Evolutionary dynamics of the E1-E2 viral populations during combination therapy in non-responder patients chronically infected with hepatitis C virus subtype 1b

Infection, Genetics and Evolution

Volumn 13, Issue 1, 2013, Pages 1-10

  Saludes, Verónica ^a,b,g   González Candelas, Fernando ^b,c   Planas, Ramón ^a,d   Solà, Ricard ^e   Ausina, Vicente ^a,f   Martró, Elisa ^a,b  

^a HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

^b CIBER EPIDEMIOLOGÍA Y SALUD PÚBLICA CIBERESP   (Spain)

^c UNIVERSITY OF VALENCIA   (Spain)

^d INSTITUTO DE SALUD CARLOS III   (Spain)

^e UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^f INSTITUTO DE SALUD CARLOS III   (Spain)

^g UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

Chronic hepatitis C; E1 E2 region; HCV 1b; PEG IFN RBV; Viral evolution

Indexed keywords

GLYCOPROTEIN E1; GLYCOPROTEIN E2; PEGINTERFERON ALPHA; RIBAVIRIN;

ADULT; AGED; AMINO ACID SUBSTITUTION; ANTIVIRAL THERAPY; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; DRUG TREATMENT FAILURE; E2 GENE; EVOLUTIONARY ADAPTATION; FEMALE; GENE E1; GENE LOCATION; GENE STRUCTURE; GENETIC ANALYSIS; GENETIC VARIABILITY; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POPULATION DYNAMICS; PRIORITY JOURNAL; RELAPSE; RETROSPECTIVE STUDY; TREATMENT DURATION; TREATMENT RESPONSE; UNINDEXED SEQUENCE; VIRAL GENETICS; VIRUS CHARACTERIZATION; VIRUS GENE;

ADAPTATION, BIOLOGICAL; ADULT; AGED; AMINO ACID SUBSTITUTION; ANTIVIRAL AGENTS; DRUG THERAPY, COMBINATION; EVOLUTION, MOLECULAR; FEMALE; GENETIC VARIATION; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; MALE; MIDDLE AGED; PHYLOGENY; RETROSPECTIVE STUDIES; TREATMENT FAILURE; VIRAL ENVELOPE PROTEINS; VIRAL LOAD;

HEPATITIS C VIRUS; HEPATITIS C VIRUS GENOTYPE 1; HEPATITIS C VIRUS SUBTYPE 1B;

EID: 84870184270     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2012.09.012     Document Type: Article

References (45)

