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Role of Glycoproteins in Virus–Human Cell Interactions

  • Thomas A. Bowden
  • Elizabeth E. FryEmail author
Chapter
  • 888 Downloads

Abstract

Glycosylation of viral proteins is clearly advantageous to virus survival, having roles in cell entry, proteolytic processing, trafficking and immune evasion. For enveloped RNA viruses, including many important human pathogens, entry into host cells tends to be mediated by viral glycoproteins. Structural studies of glycoproteins from different viral families have gradually elucidated the mechanisms by which this occurs. We illustrate this by providing examples from recent studies and show that clear differences exist between viruses which use individual glycoproteins for attachment and fusion, and those that use a single glycoprotein for both functions. However, in all cases a similar end-point is reached. Understanding the biology of infection and host responses should lead to the development of enhanced therapeutics.

Keywords

Structural virology Viral glycoprotein Protein–protein interactions Membrane fusion Immune evasion 

Abbreviations

C

core protein

CD46

cluster of differentiation 46

CFPV

canine feline parvovirus

DC-SIGN

Dendritic Cell-Specific Intercellular adhesion molecule-3-Grabbing Non-integrin

DENV

Dengue virus

α-DG

α-dystroglycan

E

envelope glycoprotein

EBOV

Ebola virus

ER

endoplasmic reticulum

G

attachment glycoprotein

GPC

viral glycoprotein precursor

GTOV

Guanarito virus

H

hemagglutinin

HIV-1

human immune deficiency virus-1

hmGL

Human macrophage C-type lectin specific for galactose and N-acetylgalactosamine

HN

hemagglutinin-neuraminidase

HPIV

human parainfluenza virus

HR

heptad repeat motif

JEV

Japanese encephalitis virus

JUNV

Junin virus

LASV

Lassa virus

LCMV

Lymphocytic Choriomeningitis Virus

MACV

Machupo virus

MARV

Marburg virus

MMTV

mouse mammary tumour virus

MV-H

measles virus H

NA

neuraminidase

NDV

Newcastle disease virus

PDB

protein data bank

PIV

parainfluenza virus

prM

precursor membrane protein

SABV

Sabia virus

SLAM

signalling lymphocyte activation molecule

SSP

stable sequence peptide

SV5

simian parainfluenza type-5

TBEV

tick-borne encephalitis virus

TfR1

human transferrin receptor 1

WNV

West Nile virus

Notes

Acknowledgements

We gratefully acknowledge D.I. Stuart, E.Y. Jones, J. Grimes, A.R. Aricescu, and M. Crispin at the Division of Structural Biology, Oxford, for their support and many helpful discussions. T.A.B. is funded as a Sir Henry Wellcome Postdoctoral Fellow by the Wellcome Trust. E.E.F. is funded by the Medical Research Council, UK.

