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PMID: 17398101 Published · ppublish English Journal Article Review

Virus glycosylation: role in virulence and immune interactions.

Trends in microbiology ·Vol. 15 ·No. 5 ·2007-05-00 ·Pages 211-8

Vigerust DJ, Shepherd VL

Abstract

The study of N-linked glycosylation as it relates to virus biology has become an area of intense interest in recent years due to its ability to impart various advantages to virus survival and virulence. HIV and influenza, two clear threats to human health, have been shown to rely on expression of specific oligosaccharides to evade detection by the host immune system. Additionally, other viruses such as Hendra, SARS-CoV, influenza, hepatitis and West Nile rely on N-linked glycosylation for crucial functions such as entry into host cells, proteolytic processing and protein trafficking. This review focuses on recent findings on the importance of glycosylation to viral virulence and immune evasion for several prominent human pathogens.

MeSH Terms
Glycoproteins/metabolism Glycosylation HIV-1/metabolism,pathogenicity Influenza A virus/metabolism,pathogenicity Models, Biological Receptors, Immunologic/metabolism Viral Proteins/metabolism Virulence Viruses/metabolism,pathogenicity West Nile virus/metabolism,pathogenicity
Chemicals
Glycoproteins Receptors, Immunologic Viral Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Vigerust David J
Department of Pediatrics, Program in Vaccine Sciences, Vanderbilt University School of Medicine, Nashville, TN 37232, USA. [email protected]
Shepherd Virginia L
References (80)
80 references, click to expand
  1. Differential N-linked glycosylation of human immunodeficiency virus and Ebola virus envelope glycoproteins modulates interactions with DC-SIGN and DC-SIGNR.
    J Virol. 2003 Jan;77(2):1337-46 PMID: 12502850
  2. Carbohydrate-binding agents efficiently prevent dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin (DC-SIGN)-directed HIV-1 transmission to T lymphocytes.
    Mol Pharmacol. 2007 Jan;71(1):3-11 PMID: 17056872
  3. Antibody neutralization and escape by HIV-1.
    Nature. 2003 Mar 20;422(6929):307-12 PMID: 12646921
  4. Hydroxychloroquine, hydroxyurea and didanosine as initial therapy for HIV-infected patients with low viral load: safety, efficacy and resistance profile after 144 weeks.
    HIV Med. 2005 Jan;6(1):13-20 PMID: 15670247
  5. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin.
    Annu Rev Biochem. 2000;69:531-69 PMID: 10966468
  6. Dissection of the carbohydrate specificity of the broadly neutralizing anti-HIV-1 antibody 2G12.
    Proc Natl Acad Sci U S A. 2005 Sep 20;102(38):13372-7 PMID: 16174734
  7. Envelope protein glycosylation status influences mouse neuroinvasion phenotype of genetic lineage 1 West Nile virus strains.
    J Virol. 2005 Jul;79(13):8339-47 PMID: 15956579
  8. Surfactant protein D enhances clearance of influenza A virus from the lung in vivo.
    J Immunol. 2001 Nov 15;167(10):5868-73 PMID: 11698462
  9. Dual function of C-type lectin-like receptors in the immune system.
    Curr Opin Cell Biol. 2003 Oct;15(5):539-46 PMID: 14519388
  10. Chloroquine exerts an additive in vitro anti-HIV type 1 effect when associated with didanosine and hydroxyurea.
    AIDS Res Hum Retroviruses. 1999 Sep 20;15(14):1241-7 PMID: 10505672
  11. Antibody domain exchange is an immunological solution to carbohydrate cluster recognition.
    Science. 2003 Jun 27;300(5628):2065-71 PMID: 12829775
  12. Resistance of human immunodeficiency virus type 1 to the high-mannose binding agents cyanovirin N and concanavalin A.
    J Virol. 2005 Jun;79(12):7777-84 PMID: 15919930
  13. Glycosylation affects cleavage of an H5N2 influenza virus hemagglutinin and regulates virulence.
    Proc Natl Acad Sci U S A. 1987 Jan;84(1):36-40 PMID: 3467357
  14. Receptor binding, fusion inhibition, and induction of cross-reactive neutralizing antibodies by a soluble G glycoprotein of Hendra virus.
