Identification, molecular cloning, and analysis of full-length hepatitis C virus transmitted/founder genotypes 1, 3, and 4

mBio

Volumn 6, Issue 2, 2015, Pages

  Stoddard, Mark B ^a   Li, Hui ^a   Wang, Shuyi ^a   Saeed, Mohsan ^b   Andrus, Linda ^b   Ding, Wenge ^a   Jiang, Xinpei ^a   Learn, Gerald H ^a   von Schaewen, Markus ^c   Wen, Jessica ^a   Goepfert, Paul A ^d   Hahn, Beatrice H ^a   Ploss, Alexander ^c   Rice, Charles M ^b   Shawa, George M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c PRINCETON UNIVERSITY   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS DNA;

3' UNTRANSLATED REGION; ACUTE HEPATITIS C; AMINO ACID SUBSTITUTION; AMPLICON; ARTICLE; CHRONIC HEPATITIS C; CONTROLLED STUDY; GENE REPLICATION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC VARIABILITY; GENOTYPE; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; MOLECULAR CLONING; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROGENY; PROTEIN GLYCOSYLATION; SEQUENCE ALIGNMENT; VIRUS CELL INTERACTION; VIRUS ENVELOPE; VIRUS GENE; VIRUS IDENTIFICATION; VIRUS STRAIN; VIRUS TRANSMISSION; CLASSIFICATION; DNA SEQUENCE; GENETIC VARIATION; GENETICS; HEPACIVIRUS; HEPATITIS C; HUMAN IMMUNODEFICIENCY VIRUS 1; ISOLATION AND PURIFICATION; MOLECULAR GENETICS; TRANSMISSION; VIROLOGY; VIRUS GENOME;

EBOLA VIRUS; HEPATITIS C VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; RNA VIRUSES;

CLONING, MOLECULAR; GENETIC VARIATION; GENOME, VIRAL; GENOTYPE; HEPACIVIRUS; HEPATITIS C; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA;

EID: 84929497785     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02518-14     Document Type: Article

References (114)

1. Lindenbach BD, Thiel HJ, Rice CM. 2007. Flaviviridae: the viruses and their replication, p 1101–1152. In Knipe DM, Howley PM (ed), Fields virology, vol 1, 5th ed, vol 1. Lippincott Williams & Wilkins, Philadelphia, PA.
2. Ray SC, Thomas DL. 2009. Hepatitis C, p 2157–2185. In Mandell GL, Bennett JE, Colin R (ed), Principles and practice of infectious diseases, 7th ed. Churchill Livingstone, Philadelphia, PA.
3. Averhoff FM, Glass N, Holtzman D. 2012. Global burden of hepatitis C: considerations for healthcare providers in the United States. Clin Infect Dis 55(Suppl 1):S10–S15.http://dx.doi.org/10.1093/cid/cis361.
4. Farci P. 2011. New insights into theHCVquasispecies and compartmentalization. Semin Liver Dis 31:356–374.http://dx.doi.org/10.1055/s-0031-1297925.
5. Simmonds P, Bukh J, Combet C, Deléage G, Enomoto N, Feinstone S, Halfon P, Inchauspé G, Kuiken C, Maertens G, Mizokami M, Murphy DG, Okamoto H, Pawlotsky JM, Penin F, Sablon E, Shin I T, Stuyver LJ, Thiel HJ, Viazov S, Weiner AJ, Widell A. 2005. Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 42:962–973.http://dx.doi.org/10.1002/hep.20819.
6. Smith DB, Bukh J, Kuiken C, Muerhoff AS, Rice CM, Stapleton JT, 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.http://dx.doi.org/10.1002/hep.26744.
7. Wang GP, Sherrill-Mix SA, Chang K-M, Quince C, Bushman FD. 2010. Hepatitis C virus transmission bottlenecks analyzed by deep sequencing. J Virol 84:6218–6228.http://dx.doi.org/10.1128/JVI.02271-09.
