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Review

The Effects of Herpes Virus Glycoprotein Glycosylation On Viral Infection and Pathogenesis

ORCID Icon, ORCID Icon & ORCID Icon
Pages 721-732 | Received 06 Dec 2022, Accepted 01 Aug 2023, Published online: 22 Aug 2023

References

  • Fishman JA . Overview: cytomegalovirus and the herpesviruses in transplantation. Am. J. Transplant., 13(Suppl. 3), 1–8 (2013).
  • Shiley K , BlumbergE. Herpes viruses in transplant recipients: HSV, VZV, human herpes viruses, and EBV. Infect. Dis. Clin. North Am., 24(2), 373–393 (2010).
  • Astuto M , PalermoCI, CostanzoCMet al. Fatal pulmonary disease and encephalic complication in a man with HSV-1 Infection: a case report. J. Clin. Virol., 59(1), 59–62 (2014).
  • Rowe AM , StLeger AJ, JeonS, DhaliwalDK, KnickelbeinJE, HendricksRL. Herpes keratitis. Prog. Retin. Eye Res., 32, 88–101 (2013).
  • Sabugo F , Espinoza-ArayaR, MenesesMF, CuchacovichM. Acute herpes simplex virus 1 pneumonitis in a patient with systemic lupus erythematosus. J. Clin. Rheumatol., 20(1), 42–44 (2014).
  • Sili U , KayaA, MertA. Herpes simplex virus encephalitis: clinical manifestations, diagnosis and outcome in 106 adult patients. J Clin Virol., 60(2), 112–118 (2014).
  • Krummenacher C , CarfíA, EisenbergRJ, CohenGH. Entry of herpesviruses into cells: the enigma variations. Adv. Exp. Med. Biol., 790, 178–195 (2013).
  • Corrales-Aguilar E , HoffmannK, HengelH. CMV-encoded Fcγ receptors: modulators at the interface of innate and adaptive immunity. Semin. Immunopathol., 36(6), 627–640 (2014).
  • Favoreel HW , Van MinnebruggenG, VanDe Walle GR, FicinskaJ, NauwynckHJ. Herpesvirus interference with virus-specific antibodies: bridging antibodies, internalizing antibodies, and hiding from antibodies. Vet. Microbiol., 113(3-4), 257–263 (2006).
  • Spiro RG . Glycoproteins. Adv. Protein Chem., 27, 349–467 (1973).
  • Montreuil J . Primary structure of glycoprotein glycans: basis for the molecular biology of glycoproteins. Adv. Carbohydr. Chem. Biochem., 37, 157–223 (1980).
  • Hebert DN , LamribenL, PowersET, KellyJW. The intrinsic and extrinsic effects of N-linked glycans on glycoproteostasis. Nat. Chem. Biol., 10(11), 902–910 (2014).
  • Schwarz F , AebiM. Mechanisms and principles of N-linked protein glycosylation. Curr. Opin. Struct. Biol., 21(5), 576–582 (2011).
  • Bennett EP , MandelU, ClausenH, GerkenTA, FritzTA, TabakLA. Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. Glycobiology., 22(6), 736–756 (2012).
  • Hang HC , BertozziCR. The chemistry and biology of mucin-type O-linked glycosylation. Bioorg. Med. Chem., 13(17), 5021–5034 (2005).
  • Kinoshita T . Biosynthesis and biology of mammalian GPI-anchored proteins. Open Biol., 10(3), 190290 (2020).
  • Suenaga T , MatsumotoM, ArisawaFet al. Sialic acids on varicella-zoster virus glycoprotein B are required for cell-cell fusion. J. Biol. Chem., 290(32), 19833–19843 (2015).
  • Yang Q , HughesTA, KelkarAet al. Inhibition of SARS-CoV-2 viral entry upon blocking N- and O-glycan elaboration. eLife., 9, e61552 (2020).
  • Vallbracht M , KluppBG, MettenleiterTC. Influence of N-glycosylation on expression and function of pseudorabies virus glycoprotein gB. Pathogens., 10(1), 61 (2021).
