Identification of conserved residues in hepatitis C virus envelope glycoprotein E2 that modulate virus dependence on CD81 and SRB1 entry factors

Journal of Virology

Volumn 88, Issue 18, 2014, Pages 10584-10597

  Lavie, Muriel ^a   Sarrazin, Stéphane ^b   Montserret, Roland ^b   Descamps, Véronique ^c   Baumert, Thomas F ^d   Duverlie, Gilles ^c   Séron, Karin ^a   Penin, François ^b   Dubuisson, Jean ^a  

^a UNIV LILLE   (France)

^b INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

^c AMIENS UNIVERSITY HOSPITAL   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD81 ANTIGEN; EPITOPE; GLYCOPROTEIN E2; NEUTRALIZING ANTIBODY; PROTEIN SRB1; UNCLASSIFIED DRUG; VIRUS FUSION PROTEIN; VIRUS RECEPTOR; GLYCOPROTEIN E2, HEPATITIS C VIRUS; PROTEIN BINDING; SCARB1 PROTEIN, HUMAN; SCAVENGER RECEPTOR B; VIRUS ENVELOPE PROTEIN;

AMINO ACID COMPOSITION; AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; GENE FUNCTION; GENETIC CONSERVATION; HEPATITIS C VIRUS; MEMBRANE FUSION; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; RESIDUE ANALYSIS; STRUCTURE ACTIVITY RELATION; VIRION; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS INFECTIVITY; VIRUS MUTATION; VIRUS NEUTRALIZATION; VIRUS PARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HEPACIVIRUS; HEPATITIS C; HUMAN; METABOLISM; SEQUENCE ALIGNMENT; VIROLOGY;

AMINO ACID SEQUENCE; ANTIGENS, CD81; CONSERVED SEQUENCE; HEPACIVIRUS; HEPATITIS C; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; RECEPTORS, VIRUS; SCAVENGER RECEPTORS, CLASS B; SEQUENCE ALIGNMENT; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

EID: 84906342318     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01402-14     Document Type: Article

References (55)