8. Bull RA, Luciani F, McElroy K, Gaudieri S, Pham ST, Chopra A, Cameron B, Maher L, Dore GJ, White PA, Lloyd AR. 2011. Sequential bottlenecks drive viral evolution in early acute hepatitis C virus infection. PLoS Pathog 7:e1002243.http://dx.doi.org/10.1371/journal.ppat.1002243.
9. Li H, Stoddard MB, Wang S, Blair LM, Giorgi EE, Parrish EH, Learn GH, Hraber P, Goepfert PA, Saag MS, Denny TN, Haynes BF, Hahn BH, Ribeiro RM, Perelson AS, Korber BT, Bhattacharya T, Shaw GM. 2012. Elucidation of hepatitis C virus transmission and early diversification by single genome sequencing. PLoS Pathog 8:e1002880.http://dx.doi.org/10.1371/journal.ppat.1002880.
10. Ribeiro RM, Li H, Wang S, Stoddard MB, Learn GH, Korber BT, Bhattacharya T, Guedj J, Parrish EH, Hahn BH, Shaw GM, Perelson AS. 2012. Quantifying the diversification of hepatitis C virus (HCV) during primary infection: estimates of the in vivo mutation rate. PLoS Pathog 8:e1002881.http://dx.doi.org/10.1371/journal.ppat.1002881.
11. Kolykhalov AA, Agapov EV, Blight KJ, Mihalik K, Feinstone SM, Rice CM. 1997. Transmission of hepatitis C by intrahepatic inoculation with transcribed RNA. Science 277:570–574.http://dx.doi.org/10.1126/science.277.5325.570.
12. Yanagi M, Purcell RH, Emerson SU, Bukh J. 1997. Transcripts from a single full-length cDNA clone of hepatitis C virus are infectious when directly transfected into the liver of a chimpanzee. Proc Natl Acad Sci U S A 94:8738–8743.http://dx.doi.org/10.1073/pnas.94.16.8738.
13. Lanford RE, Lee H, Chavez D, Guerra B, Brasky KM. 2001. Infectious cDNA clone of the hepatitis C virus genotype 1 prototype sequence. J Gen Virol 82:1291–1297.
14. Gottwein JM, Scheel TK, Callendret B, Li Y-P, Eccleston HB, Engle RE, Govindarajan S, Satterfield W, Purcell RH, Walker CM, Bukh J. 2010. Novel infectious cDNA clones of hepatitis C virus genotype 3a (strain S52) and 4a (strain ED43): genetic analyses and in vivo pathogenesis studies. J Virol 84:5277–5293.http://dx.doi.org/10.1128/JVI.02667-09.
15. Hui JM, Kench J, Farrell GC, Lin R, Samarasinghe D, Liddle C, Byth K, George J. 2002. Genotype-specific mechanisms for hepatic steatosis in chronic hepatitis C infection. J Gastroenterol Hepatol 17:873–881.http://dx.doi.org/10.1046/j.1440-1746.2002.02813.x.
16. Talaat M, Kandeel A, Rasslan O, Hajjeh R, Hallaj Z, El-Sayed N, Mahoney FJ. 2006. Evolution of infection control in Egypt: achievements and challenges. Am J Infect Control 34:193–200.http://dx.doi.org/10.1016/j.ajic.2005.05.028.
17. Lu L, Li C, Yuan J, Lu T, Okamoto H, Murphy DG. 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.http://dx.doi.org/10.1099/vir.0.049668-0.
18. Li C, Lu L, Murphy DG, Negro F, Okamoto H. 2014. Origin of hepatitis C virus genotype 3 in Africa as estimated through an evolutionary analysis of the full-length genomes of nine subtypes, including the newly sequenced 3d and 3e. J Gen Virol 95:1677–1688.http://dx.doi.org/10.1099/vir.0.065128-0.
