Processing and functions of hepatitis C virus proteins

Intervirology

Volumn 42, Issue 2-3, 1999, Pages 145-152

  Suzuki, Ryosuke ^a   Suzuki, Tetsuro ^a   Ishii, Koji ^a   Matsuura, Yoshiharu ^a   Miyamura, Tatsuo ^a  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

Hepatitis C virus; Processing; Viral proteins

Indexed keywords

CAPSID PROTEIN; GLYCOPROTEIN; RNA HELICASE; VIRUS PROTEIN; VIRUS RNA;

CELL CULTURE; ENZYME ACTIVITY; HEPATITIS C; HEPATITIS C VIRUS; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW;

GENOME, VIRAL; HEPACIVIRUS; HUMANS; VIRAL NONSTRUCTURAL PROTEINS; VIRAL PROTEINS;

EID: 0032876872     PISSN: 03005526     EISSN: None     Source Type: Journal    
DOI: 10.1159/000024973     Document Type: Review

References (84)

1. Saito I, Miyamura T, Ohbayashi A, Harada H, Katayama T, Kikuchi S, Watanabe Y, Koi S, Onji M, Ohta Y, Choo Q-L, Houghton M, Kuo G: Hepatitis C virus infection is associated with the development of hepatocellular carcinoma. Proc Natl Acad Sci USA 1990;87:6547-6549.
2. Chamberlain RW, Adams N, Saeed AA, Simmonds P, Elliott RM: Complete nucleotide sequence of a type 4 hepatitis C virus variant, the predominant genotype in the Middle East. J Gen Virol 1997;78:1341-1347.
3. Tsukiyama-Kohara K, Iizuka N, Kohara M, Nomoto A: Internal ribosome entry site within hepatitis C virus RNA. J Virol 1992;66:1476-1483.
4. Ali N, Siddiqui A: Interaction of polypyrimidinc tract-binding protein with the 5′ noncoding region of the hepatitis C virus RNA genome and its functional requirement in internal initiation of translation. J Virol 1995;69:6367-6375.
5. Ali N, Siddiqui A: The La antigen binds 5′ noncoding region of the hepatitis C virus RNA in the context of the initiator AUG codon and stimulates internal ribosome entry site-mediated translation. Proc Natl Acad Sci USA 1997;94:2249-2254.
6. Fukushi S, Kurihara C, Ishiyama N, Hoshino FB, Oya A, Katayama K: The sequence element of the internal ribosome entry site and a 25-kilodalton cellular protein contribute to efficient internal initiation of translation of hepatitis C virus RNA. J Virol 1997;71:1662-1666.
7. Hahm B, Kim YK, Kim JH, Kim TY, Jang SK: Heterogeneous nuclear ribonucleoprotein L interacts with the 3′ border of the internal ribosomal entry site of hepatitis C virus. J Virol 1998;72:8782-8788.
8. Kato N, Hijikata M, Ootsuyama Y, Nakagawa M, Ohkoshi S, Sugimura T, Shimotohno K: Molecular cloning of the human hepatitis C virus genome from Japanese patients with non-A, non-B hepatitis. Proc Natl Acad Sci USA 1990;87:9524-9528.
9. Han JH, Shyamala V, Richman KH, Brauer MJ, Irvine B, Urdea MS, Tekamp-Olson P, Kuo G, Choo Q-L, Houghton M: Characterization of the terminal regions of hepatitis C viral RNA: Identification of conserved sequences in the 5′ untranslated region and poly(A) tails at the 3′ end. Proc Natl Acad Sci USA 1991;88: 1711-1715.
10. Tanaka T, Kato N, Cho M-J, Shimotohno K: A novel sequence found at the 3′ terminus of hepatitis C virus genome. Biochem Biophys Res Commun 1995;215:744-749.
11. Blight KJ, Rice CM: Secondary structure determination of the conserved 98-base sequence at the 3′ terminus of hepatitis C virus genome RNA. J Virol 1997;71:7345-7352.
12. Tsuchihara K, Tanaka T, Hijikata M, Kuge S, Toyoda H, Nomoto A, Yamamoto N, Shimotohno K: Specific interaction of polypyrimidine tract-binding protein with the extreme 3'-terminal structure of the hepatitis C virus genome, the 3′ X. J Virol 1997;71:6720-6726.