References

  1. 1.
    Taub DD et al (2008) Immunity from smallpox vaccine persists for decades: a longitudinal study. Am J Med 121:1058–1064PubMedGoogle Scholar
  2. 2.
    Jefferson T, Jones M, Doshi P, Del Mar C (2009) Neuraminidase inhibitors for preventing and treating influenza in healthy adults: systematic review and meta-analysis. BMJ 339:b5106PubMedGoogle Scholar
  3. 3.
    Bamford DH, Grimes JM, Stuart DI (2005) What does structure tell us about virus evolution? Curr Opin Struct Biol 15:655–663PubMedGoogle Scholar
  4. 4.
    Moss B (2006) Poxvirus entry and membrane fusion. Virology 344:48–54PubMedGoogle Scholar
  5. 5.
    Daniels R, Kurowski B, Johnson AE, Hebert DN (2003) N-linked Glycans direct the cotranslational folding pathway of influenza hemagglutinin. Mol Cell 11:79–90PubMedGoogle Scholar
  6. 6.
    Amonsen M, Smith DF, Cummings RD, Air GM (2007) Human parainfluenza viruses hPIV1 and hPIV3 bind oligosaccharides with alpha2-3-linked sialic acids that are distinct from those bound by H5 avian influenza virus hemagglutinin. J Virol 81:8341–8345PubMedGoogle Scholar
  7. 7.
    Kadlec J, Loureiro S, Abrescia NG, Stuart DI, Jones IM (2008) The postfusion structure of baculovirus gp64 supports a unified view of viral fusion machines. Nat Struct Mol Biol 15:1024–30PubMedGoogle Scholar
  8. 8.
    Monroe SS, Carter MJ, Hermann JE, Kurtz JB, Matsui SM (2005) Virus taxonomy. Elsevier Academic Press, LondonGoogle Scholar
  9. 9.
    Eaton BT, Broder CC, Middleton D, Wang LF (2006) Hendra and Nipah viruses: different and dangerous. Nat Rev Microbiol 4:23–35PubMedGoogle Scholar
  10. 10.
    Gleeson PA, Feeney J, Hughes RC (1985) Structures of N-glycans of a ricin-resistant mutant of baby hamster kidney cells. Synthesis of high-mannose and hybrid N-glycans. Biochemistry 24:493–503PubMedGoogle Scholar
  11. 11.
    Tatsuo H, Ono N, Tanaka K, Yanagi Y (2000) SLAM (CDw150) is a cellular receptor for measles virus. Nature 406:893–897PubMedGoogle Scholar
  12. 12.
    Tatsuo H, Ono N, Yanagi Y (2001) Morbilliviruses use signaling lymphocyte activation molecules (CD150) as cellular receptors. J Virol 75:5842–5850PubMedGoogle Scholar
  13. 13.
    Dorig RE, Marcil A, Chopra A, Richardson CD (1993) The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 75:295–305PubMedGoogle Scholar
  14. 14.
    Naniche D, Varior-Krishnan G, Cervoni F, Wild TF, Rossi B, Rabourdin-Combe C, Gerlier D (1993) Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J Virol 67:6025–6032PubMedGoogle Scholar
  15. 15.
    Bonaparte MI et al (2005) Ephrin-B2 ligand is a functional receptor for Hendra virus and Nipah virus. Proc Natl Acad Sci USA 102:10652–10657PubMedGoogle Scholar
  16. 16.
    Negrete OA, Levroney EL, Aguilar HC, Bertolotti-Ciarlet A, Nazarian R, Tajyar S, Lee B (2005) EphrinB2 is the entry receptor for Nipah virus, an emergent deadly paramyxovirus. Nature 436:401–405PubMedGoogle Scholar
  17. 17.
    Negrete OA et al (2006) Two key residues in EphrinB3 are critical for its use as an alternative receptor for nipah virus. PLos Pathog 2:e7PubMedGoogle Scholar
  18. 18.
    Bossart KN et al (2005) Receptor binding, fusion inhibition, and induction of cross-reactive neutralizing antibodies by a soluble G glycoprotein of Hendra virus. J Virol 79:6690–6702PubMedGoogle Scholar
  19. 19.
    Bowden TA, Aricescu AR, Gilbert RJ, Grimes JM, Jones EY, Stuart DI (2008) Structural basis of Nipah and Hendra virus attachment to their cell-surface receptor ephrin-B2. Nat Struct Mol Biol 15:567–572PubMedGoogle Scholar
  20. 20.
    Crennell S, Takimoto T, Portner A, Taylor G (2000) Crystal structure of the multifunctional paramyxovirus hemagglutinin-neuraminidase. Nat Struct Biol 7:1068–74PubMedGoogle Scholar
  21. 21.
    Lawrence MC, Borg NA, Streltsov VA, Pilling PA, Epa VC, Varghese JN, McKimm-Breschkin JL, Colman PM (2004) Structure of the haemagglutinin-neuraminidase from human parainfluenza virus type III. J Mol Biol 335:1343–1357PubMedGoogle Scholar
