Three different functional microdomains in the hepatitis C virus hypervariable region 1 (HVR1) mediate entry and immune evasion

Journal of Biological Chemistry

Volumn 287, Issue 42, 2012, Pages 35631-35645

  Guan, Mo ^a   Wang, Wenbo ^a   Liu, Xiaoqing ^a   Tong, Yimin ^a,e   Liu, Yuan ^a   Ren, Hao ^a   Zhu, Shiying ^a   Dubuisson, Jean ^b   Baumert, Thomas F ^c   Zhu, Yongzhe ^a   Peng, Haoran ^a   Aurelian, Laure ^d   Zhao, Ping ^a   Qi, Zhongtian ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b UNIV LILLE   (France)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^e INSTITUTE PASTEUR OF SHANGHAI   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RESIDUES; CLASS B; ENVELOPE GLYCOPROTEINS; ENVELOPE PROTEINS; GENETIC HETEROGENEITIES; HEPARAN; HEPATITIS C VIRUS; HIGH DENSITY LIPOPROTEIN; MICRO-DOMAINS; NEUTRALIZING ANTIBODIES; NEUTRALIZING EPITOPE; PERSISTENT INFECTION; PSEUDO-PARTICLES; SCAVENGER RECEPTOR; VIRUS NEUTRALIZATION;

AMINO ACIDS; CELL CULTURE; VIRUSES;

ANTIBODIES;

GLYCOPROTEIN E2; HEPARAN; HIGH DENSITY LIPOPROTEIN; HYPERVARIABLE REGION 1 PROTEIN; NEUTRALIZING ANTIBODY; POLYPROTEIN; SCAVENGER RECEPTOR B; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL MEMBRANE; CONTROLLED STUDY; DISEASE ACTIVITY; HEPATITIS C; HEPATITIS C VIRUS; IMMUNE EVASION; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; STRUCTURE ANALYSIS; VIRUS ENTRY; VIRUS ISOLATION; VIRUS NEUTRALIZATION; VIRUS PARTICLE;

ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIGENS, CD36; HEPACIVIRUS; HEPATITIS C; HUMANS; IMMUNE EVASION; PROTEIN STRUCTURE, TERTIARY; VIRAL HEPATITIS VACCINES; VIRAL PROTEINS; VIRUS INTERNALIZATION;

EID: 84867427019     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.382341     Document Type: Article

References (69)

1. Alter, M. J. (2007) Epidemiology of hepatitis C virus infection. World J. Gastroenterol. 13, 2436-2441
2. Seeff, L. B. (2002) Natural history of chronic hepatitis C. Hepatology 36, S35-S46
3. Brown, R. S. (2005) Hepatitis C and liver transplantation. Nature 436, 973-978
4. Pawlotsky, J. M. (2011) Treatment failure and resistance with direct-acting antiviral drugs against hepatitis C virus. Hepatology 53, 1742-1751
5. Hoofnagle, J. H. (2002) Course and outcome of hepatitis C. Hepatology 36, S21-S29
6. Dustin, L. B., and Rice, C. M. (2007) Flying under the radar. The immunobiology of hepatitis C. Annu. Rev. Immunol. 25, 71-99
7. Rehermann, B. (2009) Hepatitis C virus versus innate and adaptive immune responses. A tale of co-evolution and co-existence. J. Clin. Invest. 119, 1745-1754
8. Uebelhoer, L., Han, J. H., Callendret, B., Mateu, G., Shoukry, N. H., Hanson, H. L., Rice, C. M., Walker, C. M., and Grakoui, A. (2008) Stable cytotoxic T cell escape mutation in hepatitis C virus is linked to maintenance of viral fitness. PLoS Pathog. 4, e1000143
9. Gómez, J., Martell, M., Quer, J., Cabot, B., and Esteban, J. I. (1999) Hepatitis C viral quasispecies. J. Viral. Hepat. 6, 3-16 (Pubitemid 29077621)
10. Simmonds, P., Bukh, J., Combet, C., Deléage, G., Enomoto, N., Feinstone, S., Halfon, P., Inchauspé, G., Kuiken, C., Maertens, G., Mizokami, M., Murphy, D. G., Okamoto, H., Pawlotsky, J. M., Penin, F., Sablon, E., Shin-I, T., Stuyver, L. J., Thiel, H. J., Viazov, S., Weiner, A. J., and Widell, A. (2005) Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 42, 962-973 (Pubitemid 41401136)