13. Ito T, Lai MMC: Determination of the secondary structure of and cellular protein binding to the 3'-untranslated region of the hepatitis C virus RNA genome. J Virol 1997;71:8698-8706.
14. Ito T, Tahara SM, Lai MMC: The 3'-untranslated region of the hepatitis C virus RNA enhances translation from an internal ribosomal entry site. J Virol 1998;72:8789-8796.
15. Harada S, Watanabe Y, Takeuchi K, Suzuki T, Katayama T, Takebe Y, Saito I, Miyamura T: Expression of processed core protein of hepatitis C virus in mammalian cells. J Virol 1991; 65:3015-3021.
16. Santolini E, Migliaccio G, La Monica N: Biosynthesis and biochemical properties of the hepatitis C virus core protein. J Virol 1994;68: 3631-3641.
17. Lo S-Y, Selby M, Tong M, Ou J-H: Comparative studies of the core gene products of two different hepatitis C virus isolates: Two alternative forms determined by a single amino acid substitution. Virology 1994;199:124-131.
18. Liu Q, Tackney C, Bhat RA, Prince AM, Zhang P: Regulated processing of hepatitis C virus core protein is linked to subcellular localization. J Virol 1997;71:657-662.
19. Yasui K, Wakita T, Tsukiyama-Kohara K, Funahashi S-I, Ichikawa M, Kajita T, Moradpour D, Wands JR, Kohara M: The native form and maturation process of hepatitis C virus core protein. J Virol 1998;72:6048-6055.
20. Suzuki R, Matsuura Y, Suzuki T, Ando A, Chiba J, Harada S, Saito I, Miyamura T: Nuclear localization of the truncated hepatitis C virus core protein with its hydrophobic C terminus deleted. J Gen Virol 1995;76:53-61.
21. Chang SC, Yen J-H, Kang H-Y, Jang M-H, Chang M-F: Nuclear localization signals in the core protein of hepatitis C virus. Biochem Biophys Res Commun 1994;205:1284-1290.
22. Lo S-Y, Selby MJ, Ou J-H: Interaction between hepatitis C virus core protein and E1 envelope protein. J Virol 1996;70:5177-5182.
23. Barba G, Harper F, Harada T, Kohara M, Goulinet S, Matsuura Y, Eder G, Schaff Z, Chapman MJ, Miyamura T, Bréchot C: Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc Natl Acad Sci USA 1997;94: 1200-1205.
24. Matsumoto M, Hsieh T-Y, Zhu N, VanArsdale T, Hwang SB, Jeng K-S, Gorbalenya AE, Lo S-Y, Ou J-H, Ware CF, Lai MMC: Hepatitis C virus core protein interacts with the cytoplasmic tail of lymphotoxin-β receptor. J Virol 1997;71:1301-1309.
25. Chen C-M, You L-R, Hwang L-H, Lee Y-HW: Direct interaction of hepatitis C virus core protein with the cellular lymphotoxin-β receptor modulates the signal pathway of the lymphotoxin-β receptor. J Virol 1997;71:9417-9426.
26. Zhu N, Khoshnan A, Schneider R, Matsumoto M, Dennert G, Ware C, Lai MMC: Hepatitis C virus core protein binds to the cytoplasmic domain of tumor necrosis factor (TNF) receptor 1 and enhances TNF-induced apoptosis. J Virol 1998;72:3691-3697.
27. Moriya K, Yotsuyanagi H, Shintani Y, Fujie H, Ishibashi K, Matsuura Y, Miyamura T, Koike K: Hepatitis C virus core protein induces hepatic steatosis in transgenic mice. J Gen Virol 1997;78:1527-1531.
28. Ray RB, Meyer K, Ray R: Suppression of apoptotic cell death by hepatitis C virus core protein. Virology 1996;226:176-182.
29. Ray RB, Meyer K, Steele R, Shrivastava A, Aggarwal BB, Ray R: Inhibition of tumor necrosis factor (TNF-α)-mediated apoptosis by hepatitis C virus core protein. J Biol Chem 1998;273:2256-2259.
30. Ruggieri A, Harada T, Matsuura Y, Miyamura T: Sensitization to Fas-mediated apoptosis by hepatitis C virus core protein. Virology 1997; 229:68-76.
31. Shih C-M, Lo SJ, Miyamura T, Chen S-Y, Lee Y-HW: Suppression of hepatitis B virus expression and replication by hepatitis C virus core protein in HuH-7 cells. J Virol 1993;67:5823-5832.