  22. 22.
    Yuan P, Thompson TB, Wurzburg BA, Paterson RG, Lamb RA, Jardetzky TS (2005) Structural studies of the parainfluenza virus 5 hemagglutinin-neuraminidase tetramer in complex with its receptor, sialyllactose. Structure 13:803–815PubMedGoogle Scholar
  23. 23.
    Zaitsev V, von Itzstein M, Groves D, Kiefel M, Takimoto T, Portner A, Taylor G (2004) Second sialic acid binding site in Newcastle disease virus hemagglutinin-neuraminidase: implications for fusion. J Virol 78:3733–3741PubMedGoogle Scholar
  24. 24.
    Santiago C, Celma ML, Stehle T, Casasnovas JM (2010) Structure of the measles virus hemagglutinin bound to the CD46 receptor. Nat Struct Mol Biol 17:124–129PubMedGoogle Scholar
  25. 25.
    Bowden TA, Crispin M, Harvey DJ, Aricescu AR, Grimes JM, Jones EY, Stuart DI (2008) Crystal structure and carbohydrate analysis of Nipah virus attachment glycoprotein: a template for antiviral and vaccine design. J Virol 82:11628–11636PubMedGoogle Scholar
  26. 26.
    Lee JE, Fusco ML, Hessell AJ, Oswald WB, Burton DR, Saphire EO (2008) Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Nature 454:177–82PubMedGoogle Scholar
  27. 27.
    Chan DC, Fass D, Berger JM, Kim PS (1997) Core structure of gp41 from the HIV envelope glycoprotein. Cell 89:263–273PubMedGoogle Scholar
  28. 28.
    Eschli B, Quirin K, Wepf A, Weber J, Zinkernagel R, Hengartner H (2006) Identification of an N-terminal trimeric coiled-coil core within arenavirus glycoprotein 2 permits assignment to class I viral fusion proteins. J Virol 80:5897–5907PubMedGoogle Scholar
  29. 29.
    Rojek JM, Kunz S (2008) Cell entry by human pathogenic arenaviruses. Cell Microbiol 10:828–835PubMedGoogle Scholar
  30. 30.
    Lamb RA, Jardetzky TS (2007) Structural basis of viral invasion: lessons from paramyxovirus F. Curr Opin Struct Biol 17:427–436PubMedGoogle Scholar
  31. 31.
    Colman PM, Lawrence MC (2003) The structural biology of type 1 viral membrane fusion. Nat Rev Mol Cell Biol 4:309–319PubMedGoogle Scholar
  32. 32.
    Geisbert TW, Jahrling PB (2004) Exotic emerging viral diseases: progress and challenges. Nat Med 10:S110–S121PubMedGoogle Scholar
  33. 33.
    Childs JE, Peters CJ (1993) Ecology and epidemiology of arenaviruses and their hosts. Plenum Press, New YorkGoogle Scholar
  34. 34.
    Charrel RN, de Lamballerie X, Emonet S (2008) Phylogeny of the genus Arenavirus. Curr Opin Microbiol 11:362–368PubMedGoogle Scholar
  35. 35.
    Cajimat MN, Milazzo ML, Bradley RD, Fulhorst CF (2007) Catarina virus, an arenaviral species principally associated with Neotoma micropus (southern plains woodrat) in Texas. Am J Trop Med Hyg 77:732–736PubMedGoogle Scholar
  36. 36.
    Palacios G et al (2008) A new arenavirus in a cluster of fatal transplant-associated diseases. N Engl J Med 358:991–998PubMedGoogle Scholar
  37. 37.
    Perez M, Craven RC, de la Torre JC (2003) The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc Natl Acad Sci USA 100:12978–12983PubMedGoogle Scholar
  38. 38.
    Buchmeier MJ, de la Torre JC, Peters CJ (2007) Arenaviridae: the viruses and their replication. Lippincott-Raven, Philadelphia, PAGoogle Scholar
  39. 39.
    Rojek JM, Lee AM, Nguyen N, Spiropoulou CF, Kunz S (2008) Site 1 protease is required for proteolytic processing of the glycoproteins of the South American hemorrhagic fever viruses Junin, Machupo, and Guanarito. J Virol 82:6045–6051PubMedGoogle Scholar
  40. 40.
    Rojek JM, Sanchez AB, Nguyen NT, de la Torre JC, Kunz S (2008) Different mechanisms of cell entry by human-pathogenic old world and new world arenaviruses. J Virol 82:7677–7687PubMedGoogle Scholar
  41. 41.
    Cao W et al (1998) Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 282:2079–2081PubMedGoogle Scholar
  42. 42.
    Bozzi M, Morlacchi S, Bigotti MG, Sciandra F, Brancaccio A (2009) Functional diversity of dystroglycan. Matrix Biol 28:179–187PubMedGoogle Scholar
  43. 43.
