Hepatitis C virus: variability mechanisms, classification, evolution

Cover Page

Cite item

Full Text

Abstract

Hepatitis c virus (HCV) is one of the most dynamically evolving viral pathogens. In the last decade extensive molecular epidemiological studies demonstrated great HCV diversity. This review describes the HCV variability mechanisms and the current HCV classification, presents data on the geographical spread of different HCV subtypes and its evolution, including natural recombinant forms.

About the authors

O. V. Kalinina

St. Petersburg Pasteur Institute

Author for correspondence.
Email: olgakalinina@mail.ru

Ol’ga Kalinina, MD, PhD, ScD

St. Petersburg

Russian Federation

References

  1. Choo Q.L., Kuo G., Weiner A.J., Overby L.R., Bradley D.W., Houghton M. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science. 1989; 244 (4902): 359–62.
  2. Ogata N., Alter H.J., Miller R.H., Purcell R.H. Nucleotide sequence and mutation rate of the H strain of hepatitis C virus. Proc. Natl. Acad. Sci. USA. 1991; 88 (8): 3392–6.
  3. Smith D.B., Pathirana S., Davidson F., Lawlor E., Power J., Yap P.L. et al. The origin of hepatitis C virus genotypes. J. Gen. Virol. 1997; 78 (2): 321–8.
  4. Simmonds P. Genetic diversity and evolution of hepatitis C virus–15 years on. J. Gen. Virol. 2004; 85 (11): 3173–88.
  5. Farci P., Shimoda A., Coiana A., Diaz G., Peddis G., Melpolder J.C. et al. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science. 2000; 288 (5464): 339–44.
  6. Kalinina O., Norder H., Mukomolov S., Magnius L.O. A natural intergenotypic recombinant of hepatitis C virus identified in St. Petersburg. J. Virol. 2002; 76 (8): 4034–43.
  7. Kalinina O., Norder H., Magnius L.O. Full-Length Open Reading Frame of a Recombinant hepatitis C Virus Strain from St. Petersburg: Proposed mechanism for its formation. J. Gen. Virol. 2004; 85 (7): 1853–7.
  8. Bhattacharya D., Accola M.A., Ansari I.H., Striker R., Rehrauer W.M. Naturally occurring genotype 2b/1a hepatitis C virus in the United States. Virol. J. 2011; 8: 458.
  9. Lee Y.M., Lin H.J., Chen Y.J., Lee C.M., Wang S.F., Chang K.Y. et al. Molecular epidemiology of HCV genotypes among injection drug users in Taiwan: Full-length sequences of two new subtype 6w strains and a recombinant form_2b/6w. J. Med. Virol. 2009; 82 (1): 57–68.
  10. Legrand-Abravanel F., Claudinon J., Nicot F., Dubois M., ChapuyRegaud S., Sandres-Saune K. et al. New natural intergenotypic (2/5) recombinant of hepatitis C virus. J. Virol. 2007; 81 (8): 4357–62.
  11. Noppornpanth S., Lien T.X., Poovorawan Y., Smits S.L., Osterhaus A.D., Haagmans B.L. et al. Identification of a Naturally Occurring Recombinant Genotype 2/6 Hepatitis C Virus. J. Virol. 2006; 80 (15): 7569–77.
  12. Kageyama S., Agdamag D.M., Alesna E.T., Leaño P.S., Heredia A.M., Abellanosa-Tac-An I.P. et al. A natural inter-genotypic (2b/1b) recombinant of hepatitis C virus in the Philippines. J. Med. Virol. 2006; 78 (11): 1423–8.
  13. Yokoyama K., Takahashi M., Nishizawa T., Nagashima S., Jirintai S., Yotsumoto S. et al. Identification and characterization of a natural inter-genotypic (2b/1b) recombinant hepatitis C virus in Japan. Arch. Virol. J. 2011; 156: 1591–601.