  • Crispin M , WardAB, WilsonIA. Structure and immune recognition of the HIV glycan shield. Annu. Rev. Biophys., 47, 499–523 (2018).
  • Helle F , DuverlieG, DubuissonJ. The hepatitis C virus glycan shield and evasion of the humoral immune response. Viruses., 3(10), 1909–1932 (2011).
  • Jones NA , GeraghtyRJ. Fusion activity of lipid-anchored envelope glycoproteins of herpes simplex virus type 1. Virology, 324(1), 213–228 (2004).
  • Tal-Singer R , PengC, PonceDe Leon Met al. Interaction of herpes simplex virus glycoprotein gC with mammalian cell surface molecules. J. Virol., 69(7), 4471–4483 (1995).
  • Lu H , CherepanovaNA, GilmoreR, ContessaJN, LehrmanMA. Targeting STT3A-oligosaccharyltransferase with NGI-1 causes herpes simplex virus 1 dysfunction. FASEB J., 33(6), 6801–6812 (2019).
  • Luo S , HuK, HeSet al. Contribution of N-linked glycans on HSV-2 gB to cell-cell fusion and viral entry. Virology, 483, 72–82 (2015).
  • Fukui A , MaruzuruY, TakeshimaK, KoyanagiN, KatoA, KawaguchiY. Establishment of a system to quantify wild-type herpes simplex virus-induced cell-cell fusion reveals a role of N-glycosylation of HSV-1 envelope glycoprotein B in cell-cell fusion. Microbiol. Immunol., 67(3), 114–119 (2023).
  • Rider PJF , NaderiM, BergeronS, ChouljenkoVN, BrylinskiM, KousoulasKG. Cysteines and N-Glycosylation Sites Conserved among All Alphaherpesviruses Regulate Membrane Fusion in Herpes Simplex Virus 1 Infection. J. Virol., 91(21), e00873–17 (2017).
  • Satoh T , AriiJ, SuenagaTet al. PILRalpha is a herpes simplex virus-1 entry coreceptor that associates with glycoprotein B. Cell, 132(6), 935–944 (2008).
  • Wang J , FanQ, SatohTet 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., 83(24), 13042–13045 (2009).
  • Mårdberg K , NyströmK, TarpMAet 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., 14(7), 571–581 (2004).
  • Serafini-Cessi F , MalagoliniN, NanniMet al. Characterization of N- and O-linked oligosaccharides of glycoprotein 350 from Epstein–Barr virus. Virology, 170(1), 1–10 (1989).
  • Chen J , SathiyamoorthyK, ZhangXet al. Ephrin receptor A2 is a functional entry receptor for Epstein–Barr virus. Nat. Microbiol., 3(2), 172–180 (2018).
  • Chen J , SchallerS, JardetzkyTS, LongneckerR. Epstein–Barr virus gH/gL and Kaposi’s sarcoma-associated herpesvirus gH/gL bind to different sites on EphA2 to trigger fusion. J. Virol., 94(21), e01454–20 (2020).
  • Sathiyamoorthy K , JiangJ, HuYXet al. Assembly and architecture of the EBV B cell entry triggering complex. PLOS Pathog., 10(8), e1004309 (2014).
  • Liu F , MarquardtG, KirschnerAN, LongneckerR, JardetzkyTS. Mapping the N-terminal residues of Epstein–Barr virus gp42 that bind gH/gL by using fluorescence polarization and cell-based fusion assays. J. Virol., 84(19), 10375–10385 (2010).
  • Zhang HJ , TianJ, QiXKet al. Epstein–Barr virus activates F-box protein FBXO2 to limit viral infectivity by targeting glycoprotein B for degradation. PLOS Pathog., 14(7), e1007208 (2018).
  • Möhl BS , ChenJ, ParkSJ, JardetzkyTS, LongneckerR. Epstein–Barr virus fusion with epithelial cells triggered by gB is restricted by a gL glycosylation site. J. Virol., 91(23), e01255–17 (2017).
  • Wang D , ShenkT. Human cytomegalovirus virion protein complex required for epithelial and endothelial cell tropism. Proc. Natl Acad. Sci. USA, 102(50), 18153–18158 (2005).
