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Annual Review of Virology

Volume 10, 2023

Structure and Role of O-Linked Glycans in Viral Envelope Proteins

Abstract

N- and O-glycans are both important constituents of viral envelope glycoproteins. O-linked glycosylation can be initiated by any of 20 different human polypeptide O-acetylgalactosaminyl transferases, resulting in an important functional O-glycan heterogeneity. O-glycans are organized as solitary glycans or in clusters of multiple glycans forming mucin-like domains. They are functional both in the viral life cycle and in viral colonization of their host. Negatively charged O-glycans are crucial for the interactions between glycosaminoglycan-binding viruses and their host. A novel mechanism, based on controlled electrostatic repulsion, explains how such viruses solve the conflict between optimized viral attachment to target cells and efficient egress of progeny virus. Conserved solitary O-glycans appear important for viral uptake in target cells by contributing to viral envelope fusion. Dual roles of viral O-glycans in the host B cell immune response, either epitope blocking or epitope promoting, may be exploitable for vaccine development. Finally, specific virus-induced O-glycans may be involved in viremic spread.

Keyword(s): attachment, chondroitin sulfate, egress, heparan sulfate, mucin-like domain, vaccine, virion
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2023-09-29
2024-04-28
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Literature Cited

  1. 1.
    Mascola JR, Montefiori DC. 2003. HIV-1: nature's master of disguise. Nat. Med. 9:4393–94
     [Google Scholar]
  2. 2.
    Olofsson S, Hansen J. 1998. Host cell carbohydrate tagging of viral glycoproteins—a battlefield for the struggle between host defence and viral resistance mechanisms. Scand. J. Infect. Dis. 30:435–40
     [Google Scholar]
  3. 3.
    Bagdonaite I, Wandall HH. 2018. Global aspects of viral glycosylation enveloped viruses. Glycobiology 28:443–67
     [Google Scholar]
  4. 4.
    Vigerust DJ, Shepherd VL. 2007. Virus glycosylation: role in virulence and immune interactions. Trends Microbiol. 15:5211–18
     [Google Scholar]
  5. 5.
    Watanabe Y, Bowden TA, Wilson IA, Crispin M. 2019. Exploitation of glycosylation in enveloped virus pathobiology. Biochim. Biophys. Acta 1863:101480–97
     [Google Scholar]
  6. 6.
    Nilsson J, Rüetschi U, Halim A, Hesse C, Carlsohn E et al. 2009. Enrichment of glycopeptides for glycan structure and attachment site identification. Nat. Methods 6:11809–11
     [Google Scholar]
  7. 7.
    Vakhrushev SY, Steentoft C, Vester-Christensen MB, Bennett EP, Clausen H, Levery SB. 2013. Enhanced mass spectrometric mapping of the human GalNAc-type O-glycoproteome with SimpleCells. Mol. Cell. Proteom. 12:4932–44
     [Google Scholar]
  8. 8.
    Nordén R, Halim A, Nyström K, Bennett EP, Mandel U et al. 2015. O-linked glycosylation of the mucin domain of the herpes simplex virus type 1 specific glycoprotein gC-1 is temporally regulated in a seed-and-spread manner. J. Biol. Chem. 290:85078–91
     [Google Scholar]
  9. 9.
    Bagdonaite I, Nordén R, Joshi HJ, Dabelsteen S, Nyström K et al. 2015. A strategy for O-glycoproteomics of enveloped viruses—the O-glycoproteome of herpes simplex virus type 1. PLOS Pathog. 11:4e1004784
     [Google Scholar]
  10. 10.
    Koehler M, Delguste M, Sieben C, Gillet L, Alsteens D. 2020. Initial step of virus entry: virion binding to cell-surface glycans. Annu. Rev. Virol. 7:143–65
     [Google Scholar]
  11. 11.
    Bally M, Block S, Höök F, Larson G, Parveen N, Rydell GE. 2021. Physicochemical tools for studying virus interactions with targeted cell membranes in a molecular and spatiotemporally resolved context. Anal. Bioanal. Chem. 413:297157–78
     [Google Scholar]
  12. 12.
