Evolution of Hepatitis Viruses
Peter Simmonds
Infection and Immunity Division, The Roslin Institute, University of Edinburgh, Edinburgh, UK
Search for more papers by this authorDonald B. Smith
Centre for Immunity, Infection and Evolution, Ashworth Laboratories, University of Edinburgh, Edinburgh, UK
Search for more papers by this authorPeter Simmonds
Infection and Immunity Division, The Roslin Institute, University of Edinburgh, Edinburgh, UK
Search for more papers by this authorDonald B. Smith
Centre for Immunity, Infection and Evolution, Ashworth Laboratories, University of Edinburgh, Edinburgh, UK
Search for more papers by this authorHoward C. Thomas BSc, PhD, FRCP, FRCPath, FMedSci
Emeritus Professor of Hepatology, Department of Medicine, Imperial College London, London, UK
Search for more papers by this authorAnna S.F. Lok MD
Alice Lohrman Andrews Research Professor in Hepatology, Director of Clinical Hepatology, Professor of Internal Medicine, Associate Chair for Clinical Research, Department of Internal Medicine, University of Michigan Health System, Ann Arbor, MI, USA
Search for more papers by this authorStephen A. Locarnini MBBS, BSc(Hons), PhD, FRCPath
Head, Research & Molecular Development, Victorian Infectious Diseases Reference Laboratory, Melbourne, VIC, Australia
Search for more papers by this authorArie J. Zuckerman MD, DSc, FRCP, FRCPath, FMedSci
Emeritus Professor of Medical Microbiology, Formerly Principal and Dean, Royal Free Hospital School of Medicine
Search for more papers by this authorSummary
The evolution of human hepatitis viruses A, B, C, and E (HAV, HBV, HCV, and HEV) can be studied over very different time scales. Very rapid sequence change occurs in response to a variety of selection pressures driven by the immune escape from B and T cell responses and immunization and, in treated individuals, by antiviral therapy. Each shows more gradual accumulation of largely neutral nucleotide substitutions, a process that, over a much longer term period, leads ultimately to their differentiation into genetically distinct types. Thus, hepatitis A, B, C, and E viruses are currently divided into 6, 8, 7, and 4 genotypes respectively with HCV showing the greatest genetic divergence (>30% nucleotide sequence over the length of the genome) and HBV the least (11–15%). Some hepatitis viruses infect nonhuman primates (HAV and HBV) and other mammals (HEV), while HCV infections are restricted to humans. Sequence variability influences their antigenicity, their biology, and host interactions, with implications for vaccine development and antiviral therapy.
References
- Robertson BH, Jansen RW, Khanna B, et al. Genetic relatedness of hepatitis-A virus strains recovered from different geographical regions. J Gen Virol 1992; 73: 1365–1377.
- Norder H, Courouce AM, Magnius LO. Complete genomes, phylogenetic relatedness, and structural proteins of six strains of the hepatitis B virus, four of which represent two new genotypes. Virology 1994; 198: 489–503.
- Simmonds P, Bukh J, Combet C, et al. Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 2005; 42: 962–973.
- Lu L, Li C, Hagedorn CH. Phylogenetic analysis of global hepatitis E virus sequences: genetic diversity, subtypes and zoonosis. Rev Med Virol 2006; 16: 5–36.
- Smith DB, Purdy MA, Simmonds P. Genetic variability and the classification of hepatitis E virus. J Virol 2013. EPUB Feb 6th.
- Okamoto H, Kojima M, Okada S-I, et al. Genetic drift of hepatitis C virus during an 8.2 year infection in a chimpanzee: variability and stability. Virology 1992; 190: 894–899.
- Smith DB, Pathirana S, Davidson F, et al. The origin of hepatitis C virus genotypes. J Gen Virol 1997; 78: 321–328.
- Booth JC, Kumar U, Webster D, Monjardino J, Thomas HC. Comparison of the rate of sequence variation in the hypervariable region of E2/NS1 region of hepatitis C virus in normal and hypogammaglobulinemic patients. Hepatology 1998; 27: 223–227.
- Thimme R, Oldach D, Chang KM, Steiger C, Ray SC, Chisari FV. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J Exp Med 2001; 194: 1395–1406.
- Lechner F, Wong DK, Dunbar PR, et al. Analysis of successful immune responses in persons infected with hepatitis C virus. J Exp Med 2000; 191: 1499–1512.
- Chang KM, Rehermann B, McHutchison JG, et al. Immunological significance of cytotoxic T lymphocyte epitope variants in patients chronically infected by the hepatitis C virus. J Clin Invest 1997; 100: 2376–2385.
- Cantaloube JF, Biagini P, Attoui HX. Evolution of hepatitis C virus in blood donors and their respective recipients. J Gen Virol 2003; 84: 441–446.