32. Kim DW, Suzuki R, Harada T, Saito I, Miyamura T: Trans-suppression of gene expression by hepatitis C viral core protein. Jpn J Med Sci Biol 1994;47:211-220.
33. Ray RB, Lagging LM, Meyer K, Steele R, Ray R: Transcriptional regulation of cellular and viral promoters by the hepatitis C virus core protein. Virus Res 1995;37:209-220.
34. Ray RB, Steele R, Meyer K, Ray R: Transcriptional repression of p53 promoter by hepatitis C virus core protein. J Biol Chem 1997;272: 10983-10986.
35. Hsieh T-Y, Matsumoto M, Chou H-C, Schneider R, Hwang SB, Lee AS, Lai MMC: Hepatitis C virus core protein interacts with heterogeneous nuclear ribonucleoprotein K. J Biol Chem 1998;273:17651-17659.
36. Moriya K, Fujie H, Shintani Y, Yotsuyanagi H, Tsutsuini T, Ishibashi K, Matsuura Y, Kimura S, Miyamura T, Koike K: The core protein of hepatitis C virus induces hepatocellular carcinoma in transgenic mice. Nat Med 1998;4: 1065-1067.
37. Ray RB, Lagging LM, Meyer K, Ray R: Hepatitis C virus core protein cooperates with ras and transforms primary rat embryo fibroblasts to tumorigenic phenotype. J Virol 1996;70:4438-4443.
38. Miyamura T, Matsuura Y: Structural proteins of hepatitis C virus. Trends Microbiol 1993;1: 229-231.
39. Lin C, Lindenbach BD, Prágai BM, McCourt DW, Rice CM: Processing in the hepatitis C virus E2-NS2 region: Identification of p7 and two distinct E2-specific products with different C termini. J Virol 1994;68:5063-5073.
40. Mizushima H, Hijikata M, Asabe S-I, Hirota M, Kimura K, Shimotohno K: Two hepatitis C virus glycoprotein E2 products with different C termini. J Virol 1994;68:6215-6222.
41. Matsuura Y, Suzuki T, Suzuki R, Sato M, Aizaki H, Saito I, Miyamura T: Processing of E1 and E2 glycoproteins of hepatitis C virus expressed in mammalian and insect cells. Virology 1994;205:141-150.
42. Selby MJ, Glazer E, Masiarz F, Houghton M: Complex processing and protein:protein interactions in the E2:NS2 region of HCV. Virology 1994;204:114-122.
43. Baumert TF, Ito S, Wong DT, Liang TJ: Hepatitis C virus structural proteins assemble into viruslike particles in insect cells. J Virol 1998; 72:3827-3836.
44. Kato K, Ootsuyama Y, Ohkoshi S, Nakazawa T, Sekiya H, Hijikata M, Shimotohno K: Characterization of hypervariable regions in the putative envelope protein of hepatitis C virus. Biochem Biophys Res Commun 1992;189: 119-127.
45. Weiner AJ, Brauer MJ, Rosenblatt J, Richman KH, Tung J, Crawford K, Bonino F, Saracco G, Choo Q-L, Houghton M, Han JH: 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 1991;180:842-848.
46. Zibert A, Schreier E, Roggendorf M: Antibodies in human sera specific to hypervariable region 1 of hepatitis C virus can block viral attachment. Virology 1995;208:653-661.
47. Shimizu YK, Igarashi H, Kiyohara T, Cabezon T, Farci P, Purcell RH, Yoshikura H: A hyperimmune serum against a synthetic peptide corresponding to the hypervariable region 1 of hepatitis C virus can prevent viral infection in cell cultures. Virology 1996;223:409-412.
48. Farci P, Shimoda A, Wong D, Cabezon T, De Gioannis D, Strazzera A, Shimizu Y, Shapiro M, Alter HJ, Pureell RH: Prevention of hepatitis C virus infection m chimpanzees by hyperimmune serum against the hypervariable region 1 of the envelope 2 protein. Proc Natl Acad Sci USA 1996;93:15394-15399.
49. Rosa D, Campagnoli S, Moretto C, Guenzi E, Cousens L, Chin M, Dong C, Weiner AJ, Lau JYN, Choo Q-L, Chien D, Pileri P, Houghton M, Abrignani S: A quantitative test to estimate neutralizing antibodies to the hepatitis C virus: Cytofluorimetric assessment of envelope glycoprotein 2 binding to target cells. Proc Natl Acad Sci USA 1996;93:1759-1763.