  • E X , MeranerP, LuPet al. OR14I1 is a receptor for the human cytomegalovirus pentameric complex and defines viral epithelial cell tropism. Proc Natl Acad. Sci. USA, 116(14), 7043–7052 (2019).
  • Martinez-Martin N , MarcandalliJ, HuangCSet al. An unbiased screen for human cytomegalovirus identifies neuropilin-2 as a central viral receptor. Cell, 174(5), 1158–1171.e1119 (2018).
  • Kabanova A , MarcandalliJ, ZhouTet al. Platelet-derived growth factor-α receptor is the cellular receptor for human cytomegalovirus gHgLgO trimer. Nat. Microbiol., 1(8), 16082 (2016).
  • Zhou M , LanchyJM, RyckmanBJ. Human Cytomegalovirus gH/gL/gO Promotes the Fusion Step of Entry into All Cell Types, whereas gH/gL/UL128-131 Broadens Virus Tropism through a Distinct Mechanism. J. Virol., 89(17), 8999–9009 (2015).
  • Wang D , ShenkT. Human cytomegalovirus UL131 open reading frame is required for epithelial cell tropism. J. Virol., 79(16), 10330–10338 (2005).
  • Ryckman BJ , JarvisMA, DrummondDD, NelsonJA, JohnsonDC. Human cytomegalovirus entry into epithelial and endothelial cells depends on genes UL128 to UL150 and occurs by endocytosis and low-pH fusion. J. Virol., 80(2), 710–722 (2006).
  • Isaacson MK , ComptonT. Human cytomegalovirus glycoprotein B is required for virus entry and cell-to-cell spread but not for virion attachment, assembly, or egress. J. Virol., 83(8), 3891–3903 (2009).
  • Zheng L , LiH, FuL, LiuS, YanQ, LengSX. Blocking cellular N-glycosylation suppresses human cytomegalovirus entry in human fibroblasts. Microb. Pathog., 138, 103776 (2020).
  • Biller M , MårdbergK, HassanHet 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., 10(12), 1259–1269 (2000).
  • Dall’olio F , MalagoliniN, SpezialiV, Campadelli-FiumeG, Serafini-CessiF. Sialylated oligosaccharides O-glycosidically linked to glycoprotein C from herpes simplex virus type 1. J. Virol., 56(1), 127–134 (1985).
  • Peng T , PonceDe Leon M, NovotnyMJet al. Structural and antigenic analysis of a truncated form of the herpes simplex virus glycoprotein gH-gL complex. J. Virol., 72(7), 6092–6103 (1998).
  • Serafini-Cessi F , Dall’olioF, MalagoliniN, PereiraL, Campadelli-FiumeG. Comparative study on O-linked oligosaccharides of glycoprotein D of herpes simplex virus types 1 and 2. J. Gen. Virol., 69(Pt 4), 869–877 (1988).
  • Teuton JR , BrandtCR. Sialic acid on herpes simplex virus type 1 envelope glycoproteins is required for efficient infection of cells. J. Virol., 81(8), 3731–3739 (2007).
  • Kühn JE , EingBR, BrossmerR, MunkK, BraunRW. Removal of N-linked carbohydrates decreases the infectivity of herpes simplex virus type 1. J. Gen. Virol., 69(Pt 11), 2847–2858 (1988).
  • Carfí A , WillisSH, WhitbeckJCet al. Herpes simplex virus glycoprotein D bound to the human receptor HveA. Mol. Cell., 8(1), 169–179 (2001).
  • Stone JA , NicolaAV, BaumLG, AguilarHC. Multiple novel functions of henipavirus O-glycans: the first O-glycan functions identified in the Paramyxovirus family. PLOS Pathog., 12(2), e1005445 (2016).
  • Hart GW , HousleyMP, SlawsonC. Cycling of O-linked beta-N-acetylglucosamine on nucleocytoplasmic proteins. Nature, 446(7139), 1017–1022 (2007).
  • Angelova M , Ortiz-MeozRF, WalkerS, KnipeDM. Inhibition of O-Linked n-acetylglucosamine transferase reduces replication of herpes simplex virus and human cytomegalovirus. J. Virol., 89(16), 8474–8483 (2015).