- Hannoun C, Horal P, Lindh M. Long-term mutation rates in the hepatitis B virus genome. J Gen Virol 2000; 81: 75–83.
- Carman WF, Zanetti AR, Karayiannis P, et al. Vaccine-induced escape mutant of hepatitis B virus. Lancet 1990; 336: 325–329.
- Terrault NA, Zhou S, McCory RW, et al. Incidence and clinical consequences of surface and polymerase gene mutations in liver transplant recipients on hepatitis B immunoglobulin. Hepatology 1998; 28: 555–561.
- Bonino F, Rosina F, Rizzetto M, et al. Chronic hepatitis in HBsAg carriers with serum HBV-DNA and anti-HBe. Gastroenterology 1986; 90: 1268–1273.
- Wohnsland A, Hofmann WP, Sarrazin C. Viral determinants of resistance to treatment in patients with hepatitis C. Clin Microbiol Rev 2007; 20: 23–38.
- Ghany MG, Kim HY, Stoddard A, Wright EC, Seeff LB, Lok AS. Predicting clinical outcomes using baseline and follow-up laboratory data from the hepatitis C long-term treatment against cirrhosis trial. Hepatology 2011; 54: 1527–1537.
- Yuan HJ, Jain M, Snow KK, Gale M Jr, Lee WM. Evolution of hepatitis C virus NS5A region in breakthrough patients during pegylated interferon and ribavirin therapy. J Viral Hepat 2010; 17: 208–216.
- Xiang X, Lu J, Dong Z, et al. Viral sequence evolution in Chinese genotype 1b chronic hepatitis C patients experiencing unsuccessful interferon treatment. Infect Genet Evol 2011; 11: 382–390.
- Akuta N, Suzuki F, Hirakawa M, et al. Amino acid substitution in hepatitis C virus core region and genetic variation near the interleukin 28B gene predict viral response to telaprevir with peginterferon and ribavirin. Hepatology 2010; 52: 421–429.
- Zoulim F, Locarnini S. Hepatitis B virus resistance to nucleos(t)ide analogues. Gastroenterology 2009; 137: 1593–1608.
- Dowd KA, Netski DM, Wang XH, Cox AL, Ray SC. Selection pressure from neutralizing antibodies drives sequence evolution during acute infection with hepatitis C virus. Gastroenterology 2009; 136: 2377–2386.
- Power JP, Lawlor E, Davidson F, Holmes EC, Yap PL, Simmonds P. Molecular epidemiology of an outbreak of infection with hepatitis C virus in recipients of anti-D immunoglobulin. Lancet 1995; 345: 1211–1213.
- Pudupakam RS, Kenney SP, Cordoba L, et al. Mutational analysis of the hypervariable region of hepatitis e virus reveals its involvement in the efficiency of viral RNA replication. J Virol 2011; 85: 10031–10040.
- Pudupakam RS, Huang YW, Opriessnig T, Halbur PG, Pierson FW, Meng XJ. Deletions of the hypervariable region (HVR) in open reading frame 1 of hepatitis E virus do not abolish virus infectivity: evidence for attenuation of HVR deletion mutants in vivo. J Virol 2009; 83: 384–395.
- Shukla P, Nguyen HT, Torian U, et al. Cross-species infections of cultured cells by hepatitis E virus and discovery of an infectious virus-host recombinant. Proc Natl Acad Sci USA 2011; 108: 2438–2443.
- Nguyen HT, Torian U, Faulk K, et al. A naturally occurring human/hepatitis E recombinant virus predominates in serum but not in faeces of a chronic hepatitis E patient and has a growth advantage in cell culture. J Gen Virol 2012; 93: 526–530.
- Smith DB, Vanek J, Ramalingam S, et al. The evolution of the hepatitis E virus hypervariable region. J Gen Virol 2012; 93: 2408–2416.
- Norder H, Ebert JW, Fields HA, Mushahwar IK, Magnius LO. Complete sequencing of a gibbon hepatitis B virus genome reveals a unique genotype distantly related to the chimpanzee hepatitis B virus. Virology 1996; 218: 214–223.
- Cui C, Shi J, Hui L, et al. The dominant hepatitis B virus genotype identified in Tibet is a C/D hybrid. J Gen Virol 2002; 83: 2773–2777.
- Hannoun C, Norder H, Lindh M. An aberrant genotype revealed in recombinant hepatitis B virus strains from Vietnam. J Gen Virol 2000; 81: 2267–2272.
- Sugauchi F, Orito E, Ichida T, et al. Hepatitis B virus of genotype B with or without recombination with genotype C over the precore region plus the core gene. J Virol 2002; 76: 5985–5992.
- Sugauchi F, Orito E, Ichida T, et al. Epidemiologic and virologic characteristics of hepatitis B virus genotype B having the recombination with genotype C. Gastroenterology 2003; 124: 925–932.