    J Virol. 2005 Jun;79(11):6690-702 PMID: 15890907
  15. 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 Dec 1;281(48):37183-94 PMID: 17001080
  16. Folding of the human immunodeficiency virus type 1 envelope glycoprotein in the endoplasmic reticulum.
    Biochimie. 2001 Aug;83(8):783-90 PMID: 11530211
  17. CD4-independent infection of astrocytes by human immunodeficiency virus type 1: requirement for the human mannose receptor.
    J Virol. 2004 Apr;78(8):4120-33 PMID: 15047828
  18. N-Glycans in the gp120 V1/V2 domain of the HIV-1 strain NL4-3 are indispensable for viral infectivity and resistance against antibody neutralization.
    Med Microbiol Immunol. 2006 Sep;195(3):165-72 PMID: 16547752
  19. The signal peptide of the ebolavirus glycoprotein influences interaction with the cellular lectins DC-SIGN and DC-SIGNR.
    J Virol. 2006 Jul;80(13):6305-17 PMID: 16775318
  20. Role of N-linked glycans of envelope glycoproteins in infectivity of human immunodeficiency virus type 1.
    J Virol. 1990 Jun;64(6):2841-8 PMID: 2335819
  21. Glycosylation of haemagglutinin and stalk-length of neuraminidase combine to regulate the growth of avian influenza viruses in tissue culture.
    Virus Res. 2001 Nov 5;79(1-2):177-85 PMID: 11551658
  22. Potent anti-influenza activity of cyanovirin-N and interactions with viral hemagglutinin.
    Antimicrob Agents Chemother. 2003 Aug;47(8):2518-25 PMID: 12878514
  23. Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection.
    Proc Natl Acad Sci U S A. 2005 Dec 20;102(51):18514-9 PMID: 16339909
  24. Analysis of the glycosylation sites of hepatitis C virus (HCV) glycoprotein E1 and the influence of E1 glycans on the formation of the HCV glycoprotein complex.
    J Gen Virol. 1999 Apr;80 ( Pt 4):887-896 PMID: 10211957
  25. Role of overlapping glycosylation sequons in antigenic properties, intracellular transport and biological activities of influenza A/H2N2 virus haemagglutinin.
    J Gen Virol. 2002 Dec;83(Pt 12):3067-3074 PMID: 12466483
  26. HCV E2 glycoprotein: mutagenesis of N-linked glycosylation sites and its effects on E2 expression and processing.
    Virology. 2004 Feb 5;319(1):36-48 PMID: 14967486
  27. Involvement of the mannose receptor in infection of macrophages by influenza virus.
    J Virol. 2000 Jun;74(11):5190-7 PMID: 10799594
  28. DC-SIGN: binding receptors for hepatitis C virus.
    Chin Med J (Engl). 2004 Sep;117(9):1395-400 PMID: 15377434
  29. Addition of N-glycans in the stalk of the Newcastle disease virus HN protein blocks its interaction with the F protein and prevents fusion.
    J Virol. 2006 Jan;80(2):623-33 PMID: 16378965
  30. N-linked glycosylation of west nile virus envelope proteins influences particle assembly and infectivity.
    J Virol. 2005 Nov;79(21):13262-74 PMID: 16227249
  31. Microdomains of the C-type lectin DC-SIGN are portals for virus entry into dendritic cells.
    J Cell Biol. 2004 Jan 5;164(1):145-55 PMID: 14709546
  32. Evidence for a protective role of pulmonary surfactant protein D (SP-D) against influenza A viruses.
    J Clin Invest. 1994 Jul;94(1):311-9 PMID: 8040272
  33. Biological significance of glycosylation of the envelope protein of Kunjin virus.
    Ann N Y Acad Sci. 2001 Dec;951:361-3 PMID: 11797800
  34. Collectin-mediated antiviral host defense of the lung: evidence from influenza virus infection of mice.
    J Virol. 1997 Nov;71(11):8204-12 PMID: 9343171
  35. DC-SIGN and L-SIGN are high affinity binding receptors for hepatitis C virus glycoprotein E2.
    J Biol Chem. 2003 May 30;278(22):20358-66 PMID: 12609975
  36. Crystal structures of the HIV-1 inhibitory cyanobacterial protein MVL free and bound to Man3GlcNAc2: structural basis for specificity and high-affinity binding to the core pentasaccharide from n-linked oligomannoside.