11. Hijikata, M., Kato, N., Ootsuyama, Y., Nakagawa, M., Ohkoshi, S., and Shimotohno, K. (1991) Hypervariable regions in the putative glycoprotein of hepatitis C virus. Biochem. Biophys. Res. Commun. 175, 220-228
12. Weiner, A. J., Brauer, M. J., Rosenblatt, J., Richman, K. H., Tung, J., Crawford, K., Bonino, F., Saracco, G., Choo, Q. L., Houghton, M., et al. (1991) Variable and hypervariable domains are found in the regions of HCV corresponding to the flavivirus envelope and NS1 proteins and the pestivirus envelope glycoproteins. Virology 180, 842-848
13. Wang, G. P., Sherrill-Mix, S. A., Chang, K. M., Quince, C., and Bushman, F. D. (2010) Hepatitis C virus transmission bottlenecks analyzed by deep sequencing. J. Virol. 84, 6218-6228
14. Kato, N., Sekiya, H., Ootsuyama, Y., Nakazawa, T., Hijikata, M., Ohkoshi, S., and Shimotohno, K. (1993) Humoral immune response to hypervariable region 1 of the putative envelope glycoprotein (GP70) of hepatitis C virus. J. Virol. 67, 3923-3930 (Pubitemid 23180716)
15. Farci, P., Shimoda, A., Coiana, A., Diaz, G., Peddis, G., Melpolder, J. C., Strazzera, A., Chien, D. Y., Munoz, S. J., Balestrieri, A., Purcell, R. H., and Alter, H. J. (2000) The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 288, 339-344 (Pubitemid 30226196)
16. van Doorn, L. J., Capriles, I., Maertens, G., DeLeys, R., Murray, K., Kos, T., Schellekens, H., and Quint, W. (1995) Sequence evolution of the hypervariable region in the putative envelope region E2/NS1 of hepatitis C virus is correlated with specific humoral immune responses. J. Virol. 69, 773-778
17. Farci, P., Shimoda, A., Wong, D., Cabezon, T., De Gioannis, D., Strazzera, A., Shimizu, Y., Shapiro, M., Alter, H. J., and Purcell, R. H. (1996) Prevention of hepatitis C virus infection in chimpanzees by hyperimmune serum against the hypervariable region 1 of the envelope 2 protein. Proc. Natl. Acad. Sci. U.S.A. 93, 15394-15399 (Pubitemid 27009611)
18. Dowd, K. A., Netski, D. M., Wang, X. H., Cox, A. L., and Ray, S. C. (2009) Selection pressure from neutralizing antibodies drives sequence evolution during acute infection with hepatitis C virus. Gastroenterology 136, 2377-2386
19. Weiner, A. J., Geysen, H. M., Christopherson, C., Hall, J. E., Mason, T. J., Saracco, G., Bonino, F., Crawford, K., Marion, C. D., Crawford, K. A., et al. (1992) Evidence for immune selection of hepatitis C virus (HCV) putative envelope glycoprotein variants. Potential role in chronic HCV infections. Proc. Natl. Acad. Sci. U.S.A. 89, 3468-3472
20. Laskus, T., Wilkinson, J., Gallegos-Orozco, J. F., Radkowski, M., Adair, D. M., Nowicki, M., Operskalski, E., Buskell, Z., Seeff, L. B., Vargas, H., and Rakela, J. (2004) Analysis of hepatitis C virus quasispecies transmission and evolution in patients infected through blood transfusion. Gastroenterology 127, 764-776 (Pubitemid 39208410)
21. Liu, L., Fisher, B. E., Dowd, K. A., Astemborski, J., Cox, A. L., and Ray, S. C. (2010) Acceleration of hepatitis C virus envelope evolution in humans is consistent with progressive humoral immune selection during the transition from acute to chronic infection. J. Virol. 84, 5067-5077
22. Barth, H., Schnober, E. K., Zhang, F., Linhardt, R. J., Depla, E., Boson, B., Cosset, F. L., Patel, A. H., Blum, H. E., and Baumert, T. F. (2006) Viral and cellular determinants of the hepatitis C virus envelope-heparan sulfate interaction. J. Virol. 80, 10579-10590 (Pubitemid 44628904)
