Cells under siege: Viral glycoprotein interactions at the cell surface

Journal of Structural Biology

Volumn 175, Issue 2, 2011, Pages 120-126

  Bowden, Thomas A ^a   Jones, E Yvonne ^a   Stuart, David I ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b DIAMOND LIGHT SOURCE LTD   (United Kingdom)

Author keywords

Cell signaling; Cell surface receptors; Glycoprotein structure; Virus entry; X ray crystallography

Indexed keywords

EPHRIN B2; EPHRIN B3; GLYCOPROTEIN; GLYCOPROTEIN A39R; GUANOSINE TRIPHOSPHATASE; HEV G GLYCOPROTEIN; IMMUNOGLOBULIN; INTEGRIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MEMBRANE COFACTOR PROTEIN; NIV G GLYCOPROTEIN; PLEXIN; RHO FACTOR; SEMAPHORIN; SINGLE STRANDED DNA; THROMBOSPONDIN; TRANSFERRIN RECEPTOR 2; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS GLYCOPROTEIN;

ARENAVIRUS; BINDING SITE; CELL SURFACE; CRYSTAL STRUCTURE; GENETIC VARIABILITY; GENOME; HEALTH HAZARD; HENDRA VIRUS; HENIPAVIRUS; HOST CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HYDROPHOBICITY; IMMUNE SYSTEM; IMMUNOREGULATION; MEASLES VIRUS; NATURAL HOST; NIPAH VIRUS; NONHUMAN; PARAMYXOVIRUS; PDZ DOMAIN; PH; POXVIRUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING; REVIEW; RNA VIRUS; SIGNAL TRANSDUCTION; STRUCTURAL PROTEOMICS; VACCINIA VIRUS; VIRULENCE; VIRUS ATTACHMENT; VIRUS ENVELOPE; VIRUS GENE; VIRUS REPLICATION; VIRUS TRANSMISSION;

ANIMALS; CELL MEMBRANE; GLYCOPROTEINS; HENIPAVIRUS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOLOGIC FACTORS; PROTEIN CONFORMATION; RECEPTORS, TRANSFERRIN; SEMAPHORINS; VIRAL PROTEINS; VIRUS INTERNALIZATION;

ARENAVIRUS; PARAMYXOVIRIDAE; POXVIRIDAE;

EID: 79959923466     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2011.03.016     Document Type: Review

References (75)

