The chimpanzee model of hepatitis C virus infections

ILAR Journal

Volumn 42, Issue 2, 2001, Pages 117-126

  Lanford, Robert E ^a   Bigger, Catherine ^a   Bassett, Suzanne ^b   Klimpel, Gary ^b  

^a SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

Author keywords

DNA microarray; HCV; Hepatitis C virus; Pan troglodytes; T cell

Indexed keywords

VIRUS DNA;

ANIMAL; DISEASE COURSE; DISEASE MODEL; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETICS; HEPATITIS C VIRUS; HUMAN; LIVER; PAN TROGLODYTES; PATHOGENICITY; PATHOLOGY; REVIEW; T LYMPHOCYTE; VIROLOGY; VIRUS REPLICATION;

ANIMALS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DNA, VIRAL; GENE EXPRESSION REGULATION; HEPACIVIRUS; HUMANS; LIVER; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PAN TROGLODYTES; T-LYMPHOCYTES; VIRUS REPLICATION;

EID: 0035235411     PISSN: 10842020     EISSN: None     Source Type: Journal    
DOI: 10.1093/ilar.42.2.117     Document Type: Article

References (89)

1. Ahmed A, Keeffe EB. 1999. Treatment strategies for chronic hepatitis C: Update since the 1997 National Institutes of Health Consensus Development Conference. J Gastroenterol Hepatol 14:S12-S18.
2. Alter HJ. 1995. To C or not to C: These are the questions. J Am Soc Hematol 85:1681-1695.
3. Alter MJ, Kruszon-Moran D, Nainan OV, McQuillan GM, Gao FX, Moyer LA, Kaslow RA, Margolis HS. 1999. The prevalence of hepatitis C virus infection in the United States, 1988 through 1994. N Engl J Med 341:556-562.
4. Anonymous. 1997. Hepatitis C: Global prevalence. Wkly Epidemiol Rec 72:341-344.
5. Arber N, Konikoff FM, Moshkowitz M, Baratz M, Hallak A, Santo M, Halpern Z, Weiss H, Gilat T. 1994. Increased serum iron and iron saturation without liver iron accumulation distinguish chronic hepatitis C virus from other chronic liver diseases. Dig Dis Sci 39:2656-2659.
6. Bacon BR, Rebholz AE, Fried M, DiBisceglie AM. 1993. Beneficial effect of iron reduction therapy in patients with chronic hepatitis C who failed to respond to interferon-alpha (Abstract). Hepatology 18:90A.
7. Barrett S, Ryan E, Crowe J. 1999. Association of the HLA-DRB1*01 allele with spontaneous viral clearance in an Irish cohort infected with hepatitis C virus via contaminated anti-D immunoglobulin. J Hepatol 30:979-983.
8. Bassett SE, Brasky KM, Lanford RE. 1998. Analysis of hepatitis C virus-inoculated chimpanzees reveals unexpected clinical profiles. J Virol 72:2589-2599.
9. Bassett SE, DiBisceglie AM, Bacon BR, Sharp RM, Govindarajan S, Hubbard GB, Brasky KM, Lanford RE. 1999a. Effects of iron loading on pathogenicity in hepatitis C virus-infected chimpanzees. Hepatology 29:1884-1892.
10. Bassett SE, Thomas DL, Brasky KM, Lanford RE. 1999b. Viral persistence, antibody to El and E2, and hypervariable region 1 sequence stability in hepatitis C virus-inoculated chimpanzees. J Virol 73:1118-1126.
11. Beard MR, Abell G, Honda M, Carroll A, Gartland M, Clarke B, Suzuki K, Lanford R, Sangar DV, Lemon SM. 1999. An infectious molecular clone of a Japanese genotype Ib hepatitis C virus. Hepatology 30:316-324.
12. Bertoni R, Sette A, Sidney J, Guidotti LG, Shapiro M, Purcell R, Chisari FV. 1998. Human class I supertypes and CTL repertoires extend to chimpanzees. J Immunol 161:4447-4455.