    J Biol Chem. 2005 Aug 12;280(32):29269-76 PMID: 15937331
  37. Enhanced antiviral and opsonic activity of a human mannose-binding lectin and surfactant protein D chimera.
    J Immunol. 2000 Aug 15;165(4):2108-15 PMID: 10925296
  38. Interdependence of hemagglutinin glycosylation and neuraminidase as regulators of influenza virus growth: a study by reverse genetics.
    J Virol. 2000 Jul;74(14):6316-23 PMID: 10864641
  39. The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120.
    J Virol. 2002 Jul;76(14):7293-305 PMID: 12072528
  40. Influence of N-linked glycans on intracellular transport of hepatitis C virus E1 chimeric glycoprotein and its role in pseudotype virus infectivity.
    Virology. 2004 Jul 1;324(2):273-85 PMID: 15207615
  41. LSECtin interacts with filovirus glycoproteins and the spike protein of SARS coronavirus.
    Virology. 2005 Sep 30;340(2):224-36 PMID: 16051304
  42. Structure of antigenic sites on the haemagglutinin molecule of H5 avian influenza virus and phenotypic variation of escape mutants.
    J Gen Virol. 2002 Oct;83(Pt 10):2497-2505 PMID: 12237433
  43. Eight-plasmid system for rapid generation of influenza virus vaccines.
    Vaccine. 2002 Aug 19;20(25-26):3165-70 PMID: 12163268
  44. DC-SIGN and DC-SIGNR interact with the glycoprotein of Marburg virus and the S protein of severe acute respiratory syndrome coronavirus.
    J Virol. 2004 Nov;78(21):12090-5 PMID: 15479853
  45. Interaction of C1q and mannan-binding lectin with viruses.
    Immunobiology. 2002 Sep;205(4-5):563-74 PMID: 12396016
  46. Influence of N-glycans on processing and biological activity of the nipah virus fusion protein.
    J Virol. 2004 Jul;78(13):7274-8 PMID: 15194804
  47. The role of single N-glycans in proteolytic processing and cell surface transport of the Lassa virus glycoprotein GP-C.
    Virol J. 2006 May 31;3:41 PMID: 16737539
  48. HIV-1 Nef mediates post-translational down-regulation and redistribution of the mannose receptor.
    J Leukoc Biol. 2005 Apr;77(4):522-34 PMID: 15637102
  49. Surfactant protein D binds to human immunodeficiency virus (HIV) envelope protein gp120 and inhibits HIV replication.
    J Gen Virol. 2005 Nov;86(Pt 11):3097-3107 PMID: 16227233
  50. Importance of hemagglutinin glycosylation for the biological functions of influenza virus.
    Virus Res. 2002 Jan 30;82(1-2):73-5 PMID: 11885954
  51. Mannose binding lectin (MBL) and HIV.
    Mol Immunol. 2005 Feb;42(2):145-52 PMID: 15488604
  52. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells.
    Cell. 2000 Mar 3;100(5):587-97 PMID: 10721995
  53. High mannose glycans and sialic acid on gp120 regulate binding of mannose-binding lectin (MBL) to HIV type 1.
    AIDS Res Hum Retroviruses. 2002 Nov 20;18(17):1311-7 PMID: 12487819
  54. Viral envelope protein glycosylation is a molecular determinant of the neuroinvasiveness of the New York strain of West Nile virus.
    J Gen Virol. 2004 Dec;85(Pt 12):3637-3645 PMID: 15557236
  55. The glycosylation site in the envelope protein of West Nile virus (Sarafend) plays an important role in replication and maturation processes.
    J Gen Virol. 2006 Mar;87(Pt 3):613-22 PMID: 16476982
  56. Carbohydrates of influenza virus. V. Oligosaccharides attached to individual glycosylation sites of the hemagglutinin of fowl plague virus.
    Virology. 1984 Feb;133(1):77-91 PMID: 6422625
  57. Chloroquine and hydroxychloroquine as inhibitors of human immunodeficiency virus (HIV-1) activity.
    Curr Pharm Des. 2004;10(21):2643-8 PMID: 15320751
  58. Effect of tunicamycin on expression of epitopes on Japanese encephalitis virus glycoprotein E in porcine kidney cells.
    Acta Virol. 2000 Dec;44(6):359-64 PMID: 11332279
  59. Characterization of human metapneumovirus F protein-promoted membrane fusion: critical roles for proteolytic processing and low pH.