1. Abraham J., Corbett K.D., Farzan M., Choe H., Harrison S.C. Structural basis for receptor recognition by New World hemorrhagic fever arenaviruses. Nat. Struct. Mol. Biol. 2010, 17:438-444.
2. Aguilar H.C., Ataman Z.A., Aspericueta V., Fang A.Q., Stroud M., Negrete O.A., Kammerer R.A., Lee B. A novel receptor-induced activation site in the Nipah virus attachment glycoprotein (G) involved in triggering the fusion glycoprotein (F). J. Biol. Chem. 2009, 284:1628-1635.
3. Antipenko A., Himanen J.P., van Leyen K., Nardi-Dei V., Lesniak J., Barton W.A., Rajashankar K.R., Lu M., Hoemme C., Puschel A.W., Nikolov D.B. Structure of the semaphorin-3A receptor binding module. Neuron 2003, 39:589-598.
4. Aricescu A.R., Lu W., Jones E.Y. A time- and cost-efficient system for high-level protein production in mammalian cells. Acta Crystallogr. D Biol. Crystallogr. 2006, 62:1243-1250.
5. Avota E., Gassert E., Schneider-Schaulies S. Measles virus-induced immunosuppression: from effectors to mechanisms. Med. Microbiol. Immunol. 2010, 199:227-237.
6. Bahar M.W., Graham S.C., Chen R., Cooray S., Smith G.L., Stuart D.I., Grimes J.M. How vaccinia virus has evolved to subvert the host immune response. J. Struct. Biol. 2011, 175:127-134.
7. Bennett M.J., Lebron J.A., Bjorkman P.J. Crystal structure of the hereditary haemochromatosis protein HFE complexed with transferrin receptor. Nature 2000, 403:46-53.
8. Bomford A. Genetics of haemochromatosis. Lancet 2002, 360:1673-1681.
9. Bonaparte M.I., Dimitrov A.S., Bossart K.N., Crameri G., Mungall B.A., Bishop K.A., Choudhry V., Dimitrov D.S., Wang L.F., Eaton B.T., Broder C.C. Ephrin-B2 ligand is a functional receptor for Hendra virus and Nipah virus. Proc. Natl. Acad. Sci. USA 2005, 102:10652-10657.
10. Bork P., Doerks T., Springer T.A., Snel B. Domains in plexins: links to integrins and transcription factors. Trends Biochem. Sci. 1999, 24:261-263.
11. Bossart K.N., Tachedjian M., McEachern J.A., Crameri G., Zhu Z., Dimitrov D.S., Broder C.C., Wang L.F. Functional studies of host-specific ephrin-B ligands as Henipavirus receptors. Virology 2008, 372:357-371.
12. Bowden T.A., Crispin M., Jones E.Y., Stuart D.I. Shared paramyxoviral glycoprotein architecture is adapted for diverse attachment strategies. Biochem. Soc. Trans. 2010, 38:1349-1355.
13. Bowden T.A., Crispin M., Harvey D.J., Jones E.Y., Stuart D.I. Dimeric architecture of the Hendra virus attachment glycoprotein: evidence for a conserved mode of assembly. J. Virol. 2010, 84:6208-6217.
14. Bowden T.A., Aricescu A.R., Gilbert R.J., Grimes J.M., Jones E.Y., Stuart D.I. Structural basis of Nipah and Hendra virus attachment to their cell-surface receptor ephrin-B2. Nat. Struct. Mol. Biol. 2008, 15:567-572.
15. Bowden T.A., Crispin M., Harvey D.J., Aricescu A.R., Grimes J.M., Jones E.Y., Stuart D.I. Crystal structure and carbohydrate analysis of Nipah virus attachment glycoprotein: a template for antiviral and vaccine design. J. Virol. 2008, 82:11628-11636.
16. Bowden T.A., Crispin M., Graham S.C., Harvey D.J., Grimes J.M., Jones E.Y., Stuart D.I. Unusual molecular architecture of the machupo virus attachment glycoprotein. J. Virol. 2009, 83:8259-8265.
17. Bowden T.A., Aricescu A.R., Nettleship J.E., Siebold C., Rahman-Huq N., Owens R.J., Stuart D.I., Jones E.Y. Structural plasticity of eph receptor A4 facilitates cross-class ephrin signaling. Structure 2009, 17:1386-1397.
18. Chang V.T., Crispin M., Aricescu A.R., Harvey D.J., Nettleship J.E., Fennelly J.A., Yu C., Boles K.S., Evans E.J., Stuart D.I., Dwek R.A., Jones E.Y., Owens R.J., Davis S.J. Glycoprotein structural genomics: solving the glycosylation problem. Structure 2007, 15:267-273.