23. Barth, H., Schafer, C., Adah, M. I., Zhang, F., Linhardt, R. J., Toyoda, H., Kinoshita-Toyoda, A., Toida, T., Van Kuppevelt, T. H., Depla, E., Von Weizsacker, F., Blum, H. E., and Baumert, T. F. (2003) Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J. Biol. Chem. 278, 41003-41012 (Pubitemid 37280923)
24. Molina, S., Castet, V., Fournier-Wirth, C., Pichard-Garcia, L., Avner, R., Harats, D., Roitelman, J., Barbaras, R., Graber, P., Ghersa, P., Smolarsky, M., Funaro, A., Malavasi, F., Larrey, D., Coste, J., Fabre, J. M., Sa-Cunha, A., and Maurel, P. (2007) The low density lipoprotein receptor plays a role in the infection of primary human hepatocytes by hepatitis C virus. J. Hepatol. 46, 411-419 (Pubitemid 46201721)
25. Owen, D. M., Huang, H., Ye, J., and Gale, M., Jr. (2009) Apolipoprotein E on hepatitis C virion facilitates infection through interaction with low density lipoprotein receptor. Virology 394, 99-108
26. Scarselli, E., Ansuini, H., Cerino, R., Roccasecca, R. M., Acali, S., Filocamo, G., Traboni, C., Nicosia, A., Cortese, R., and 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
27. Zeisel, M. B., Koutsoudakis, G., Schnober, E. K., Haberstroh, A., Blum, H. E., Cosset, F. L., Wakita, T., Jaeck, D., Doffoel, M., Royer, C., Soulier, E., Schvoerer, E., Schuster, C., Stoll-Keller, F., Bartenschlager, R., Pietschmann, T., Barth, H., and Baumert, T. F. (2007) Scavenger receptor class B type I is a key host factor for hepatitis C virus infection required for an entry step closely linked to CD81. Hepatology 46, 1722-1731
28. Dreux, M., Dao Thi, V. L., Fresquet, J., Guérin, M., Julia, Z., Verney, G., Durantel, D., Zoulim, F., Lavillette, D., Cosset, F. L., and Bartosch, B. (2009) Receptor complementation and mutagenesis reveal SR-BI as an essential HCV entry factor and functionally imply its intra- and extracellular domains. PLoS Pathog. 5, e1000310
29. Pileri, P., Uematsu, Y., Campagnoli, S., Galli, G., Falugi, F., Petracca, R., Weiner, A. J., Houghton, M., Rosa, D., Grandi, G., and Abrignani, S. (1998) Binding of hepatitis C virus to CD81. Science 282, 938-941 (Pubitemid 28507525)
30. Evans, M. J., von Hahn, T., Tscherne, D. M., Syder, A. J., Panis, M., Wölk, B., Hatziioannou, T., McKeating, J. A., Bieniasz, P. D., and Rice, C. M. (2007) Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446, 801-805 (Pubitemid 46582027)
31. Ploss, A., Evans, M. J., Gaysinskaya, V. A., Panis, M., You, H., de Jong, Y. P., and Rice, C. M. (2009) Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457, 882-886
32. Bartosch, B., Vitelli, A., Granier, C., Goujon, C., Dubuisson, J., Pascale, S., Scarselli, E., Cortese, R., Nicosia, A., and Cosset, F. L. (2003) Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-BI scavenger receptor. J. Biol. Chem. 278, 41624-41630 (Pubitemid 37310418)
33. Bartosch, B., Verney, G., Dreux, M., Donot, P., Morice, Y., Penin, F., Pawlotsky, J. M., Lavillette, D., and Cosset, F. L. (2005) An interplay between hypervariable region 1 of the hepatitis C virus E2 glycoprotein, the scavenger receptor BI, and high density lipoprotein promotes both enhancement of infection and protection against neutralizing antibodies. J. Virol. 79, 8217-8229 (Pubitemid 40853525)
