1887

Abstract

We characterized the full-length genomes of nine hepatitis C virus genotype 3 (HCV-3) isolates: QC7, QC8, QC9, QC10, QC34, QC88, NE145, NE274 and 811. To the best of our knowledge, NE274 and NE145 were the first full-length genomes for confirming the provisionally assigned subtypes 3d and 3e, respectively, whereas 811 represented the first HCV-3 isolate that had its extreme 3′ UTR terminus sequenced. Based on these full-length genomes, together with 42 references representing eight assigned subtypes and an unclassified variant of HCV-3, and 10 sequences of six other genotypes, a timescaled phylogenetic tree was reconstructed after an evolutionary analysis using a coalescent Bayesian procedure. The results indicated that subtypes 3a, 3d and 3e formed a subset with a common ancestor dated to ~202.89 [95 % highest posterior density (HPD): 160.11, 264.6] years ago. The analysis of all of the HCV-3 sequences as a single lineage resulted in the dating of the divergence time to ~457.81 (95 % HPD: 350.62, 587.53) years ago, whereas the common ancestor of all of the seven HCV genotypes dated to ~780.86 (95 % HPD: 592.15, 1021.34) years ago. As subtype 3h and the unclassified variant were relatives, and represented the oldest HCV-3 lineages with origins in Africa and the Middle East, these findings may indicate the ancestral origin of HCV-3 in Africa. We speculate that the ancestral HCV-3 strains may have been brought to South Asia from Africa by land and/or across the sea to result in its indigenous circulation in that region. The spread was estimated to have occurred in the era after Vasco da Gama had completed his expeditions by sailing along the eastern coast of Africa to India. However, before this era, Arabians had practised slave trading from Africa to the Middle East and South Asia for centuries, which may have mediated the earliest spread of HCV-3.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.065128-0
2014-08-01
2019-11-22
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/8/1677.html?itemId=/content/journal/jgv/10.1099/vir.0.065128-0&mimeType=html&fmt=ahah

References

  1. Abid K. , Quadri R. , Veuthey A. L. , Hadengue A. , Negro F. . ( 2000; ). A novel hepatitis C virus (HCV) subtype from Somalia and its classification into HCV clade 3. . J Gen Virol 81:, 1485–1493.[PubMed]
    [Google Scholar]
  2. Abid K. , Pazienza V. , de Gottardi A. , Rubbia-Brandt L. , Conne B. , Pugnale P. , Rossi C. , Mangia A. , Negro F. . ( 2005; ). An in vitro model of hepatitis C virus genotype 3a-associated triglycerides accumulation. . J Hepatol 42:, 744–751. [CrossRef] [PubMed]
    [Google Scholar]
  3. Alter M. J. . ( 1999; ). Hepatitis C virus infection in the United States. . J Hepatol 31: (Suppl. 1), 88–91. [CrossRef] [PubMed]
    [Google Scholar]
  4. Amini S. , Ahmadi Pour M. H. , Azadmanesh K. . ( 2006; ). The phylogenetic analysis of hepatitis C virus isolates obtained from two Iranian carriers revealed evidence for a new subtype of HCV genotype 3. . Virus Genes 33:, 271–278.[PubMed]
    [Google Scholar]
  5. Bernier L. , Willems B. , Delage G. , Murphy D. G. . ( 1996; ). Identification of numerous hepatitis C virus genotypes in Montreal, Canada. . J Clin Microbiol 34:, 2815–2818.[PubMed]
    [Google Scholar]
  6. Blight K. J. , Rice C. M. . ( 1997; ). Secondary structure determination of the conserved 98-base sequence at the 3′ terminus of hepatitis C virus genome RNA. . J Virol 71:, 7345–7352.[PubMed]
    [Google Scholar]
  7. Bochud P. Y. , Cai T. , Overbeck K. , Bochud M. , Dufour J. F. , Müllhaupt B. , Borovicka J. , Heim M. , Moradpour D. . & other authors ( 2009; ). Genotype 3 is associated with accelerated fibrosis progression in chronic hepatitis C. . J Hepatol 51:, 655–666. [CrossRef] [PubMed]
    [Google Scholar]