  • Jochmann R , PfannstielJ, ChudasamaP, KuhnE, KonradA, StürzlM. O-GlcNAc transferase inhibits KSHV propagation and modifies replication relevant viral proteins as detected by systematic O-GlcNAcylation analysis. Glycobiology., 23(10), 1114–1130 (2013).
  • Xu Y , AucoinDP, HueteAR, CeiSA, HansonLJ, PariGS. A Kaposi’s sarcoma-associated herpesvirus/human herpesvirus 8 ORF50 deletion mutant is defective for reactivation of latent virus and DNA replication. J. Virol., 79(6), 3479–3487 (2005).
  • Papp B , MotlaghN, SmindakRJet al. Genome-wide identification of direct RTA targets reveals key host factors for Kaposi’s sarcoma-associated herpesvirus lytic reactivation. J. Virol., 93(5), e01978–18 (2019).
  • Ko YC , TsaiWH, WangPWet al. Suppressive regulation of KSHV RTA with O-GlcNAcylation. J Biomed Sci., 19(1), 12 (2012).
  • Altgärde N , ErikssonC, PeerboomNet al. Mucin-like region of herpes simplex virus Type 1 attachment protein glycoprotein C (gC) modulates the virus–glycosaminoglycan interaction. J. Biol. Chem., 290(35), 21473–21485 (2015).
  • Delguste M , PeerboomN, LeBrun Get al. Regulatory mechanisms of the mucin-like region on herpes simplex virus during cellular attachment. ACS Chem. Biology., 14(3), 534–542 (2019).
  • Alexander S , ElderJH. Carbohydrate dramatically influences immune reactivity of antisera to viral glycoprotein antigens. Science, 226(4680), 1328–1330 (1984).
  • Khyatti M , PatelPC, StefanescuI, MenezesJ. Epstein–Barr virus (EBV) glycoprotein gp350 expressed on transfected cells resistant to natural killer cell activity serves as a target antigen for EBV-specific antibody-dependent cellular cytotoxicity. J. Virol., 65(2), 996–1001 (1991).
  • Thorley-Lawson DA , PoodryCA. Identification and isolation of the main component (gp350-gp220) of Epstein–Barr virus responsible for generating neutralizing antibodies in vivo. J. Virol., 43(2), 730–736 (1982).
  • Servat E , RoBW, CayatteCet al. Identification of the critical attribute(s) of EBV gp350 antigen required for elicitation of a neutralizing antibody response in vivo. Vaccine, 33(48), 6771–6777 (2015).
  • Khyatti M , AhmadA, BlagdonM, FradeR, MenezesJ. Binding of the endogenously expressed Epstein–Barr virus (EBV) envelope glycoprotein gp350 with the viral receptor masks the major EBV-neutralizing epitope and affects gp350-specific ADCC. J. Leukoc. Biol., 64(2), 192–197 (1998).
  • Machiels B , LétéC, GuillaumeAet al. Antibody evasion by a gammaherpesvirus O-glycan shield. PLOS Pathog., 7(11), e1002387 (2011).
  • Gram AM , OosenbrugT, LindenberghMFet al. The Epstein–Barr Virus glycoprotein gp150 forms an immune-evasive glycan shield at the surface of infected cells. PLOS Pathog., 12(4), e1005550 (2016).
  • Pötzsch S , SpindlerN, WiegersAKet al. B cell repertoire analysis identifies new antigenic domains on glycoprotein B of human cytomegalovirus which are target of neutralizing antibodies. PLOS Pathog., 7(8), e1002172 (2011).
  • Burke HG , HeldweinEE. Crystal structure of the human cytomegalovirus glycoprotein B. PLOS Pathog., 11(10), e1005227 (2015).
  • Kropff B , BurkhardtC, SchottJet al. Glycoprotein N of human cytomegalovirus protects the virus from neutralizing antibodies. PLOS Pathog., 8(10), e1002999 (2012).
  • Jiang XJ , SampaioKL, EttischerNet al. UL74 of human cytomegalovirus reduces the inhibitory effect of gH-specific and gB-specific antibodies. Arch. Virol., 156(12), 2145–2155 (2011).