19. Cheng Y., Zak O., Aisen P., Harrison S.C., Walz T. Structure of the human transferrin receptor-transferrin complex. Cell 2004, 116:565-576.
20. Chrencik J.E., Brooun A., Kraus M.L., Recht M.I., Kolatkar A.R., Han G.W., Seifert J.M., Widmer H., Auer M., Kuhn P. Structural and biophysical characterization of the EphB4-ephrinB2 protein-protein interaction and receptor specificity. J. Biol. Chem. 2006, 281:28185-28192.
21. Chrencik J.E., Brooun A., Recht M.I., Kraus M.L., Koolpe M., Kolatkar A.R., Bruce R.H., Martiny-Baron G., Widmer H., Pasquale E.B., Kuhn P. Structure and thermodynamic characterization of the EphB4-Ephrin-B2 antagonist peptide complex reveals the determinants for receptor specificity. Structure 2006, 14:321-330.
22. Cianciolo G.J., Copeland T.D., Oroszlan S., Snyderman R. Inhibition of lymphocyte proliferation by a synthetic peptide homologous to retroviral envelope proteins. Science 1985, 230:453-455.
23. Comeau M.R., Johnson R., DuBose R.F., Petersen M., Gearing P., VandenBos T., Park L., Farrah T., Buller R.M., Cohen J.I., Strockbine L.D., Rauch C., Spriggs M.K. A poxvirus-encoded semaphorin induces cytokine production from monocytes and binds to a novel cellular semaphorin receptor, VESPR. Immunity 1998, 8:473-482.
24. Eaton B.T., Broder C.C., Middleton D., Wang L.F. Hendra and Nipah viruses: different and dangerous. Nat. Rev. Microbiol. 2006, 4:23-35.
25. Edwards R.A., Rohwer F. Viral metagenomics. Nat. Rev. Microbiol. 2005, 3:504-510.
26. Ensser A., Fleckenstein B. Alcelaphine herpesvirus type 1 has a semaphorin-like gene. J. Gen. Virol. 1995, 76(Pt 4):1063-1067.
27. Eschli B., Quirin K., Wepf A., Weber J., Zinkernagel R., Hengartner H. Identification of an N-terminal trimeric coiled-coil core within arenavirus glycoprotein 2 permits assignment to class I viral fusion proteins. J. Virol. 2006, 80:5897-5907.
28. Goodman L.B., Lyi S.M., Johnson N.C., Cifuente J.O., Hafenstein S.L., Parrish C.R. Binding site on the transferrin receptor for the parvovirus capsid and effects of altered affinity on cell uptake and infection. J. Virol. 2010, 84:4969-4978.
29. Hafenstein S., Palermo L.M., Kostyuchenko V.A., Xiao C., Morais M.C., Nelson C.D., Bowman V.D., Battisti A.J., Chipman P.R., Parrish C.R., Rossmann M.G. Asymmetric binding of transferrin receptor to parvovirus capsids. Proc. Natl. Acad. Sci. USA 2007, 104:6585-6589.
30. Hafner C., Schmitz G., Meyer S., Bataille F., Hau P., Langmann T., Dietmaier W., Landthaler M., Vogt T. Differential gene expression of Eph receptors and ephrins in benign human tissues and cancers. Clin. Chem. 2004, 50:490-499.
31. Hashiguchi T., Ose T., Kubota M., Maita N., Kamishikiryo J., Maenaka K., Yanagi Y. Structure of the measles virus hemagglutinin bound to its cellular receptor SLAM. Nat. Struct. Mol. Biol. 2011, 18:135-141.
32. Himanen J.P., Rajashankar K.R., Lackmann M., Cowan C.A., Henkemeyer M., Nikolov D.B. Crystal structure of an Eph receptor-ephrin complex. Nature 2001, 414:933-938.
33. Himanen J.P., Goldgur Y., Miao H., Myshkin E., Guo H., Buck M., Nguyen M., Rajashankar K.R., Wang B., Nikolov D.B. Ligand recognition by A-class Eph receptors: crystal structures of the EphA2 ligand-binding domain and the EphA2/ephrin-A1 complex. EMBO Rep. 2009, 10:722-728.
34. Himanen J.P., Yermekbayeva L., Janes P.W., Walker J.R., Xu K., Atapattu L., Rajashankar K.R., Mensinga A., Lackmann M., Nikolov D.B., Dhe-Paganon S. Architecture of Eph receptor clusters. Proc. Natl. Acad. Sci. USA 2010, 107:10860-10865.
35. Himanen J.P., Chumley M.J., Lackmann M., Li C., Barton W.A., Jeffrey P.D., Vearing C., Geleick D., Feldheim D.A., Boyd A.W., Henkemeyer M., Nikolov D.B. Repelling class discrimination: ephrin-A5 binds to and activates EphB2 receptor signaling. Nat. Neurosci. 2004, 7:501-509.