    Hanisch FG. 2001. O-glycosylation of the mucin type. Biol. Chem. 382:2143–49
     [Google Scholar]
  13. 13.
    Gill DJ, Clausen H, Bard F. 2011. Location, location, location: new insights into O-GalNAc protein glycosylation. Trends Cell Biol. 21:3149–58
     [Google Scholar]
  14. 14.
    Bennett EP, Mandel U, Clausen H, Gerken TA, Fritz TA, Tabak LA. 2012. Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. Glycobiology 22:6736–56
     [Google Scholar]
  15. 15.
    Jones J, Krag SS, Betenbaugh MJ. 2005. Controlling N-linked glycan site occupancy. Biochim. Biophys. Acta 1726:2121–37
     [Google Scholar]
  16. 16.
    Lairson LL, Henrissat B, Davies GJ, Withers SG. 2008. Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77:521–55
     [Google Scholar]
  17. 17.
    Bagdonaite I, Pallesen EMH, Nielsen MI, Bennett EP, Wandall HH. 2021. Mucin-type O-GalNAc glycosylation in health and disease. Adv. Exp. Med. Biol. 1325:25–60
     [Google Scholar]
  18. 18.
    Wandall HH, Nielsen MAI, King-Smith S, de Haan N, Bagdonaite I. 2021. Global functions of O-glycosylation: promises and challenges in O-glycobiology. FEBS J. 288:247183–212
     [Google Scholar]
  19. 19.
    Schmitt S, Glebe D, Alving K, Tolle TK, Linder M et al. 1999. Analysis of the pre-S2 N- and O-linked glycans of the M surface protein from human hepatitis B virus. J. Biol. Chem. 274:1711945–57
     [Google Scholar]
  20. 20.
    Bräutigam J, Scheidig AJ, Egge-Jacobsen W. 2013. Mass spectrometric analysis of hepatitis C viral envelope protein E2 reveals extended microheterogeneity of mucin-type O-linked glycosylation. Glycobiology 23:4453–74
     [Google Scholar]
  21. 21.
    Altgärde N, Eriksson C, Peerboom N, Phan-Xuan T, Moeller S et al. 2015. Mucin-like region of herpes simplex virus type 1 attachment protein glycoprotein C (gC) modulates the virus-glycosaminoglycan interaction. J. Biol. Chem. 290:3521473–85
     [Google Scholar]
  22. 22.
    Kannagi R. 2001. Transcriptional regulation of expression of carbohydrate ligands for cell adhesion molecules in the selectin family. Adv. Exp. Med. Biol. 491:267–78
     [Google Scholar]
  23. 23.
    Cebulla C, Miller D, Knight D, Briggs B, McGaughy V, Sedmak D. 2000. Cytomegalovirus induces sialyl Lewisx and Lewisx on human endothelial cells. Transplantation 69:61202–9
     [Google Scholar]
  24. 24.
    Nyström K, Grahn A, Lindh M, Brytting M, Mandel U et al. 2007. Virus-induced transcriptional activation of host FUT genes associated with neo-expression of Ley in cytomegalovirus-infected and sialyl-Lex in varicella-zoster virus-infected diploid human cells. Glycobiology 17:4355–66
     [Google Scholar]
  25. 25.
    Bagdonaite I, Nordén R, Joshi HJ, King SL, Vakhrushev SY et al. 2016. Global mapping of O-glycosylation of varicella zoster virus, human cytomegalovirus, and Epstein-Barr virus. J. Biol. Chem. 291:2312014–28
     [Google Scholar]
  26. 26.
    Olofsson S, Blixt O, Bergström T, Frank M, Wandall HH. 2016. Viral O-GalNAc peptide epitopes: a novel potential target in viral envelope glycoproteins. Rev. Med. Virol. 26:134–48
     [Google Scholar]
  27. 27.
    Norberg P, Olofsson S, Tarp MA, Clausen H, Bergström T, Liljeqvist JA. 2007. Glycoprotein I of herpes simplex virus type 1 contains a unique polymorphic tandem-repeated mucin region. J. Gen. Virol. 88:Part 61683–88
     [Google Scholar]
  28. 28.
    Gerken TA, Revoredo L, Thome JJC, Tabak LA, Vester-Christensen MB et al. 2013. The lectin domain of the polypeptide GalNAc transferase family of glycosyltransferases (ppGalNAc Ts) acts as a switch directing glycopeptide substrate glycosylation in an N- or C-terminal direction, further controlling mucin type O-glycosylation. J. Biol. Chem. 288:2719900–14
     [Google Scholar]
  29. 29.
    Revoredo L, Wang S, Bennett EP, Clausen H, Moremen KW et al. 2015. Mucin-type O-glycosylation is controlled by short- and long-range glycopeptide substrate recognition that varies among members of the polypeptide GalNAc transferase family. Glycobiology 26:360–76
     [Google Scholar]
  30. 30.
    Olofsson S, Bergström T. 2005. Glycoconjugate glycans as viral receptors. Ann. Med. 37:3154–72
     [Google Scholar]
  31. 31.
    Kamhi E, Joo EJ, Dordick JS, Linhardt RJ. 2013. Glycosaminoglycans in infectious disease. Biol. Rev. 88:4928–43
     [Google Scholar]
  32. 32.
    Trybala E, Peerboom N, Adamiak B, Krzyzowska M, Liljeqvist JA et al. 2021. Herpes simplex virus type 2 mucin-like glycoprotein mgG promotes virus release from the surface of infected cells. Viruses 13:5887
     [Google Scholar]
  33. 33.
    Lundin A, Bergström T, Andrighetti-Fröhner CR, Bendrioua L, Ferro V, Trybala E. 2012. Potent anti-respiratory syncytial virus activity of a cholestanol-sulfated tetrasaccharide conjugate. Antiviral Res. 93:1101–9
     [Google Scholar]
  34. 34.
    de Lima BD, May JS, Stevenson PG. 2004. Murine gammaherpesvirus 68 lacking gp150 shows defective virion release but establishes normal latency in vivo. J. Virol. 78:105103–12
     [Google Scholar]
  35. 35.
    Roseman S. 2001. Reflections on glycobiology. J. Biol. Chem. 276:4541527–42
     [Google Scholar]
  36. 36.
    Rivara S, Milazzo FM, Giannini G. 2016. Heparanase: a rainbow pharmacological target associated to multiple pathologies including rare diseases. Future Med. Chem. 8:6647–80
     [Google Scholar]
  37. 37.
    Gao L, Lipowsky HH. 2010. Composition of the endothelial glycocalyx and its relation to its thickness and diffusion of small solutes. Microvasc. Res. 80:3394–401
     [Google Scholar]
  38. 38.
    Xu D, Esko JD. 2014. Demystifying heparan sulfate–protein interactions. Annu. Rev. Biochem. 83:129–57
     [Google Scholar]
  39. 39.
    Kjellén L, Lindahl U. 2018. Specificity of glycosaminoglycan–protein interactions. Curr. Opin. Struct. Biol. 50:101–8
     [Google Scholar]
  40. 40.
    Peerboom N, Block S, Altgärde N, Wahlsten O, Möller S et al. 2017. Binding kinetics and lateral mobility of HSV-1 on end-grafted sulfated glycosaminoglycans. Biophys. J. 113:61223–34
     [Google Scholar]
  41. 41.
    Abidine Y, Liu L, Wallén O, Trybala E, Olofsson S et al. 2022. Cellular chondroitin sulfate and the mucin-like domain of viral glycoprotein C promote diffusion of herpes simplex virus 1 while heparan sulfate restricts mobility. Viruses 14:81836
     [Google Scholar]
  42. 42.
    Shukla D, Spear PG. 2001. Herpesviruses and heparan sulfate: an intimate relationship in aid of viral entry. J. Clin. Invest. 108:4503–10
     [Google Scholar]
  43. 43.
    Agelidis AM, Shukla D. 2015. Cell entry mechanisms of HSV: what we have learned in recent years. Future Virol. 10:101145–54
     [Google Scholar]
  44. 44.