  8. Bourlière M. , Barberin J. M. , Rotily M. , Guagliardo V. , Portal I. , Lecomte L. , Benali S. , Boustière C. , Perrier H. . & other authors ( 2002; ). Epidemiological changes in hepatitis C virus genotypes in France: evidence in intravenous drug users. . J Viral Hepat 9:, 62–70. [CrossRef] [PubMed]
    [Google Scholar]
  9. Castillo I. , Rodríguez-Iñigo E. , López-Alcorocho J. M. , Pardo M. , Bartolomé J. , Carreño V. . ( 2006; ). Hepatitis C virus replicates in the liver of patients who have a sustained response to antiviral treatment. . Clin Infect Dis 43:, 1277–1283. [CrossRef] [PubMed]
    [Google Scholar]
  10. Chowdhury A. , Santra A. , Chaudhuri S. , Dhali G. K. , Chaudhuri S. , Maity S. G. , Naik T. N. , Bhattacharya S. K. , Mazumder D. N. . ( 2003; ). Hepatitis C virus infection in the general population: a community-based study in West Bengal, India. . Hepatology 37:, 802–809.[CrossRef]
    [Google Scholar]
  11. Colson P. , Gayet S. , Gerolami R. . ( 2011; ). NS3 protease of genotype 3 subtype h HCV identified in southeastern France. . Antivir Ther 16:, 615–619. [CrossRef] [PubMed]
    [Google Scholar]
  12. Corbet S. , Bukh J. , Heinsen A. , Fomsgaard A. . ( 2003; ). Hepatitis C virus subtyping by a core-envelope 1-based reverse transcriptase PCR assay with sequencing and its use in determining subtype distribution among Danish patients. . J Clin Microbiol 41:, 1091–1100. [CrossRef] [PubMed]
    [Google Scholar]
  13. Drummond A. J. , Rambaut A. . ( 2007; ). beast: Bayesian evolutionary analysis by sampling trees. . BMC Evol Biol 7:, 214. [CrossRef] [PubMed]
    [Google Scholar]
  14. Feld J. J. , Hoofnagle J. H. . ( 2005; ). Mechanism of action of interferon and ribavirin in treatment of hepatitis C. . Nature 436:, 967–972.[CrossRef]
    [Google Scholar]
  15. Gordon M. . ( 1989; ). Slavery in the Arab World. New York:: New Amsterdam Press;.
    [Google Scholar]
  16. Greene W. K. , Cheong M. K. , Ng V. , Yap K. W. . ( 1995; ). Prevalence of hepatitis C virus sequence variants in South-East Asia. . J Gen Virol 76:, 211–215. [CrossRef] [PubMed]
    [Google Scholar]
  17. Hoofnagle J. H. . ( 2002; ). Course and outcome of hepatitis C. . Hepatology 36: (Suppl 1), S21–S29. [CrossRef] [PubMed]
    [Google Scholar]
  18. Hotta H. , Handajani R. , Lusida M. I. , Soemarto W. , Doi H. , Miyajima H. , Homma M. . ( 1994; ). Subtype analysis of hepatitis C virus in Indonesia on the basis of NS5b region sequences. . J Clin Microbiol 32:, 3049–3051.[PubMed]
    [Google Scholar]
  19. Hourioux C. , Patient R. , Morin A. , Blanchard E. , Moreau A. , Trassard S. , Giraudeau B. , Roingeard P. . ( 2007; ). The genotype 3-specific hepatitis C virus core protein residue phenylalanine 164 increases steatosis in an in vitro cellular model. . Gut 56:, 1302–1308. [CrossRef] [PubMed]
    [Google Scholar]
  20. Jackel-Cram C. , Babiuk L. A. , Liu Q. . ( 2007; ). Up-regulation of fatty acid synthase promoter by hepatitis C virus core protein: genotype-3a core has a stronger effect than genotype-1b core. . J Hepatol 46:, 999–1008. [CrossRef] [PubMed]
    [Google Scholar]
  21. Kolykhalov A. A. , Feinstone S. M. , Rice C. M. . ( 1996; ). Identification of a highly conserved sequence element at the 3′ terminus of hepatitis C virus genome RNA. . J Virol 70:, 3363–3371.[PubMed]
    [Google Scholar]
  22. Kuiken C. , Combet C. , Bukh J. , Shin-I T. , Deleage G. , Mizokami M. , Richardson R. , Sablon E. , Yusim K. . & other authors ( 2006; ). A comprehensive system for consistent numbering of HCV sequences, proteins and epitopes. . Hepatology 44:, 1355–1361. [CrossRef] [PubMed]
    [Google Scholar]
  23. Lee Y. M. , Lin H. J. , Chen Y. J. , Lee C. M. , Wang S. F. , Chang K. Y. , Chen T. L. , Liu H. F. , Chen Y. M. . ( 2010; ). Molecular epidemiology of HCV genotypes among injection drug users in Taiwan: full-length sequences of two new subtype 6w strains and a recombinant form_2b6w. . J Med Virol 82:, 57–68. [CrossRef] [PubMed]
