immunoglobulin-like type 2 receptor alpha depends on specific sialylated O-linked glycans on gB. J Virol. 2009;83(24):13042–5. doi: 10.1128/JVI.00792-09. pmid:19812165
[5]
Rogers KM, Heise M. Modulation of cellular tropism and innate antiviral response by viral glycans. Journal of innate immunity. 2009;1(5):405–12. doi: 10.1159/000226422. pmid:20375598
[6]
Helle F, Duverlie G, Dubuisson J. The hepatitis C virus glycan shield and evasion of the humoral immune response. Viruses. 2011;3(10):1909–32. doi: 10.3390/v3101909. pmid:22069522
[7]
Machiels B, Lete C, Guillaume A, Mast J, Stevenson PG, Vanderplasschen A, et al. Antibody evasion by a gammaherpesvirus O-glycan shield. PLoS Pathog. 2011;7(11):e1002387. doi: 10.1371/journal.ppat.1002387. pmid:22114560
[8]
Doores KJ, Bonomelli C, Harvey DJ, Vasiljevic S, Dwek RA, Burton DR, et al. Envelope glycans of immunodeficiency virions are almost entirely oligomannose antigens. Proc Natl Acad Sci U S A. 2010;107(31):13800–5. doi: 10.1073/pnas.1006498107. pmid:20643940
[9]
Lennemann NJ, Rhein BA, Ndungo E, Chandran K, Qiu X, Maury W. Comprehensive functional analysis of N-linked glycans on Ebola virus GP1. mBio. 2014;5(1):e00862–13. doi: 10.1128/mBio.00862-13. pmid:24473128
[10]
Helle F, Vieyres G, Elkrief L, Popescu CI, Wychowski C, Descamps V, et al. Role of N-linked glycans in the functions of hepatitis C virus envelope proteins incorporated into infectious virions. J Virol. 2010;84(22):11905–15. doi: 10.1128/JVI.01548-10. pmid:20844034
[11]
Ogert RA, Lee MK, Ross W, Buckler-White A, Martin MA, Cho MW. N-linked glycosylation sites adjacent to and within the V1/V2 and the V3 loops of dualtropic human immunodeficiency virus type 1 isolate DH12 gp120 affect coreceptor usage and cellular tropism. J Virol. 2001;75(13):5998–6006. pmid:11390601 doi: 10.1128/jvi.75.13.5998-6006.2001
[12]
Wang W, Nie J, Prochnow C, Truong C, Jia Z, Wang S, et al. A systematic study of the N-glycosylation sites of HIV-1 envelope protein on infectivity and antibody-mediated neutralization. Retrovirology. 2013;10:14. doi: 10.1186/1742-4690-10-14. pmid:23384254
[13]
Davis CW, Mattei LM, Nguyen HY, Ansarah-Sobrinho C, Doms RW, Pierson TC. The location of asparagine-linked glycans on West Nile virions controls their interactions with CD209 (dendritic cell-specific ICAM-3 grabbing nonintegrin). J Biol Chem. 2006;281(48):37183–94. pmid:17001080 doi: 10.1074/jbc.m605429200
[14]
Sanders RW, Venturi M, Schiffner L, Kalyanaraman R, Katinger H, Lloyd KO, et al. The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120. J Virol. 2002;76(14):7293–305. pmid:12072528 doi: 10.1128/jvi.76.14.7293-7305.2002
[15]
Sok D, Doores KJ, Briney B, Le KM, Saye-Francisco KL, Ramos A, et al. Promiscuous glycan site recognition by antibodies to the high-mannose patch of gp120 broadens neutralization of HIV. Science translational medicine. 2014;6(236):236ra63. doi: 10.1126/scitranslmed.3008169. pmid:24828079
[16]
Hansen JE, Clausen H, Nielsen C, Teglbjaerg LS, Hansen LL, Nielsen CM, et al. Inhibition of human immunodeficiency virus (HIV) infection in vitro by anticarbohydrate monoclonal antibodies: peripheral glycosylation of HIV envelope glycoprotein gp120 may be a target for virus neutralization. J Virol. 1990;64(6):2833–40. pmid:1692349