50. Ishii K, Rosa D, Watanabe Y, Katayama T, Harada H, Wyatt C, Kiyosawa K, Aizaki H, Matsuura Y, Houghton M, Abriguani S, Miyamura T: High titers of antibodies inhibiting the binding of envelope to human cells correlate with natural resolution of chronic hepatitis C. Hepatology 1998;28:1117-1120.
51. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, Petracca R, Weiner AJ, Houghton M, Rosa D, Grandi G, Abrignani S: Binding of hepatitis C virus to CD81. Science 1998;282: 938-941.
52. Koike K, Moriya K, Ishibashi K, Yotsuyanagi H, Shintani Y, Fujie H, Kurokawa K, Matsuura Y, Miyamura T: Sialadenitis histologically resembling Sjögren syndrome in mice transgenic for hepatitis C virus envelope genes. Proc Natl Acad Sci USA 1997;94:233-236.
53. Santolini E, Pacini L, Fipaldini C, Migliaccio G, La Monica N: The NS2 protein of hepatitis C virus is a transmembrane polypeptide. J Virol 1995;69:7461-7471.
54. Hijikata M, Mizushima H, Akagi T, Mori S, Kakiuchi N, Kato N, Tanaka T, Kimura K, Shimotohno K: Two distinct proteinase activities required for the processing of a putative nonstructural precursor protein of hepatitis C virus. J Virol 1993;67:4665-4675.
55. Grakoui A, McCourt DW, Wychowski C, Feinstone SM, Rice CM: A second hepatitis C virus-encoded protease. Proc Natl Acad Sci USA 1993;90:10583-10587.
56. Bartenschlager R, Ahlborn-Laake L, Mous J, Jacobsen H: Nonstructural protein 3 of the hepatitis C virus encodes a serine-type proteinase required for cleavage at the NS3/4 and NS4/5 junctions. J Virol 1993;67:3835-3844.
57. Eckart MR, Selby M, Masiarz F, Lee C, Berger K, Crawford K, Kuo C, Kuo G, Houghton M, Choo Q-L: 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 1993;192:399-406.
58. Grakoui A, McCourt DW, Wychowski C, Feinstone SM, Rice CM: Characterization of the hepatitis C virus-encoded serine proteinase: Determination of proteinase-dependent polyprotein cleavage sites. J Virol 1993;67:2832-2843.
59. Tomei L, Failla C, Santolini E, De Francesco R, La Monica N: NS3 is a serine protease required for processing of hepatitis C virus polyprotein. J Virol 1993;67:4017-4026.
60. D'Souza EDA, O'Sullivan E, Amphlett EM, Rowlands DJ, Sanger DV, Clarke BE: Analysis of NS3-mediated processing of the hepatitis C virus non-structural region in vitro. J Gen Virol 1994;75:3469-3476.
61. Manabe S, Fuke I, Tanishita O, Kaji C, Gomi Y, Yoshida S, Mori C, Takamizawa A, Yoshida I, Okayama H: Production of nonstructural proteins of hepatitis C virus requires a putative viral protease encoded by NS3. Virology 1994; 198:636-644.
62. Shoji I, Suzuki T, Chieda S, Sato M, Harada T, Chiba T, Matsuura Y, Miyamura T: Proteolytic activity of NS3 serine proteinase of hepatitis C virus efficiently expressed in Escherichia coli. Hepatology 1995;22:1648-1655.
63. Suzuki T, Sato M, Chieda S, Shoji I, Harada T, Yamakawa Y, Watabe S, Matsuura Y, Miyamura T: In vivo and in vitro trans-cleavage activity of hepatitis C virus serine proteinase expressed by recombinant baculoviruses. J Gen Virol 1995;76:3021-3029.
64. Failla C, Tomei L, De Francesco R: Both NS3 and NS4A are required for proteolytic processing of hepatitis C virus nonstructural proteins. J Virol 1994;68:3753-3760.
65. Bartenschlager R, Ahlborn-Laake L, Mous J, Jacobsen H: Kinetic and structural analyses of hepatitis C virus polyprotein processing. J Virol 1994;68:5045-5055.
66. Koch JO, Lohmann V, Herian U, Bartenschlager R: In vitro studies on the activation of the hepatitis C virus NS3 proteinase by the NS4A cofactor. Virology 1996;221:54-66.