36. Janssen B.J., Robinson R.A., Perez-Branguli F., Bell C.H., Mitchell K.J., Siebold C., Jones E.Y. Structural basis of semaphorin-plexin signalling. Nature 2010, 467:1118-1122.
37. Kadlec J., Loureiro S., Abrescia N.G., Stuart D.I., Jones I.M. The postfusion structure of baculovirus gp64 supports a unified view of viral fusion machines. Nat. Struct. Mol. Biol. 2008, 15:1024-1030.
38. Kleinerman E.S., Lachman L.B., Knowles R.D., Snyderman R., Cianciolo G.J. A synthetic peptide homologous to the envelope proteins of retroviruses inhibits monocyte-mediated killing by inactivating interleukin 1. J. Immunol. 1987, 139:2329-2337.
39. Kruger R.P., Aurandt J., Guan K.L. Semaphorins command cells to move. Nat. Rev. Mol. Cell Biol. 2005, 6:789-800.
40. Kwong P.D., Wyatt R., Robinson J., Sweet R.W., Sodroski J., Hendrickson W.A. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 1998, 393:648-659.
41. Lamb R.A., Jardetzky T.S. Structural basis of viral invasion: lessons from paramyxovirus F. Curr. Opin. Struct. Biol. 2007, 17:427-436.
42. Lawrence C.M., Ray S., Babyonyshev M., Galluser R., Borhani D.W., Harrison S.C. Crystal structure of the ectodomain of human transferrin receptor. Science 1999, 286:779-782.
43. Lebron J.A., West A.P., Bjorkman P.J. The hemochromatosis protein HFE competes with transferrin for binding to the transferrin receptor. J. Mol. Biol. 1999, 294:239-245.
44. Lee J.E., Fusco M.L., Hessell A.J., Oswald W.B., Burton D.R., Saphire E.O. Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Nature 2008, 454:177-182.
45. Liu H., Juo Z.S., Shim A.H., Focia P.J., Chen X., Garcia K.C., He X. Structural basis of semaphorin-plexin recognition and viral mimicry from Sema7A and A39R complexes with PlexinC1. Cell 2010, 142:749-761.
46. Lou Z., Xu Y., Xiang K., Su N., Qin L., Li X., Gao G.F., Bartlam M., Rao Z. Crystal structures of Nipah and Hendra virus fusion core proteins. FEBS J. 2006, 273:4538-4547.
47. Love C.A., Harlos K., Mavaddat N., Davis S.J., Stuart D.I., Jones E.Y., Esnouf R.M. The ligand-binding face of the semaphorins revealed by the high-resolution crystal structure of SEMA4D. Nat. Struct. Biol. 2003, 10:843-848.
48. Negrete O.A., Levroney E.L., Aguilar H.C., Bertolotti-Ciarlet A., Nazarian R., Tajyar S., Lee B. EphrinB2 is the entry receptor for Nipah virus, an emergent deadly paramyxovirus. Nature 2005, 436:401-405.
49. Negrete O.A., Wolf M.C., Aguilar H.C., Enterlein S., Wang W., Muhlberger E., Su S.V., Bertolotti-Ciarlet A., Flick R., Lee B. Two key residues in EphrinB3 are critical for its use as an alternative receptor for nipah virus. PLos Pathog. 2006, 2:e7.
50. Nikolov D., Li C., Lackmann M., Jeffrey P., Himanen J. Crystal structure of the human ephrin-A5 ectodomain. Protein Sci. 2007, 16:996-1000.
51. Nikolov D.B., Li C., Barton W.A., Himanen J.P. Crystal structure of the ephrin-B1 ectodomain: implications for receptor recognition and signaling. Biochemistry 2005, 44:10947-10953.
52. Nogi T., Yasui N., Mihara E., Matsunaga Y., Noda M., Yamashita N., Toyofuku T., Uchiyama S., Goshima Y., Kumanogoh A., Takagi J. Structural basis for semaphorin signalling through the plexin receptor. Nature 2010, 467:1123-1127.
53. Palermo L.M., Hueffer K., Parrish C.R. 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. 2003, 77:8915-8923.
54. Parker J.S., Murphy W.J., Wang D., O'Brien S.J., Parrish C.R. Canine and feline parvoviruses can use human or feline transferrin receptors to bind, enter, and infect cells. J. Virol. 2001, 75:3896-3902.
55. Pasquale E.B. Eph receptor signalling casts a wide net on cell behaviour. Nat. Rev. Mol. Cell Biol. 2005, 6:462-475.
56. Ponka P., Lok C.N. The transferrin receptor: role in health and disease. Int. J. Biochem. Cell Biol. 1999, 31:1111-1137.