19. Katsume A, Tokunaga Y, Hirata Y, Munakata T, Saito M, Hayashi H, Okamoto K, Ohmori Y, Kusanagi I, Fujiwara S, Tsukuda T, Aoki Y, Klumpp K, Tsukiyama-Kohara K, El-Gohary A, Sudoh M, Kohara M. 2013. A serine palmitoyltransferase inhibitor blocks hepatitis C virus replication in human hepatocytes. Gastroenterology 145:865–873.http://dx.doi.org/10.1053/j.gastro.2013.06.012.
20. Saeed M, Scheel TK, Gottwein JM, Marukian S, Dustin LB, Bukh J, Rice CM. 2012. Efficient replication of genotype 3a and 4a hepatitis C virus replicons in human hepatoma cells. Antimicrob Agents Chemother 56:5365–5373.http://dx.doi.org/10.1128/AAC.01256-12.
21. Saeed M, Gondeau C, Hmwe S, Yokokawa H, Date T, Suzuki T, Kato T, Maurel P, Wakita T. 2013. Replication of hepatitis C virus genotype 3a in cultured cells. Gastroenterology 144:56–58.e7.http://dx.doi.org/10.1053/j.gastro.2012.09.017.
22. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, Murthy K, Habermann A, Kräusslich H-G, Mizokami M, Bartenschlager R, Liang TJ. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11:791–796.http://dx.doi.org/10.1038/nm1268.
23. Yi M, Villanueva RA, Thomas DL, Wakita T, Lemon SM. 2006. Production of infectious genotype 1a hepatitis C virus (Hutchinson strain) in cultured human hepatoma cells. Proc Natl Acad Sci U S A 103:2310–2315.http://dx.doi.org/10.1073/pnas.0510727103.
24. Yi M, Hu F, Joyce M, Saxena V, Welsch C, Chavez D, Guerra B, Yamane D, Veselenak R, Pyles R, Walker CM, Tyrrell L, Bourne N, Lanford RE, Lemon SM. 2014. Evolution of a cell culture-derived genotype 1a hepatitis C virus (H77S.2) during persistent infection with chronic hepatitis in a chimpanzee. J Virol 88:3678–3694.http://dx.doi.org/10.1128/JVI.03540-13.
25. Salazar-Gonzalez JF, Bailes E, Pham KT, Salazar MG, Guffey MB, Keele BF, Derdeyn CA, Farmer P, Hunter E, Allen S, Manigart O, Mulenga J, Anderson JA, Swanstrom R, Haynes BF, Athreya GS, Korber BT, Sharp PM, Shaw GM, Hahn BH. 2008. Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J Virol 82: 3952–3970.http://dx.doi.org/10.1128/JVI.02660-07.
26. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, Salazar MG, Sun C, Grayson T, Wang S, Li H, Wei X, Jiang C, Kirchherr JL, Gao F, Anderson JA, Ping L-H, Swanstrom R, Tomaras GD, Blattner WA, Goepfert PA, Kilby JM, Saag MS, Delwart EL, Busch MP, Cohen MS, Montefiori DC, Haynes BF, Gaschen B, Athreya GS, Lee HY, Wood N, Seoighe C, Perelson AS, Bhattacharya T, Korber BT, Hahn BH, Shaw GM. 2008. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 105:7552–7557.http://dx.doi.org/10.1073/pnas.0802203105.
27. Keele BF, Li H, Learn GH, Hraber P, Giorgi EE, Grayson T, Sun C, Chen Y, Yeh WW, Letvin NL, Mascola JR, Nabel GJ, Haynes BF, Bhattacharya T, Perelson AS, Korber BT, Hahn BH, Shaw GM. 2009. Low-dose rectal inoculation of rhesus macaques by SIVsmE660 or SIVmac251 recapitulates human mucosal infection by HIV-1. J Exp Med 206:1117–1134.http://dx.doi.org/10.1084/jem.20082831.