    J Virol. 2006 Nov;80(22):10931-41 PMID: 16971452
  60. Salivary agglutinin and lung scavenger receptor cysteine-rich glycoprotein 340 have broad anti-influenza activities and interactions with surfactant protein D that vary according to donor source and sialylation.
    Biochem J. 2006 Jan 15;393(Pt 2):545-53 PMID: 16190864
  61. Pulmonary collectins modulate strain-specific influenza a virus infection and host responses.
    J Virol. 2004 Aug;78(16):8565-72 PMID: 15280465
  62. Cooperative anti-influenza activities of respiratory innate immune proteins and neuraminidase inhibitor.
    Am J Physiol Lung Cell Mol Physiol. 2005 May;288(5):L831-40 PMID: 15608147
  63. West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection.
    J Virol. 2006 Feb;80(3):1290-301 PMID: 16415006
  64. Hydroxychloroquine treatment of patients with human immunodeficiency virus type 1.
    Clin Ther. 1995 Jul-Aug;17(4):622-36 PMID: 8565026
  65. Role of N-linked glycans on bunyamwera virus glycoproteins in intracellular trafficking, protein folding, and virus infectivity.
    J Virol. 2005 Nov;79(21):13725-34 PMID: 16227292
  66. Glycosylation of hepatitis C virus envelope proteins.
    Biochimie. 2003 Mar-Apr;85(3-4):295-301 PMID: 12770768
  67. HIV gp120 receptors on human dendritic cells.
    Blood. 2001 Oct 15;98(8):2482-8 PMID: 11588046
  68. Effect of addition of new oligosaccharide chains to the globular head of influenza A/H2N2 virus haemagglutinin on the intracellular transport and biological activities of the molecule.
    J Gen Virol. 2002 May;83(Pt 5):1137-1146 PMID: 11961269
  69. Role of N-linked glycans in the functions of hepatitis C virus envelope glycoproteins.
    J Virol. 2005 Jul;79(13):8400-9 PMID: 15956584
  70. Role of protein N-glycosylation in pathogenesis of human immunodeficiency virus type 1.
    Proc Natl Acad Sci U S A. 1988 Dec;85(23):9248-52 PMID: 3264072
  71. Effect of the addition of oligosaccharides on the biological activities and antigenicity of influenza A/H3N2 virus hemagglutinin.
    J Virol. 2004 Sep;78(18):9605-11 PMID: 15331693
  72. Evolutionary and immunological implications of contemporary HIV-1 variation.
    Br Med Bull. 2001;58:19-42 PMID: 11714622
  73. Involvement of macrophage mannose receptor in the binding and transmission of HIV by macrophages.
    Eur J Immunol. 2003 Feb;33(2):483-93 PMID: 12645947
  74. Human immunodeficiency virus type 1 V1-V2 envelope loop sequences expand and add glycosylation sites over the course of infection, and these modifications affect antibody neutralization sensitivity.
    J Virol. 2006 Oct;80(19):9586-98 PMID: 16973562
  75. N-linked glycans direct the cotranslational folding pathway of influenza hemagglutinin.
    Mol Cell. 2003 Jan;11(1):79-90 PMID: 12535523
  76. N-glycans on Nipah virus fusion protein protect against neutralization but reduce membrane fusion and viral entry.
    J Virol. 2006 May;80(10):4878-89 PMID: 16641279
  77. New insights into the antiviral effects of chloroquine.
    Lancet Infect Dis. 2006 Feb;6(2):67-9 PMID: 16439323
  78. Evolutionary interactions between N-linked glycosylation sites in the HIV-1 envelope.
    PLoS Comput Biol. 2007 Jan 19;3(1):e11 PMID: 17238283
  79. Epidemiology and pathogenesis of influenza.
    J Antimicrob Chemother. 1999 Nov;44 Suppl B:3-9 PMID: 10877456
  80. Glycosylation of the severe acute respiratory syndrome coronavirus triple-spanning membrane proteins 3a and M.
    J Virol. 2006 Mar;80(5):2326-36 PMID: 16474139
Article Info
Journal
Trends in microbiology
Abbr.
Trends Microbiol
ISSN
0966-842X
Published
2007-05-00
Epub
2007-00-29
Pages
211-8
Language
English
Region
England
NLM ID
9310916
PMCID
PMC7127133
Subset
IM
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