1. Pawlotsky JM. 2014. New hepatitis C therapies: the toolbox, strategies, and challenges. Gastroenterology 146:1176-1192. http://dx.doi.org/10 .1053/j.gastro.2014.03.003.
2. Manns MP, von Hahn T. 2013. Novel therapies for hepatitis C-one pill fits all? Nat. Rev. Drug Discov. 12:595-610. http://dx.doi.org/10.1038 /nrd4050.
3. Chung RT, Baumert TF. 2014. Curing chronic hepatitis C-the arc of a medical triumph. N. Engl. J. Med. 370:1576-1578. http://dx.doi.org/10 .1056/NEJMp1400986.
4. Simmonds P, Bukh J, Combet C, Deléage G, Enomoto N, Feinstone S, Halfon P, Inchauspé G, Kuiken C, Maertens G, Mizokami M, Murphy D, Okamoto H, Pawlotsky JM, Penin F, Sablon E, Shin IT, Stuyver LJ, Thiel H-J, Viazov S, Weiner AJ, Widell A. 2005. Consensus proposals for the unified system of nomenclature of hepatitis C virus genotypes. Hepatology 42:962-973. http://dx.doi.org/10.1002/hep.20819.
5. Krey T, d'Alayer J, Kikuti CM, Saulnier A, Damier-Piolle L, Petitpas I, Johansson DX, Tawar RG, Baron B, Robert B, England P, Persson MA, Martin A, Rey FA. 2010. The disulfide bonds in glycoprotein E2 of hepatitisCvirus reveal the tertiary organization of the molecule. PLoS Pathog. 6:e1000762. http://dx.doi.org/10.1371/journal.ppat.1000762.
6. Wang Y, Keck ZY, Foung SK. 2011. Neutralizing antibody response to hepatitis Cvirus. Viruses 3:2127-2145. http://dx.doi.org/10.3390/v3112127.
7. Kachko A, Kochneva G, Sivolobova G, Grazhdantseva A, Lupan T, Zubkova I, Wells F, Merchlinsky M, Williams O, Watanabe H, Ivanova A, Shvalov A, Loktev V, Netesov S, Major ME. 2011. New neutralizing antibody epitopes in hepatitis C virus envelope glycoproteins are revealed by dissecting peptide recognition profiles. Vaccine 30:69-77. http://dx .doi.org/10.1016/j.vaccine.2011.10.045.
8. Kong L, Giang E, Nieusma T, Kadam RU, Cogburn KE, Hua Y, Dai X, Stanfield RL, Burton DR, Ward AB, Wilson IA, Law M. 2013. Hepatitis C virus E2 envelope glycoprotein core structure. Science 342:1090-1094. http://dx.doi.org/10.1126/science.1243876.
9. Khan AG, Whidby J, Miller MT, Scarborough H, Zatorski AV, Cygan A, Price AA, Yost SA, Bohannon CD, Jacob J, Grakoui A, Marcotrigiano J. 2014. Structure of the core ectodomain of the hepatitis C virus envelope glycoprotein 2. Nature 509:381-384. http://dx.doi.org/10.1038 /nature13117.
10. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, Petracca R, Weiner AJ, Houghton M, Rosa D, Grandi G, Abrignani S. 1998. Binding of hepatitis C virus to CD81. Science 282:938-941. http://dx.doi.org/10 .1126/science.282.5390.938.
11. Scarselli E, Ansuini H, Cerino R, Roccasecca RM, Acali S, Filocamo G, Traboni C, Nicosia A, Cortese R, Vitelli A. 2002. The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J. 21:5017-5025. http://dx.doi.org/10.1093/emboj/cdf529.
12. Meredith LW, Wilson GK, Fletcher NF, McKeating JA. 2012. Hepatitis C virus entry: beyond receptors. Rev. Med. Virol. 22:182-193. http://dx .doi.org/10.1002/rmv.723.
13. Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, Wolk B, Hatziioannou T, McKeating JA, Bieniasz PD, Rice CM. 2007. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446:801-805. http://dx.doi.org/10.1038/nature05654.
14. Ploss A, Evans MJ, Gaysinskaya VA, Panis M, You H, de Jong YP, Rice CM. 2009. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457:882-886. http://dx.doi.org/10.1038 /nature07684.