28. Salazar-Gonzalez JF, Salazar MG, Keele BF, Learn GH, Giorgi EE, Li H, Decker JM, Wang S, Baalwa J, Kraus MH, Parrish NF, Shaw KS, Guffey MB, Bar KJ, Davis KL, Ochsenbauer-Jambor C, Kappes JC, Saag MS, Cohen MS, Mulenga J, Derdeyn CA, Allen S, Hunter E, Markowitz M, Hraber P, Perelson AS, Bhattacharya T, Haynes BF, Korber BT, Hahn BH, Shaw GM. 2009. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J Exp Med 206:1273–1289.http://dx.doi.org/10.1084/jem.20090378.
29. Goonetilleke N, Liu MK, Salazar-Gonzalez JF, Ferrari G, Giorgi E, Ganusov VV, Keele BF, Learn GH, Turnbull EL, Salazar MG, Weinhold KJ, Moore S, CHAVI Clinical Core B, Letvin N, Haynes BF, Cohen MS, Hraber P, Bhattacharya T, Borrow P, Perelson AS, Hahn BH, Shaw GM, Korber BT, McMichael AJ. 2009. The first T cell response to transmitted/founder virus contributes to the control of acute viremia in HIV-1 infection. J Exp Med 206:1253–1272.http://dx.doi.org/10.1084/jem.20090365.
30. Bar KJ, Li H, Chamberland A, Tremblay C, Routy JP, Grayson T, Sun C, Wang S, Learn GH, Morgan CJ, Schumacher JE, Haynes BF, Keele BF, Hahn BH, Shaw GM. 2010. Wide variation in the multiplicity of HIV-1 infection among injection drug users. J Virol 84:6241–6247.http://dx.doi.org/10.1128/JVI.00077-10.
31. Li H, Bar KJ, Wang S, Decker JM, Chen Y, Sun C, Salazar-Gonzalez JF, Salazar MG, Learn GH, Morgan CJ, Schumacher JE, Hraber P, Giorgi EE, Bhattacharya T, Korber BT, Perelson AS, Eron JJ, Cohen MS, Hicks CB, Haynes BF, Markowitz M, Keele BF, Hahn BH, Shaw GM. 2010. High multiplicity infection by HIV-1 in men who have sex with men. PLoS Pathog 6:e1000890.http://dx.doi.org/10.1371/journal.ppat.1000890.
32. Rolland M, Edlefsen PT, Larsen BB, Tovanabutra S, Sanders-Buell E, Hertz T, deCamp AC, Carrico C, Menis S, Magaret CA, Ahmed H, Juraska M, Chen L, Konopa P, Nariya S, Stoddard JN, Wong K, Zhao H, Deng W, Maust BS, Bose M, Howell S, Bates A, Lazzaro M, O’Sullivan A, Lei E, Bradfield A, Ibitamuno G, Assawadarachai V, O’Connell RJ, deSouza MS, Nitayaphan S, Rerks-Ngarm S, Robb ML, McLellan JS, Georgiev I, Kwong PD, Carlson JM, Michael NL, Schief WR, Gilbert PB, Mullins JI, Kim JH. 2012. Increased HIV-1 vaccine efficacy against viruses with genetic signatures in Env V2. Nature 490: 417–420.http://dx.doi.org/10.1038/nature11519.
33. Vaccari M, Keele BF, Bosinger SE, Doster MN, Ma Z-M, Pollara J, Hryniewicz A, Ferrari G, Guan Y, Forthal DN, Venzon D, Fenizia C, Morgan T, Montefiori D, Lifson JD, Miller CJ, Silvestri G, Rosati M, Felber BK, Pavlakis GN, Tartaglia J, Franchini G. 2013. Protection afforded by an HIV vaccine candidate in macaques depends on the dose of SIVmac251 at challenge exposure. J Virol 87:3538–3548.http://dx.doi.org/10.1128/JVI.02863-12.
34. Roederer M, Keele BF, Schmidt SD, Mason RD, Welles HC, Fischer W, Labranche C, Foulds KE, Louder MK, Yang Z-Y, Todd JP, Buzby AP, Mach LV, Shen L, Seaton KE, Ward BM, Bailer RT, Gottardo R, Gu W, Ferrari G, Alam SM, Denny TN, Montefiori DC, Tomaras GD, Korber BT, Nason MC, Seder RA, Koup RA, Letvin NL, Rao SS, Nabel GJ, Mascola JR. 2014. Immunological and virological mechanisms of vaccine-mediated protection against SIV and HIV. Nature 505:502–508.http://dx.doi.org/10.1038/nature12893.
35. Sterrett S, Learn GH, Edlefsen PT, Haynes BF, Hahn BH, Shaw GM, Bar KJ. 14 July 2014. Low multiplicity of HIV-1 infection and no vaccine enhancement in VAX003 injection drug users. Open Forum Infect Dishttp://dx.doi.org/10.1093/ofid/ofu056.
36. Derdeyn CA, Decker JM, Bibollet-Ruche F, Mokili JL, Muldoon M, Denham SA, Heil ML, Kasolo F, Musonda R, Hahn BH, Shaw GM, Korber BT, Allen S, Hunter E. 2004. Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science 303:2019–2022.http://dx.doi.org/10.1126/science.1093137.
37. Ochsenbauer C, Edmonds TG, Ding H, Keele BF, Decker J, Salazar MG, Salazar-Gonzalez JF, Shattock R, Haynes BF, Shaw GM, Hahn BH, Kappes JC. 2012. Generation of transmitted/founder HIV-1 infectious molecular clones and characterization of their replication capacity in CD4 T lymphocytes and monocyte-derived macrophages. J Virol 86: 2715–2728.http://dx.doi.org/10.1128/JVI.06157-11.
38. Parrish NF, Gao F, Li H, Giorgi EE, Barbian HJ, Parrish EH, Zajic L, Iyer SS, Decker JM, Kumar A, Hora B, Berg A, Cai F, Hopper J, Denny TN, Ding H, Ochsenbauer C, Kappes JC, Galimidi RP, West AP, Bjorkman PJ, Wilen CB, Doms RW, O’Brien M, Bhardwaj N, Borrow P, Haynes BF, Muldoon M, Theiler JP, Korber B, Shaw GM, Hahn BH. 2013. Phenotypic properties of transmitted founder HIV-1. Proc Natl Acad Sci U S A 110:6626–6633.http://dx.doi.org/10.1073/pnas.1304288110.
39. Fenton-May AE, Dibben O, Emmerich T, Ding H, Pfafferott K, Aasa-Chapman MM, Pellegrino P, Williams I, Cohen MS, Gao F, Shaw GM, Hahn BH, Ochsenbauer C, Kappes JC, Borrow P. 2013. Relative resistance of HIV-1 founder viruses to control by interferonalpha. Retrovirology 10:146.http://dx.doi.org/10.1186/1742-4690-10-146.
40. Ping L-H, Joseph SB, Anderson JA, Abrahams M-R, Salazar-Gonzalez JF, Kincer LP, Treurnicht FK, Arney L, Ojeda S, Zhang M, Keys J, Potter EL, Chu H, Moore P, Salazar MG, Iyer S, Jabara C, Kirchherr J, Mapanje C, Ngandu N, Seoighe C, Hoffman I, Gao F, Tang Y, Labranche C, Lee B, Saville A, Vermeulen M, Fiscus S, Morris L, Karim SA, Haynes BF, Shaw GM, Korber BT, Hahn BH, Cohen MS, Montefiori D, Williamson C, Swanstrom R, CAPRISA Acute Infection Study and Center for HIV-AIDS Vaccine Immunology Consortium. 2013. Comparison of viral Env proteins from acute and chronic infections with subtype C human immunodeficiency virus type 1 identifies differences in glycosylation and CCR5 utilization and suggests a new strategy for immunogen design. J Virol 87:7218–7233.http://dx.doi.org/10.1128/JVI.03577-12.
