Correlation of amino acid variations within nonstructural 4B protein with initial viral kinetics during interferon-alpha-based therapy in HCV-1b-infected patients

Journal of Viral Hepatitis

Volumn 14, Issue 5, 2007, Pages 338-349

  Welker, M W ^a   Hofmann, W P ^a   Welsch, C ^a,b   Von Wagner, M ^a   Herrmann, E ^a   Lengauer, T ^b   Zeuzem, S ^a   Sarrazin, C ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE FOR INFORMATICS   (Germany)

Author keywords

Conformational analyses; Hepatitis C virus resistance mechanisms; Sequencing; Smoothed mutational frequency

Indexed keywords

ALPHA2B INTERFERON; NONSTRUCTURAL PROTEIN 4B; PEGINTERFERON ALPHA2A; RIBAVIRIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ADULT; AGED; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BLOOD ANALYSIS; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG WITHDRAWAL; FEMALE; GENE AMPLIFICATION; GENE FUNCTION; GENETIC CONSERVATION; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; KINETICS; MALE; MOLECULAR PHYLOGENY; MUTATIONAL ANALYSIS; PATIENT COMPLIANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; SEQUENCE ANALYSIS; TREATMENT DURATION; TREATMENT OUTCOME; VIRUS MUTATION;

ADULT; AGED; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO ACIDS; ANTIVIRAL AGENTS; CONSENSUS SEQUENCE; DNA MUTATIONAL ANALYSIS; EUROPEAN CONTINENTAL ANCESTRY GROUP; GENOTYPE; HEPATITIS C, CHRONIC; HUMANS; INTERFERON-ALPHA; KINETICS; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; NUCLEIC ACID AMPLIFICATION TECHNIQUES; PHYLOGENY; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; TREATMENT OUTCOME; VIRAL NONSTRUCTURAL PROTEINS;

EID: 34247093714     PISSN: 13520504     EISSN: 13652893     Source Type: Journal    
DOI: 10.1111/j.1365-2893.2006.00798.x     Document Type: Article

References (65)

