Combined therapy of interferon plus ribavirin promotes multiple adaptive solutions in hepatitis C virus

Journal of Medical Virology

Volumn 81, Issue 4, 2009, Pages 650-656

  Cuevas, José M ^a,b   Torres Puente, Manuela ^a   Jiménez Hernández, Nuria ^a,b,c   Bracho, María A ^a,b,c   García Robles, Inmaculada ^a   Carnicer, Fernando ^d   Olmo, Juan Del ^e   Ortega, Enrique ^f   González Candelas, Fernando ^a,b,c   Moya, Andrés ^a,b,c  

^a UNIVERSITY OF VALENCIA   (Spain)

^b CIBER EPIDEMIOLOGÍA Y SALUD PÚBLICA CIBERESP   (Spain)

^c CSISP ^*  (Spain)

^d HOSPITAL GENERAL UNIVERSITARIO DE ALICANTE   (Spain)

^e HOSPITAL CLÍNICO UNIVERSITARIO   (Spain)

^f HOSPITAL GENERAL UNIVERSITARIO DE VALENCIA   (Spain)

Author keywords

HVR1; HVR2; HVR3; PKR BD; V3 domain

Indexed keywords

ALPHA2A INTERFERON; RIBAVIRIN; ANTIVIRUS AGENT; GLYCOPROTEIN E2, HEPATITIS C VIRUS; NS 5 PROTEIN, HEPATITIS C VIRUS; NS-5 PROTEIN, HEPATITIS C VIRUS; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; COHORT ANALYSIS; DRUG EFFICACY; DRUG TOLERABILITY; GENOME; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; IMMUNE SYSTEM; MOLECULAR CLONING; VIRUS DETECTION; ANTIVIRAL RESISTANCE; CHEMISTRY; DRUG COMBINATION; DRUG EFFECT; GENETICS; MOLECULAR GENETICS; MUTATION; TREATMENT FAILURE; VIROLOGY;

HEPATITIS C VIRUS;

AMINO ACID SEQUENCE; ANTIVIRAL AGENTS; DRUG RESISTANCE, VIRAL; DRUG THERAPY, COMBINATION; HEPACIVIRUS; HEPATITIS C; HUMANS; INTERFERON ALFA-2A; MOLECULAR SEQUENCE DATA; MUTATION; RIBAVIRIN; TREATMENT FAILURE; VIRAL ENVELOPE PROTEINS; VIRAL NONSTRUCTURAL PROTEINS;

EID: 62849100237     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.21460     Document Type: Article

References (43)