  14. Hoshino H., Hino K., Miyakawa H., Takahashi K. Inter-genotypic recombinant hepatitis C virus strains in Japan noted by discrepancies between immunoassay and sequencing. J. Med. Virol. 2012; 1024: 1018–24.
  15. Collier A.J., Tang S., Elliott R.M. Translation efficiencies of the 5’ untranslated region from representatives of the six major genotypes of hepatitis C virus using a novel bicistronic reporter assay system. J. Gen. Virol. 1998; 79 (10): 2359–66.
  16. Colina R., Casane D., Vasquez S., Garcıa-Aguirre L., Chunga A., Romero H. et al. Evidence of intratypic recombination in natural populations of hepatitis C virus. J. Gen. Virol. 2004; 85 (1): 31–7.
  17. Gao F., Nainan O.V., Khudyakov Y., Li J., Hong Y., Gonzales A. et al. Recombinant hepatitis C virus in experimentally infected chimpanzees. J. Gen. Virol. 2007; 88 (1): 143–47.
  18. Simmonds P., Bukh J., Combet C., Deléage G., Enomoto N., Feinstone S. et al. Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology. 2005; 42 (4): 962–73.
  19. Smith D.B., Bukh J., Kuiken C., Muerhoff A.S., Rice C.M., Stapleton J.T. et al. Expanded classification of hepatitis C virus into 7 genotypes and 67 subtypes: updated criteria and genotype assignment WEB resource. Hepatology. 2014; 59 (1): 318–27.
  20. Pybus O.G., Charleston M.A., Gupta S., Rambaut A., Holmes E.C., Harvey P.H. The epidemic behavior of the hepatitis C virus. Science. 2001; 292 (5525): 2323–5.
  21. Cornberg M., Razavi H., Alberti A., Bernasconi E., Buti M., Cooper C. et al. A systematic review of hepatitis C virus epidemiology in Europe, Canada and Israel. Liver Int. 2011; 31 (Suppl. 2): 30–60.
  22. Sievert W., Altraif I., Razavi H.A., Abdo A., Ahmed E.A., Alomair A. et al. A systematic review of hepatitis C virus epidemiology in Asia, Australia and Egypt. Liver Int. 2011; 31 (Suppl. 2): 61–80.
  23. Львов Д.К., Самохвалов Е.И., Миширо С., Тсуда Ф., Селиванов Н.А., Окамото Х. и др. Закономерности распространения вируса гепатита С и его генотипов в России и странах СНГ. Вопросы вирусологии. 1997; 4: 157–61.
  24. Shustov A.V., Kochneva G.V., Sivolobova G.F., Grazhdantseva A.A., Gavrilova I.V., Akinfeeva L.A. et al. Molecular epidemiology of the hepatitis C virus in Western Siberia. J. Med. Virol. 2005; 77 (3): 382–9.
  25. Гаврилова И.В., Кочнева Г.В., Сиволобова Г.Ф., Гражданцева А.А., Баяндин Р.Б., Нетесов С.В. Распространенность, генотипическое разнообразие и факторы риска гепатита С среди больных с хроническими вирусными гепатитами в Новосибирской области. Инфекционные болезни. 2007; 5 (3): 9–15.
  26. Ковалев С.Ю., Малиушенко О.И., Глинских Н.П. Генетические варианты вирусв гепатита С, циркулирующие в Уральском регионе. Вопросы вирусологии. 2003; 48 (5): 11–4.
  27. Кузин С.Н., Самохвалов Е.И., Заботина Е.Е., Кудрявцева Е.Н., Крель П.Е., Корабельникова М.И. и др. Структура генотипов вируса гепатита у пациентов с хроническим гепатитом С. Журнал микробиологии, эпидемиологии и иммунобиологии. 2011; 3: 33–8.
  28. Tallo T., Norder H., Tefanova V., Krispin T., Schmidt J., Ilmoja M. et al. Genetic characterization of hepatitis C virus strains in Estonia: fluctuations in the predominating subtype with time. J. Med. Virol. 2007; 79 (4): 374–82.