13. Blight KJ, Rice CM. 1997. Secondary structure determination of the conserved 98-base sequence at the 3′ terminus of hepatitis C virus genome RNA. J Virol 71:7345-7352.
14. Bonkovsky H, Banner BF, Rothman AL. 1997. Iron and chronic viral hepatitis. Hepatology 25:759-768.
15. Bronowicki JP, Vetter D, Uhl G, Hudziak H, Uhrlacher A, Vetter JM, Doffoel M. 1997. Lymphocyte reactivity to hepatitis C virus (HCV) antigens shows evidence for exposure to HCV in HCV-seronegative spouses of HCV- infected patients. J Infect Dis 176:518-522.
16. Bukh J, Apgar CL, Engle R, Govindarajan S, Hegerich PA, Tellier R, Wong DC, Elkins R, Ke w MC. 1998. Experimental infection of chimpanzees with hepatitis C virus of genotype 5a: Genetic analysis of the virus and generation of a standardized challenge pool. J Infect Dis 178:1193-1197.
17. Chang KM, Rehermann B, McHutchison JG, Pasquinelli C, Southwood S, Sette A, Chisari FV. 1997. Immunological significance of cytotoxic T lymphocyte epitope variants in patients chronically infected by the hepatitis C virus. J Clin Invest 100:2376-2385.
18. Chang YE, Laimins LA. 2000. Microarray analysis identifies interferon-inducible genes and Stat-1 as major transcriptional targets of human papillomavirus type 31. J Virol 74:4174-4182.
19. Choo Q-L, Kuo G, Ralston R, Weiner A, Chien D, Van Nest G, Han J, Berger K, Thudium K, Kuo C, Kansopon J, McFarland J, Tabrizi A, Ching K, Moss B, Cummins LB, Houghton M, Muchmore E. 1994. Vaccination of chimpanzees against infection by the hepatitis C virus. Proc Natl Acad Sci U S A 91:1294-1298.
20. Choo Q-L, Kuo G, Weiner AJ, Overby LJ, Bradley DW, Houghton M. 1989. Isolation of a cDNA clone derived from blood-borne non-A, non-B viral hepatitis genome. Science 244:359-362.
21. Cooper S, Erickson AL, Adams EJ, Kansopon J, Weiner AJ, Chien DY, Houghton M, Parham P, Walker CM. 1999. Analysis of a successful immune response against hepatitis C virus. Immunity 10:439-449.
22. Di Bisceglie AM, Axiotis CA, Hoofnagle JH, Bacon BR. 1992. Measurements of iron status in patients with chronic hepatitis. Gastroenterology 102:2108-2113.
23. Diepolder HM, Gerlach J, Zachoval R, Hoffmann RM, Jung M-C, Wierenga EA, Scholz S, Santantonio T, Houghton M, Southwood S, Sette A, Pape GR. 1997. Immunodominant CD4+ T-Cell epitope within nonstructural protein 3 in acute hepatitis C virus infection. J Virol 71:6011-6019.
24. Diepolder HM, Zachoval R, Hoffmann RM, Jung MC, Gerlach T, Pape GR. 1996. The role of hepatitis C virus specific CD4+ T lymphocytes in acute and chronic hepatitis C. J Mol Med 74:583-588.
25. Eckels DD, Zhou H, Bian TH, Wang H. 1999. Identification of antigenic escape variants in an immunodominant epitope of hepatitis C virus. Int Immunol 11:577-583.
26. Erickson AL, Houghton M, Choo Q-L, Weiner AJ, Ralston R, Muchmore E. 1993. Hepatitis C virus-specific CTL responses in the liver of chimpanzees with acute and chronic hepatitis C. J Immunol 151:4189-4199.
27. Farci P, Alter HJ, Wong DC, Miller RH, Govindarajan S, Engle R, Shapiro M, Purcell RH. 1994. Prevention of hepatitis C virus infection in chimpanzees after antibody-mediated in vitro neutralization. Proc Natl Acad Sci U S A 91:7792-7796.
