The long and winding road leading to the identification of the hepatitis C virus

Journal of Hepatology

Volumn 51, Issue 5, 2009, Pages 939-948

  Houghton, Michael ^a  

^a Epiphany Biosciences Inc   (United States)

Author keywords

HCV history; Hepatitis C virus discovery; Identification of HCV; Non A; Non B hepatitis NANBH

Indexed keywords

COMPLEMENTARY DNA; GENOMIC DNA; VIRUS ANTIBODY;

BIOTECHNOLOGY; CHIMPANZEE; DISEASE MODEL; GENE ACTIVITY; GENETIC IDENTIFICATION; GENOMICS; HEPATITIS C VIRUS; HEPATITIS DELTA VIRUS; HEPATITIS NON A NON B; MOLECULAR CLONING; NONHUMAN; OPEN READING FRAME; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REVIEW; SEROCONVERSION; SEROLOGY; VIRUS GENOME; VIRUS IDENTIFICATION;

ANIMALS; DISEASE MODELS, ANIMAL; GENOME, VIRAL; HEPACIVIRUS; HEPATITIS C; HISTORY, 20TH CENTURY; HUMANS; PAN TROGLODYTES; VIROLOGY;

EID: 70349730223     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2009.08.004     Document Type: Review

References (88)

1. Krugman S., Ward R., and Giles J.P. The natural history of infectious hepatitis. Am J Med 32 (1962) 717-728
2. Feinstone S.M., Kapikian A.Z., and Purcell R.H. Hepatitis A: detection by immune electron microscopy of a viruslike antigen associated with acute illness. Science 182 (1973) 1026-1028
3. Bayer M.E., Blumberg B.S., and Werner B. Particles associated with Australia antigen in the sera of patients with leukaemia, Down's Syndrome and hepatitis. Nature 218 (1968) 1057-1059
4. Feinstone S.M., Kapikian A.Z., Purcell R.H., Alter H.J., and Holland P.V. Transfusion-associated hepatitis not due to viral hepatitis type A or B. N Engl J Med 292 (1975) 767-770
5. Alter H.J., Purcell R.H., Holland P.V., and Popper H. Transmissible agent in non-A, non-B hepatitis. Lancet 1 (1978) 459-463
6. Hollinger F.B., Gitnick G.L., Aach R.D., Szmuness W., Mosley J.W., Stevens C.E., et al. Non-A, non-B hepatitis transmission in chimpanzees: a project of the transfusion-transmitted viruses study group. Intervirology 10 (1978) 60-68
7. Shimizu Y.K., Feinstone S.M., Purcell R.H., Alter H.J., and London W.T. Non-A, non-B hepatitis: ultrastructural evidence for two agents in experimentally infected chimpanzees. Science 205 (1979) 197-200
8. Bradley D.W., Maynard J.E., Popper H., Cook E.H., Ebert J.W., McCaustland K.A., et al. Posttransfusion non-A, non-B hepatitis: physicochemical properties of two distinct agents. J Infect Dis 148 (1983) 254-265
9. Feinstone S.M., Mihalik K.B., Kamimura T., Alter H.J., London W.T., and Purcell R.H. Inactivation of hepatitis B virus and non-A, non-B hepatitis by chloroform. Infect Immun 41 (1983) 816-821
10. Bradley D.W. The agents of non-A, non-B viral hepatitis. J Virol Methods 10 (1985) 307-319
11. He L.F., Alling D., Popkin T., Shapiro M., Alter H.J., and Purcell R.H. Determining the size of non-A, non-B hepatitis virus by filtration. J Infect Dis 156 (1987) 636-640
12. Dienstag J.L., and Alter H.J. Non-A, non-B hepatitis: evolving epidemiologic and clinical perspective. Semin Liver Dis 6 (1986) 67-68
13. Seeff L.B., and Dienstag J.L. Transfusion-associated non-A, non-B hepatitis. Where do we go from here?. Gastroenterology 95 (1988) 530-533
14. Alter H.J. The dominant role of non-A, non-B in the pathogenesis of post-transfusion hepatitis: a clinical assessment. Clin Gastroenterol 9 (1980) 155-170
15. Hollinger F.B., Mosley J.W., Szmuness W., Aach R.D., Peters R.L., and Stevens C. Transfusion-transmitted viruses study: experimental evidence for two non-A, non-B, hepatitis agents. J Infect Dis 142 (1980) 400-407