  29. Ciccozzi M., Ciccaglione A.R., Presti A.Lo, Yalcinkaya T., Taskan Z.P., Equestre M. et al. Reconstruction of the evolutionary dynamics of the hepatitis C virus 1b epidemic in Turkey. Infect. Genet. Evol. 2011; 11 (5): 863–8.
  30. Chlabicz S., Flisiak R., Kowalczuk O., Grzeszczuk A., Pytel-Krolczuk B., Prokopowicz D. et al. Changing HCV genotypes distribution in Poland–relation to source and time of infection. J. Clin. Virol. 2008; 42 (2): 156–9.
  31. Demetriou V.L., van de Vijver D.A., Cyprus HCV Network, Kostrikis L.G., Chimonides S., Evgeniou A. et al. Molecular epidemiology of hepatitis C infection in Cyprus: evidence of polyphyletic infection. J. Med. Virol. 2009; 81 (2): 238–48.
  32. Tanaka Y., Agha S., Saudy N., Kurbanov F., Orito E., Kato T. et al. Exponential spread of hepatitis C virus genotype 4a in Egypt. J. Mol. Evol. 2004; 58 (2): 191–5.
  33. Mizokami M., Tanaka Y. Tracing the evolution of hepatitis C virus in the United States, Japan, and Egypt by using the molecular clock. Clin. Gastroenterol. Hepatol. 2005; 3 (10): 82–5.
  34. Chaudhuri S., Das S., Chowdhury A., Santra A., Bhattacharya S.K., Naik T.N. Molecular epidemiology of HCV infection among acute and chronic liver disease patients in Kolkata, India. J. Clin. Virol. 2005; 32 (1): 38–46.
  35. Pybus O.G., Barnes E., Taggart R., Lemey P., Markov P.V., Rasachak B. et al. Genetic history of hepatitis C virus in East Asia. J. Virol. 2009; 83 (2): 1071–82.
  36. Lu L., Murphy D., Li C., Liu S., Xia X., Pham P.H. et al. Complete genomes of three subtype 6t isolates and analysis of many novel hepatitis C virus variants within genotype 6. J. Gen. Virol. 2008; 89 (2): 444–52.
  37. Bracho M.A., Carrillo-Cruz F.Y., Ortega E., Moya A., GonzálezCandelas F. A new subtype of hepatitis C virus genotype 1: complete genome and phylogenetic relationships of an Equatorial Guinea isolate. J. Gen. Virol. 2006; 87 (6): 1697–702.
  38. Jeannel D., Fretz C., Traore Y., Kohdjo N., Bigot A., Pê Gamy E. et al. Evidence for high genetic diversity and long-term endemicity of hepatitis C virus genotypes 1 and 2 in West Africa. J. Med. Virol. 1998; 55 (2): 92–7.
  39. Pouillot R., Lachenal G., Pybus O.G., Rousset D., Njouom R. Variable epidemic histories of hepatitis C virus genotype 2 infection in West Africa and Cameroon. Infect. Genet. Evol. 2008; 8 (5): 676–81.
  40. Pybus O.G., Markov P.V., Wu A., Tatem A.J. Investigating the endemic transmission of the hepatitis C virus. Int. J. Parasitol. 2007; 37 (8): 839–49.
  41. Pybus O.G., Cochrane A., Holmes E.C., Simmonds P. The hepatitis C virus epidemic among injecting drug users. Infect. Genet. Evol. 2005; 5 (2): 131–9.
  42. Henquell C., Guglielmini J., Verbeeck J., Mahul A., Thibault V., Lebray P. et al. Evolutionary history of hepatitis C virus genotype 5a in France, a multicenter ANRS study. Infect. Genet. Evol. 2011; 11 (2): 496–503.
  43. Verbeeck J., Maes P., Lemey P., Pybus O.G., Wollants E., Song E. et al. Investigating the origin and spread of hepatitis C virus genotype 5a. J. Virol. 2006; 80 (9): 4220–6.
  44. Li C., Cao H., Lu L., Murphy D. Full-length sequences of 11 hepatitis C virus genotype 2 isolates representing five subtypes and six unclassified lineages with unique geographical distributions and genetic variation patterns. J. Gen. Virol. 2012; 93 (6): 1173–84.