34. Bankwitz, D., Steinmann, E., Bitzegeio, J., Ciesek, S., Friesland, M., Herrmann, E., Zeisel, M. B., Baumert, T. F., Keck, Z. Y., Foung, S. K., Pécheur, E. I., and 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
35. Wakita, T., Pietschmann, T., Kato, T., Date, T., Miyamoto, M., Zhao, Z., Murthy, K., Habermann, A., Kräusslich, H. G., Mizokami, M., Bartenschlager, R., and Liang, T. J. (2005) Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11, 791-796 (Pubitemid 41021213)
36. Forns, X., Thimme, R., Govindarajan, S., Emerson, S. U., Purcell, R. H., Chisari, F. V., and Bukh, J. (2000) Hepatitis C virus lacking the hypervariable region 1 of the second envelope protein is infectious and causes acute resolving or persistent infection in chimpanzees. Proc. Natl. Acad. Sci. U.S.A. 97, 13318-13323
37. Prentoe, J., Jensen, T. B., Meuleman, P., Serre, S. B., Scheel, T. K., Leroux- Roels, G., Gottwein, J. M., and Bukh, J. (2011) Hypervariable region 1 differentially impacts viability of hepatitis C virus strains of genotypes 1-6 and impairs virus neutralization. J. Virol. 85, 2224-2234
38. Dreux, M., Pietschmann, T., Granier, C., Voisset, C., Ricard-Blum, S., Mangeot, P. E., Keck, Z., Foung, S., Vu-Dac, N., Dubuisson, J., Bartenschlager, R., Lavillette, D., and Cosset, F. L. (2006) High density lipoprotein inhibits hepatitis C virus-neutralizing antibodies by stimulating cell entry via activation of the scavenger receptor BI. J. Biol. Chem. 281, 18285-18295 (Pubitemid 44035485)
39. Dreux, M., Boson, B., Ricard-Blum, S., Molle, J., Lavillette, D., Bartosch, B., Pécheur, E. I., and Cosset, F. L. (2007) The exchangeable apolipoprotein apoC-I promotes membrane fusion of hepatitis C virus. J. Biol. Chem. 282, 32357-32369 (Pubitemid 350106439)
40. Meunier, J. C., Engle, R. E., Faulk, K., Zhao, M., Bartosch, B., Alter, H., Emerson, S. U., Cosset, F. L., Purcell, R. H., and Bukh, J. (2005) Evidence for cross-genotype neutralization of hepatitis C virus pseudo-particles and enhancement of infectivity by apolipoprotein C1. Proc. Natl. Acad. Sci. U.S.A. 102, 4560-4565 (Pubitemid 40397151)
41. Penin, F., Combet, C., Germanidis, G., Frainais, P. O., Deléage, G., and Pawlotsky, J. M. (2001) Conservation of the conformation and positive charges of hepatitis C virus E2 envelope glycoprotein hypervariable region 1 points to a role in cell attachment. J. Virol. 75, 5703-5710 (Pubitemid 32488166)
42. Callens, N., Ciczora, Y., Bartosch, B., Vu-Dac, N., Cosset, F. L., Pawlotsky, J. M., Penin, F., and Dubuisson, J. (2005) Basic residues in hypervariable region 1 of hepatitis C virus envelope glycoprotein E2 contribute to virus entry. J. Virol. 79, 15331-15341 (Pubitemid 43032315)
43. Bartosch, B., Dubuisson, J., and Cosset, F. L. (2003) Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J. Exp. Med. 197, 633-642 (Pubitemid 36314658)
44. Fafi-Kremer, S., Fofana, I., Soulier, E., Carolla, P., Meuleman, P., Leroux- Roels, G., Patel, A. H., Cosset, F. L., Pessaux, P., Doffoël, M., Wolf, P., Stoll-Keller, F., and Baumert, T. F. (2010) Viral entry and escape from antibody-mediated neutralization influence hepatitis C virus reinfection in liver transplantation. J. Exp. Med. 207, 2019-2031