28. Farci P, Shimoda A, Wong D, Cabezon T, De Gioannis D, Strazzera A, Shimizu Y, Shapiro M, Alter HJ, Purcell RH. 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.
29. Fong TL, Han SH, Tsai NC, Morgan TR, Mizokami M, Qian DJ, Phan C, Goad K, Redeker AG. 1998. A pilot randomized, controlled trial of the effect of iron depletion on long-term response to (-interferon in patients with chronic hepatitis C. J Hepatol 28:369-374.
30. Forns X, Purcell RH, Bukh J. 1999. Quasispecies in viral persistence and pathogenesis of hepatitis C virus. Trends Microbiol 7:402-410.
31. Geiss GK, Bumgamer RE, An MC, Agy MB, van 't Wout, Hammersmark E, Carter VS, Upchurch D, Mullins JI, Katze MG. 2000. Large-scale monitoring of host cell gene expression during HIV-I infection using cDNA microarrays. Virology 266:8-16.
32. Giuggio VM, Bonkovsky HL, Smith J, Rothman AL. 1998. Inefficient recognition of autologous viral sequences by intrahepatic hepatitis C virus-specific cytotoxic T lymphocytes in chronically infected subjects. Virology 251:132-140.
33. +T cells with viral clearance in acute hepatitis C. J Infect Dis 181:1528-1536.
34. Guyader D, Boucher E, André P, Even C, Cottereau J, Bianchi A, Gasser P, Mendier MH, Deugnier Y, Brissot P. 1999. A pilot study of iron depletion as adjuvant therapy in chronic hepatitis C patients not responding to interferon. Am J Gastroenterol 94:1696-1698.
35. Haque S, Chandra B, Gerber MA, Lok ASF. 1996. Iron overload in patients with chronic hepatitis C: A clinicopathologic study. Hum Pathol 27:1277-1281.
36. Hayashi H, Takikawa T, Nishimura N, Yano M, Isomura T, and Sakamoto N. 1994. Improvement of serum aminotransferase levels after phlebotomy in patients with chronic active hepatitis C and excess hepatic iron. Am J Gastroenterol 89:986-988.
37. Henkler F, Waseem N, Golding MHC, Alison MR, Koshy R. 1995. Mutant p53 but not hepatitis B virus X protein is present in hepatitis B virus-related human hepatocellular carcinoma. Cancer Res 55:6084-6091.
38. Hiroishi K, Kita H, Kojima M, Okamoto H, Moriyama T, Kaneko T, Ishikawa T, Ohnishi S, Aikawa T, Tanaka N, Yazaki Y, Mitamura K, Imawari M. 1997. Cytotoxic T lymphocyte response and viral load in hepatitis C virus infection. Hepatology 25:705-712.
39. Honda M, Beard MR, Ping LH, Lemon SM. 1999. A phylogenetically conserved stem-loop structure at the 5′ border of the internal ribosome entry site of hepatitis C virus is required for cap-independent viral translation. J Virol 73:1165-1174.
40. Hong Z, Beaudet-Miller M, Lanford RE, Guerra B, Wright-Minogue J, Skelton A, Baroudy BM, Reyes GR, Lau JY. 1999. Generation of transmissible hepatitis C virions from a molecular clone in chimpanzees. Virology 256:36-44.
41. Hoofnagle JH. 1997. Hepatitis C: The clinical spectrum of disease. Hepatology 26(Suppl):15S-20S.
42. Houghton M, Selby M, Weiner A, Choo QL. 1994. Hepatitis C virus: structure, protein products and processing of the polyprotein precursor. Curr Stud Hematol Blood Transfus 61:1-11.
43. Houghton M, Weiner A, Han J, Kuo G, Choo Q-L. 1991. Molecular biology of the hepatitis C viruses: Implications for diagnosis, development and control of disease. Hepatology 14:381-388.
44. Ikura Y, Morimoto H, Johmura H, Fukui M, Sakurai M. 1996. Relationship between hepatic iron deposits and response to interferon in chronic hepatitis C. Am J Gastroenterol 91:1367-1373.