    Trybala E, Bergstrom T, Svennerholm B, Jeansson S, Glorioso JC, Olofsson S. 1994. Localization of a functional site on herpes simplex virus type 1 glycoprotein C involved in binding to cell surface heparan sulphate. J. Gen. Virol. 75:Part 4743–52
     [Google Scholar]
  45. 45.
    Lundström M, Olofsson S, Jeansson S, Lycke E, Datema R, Månsson JE. 1987. Host cell-induced differences in O-glycosylation of herpes simplex virus gC-1. I. Structures of nonsialylated HPA- and PNA-binding carbohydrates. Virology 1612385–94
  46. 46.
    Norberg P. 2010. Divergence and genotyping of human α-herpesviruses: an overview. Infect. Genet. Evol. 10:114–25
     [Google Scholar]
  47. 47.
    Mårdberg K, Nyström K, Tarp MA, Trybala E, Clausen H et al. 2004. 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 14:7571–81
     [Google Scholar]
  48. 48.
    Sun Y, MacLean AR, Aitken JD, Brown SM. 1996. The role of the gene 71 product in the life cycle of equine herpesvirus 1. J. Gen. Virol. 77:Part 3493–500
     [Google Scholar]
  49. 49.
    Delguste M, Peerboom N, Le Brun G, Trybala E, Olofsson S et al. 2019. Regulatory mechanisms of the mucin-like region on herpes simplex virus during cellular attachment. ACS Chem. Biol. 14:3534–42
     [Google Scholar]
  50. 50.
    Oxford J. 2005. Oseltamivir in the management of influenza. Expert Opin. Pharmacother. 6:142493–500
     [Google Scholar]
  51. 51.
    Smith AE, Helenius A. 2004. How viruses enter animal cells. Science 304:5668237–42
     [Google Scholar]
  52. 52.
    Kielian M. 2013. Mechanisms of virus membrane fusion proteins. Annu. Rev Virol. 1:171–89
     [Google Scholar]
  53. 53.
    Liu H-Y, Yang PL. 2021. Small-molecule inhibition of viral fusion glycoproteins. Annu. Rev. Virol. 8:459–89
     [Google Scholar]
  54. 54.
    McGeoch DJ, Cook S, Dolan A, Jamieson FE, Telford EA. 1995. Molecular phylogeny and evolutionary timescale for the family of mammalian herpesviruses. J. Mol. Biol. 247:3443–58
     [Google Scholar]
  55. 55.
    Heldwein EE, Lou H, Bender FC, Cohen GH, Eisenberg RJ, Harrison SC. 2006. Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313:5784217–20
     [Google Scholar]
  56. 56.
    Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM et al. 2004. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25:131605–12
     [Google Scholar]
  57. 57.
    Backovic M, Longnecker R, Jardetzky TS. 2009. Structure of a trimeric variant of the Epstein-Barr virus glycoprotein B. PNAS 106:82880–85
     [Google Scholar]
  58. 58.
    Satoh T, Arii J, Suenaga T, Wang J, Kogure A et al. 2008. PILRα is a herpes simplex virus-1 entry coreceptor that associates with glycoprotein B. Cell 132:6935–44
     [Google Scholar]
  59. 59.
    Tabata S, Kuroki K, Wang J, Kajikawa M, Shiratori I et al. 2008. Biophysical characterization of O-glycosylated CD99 recognition by paired Ig-like type 2 receptors. J. Biol. Chem. 283:148893–901
     [Google Scholar]
  60. 60.
    Kuroki K, Wang J, Ose T, Yamaguchi M, Tabata S et al. 2014. Structural basis for simultaneous recognition of an O-glycan and its attached peptide of mucin family by immune receptor PILRα. PNAS 111:248877–82
     [Google Scholar]
  61. 61.
    Furukawa A, Kakita K, Yamada T, Ishizuka M, Sakamoto J et al. 2017. Structural and thermodynamic analyses reveal critical features of glycopeptide recognition by the human PILRα immune cell receptor. J. Biol. Chem. 292:5121128–36
     [Google Scholar]
  62. 62.