- Morel V, Fournier C, Francois C, et al. Genetic recombination of the hepatitis C virus: clinical implications. J Viral Hepat 2011; 18: 77–83.
- Bhattacharya D, Accola MA, Ansari IH, Striker R, Rehrauer WM. Naturally occurring genotype 2b/1a hepatitis C virus in the United States. Virol J 2011; 8: 458.
- Viazov S, Ross SS, Kyuregyan KK, et al. Hepatitis C virus recombinants are rare even among intravenous drug users. J Med Virol 2010; 82: 232–238.
- Gonzalez-Candelas F, Lopez-Labrador FX, Bracho MA. Recombination in hepatitis C virus. Viruses 2011; 3: 2006–2024.
- Fan J. Open reading frame structure analysis as a novel genotyping tool for hepatitis E virus and the subsequent discovery of an inter-genotype recombinant. J Gen Virol 2009; 90: 1353–1358.
- Wang H, Zhang W, Ni B, et al. Recombination analysis reveals a double recombination event in hepatitis E virus. Virol J 2010; 7: 129.
- Costa-Mattioli M, Ferre V, Casane D, et al. Evidence of recombination in natural populations of hepatitis A virus. Virology 2003; 311: 51–59.
- Belalov IS, Isaeva OV, Lukashev AN. Recombination in hepatitis A virus: evidence for reproductive isolation of genotypes. J Gen Virol 2011; 92: 860–872.
- Ray SC, Fanning L, Wang XH, Netski DM, Kenny-Walsh E, Thomas DL. Divergent and convergent evolution after a common-source outbreak of hepatitis C virus. J Exp Med 2005; 201: 1753–1759.
- Candotti D, Temple J, Sarkodie F, Allain JP. Frequent recovery and broad genotype 2 diversity characterize hepatitis C virus infection in Ghana, West Africa. J Virol 2003; 77: 7914–7923.
-
Jeannel D,
Fretz C,
Traore Y, 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:
92–97.
10.1002/(SICI)1096-9071(199806)55:2<92::AID-JMV2>3.0.CO;2-I CAS PubMed Web of Science® Google Scholar
- Simmonds P, Smith DB. Structural constraints on RNA virus evolution. J Virol 1999; 73: 5787–5794.
- Simmonds P, Tuplin A, Evans DJ. Detection of genome-scale ordered RNA structure (GORS) in genomes of positive-stranded RNA viruses: implications for virus evolution and host persistence. RNA 2004; 10: 1337–1351.
- Jeannel D. Why is hepatitis C virus (HCV) epidemic in Southern Burkina Faso? Hepatitis C virus Infection: Epidemiology and Diagnosis 2003;n.p.
- Norder H, Courouce AM, Coursaget P, et al. Genetic diversity of hepatitis B virus strains derived worldwide: genotypes, subgenotypes, and HBsAg subtypes. Intervirology 2004; 47: 289–309.
- Alestig E, Hannoun C, Horal P, Lindh M. Hepatitis B virus genotypes in Mongols and Australian Aborigines. Arch Virol 2001; 146: 2321–2329.
- Sugauchi F, Mizokami M, Orito E, et al. A novel variant genotype C of hepatitis B virus identified in isolates from Australian Aborigines: complete genome sequence and phylogenetic relatedness. J Gen Virol 2001; 82: 883–892.
- Arauz-Ruiz P, Norder H, Robertson BH, Magnius LO. Genotype H: a new Amerindian genotype of hepatitis B virus revealed in Central America. J Gen Virol 2002; 83: 2059–2073.
- Bollyky PL, Holmes EC. Reconstructing the complex evolutionary history of hepatitis B virus. J Mol Evol 1999; 49: 130–141.
- Makuwa M, Souquiere S, Telfer P, et al. Occurrence of hepatitis viruses in wild-born non-human primates: a 3 year (1998–32001) epidemiological survey in Gabon. J Med Primatol 2003; 32: 307–314.
- Starkman S, MacDonald DM, Lewis JCM, Holmes EC, Simmonds P. Geographic and species association of hepatitis B virus genotypes in non-human primates. Virology 2003; 314: 381–393.
- Njouom R, Mba SA, Nerrienet E, Foupouapouognigni Y, Rousset D. Detection and characterization of hepatitis B virus strains from wild-caught gorillas and chimpanzees in Cameroon, Central Africa. Infect Genet Evol 2010; 10: 790–796.
- Pybus OG, Barnes E, Taggart R, et al. Genetic history of hepatitis C virus in East Asia. J Virol 2009; 83: 1071–1082.
- Gao F, Bailes E, Robertson DL, et al. Origins of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 1999; 397: 436–441.