15. Lupberger J, Zeisel MB, Xiao F, Thumann C, Fofana I, Zona L, Davis C, Mee CJ, Turek M, Gorke S, Royer C, Fischer B, Zahid MN, Lavillette D, Fresquet J, Cosset FL, Rothenberg SM, Pietschmann T, Patel AH, Pessaux P, Doffoel M, Raffelsberger W, Poch O, McKeating JA, Brino L, Baumert TF. 2011. EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nat. Med. 17:589-595. http://dx.doi.org/10.1038/nm.2341.
16. Sainz B, Jr, Barretto N, Martin DN, Hiraga N, Imamura M, Hussain S, Marsh KA, Yu X, Chayama K, Alrefai WA, Uprichard SL. 2012. Identification of the Niemann-Pick C1-like 1 cholesterol absorption receptor as a new hepatitis C virus entry factor. Nat. Med. 18:281-285. http://dx .doi.org/10.1038/nm.2581.
17. Martin DN, Uprichard SL. 2013. Identification of transferrin receptor 1 as a hepatitisCvirus entry factor. Proc. Natl. Acad. Sci. U. S. A. 110:10777-10782. http://dx.doi.org/10.1073/pnas.1301764110.
18. Albecka A, Monserret R, Krey T, Tarr AW, Diesis A, Ball JK, Duverlie G, Rey F, Penin F, Dubuisson J. 2011. Identification of new functional regions in hepatitis C virus envelope glycoproteins E2. J. Virol. 85:1777-1792. http://dx.doi.org/10.1128/JVI.02170-10.
19. Nakabayashi H, Taketa K, Miyano K, Yamane T, Sato J. 1982. Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res. 42:3858-3863.
20. Dubuisson J, Hsu HH, Cheung RC, Greenberg HB, Russell DG, Rice CM. 1994. Formation and intracellular localization of hepatitis C virus envelope glycoprotein complexes expressed by recombinant vaccinia and Sindbis viruses. J. Virol. 68:6147-6160.
21. Flint M, Maidens C, Loomis-Price LD, Shotton C, Dubuisson J, Monk P, Higginbottom A, Levy S, McKeating JA. 1999. Characterization of hepatitis C virus E2 glycoprotein interaction with a putative cellular receptor, CD81. J. Virol. 73:6235-6244.
22. Lindenbach BD, Evans MJ, Syder AJ, Wolk B, Tellinghuisen TL, Liu CC, Maruyama T, Hynes RO, Burton DR, McKeating JA, Rice CM. 2005. Complete replication of hepatitis C virus in cell culture. Science 309:623-626. http://dx.doi.org/10.1126/science.1114016.
23. Fofana I, Krieger SE, Grunert F, Glauben S, Xiao F, Fafi-Kremer S, Soulier E, Royer C, Thumann C, Mee CJ, McKeating JA, Dragic T, Pessaux P, Stoll-Keller F, Schuster C, Thompson J, Baumert TF. 2010. Monoclonal anti-claudin 1 antibodies prevent hepatitis C virus infection of primary human hepatocytes. Gastroenterology 139:953-964, 964 e951- e954. http://dx.doi.org/10.1053/j.gastro.2010.05.073.
24. Giang E, Dorner M, Prentoe JC, Dreux M, Evans MJ, Bukh J, Rice CM, Ploss A, Burton DR, Law M. 2012. Human broadly neutralizing antibodies to the envelope glycoprotein complex of hepatitis C virus. Proc. Natl. Acad. Sci. U. S. A. 109:6205-6210. http://dx.doi.org/10.1073/pnas .1114927109.
25. Macdonald A, Crowder K, Street A, McCormick C, Saksela K, Harris M. 2003. The hepatitis C virus non-structural NS5A protein inhibits activating protein-1 function by perturbing ras-ERK pathway signaling. J. Biol. Chem. 278:17775-17784. http://dx.doi.org/10.1074/jbc.M210900200.
26. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, Murthy K, Habermann A, Krausslich HG, Mizokami M, Bartenschlager R, Liang TJ. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11:791-796. http://dx.doi .org/10.1038/nm1268.
27. Goueslain L, Alsaleh K, Horellou P, Roingeard P, Descamps V, Duverlie G, Ciczora Y, Wychowski C, Dubuisson J, Rouille Y. 2010. Identification of GBF1 as a cellular factor required for hepatitis C virus RNA replication. J. Virol. 84:773-787. http://dx.doi.org/10.1128/JVI.01190-09.