    [Google Scholar]
  24. Legrand-Abravanel F. , Claudinon J. , Nicot F. , Dubois M. , Chapuy-Regaud S. , Sandres-Saune K. , Pasquier C. , Izopet J. . ( 2007; ). New natural intergenotypic (2/5) recombinant of hepatitis C virus. . J Virol 81:, 4357–4362. [CrossRef] [PubMed]
    [Google Scholar]
  25. Li C. , Cao H. , Lu L. , Murphy D. . ( 2012; ). 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 93:, 1173–1184. [CrossRef] [PubMed]
    [Google Scholar]
  26. Lole K. S. , Jha J. A. , Shrotri S. P. , Tandon B. N. , Prasad V. G. , Arankalle V. A. . ( 2003; ). Comparison of hepatitis C virus genotyping by 5′ noncoding region- and core-based reverse transcriptase PCR assay with sequencing and use of the assay for determining subtype distribution in India. . J Clin Microbiol 41:, 5240–5244. [CrossRef] [PubMed]
    [Google Scholar]
  27. Lu L. , Nakano T. , He Y. , Fu Y. , Hagedorn C. H. , Robertson B. H. . ( 2005; ). Hepatitis C virus genotype distribution in China: predominance of closely related subtype 1b isolates and existence of new genotype 6 variants. . J Med Virol 75:, 538–549. [CrossRef] [PubMed]
    [Google Scholar]
  28. Lu L. , Li C. , Fu Y. , Gao F. , Pybus O. G. , Abe K. , Okamoto H. , Hagedorn C. H. , Murphy D. . ( 2007; ). Complete genomes of hepatitis C virus (HCV) subtypes 6c, 6l, 6o, 6p and 6q: completion of a full panel of genomes for HCV genotype 6. . J Gen Virol 88:, 1519–1525. [CrossRef] [PubMed]
    [Google Scholar]
  29. Lu L. , Tatsunori N. , Li C. , Waheed S. , Gao F. , Robertson B. H. . ( 2008; ). HCV selection and HVR1 evolution in a chimpanzee chronically infected with HCV-1 over 12 years. . Hepatol Res 38:, 704–716. [CrossRef] [PubMed]
    [Google Scholar]
  30. Lu L. , Li C. , Yuan J. , Lu T. , Okamoto H. , Murphy D. G. . ( 2013; ). Full-length genome sequences of five hepatitis C virus isolates representing subtypes 3g, 3h, 3i and 3k, and a unique genotype 3 variant. . J Gen Virol 94:, 543–548. [CrossRef] [PubMed]
    [Google Scholar]
  31. Manns M. P. , Wedemeyer H. , Cornberg M. . ( 2006; ). Treating viral hepatitis C: efficacy, side effects, and complications. . Gut 55:, 1350–1359. [CrossRef] [PubMed]
    [Google Scholar]
  32. Martin D. P. , Lemey P. , Lott M. , Moulton V. , Posada D. , Lefeuvre P. . ( 2010; ). rdp3: a flexible and fast computer program for analyzing recombination. . Bioinformatics 26:, 2462–2463. [CrossRef] [PubMed]
    [Google Scholar]
  33. McCaw R. , Moaven L. , Locarnini S. A. , Bowden D. S. . ( 1997; ). Hepatitis C virus genotypes in Australia. . J Viral Hepat 4:, 351–357. [CrossRef] [PubMed]
    [Google Scholar]
  34. Murphy D. G. , Willems B. , Deschênes M. , Hilzenrat N. , Mousseau R. , Sabbah S. . ( 2007; ). Use of sequence analysis of the NS5B region for routine genotyping of hepatitis C virus with reference to C/E1 and 5′ untranslated region sequences. . J Clin Microbiol 45:, 1102–1112. [CrossRef] [PubMed]
    [Google Scholar]
  35. Negro F. . ( 2006; ). Mechanisms and significance of liver steatosis in hepatitis C virus infection. . World J Gastroenterol 12:, 6756–6765.[PubMed]
    [Google Scholar]
  36. Newman R. M. , Kuntzen T. , Weiner B. , Berical A. , Charlebois P. , Kuiken C. , Murphy D. G. , Simmonds P. , Bennett P. . & other authors ( 2013; ). Whole genome pyrosequencing of rare hepatitis C virus genotypes enhances subtype classification and identification of naturally occurring drug resistance variants. . J Infect Dis 208:, 17–31. [CrossRef] [PubMed]
    [Google Scholar]
  37. Nkontchou G. , Ziol M. , Aout M. , Lhabadie M. , Baazia Y. , Mahmoudi A. , Roulot D. , Ganne-Carrie N. , Grando-Lemaire V. . & other authors ( 2011; ). HCV genotype 3 is associated with a higher hepatocellular carcinoma incidence in patients with ongoing viral C cirrhosis. . J Viral Hepat 18:, e516–e522. [CrossRef] [PubMed]