    Suenaga T, Satoh T, Somboonthum P, Kawaguchi Y, Mori Y, Arase H. 2010. Myelin-associated glycoprotein mediates membrane fusion and entry of neurotropic herpesviruses. PNAS 107:2866–71
     [Google Scholar]
  63. 63.
    Suenaga T, Matsumoto M, Arisawa F, Kohyama M, Hirayasu K et al. 2015. Sialic acids on varicella-zoster virus glycoprotein B are required for cell-cell fusion. J. Biol. Chem. 290:3219833–43
     [Google Scholar]
  64. 64.
    Bose S, Jardetzky TS, Lamb RA. 2015. Timing is everything: Fine-tuned molecular machines orchestrate paramyxovirus entry. Virology 479–480518–31
  65. 65.
    Stone JA, Nicola AV, Baum LG, Aguilar HC. 2016. Multiple novel functions of henipavirus O-glycans: the first O-glycan functions identified in the paramyxovirus family. PLOS Pathog. 12:2e1005445
     [Google Scholar]
  66. 66.
    Falkowska E, Kajumo F, Garcia E, Reinus J, Dragic T. 2007. Hepatitis C virus envelope glycoprotein E2 glycans modulate entry, CD81 binding, and neutralization. J. Virol. 81:158072–79
     [Google Scholar]
  67. 67.
    Tran EEH, Simmons JA, Bartesaghi A, Shoemaker CJ, Nelson E et al. 2014. Spatial localization of the Ebola virus glycoprotein mucin-like domain determined by cryo-electron tomography. J. Virol. 88:1810958–62
     [Google Scholar]
  68. 68.
    Yang ZY, Duckers HJ, Sullivan NJ, Sanchez A, Nabel EG, Nabel GJ. 2000. Identification of the Ebola virus glycoprotein as the main viral determinant of vascular cell cytotoxicity and injury. Nat. Med. 6:8886–89
     [Google Scholar]
  69. 69.
    Simmons G, Wool-Lewis RJ, Baribaud F, Netter RC, Bates P. 2002. Ebola virus glycoproteins induce global surface protein down-modulation and loss of cell adherence. J. Virol. 76:52518–28
     [Google Scholar]
  70. 70.
    Simon EJ, Linstedt AD. 2018. Site-specific glycosylation of Ebola virus glycoprotein by human polypeptide GalNAc-transferase 1 induces cell adhesion defects. J. Biol. Chem. 293:19866–73
     [Google Scholar]
  71. 71.
    Song L, Linstedt AD. 2017. Inhibitor of ppGalNAc-T3-mediated O-glycosylation blocks cancer cell invasiveness and lowers FGF23 levels. eLife 6:e24051
     [Google Scholar]
  72. 72.
    Bagdonaite I, Thompson AJ, Wang X, Søgaard M, Fougeroux C et al. 2021. Site-specific O-glycosylation analysis of SARS-CoV-2 spike protein produced in insect and human cells. Viruses 13:4551
     [Google Scholar]
  73. 73.
    Eldrid CFS, Allen JD, Newby ML, Crispin M. 2021. Suppression of O-linked glycosylation of the SARS-CoV-2 spike by quaternary structural restraints. Anal. Chem. 93:4314392–400
     [Google Scholar]
  74. 74.
    Zhang S, Go EP, Ding H, Anang S, Kappes JC et al. 2022. Analysis of glycosylation and disulfide bonding of wild-type SARS-CoV-2 spike glycoprotein. J. Virol. 96:3e0162621
     [Google Scholar]
  75. 75.
    Rong Y, Wang X, Mao W, Yuan F, Chen M et al. 2022. Chemoenzymatic synthesis of SARS-CoV-2 homogeneous O-linked glycopeptides for exploring their inhibition functions. ACS Infect. Dis. 8:102198–206
     [Google Scholar]
  76. 76.
    Machiels B, Lété C, Guillaume A, Mast J, Stevenson PG et al. 2011. Antibody evasion by a gammaherpesvirus O-glycan shield. PLOS Pathog. 7:11e1002387
     [Google Scholar]
  77. 77.