1. Alter MJ, Gallagher M, Morris TT et al. Acute non-A-E hepatitis in the United States and the role of hepatitis G virus infection. Sentinel Counties Viral Hepatitis Study Team. N Engl J Med 1997; 336: 741-746.
2. Saito I, Miyamura T, Ohbayashi A et al. Hepatitis C virus infection is associated with the development of hepatocellular carcinoma. Proc Natl Acad Sci USA 1990; 87: 6547-6549.
3. Fried MW, Shiffman ML, Reddy KR et al. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N Engl J Med 2002; 347: 975-982.
4. Hadziyannis SJ, Sette H Jr, Morgan TR et al. Peginterferon-alpha2a and ribavirin combination therapy in chronic hepatitis C: a randomized study of treatment duration and ribavirin dose. Ann Intern Med 2004; 140: 346-355.
5. Lindsay KL, Trepo C, Heintges T et al. A randomized, double-blind trial comparing pegylated interferon alfa-2b to interferon alfa-2b as initial treatment for chronic hepatitis C. Hepatology 2001; 34: 395-403.
6. Manns MP, McHutchison JG, Gordon SC et al. Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: a randomised trial. Lancet 2001; 358: 958-965.
7. Zeuzem S, Feinman SV, Rasenack J et al. Peginterferon alfa-2a in patients with chronic hepatitis C. N Engl J Med 2000; 343: 1666-1672.
8. Blindenbacher A, Duong FH, Hunziker L et al. Expression of hepatitis c virus proteins inhibits interferon alpha signaling in the liver of transgenic mice. Gastroenterology 2003; 124: 1465-1475.
9. de Lucas S, Bartolome J, Carreno V. Hepatitis C virus core protein down-regulates transcription of interferon-induced antiviral genes. J Infect Dis 2005; 191: 93-99.
10. Duong FH, Filipowicz M, Tripodi M, La Monica N, Heim MH. Hepatitis C virus inhibits interferon signaling through up-regulation of protein phosphatase 2A. Gastroenterology 2004; 126: 263-277.
11. Heim MH, Moradpour D, Blum HE. Expression of hepatitis C virus proteins inhibits signal transduction through the Jak-STAT pathway. J Virol 1999; 73: 8469-8475.
12. Sarrazin C, Bruckner M, Herrmann E et al. Quasispecies heterogeneity of the carboxy-terminal part of the E2 gene including the PePHD and sensitivity of hepatitis C virus 1b isolates to antiviral therapy. Virology 2001; 289: 150-163.
13. Taylor DR, Shi ST, Romano PR, Barber GN, Lai MM. Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science 1999; 285: 107-110.
14. Foy E, Li K, Wang C et al. Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science 2003; 300: 1145-1148.
15. Francois C, Duverlie G, Rebouillat D et al. Expression of hepatitis C virus proteins interferes with the antiviral action of interferon independently of PKR-mediated control of protein synthesis. J Virol 2000; 74: 5587-5596.
16. Gale MJ Jr, Korth MJ, Katze MG. Repression of the PKR protein kinase by the hepatitis C virus NS5A protein: a potential mechanism of interferon resistance. Clin Diagn Virol 1998; 10: 157-162.
17. Gale MJ Jr, Korth MJ, Tang NM et al. Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology 1997; 230: 217-227.
18. Nousbaum J, Polyak SJ, Ray SC et al. Prospective characterization of full-length hepatitis C virus NS5A quasispecies during induction and combination antiviral therapy. J Virol 2000; 74: 9028-9038.
19. Paterson M, Laxton CD, Thomas HC, Ackrill AM, Foster GR. Hepatitis C virus NS5A protein inhibits interferon antiviral activity, but the effects do not correlate with clinical response. Gastroenterology 1999; 117: 1187-1197.
20. Polyak SJ, Khabar KS, Paschal DM et al. Hepatitis C virus nonstructural 5A protein induces interleukin-8, leading to partial inhibition of the interferon-induced antiviral response. J Virol 2001; 75: 6095-6106.
21. Sarrazin C, Berg T, Lee JH et al. Mutations in the protein kinase-binding domain of the NS5A protein in patients infected with hepatitis C virus type 1a are associated with treatment response. J Infect Dis 2000; 181: 432-441.
22. Sarrazin C, Herrmann E, Bruch K, Zeuzem S. Hepatitis C virus nonstructural 5A protein and interferon resistance: a new model for testing the reliability of mutational analyses. J Virol 2002; 76: 11079-11090.