1. Abbate I., Lo I.O., Di Stefano R., Cappiello G., Girardi E., Longo R., Ferraro D., Antonucci G., Di Marco V., Solmone M., Craxi A., Ippolito G., Capobianchi M.R. HVR-1 quasispecies modifications occur early and are correlated to initial but not sustained response in HCV-infected patients treated with pegylated- or standard-interferon and ribavirin. J. Hepatol. 2004, 40:831-836.
2. Aurora R., Donlin M.J., Cannon N.A., Tavis J.E. Genome-wide hepatitis C virus amino acid covariance networks can predict response to antiviral therapy in humans. J. Clin. Invest. 2009, 119:225-236.
3. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Royal Stat. Soc., Ser. B 1995, 57:289-300.
4. Chambers T.J., Fan X., Droll D.A., Hembrador E., Slater T., Nickells M.W., Dustin L.B., Dibisceglie A.M. Quasispecies heterogeneity within the E1/E2 region as a pretreatment variable during pegylated interferon therapy of chronic hepatitis C virus infection. J. Virol. 2005, 79:3071-3083.
5. Cuevas J.M., González M., Torres-Puente M., Jiménez-Hernández N., Bracho M.A., García-Robles I., González-Candelas F., Moya A. The role of positive selection in hepatitis C virus. Infect. Genet. Evol. 2009, 9:860-866.
6. Cuevas J.M., Torres-Puente M., Jiménez-Hernández N., Bracho M.A., García-Robles I., Carnicer F., Olmo J.D., Ortega E., González-Candelas F., Moya A. Combined therapy of interferon plus ribavirin promotes multiple adaptive solutions in hepatitis C virus. J. Med. Virol. 2009, 81:650-656.
7. Cuevas J.M., Torres-Puente M., Jiménez-Hernandez N., Bracho M.A., García-Robles I., Carnicer F., Olmo J.D., Ortega E., Moya A., González-Candelas F. Refined analysis of genetic variability parameters in hepatitis C virus and the ability to predict antiviral treatment response. J. Viral Hepat. 2008, 15:578-590.
8. Cuevas J.M., Torres-Puente M., Jiménez-Hernández N., Bracho M.A., García-Robles I., Wróbel B., Carnicer F., del Olmo J., Ortega E., Moya A., González-Candelas F. Genetic variability of hepatitis C virus before and after combined therapy of interferon plus ribavirin. PLoS One 2008, 3:e3058.
9. Esteban J.I., Sauleda S., Quer J. The changing epidemiology of hepatitis C virus infection in Europe. J. Hepatol. 2008, 48:148-162.
10. Fan X., Mao Q., Zhou D., Lu Y., Xing J., Xu Y., Ray S.C., Di Bisceglie A.M. High diversity of hepatitis C viral quasispecies is associated with early virological response in patients undergoing antiviral therapy. Hepatology 2009, 50:1765-1772.
11. Farci P., Alter H.J., Wong D.C., Miller R.H., Govindarajan S., Engle R., Shapiro M., Purcell R.H. Prevention of hepatitis C virus infection in chimpanzees after antibody-mediated in vitro neutralization. Proc. Natl. Acad. Sci. USA 1994, 91:7792-7796.
12. Farci P., Purcell R.H. Clinical significance of hepatitis C virus genotypes and quasispecies. Semin. Liver Dis. 2000, 20:103-126.
13. Farci P., Shimoda A., Wong D., Cabezon T., De G.D., Strazzera A., Shimizu Y., Shapiro M., Alter H.J., Purcell R.H. 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. USA 1996, 93:15394-15399.
14. Farci P., Strazzera R., Alter H.J., Farci S., Degioannis D., Coiana A., Peddis G., Usai F., Serra G., Chessa L., Diaz G., Balestrieri A., Purcell R.H. Early changes in hepatitis C viral quasispecies during interferon therapy predict the therapeutic outcome. Proc. Natl. Acad. Sci. USA 2002, 99:3081-3086.
15. Feliu A., Gay E., García-Retortillo M., Saiz J.C., Forns X. Evolution of hepatitis C virus quasispecies immediately following liver transplantation. Liver Transpl. 2004, 10:1131-1139.
16. Fried M.W., Shiffman M.L., Reddy K.R., Smith C., Marinos G., Goncales F.L., Haussinger D., Diago M., Carosi G., Dhumeaux D., Craxi A., Lin A., Hoffman J., Yu J. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N. Engl. J. Med. 2002, 347:975-982.
17. Ghany M., Nelson D.R., Strader D.B., Thomas D.L., Seeff L.B. An update on treatment of genotype 1 chronic hepatitis C virusi nfection: 2011 practice guidelines by the American Association for the Study of Liver Diseases. Hepatology 2011, 54:1433-1444.
18. Ghany M.G., Strader D.B., Thomas D.L., Seeff L.B. Diagnosis, management, and treatment of hepatitis C: an update. Hepatology 2009, 49:1335-1374.
19. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
20. Korber B., Myers G. Signature pattern analysis: a method for assessing viral sequence relatedness. AIDS Res. Hum. Retroviruses 1992, 8:1549-1560.
21. Kurbanov F., Tanaka Y., Matsuura K., Sugauchi F., Elkady A., Khan A., Hasegawa I., Ohno T., Tokuda H., Mizokami M. Positive selection of core 70Q variant genotype 1b hepatitis C virus strains induced by pegylated interferon and ribavirin. J. Infect. Dis. 2010, 201:1663-1671.
22. Manns M.P., McHutchison J.G., Gordon S.C., Rustgi V.K., Shiffman M., Reindollar R., Goodman Z.D., Koury K., Ling M., Albrecht J.K. 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.