    Silver ZA, Antonopoulos A, Haslam SM, Dell A, Dickinson GM et al. 2020. Discovery of O-linked carbohydrate on HIV-1 envelope and its role in shielding against one category of broadly neutralizing antibodies. Cell Rep. 30:61862–64
     [Google Scholar]
  78. 78.
    Peng W, Rayaprolu V, Parvate AD, Pronker MF, Hui S et al. 2022. Glycan shield of the ebolavirus envelope glycoprotein GP. Commun. Biol. 5:1785
     [Google Scholar]
  79. 79.
    Cló E, Kracun SK, Nudelman AS, Jensen KJ, Liljeqvist JA et al. 2012. Characterization of the viral O-glycopeptidome: a novel tool of relevance for vaccine design and serodiagnosis. J. Virol. 86:116268–78
     [Google Scholar]
  80. 80.
    Nordén R, Nilsson J, Samuelsson E, Risinger C, Sihlbom C et al. 2019. Recombinant glycoprotein E of varicella zoster virus contains glycan-peptide motifs that modulate B cell epitopes into discrete immunological signatures. Int. J. Mol. Sci. 20:4954
     [Google Scholar]
  81. 81.
    Lal H, Cunningham AL, Godeaux O, Chlibek R, Diez-Domingo J et al. 2015. Efficacy of an adjuvanted herpes zoster subunit vaccine in older adults. N. Engl. J. Med. 372:222087–96
     [Google Scholar]
  82. 82.
    Fochesato M, Dendouga N, Boxus M. 2016. Comparative preclinical evaluation of AS01 versus other adjuvant systems in a candidate herpes zoster glycoprotein E subunit vaccine. Hum. Vaccines Immunother. 12:82092–95
     [Google Scholar]
  83. 83.
    Serafini-Cessi F, Malagolini N, Dall'Olio F, Pereira L, Campadelli-Fiume G. 1985. Oligosaccharide chains of herpes simplex virus type 2 glycoprotein gG.2. Arch. Biochem. Biophys. 240:2866–76
     [Google Scholar]
  84. 84.
    Olofsson S, Lundström M, Marsden H, Jeansson S, Vahlne A. 1986. Characterization of a herpes simplex virus type 2-specified glycoprotein with affinity for N-acetylgalactosamine-specific lectins and its identification as g92K or gG. J. Gen. Virol. 67:Part 4737–44
     [Google Scholar]
  85. 85.
    D'Arrigo I, Cló E, Bergström T, Olofsson S, Blixt O. 2013. Diverse IgG serum response to novel glycopeptide epitopes detected within immunodominant stretches of Epstein-Barr virus glycoprotein 350/220: diagnostic potential of O-glycopeptide microarrays. Glycoconj. J. 30:7633–40
     [Google Scholar]
  86. 86.
    Kennedy PGE, Gershon AA. 2018. Clinical features of varicella-zoster virus infection. Viruses 10:11609
     [Google Scholar]
  87. 87.
    Johnson RW. 2010. Herpes zoster and postherpetic neuralgia. Expert Rev. Vaccines 9:Suppl. 321–26
     [Google Scholar]
  88. 88.
    Gershon AA. 2013. Varicella zoster vaccines and their implications for development of HSV vaccines. Virology 435:129–36
     [Google Scholar]
  89. 89.
    Schmid DS, Miao C, Leung J, Johnson M, Weinberg A, Levin MJ. 2021. Comparative antibody responses to the live-attenuated and recombinant herpes zoster vaccines. J. Virol. 95:12e00240–21
     [Google Scholar]
  90. 90.
    Pihl AF, Feng S, Offersgaard A, Alzua GP, Augestad EH et al. 2022. Inactivated whole hepatitis C virus vaccine employing a licensed adjuvant elicits cross-genotype neutralizing antibodies in mice. J. Hepatol. 76:51051–61
     [Google Scholar]
  91. 91.
    Martinez O, Tantral L, Mulherkar N, Chandran K, Basler CF. 2011. Impact of Ebola mucin-like domain on antiglycoprotein antibody responses induced by Ebola virus-like particles. J. Infect. Dis. 204:Suppl. 3S825–32
     [Google Scholar]
  92. 92.