57. Qin H., Noberini R., Huan X., Shi J., Pasquale E.B., Song J. Structural characterization of the EphA4-Ephrin-B2 complex reveals new features enabling Eph-ephrin binding promiscuity. J. Biol. Chem. 2010, 285:644-654.
58. Radoshitzky S.R., Abraham J., Spiropoulou C.F., Kuhn J.H., Nguyen D., Li W., Nagel J., Schmidt P.J., Nunberg J.H., Andrews N.C., Farzan M., Choe H. Transferrin receptor 1 is a cellular receptor for New World haemorrhagic fever arenaviruses. Nature 2007, 446:92-96.
59. Ross S.R., Schofield J.J., Farr C.J., Bucan M. Mouse transferrin receptor 1 is the cell entry receptor for mouse mammary tumor virus. Proc. Natl. Acad. Sci. USA 2002, 99:12386-12390.
60. Santiago C., Celma M.L., Stehle T., Casasnovas J.M. Structure of the measles virus hemagglutinin bound to the CD46 receptor. Nat. Struct. Mol. Biol. 2010, 17:124-129.
61. Seiradake E., Harlos K., Sutton G., Aricescu A.R., Jones E.Y. An extracellular steric seeding mechanism for Eph-ephrin signaling platform assembly. Nat. Struct. Mol. Biol. 2010, 17:398-402.
62. Stehle T., Casasnovas J.M. Specificity switching in virus-receptor complexes. Curr. Opin. Struct. Biol. 2009, 19:181-188.
63. Suzuki K., Kumanogoh A., Kikutani H. Semaphorins and their receptors in immune cell interactions. Nat. Immunol. 2008, 9:17-23.
64. Suzuki K., Okuno T., Yamamoto M., Pasterkamp R.J., Takegahara N., Takamatsu H., Kitao T., Takagi J., Rennert P.D., Kolodkin A.L., Kumanogoh A., Kikutani H. Semaphorin 7A initiates T-cell-mediated inflammatory responses through alpha1beta1 integrin. Nature 2007, 446:680-684.
65. Toth J., Cutforth T., Gelinas A.D., Bethoney K.A., Bard J., Harrison C.J. Crystal structure of an ephrin ectodomain. Dev. Cell 2001, 1:83-92.
66. Volchkov V.E., Volchkova V.A., Muhlberger E., Kolesnikova L.V., Weik M., Dolnik O., Klenk H.D. Recovery of infectious Ebola virus from complementary DNA: RNA editing of the GP gene and viral cytotoxicity. Science 2001, 291:1965-1969.
67. Wang E., Albritton L., Ross S.R. Identification of the segments of the mouse transferrin receptor 1 required for mouse mammary tumor virus infection. J. Biol. Chem. 2006, 281:10243-10249.
68. Wang J.H., Meijers R., Xiong Y., Liu J.H., Sakihama T., Zhang R., Joachimiak A., Reinherz E.L. Crystal structure of the human CD4 N-terminal two-domain fragment complexed to a class II MHC molecule. Proc. Natl. Acad. Sci. USA 2001, 98:10799-10804.
69. Weis W., Brown J.H., Cusack S., Paulson J.C., Skehel J.J., Wiley D.C. Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature 1988, 333:426-431.
70. Wild T.F. Henipaviruses: a new family of emerging Paramyxoviruses. Pathol. Biol. (Paris) 2009, 57:188-196.
71. Wilson I.A., Skehel J.J., Wiley D.C. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 1981, 289:366-373.
72. Wyatt R., Kwong P.D., Desjardins E., Sweet R.W., Robinson J., Hendrickson W.A., Sodroski J.G. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 1998, 393:705-711.
73. Xu K., Rajashankar K.R., Chan Y.P., Himanen J.P., Broder C.C., Nikolov D.B. Host cell recognition by the henipaviruses: crystal structures of the Nipah G attachment glycoprotein and its complex with ephrin-B3. Proc. Natl. Acad. Sci. USA 2008, 105:9953-9958.
74. Yang Z.Y., Duckers H.J., Sullivan N.J., Sanchez A., Nabel E.G., Nabel G.J. Identification of the Ebola virus glycoprotein as the main viral determinant of vascular cell cytotoxicity and injury. Nat. Med.' 2000, 6:886-889.
75. Zhu P., Chertova E., Bess J., Lifson J.D., Arthur L.O., Liu J., Taylor K.A., Roux K.H. Electron tomography analysis of envelope glycoprotein trimers on HIV and simian immunodeficiency virus virions. Proc. Natl. Acad. Sci. USA 2003, 100:15812-15817.