  • Glorioso J , SzczesiulMS, MarlinSD, LevineM. Inhibition of glycosylation of herpes simplex virus glycoproteins: identification of antigenic and immunogenic partially glycosylated glycopeptides on the cell surface membrane. Virology, 126(1), 1–18 (1983).
  • Fukui A , MaruzuruY, OhnoSet al. Dual impacts of a glycan shield on the envelope glycoprotein B of HSV-1: evasion from human antibodies in vivo and neurovirulence. mBio. doi:10.1128/mbio.00992-23e0099223 (2023).
  • Cocchi F , MenottiL, MirandolaP, LopezM, Campadelli-FiumeG. The ectodomain of a novel member of the immunoglobulin subfamily related to the poliovirus receptor has the attributes of a bona fide receptor for herpes simplex virus types 1 and 2 in human cells. J. Virol., 72(12), 9992–10002 (1998).
  • Hidaka Y , SakaiY, TohY, MoriR. Glycoprotein C of herpes simplex virus type 1 is essential for the virus to evade antibody-independent complement-mediated virus inactivation and lysis of virus-infected cells. J. Gen. Virol., 72(Pt 4), 915–921 (1991).
  • Smiley ML , HoxieJA, FriedmanHM. Herpes simplex virus type 1 infection of endothelial, epithelial, and fibroblast cells induces a receptor for C3b. J. Immunol., 134(4), 2673–2678 (1985).
  • Mcgreal EP , MillerJL, GordonS. Ligand recognition by antigen-presenting cell C-type lectin receptors. Curr. Opin. Immunol., 17(1), 18–24 (2005).
  • Geijtenbeek TB , KwonDS, TorensmaRet al. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell, 100(5), 587–597 (2000).
  • Gardai SJ , XiaoYQ, DickinsonMet al. By binding SIRPalpha or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell, 115(1), 13–23 (2003).
  • Turner MW , HamvasRM. Mannose-binding lectin: structure, function, genetics and disease associations. Rev. Immunogenet., 2(3), 305–322 (2000).
  • Drickamer K . Two distinct classes of carbohydrate-recognition domains in animal lectins. J. Biol. Chem., 263(20), 9557–9560 (1988).
  • Haagsman HP , HawgoodS, SargeantTet al. The major lung surfactant protein, SP 28–36, is a calcium-dependent, carbohydrate-binding protein. J. Biol. Chem., 262(29), 13877–13880 (1987).
  • Van Iwaarden JF , Van StrijpJA, EbskampMJ, WelmersAC, VerhoefJ, Van GoldeLM. Surfactant protein A is opsonin in phagocytosis of herpes simplex virus type 1 by rat alveolar macrophages. Am. J. Physiol., 261(2 Pt 1), L204–209 (1991).
  • Van Iwaarden JF , Van StrijpJA, VisserH, HaagsmanHP, VerhoefJ, Van GoldeLM. Binding of surfactant protein A (SP-A) to herpes simplex virus type 1-infected cells is mediated by the carbohydrate moiety of SP-A. J. Biol. Chemistry., 267(35), 25039–25043 (1992).
  • Weyer C , SabatR, WisselH, KrügerDH, StevensPA, PröschS. Surfactant protein A binding to cytomegalovirus proteins enhances virus entry into rat lung cells. Am. J. Respir. Cell Mol. Biol., 23(1), 71–78 (2000).
  • Lubinski J , NagashunmugamT, FriedmanHM. Viral interference with antibody and complement. Semin. Cell Dev. Biol., 9(3), 329–337 (1998).
  • Thielens NM , Tacnet-DelormeP, ArlaudGJ. Interaction of C1q and mannan-binding lectin with viruses. Immunobiology, 205(4-5), 563–574 (2002).
  • Hart ML , SaifuddinM, SpearGT. Glycosylation inhibitors and neuraminidase enhance human immunodeficiency virus type 1 binding and neutralization by mannose-binding lectin. J. Gen. Virol., 84(Pt 2), 353–360 (2003).