45. Kageyama F, Kobayashi Y, Murohisa G, Shimizu E, Suzuki F, Kikuyama M, Souda K, Kawasaki T, Nakamura H. 1998. Failure to respond to interferon-α 2a therapy is associated with increased hepatic iron levels in patients with chronic hepatitis C. Biol Trace Elem Res 64:185-196.
46. Kato N, Ootsuyama Y, Tanaka T, Nakagawa M, Nakazawa T, Muraiso K, Ohkoshi S, Hijikata M, Shimotohno K. 1992. Marked sequence diversity in the putative envelope proteins of hepatitis C viruses. Virus Res 22:107-123.
47. Kato N, Sekiya H, Ootsuyama Y, Nakazawa T, Hijikata M, Ohkoshi S, 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.
48. Kolykhalov AA, Agapov EV, Blight KJ, Mihalik K, Feinstone SM, Rice CM. 1997. Transmission of hepatitis C by intrahepatic inoculation with transcribed RNA. Science 277:570-574.
49. Kolykhalov AA, Feinstone SM, Rice CM. 1996. Identification of a highly conserved sequence element at the 3′ terminus of hepatitis C virus genome RNA. J Virol 70:3363-3371.
50. Kolykhalov AA, Mihalik K, Feinstone SM, Rice CM. 2000. Hepatitis C virus-encoded enzymatic activities and conserved RNA elements in the 3′ nontranslated region are essential for virus replication in vivo. J Virol 74:2046-2051.
51. Kowalski H, Erickson AL, Cooper S, Domena JD, Parham P, Walker CM. 1996. Patr-A and B, the orthologues of HLA-A and B, present hepatitis C virus epitopes to CD8+ cytotoxic T cells from two chronically infected chimpanzees. J Exp Med 183:1761-1775.
52. Koziel MJ, Dudley D, Afdhal N, Grakoui A, Rice CM, Choo Q-L, Houghton M, Walker BD. 1993. Hepatitis C virus (HCV)-specific cytotoxic T lymphocytes recognize epitopes in the core and envelope proteins of HCV. J Virol 67:7522-7532.
53. Lanford RE, Lee H, Chavez D, Guerra B, Brasky KM. 2001. An infectious clone of the HCV-1 prototype sequence. J Gen Virol (In Press).
54. Koziel MJ, Wong DKH, Dudley D, Houghton M, Walker BD. 1997. Hepatitis C virus-specific cytolytic T lymphocyte and T helper cell responses in seronegative persons. J Infect Dis 176:859-866.
55. Krawczynski K, Alter MJ, Tankersley DL, Beach M, Robertson BH, Lambert S, Kuo G, Spelbring JE, Meeks E, Sinha S, Carson DA. 1996. Effect of immune globulin on the prevention of experimental hepatitis C virus infection. J Infect Dis 173:822-828.
56. Lechner F, Wong DK, Dunbar PR, Chapman R, Chung RT, Dohrenwend P, Robbins G, Phillips R, Klenerman P, Walker BD. 2000. Analysis of successful immune responses in persons infected with hepatitis C virus. J Exp Med 191:1499-1512.
57. Lohmann V, Körner F, Koch JO, Herian U, Theilmann L, Bartenschlager R. 1999. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285:110-113.
58. Missale G, Bertoni R, Lamonaca V, Valli A, Massari M, Mori C, Rumi MG, Houghton M, Fiaccadori F, Ferrari C. 1996. Different clinical behaviors of acute hepatitis C virus infection are associated with different vigor of the anti-viral cell-mediated immune response. J Clin Invest 98:706-714.
59. Muchmore E, Popper H, Peterson DA, Miller MF, Lieberman HM. 1988. Non-A, non-B hepatitis-related hepatocellular carcinoma in a chimpanzee. J Med Primatol 17:235-246.