[17]
Hansen JE, Jansson B, Gram GJ, Clausen H, Nielsen JO, Olofsson S. Sensitivity of HIV-1 to neutralization by antibodies against O-linked carbohydrate epitopes despite deletion of O-glycosylation signals in the V3 loop. Arch Virol. 1996;141(2):291–300. pmid:8634021 doi: 10.1007/bf01718400
[18]
Dowling W, Thompson E, Badger C, Mellquist JL, Garrison AR, Smith JM, et al. Influences of glycosylation on antigenicity, immunogenicity, and protective efficacy of ebola virus GP DNA vaccines. J Virol. 2007;81(4):1821–37. pmid:17151111 doi: 10.1128/jvi.02098-06
[19]
Hobman TC. Targeting of viral glycoproteins to the Golgi complex. Trends in microbiology. 1993;1(4):124–30. pmid:8143127 doi: 10.1016/0966-842x(93)90126-c
[20]
Stanley P. Golgi glycosylation. Cold Spring Harbor perspectives in biology. 2011;3(4). doi: 10.1101/cshperspect.a004630. pmid:21441593
[21]
Iacob RE, Perdivara I, Przybylski M, Tomer KB. Mass spectrometric characterization of glycosylation of hepatitis C virus E2 envelope glycoprotein reveals extended microheterogeneity of N-glycans. Journal of the American Society for Mass Spectrometry. 2008;19(3):428–44. doi: 10.1016/j.jasms.2007.11.022. pmid:18187336
[22]
Go EP, Liao HX, Alam SM, Hua D, Haynes BF, Desaire H. Characterization of host-cell line specific glycosylation profiles of early transmitted/founder HIV-1 gp120 envelope proteins. Journal of proteome research. 2013;12(3):1223–34. doi: 10.1021/pr300870t. pmid:23339644
[23]
Bause E. Structural requirements of N-glycosylation of proteins. Studies with proline peptides as conformational probes. Biochem J. 1983;209(2):331–6. pmid:6847620
[24]
Olofsson S, Sjoblom I, Lundstrom M, Jeansson S, Lycke E. Glycoprotein C of herpes simplex virus type 1: characterization of O-linked oligosaccharides. J Gen Virol. 1983;64 (Pt 12):2735–47. pmid:6319556 doi: 10.1099/0022-1317-64-12-2735
[25]
Yang ZY, Duckers HJ, Sullivan NJ, Sanchez A, Nabel EG, Nabel GJ. Identification of the Ebola virus glycoprotein as the main viral determinant of vascular cell cytotoxicity and injury. Nature medicine. 2000;6(8):886–9. pmid:10932225 doi: 10.1038/78645
[26]
Steentoft C, Vakhrushev SY, Joshi HJ, Kong Y, Vester-Christensen MB, Schjoldager KT, et al.—Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology. Embo J. 2013;32(10):1478–88. doi: 10.1038/emboj.2013.79. pmid:23584533
[27]
Schjoldager KT, Clausen H. Site-specific protein O-glycosylation modulates proprotein processing—deciphering specific functions of the large polypeptide GalNAc-transferase gene family. Biochimica et biophysica acta. 2012;1820(12):2079–94. doi: 10.1016/j.bbagen.2012.09.014. pmid:23022508
[28]
Pasquato A, Ramos da Palma J, Galan C, Seidah NG, Kunz S. Viral envelope glycoprotein processing by proprotein convertases. Antiviral research. 2013;99(1):49–60. doi: 10.1016/j.antiviral.2013.04.013. pmid:23611717
[29]
Dolnik O, Volchkova V, Garten W, Carbonnelle C, Becker S, Kahnt J, et al. Ectodomain shedding of the glycoprotein GP of Ebola virus. EMBO J. 2004;23(10):2175–84. pmid:15103332 doi: 10.1038/sj.emboj.7600219
[30]
Bennett EP, Mandel U, Clausen H, Gerken TA, Fritz TA, Tabak LA. Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. 2012(1460–2423 (Electronic)).