    Flanagan ML, Oldenburg J, Reignier T, Holt N, Hamilton GA, Martin VK, Cannon PM (2008) New world clade B arenaviruses can use transferrin receptor 1 (TfR1)-dependent and -independent entry pathways, and glycoproteins from human pathogenic strains are associated with the use of TfR1. J Virol 82:938–948PubMedGoogle Scholar
  44. 44.
    Radoshitzky SR et al (2007) Transferrin receptor 1 is a cellular receptor for New World haemorrhagic fever arenaviruses. Nature 446:92–96PubMedGoogle Scholar
  45. 45.
    Kunz S, Sevilla N, McGavern DB, Campbell KP, Oldstone MB (2001) Molecular analysis of the interaction of LCMV with its cellular receptor [alpha]-dystroglycan. J Cell Biol 155:301–310PubMedGoogle Scholar
  46. 46.
    Radoshitzky SR et al (2008) Receptor determinants of zoonotic transmission of New World hemorrhagic fever arenaviruses. Proc Natl Acad Sci USA 105:2664–2669PubMedGoogle Scholar
  47. 47.
    Wang E, Albritton L, Ross SR (2006) Identification of the segments of the mouse transferrin receptor 1 required for mouse mammary tumor virus infection. J Biol Chem 281:10243–10249PubMedGoogle Scholar
  48. 48.
    Palermo LM, Hueffer K, Parrish CR (2003) Residues in the apical domain of the feline and canine transferrin receptors control host-specific binding and cell infection of canine and feline parvoviruses. J Virol 77:8915–8923PubMedGoogle Scholar
  49. 49.
    Cheng Y, Zak O, Aisen P, Harrison SC, Walz T (2004) Structure of the human transferrin receptor-transferrin complex. Cell 116:565–576PubMedGoogle Scholar
  50. 50.
    Bowden TA, Crispin M, Graham SC, Harvey DJ, Grimes JM, Jones EY, Stuart DI (2009) Unusual molecular architecture of the machupo virus attachment glycoprotein. J Virol 83:8259–8265PubMedGoogle Scholar
  51. 51.
    Abraham J et al (2009) Host-species transferrin receptor 1 orthologs are cellular receptors for nonpathogenic new world clade B arenaviruses. PLoS Pathog 5:e1000358PubMedGoogle Scholar
  52. 52.
    Mackenzie JS, Gubler DJ, Petersen LR (2004) Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat Med 10:S98–S109PubMedGoogle Scholar
  53. 53.
    Thiel H-J, Collett MS, Could EA, Heinz FX, Houghton M, Meyers G, Purcell RH, Riche CM (2005) Flaviviridae. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) Virus taxonomy. Elsevier Academic Press, LondonGoogle Scholar
  54. 54.
    Li L, Lok SM, Yu IM, Zhang Y, Kuhn RJ, Chen J, Rossmann MG (2008) The flavivirus precursor membrane-envelope protein complex: structure and maturation. Science 319:1830–1834PubMedGoogle Scholar
  55. 55.
    Elshuber S, Allison SL, Heinz FX, Mandl CW (2003) Cleavage of protein prM is necessary for infection of BHK-21 cells by tick-borne encephalitis virus. J Gen Virol 84:183–191PubMedGoogle Scholar
  56. 56.
    Lee E, Hall RA, Lobigs M (2004) Common E protein determinants for attenuation of glycosaminoglycan-binding variants of Japanese encephalitis and West Nile viruses. J Virol 78:8271–8280PubMedGoogle Scholar
  57. 57.
    Chu JJ, Ng ML (2004) Interaction of West Nile virus with alpha v beta 3 integrin mediates virus entry into cells. J Biol Chem 279:54533–54541PubMedGoogle Scholar
  58. 58.
    Lee JW, Chu JJ, Ng ML (2006) Quantifying the specific binding between West Nile virus envelope domain III protein and the cellular receptor alphaVbeta3 integrin. J Biol Chem 281:1352–1360PubMedGoogle Scholar
  59. 59.
    Tassaneetrithep B et al (2003) DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med 197:823–829PubMedGoogle Scholar
  60. 60.
    Davis CW, Nguyen HY, Hanna SL, Sanchez MD, Doms RW, Pierson TC (2006) West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection. J Virol 80:1290–1301PubMedGoogle Scholar
  61. 61.
    Miller JL, de Wet BJ, Martinez-Pomares L, Radcliffe CM, Dwek RA, Rudd PM, Gordon S (2008) The mannose receptor mediates dengue virus infection of macrophages. PLoS Pathog 4:e17PubMedGoogle Scholar
  62. 62.
    Pokidysheva E et al (2006) Cryo-EM reconstruction of dengue virus in complex with the carbohydrate recognition domain of DC-SIGN. Cell 124:485–493PubMedGoogle Scholar