    Sanchez AJ, Vincent MJ, Erickson BR, Nichol ST. 2006. Crimean-Congo hemorrhagic fever virus glycoprotein precursor is cleaved by furin-like and SKI-1 proteases to generate a novel 38-kilodalton glycoprotein. J. Virol. 80:1514–25
     [Google Scholar]
  93. 93.
    Samuelsson E, Mirgorodskaya E, Nyström K, Bäckström M, Liljeqvist JA, Nordén R. 2022. Sialic acid and fucose residues on the SARS-CoV-2 receptor-binding domain modulate IgG antibody reactivity. ACS Infect. Dis. 8:91883–93
     [Google Scholar]
  94. 94.
    Wong P, Pamer EG. 2003. CD8 T cell responses to infectious pathogens. Annu. Rev. Immunol. 21:29–70
     [Google Scholar]
  95. 95.
    Neefjes J, Jongsma MLM, Paul P, Bakke O. 2011. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat. Rev. Immunol. 11:12823–36
     [Google Scholar]
  96. 96.
    Ninkovic T, Kinarsky L, Engelmann K, Pisarev V, Sherman S et al. 2009. Identification of O-glycosylated decapeptides within the MUC1 repeat domain as potential MHC class I (A2) binding epitopes. Mol. Immunol. 47:1131–40
     [Google Scholar]
  97. 97.
    Sun L, Middleton DR, Wantuch PL, Ozdilek A, Avci FY. 2016. Carbohydrates as T-cell antigens with implications in health and disease. Glycobiology 26:101029–40
     [Google Scholar]
  98. 98.
    Francica JR, Varela-Rohena A, Medvec A, Plesa G, Riley JL, Bates P. 2010. Steric shielding of surface epitopes and impaired immune recognition induced by the Ebola virus glycoprotein. PLOS Pathog. 6:9e1001098
     [Google Scholar]
  99. 99.
    Iversen MB, Reinert LS, Thomsen MK, Bagdonaite I, Nandakumar R et al. 2015. An innate antiviral pathway acting before interferons at epithelial surfaces. Nat. Immunol. 17:150–58
     [Google Scholar]
  100. 100.
    Sperandio M. 2006. Selectins and glycosyltransferases in leukocyte rolling in vivo. FEBS J. 273:194377–89
     [Google Scholar]
  101. 101.
    Sperandio M, Gleissner CA, Ley K. 2009. Glycosylation in immune cell trafficking. Immunol. Rev. 230:197–113
     [Google Scholar]
  102. 102.
    Kannagi R. 2002. Regulatory roles of carbohydrate ligands for selectins in the homing of lymphocytes. Curr. Opin. Struct. Biol. 12:5599–608
     [Google Scholar]
  103. 103.
    Hiraiwa N, Yabuta T, Yoritomi K, Hiraiwa M, Tanaka Y et al. 2003. Transactivation of the fucosyltransferase VII gene by human T-cell leukemia virus type 1 Tax through a variant cAMP-responsive element. Blood 101:93615–21
     [Google Scholar]
  104. 104.
    Nyström K, Nordén R, Muylaert I, Elias P, Larson G, Olofsson S. 2009. Induction of sialyl-Lex expression by herpes simplex virus type 1 is dependent on viral immediate early RNA-activated transcription of host fucosyltransferase genes. Glycobiology 19:8847–59
     [Google Scholar]
  105. 105.
    Gonzalez-Rodriguez E, Zol-Hanlon M, Bineva-Todd G, Marchesi A, Skehel Met al 2023. O-linked sialoglycans modulate the proteolysis of SARS-CoV-2 spike and likely contribute to the mutational trajectory in variants of concern. ACS Cent. Sci 9:3393–404
     [Google Scholar]
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Structure and Role of O-Linked Glycans in Viral Envelope Proteins
Annual Review of Virology 10, 283 (2023); https://doi.org/10.1146/annurev-virology-111821-121007
/content/journals/10.1146/annurev-virology-111821-121007
/content/journals/10.1146/annurev-virology-111821-121007
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