[31]
Steentoft C, Vakhrushev SY, Vester-Christensen MB, Schjoldager KT, Kong Y, Bennett EP, et al. Mining the O-glycoproteome using zinc-finger nuclease-glycoengineered SimpleCell lines. Nature methods. 2011;8(11):977–82. doi: 10.1038/nmeth.1731. pmid:21983924
[32]
Yang Z, Halim A, Narimatsu Y, Joshi HJ, Steentoft C, Schjoldager KT, et al. The GalNAc-type O-glycoproteome of CHO cells characterized by the SimpleCell strategy. Mol Cell Proteomics. 2014.
[33]
Cai WH, Gu B, Person S. Role of glycoprotein B of herpes simplex virus type 1 in viral entry and cell fusion. J Virol. 1988;62(8):2596–604. pmid:2839688
[34]
Ligas MW, Johnson DC. A herpes simplex virus mutant in which glycoprotein D sequences are replaced by beta-galactosidase sequences binds to but is unable to penetrate into cells. J Virol. 1988;62(5):1486–94. pmid:2833603
[35]
Forrester A, Farrell H, Wilkinson G, Kaye J, Davis-Poynter N, Minson T. Construction and properties of a mutant of herpes simplex virus type 1 with glycoprotein H coding sequences deleted. J Virol. 1992;66(1):341–8. pmid:1309250
[36]
Roop C, Hutchinson L, Johnson DC. A mutant herpes simplex virus type 1 unable to express glycoprotein L cannot enter cells, and its particles lack glycoprotein H. J Virol. 1993;67(4):2285–97. pmid:8383241
[37]
Arii J, Wang J, Morimoto T, Suenaga T, Akashi H, Arase H, et al. A single-amino-acid substitution in herpes simplex virus 1 envelope glycoprotein B at a site required for binding to the paired immunoglobulin-like type 2 receptor alpha (PILRalpha) abrogates PILRalpha-dependent viral entry and reduces pathogenesis. J Virol. 2010;84(20):10773–83. doi: 10.1128/JVI.01166-10. pmid:20686018
[38]
Heldwein EE, Lou H, Bender FC, Cohen GH, Eisenberg RJ, Harrison SC. Crystal structure of glycoprotein B from herpes simplex virus 1. Science. 2006;313(5784):217–20. pmid:16840698 doi: 10.1126/science.1126548
[39]
Krummenacher C, Supekar VM, Whitbeck JC, Lazear E, Connolly SA, Eisenberg RJ, et al.—Structure of unliganded HSV gD reveals a mechanism for receptor-mediated activation of virus entry. Embo J. 2005;24(23):4144–53. pmid:16292345 doi: 10.1038/sj.emboj.7600875
[40]
Krummenacher C, Carfi A, Eisenberg RJ, Cohen GH. Entry of herpesviruses into cells: the enigma variations. Adv Exp Med Biol. 2013;790:178–95. doi: 10.1007/978-1-4614-7651-1_10. pmid:23884592
[41]
Di Giovine P, Settembre EC, Bhargava AK, Luftig MA, Lou H, Cohen GH, et al.—Structure of herpes simplex virus glycoprotein D bound to the human receptor nectin-1. PLoS Pathog. 2011;7(9):29. doi: 10.1371/journal.ppat.1002277
Friedman HM, Cohen GH, Eisenberg RJ, Seidel CA, Cines DB. Glycoprotein C of herpes simplex virus 1 acts as a receptor for the C3b complement component on infected cells. Nature. 1984;309(5969):633–5. pmid:6328323 doi: 10.1038/309633a0
[44]
Spear PG, Shieh MT, Herold BC, WuDunn D, Koshy TI. Heparan sulfate glycosaminoglycans as primary cell surface receptors for herpes simplex virus. Adv Exp Med Biol. 1992;313:341–53. pmid:1332443 doi: 10.1007/978-1-4899-2444-5_33