23. Duverlie G, Khorsi H, Castelain S et al. Sequence analysis of the NS5A protein of European hepatitis C virus 1b isolates and relation to interferon sensitivity. J Gen Virol 1998; 79 (Pt 6): 1373-1381.
24. Enomoto N, Sakuma I, Asahina Y et al. Mutations in the nonstructural protein 5A gene and response to interferon in patients with chronic hepatitis C virus 1b infection. N Engl J Med 1996; 334: 77-81.
25. Gerotto M, Dal Pero F, Pontisso P, Noventa F, Gatta A, Alberti A. Two PKR inhibitor HCV proteins correlate with early but not sustained response to interferon. Gastroenterology 2000; 119: 1649-1655.
26. Polyak SJ, Nousbaum JB, Larson AM, Cotler S, Carithers RL Jr, Gretch DR. The protein kinase-interacting domain in the hepatitis C virus envelope glycoprotein-2 gene is highly conserved in genotype 1-infected patients treated with interferon. J Infect Dis 2000; 182: 397-404.
27. Saiz JC, Lopez-Labrador FX, Ampurdanes S et al. The prognostic relevance of the nonstructural 5A gene interferon sensitivity determining region is different in infections with genotype 1b and 3a isolates of hepatitis C virus. J Infect Dis 1998; 177: 839-847.
28. Sarrazin C, Berg T, Lee JH et al. Improved correlation between multiple mutations within the NS5A region and virological response in European patients chronically infected with hepatitis C virus type 1b undergoing combination therapy. J Hepatol 1999; 30: 1004-1013.
29. Sarrazin C, Mihm U, Herrmann E et al. Clinical significance of in vitro replication-enhancing mutations of the hepatitis C virus (HCV) replicon in patients with chronic HCV infection. J Infect Dis 2005; 192: 1710-1719.
30. Squadrito G, Leone F, Sartori M et al. Mutations in the nonstructural 5A region of hepatitis C virus and response of chronic hepatitis C to interferon alfa. Gastroenterology 1997; 113: 567-572.
31. Vuillermoz I, Khattab E, Sablon E et al. Genetic variability of hepatitis C virus in chronically infected patients with viral breakthrough during interferon-ribavirin therapy. J Med Virol 2004; 74: 41-53.
32. Pascu M, Martus P, Hohne M et al. Sustained virological response in hepatitis C virus type 1b infected patients is predicted by the number of mutations within the NS5A-ISDR: a meta-analysis focused on geographical differences. Gut 2004; 53: 1345-1351.
33. Squadrito G, Leone F, Sartori M et al. Mutations in the non structural 5A region of hepatitis C virus and response of chronic hepatitis C to interferon alfa. Gastroenterology 1997; 113: 567-572.
34. Ibarrola N, Moreno-Monteagudo JA, Saiz M et al. Response to retreatment with interferon-alpha plus ribavirin in chronic hepatitis C patients is independent of the NS5A gene nucleotide sequence. Am J Gastroenterol 1999; 94: 2487-2495.
35. Blight KJ, Kolykhalov AA, Rice CM. Efficient initiation of HCV RNA replication in cell culture. Science 2000; 290: 1972-1974.
36. Blight KJ, McKeating JA, Rice CM. Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J Virol 2002; 76: 13001-13014.
37. Grobler JA, Markel EJ, Fay JF et al. Identification of a key determinant of hepatitis C virus cell culture adaptation in domain II of NS3 helicase. J Biol Chem 2003; 278: 16741-16746.
38. Krieger N, Lohmann V, Bartenschlager R. Enhancement of hepatitis C virus RNA replication by cell culture-adaptive mutations. J Virol 2001; 75: 4614-4624.
39. Lohmann V, Hoffmann S, Herian U, Penin F, Bartenschlager R. Viral and cellular determinants of hepatitis C virus RNA replication in cell culture. J Virol 2003; 77: 3007-3019.
40. Hugle T, Fehrmann F, Bieck E et al. The hepatitis C virus nonstructural protein 4B is an integral endoplasmic reticulum membrane protein. Virology 2001; 284: 70-81.
41. Lundin M, Monne M, Widell A, Von Heijne G, Persson MA. Topology of the membrane-associated hepatitis C virus protein NS4B. J Virol 2003; 77: 5428-5438.
42. Egger D, Wolk B, Gosert R et al. Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J Virol 2002; 76: 5974-5984.