1. Alter HJ, Seeff LB. 2000. Recovery, persistence, and sequelae in hepatitis C virus infection: A perspective on long-term outcome. Semin Liver Dis 20:17-35.
2. Chambers TJ, Fan X, Droll DA, Hembrador E, Slater T, Nickells MW, Dustin LB, Dibisceglie AM. 2005. Quasispecies heterogeneity within the E1/E2 region as a pretreatment variable during pegylated interferon therapy of chronic hepatitis C virus infection. J Virol 79:3071-3083.
3. Chevaliez S, Brillet R, Lazaro E, Hezode C, Pawlotsky JM. 2007. Analysis of ribavirin mutagenicity in human hepatitis C virus infection. J Virol 81:7732-7741.
4. Cuevas JM, Torres-Puente M, Jiménez-Hernández N, Bracho MA, García-Robles I, Carnicer F, del Olmo J, Ortega E, Moya A, González-Candelas F. 2008a. Refined analysis of genetic variability parameters in hepatitis C virus and the ability to predict antiviral treatment response. J Viral Hepat 15:578-590.
5. Cuevas JM, Torres-Puente M, Jiménez-Hernández N, Bracho MA, García-Robles I, Wrobel B, Carnicer F, del Olmo J, Ortega E, Moya A, González-Candelas F. 2008b. Genetic variability of hepatitis C virus before and after combined therapyofinterferon plus ribavirin. PLoS One 3:e3058.
6. Dienstag JL, McHutchison JG. 2006. American gastroenterological association technical review on the management of hepatitis C. Gastroenterology 130:231-264.
7. Durante ME, Forton DM, Ruggiero G, Karayiannis P. 2003. Hepatitis C virus E2 and NS5A region variability during sequential treatment with two interferon-alpha preparations. J Med Virol 70:62-73.
8. Duverlie G, Khorsi H, Castelain S, Jaillon O, Izopet J, Lunel F, Eb F, Penin F, Wychowski C. 1998. Sequence analysis of the NS5A protein of European hepatitis C virus 1b isolates and relation to interferon sensitivity. J Gen Virol 79:1373-1381.
9. Enomoto N, Sakuma I, Asahina Y, Kurosaki M, Murakami T, Yamamoto C, Izumi N, Marumo F, Sato C. 1995. 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 96:224-230.
10. Enomoto N, Sakuma I, Asahina Y, Kurosaki M, Murakami T, Yamamoto C, Ogura Y, Izumi N, Marumo F, Sato C. 1996. Mutations in the nonstructural protein 5A gene and response to interferon in patients with chronic hepatitis C virus 1b infection. N Engl J Med 334:77-81.
11. Fried MW, Shiffman ML, Reddy KR, Smith C, Marinos G, Goncales FL, Jr., Haussinger D, Diago M, Carosi G, Dhumeaux D, Craxi A, Lin A, Hoffman J, Yu J. 2002. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N Engl J Med 347:975-982.
12. Gale MJ, Jr., Korth MJ, Tang NM, Tan SL, Hopkins DA, Dever TE, Polyak SJ, Gretch DR, Katze MG. 1997. Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology 230:217-227.
13. Gale MJ, Jr., Korth MJ, Katze MG. 1998. Repression of the PKR protein kinase by the hepatitis C virus NS5A protein: A potential mechanism of interferon resistance. Clin Diagn Virol 10:157-162.
14. Heathcote J, Main J. 2005. Treatment of hepatitis C. J Viral Hepat 12:223-235.
15. Herion D, Hoofnagle JH. 1997. The interferon sensitivity determining region: All hepatitis C virus isolates are not the same. Hepatology 25:769-771.
16. Hofmann WP, Polta A, Herrmann E, Mihm U, Kronenberger B, Sonntag T, Lohmann V, Schonberger B, Zeuzem S, Sarrazin C. 2007. Mutagenic effect of ribavirin on hepatitis C nonstructural 5B quasispecies in vitro and during antiviral therapy. Gastroenterology 132:921-930.
17. Inchauspe G, Zebedee S, Lee DH, Sugitani M, Nasoff M, Prince AM. 1991. Genomic structure of the human prototype strain H of hepatitis C virus: Comparison with American and Japanese isolates. Proc Natl Acad Sci USA 88:10292-10296.
18. Jiménez-Hernández N, Torres-Puente M, Bracho MA, García-Robles I, Ortega E, del Olmo J, Carnicer F, Gonzalez-Candelas F, Moya A. 2007. Epidemic dynamics of two coexisting hepatitis C virus subtypes. J Gen Virol 88:123-133.
19. Kato N, Hijikata M, Ootsuyama Y, Nakagawa M, Ohkoshi S, Sugimura T, Shimotohno K. 1990. Molecular cloning of the human hepatitis C virus genome from Japanese patients with non-A, non-B hepatitis. Proc Natl Acad Sci USA 87:9524-9528.
20. 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.
21. Korber B, Myers G. 1992. Signature pattern analysis: A method for assessing viral sequence relatedness. AIDS Res Hum Retroviruses 8:1549-1560.
22. Kuiken C, Combet C, Bukh J, Shin I, Deleage G, Mizokami M, Richardson R, Sablon E, Yusim K, Pawlotsky JM, Simmonds P. 2006. A comprehensive system for consistent numbering of HCV sequences, proteins and epitopes. Hepatology 44:1355-1361.