16. Alter M.J., Hadler S.C., Francis D.P., and Maynard J.E. The epidemiology of non-A, non-B hepatitis in the United States. Prog Clin Biol Res 182 (1985) 71-719
17. Shih J.W., Mur J.I., and Alter H.J. Non-A, non-B hepatitis: advances and unfulfilled expectations of the first decade. Prog Liver Dis 8 (1986) 433-452
18. Houghton M., Stewart A.G., Doel S.M., Emtage J.S., Eaton M.A., Smith J.C., et al. The amino-terminal sequence of human fibroblast interferon as deduced from reverse transcripts obtained using synthetic oligonucleotide primers. Nucleic Acids Res 8 (1980) 1913-1931
19. Houghton M., Jackson I.J., Porter A.G., Doel S.M., Catlin G.H., Barber C., et al. The absence of introns within a human fibroblast interferon gene. Nucleic Acids Res 9 (1981) 247-266
20. Rizzetto M., Canese M.G., Aricò S., Crivelli O., Trepo C., Bonino F., et al. Immunofluorescence detection of new antigen-antibody system (delta/anti-delta) associated to hepatitis B virus in liver and in serum of HBsAg carriers. Gut 12 (1977) 997-1003
21. Rizzetto M., and Verme G. Delta hepatitis-present status. J Hepatol 1 (1985) 187-193
22. Denniston K.J., Hoyer B.H., Smedile A., Wells F.V., Nelson J., and Gerin J.L. Cloned fragment of the hepatitis delta virus RNA genome: sequence and diagnostic application. Science 232 (1986) 873-875
23. Kamimura T., Ponzetto A., Bonino F., Feinstone S.M., Gerin J.L., and Purcell R.H. Cytoplasmic tubular structures in liver of HBsAg carrier chimpanzees infected with delta agent and comparison with cytoplasmic structures in non-A, non-B hepatitis. Hepatology 3 (1983) 631-637
24. Wang K.S., Choo Q.L., Weiner A.J., Ou J.H., Najarian R.C., Thayer R.M., et al. Structure, sequence and expression of the hepatitis delta (delta) viral genome. Nature 323 (1986) 508-514 [Erratum in: Nature 1987;5:328, 456]
25. Weiner A.J., Choo Q.L., Wang K.S., Govindarajan S., Redeker A.G., Gerin J.L., et al. A single antigenomic open reading frame of the hepatitis delta virus encodes the epitope(s) of both hepatitis delta antigen polypeptides p24 delta and p27 delta. J Virol 62 (1988) 594-599
26. Weiner A.J., Wang K.S., Choo Q.L., Gerin J.L., Bradley D.W., and Houghton M. Hepatitis delta (delta) cDNA clones: undetectable hybridization to nucleic acids from infectious non-A, non-B hepatitis materials and hepatitis B DNA. J Med Virol 21 (1987) 239-247
27. Wakita T., Pietschmann T., Kato T., Date T., Miyamoto M., Zhao Z., et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11 7 (2005) 791-796 [Epub 2005 Jun 12. Erratum in: Nat Med 2005;11:905]
28. Seto B., Coleman Jr. W.G., Iwarson S., and Gerety R.J. Detection of reverse transcriptase activity in association with the non-A, non-B hepatitis agent(s). Lancet 8409 (1984) 941-943
29. Prince A.M., Huima T., Williams B.A., Bardina L., and Brotman B. Isolation of a virus from chimpanzee liver cell cultures inoculated with sera containing the agent of non-A, non-B hepatitis. Lancet 8411 (1984) 1071-1075
30. Shimizu Y.K., Oomura M., Abe K., Uno M., Yamada E., Ono Y., et al. Production of antibody associated with non-A, non-B hepatitis in a chimpanzee lymphoblastoid cell line established by in vitro transformation with Epstein-Barr virus. Proc Natl Acad Sci USA 82 (1985) 2138-2142
31. Maeda T., Honda Y., Hanawa M., Yamada E., Ono Y., Shikata T., et al. Production of antibodies directed against microtubular aggregates in hepatocytes of chimpanzees with non-A, non-B hepatitis. J Gen Virol 70 Pt. 6 (1989) 1401-1407
32. Broome S., and Gilbert W. Immunological screening method to detect specific translation products. Proc Natl Acad Sci USA 75 (1978) 2746-2749
33. Young R.A., and Davis R.W. Efficient isolation of genes by using antibody probes. Proc Natl Acad Sci USA 80 (1983) 1194-1198
34. Bradley D.W. Hepatitis non-A, non-B viruses become identified as hepatitis C and E viruses. Prog Med Virol 37 (1990) 101-135
35. Feinstone S.M., Alter H.J., Dienes H.P., Shimizu Y., Popper H., Blackmore D., et al. Non-A, non-B hepatitis in chimpanzees and marmosets. J Infect Dis 144 (1981) 588-598
36. Choo Q.L., Kuo G., Weiner A.J., Overby L.R., Bradley D.W., and Houghton M. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244 (1989) 359-362
37. Kuo G., Choo Q.L., Alter H.J., Gitnick G.L., Redeker A.G., Purcell R.H., et al. An assay for circulating antibodies to a major etiologic virus of human non-A, non-B hepatitis. Science 244 (1989) 362-364
38. Miyamura T., Saito I., Katayama T., Kikuchi S., Tateda A., Houghton M., et al. Detection of antibody against antigen expressed by molecularly cloned hepatitis C virus cDNA: application to diagnosis and blood screening for posttransfusion hepatitis. Proc Natl Acad Sci USA 87 (1990) 983-987
39. Kubo Y., Takeuchi K., Boonmar S., Katayama T., Choo Q.L., Kuo G., et al. A cDNA fragment of hepatitis C virus isolated from an implicated donor of post-transfusion non-A, non-B hepatitis in Japan. Nucleic Acids Res 17 (1989) 1367-1372
40. Simmonds P. Variability of hepatitis C virus. Hepatology 21 (1995) 570-583
41. Robertson B., Myers G., Howard C., Brettin T., Bukh J., Gaschen B., et al. Classification, nomenclature, and database development for hepatitis C virus (HCV) and related viruses: proposals for standardization. International Committee on Virus Taxonomy. Arch Virol 143 (1998) 2493-2503
42. Patel K., and McHutchison J.G. Initial treatment for chronic hepatitis C: current therapies and their optimal dosing and duration. Cleve Clin J Med 71 Suppl. 3 (2004) S8-S12
43. Bukh J., Purcell R.H., and Miller R.H. Sequence analysis of the core gene of 14 hepatitis C virus genotypes. Proc Natl Acad Sci USA 91 (1994) 8239-8243
44. Choo Q.L., Richman K.H., Han J.H., Berger K., Lee C., Dong C., et al. Genetic organization and diversity of the hepatitis C virus. Proc Natl Acad Sci USA 88 (1991) 2451-2455
45. Kato N., Hijikata M., Ootsuyama Y., Nakagawa M., Ohkoshi S., Sugimura T., et al. Molecular cloning of the human hepatitis C virus genome from Japanese patients with non-A, non-B hepatitis. Proc Natl Acad Sci USA 87 (1990) 9524-9528
46. Grakoui A., McCourt D.W., Wychowski C., Feinstone S.M., and Rice C.M. Characterization of the hepatitis C virus-encoded serine proteinase: determination of proteinase-dependent polyprotein cleavage sites. J Virol 67 (1993) 2832-2843
47. Hijikata M., Mizushima H., Akagi T., Mori S., Kakiuchi N., Kato N., et al. Two distinct proteinase activities required for the processing of a putative nonstructural precursor protein of hepatitis C virus. J Virol 67 (1993) 4665-4675
48. Eckart M.R., Selby M., Masiarz F., Lee C., Berger K., Crawford K., et al. The hepatitis C virus encodes a serine protease involved in processing of the putative nonstructural proteins from the viral polyprotein precursor. Biochem Biophys Res Commun 192 (1993) 399-406
49. Suzich J.A., Tamura J.K., Palmer-Hill F., Warrener P., Grakoui A., Rice C.M., et al. Hepatitis C virus NS3 protein polynucleotide-stimulated nucleoside triphosphatase and comparison with the related pestivirus and flavivirus enzymes. J Virol 67 (1993) 6152-6158