[45]
Lundstrom M, Olofsson S, Jeansson S, Lycke E, Datema R, Mansson JE. Host cell-induced differences in O-glycosylation of herpes simplex virus gC-1. I. Structures of nonsialylated HPA- and PNA-binding carbohydrates. Virology. 1987;161(2):385–94. pmid:2825412 doi: 10.1016/0042-6822(87)90131-0
[46]
Dingwell KS, Brunetti CR, Hendricks RL, Tang Q, Tang M, Rainbow AJ, et al. Herpes simplex virus glycoproteins E and I facilitate cell-to-cell spread in vivo and across junctions of cultured cells. J Virol. 1994;68(2):834–45. pmid:8289387
[47]
Johnson DC, Frame MC, Ligas MW, Cross AM, Stow ND. Herpes simplex virus immunoglobulin G Fc receptor activity depends on a complex of two viral glycoproteins, gE and gI. J Virol. 1988;62(4):1347–54. pmid:2831396
[48]
Sprague ER, Wang C, Baker D, Bjorkman PJ. Crystal structure of the HSV-1 Fc receptor bound to Fc reveals a mechanism for antibody bipolar bridging. PLoS Biol. 2006;4(6):e148. pmid:16646632 doi: 10.1371/journal.pbio.0040148
[49]
Basu S, Dubin G, Nagashunmugam T, Basu M, Goldstein LT, Wang L, et al. Mapping regions of herpes simplex virus type 1 glycoprotein I required for formation of the viral Fc receptor for monomeric IgG. J Immunol. 1997;158(1):209–15. pmid:8977192
[50]
Norberg P, Olofsson S, Tarp MA, Clausen H, Bergstrom T, Liljeqvist JA. Glycoprotein I of herpes simplex virus type 1 contains a unique polymorphic tandem-repeated mucin region. J Gen Virol. 2007;88(Pt 6):1683–8. doi: 10.1099/vir.0.82500-0
[51]
Viejo-Borbolla A, Martinez-Martin N, Nel HJ, Rueda P, Martin R, Blanco S, et al. Enhancement of chemokine function as an immunomodulatory strategy employed by human herpesviruses. PLoS Pathog. 2012;8(2):e1002497. doi: 10.1371/journal.ppat.1002497. pmid:22319442
[52]
Campadelli G, Brandimarti R, Di Lazzaro C, Ward PL, Roizman B, Torrisi MR. Fragmentation and dispersal of Golgi proteins and redistribution of glycoproteins and glycolipids processed through the Golgi apparatus after infection with herpes simplex virus 1. Proc Natl Acad Sci U S A. 1993;90(7):2798–802. pmid:8385343 doi: 10.1073/pnas.90.7.2798
[53]
Hang HC, Yu C, Ten Hagen KG, Tian E, Winans KA, Tabak LA, et al. Small molecule inhibitors of mucin-type O-linked glycosylation from a uridine-based library. Chemistry & biology. 2004;11(3):337–45. doi: 10.1016/j.chembiol.2004.02.023
[54]
Patsos G, Hebbe-Viton V, Robbe-Masselot C, Masselot D, San Martin R, Greenwood R, et al. O-glycan inhibitors generate aryl-glycans, induce apoptosis and lead to growth inhibition in colorectal cancer cell lines. Glycobiology. 2009;19(4):382–98. doi: 10.1093/glycob/cwn149. pmid:19122213
[55]
Ulloa F, Real FX. Benzyl-N-acetyl-alpha-D-galactosaminide induces a storage disease-like phenotype by perturbing the endocytic pathway. J Biol Chem. 2003;278(14):12374–83. pmid:12538583 doi: 10.1074/jbc.m211909200
[56]
Radhakrishnan P, Dabelsteen S, Madsen FB, Francavilla C, Kopp KL, Steentoft C, et al. Immature truncated O-glycophenotype of cancer directly induces oncogenic features. Proc Natl Acad Sci U S A. 2014.