  • Friedman HM , WangL, PangburnMK, LambrisJD, LubinskiJ. Novel mechanism of antibody-independent complement neutralization of herpes simplex virus type 1. J. Immunol., 165(8), 4528–4536 (2000).
  • Zheng ZM , HsiungGD. Complement-requiring neutralizing antibody in guinea pigs with primary and recurrent genital herpes. Proc. Soc. Exp. Biol. Med., 177(2), 332–336 (1984).
  • Verschoor A , BrockmanMA, GadjevaM, KnipeDM, CarrollMC. Myeloid C3 determines induction of humoral responses to peripheral herpes simplex virus infection. J. Immunol., 171(10), 5363–5371 (2003).
  • Gadjeva M , PaludanSR, ThielSet al. Mannan-binding lectin modulates the response to HSV-2 infection. Clin. Exp. Immunol., 138(2), 304–311 (2004).
  • Manuel O , PascualM, TrendelenburgM, MeylanPR. Association between mannose-binding lectin deficiency and cytomegalovirus infection after kidney transplantation. Transplantation, 83(3), 359–362 (2007).
  • Wu W , ChenY, QiaoH, TaoR, GuW, ShangS. Human mannose-binding lectin inhibits human cytomegalovirus infection in human embryonic pulmonary fibroblast. APMIS, 120(8), 675–682 (2012).
  • De Jong M , DeWitte L, BolmstedtA, Van KooykY, GeijtenbeekTBH. Dendritic cells mediate herpes simplex virus infection and transmission through the C-type lectin DC-SIGN. J. Gen. Virol., 89(Pt 10), 2398–2409 (2008).
  • Plazolles N , HumbertJM, VachotL, VerrierB, HockeC, HalaryF. Pivotal advance: the promotion of soluble DC-SIGN release by inflammatory signals and its enhancement of cytomegalovirus-mediated cis-infection of myeloid dendritic cells. J. Leukoc. Biol., 89(3), 329–342 (2011).
  • Kalu NN , DesaiPJ, ShirleyCM, GibsonW, DennisPA, AmbinderRF. Nelfinavir inhibits maturation and export of herpes simplex virus 1. J. Virol., 88(10), 5455–5461 (2014).
  • Le Tortorec A , WilleyS, NeilSJ. Antiviral inhibition of enveloped virus release by tetherin/BST-2: action and counteraction. Viruses., 3(5), 520–540 (2011).
  • Swiecki M , OmattageNS, BrettTJ. BST-2/tetherin: structural biology, viral antagonism, and immunobiology of a potent host antiviral factor. Mol.Immunology., 54(2), 132–139 (2013).
  • Mansouri M , ViswanathanK, DouglasJLet al. Molecular mechanism of BST2/tetherin downregulation by K5/MIR2 of Kaposi’s sarcoma-associated herpesvirus. J. Virol., 83(19), 9672–9681 (2009).
  • Pardieu C , ViganR, WilsonSJet al. The RING-CH ligase K5 antagonizes restriction of KSHV and HIV-1 particle release by mediating ubiquitin-dependent endosomal degradation of tetherin. PLOS Pathog., 6(4), e1000843 (2010).
  • Zenner HL , MauricioR, BantingG, CrumpCM. Herpes simplex virus 1 counteracts tetherin restriction via its virion host shutoff activity. J. Virol., 87(24), 13115–13123 (2013).
  • Viswanathan K , SmithMS, MalouliD, MansouriM, NelsonJA, FrühK. BST2/Tetherin enhances entry of human cytomegalovirus. PLOS Pathog., 7(11), e1002332 (2011).
  • Del Solar V , GuptaR, ZhouY, PawlowskiG, MattaKL, NeelameghamS. Robustness in glycosylation systems: effect of modified monosaccharides, acceptor decoys and azido sugars on cellular nucleotide-sugar levels and pattern of N-linked glycosylation. Mol Omics., 16(4), 377–386 (2020).
  • Pastuch-Gawolek G , ChaubeyB, SzewczykB, KrolE. Novel thioglycosyl analogs of glycosyltransferase substrates as antiviral compounds against classical swine fever virus and hepatitis C virus. Eur. J. Med. Chem., 137, 247–262 (2017).

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