43. Gosert R, Egger D, Lohmann V et al. Identification of the hepatitis C virus RNA replication complex in Huh-7 cells harboring subgenomic replicons. J Virol 2003; 77: 5487-5492.
44. Gao L, Aizaki H, He JW, Lai MM. Interactions between viral nonstructural proteins and host protein hVAP-33 mediate the formation of hepatitis C virus RNA replication complex on lipid raft. J Virol 2004; 78: 3480-3488.
45. Koch JO, Bartenschlager R. Modulation of hepatitis C virus NS5A hyperphosphorylation by nonstructural proteins NS3, NS4A, and NS4B. J Virol 1999; 73: 7138-7146.
46. Neddermann P, Clementi A, De Francesco R. Hyperphosphorylation of the hepatitis C virus NS5A protein requires an active NS3 protease, NS4A, NS4B, and NS5A encoded on the same polyprotein. J Virol 1999; 73: 9984-9991.
47. Simmonds P, Holmes EC, Cha TA et al. Classification of hepatitis C virus into six major genotypes and a series of subtypes by phylogenetic analysis of the NS-5 region. J Gen Virol 1993; 74 (Pt 11): 2391-2399.
48. Kwok S, Higuchi R. Avoiding false positives with PCR. Nature 1989; 339: 237-238.
49. Kato N, Hijikata M, Ootsuyama Y 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 1990; 87: 9524-9528.
50. Van de Peer Y, De Wachter R. TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 1994; 10: 569-570.
51. Rost B, Sander C. Combining evolutionary information and neural networks to predict protein secondary structure. Proteins 1994; 19: 55-72.
52. Mirny LA, Shakhnovich EI. Universally conserved positions in protein folds: reading evolutionary signals about stability, folding kinetics and function. J Mol Biol 1999; 291: 177-196.
53. Welsch C, Albrecht M, Maydt J et al. In-silico structure and function analysis of the hepatitis C virus non-structural protein 4B (NS4B). J Hepatol 2005; 42 (Suppl. 2): 169A.
54. Kato N, Nakamura T, Dansako H et al. Genetic variation and dynamics of hepatitis C virus replicons in long-term cell culture. J Gen Virol 2005; 86: 645-656.
55. Lohmann V, Korner F, Dobierzewska A, Bartenschlager R. Mutations in hepatitis C virus RNAs conferring cell culture adaptation. J Virol 2001; 75: 1437-1449.
56. Bells MJ, Russell RB. Amino acid properties and consequences of substitutions. In: Barnes MR, Gray IC, eds. Bioinformatics for Geneticists. New York: Wiley, 2003.
57. Elazar M, Liu P, Rice CM, Glenn JS. An N-terminal amphipathic helix in hepatitis C virus (HCV) NS4B mediates membrane association, correct localization of replication complex proteins, and HCV RNA replication. J Virol 2004; 78: 11393-11400.
58. Einav S, Elazar M, Danieli T, Glenn JS. A nucleotide binding motif in hepatitis C virus (HCV) NS4B mediates HCV RNA replication. J Virol 2004; 78: 11288-11295.
59. Florese RH, Nagano-Fujii M, Iwanaga Y, Hidajat R, Hotta H. Inhibition of protein synthesis by the nonstructural proteins NS4A and NS4B of hepatitis C virus. Virus Res 2002; 90: 119-131.
60. Kato J, Kato N, Yoshida H, Ono-Nita SK, Shiratori Y, Omata M. Hepatitis C virus NS4A and NS4B proteins suppress translation in vivo. J Med Virol 2002; 66: 187-199.
61. Park JS, Yang JM, Min MK. Hepatitis C virus nonstructural protein NS4B transforms NIH3T3 cells in cooperation with the Ha-ras oncogene. Biochem Biophys Res Commun 2000; 267: 581-587.
62. Piccininni S, Varaklioti A, Nardelli M, Dave B, Raney KD, McCarthy JE. Modulation of the hepatitis C virus RNA-dependent RNA polymerase activity by the non-structural (NS) 3 helicase and the NS4B membrane protein. J Biol Chem 2002; 277: 45670-45679.
63. Bukh J, Pietschmann T, Lohmann V et al. Mutations that permit efficient replication of hepatitis C virus RNA in Huh-7 cells prevent productive replication in chimpanzees. Proc Natl Acad Sci USA 2002; 99: 14416-14421.
64. Graether SP, Slupsky CM, Sykes BD. Effect of a mutation on the structure and dynamics of an alpha-helical antifreeze protein in water and ice. Proteins 2006; 63: 603-610.
65. Herrmann E, Neumann AU, Schmidt JM, Zeuzem S. Hepatitis C virus kinetics. Antivir Ther 2000; 5: 85-90.