67. Shimizu Y, Yamaji K, Masuho Y, Yokota T, Inone H, Sudo K, Satoh S, Shimotohno K: Identification of the sequence on NS4A required for enhanced cleavage of the NS5A/5B site by hepatitis C virus NS3 protease. J Virol 1996;70:127-132.
68. Love RA, Parge HE, Wickersham JA, Hostomsky Z, Habuka N, Moomaw EW, Adachi T, Hostomska Z: The crystal structure of hepatitis C virus NS3 proteinase reveals a trypsin-like fold and a structural zinc binding site. Cell 1996;87:331-342.
69. Kim JL, Morgenstern KA, Lin C, Fox T, Dwyer MD, Landro JA, Chambers SP, Markland W, Lepre CA, O'Malley ET, Harbeson SL, Rice CM, Murcko MA, Caron PR, Thomson JA: Crystal structure of the hepatitis C virus NS3 protease domain complexed with a synthetic NS4A cofactor peptide. Cell 1996;87: 343-355.
70. Kanai A, Tanabe K, Kohara M: Poly(U) binding activity of hepatitis C virus NS3 protein, a putative RNA helicase. FEBS Lett 1995;376: 221-224.
71. Tai C-L, Chi W-K, Chen D-S, Hwang L-H: The helicase activity associated with hepatitis C virus nonstructural protein 3 (NS3). J Virol 1996;70:8477-8484.
72. Yao N, Hesson T, Cable M, Hong Z, Kwong AD, Le HV, Weber PC: Structure of the hepatitis C virus RNA helicase domain. Nat Struct Biol 1997;4:463-467.
73. Shoji I, Suzuki T, Sato M, Aizaki H, Chiba T, Matsuura Y, Miyamura T: Internal processing of hepatitis C virus NS3 protein. Virology 1999;254:315-323.
74. Asabe S-I, Tanji Y, Satoh S, Kaneko T, Kimura K, Shimotohno K: The N-terminal region of hepatitis C virus-encoded NS5A is important for NS4A-dependent phosphorylation. J Virol 1997;71:790-796.
75. Reed KE, Gorbalenya AE, Rice CM: The NS5A/NS5 proteins of viruses from three genera of the family Flaviviridae are phosphorylated by associated serine/threonine kinases. J Virol 1998;72:6199-6206.
76. Kaneko T, Tanji Y, Satoh S, Hijikata M, Asabe S, Kimura K, Shimotohno K: Production of two phosphoproteins from the NS5A region of the hepatitis C viral genome. Biochem Biophys Res Commun 1994;205:320-326.
77. Tanji Y, Kaneko T, Satoh S, Shimotohno K: Phosphorylation of hepatitis C virus-encoded nonstructural protein NS5A. J Virol 1995;69: 3980-3986.
78. Enomoto N, Sakuma I, Asahina Y, Kurosaki M, Murakami T, Yamamoto C, Izumi N, Marumo F, Sato C: Comparison of full-length sequences of interferon-sensitive and resistant hepatitis C virus 1b: Sensitivity to interferon is conferred by amino acid substitutions in the NS5A region. J Clin Invest 1995;96:224-230.
79. Gale M Jr, Blakely CM, Kwieciszewski B, Tan S-L, Dossett M, Tang NM, Korth MJ, Polyak SJ, Gretch DR, Katze MG: Control of PKR protein kinase by hepatitis C virus nonstructural 5A protein: Molecular mechanisms of kinase regulation. J Virol 1998;18:5208-5218.
80. Behrens S-E, Tomei L, De Francesco R: Identification and properties of the RNA-dependent RNA polymerase of hepatitis C virus. EMBO J 1996;15:12-22.
81. Lohmann V, Körner F, Herian U, 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 1998;71:8416-8428.
82. Ishii K, Tanaka Y, Yap C-C, Aizaki H, Matsuura Y, Miyamura T: Expression of hepatitis C virus NS5B protein: Characterization of its RNA polymerase activity and RNA binding. Hepatology 1999;29:1227-1235.
83. Kolykhalov AA, Agapov EV, Blight KJ, Mihalik K, Feinstone SM, Rice CM: Transmission of hepatitis C by intrahepatic inoculation with transcribed RNA. Science 1997;277:570-574.
84. Yanagi M, Purcell RH, Emerson SU, Bukh J: 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 USA 1997;94:8738-8743.