28. Delgrange D, Pillez A, Castelain S, Cocquerel L, Rouillé Y, Dubuisson J, Wakita T, Duverlie G, Wychowski C. 2007. Robust production of infectious viral particles in Huh-7 cells by introducing mutations in hepatitis C virus structural proteins. J. Gen. Virol. 88:2495-2503. http://dx .doi.org/10.1099/vir.0.82872-0.
29. Cormack B, Castano I. 2002. Introduction of point mutations into cloned genes. Methods Enzymol. 350:199-218. http://dx.doi.org/10.1016/S0076 -6879(02)50964-2.
30. Rouille Y, Helle F, Delgrange D, Roingeard P, Voisset C, Blanchard E, Belouzard S, McKeating J, Patel AH, Maertens G, Wakita T, Wychowski C, Dubuisson J. 2006. Subcellular localization of hepatitis C virus structural proteins in a cell culture system that efficiently replicates the virus. J. Virol. 80:2832-2841. http://dx.doi.org/10.1128/JVI.80.6.2832-2841.2006.
31. Mederacke I, Wedemeyer H, Ciesek S, Steinmann E, Raupach R, Wursthorn K, Manns MP, Tillmann HL. 2009. Performance and clinical utility of a novel fully automated quantitative HCV-core antigen assay. J. Clin. Virol. 46:210-215. http://dx.doi.org/10.1016/j.jcv.2009.08.014.
32. Shen Y, Delaglio F, Cornilescu G, Bax A. 2009. TALOS+: a hybrid method for predicting protein backbone torsion angles fromNMRchemical shifts. J. Biomol. NMR 44:213-223. http://dx.doi.org/10.1007/s10858 -009-9333-z.
33. Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM. 2003. The Xplor- NIH NMR molecular structure determination package. J. Magn. Reson. 160:65-73. http://dx.doi.org/10.1016/S1090-7807(02)00014-9.
34. Petracca R, Falugi F, Galli G, Norais N, Rosa D, Campagnoli S, Burgio V, Di Stasio E, Giardina B, Houghton M, Abrignani S, Grandi G. 2000. Structure-function analysis of hepatitis C virus envelope-CD81 binding. J. Virol. 74:4824-4830. http://dx.doi.org/10.1128/JVI.74.10.4824-4830.2000.
35. Vieyres G, Thomas X, Descamps V, Duverlie G, Patel AH, Dubuisson J. 2010. Characterization of the envelope glycoproteins associated with infectious hepatitisCvirus. J. Virol. 84:10159-10168. http://dx.doi.org/10 .1128/JVI.01180-10.
36. Grove J, Nielsen S, Zhong J, Bassendine MF, Drummer HE, Balfe P, McKeating JA. 2008. Identification of a residue in hepatitis C virus E2 glycoprotein that determines scavenger receptor BI and CD81 receptor dependency and sensitivity to neutralizing antibodies. J. Virol. 82:12020-12029. http://dx.doi.org/10.1128/JVI.01569-08.
37. Law M, Maruyama T, Lewis J, Giang E, Tarr AW, Stamataki Z, Gastaminza P, Chisari FV, Jones IM, Fox RI, Ball JK, McKeating JA, Kneteman NM, Burton DR. 2008. Broadly neutralizing antibodies protect against hepatitis C virus quasispecies challenge. Nat. Med. 14:25-27. http: //dx.doi.org/10.1038/nm1698.
38. Hsu M, Zhang J, Flint M, Logvinoff C, Cheng-Mayer C, Rice CM, McKeating JA. 2003. Hepatitis C virus glycoproteins mediate pHdependent cell entry of pseudotyped retroviral particles. Proc. Natl. Acad. Sci. U. S. A. 100:7271-7276. http://dx.doi.org/10.1073/pnas.0832180100.
39. Bartenschlager R, Penin F, Lohmann V, Andre P. 2011. Assembly of infectious hepatitis C virus particles. Trends Microbiol. 19:95-103. http: //dx.doi.org/10.1016/j.tim.2010.11.005.
40. Andreo U, Maillard P, Kalinina O, Walic M, Meurs E, Martinot M, Marcellin P, Budkowska A. 2007. Lipoprotein lipase mediates hepatitis C virus (HCV) cell entry and inhibits HCV infection. Cell. Microbiol. 9:2445-2456. http://dx.doi.org/10.1111/j.1462-5822.2007.00972.x.
41. Chang KS, Jiang J, Cai Z, Luo G. 2007. Human apolipoprotein E is required for infectivity and production of hepatitis C virus in cell culture. J. Virol. 81:13783-13793. http://dx.doi.org/10.1128/JVI.01091-07.