[57]
Levery SB, Steentoft C, Halim A, Narimatsu Y, Clausen H, Vakhrushev SY. Advances in Mass Spectrometry Driven O-Glycoproteomics. Biochimica et biophysica acta. 2014.
[58]
Bunkenborg J, Pilch BJ, Podtelejnikov AV, Wisniewski JR. Screening for N-glycosylated proteins by liquid chromatography mass spectrometry. Proteomics. 2004;4(2):454–65. pmid:14760718 doi: 10.1002/pmic.200300556
[59]
Zielinska DF, Gnad F, Wisniewski JR, Mann M. Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell. 2010;141(5):897–907. doi: 10.1016/j.cell.2010.04.012. pmid:20510933
[60]
Grinde B.—Herpesviruses: latency and reactivation—viral strategies and host response. LID— doi: 10.3402/jom.v5i0.22766 J Oral Microbiol. 2013;25(5).
[61]
Sauerbrei A, Schmitt S, Scheper T, Brandstadt A, Saschenbrecker S, Motz M, et al.—Seroprevalence of herpes simplex virus type 1 and type 2 in Thuringia, Germany, 1999 to 2006. LID—20005 [pii]. Euro Surveill. 2011;16(44):20005. pmid:22085620
[62]
Bradley H, Markowitz LE, Gibson T, McQuillan GM.—Seroprevalence of herpes simplex virus types 1 and 2—United States, 1999–2010. J Infect Dis. 2014;209(3):325–33. doi: 10.1093/infdis/jit458. pmid:24136792
[63]
Grunewald K, Desai P, Winkler DC, Heymann JB, Belnap DM, Baumeister W, et al. Three-dimensional structure of herpes simplex virus from cryo-electron tomography. Science. 2003;302(5649):1396–8. pmid:14631040 doi: 10.1126/science.1090284
[64]
Campadelli-Fiume G, Poletti L, Dall'Olio F, Serafini-Cessi F. Infectivity and glycoprotein processing of herpes simplex virus type 1 grown in a ricin-resistant cell line deficient in N-acetylglucosaminyl transferase I. J Virol. 1982;43(3):1061–71. pmid:6292449 doi: 10.1007/bf01108613
[65]
Serafini-Cessi F, Dall'Olio F, Pereira L, Campadelli-Fiume G. Processing of N-linked oligosaccharides from precursor- to mature-form herpes simplex virus type 1 glycoprotein gC. J Virol. 1984;51(3):838–44. pmid:6088806 doi: 10.1007/bf01314424
[66]
Olofsson S, Bolmstedt A, Biller M, Mardberg K, Leckner J, Malmstrom BG, et al. The role of a single N-linked glycosylation site for a functional epitope of herpes simplex virus type 1 envelope glycoprotein gC. Glycobiology. 1999;9(1):73–81. pmid:9884409 doi: 10.1093/glycob/9.1.73
[67]
Dall'Olio F, Malagolini N, Speziali V, Campadelli-Fiume G, Serafini-Cessi F. Sialylated oligosaccharides O-glycosidically linked to glycoprotein C from herpes simplex virus type 1. J Virol. 1985;56(1):127–34. pmid:2993643 doi: 10.1016/0003-9861(85)90097-9
[68]
Serafini-Cessi F, Dall'Olio F, Malagolini N, Pereira L, Campadelli-Fiume G. Comparative study on O-linked oligosaccharides of glycoprotein D of herpes simplex virus types 1 and 2. J Gen Virol. 1988;69 (Pt 4):869–77. doi: 10.1099/0022-1317-69-4-869
[69]
Norden R, Nystrom K, Adamiak B, Halim A, Nilsson J, Larson G, et al. Involvement of viral glycoprotein gC-1 in expression of the selectin ligand sialyl-Lewis X induced after infection with herpes simplex virus type 1. APMIS. 2013;121(4):280–9. doi: 10.1111/j.1600-0463.2012.02967.x. pmid:23030500
[70]