60. Nelson DR, Marousis CG, Davis GL, Rice CM, Wong J, Houghton M, Lau JYN. 1997. The role of hepatitis C virus-specific cytotoxic T lymphocytes in chronic hepatitis C. J Immunol 158:1473-1481.
61. NIH [National Institutes of Health]. 1997. National Institutes of Health Consensus Development Conference Panel statement: Management of hepatitis C. Hepatology 26(Suppl):2S-10S.
62. Okamoto H, Kojima M, Okada S-I, Yoshizawa H, Iizuka H, Tanaka T, Muchmore EE, Peterson DA, Ito Y, Mishiro S. 1992. Genetic drift of hepatitis C virus during an 8.2-year infection in a chimpanzee: Variability and stability. Virology 190:894-899.
63. Olynyk JK, Reddy KR, Di Bisceglie AM, Jeffers LJ, Parker TI, Radick JL, Schiff ER, Bacon BR. 1995. Hepatic iron concentration as a predictor of response to interferon alfa therapy in chronic hepatitis C. Gastroenterology 108:1104-1109.
64. Prince AM, Brotman B. 1994. The biology of hepatitis C virus infection. Curr Stud Hematol Blood Transfus 61:195-207.
65. Ray SC, Mao Q, Lanford RE, Bassett S, Laeyendecker O, Wang YM, Thomas DL. 2000. Hypervariable region 1 sequence stability during hepatitis C virus replication in chimpanzees. J Virol 74:3058-3066.
66. Ray SC, Wang YM, Laeyendecker O, Ticehurst JR, Villano SA, Thomas DL. 1999. Acute hepatitis C virus structural gene sequences as predictors of persistent viremia: Hypervariable region 1 as a decoy. J Virol 73:2938-2946.
67. Reed KE, Rice CM. 1998. Molecular characterization of hepatitis C virus. Curr Stud Hematol Blood Transfus 1-37.
68. Rehermann B, Chang KM, McHutchison J, Kokka F, Houghton M, Rice CM, Chisari FV. 1996. Differential cytotoxic T-lymphocyte responsiveness to the hepatitis B and C viruses in chronically infected patients. J Virol 70:7092-7102.
69. Rehermann B, Chisari FV. 2000. Cell mediated immune response to the hepatitis C virus. Curr Top Microbiol Immunol 242:299-325.
70. Riggio O, Montagnese F, Fiore P, Folino S, Giambartolomei S, Gandin C, Merli M, Quinti I, Violante N, Caroli S, Senofonte O, Capocaccia L. 1997. Iron overload in patients with chronic viral hepatitis: How common is it? Am J Gastroenterol 92:1298-1301.
71. Robertson B, Myers G, Howard C, BrettinT, Bukh J, Gaschen B, Gojobori T, Maertens G, Mizokami M, Nainan O, Netesov S, Nishioka K, Shin, Simmonds P, Smith D, Stuyver L, Weiner A. 1998. Classification, nomenclature, and database development for hepatitis C virus (HCV) and related viruses: Proposals for standardization. International Committee on Virus Taxonomy. Arch Virol 143:2493-2503.
72. Scognamiglio P, Accapezzato D, Casciaro MA, Cacciani A, Artini M, Bruno G, Chircu ML, Sidney J, Southwood S, Abrignani S, Sette A, Barnaba V. 1999. Presence of effector CD8+ T cells in hepatitis C virus-exposed healthy seronegative donors. J Immunol 162:6681-6689.
73. Seeff LB, Buskell-Bales Z, Wright EC, Durako SJ, Alter HJ, Iber FL, Hollinger FB, Gitnick G, Knodell RG, Perrillo RP, Stevens CE, Hollingsworth CG. 1992. Long-term mortality after tranfusion-associated non-A, non-B hepatitis. N Engl J Med 327:1906-1911.
74. Seeff LB, Miller RN, Rabkin CS, Buskell-Bales Z, Straley-Eason KD, Smoak BL, Johnson LD, Lee SR, Kaplan EL. 2000.45-year follow-up of hepatitis C virus infection in healthy young adults. Ann Int Med 132:105-111.