23. McHutchison J.G., Manns M., Patel K., Poynard T., Lindsay K.L., Trepo C., Dienstag J., Lee W.M., Mak C., Garaud J.J., Albrecht J.K. Adherence to combination therapy enhances sustained response in genotype-1-infected patients with chronic hepatitis C. Gastroenterology 2002, 123:1061-1069. International Hepatitis Interventional Therapy Group.
24. Morishima C., Polyak S.J., Ray R., Doherty M.C., Di Bisceglie A.M., Malet P.F., Bonkovsky H.L., Sullivan D.G., Gretch D.R., Rothman A.L., Koziel M.J., Lindsay K.L. Hepatitis C virus-specific immune responses and quasi-species variability at baseline are associated with nonresponse to antiviral therapy during advanced hepatitis C. J. Infect. Dis. 2006, 193:931-940.
25. Pond S.L., Frost S.D. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 2005, 21:2531-2533.
26. Posada D. JModelTest: phylogenetic model averaging. Mol. Biol. Evol. 2008, 25:1253-1256.
27. Raimondi S., Bruno S., Mondelli M.U., Maisonneuve P. Hepatitis C virus genotype 1b as a risk factor for hepatocellular carcinoma development: a meta-analysis. J. Hepatol. 2009, 50:1142-1154.
28. Rolland M., Tovanabutra S., deCamp A.C., Frahm N., Gilbert P.B., Sanders-Buell E., Heath L., Magaret C.A., Bose M., Bradfield A., O'Sullivan A., Crossler J., Jones T., Nau M., Wong K., Zhao H., Raugi D.N., Sorensen S., Stoddard J.N., Maust B.S., Deng W., Hural J., Dubey S., Michael N.L., Shiver J., Corey L., Li F., Self S.G., Kim J., Buchbinder S., Casimiro D.R., Robertson M.N., Duerr A., McElrath M.J., McCutchan F.E., Mullins J.I. Genetic impact of vaccination on breakthrough HIV-1 sequences from the STEP trial. Nat. Med. 2011, 17:366-371.
29. Roque-Afonso A.M., Ducoulombier D., Di Liberto G., Kara R., Gigou M., Dussaix E., Samuel D., Feray C. Compartmentalization of hepatitis C virus genotypes between plasma and peripheral blood mononuclear cells. J. Virol. 2005, 79:6349-6357.
30. Rozas J., Sánchez-Del Barrio J.C., Messeguer X., Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003, 19:2496-2497.
31. Saludes V., Bracho M.A., Valero O., Ardèvol M., Planas R., González-Candelas F., Ausina V., Martró E. Baseline prediction of combination therapy outcome in hepatitis C virus 1b infected patients by discriminant analysis using viral and host factors. PLoS One 2010, 5:e14132.
32. Scheuer P.J. Classification of chronic viral hepatitis: a need for reassessment. J. Hepatol. 1991, 13:372-374.
33. Schlütter J. Therapeutics: new drugs hit the target. Nature 2011, 474:S5-S7.
34. Schvoerer E., Soulier E., Royer C., Renaudin A.C., Thumann C., Fafi-Kremer S., Brignon N., Doridot S., Meyer N., Pinson P., Ellero B., Woehl-Jaegle M.L., Meyer C., Wolf P., Zachary P., Baumert T., Stoll-Keller F. Early evolution of hepatitis C virus (HCV) quasispecies after liver transplant for HCV-related disease. J. Infect. Dis. 2007, 196:528-536.
35. Simmonds P., Bukh J., Combet C., Deleage G., Enomoto N., Feinstone S., Halfon P., Inchauspe G., Kuiken C., Maertens G., Mizokami M., Murphy D.G., Okamoto H., Pawlotsky J.M., Penin F., Sablon E., Shin I., Stuyver L.J., Thiel H.J., Viazov S., Weiner A.J., Widell A. Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 2005, 42:962-973.
36. Stamatakis A., Hoover P., Rougemont J. A rapid bootstrap algorithm for the RAxML Web servers. Syst. Biol. 2008, 57:758-771.
37. Sy T., Jamal M.M. Epidemiology of hepatitis C virus (HCV) infection. Int. J. Med. Sci. 2006, 3:41-46.
38. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
39. Torres-Puente M., Cuevas J.M., Jiménez-Hernández N., Bracho M.A., García-Robles I., Wrobel B., Carnicer F., del Olmo J., Ortega E., Moya A., González-Candelas F. Genetic variability in hepatitis C virus and its role in antiviral treatment response. J. Viral Hepat. 2008, 15:188-199.
40. Torres-Puente M., Cuevas J.M., Jiménez-Hernández N., Bracho M.A., García-Robles I., Wrobel B., Carnicer F., del Olmo J., Ortega E., Moya A., González-Candelas F. Using evolutionary tools to refine the new hypervariable region 3 within the envelope 2 protein of hepatitis C virus. Infect. Genet. Evol. 2008, 8:74-82.
41. Ueda E., Enomoto N., Sakamoto N., Hamano K., Sato C., Izumi N., Watanabe M. Changes of HCV quasispecies during combination therapy with interferon and ribavirin. Hepatol. Res. 2004, 29:89-96.
42. Weiner A.J., Brauer M.J., Rosenblatt J., Richman K.H., Tung J., Crawford K., Bonino F., Saracco G., Choo Q.L., Houghton M., Han J.H. 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.
43. Weiner A.J., Geysen H.M., Christopherson C., Hall J.E., Mason T.J., Saracco G., Bonino F., Crawford K., Marion C.D., Crawford K.A., et al. Evidence for immune selection of hepatitis C virus (HCV) putative envelope glycoprotein variants: potential role in chronic HCV infections. Proc. Natl. Acad. Sci. USA 1992, 89:3468-3472.
44. Wohnsland A., Hofmann W.P., Sarrazin C. Viral determinants of resistance to treatment in patients with hepatitis C. Clin. Microbiol. Rev. 2007, 20:23-38.
45. World Health Organization, 2010. Viral Cancers: Hepatitis C virus. Available from: www.who.int/vaccine_research/diseases/viral_cancers/en/index2.html#disease%20burden.