    [Google Scholar]
  38. Okamoto H. , Kojima M. , Sakamoto M. , Iizuka H. , Hadiwandowo S. , Suwignyo S. , Miyakawa Y. , Mayumi M. . ( 1994; ). The entire nucleotide sequence and classification of a hepatitis C virus isolate of a novel genotype from an Indonesian patient with chronic liver disease. . J Gen Virol 75:, 629–635. [CrossRef] [PubMed]
    [Google Scholar]
  39. Panigrahi A. K. , Roca J. , Acharya S. K. , Jameel S. , Panda S. K. . ( 1996; ). Genotype determination of hepatitis C virus from northern India: identification of a new subtype. . J Med Virol 48:, 191–198. [CrossRef] [PubMed]
    [Google Scholar]
  40. Pawlotsky J. M. , Tsakiris L. , Roudot-Thoraval F. , Pellet C. , Stuyver L. , Duval J. , Dhumeaux D. . ( 1995; ). Relationship between hepatitis C virus genotypes and sources of infection in patients with chronic hepatitis C. . J Infect Dis 171:, 1607–1610. [CrossRef] [PubMed]
    [Google Scholar]
  41. Ross R. S. , Viazov S. O. , Holtzer C. D. , Beyou A. , Monnet A. , Mazure C. , Roggendorf M. . ( 2000; ). Genotyping of hepatitis C virus isolates using CLIP sequencing. . J Clin Microbiol 38:, 3581–3584.[PubMed]
    [Google Scholar]
  42. Rubbia-Brandt L. , Quadri R. , Abid K. , Giostra E. , Malé P. J. , Mentha G. , Spahr L. , Zarski J. P. , Borisch B. . & other authors ( 2000; ). Hepatocyte steatosis is a cytopathic effect of hepatitis C virus genotype 3. . J Hepatol 33:, 106–115. [CrossRef] [PubMed]
    [Google Scholar]
  43. Samimi-Rad K. , Asgari F. , Nasiritoosi M. , Esteghamati A. , Azarkeyvan A. , Eslami S. M. , Zamani F. , Magnius L. , Alavian S. M. , Norder H. . ( 2013; ). Patient-to-patient transmission of hepatitis C at Iranian thalassemia centers shown by genetic characterization of viral strains. . Hepat Mon 13:, e7699. [CrossRef] [PubMed]
    [Google Scholar]
  44. Silini E. , Bono F. , Cividini A. , Cerino A. , Maccabruni A. , Tinelli C. , Bruno S. , Bellobuono A. , Mondelli M. . ( 1995; ). Molecular epidemiology of hepatitis C virus infection among intravenous drug users. . J Hepatol 22:, 691–695. [CrossRef] [PubMed]
    [Google Scholar]
  45. Simmonds P. , Mellor J. , Sakuldamrongpanich T. , Nuchaprayoon C. , Tanprasert S. , Holmes E. C. , Smith D. B. . ( 1996; ). Evolutionary analysis of variants of hepatitis C virus found in South-East Asia: comparison with classifications based upon sequence similarity. . J Gen Virol 77:, 3013–3024. [CrossRef] [PubMed]
    [Google Scholar]
  46. Simmonds P. , Bukh J. , Combet C. , Deléage G. , Enomoto N. , Feinstone S. , Halfon P. , Inchauspé G. , Kuiken C. . & other authors ( 2005; ). Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. . Hepatology 42:, 962–973. [CrossRef] [PubMed]
    [Google Scholar]
  47. Smith D. B. , Bukh J. , Kuiken C. , Muerhoff A. S. , Rice C. M. , Stapleton J. T. , Simmonds P. . ( 2014; ). Expanded classification of hepatitis C virus into 7 genotypes and 67 subtypes: updated criteria and genotype assignment web resource. . Hepatology 59:, 318–327. [CrossRef] [PubMed]
    [Google Scholar]
  48. Stuyver L. , Wyseur A. , van Arnhem W. , Hernandez F. , Maertens G. . ( 1996; ). Second-generation line probe assay for hepatitis C virus genotyping. . J Clin Microbiol 34:, 2259–2266.[PubMed]
    [Google Scholar]
  49. Tamura K. , Peterson D. , Peterson N. , Stecher G. , Nei M. , Kumar S. . ( 2011; ). mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. . Mol Biol Evol 28:, 2731–2739. [CrossRef] [PubMed]
    [Google Scholar]
  50. Thiel H. J. , Collett M. S. , Gould E. A. , Heinz F. X. , Houghton M. , Meyers G. , Purcell R. H. , Rice C. M. . ( 2005; ). Flaviviridae. . In Virus Taxonomy: VIIIth Report of the International Committee on Taxonomy of Viruses, pp. 981–998. Edited by Fauquet C. M. , Mayo, M. , Maniloff J. , Desselberger U. , Ball L. A. . . San Diego, CA:: Academic Press;.