  45. Sulbarán M.Z., Di Lello F.A., Sulbarán Y., Cosson C., Loureiro C.L., Rangel H.R. et al. Genetic history of hepatitis C virus in Venezuela: high diversity and long time of evolution of HCV genotype 2. PLoS One. 2010; 5 (12): e14315.
  46. Gededzha M.P., Selabe S.G., Kyaw T., Rakgole J.N., Blackard J.T., Mphahlele M.J. Introduction of new subtypes and variants of hepatitis C virus genotype 4 in South Africa. J. Med. Virol. 2012; 84 (4): 601–7.
  47. Katsoulidou A., Sypsa V., Tassopoulos N.C., Boletis J., Karafoulidou A., Ketikoglou I. et al. Molecular epidemiology of hepatitis C virus (HCV) in Greece: temporal trends in HCV genotype-specific incidence and molecular characterization of genotype 4 isolates. J. Viral. Hepat. 2006; 13 (1): 19–27.
  48. Eriksen M.B., Jørgensen L.B., Krarup H., Laursen A.L., Christensen P.B., Møller A. et al. Molecular and epidemiological profiles of hepatitis C virus genotype 4 in Denmark. J. Med. Virol. 2010; 82 (11): 1869–77.
  49. Ciccozzi M., Equestre M., Costantino A., Marascio N., Quirino A., Lo Presti A. et al. Hepatitis C virus genotype 4d in Southern Italy: Reconstruction of its origin and spread by a phylodynamic analysis. J. Med. Virol. 2012; 84 (10): 1613–9.
  50. Moreau I., Hegarty S., Levis J., Sheehy P., Crosbie O., Kenny-Walsh E. et al. Serendipitous identification of natural intergenotypicrecombinants of hepatitis C in Ireland. Virol. J. 2006; 3: 95.
  51. Чуб Е.В., Кочнева Г.В., Гранитов В.М., Нетесов С.В. Рекомбинанты вируса гепатита С типа 2k/1b у населения Алтайского края. Инфекционные болезни. 2007; 5 (4): 5–11.
  52. Kurbanov F., Tanaka Y., Chub E., Maruyama I., Azlarova A., Kamitsukasa H. et al. Molecular epidemiology and interferon susceptibility of the natural recombinant hepatitis C virus strain RF1_2k/1b. J. Infect. Dis. 2008; 198 (10): 1448–56.
  53. Morel V., Descamps V., François C., Fournier C., Brochot E., Capron D. et al. Emergence of a genomic variant of the recombinant 2k/1b strain during a mixed hepatitis C infection: a case report. J. Clin. Virol. 2010; 47 (4): 382–6.
  54. Кюрегян К.К. Молекулярно-биологические основы контроля вирусных гепатитов: Дисс. … докт. биол. наук. М.; 2012.
  55. Самохвалов Е.И., Николаева Л.И., Альховский С.В., Хлопова И.Н., Макашова В.В., Петрова Е.В. и др. Частота встречаемости отдельных субтипов вируса гепатита С в Московском регионе. Вопросы вирусологии. 2013: 58 (1): 36–40.
  56. Raghwani J., Thomas X.V., Koekkoek S.M., Schinkel J., Molenkamp R., van de Laar T. et al. Origin and evolution of the unique hepatitis C virus circulating recombinant form 2k/1b. J. Virol. 2012; 86 (4): 2212–20.
  57. Калинина О.В. Организация генома и география природного межгенотипного рекомбинанта вируса гепатита С RF1_2k/1b. Инфекция и иммунитет. 2012; 2 (4): 677–86.
  58. Newman R.M., Kuntzen T., Weiner B., Berical A., Charlebois P., Kuiken C. et al. Whole Genome Pyrosequencing of Rare Hepatitis C Virus Genotypes Enhances Subtype Classification and Identification of Naturally Occurring Drug Resistance Variants. J. Infect. Dis. 2013; 208 (1): 17–31.

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2015 Kalinina O.V.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС77-77676 от 29.01.2020.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies