Recombination in hepatitis C virus

Viruses

Volumn 3, Issue 10, 2011, Pages 2006-2024

  González Candelas, Fernando ^a   Xavier Lopez Labrador F ^a   Bracho, María Alma ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Breakpoint; Congruence; Homoplasy; Phylogenetic tree; Superinfection

Indexed keywords

EVIDENCE BASED MEDICINE; GENE SEQUENCE; GENETIC DISTANCE; GENETIC VARIABILITY; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; NONHUMAN; OUTCOME ASSESSMENT; PHYLOGENETIC TREE; REVIEW; VIRUS DETECTION; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS ISOLATION; VIRUS MORPHOLOGY; VIRUS RECOMBINATION; VIRUS STRAIN;

BREAKPOINT; CONGRUENCE; HOMOPLASY; PHYLOGENETIC TREE; SUPERINFECTION;

DRUG RESISTANCE, VIRAL; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOME, VIRAL; GENOTYPE; HEPACIVIRUS; HEPATITIS C; HUMANS; MUTATION; PHYLOGENY; RECOMBINATION, GENETIC; RNA, VIRAL;

FLAVIVIRUS; HEPATITIS C VIRUS; RNA VIRUSES;

EID: 80055004056     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v3102006     Document Type: Review

References (84)

1. Shepard, C.W.; Finelli, L.; Alter, M.J. Global epidemiology of hepatitis C virus infection. Lancet Infect. Dis. 2005, 5, 558-567.
2. Simmonds, P. Genetic diversity and evolution of hepatitis C virus-15 years on. J. Gen. Virol. 2004, 85, 3173-3188.
3. Kapoor, A.; Simmonds, P.; Gerold, G.; Qaisar, N.; Jain, K.; Henriquez, J.A.; Firth, C.; Hirschberg, D.L.; Rice, C.M.; Shields, S. et al. Characterization of a canine homolog of hepatitis C virus. Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 11608-11613.
4. Walewski, J.L.; Keller, T.R.; Stump, D.D.; Branch, A.D. Evidence for a new hepatitis C virus antigen encoded in an overlapping reading frame. RNA 2001, 7, 710-721.
5. Dubuisson, J. Hepatitis C virus proteins. World J. Gastroenterol. 2007, 13, 2406-2415.
6. Schulze zur Wiesch, J.; Schmitz, H.; Borowski, E.; Borowski, P. The proteins of the Hepatitis C virus: Their features and interactions with intracellular protein phosphorylation. Arch. Virol. 2003, 148, 1247-1267.
7. Simmonds, P.; Holmes, E.C.; Cha, T.A.; Chan, S.W.; McOmish, F.; Irvine, B.; Beall, E.; Yap, P.L.; Kolberg, J.; Urdea, M.S. Classification of hepatitis C virus into six major genotypes and a series of subtypes by phylogenetic analysis of the NS-5 region. J. Gen. Virol. 1993, 74, 2391-2399.
8. Simmonds, P.; Bukh, J.; Combet, C.; Deleage, G.; Enomoto, N.; Feinstone, S.; Halfon, P.; Inchauspe, G.; Kuiken, C.; Maertens, G. et al. Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 2005, 42, 962-973.
9. Hadziyannis, S.J.; Sette, H. Jr.; Morgan, T.R.; Balan, V.; Diago, M.; Marcellin, P.; Ramadori, G.; Bodenheimer, H.C., Jr.; Bernstein, D.; Rizzetto, M. et al. Peginterferon-alpha2a and ribavirin combination therapy in chronic hepatitis C: A randomized study of treatment duration and ribavirin dose. Ann. Intern. Med. 2004, 140, 346-355.
10. Hnatyszyn, H.J. Chronic hepatitis C and genotyping: The clinical significance of determining HCV genotypes. Antivir. Ther. 2005, 10, 1-11.
11. Pybus, O.G.; Cochrane, A.; Holmes, E.C.; Simmonds, P. The hepatitis C virus epidemic among injecting drug users. Infect. Genet. Evol. 2005, 5, 131-139.
12. Thomson, B.J.; Finch, R.G. Hepatitis C virus infection. Clin. Microbiol. Infect. 2005, 11, 86-94.
13. Jimenez-Hernandez, N.; Torres-Puente, M.; Bracho, M.A.; Garcia-Robles, I.; Ortega, E.; Del Olmo, J.; Carnicer, F.; Gonzalez-Candelas, F.; Moya, A. Epidemic dynamics of two coexisting hepatitis C virus subtypes. J. Gen. Virol. 2007, 88, 123-133.
14. Lauer, G.M.; Walker, B.D. Hepatitis C virus infection. N. Engl. J. Med. 2001, 345, 41-52.
15. Amin, J.; Kaye, M.; Skidmore, S.; Pillay, D.; Cooper, D.A.; Dore, G.J. HIV and hepatitis C coinfection within the CAESAR study. HIV Med. 2004, 5, 174-179.
16. Okamoto, H.; Kurai, K.; Okada, S.I.; Yamamoto, K.; Iizuka, H.; Tanaka, T.; Fukuda, S.; Tsuda, F. Full length sequence of hepatitis C virus genome having poor homology to reported isolates: Comparative studiy of four distinct genotypes. J. Gen. Virol. 1992, 188, 331-341.
17. Smith, D.B.; Pathirana, S.; Davidson, F.; Lawlor, E.; Power, J.; Yap, P.L.; Simmonds, P. The origin of hepatitis C virus genotypes. J. Gen. Virol. 1997, 78, 321-328.
18. Zein, N.N. Clinical significance of hepatitis C virus genotypes. Clin. Microbiol. Rev. 2000, 13, 223-235.
19. Farci, P.; Shimoda, A.; Coiana, A.; Diaz, G.; Peddis, G.; Melpolder, J.C.; Strazzera, A.; Chien, D.Y.; Munoz, S.J.; Balestrieri, A. et al. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 2000, 288, 339-344.
20. Farci, P.; Purcell, R.H. Clinical significance of hepatitis C virus genotypes and quasispecies. Semin. Liver Dis. 2000, 20, 103-126.
21. Cuevas, J.M.; Gonzalez-Candelas, F.; Moya, A.; Sanjuan, R. Effect of ribavirin on the mutation rate and spectrum of Hepatitis C virus in vivo. J. Virol. 2009, 83, 5760-5764.
22. Sanjuan, R.; Nebot, M.R.; Chirico, N.; Mansky, L.M.; Belshaw, R. Viral mutation rates. J. Virol. 2010, 84, 9733-9748.
23. Torres-Puente, M.; Cuevas, J.M.; Jiménez, N.; Bracho, M.A.; García-Robles, I.; Carnicer, F.; Del Olmo, J.; Ortega, E.; Moya, A.; González-Candelas, F. Contribution of insertions and deletions to the variability of hepatitis C virus populations. J. Gen. Virol. 2007, 88, 2198-2203.
24. Yun, Z.; Lara, C.; Johansson, B.; Lorenzana, D.R., I; Sonnerborg, A. Discrepancy of hepatitis C virus genotypes as determined by phylogenetic analysis of partial NS5 and core sequences. J. Med. Virol. 1996, 49, 155-160.
25. Viazov, S.; Widell, A.; Nordenfelt, E. Mixed infection with two types of hepatitis C virus is probably a rare event. Infection 2000, 28, 21-25.
26. 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, 4034-4043.
27. Tscherne, D.M.; Evans, M.J.; von Hahn, T.; Jones, C.T.; Stamataki, Z.; McKeating, J.A.; Lindenbach, B.D.; Rice, C.M. Superinfection exclusion in cells infected with hepatitis C virus. J. Virol. 2007, 81, 3693-3703.
28. 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, 1853-1857.
29. Moreau, I.; Hegarty, S.; Levis, J.; Sheehy, P.; Crosbie, O.; Kenny-Walsh, E.; Fanning, L. Serendipitous identification of natural Intergenotypic recombinants of hepatitis C in Ireland. Virol. J. 2006, 3, 95.
30. Kurbanov, F.; Tanaka, Y.; Avazova, D.; Khan, A.; Sugauchi, F.; Kan, N.; Kurbanova-Khudayberganova, D.; Khikmatullaeva, A.; Musabaev, E.; Mizokami, M. Detection of hepatitis C virus natural recombinant RF1_2k/1b strain among intravenous drug users in Uzbekistan. Hepatol. Res. 2008, 38, 457-464.
31. Demetriou, V.L.; Kyriakou, E.; Kostrikis, L.G. Near-full genome characterisation of two natural intergenotypic 2k/1b recombinant Hepatitis C virus isolates. Adv. Virol. 2011, 2011, 710438.
32. Morel, V.; Descamps, V.; Frantois, C.; Fournier, C.; Brochot, E.; Capron, D.; Duverlie, G.; Castelain, S. 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, 382-386.
33. Lee, Y.M.; Lin, H.J.; Chen, Y.J.; Lee, C.M.; Wang, S.F.; Chang, K.Y.; Chen, T.L.; Liu, H.F.; Arthur Chen, Y.M. 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. 2010, 82, 57-68.
34. Cristina, J.; Colina, R. Evidence of structural genomic region recombination in Hepatitis C virus. Virol. J. 2006, 3, 53.
35. Ross, R.S.; Verbeeck, J.; Viazov, S.; Lemey, P.; Ranst, M.V.; Roggendorf, M. Evidence for a complex mosaic genome pattern in a full-length Hepatitis C virus sequence. Evol. Bioinformatics 2008, 2008, 249.
36. Calado, R.A.; Rocha, M.R.; Parreira, R.; Piedade, J.; Venenno, T.; Esteves, A. Hepatitis C virus subtypes circulating among intravenous drug users in Lisbon, Portugal. J. Med. Virol. 2011, 83, 608-615.
37. Colina, R.; Casane, D.; Vasquez, S.; Garcia-Aguirre, L.; Chunga, A.; Romero, H.; Khan, B.; Cristina, J. Evidence of intratypic recombination in natural populations of Hepatitis C virus. J. Gen. Virol. 2004, 85, 31-37.
38. Moreno, P.; Alvarez, M.; Lopez, L.; Moratorio, G.; Casane, D.; Castells, M.; Castro, S.; Cristina, J.; Colina, R. Evidence of recombination in Hepatitis C virus populations infecting a hemophiliac patient. Virol. J. 2009, 6, 203.
39. Noppornpanth, S.; Lien, T.X.; Poovorawan, Y.; Smits, S.L.; Osterhaus, A.D.M.E.; Haagmans, B.L. Identification of a naturally occurring recombinant genotype 2/6 Hepatitis C virus. J. Virol. 2006, 80, 7569-7577.
40. Kageyama, S.; Agdamag, D.M.; Alesna, E.T.; Leano, P.S.; Heredia, A.M.; bellanosa-Tac-An, I.P.; Jereza, L.D.; Tanimoto, T.; Yamamura, J.I.; Ichimura, H. A natural inter-genotypic (2b/1b) recombinant of Hepatitis C virus in the Philippines. J. Med. Virol. 2006, 78, 1423-1428.
41. Legrand-Abravanel, F.; Claudinon, J.; Nicot, F.; Dubois, M.; Chapuy-Regaud, S.; Sandres-Saune, K.; Pasquier, C.; Izopet, J. A new natural intergenotypic (2/5) recombinant of Hepatitis C virus. J. Virol. 2007, 81, 4357-4362.
42. Yokoyama, K.; Takahashi, M.; Nishizawa, T.; Nagashima, S.; Jirintai, S.; Yotsumoto, S.; Okamoto, H.; Momoi, M.Y. Identification and characterization of a natural inter-genotypic (2b/1b) recombinant Hepatitis C virus in Japan. Arch. Virol 2011, 156, 1591-1601.
43. Bhattacharya, D.; Accola, M.; Ansari, I.; Striker, R.; Rehrauer, W. Naturally occurring genotype 2b/1a hepatitis C virus in the United States. Virol. J. 2011, 8, 458.
44. Moreno, M.P.; Casane, D.; Lopez, L.; Cristina, J. Evidence of recombination in quasispecies populations of an Hepatitis C virus patient undergoing anti-viral therapy. Virol. J. 2006, 3, 87.
45. Sentandreu, V.; Jiménez-Hernández, N.; Torres-Puente, M.; Bracho, M.A.; Valero, A.; Gosalbes, M.J.; Ortega, E.; Moya, A.; González-Candelas, F. Evidence of recombination in intrapatient populations of Hepatitis C Virus. PLoS One 2008, 3, e3239.
46. Puig-Basagoiti, F.; Forns, X.; Furcic, I.; Ampurdanes, S.; Gimenez-Barcons, M.; Franco, S.; Sanchez-Tapias, J.M.; Saiz, J.C. 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. 2005, 86, 1067-1075.
47. Martin, D.P.; Lemey, P.; Lott, M.; Moulton, V.; Posada, D.; Lefeuvre, P. RDP3: A flexible and fast computer program for analyzing recombination. Bioinformatics 2010, 26, 2462-2463.
48. Gao, F.; Nainan, O.V.; Khudyakov, Y.; Li, J.; Hong, Y.; Gonzales, A.C.; Spelbring, J.; Margolis, H.S. Recombinant hepatitis C virus in experimentally infected chimpanzees. J. Gen. Virol. 2007, 88, 143-147.
49. Reiter, J.; Perez-Vilaro, G.; Scheller, N.; Mina, L.B.; Diez, J.; Meyerhans, A. Hepatitis C virus RNA recombination in cell culture. J. Hepatol. 2011, 55, 777-783.
50. Bernardin, F.; Herring, B.; Page-Shafer, K.; Kuiken, C.; Delwart, E. Absence of HCV viral recombination following superinfection. J. Viral Hepat. 2006, 13, 532-537.
51. Hmaied, F.; Legrand-Abravanel, F.; Nicot, F.; Garrigues, N.; Chapuy-Regaud, S.; Dubois, M.; Njouom, R.; Izopet, J.; Pasquier, C. Full-length genome sequences of hepatitis C virus subtype 4f. J. Gen. Virol. 2007, 88, 2985-2990.
52. Bracho, M.A.A.; Saludes, V.; Martro, E.; Bargallo, A.; González-Candelas, F.; Ausina, V. Complete genome of a European hepatitis C virus subtype 1g isolate: Phylogenetic and genetic analyses. Virol. J. 2008, 5, 72.
53. Bracho, M.A.; Carrillo-Cruz, F.Y.; Ortega, E.; Moya, A.; Gonzalez-Candelas, 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, 1697-1702.
54. Martró, E.; Valero, A.; Jordana-Lluch, E.; Saludes, V.; Planas, R.; González-Candelas, F.; Ausina, V.; Bracho, M.A. Hepatitis C virus sequences from different patients confirm the existence and transmissibility of subtype 2q, a rare subtype circulating in the metropolitan area of Barcelona, Spain. J. Med. Virol. 2011, 83, 820-826.
55. Gupte, G.M.; Ramdasi, A.Y.; Kulkarni, A.S.; Arankalle, V.A. Complete genome sequences of hepatitis C virus subtype 3i and 3a subtype isolates from India. Indian J. Gastroenterol. 2010, 29, 101-105.
56. Kuntzen, T.; Berical, A.; Ndjomou, J.; Bennett, P.; Schneidewind, A.; Lennon, N.; Birren, B.W.; Kuiken, C.; Henn, M.R.; Simmonds, P. et al. A set of reference sequences for the hepatitis C genotypes 4d, 4f, and 4k covering the full open reading frame. J. Med. Virol. 2008, 80, 1370-1378.
57. Lu, L.; Li, C.; Fu, Y.; Gao, F.; Pybus, O.G.; Abe, K.; Okamoto, H.; Hagedorn, C.H.; Murphy, D. 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. 2007, 88, 1519-1525.
58. Viazov, S.; Ross, S.S.; Kyuregyan, K.K.; Timm, J.; Neumann-Haefelin, C.; Isaeva, O.V.; Popova, O.E.; Dmitriev, P.N.; El, S.F.; Thimme, R. et al. Hepatitis C virus recombinants are rare even among intravenous drug users. J. Med. Virol. 2010, 82, 232-238.
59. Magiorkinis, G.; Ntziora, F.; Paraskevis, D.; Magiorkinis, E.; Hatzakis, A. Analysing the evolutionary history of HCV: Puzzle of ancient phylogenetic discordance. Infect. Genet. Evol. 2007, 7, 354-360.
60. Schaller, T.; Appel, N.; Koutsoudakis, G.; Kallis, S.; Lohmann, V.; Pietschmann, T.; Bartenschlager, R. Analysis of hepatitis C virus superinfection exclusion by using novel fluorochrome gene-tagged viral genomes. J. Virol. 2007, 81, 4591-4603.
61. Pham, S.T.; Bull, R.A.; Bennett, J.M.; Rawlinson, W.D.; Dore, G.J.; Lloyd, A.R.; White, P.A. Frequent multiple hepatitis C virus infections among injection drug users in a prison setting. Hepatology 2010, 52, 1564-1572.
62. Van Asten, L.; Prins, M. Infection with concurrent multiple hepatitis C virus genotypes is associated with faster HIV disease progression. AIDS 2004, 18, 2319-2324.
63. van de Laar, T.J.W.; Molenkamp, R.; van den Berg, C.; Schinkel, J.; Beld, M.G.H.M.; Prins, M.; Coutinho, R.A.; Bruisten, S.M. Frequent HCV reinfection and superinfection in a cohort of injecting drug users in Amsterdam. J. Hepatol. 2009, 51, 667-674.
64. Martro, E.; Gonzalez, V.; Buckton, A.J.; Saludes, V.; Fernandez, G.; Matas, L.; Planas, R.; Ausina, V. Evaluation of a new assay in comparison with reverse hybridization and sequencing methods for Hepatitis C Virus genotyping targeting both 5' noncoding and nonstructural 5b genomic regions. J. Clin. Microbiol. 2008, 46, 192-197.
65. Mes, T.H.M.; van Doornum, G.J.J. Recombination in hepatitis C virus genotype 1 evaluated by phylogenetic and population-genetic methods. J. Gen. Virol. 2011, 92, 279-286.
66. Betran, E.; Rozas, J.; Navarro, A.; Barbadilla, A. The estimation of the number and the length distribution of gene conversion tracts from population DNA sequence data. Genetics 1997, 146, 89-99.
67. Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 2000, 17, 540-552.
68. Capella-Gutierrez, S.; Silla-Martinez, J.M.; Gabaldon, T. Trimal: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009, 25, 1972-1973.
69. 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.
70. Kumar, S.; Filipski, A. Multiple sequence alignment: In pursuit of homologous DNA positions. Genome Res. 2007, 17, 127-135.
71. Kemena, C.; Notredame, C. Upcoming challenges for multiple sequence alignment methods in the high-throughput era. Bioinformatics 2009, 25, 2455-2465.
72. Thompson, J.D.; Linard, B.; Lecompte, O.; Poch, O. A Comprehensive benchmark study of multiple sequence alignment methods: Current challenges and future perspectives. PLoS One 2011, 6, e18093.
73. Wilm, A.; Higgins, D.G.; Notredame, C. R-Coffee: A method for multiple alignment of non-coding RNA. Nucl. Acids Res. 2008, 36, e52.
74. Nawrocki, E.P.; Kolbe, D.L.; Eddy, S.R. Infernal 1.0: Inference of RNA alignments. Bioinformatics 2009, 25, 1335-1337.
75. Strimmer, K.; von Haeseler, A. Likelihood mapping: A simple method to visualize phylogenetic content of a sequence alignment. Proc. Natl. Acad. Sci. U. S. A. 1997, 94, 6815-6819.
76. Strimmer, K.; von Haeseler, A. Quartet puzzling: A quartet maximum-likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 1996, 13, 964-969.
77. Posada, D. Jmodeltest: Phylogenetic model averaging. Mol. Biol. Evol. 2008, 25, 1253-1256.
78. Darriba, D.; Taboada, G.L.; Doallo, R.N.; Posada, D. ProtTest 3: Fast selection of best-fit models of protein evolution. Bioinformatics 2011, 27, 1164-1165.
79. Posada, D.; Crandall, K.A. Selecting the best-fit model of nucleotide substitution. Syst. Biol. 2001, 50, 580-601.
80. Shimodaira, H.; Hasegawa, M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 1999, 16, 1114-1116.
81. Strimmer, K.; Rambaut, A. Inferring confidence sets of possibly misspecified gene trees. Proc. R. Soc. Lond. Ser. B 2002, 269, 137-142.
82. Morel, V.; Fournier, C.; François, C.; Brochot, E.; Helle, F.; Duverlie, G.; Castelain, S. Genetic recombination of the hepatitis C virus: Clinical implications. J. Viral Hepat. 2011, 18, 77-83.
83. Bartels, D.J.; Zhou, Y.; Zhang, E.Z.; Marcial, M.; Byrn, R.A.; Pfeiffer, T.; Tigges, A.M.; Adiwijaya, B.S.; Lin, C.; Kwong, A.D. et al. Natural prevalence of Hepatitis C Virus variants with decreased sensitivity to NS3.4A protease inhibitors in treatment-naive subjects. J. Infect. Dis. 2008, 198, 800-807.
84. López-Labrador, F.X.; Moya, A.; González-Candelas, F. Mapping natural polymorphisms of hepatitis C virus NS3/4A protease and antiviral resistance to inhibitors in worldwide isolates. Antivir. Ther. 2008, 13, 481-494.