  63. 63.
    Kanai R et al (2006) Crystal structure of west nile virus envelope glycoprotein reveals viral surface epitopes. J Virol 80:11000–11008PubMedGoogle Scholar
  64. 64.
    Li L, Lok SM, Yu IM, Zhang Y, Kuhn RJ, Chen J, Rossmann MG (2008) The flavivirus precursor membrane-envelope protein complex: structure and maturation. Science 319:1830–4PubMedGoogle Scholar
  65. 65.
    Modis Y, Ogata S, Clements D, Harrison SC (2003) A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc Natl Acad Sci USA 100:6986–6991PubMedGoogle Scholar
  66. 66.
    Nybakken GE, Nelson CA, Chen BR, Diamond MS, Fremont DH (2006) Crystal structure of the West Nile virus envelope glycoprotein. J Virol 80:11467–11474PubMedGoogle Scholar
  67. 67.
    Rey FA, Heinz FX, Mandl C, Kunz C, Harrison SC (1995) The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature 375:291–298PubMedGoogle Scholar
  68. 68.
    Zhang Y, Zhang W, Ogata S, Clements D, Strauss JH, Baker TS, Kuhn RJ, Rossmann MG (2004) Conformational changes of the flavivirus E glycoprotein. Structure 12:1607–1618PubMedGoogle Scholar
  69. 69.
    Kielian M (2006) Class II virus membrane fusion proteins. Virology 344:38–47PubMedGoogle Scholar
  70. 70.
    Lescar J, Roussel A, Wien MW, Navaza J, Fuller SD, Wengler G, Rey FA (2001) The Fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 105:137–148PubMedGoogle Scholar
  71. 71.
    Kuhn RJ et al (2002) Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108:717–725PubMedGoogle Scholar
  72. 72.
    Mukhopadhyay S, Kuhn RJ, Rossmann MG (2005) A structural perspective of the flavivirus life cycle. Nat Rev Microbiol 3:13–22PubMedGoogle Scholar
  73. 73.
    Allison SL, Schalich J, Stiasny K, Mandl CW, Kunz C, Heinz FX (1995) Oligomeric rearrangement of tick-borne encephalitis virus envelope proteins induced by an acidic pH. J Virol 69:695–700PubMedGoogle Scholar
  74. 74.
    Modis Y, Ogata S, Clements D, Harrison SC (2004) Structure of the dengue virus envelope protein after membrane fusion. Nature 427:313–319PubMedGoogle Scholar
  75. 75.
    Stiasny K, Allison SL, Schalich J, Heinz FX (2002) Membrane interactions of the tick-borne encephalitis virus fusion protein E at low pH. J Virol 76:3784–90PubMedGoogle Scholar
  76. 76.
    Bressanelli S, Stiasny K, Allison SL, Stura EA, Duquerroy S, Lescar J, Heinz FX, Rey FA (2004) Structure of a flavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformation. EMBO J 23:728–738PubMedGoogle Scholar
  77. 77.
    Gibbons DL, Vaney MC, Roussel A, Vigouroux A, Reilly B, Lepault J, Kielian M, Rey FA (2004) Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 427:320–325PubMedGoogle Scholar
  78. 78.
    Ascenzi P, Bocedi A, Heptonstall J, Capobianchi MR, Di Caro A, Mastrangelo E, Bolognesi M, Ippolito G (2008) Ebolavirus and Marburgvirus: insight the Filoviridae family. Mol Aspects Med 29:151–185PubMedGoogle Scholar
  79. 79.
    Dolnik O et al (2004) Ectodomain shedding of the glycoprotein GP of Ebola virus. EMBO J 23:2175–2184PubMedGoogle Scholar
  80. 80.
    Falzarano D, Krokhin O, Wahl-Jensen V, Seebach J, Wolf K, Schnittler HJ, Feldmann H (2006) Structure-function analysis of the soluble glycoprotein, sGP, of Ebola virus. Chembiochem 7:1605–1611PubMedGoogle Scholar
  81. 81.
    Volchkov VE, Feldmann H, Volchkova VA, Klenk HD (1998) Processing of the Ebola virus glycoprotein by the proprotein convertase furin. Proc Natl Acad Sci USA 95:5762–5677PubMedGoogle Scholar
  82. 82.
    Alvarez CP, Lasala F, Carrillo J, Muniz O, Corbi AL, Delgado R (2002) C-type lectins DC-SIGN and L-SIGN mediate cellular entry by Ebola virus in cis and in trans. J Virol 76:6841–6844PubMedGoogle Scholar
  83. 83.
    Takada A et al (2004) Human macrophage C-type lectin specific for galactose and N-acetylgalactosamine promotes filovirus entry. J Virol 78:2943–2947PubMedGoogle Scholar
  84. 84.
    Schornberg KL, Shoemaker CJ, Dube D, Abshire MY, Delos SE, Bouton AH, White JM (2009) Alpha5beta1-integrin controls ebolavirus entry by regulating endosomal cathepsins. Proc Natl Acad Sci USA 106:8003–8008PubMedGoogle Scholar
  85. 85.
    Takada A, Watanabe S, Ito H, Okazaki K, Kida H, Kawaoka Y (2000) Downregulation of beta1 integrins by Ebola virus glycoprotein: implication for virus entry. Virology 278:20–26PubMedGoogle Scholar
  86. 86.
    Chan SY, Empig CJ, Welte FJ, Speck RF, Schmaljohn A, Kreisberg JF, Goldsmith MA (2001) Folate receptor-alpha is a cofactor for cellular entry by Marburg and Ebola viruses. Cell 106:117–126PubMedGoogle Scholar
  87. 87.
    Dolnik O, Kolesnikova L, Becker S (2008) Filoviruses: Interactions with the host cell. Cell Mol Life Sci 65:756–776PubMedGoogle Scholar
  88. 88.
    Chandran K, Sullivan NJ, Felbor U, Whelan SP, Cunningham JM (2005) Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 308:1643–5PubMedGoogle Scholar
  89. 89.
    Kaletsky RL, Simmons G, Bates P (2007) Proteolysis of the Ebola virus glycoproteins enhances virus binding and infectivity. J Virol 81:13378–13384PubMedGoogle Scholar
  90. 90.
    Schornberg K, Matsuyama S, Kabsch K, Delos S, Bouton A, White J (2006) Role of endosomal cathepsins in entry mediated by the Ebola virus glycoprotein. J Virol 80:4174–4178PubMedGoogle Scholar
  91. 91.
    Lee JE, Fusco ML, Hessell AJ, Oswald WB, Burton DR, Saphire EO (2008) Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Nature 454:177–182PubMedGoogle Scholar
  92. 92.
    Ito H, Watanabe S, Sanchez A, Whitt MA, Kawaoka Y (1999) Mutational analysis of the putative fusion domain of Ebola virus glycoprotein. J Virol 73:8907–8912PubMedGoogle Scholar
  93. 93.
    Malashkevich VN, Schneider BJ, McNally ML, Milhollen MA, Pang JX, Kim PS (1999) Core structure of the envelope glycoprotein GP2 from Ebola virus at 1.9-A resolution. Proc Natl Acad Sci USA 96:2662–2667PubMedGoogle Scholar
  94. 94.
    Weissenhorn W, Carfi A, Lee KH, Skehel JJ, Wiley DC (1998) Crystal structure of the Ebola virus membrane fusion subunit, GP2, from the envelope glycoprotein ectodomain. Mol Cell 2:605–616PubMedGoogle Scholar
  95. 95.
    Skehel JJ, Wiley DC (2000) A comprehensive review of the known properties of the influenza virus haemagglutinin and the structural basis of these properties. Ann Rev Biochem 69:531–569PubMedGoogle Scholar
  96. 96.
    Tsuchiya E, Sugawara K, Hongo S, Matsuzaki Y, Muraki Y, Li Z-N, Nakamura K (2002) Effect of addition of new oligosaccharide chains to the globularhead of influenza A/H2N2 virus haemagglutinin on the intracellular transport and biological activities of the molecule. J Gen Virol 83:1137–1146PubMedGoogle Scholar
  97. 97.
    Wei X, Decker JM, Wang S, Huxiong H, Kappes JC, Wu X, Salazar-Gonzalez JF, Salazar MG (2003) Antibody neutralization and escape by HIV-1. Nature 422:307–312PubMedGoogle Scholar
  98. 98.
    Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (2005) Virus Taxonomy:VIIIth Report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, LondonGoogle Scholar
  99. 99.
    Sagar M, Wu X, Lee S, Overbaugh J (2006) HIV-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 80:9586–9598PubMedGoogle Scholar
  100. 100.
    Kwong PD, Wilson IA (2009) HIV-1 and influenza antibodies: seeing antigens in new ways. Nat Immunol 10:573–578PubMedGoogle Scholar
  101. 101.
    Calarese DA et al (2005) Dissection of the carbohydrate specificity of the broadly neutralizaing anti-HIV-1 antibody 2G12. PNAS 102:13372–13377PubMedGoogle Scholar
  102. 102.
    Santiago C, Celma ML, Stehle T, Casasnovas JM (2009) Structure of the measles virus hemagglutinin bound to the CD46 receptor. Nature Struct Mol Biol 17:124–129Google Scholar

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© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.The Division of Structural BiologyThe Wellcome Trust Centre for Human Genetics, University of Oxford, Roosevelt DriveOxfordUK

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