42. Maillard P, Huby T, Andreo U, Moreau M, Chapman J, Budkowska A. 2006. The interaction of natural hepatitis C virus with human scavenger receptor SR-BI/ClaI is mediated by ApoB-containing lipoproteins. FASEB J. 20:735-737. http://dx.doi.org/10.1096/fj.05-4728fje.
43. Bankwitz D, Steinmann E, Bitzegeio J, Ciesek S, Friesland M, Herrmann E, Zeisel MB, Baumert TF, Keck ZY, Foung SK, Pecheur EI, Pietschmann T. 2010. Hepatitis C virus hypervariable region 1 modulates receptor interactions, conceals the CD81 binding site, and protects conserved neutralizing epitopes. J. Virol. 84:5751-5763. http://dx.doi.org/10 .1128/JVI.02200-09.
44. Prentoe J, Jensen TB, Meuleman P, Serre SB, Scheel TK, Leroux-Roels G, Gottwein JM, Bukh J. 2011. Hypervariable region 1 differentially impacts viability of hepatitisCvirus strains of genotypes 1 to 6 and impairs virus neutralization. J. Virol. 85:2224-2234. http://dx.doi.org/10.1128 /JVI.01594-10.
45. Perez-Berna AJ, Moreno MR, Guillen J, Bernabeu A, Villalain J. 2006. The membrane-active regions of the hepatitis C virus E1 and E2 envelope glycoproteins. Biochemistry 45:3755-3768. http://dx.doi.org/10.1021 /bi0523963.
46. Lavillette D, Pecheur EI, Donot P, Fresquet J, Molle J, Corbau R, Dreux M, Penin F, Cosset FL. 2007. Characterization of fusion determinants points to the involvement of three discrete regions of both E1 and E2 glycoproteins in the membrane fusion process of hepatitisCvirus. J. Virol. 81:8752-8765. http://dx.doi.org/10.1128/JVI.02642-06.
47. El Omari K, Iourin O, Harlos K, Grimes JM, Stuart DI. 2013. Structure of a pestivirus envelope glycoprotein e2 clarifies its role in cell entry. Cell Rep. 3:30-35. http://dx.doi.org/10.1016/j.celrep.2012.12.001.
48. Li Y, Modis Y. 2014. A novel membrane fusion protein family in Flaviviridae? Trends Microbiol. 22:176-182. http://dx.doi.org/10.1016/j.tim .2014.01.008.
49. Li Y, Wang J, Kanai R, Modis Y. 2013. Crystal structure of glycoprotein E2 from bovine viral diarrhea virus. Proc. Natl. Acad. Sci. U. S. A. 110: 6805-6810. http://dx.doi.org/10.1073/pnas.1300524110.
50. Bitzegeio J, Bankwitz D, Hueging K, Haid S, Brohm C, Zeisel MB, Herrmann E, Iken M, Ott M, Baumert TF, Pietschmann T. 2010. Adaptation of hepatitisCvirus to mouse CD81 permits infection of mouse cells in the absence of human entry factors. PLoS Pathog. 6:e1000978. http://dx.doi.org/10.1371/journal.ppat.1000978.
51. McCaffrey K, Boo I, Tewierek K, Edmunds ML, Poumbourios P, Drummer HE. 2012. Role of conserved cysteine residues in hepatitis C virus glycoprotein e2 folding and function. J. Virol. 86:3961-3974. http: //dx.doi.org/10.1128/JVI.05396-11.
52. Cocquerel L, Quinn ER, Flint M, Hadlock KG, Foung SK, Levy S. 2003. Recognition of native hepatitis C virus E1E2 heterodimers by a human monoclonal antibody. J. Virol. 77:1604-1609. http://dx.doi.org/10.1128 /JVI.77.2.1604-1609.2003.
53. Kuiken C, Mizokami M, Deleage G, Yusim K, Penin F, Shin IT, Charavay C, Tao N, Crisan D, Grando D, Dalwani A, Geourjon C, Agrawal A, Combet C. 2006. Hepatitis C databases, principles and utility to researchers. Hepatology 43:1157-1165. http://dx.doi.org/10.1002/hep.21162.
54. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680. http://dx.doi.org/10.1093/nar /22.22.4673.
55. Merutka G, Dyson HJ, Wright PE. 1995. 'Random coil' 1H chemical shifts obtained as a function of temperature and trifluoroethanol concentration for the peptide series GGXGG. J. Biomol. NMR 5:14-24. http://dx .doi.org/10.1007/BF00227466.