23. Layden-Almer JE, Kuiken C, Ribeiro RM, Kunstman KJ, Perelson AS, Layden TJ, Wolinsky SM. 2005. Hepatitis C virus genotype 1a NS5A pretreatment sequence variation and viral kinetics in African American and white patients. J Infect Dis 192:1078-1087.
24. Lindenbach BD, Rice CM. 2005. Unravelling hepatitis C virus replication from genome to function. Nature 436:933-938.
25. Liu WL, Su WC, Cheng CW, Hwang LH, Wang CC, Chen HL, Chen DS, Lai MY. 2007. Ribavirin up-regulates the activity of double-stranded RNA-activated protein kinase and enhances the action of interferon-alpha against hepatitis C virus. J Infect Dis 196:425-434.
26. Lusida MI, Nagano-Fujii M, Nidom CA, Soetjipto, Handajani R, Fujita T, Oka K, Hotta H. 2001. Correlation between mutations in the interferon sensitivity-determining region of NS5A protein and viral load of hepatitis C virus subtypes 1b, 1c, and 2a. J Clin Microbiol 39:3858-3864.
27. Macdonald A, Harris M. 2004. Hepatitis C virus NS5A: Tales of a promiscuous protein. J Gen Virol 85:2485-2502.
28. Manns MP, McHutchison JG, Gordon SC, Rustgi VK, Shiffman M, Reindollar R, Goodman ZD, Koury K, Ling M, Albrecht JK. 2001. Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: A randomised trial. Lancet 358:958-965.
29. Pascu M, Martus P, Hohne M, Wiedenmann B, Hopf U, Schreier E, Berg T. 2004. 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 53:1345-1351.
30. Pawlotsky JM. 2006. Therapy of hepatitis C: From empiricism to eradication. Hepatology 43:S207-S220.
31. Penin F, Combet C, Germanidis G, Frainais PO, Deleage G, Pawlotsky JM. 2001. Conservation ofthe 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.
32. Puig-Basagoiti F, Forns X, Furcic I, Ampurdanes S, Gimenez-Barcons M, Franco S, Sanchez-Tapias JM, Saiz JC. 2005. Dynamics of hepatitis C virus NS5A quasispecies during interferon and ribavirin therapy in responder and non-responder patients with genotype 1b chronic hepatitis C. J Gen Virol 86:1067-1075.
33. Taylor DR, Shi ST, Romano PR, Barber GN, Lai MM. 1999. Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science 285:107-110.
34. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL-X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-4882.
35. Torres-Puente M, Cuevas JM, Jiménez-Hernández N, Bracho MA, García-Robles I, Carnicer F, del Olmo J, Ortega E, Moya A, González-Candelas F. 2007. Contribution of insertions and deletions to the variability ofhepatitis C virus populations. J Gen Virol 88:2198-2203.
36. Torres-Puente M, Cuevas JM, Jiménez-Hernández N, Bracho MA, García-Robles I, Carnicer F, del Olmo J, Ortega E, Moya A, González-Candelas F. 2008a. Hepatitis C virus and the controversial role of the interferon sensitivity determining region in the response to interferon treatment. J Med Virol 80:247-253.
37. Torres-Puente M, Cuevas JM, Jiménez-Hernández N, Bracho MA, García-Robles I, Wrobel B, Carnicer F, del Olmo J, Ortega E, Moya A, Gonzai lez-Candelas F. 2008b. Genetic variability in hepatitis C virus and its role in antiviral treatment response. J Viral Hepat 15:188-199.
38. Torres-Puente M, Cuevas JM, Jiménez-Hernández N, Bracho MA, Garcia-Robles I, Wrobel B, Carnicer F, del Olmo J, Ortega E, Moya A, Gonzalez-Candelas F. 2008c. Using evolutionary tools to refine the new hypervariable region 3 within the envelope 2 protein of hepatitis C virus. Infect Genet Evol 8:74-82.
39. Troesch M, Meunier I, Lapierre P, Lapointe N, Alvarez F, Boucher M, Soudeyns H. 2006. Study of a novel hypervariable region in hepatitis C virus (HCV) E2 envelope glycoprotein. Virology 352: 357-367.
40. Ward CL, Dev A, Rigby S, Symonds WT, Patel K, Zekry A, Pawlotsky JM, McHutchison JG. 2008. Interferon and ribavirin therapy does not select for resistance mutations in hepatitis C virus polymerase. J Viral Hepat 15:571-577.
41. Weiner AJ, Brauer MJ, Rosenblatt J, Richman KH, Tung J, Crawford K, Bonino F, Saracco G, Choo QL, Houghton M. 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.
42. Yagnik AT, Lahm A, Meola A, Roccasecca RM, Ercole BB, Nicosia A, Tramontano A. 2000. A model for the hepatitis C virus envelope glycoprotein E2. Proteins 40:355-366.
43. Young KC, Lindsay KL, Lee KJ, Liu WC, He JW, Milstein SL, Lai MM. 2003. Identification of a ribavirin-resistant NS5B mutation of hepatitis C virus during ribavirin monotherapy. Hepatology 38:869-878.