50. Lohmann V., Körner F., Herian U., and Bartenschlager R. Biochemical properties of hepatitis C virus NS5B RNA-dependent RNA polymerase and identification of amino acid sequence motifs essential for enzymatic activity. J Virol 71 (1997) 8416-8428
51. Lohmann V., Körner F., Koch J., Herian U., Theilmann L., and Bartenschlager R. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285 (1999) 110-113
52. Blight K.J., Kolykhalov A.A., and Rice C.M. Efficient initiation of HCV RNA replication in cell culture. Science 290 (2000) 1972-1974
53. Grakoui A., McCourt D.W., Wychowski C., Feinstone S.M., and Rice C.M. A second hepatitis C virus-encoded proteinase. Proc Natl Acad Sci USA 90 (1993) 10583-10587
54. Jones C.T., Murray C.L., Eastman D.K., Tassello J., and Rice C.M. Hepatitis C virus p7 and NS2 proteins are essential for production of infectious virus. J Virol 81 (2007) 8374-8383
55. Griffin S.D., Beales L.P., Clarke D.S., Worsfold O., Evans S.D., Jaeger J., et al. The p7 protein of hepatitis C virus forms an ion channel that is blocked by the antiviral drug, Amantadine. FEBS Lett 535 (2003) 34-38
56. Luik P., Chew C., Aittoniemi J., Chang J., Wentworth Jr. P., Dwek R.A., et al. The 3-dimensional structure of a hepatitis C virus p7 ion channel by electron microscopy. Proc Natl Acad Sci USA 106 (2009) 12567-12568
57. Steinmann E., Penin F., Kallis S., Patel A.H., Bartenschlager R., and Pietschmann T. Hepatitis C virus p7 protein is crucial for assembly and release of infectious virions. PLoS Pathog 7 (2007) e103
58. Tellinghuisen T.L., Foss K.L., and Treadaway J. Regulation of hepatitis C virion production via phosphorylation of the NS5A protein. PLoS Pathog. 4 (2008) e1000032
59. Einav S., Gerber D., Bryson P.D., Sklan E.H., Elazar M., Maerkl S.J., et al. Discovery of a hepatitis C target and its pharmacological inhibitors by microfluidic affinity analysis. Nat Biotechnol 9 (2008) 1019-1027
60. Randall G., Panis M., Cooper J.D., Tellinghuisen T.L., Sukhodolets K.E., Pfeffer S., et al. Cellular cofactors affecting hepatitis C virus infection and replication. Proc Natl Acad Sci USA 104 (2007) 12884-12889
61. Watashi K., Ishii N., Hijikata M., Inoue D., Murata T., Miyanari Y., et al. Cyclophilin B is a functional regulator of hepatitis C virus RNA polymerase. Mol Cell 19 (2005) 111-122
62. Nakagawa M., Sakamoto N., Tanabe Y., Koyama T., Itsui Y., Takeda Y., et al. Suppression of hepatitis C virus replication by cyclosporin a is mediated by blockade of cyclophilins. Gastroenterology 129 (2005) 1031-1041
63. Pileri P., Uematsu Y., Campagnoli S., Galli G., Falugi F., Petracca R., et al. Binding of hepatitis C virus to CD81. Science 5390 (1998) 938-941
64. McKeating J.A., Zhang L.Q., Logvinoff C., Flint M., Zhang J., Yu J., et al. Diverse hepatitis C virus glycoproteins mediate viral infection in a CD81-dependent manner. J Virol 78 (2004) 8496-8505
65. Zeisel M.B., Koutsoudakis G., Schnober E.K., Haberstroh A., Blum H.E., Cosset F.L., et al. 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 (2007) 1722-1731
66. Evans M.J., von Hahn T., Tscherne D.M., Syder A.J., Panis M., Wölk B., et al. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446 (2007) 801-805
67. Ploss A., Evans M.J., Gaysinskaya V.A., Panis M., You H., de Jong Y.P., et al. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457 (2009) 882-886
68. Rosa D., Saletti G., De Gregorio E., Zorat F., Comar C., D'Oro U., et al. Activation of naïve B lymphocytes via CD81, a pathogenetic mechanism for hepatitis C virus-associated B lymphocyte disorders. Proc Natl Acad Sci USA 102 (2005) 18544-185449