75. Takaki A, Wiese M, Maertens G, Depla E, Seifert U, Liebetrau A, Miller JL, Manns MP, Rehermann B. 2000. Cellular immune responses persist and humoral responses decrease two decades after recovery from a single-source outbreak of hepatitis C. Nat Med 6:578-582.
76. Tanaka T, Kato N, Cho MJ, Shimotohno K. 1995. A novel sequence found at the 3′ terminus of hepatitis C virus genome. Biochem Biophys Res Commun 215:744-749.
77. Tanaka T, Kato N, Cho MJ, Sugiyama K, Shimotohno K. 1996. Structure of the 3′ terminus of the hepatitis C virus genome. J Virol 70:3307-3312.
78. Taniguchi S, Okamoto H, Sakamoto M, Kojima M, Tsuda F, Tanaka T, Munekata E, Muchmore EE, Peterson DA, Mishiro S. 1993. A structurally flexible and antigenically variable N-terminal domain of the hepatitis C virus E2/NS1 protein: Implication for an escape from antibody. Virology 195:297-301.
79. Tsai NCS, Zuckerman E, Han SH, Goad K, Redeker AG, Fong TL. 1997a. Effect of iron depletion on long-term response to interferon-α in patients with chronic hepatitis C who previously did not respond to interferon therapy. Am J Gastroenterol 92:1831-1834.
80. Tsai SL, Liaw YF, Chen MH, Huang CY, Kuo GC. 1997b. Detection of type 2-like T-helper cells in hepatitis C virus infection: Implications for hepatitis C virus chronicity. Hepatology 25:449-458.
81. Van Thiel DH, Friedlander L, Faginoli S, Wright HI, Irish W, Gavaler JS. 1994. Response to interferon alpha-therapy is influenced by the iron content of the liver. J Hepatol 20:410-415.
82. Walker CM. 1997. Comparative features of hepatitis C virus infection in humans and chimpanzees. Springer Semin Immunopathol 19:85-98.
83. Weiner A, Erickson AL, Kansopon J, Crawford K, Muchmore E, Hughes AL, Houghton M, Walker CM. 1995. Persistent hepatitis C virus infection in a chimpanzee is associated with emergence of a cytotoxic T lymphocyte escape variant. Proc Natl Acad SCi U S A 92:2755-2759.
84. Weiner AJ, Brauer MJ, Rosenblatt J, Richman KH, Tung J, Crawford K, Bonino F, Saracco G, Choo QL, Houghton M, Han JH. 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.
85. Weiner AJ, Geysen M, Christopherson C, Hall JE, Mason TJ, Saracco G, Bonino F, Crawford K, Marion CD, Crawford KA, Brunetto M, Barr PJ, Miyamura T, McHutchinson J, Houghton M. 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.
86. Wong DK, Dudley DD, Afdhal NH, Dienstag J, Rice CM, Wang LP, Houghton M, Walker BD, Koziel MJ. 1998. Liver-derived CTL in hepatitis C virus infection: Breadth and specificity of responses in a cohort of persons with chronic infection. J Immunol 160:1479-1488.
87. Yanagi M, Purcell RH, Emerson SU, Bukh J. 1997. Transcripts from a single full-length cDNA clone of hepatitis C virus are infectious when directly transfected into the liver of a chimpanzee. Proc Natl Acad Sci U S A 94:8738-8743.
88. Yanagi M, St Claire M, Emerson SU, Purcell RH, Bukh J. 1999. In vivo analysis of the 3′ untranslated region of the hepatitis C virus after in vitro mutagenesis of an infectious cDNA clone. Proc Natl Acad Sci U S A 96:2291-2295.
89. Zhu H, Cong JP, Mamtora G, Gingeras T, Shenk T. 1998. Cellular gene expression altered by human cytomegalovirus: Global monitoring with oligonucleotide arrays. Proc Natl Acad Sci U S A 95:14470-14475.