45. Tong, Y., Zhu, Y., Xia, X., Liu, Y., Feng, Y., Hua, X., Chen, Z., Ding, H., Gao, L., Wang, Y., Feitelson, M. A., Zhao, P., and Qi, Z. T. (2011) Tupaia CD81, SR-BI, claudin-1, and occludin support hepatitis C virus infection. J. Virol. 85, 2793-2802
46. Blight, K. J., McKeating, J. A., and Rice, C. M. (2002) Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J. Virol. 76, 13001-13014 (Pubitemid 35386984)
47. Yi, M., Ma, Y., Yates, J., and Lemon, S. M. (2007) Compensatory mutations in E1, p7, NS2, and NS3 enhance yields of cell culture-infectious intergenotypic chimeric hepatitis C virus. J. Virol. 81, 629-638 (Pubitemid 46067890)
48. Pestka, J. M., Zeisel, M. B., Bläser, E., Schürmann, P., Bartosch, B., Cosset, F. L., Patel, A. H., Meisel, H., Baumert, J., Viazov, S., Rispeter, K., Blum, H. E., Roggendorf, M., and Baumert, T. F. (2007) Rapid induction of virus-neutralizing antibodies and viral clearance in a single-source outbreak of hepatitis C. Proc. Natl. Acad. Sci. U.S.A. 104, 6025-6030 (Pubitemid 47175652)
49. Op De Beeck, A., Voisset, C., Bartosch, B., Ciczora, Y., Cocquerel, L., Keck, Z., Foung, S., Cosset, F. L., and Dubuisson, J. (2004) Characterization of functional hepatitis C virus envelope glycoproteins. J. Virol. 78, 2994-3002 (Pubitemid 38314357)
50. Lucas, M., Tsitoura, E., Montoya, M., Laliotou, B., Aslanoglou, E., Kouvatsis, V., Entwisle, C., Miller, J., Klenerman, P., Hadziyannis, A., Hadziyannis, S., Borrow, P., and Mavromara, P. (2003) Characterization of secreted and intracellular forms of a truncated hepatitis C virus E2 protein expressed by a recombinant herpes simplex virus. J. Gen. Virol. 84, 545-554 (Pubitemid 36267126)
51. Flint, M., Dubuisson, J., Maidens, C., Harrop, R., Guile, G. R., Borrow, P., and McKeating, J. A. (2000) Functional characterization of intracellular and secreted forms of a truncated hepatitis C virus E2 glycoprotein. J. Virol. 74, 702-709 (Pubitemid 30036206)
52. Flint, M., Maidens, C., Loomis-Price, L. D., Shotton, C., Dubuisson, J., Monk, P., Higginbottom, A., Levy, S., and McKeating, J. A. (1999) Characterization of hepatitis C virus E2 glycoprotein interaction with a putative cellular receptor, CD81. J. Virol. 73, 6235-6244 (Pubitemid 29327798)
53. Lindenbach, B. D., Evans, M. J., Syder, A. J., Wölk, B., Tellinghuisen, T. L., Liu, C. C., Maruyama, T., Hynes, R. O., Burton, D. R., McKeating, J. A., and Rice, C. M. (2005) Complete replication of hepatitis C virus in cell culture. Science 309, 623-626 (Pubitemid 41033648)
54. Zhong, J., Gastaminza, P., Cheng, G., Kapadia, S., Kato, T., Burton, D. R., Wieland, S. F., Uprichard, S. L., Wakita, T., and Chisari, F. V. (2005) Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. U.S.A. 102, 9294-9299 (Pubitemid 40923557)
55. Zhong, J., Gastaminza, P., Chung, J., Stamataki, Z., Isogawa, M., Cheng, G., McKeating, J. A., and Chisari, F. V. (2006) Persistent hepatitis C virus infection in vitro. Co-evolution of virus and host. J. Virol. 80, 11082-11093 (Pubitemid 44706549)
56. Zhang, P., Wu, C. G., Mihalik, K., Virata-Theimer, M. L., Yu, M. Y., Alter, H. J., and Feinstone, S. M. (2007) Hepatitis C virus epitope-specific neutralizing antibodies in IGs prepared from human plasma. Proc. Natl. Acad. Sci. U.S.A. 104, 8449-8454 (Pubitemid 47175508)
57. Cao, J., Chen, Z., Ren, Y., Luo, Y., Cao, M., Lu, W., Zhao, P., and Qi, Z. (2011) Oral immunization with attenuated Salmonella carrying a co-expression plasmid encoding the core and E2 proteins of hepatitis C virus capable of inducing cellular immune responses and neutralizing antibodies in mice. Vaccine 29, 3714-3723