Lundstrom M, Jeansson S, Olofsson S. Host cell-induced differences in the O-glycosylation of herpes simplex virus gC-1. II. Demonstration of cell-specific galactosyltransferase essential for formation of O-linked oligosaccharides. Virology. 1987;161(2):395–402. pmid:2825413 doi: 10.1016/0042-6822(87)90132-2
[71]
Whitbeck JC, Peng C, Lou H, Xu R, Willis SH, Ponce de Leon M, et al. Glycoprotein D of herpes simplex virus (HSV) binds directly to HVEM, a member of the tumor necrosis factor receptor superfamily and a mediator of HSV entry. J Virol. 1997;71(8):6083–93. pmid:9223502
[72]
Geraghty RJ, Krummenacher C, Cohen GH, Eisenberg RJ, Spear PG. Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science. 1998;280(5369):1618–20. pmid:9616127 doi: 10.1126/science.280.5369.1618
[73]
Shukla D, Liu J, Blaiklock P, Shworak NW, Bai X, Esko JD, et al. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell. 1999;99(1):13–22. pmid:10520990 doi: 10.1016/s0092-8674(00)80058-6
[74]
Uyama T, Ishida M, Izumikawa T, Trybala E, Tufaro F, Bergstrom T, et al. Chondroitin 4-O-sulfotransferase-1 regulates E disaccharide expression of chondroitin sulfate required for herpes simplex virus infectivity. J Biol Chem. 2006;281(50):38668–74. pmid:17040900 doi: 10.1074/jbc.m609320200
[75]
Satoh T, Arii J, Suenaga T, Wang J, Kogure A, Uehori J, et al. PILRalpha is a herpes simplex virus-1 entry coreceptor that associates with glycoprotein B. Cell. 2008;132(6):935–44. doi: 10.1016/j.cell.2008.01.043. pmid:18358807
[76]
Gianni T, Salvioli S, Chesnokova LS, Hutt-Fletcher LM, Campadelli-Fiume G. alphavbeta6- and alphavbeta8-integrins serve as interchangeable receptors for HSV gH/gL to promote endocytosis and activation of membrane fusion. PLoS Pathog. 2013;9(12):e1003806. doi: 10.1371/journal.ppat.1003806. pmid:24367260
[77]
Kuroki K, Wang J, Ose T, Yamaguchi M, Tabata S, Maita N, et al. Structural basis for simultaneous recognition of an O-glycan and its attached peptide of mucin family by immune receptor PILRalpha. Proc Natl Acad Sci U S A. 2014;111(24):8877–82. doi: 10.1073/pnas.1324105111. pmid:24889612
[78]
Gallagher JR, Atanasiu D, Saw WT, Paradisgarten MJ, Whitbeck JC, Eisenberg RJ, et al. Functional Fluorescent Protein Insertions in Herpes Simplex Virus gB Report on gB Conformation before and after Execution of Membrane Fusion. PLoS Pathog. 2014;10(9):e1004373. doi: 10.1371/journal.ppat.1004373. pmid:25233449
[79]
Carfi A, Willis SH, Whitbeck JC, Krummenacher C, Cohen GH, Eisenberg RJ, et al.—Herpes simplex virus glycoprotein D bound to the human receptor HveA. Mol Cell. 2001;8(1):169–79. pmid:11511370 doi: 10.1016/s1097-2765(01)00298-2
[80]
Mardberg K, Nystrom K, Tarp MA, Trybala E, Clausen H, Bergstrom T, et al. Basic amino acids as modulators of an O-linked glycosylation signal of the herpes simplex virus type 1 glycoprotein gC: functional roles in viral infectivity. Glycobiology. 2004;14(7):571–81. pmid:15044392 doi: 10.1093/glycob/cwh075
[81]
Biller M, Mardberg K, Hassan H, Clausen H, Bolmstedt A, Bergstrom T, et al. Early steps in O-linked glycosylation and clustered O-linked glycans of herpes simplex virus type 1 glycoprotein C: effects on glycoprotein properties. Glycobiology. 2000;10(12):1259–69. pmid:11159917 doi: 10.1093/glycob/10.12.1259