    [Google Scholar]
  51. Tippmann H. F. . ( 2004; ). Analysis for free: comparing programs for sequence analysis. . Brief Bioinform 5:, 82–87. [CrossRef] [PubMed]
    [Google Scholar]
  52. Tokita H. , Shrestha S. M. , Okamoto H. , Sakamoto M. , Horikita M. , Iizuka H. , Shrestha S. , Miyakawa Y. , Mayumi M. . ( 1994; ). Hepatitis C virus variants from Nepal with novel genotypes and their classification into the third major group. . J Gen Virol 75:, 931–936. [CrossRef] [PubMed]
    [Google Scholar]
  53. Tokita H. , Okamoto H. , Iizuka H. , Kishimoto J. , Tsuda F. , Lesmana L. A. , Miyakawa Y. , Mayumi M. . ( 1996; ). Hepatitis C virus variants from Jakarta, Indonesia classifiable into novel genotypes in the second (2e and 2f), tenth (10a) and eleventh (11a) genetic groups. . J Gen Virol 77:, 293–301. [CrossRef] [PubMed]
    [Google Scholar]
  54. Valliammai T. , Thyagarajan S. P. , Zuckerman A. J. , Harrison T. J. . ( 1995; ). Diversity of genotypes of hepatitis C virus in southern India. . J Gen Virol 76:, 711–716. [CrossRef] [PubMed]
    [Google Scholar]
  55. van der Meer A. J. , Veldt B. J. , Feld J. J. , Wedemeyer H. , Dufour J. F. , Lammert F. , Duarte-Rojo A. , Heathcote E. J. , Manns M. P. . & other authors ( 2012; ). Association between sustained virological response and all-cause mortality among patients with chronic hepatitis C and advanced hepatic fibrosis. . JAMA 308:, 2584–2593. [CrossRef] [PubMed]
    [Google Scholar]
  56. van Doorn L. J. , Kleter B. , Stuyver L. , Maertens G. , Brouwer H. , Schalm S. , Heijtink R. , Quint W. . ( 1994; ). Analysis of hepatitis C virus genotypes by a line probe assay and correlation with antibody profiles. . J Hepatol 21:, 122–129. [CrossRef] [PubMed]
    [Google Scholar]
  57. Wang H. , Yuan Z. , Barnes E. , Yuan M. , Li C. , Fu Y. , Xia X. , Li G. , Newton P. N. . & other authors ( 2013; ). Eight novel hepatitis C virus genomes reveal the changing taxonomic structure of genotype 6. . J Gen Virol 94:, 76–80. [CrossRef] [PubMed]
    [Google Scholar]
  58. Williams I. . ( 1999; ). Epidemiology of hepatitis C in the United States. . Am J Med 107: (Suppl 2), 2–9. [CrossRef] [PubMed]
    [Google Scholar]
  59. Xu R. , Tong W. , Gu L. , Li C. , Fu Y. , Lu L. . ( 2013; ). A panel of full-length HCV genome sequences characterized in China representing 11 subtypes and two novel variants. . Infect Genet Evol 20:, 225–229.[CrossRef]
    [Google Scholar]
  60. Yamada N. , Tanihara K. , Takada A. , Yorihuzi T. , Tsutsumi M. , Shimomura H. , Tsuji T. , Date T. . ( 1996; ). Genetic organization and diversity of the 3′ noncoding region of the hepatitis C virus genome. . Virology 223:, 255–261. [CrossRef] [PubMed]
    [Google Scholar]
  61. Yuan M. , Lu T. , Li C. , Lu L. . ( 2013; ). The evolutionary rates of HCV estimated with subtype 1a and 1b sequences over the ORF length and in different genomic regions. . PLoS ONE 8:, e64698. [CrossRef] [PubMed]
    [Google Scholar]
  62. Zoulim F. , Chevallier M. , Maynard M. , Trepo C. . ( 2003; ). Clinical consequences of hepatitis C virus infection. . Rev Med Virol 13:,57–68. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.065128-0
Loading
/content/journal/jgv/10.1099/vir.0.065128-0
Loading

Data & Media loading...

Supplements

Supplementary Material 

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error