58. Roccasecca, R., Ansuini, H., Vitelli, A., Meola, A., Scarselli, E., Acali, S., Pezzanera, M., Ercole, B. B., McKeating, J., Yagnik, A., Lahm, A., Tramontano, A., Cortese, R., and Nicosia, A. (2003) Binding of the hepatitis C virus E2 glycoprotein to CD81 is strain-specific and is modulated by a complex interplay between hypervariable regions 1 and 2. J. Virol. 77, 1856-1867 (Pubitemid 36109998)
59. Basu, A., Kanda, T., Beyene, A., Saito, K., Meyer, K., and Ray, R. (2007) Sulfated homologues of heparin inhibit hepatitis C virus entry into mammalian cells. J. Virol. 81, 3933-3941 (Pubitemid 46586889)
60. Goffard, A., Callens, N., Bartosch, B., Wychowski, C., Cosset, F. L., Montpellier, C., and Dubuisson, J. (2005) Role of N-linked glycans in the functions of hepatitis C virus envelope glycoproteins. J. Virol. 79, 8400-8409 (Pubitemid 40853542)
61. Hsu, M., Zhang, J., Flint, M., Logvinoff, C., Cheng-Mayer, C., Rice, C. M., and McKeating, J. A. (2003) Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc. Natl. Acad. Sci. U.S.A. 100, 7271-7276 (Pubitemid 36706428)
62. Scarselli, E., Cerino, A., Esposito, G., Silini, E., Mondelli, M. U., and Traboni, C. (1995) Occurrence of antibodies reactive with more than one variant of the putative envelope glycoprotein (GP70) hypervariable region 1 in viremic hepatitis C virus-infected patients. J. Virol. 69, 4407-4412
63. Zibert, A., Kraas, W., Meisel, H., Jung, G., and Roggendorf, M. (1997) Epitope mapping of antibodies directed against hypervariable region 1 in acute self-limiting and chronic infections due to hepatitis C virus. J. Virol. 71, 4123-4127 (Pubitemid 27172432)
64. Mondelli, M. U., Cerino, A., Lisa, A., Brambilla, S., Segagni, L., Cividini, A., Bissolati, M., Missale, G., Bellati, G., Meola, A., Bruniercole, B., Nicosia, A., Galfrè, G., and Silini, E. (1999) Antibody responses to hepatitis C virus hypervariable region 1. Evidence for cross-reactivity and immune-mediated sequence variation. Hepatology 30, 537-545 (Pubitemid 29357522)
65. Vieyres, G., Dubuisson, J., and Patel, A. H. (2011) Characterization of antibody-mediated neutralization directed against the hypervariable region 1 of hepatitis C virus E2 glycoprotein. J. Gen. Virol. 92, 494-506
66. Ogata, N., Alter, H. J., Miller, R. H., and Purcell, R. H. (1991) Nucleotide sequence and mutation rate of the H strain of hepatitis C virus. Proc. Natl. Acad. Sci. U.S.A. 88, 3392-3396 (Pubitemid 21916627)
67. André, P., Komurian-Pradel, F., Deforges, S., Perret, M., Berland, J. L., Sodoyer, M., Pol, S., Bréchot, C., Paranhos-Baccalà, G., and Lotteau, V. (2002) Characterization of low and very low density hepatitis C virus RNA-containing particles. J. Virol. 76, 6919-6928 (Pubitemid 41246207)
68. Chang, K. S., Jiang, J., Cai, Z., and Luo, G. (2007) Human apolipoprotein E is required for infectivity and production of hepatitis C virus in cell culture. J. Virol. 81, 13783-13793 (Pubitemid 350247871)
69. Kawaguchi, K., Faulk, K., Purcell, R. H., and Emerson, S. U. (2011) Reproduction in vitro of a quasispecies from a hepatitis C virus-infected patient and determination of factors that influence selection of a dominant species. J. Virol. 85, 3408-3414