[82]
Geyer H, Will C, Feldmann H, Klenk HD, Geyer R. Carbohydrate structure of Marburg virus glycoprotein. Glycobiology. 1992;2(4):299–312. pmid:1421752 doi: 10.1093/glycob/2.4.299
[83]
Sanchez AJ, Vincent MJ, Nichol ST. Characterization of the glycoproteins of Crimean-Congo hemorrhagic fever virus. J Virol. 2002;76(14):7263–75. pmid:12072526 doi: 10.1128/jvi.76.14.7263-7275.2002
[84]
Brooks CL, Schietinger A, Borisova SN, Kufer P, Okon M, Hirama T, et al. Antibody recognition of a unique tumor-specific glycopeptide antigen. Proc Natl Acad Sci U S A. 2010;107(22):10056–61. doi: 10.1073/pnas.0915176107. pmid:20479270
[85]
Wandall HH, Blixt O, Tarp MA, Pedersen JW, Bennett EP, Mandel U, et al. Cancer biomarkers defined by autoantibody signatures to aberrant O-glycopeptide epitopes. Cancer research. 2010;70(4):1306–13. doi: 10.1158/0008-5472.CAN-09-2893. pmid:20124478
[86]
Clo E, Kracun SK, Nudelman AS, Jensen KJ, Liljeqvist JA, Olofsson S, et al.—Characterization of the viral O-glycopeptidome: a novel tool of relevance for vaccine design and serodiagnosis. J Virol. 2012;86(11):6268–78. doi: 10.1128/JVI.00392-12. pmid:22491453
[87]
Jae LT, Raaben M, Riemersma M, van Beusekom E, Blomen VA, Velds A, et al. Deciphering the glycosylome of dystroglycanopathies using haploid screens for lassa virus entry. Science. 2013;340(6131):479–83. doi: 10.1126/science.1233675. pmid:23519211
[88]
Marsden HS, Crombie IK, Subak-Sharpe JH. Control of protein synthesis in herpesvirus-infected cells: analysis of the polypeptides induced by wild type and sixteen temperature-sensitive mutants of HSV strain 17. J Gen Virol. 1976;31(3):347–72. pmid:180249 doi: 10.1099/0022-1317-31-3-347
[89]
Guenalp A. GROWTH AND CYTOPATHIC EFFECT OF RUBELLA VIRUS IN A LINE OF GREEN MONKEY KIDNEY CELLS. Proc Soc Exp Biol Med. 1965;118:85–90. pmid:14254593 doi: 10.3181/00379727-118-29763
[90]
Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, Fusenig NE. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. The Journal of cell biology. 1988;106(3):761–71. pmid:2450098 doi: 10.1083/jcb.106.3.761
[91]
Mandel U, Hassan H, Therkildsen MH, Rygaard J, Jakobsen MH, Juhl BR, et al. Expression of polypeptide GalNAc-transferases in stratified epithelia and squamous cell carcinomas: immunohistological evaluation using monoclonal antibodies to three members of the GalNAc-transferase family. Glycobiology. 1999;9(1):43–52. pmid:9884405 doi: 10.1093/glycob/9.1.43
[92]
Vakhrushev SY, Steentoft C, Vester-Christensen MB, Bennett EP, Clausen H, Levery SB.—Enhanced mass spectrometric mapping of the human GalNAc-type O-glycoproteome with SimpleCells. Mol Cell Proteomics. 2013;12(4):932–44. doi: 10.1074/mcp.O112.021972. pmid:23399548
[93]
Namvar L, Olofsson S, Bergstrom T, Lindh M. Detection and typing of Herpes Simplex virus (HSV) in mucocutaneous samples by TaqMan PCR targeting a gB segment homologous for HSV types 1 and 2. J Clin Microbiol. 2005;43(5):2058–64. pmid:15872222 doi: 10.1128/jcm.43.5.2058-2064.2005