- Gao F, Yue L, White AT, et al. Human infection by genetically diverse SIVSM-related HIV-2 in west Africa. Nature 1992; 358: 495–499.
- Simons JN, Pilot-Matias TJ, Leary TP, et al. Identification of two flavivirus-like genomes in the GB hepatitis agent. Proc Natl Acad Sci USA 1995; 92: 3401–3405.
- Muerhoff AS, Leary TP, Simons JN, et al. Genomic organization of GB viruses A and B: two new members of the Flaviviridae associated with GB agent hepatitis. J Virol 1995; 69: 5621–5630.
- Makuwa M, Souquiere S, Telfer P, et al. Hepatitis viruses in non-human primates. J Med Primatol 2006; 35: 384–387.
- Bukh J. Hepatitis C homolog in dogs with respiratory illness. Proc Natl Acad Sci USA 2011; 108: 12563–12564.
- Kapoor A, Simmonds P, Gerold G, et al. Characterization of a canine homolog of hepatitis C virus. Proc Natl Acad Sci USA 2011; 108: 11608–11613.
- Burbelo PD, Dubovi EJ, Simmonds P, et al. Serology-enabled discovery of genetically diverse hepaciviruses in a new host. J Virol 2012; 86: 6171–6178.
- Liu P, Li L, Wang L, et al. Phylogenetic analysis of 626 hepatitis E virus (HEV) isolates from humans and animals in China (1986–2011) showing genotype diversity and zoonotic transmission. Infect Genet Evol 2012; 12: 428–434.
- Takahashi M, Nishizawa T, Sato H, et al. Analysis of the full-length genome of a hepatitis E virus isolate obtained from a wild boar in Japan that is classifiable into a novel genotype. J Gen Virol 2011; 92: 902–908.
- Johne R, Heckel G, Plenge-Bonig A, et al. Novel hepatitis E virus genotype in Norway rats, Germany. Emerg Infect Dis 2010; 16: 1452–1455.
- Gilbert C, Feschotte C. Genomic fossils calibrate the long-term evolution of hepadnaviruses. PLoS Biol 2010; 8: e1000495.
- Katzourakis A, Gifford RJ. Endogenous viral elements in animal genomes. PLoS Genet 2010; 6: e1001191.
- Baylis SA, Hanschmann KM, Blumel J, Nubling CM. Standardization of hepatitis E virus (HEV) nucleic acid amplification technique-based assays: an initial study to evaluate a panel of HEV strains and investigate laboratory performance. J Clin Microbiol 2011; 49: 1234–1239.
- Mulligan EK, Germer JJ, Arens MQ, et al. Detection and quantification of hepatitis C virus (HCV) by MultiCode-RTx real-time PCR targeting the HCV 3′ untranslated region. J Clin Microbiol 2009; 47: 2635–2638.
- Nakatani SM, Santos CA, Riediger IN, et al. Development of hepatitis C virus genotyping by real-time PCR based on the NS5B region. PLoS ONE 2010; 5: e10150.
- Servant-Delmas A, Mercier-Darty M, Ly TD, et al. Variable capacity of 13 hepatitis B virus surface antigen assays for the detection of HBsAg mutants in blood samples. J Clin Virol 2012; 53: 338–345.
- Shrestha MP, Scott RM, Joshi DM, et al. Safety and efficacy of a recombinant hepatitis E vaccine. N Engl J Med 2007; 356: 895–903.
- Zhu FC, Zhang J, Zhang XF, et al. Efficacy and safety of a recombinant hepatitis E vaccine in healthy adults: a large-scale, randomised, double-blind placebo-controlled, phase 3 trial. Lancet 2010; 376: 895–902.
- Shemer-Avni Y, Cohen M, Keren-Naus A, et al. Iatrogenic transmission of hepatitis C virus (HCV) by an anesthesiologist: comparative molecular analysis of the HCV-E1 and HCV-E2 hypervariable regions. Clin Infect Dis 2007; 45: e32–e38.
- Mansuy JM, Huynh A, Abravanel F, Recher C, Peron JM, Izopet J. Molecular evidence of patient-to-patient transmission of hepatitis E virus in a hematology ward. Clin Infect Dis 2009; 48: 373–374.
- Takahashi K, Kitajima N, Abe N, Mishiro S. Complete or near-complete nucleotide sequences of hepatitis E virus genome recovered from a wild boar, a deer, and four patients who ate the deer. Virology 2004; 330: 501–505.
- Grandadam M, Tebbal S, Caron M, et al. Evidence for hepatitis E virus quasispecies. J Gen Virol 2004; 85: 3189–3194.
- van Houdt R, Bruisten SM, Geskus RB, et al. Ongoing transmission of a single hepatitis B virus strain among men having sex with men in Amsterdam. J Viral Hepat 2010; 17: 108–114.
- Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011; 28: 2731–2739.