69. Quinn E.R., Chan C.H., Hadlock K.G., Foung S.K., Flint M., and Levy S. The B-cell receptor of a hepatitis C virus (HCV)-associated non-Hodgkin lymphoma binds the viral E2 envelope protein, implicating HCV in lymphomagenesis. Blood 98 (2001) 3745-3749
70. Lai M.E., Mazzoleni A.P., Argiolu F., De Virgilis S., Balestrieri A., Purcell R.H., et al. Hepatitis C virus in multiple episodes of acute hepatitis in polytransfused thalassaemic children. Lancet 343 (1994) 388-390
71. Prince A.M., Brotman B., Huima T., Pascual D., Jaffery M., and Inchauspé G. Immunity in hepatitis C infection. J Infect Dis 165 (1992) 438-443
72. Weiner A.J., Paliard X., Selby M.J., Medina-Selby A., Coit D., Nguyen S., et al. Intrahepatic genetic inoculation of hepatitis C virus RNA confers cross-protective immunity. J Virol 75 (2001) 7142-7148
73. Bassett S.E., Guerra B., Brasky K., Miskovsky E., Houghton M., Klimpel G.R., et al. Protective immune response to hepatitis C virus in chimpanzees rechallenged following clearance of primary infection. Hepatology 33 (2001) 1479-1487
74. Choo Q.L., Kuo G., Ralston R., Weiner A., Chien D., Van Nest G., et al. Vaccination of chimpanzees against infection by the hepatitis C virus. Proc Natl Acad Sci USA 91 (1994) 1294-1298
75. Houghton M., and Abrignani S. Prospects for a vaccine against the hepatitis C virus. Nature 436 (2005) 961-966
76. Stamataki Z., Coates S., Evans M.J., Wininger M., Crawford K., Dong C., et al. Hepatitis C virus envelope glycoprotein immunization of rodents elicits cross-reactive neutralizing antibodies. Vaccine (2007) 257773-257784
77. Folgori A., Capone S., Ruggeri L., Meola A., Sporeno E., Ercole B.B., et al. A T-cell HCV vaccine eliciting effective immunity against heterologous virus challenge in chimpanzees. Nat Med (2006) 12190-12197
78. Alter M.J. Epidemiology of hepatitis C virus infection. World J Gastroenterol 13 (2007) 2436-2441
79. Umemura T., Ichijo T., Yoshizawa K., Tanaka E., and Kiyosawa K. Epidemiology of hepatocellular carcinoma in Japan. J Gastroenterol. 44 (2009) 102-107
80. Crotta S., Stilla A., Wack A., D'Andrea A., Nuti S., D'Oro U., et al. Inhibition of natural killer cells through engagement of CD81 by the major hepatitis C virus envelope protein. J Exp Med 195 (2002) 35-41
81. Tseng C., and Klimpel G. Binding of the hepatitis C virus envelope protein E2 to CD81 inhibits natural killer functions. J Exp Med 195 (2002) 43-49
82. Loo Y.M., and Gale Jr. M. Viral regulation and evasion of the host response. Curr Top Microbiol Immunol 316 (2007) 295-313
83. Bowen D.G., and Walker C.M. Mutational escape from CD8+ T cell immunity: HCV evolution, from chimpanzees to man. J Exp Med 201 (2005) 1709-1714
84. Hijikata M., Shimizu Y.K., Kato H., Iwamoto A., Shih J.W., Alter H.J., et al. Equilibrium centrifugation studies of hepatitis C virus: evidence for circulating immune complexes. J Virol 67 (1993) 1953-1958
85. Timpe J.M., Stamataki Z., Jennings A., Hu K., Farquhar M.J., Harris H.J., et al. Hepatitis C virus cell-cell transmission in hepatoma cells in the presence of neutralizing antibodies. Hepatology 47 (2008) 17-24
86. Witteveldt J., Evans M.J., Bitzegeio J., Koutsoudakis G., Owsianka A.M., Angus A.G., et al. CD81 is dispensable for hepatitis C virus cell-to-cell transmission in hepatoma cells. J Gen Virol 90 (2009) 48-58
87. Crispe N. Mechanisms of self-tolerance. Immunol Today 9 (1988) 329-331
88. Moradpour D., Penin F., and Rice C.M. Replication of hepatitis C virus. Nat Rev Microbiol 5 (2007) 453-463