41. Rolland M, Tovanabutra S, deCamp AC, Frahm N, Gilbert PB, Sanders-Buell E, Heath L, Magaret CA, Bose M, Bradfield A, O’Sullivan A, Crossler J, Jones T, Nau M, Wong K, Zhao H, Raugi DN, Sorensen S, Stoddard JN, Maust BS, Deng W, Hural J, Dubey S, Michael NL, Shiver J, Corey L, Li F, Self SG, Kim J, Buchbinder S, Casimiro DR, Robertson MN, Duerr A, McElrath MJ, McCutchan FE, Mullins JI. 2011. Genetic impact of vaccination on breakthrough HIV-1 sequences from the STEP trial. Nat Med 17:366–371.http://dx.doi.org/10.1038/nm.2316.
42. Tuplin A, Evans DJ, Simmonds P. 2004. Detailed mapping of RNA secondary structures in core and NS5B-encoding region sequences of hepatitis C virus by RNase cleavage and novel bioinformatic prediction methods. J Gen Virol 85:3037–3047.http://dx.doi.org/10.1099/vir.0.80141-0.
43. Kolykhalov AA, Feinstone SM, Rice CM. 1996. Identification of a highly conserved sequence element at the 3= terminus of hepatitis C virus genome RNA. J Virol 70:3363–3371.
44. Tellinghuisen TL, Evans MJ, von Hahn T, You S, Rice CM. 2007. Studying hepatitis C virus: making the best of a bad virus. J Virol 81: 8853–8867.http://dx.doi.org/10.1128/JVI.00753-07.
45. Quinkert D, Bartenschlager R, Lohmann V. 2005. Quantitative analysis of the hepatitis C virus replication complex. J Virol 79:13594–13605.http://dx.doi.org/10.1128/JVI.79.21.13594-13605.2005.
46. Farci P, Shimoda A, Coiana A, Diaz G, Peddis G, Melpolder JC, Strazzera A, Chien DY, Munoz SJ, Balestrieri A, Purcell RH, Alter HJ. 2000. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 288:339–344.http://dx.doi.org/10.1126/science.288.5464.339.
47. Kuntzen T, Timm J, Berical A, Lewis-Ximenez LL, Jones A, Nolan B, Schulze zur Wiesch J, Li B, Schneidewind A, Kim AY, Chung RT, Lauer GM, Allen TM. 2007. Viral sequence evolution in acute hepatitis C virus infection. J Virol 81:11658–11668.http://dx.doi.org/10.1128/JVI.00995-07.
48. Nevot M, Boesecke C, Parera M, Andrés C, Franco S, Revollo B, Ingiliz P, Tural C, Clotet B, Rockstroh JK, Martinez MA, NEAT Study Group. 2014. Hepatitis C virus NS3/4A quasispecies diversity in acute hepatitis C infection in HIV-1 co-infected patients. J Viral Hepat 21:e19–e28.http://dx.doi.org/10.1111/jvh.12254.
49. Smith JA, Aberle JH, Fleming VM, Ferenci P, Thomson EC, Karayiannis P, McLean AR, Holzmann H, Klenerman P. 2010. Dynamic coinfection with multiple viral subtypes in acute hepatitis C. J Infect Dis 202:1770–1779.http://dx.doi.org/10.1086/657317.
50. Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SD. 2006. GARD: a genetic algorithm for recombination detection. Bioinformatics 22:3096–3098.http://dx.doi.org/10.1093/bioinformatics/btl474.
51. Maydt J, Lengauer T. 2006. Recco: recombination analysis using cost optimization. Bioinformatics 22:1064–1071.http://dx.doi.org/10.1093/bioinformatics/btl057.
52. Lohmann V, Körner F, Koch J, Herian U, Theilmann L, Bartenschlager R. 1999. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285:110–113.http://dx.doi.org/10.1126/science.285.5424.110.
53. Kumar U, Tuthill T, Thomas HC, Monjardino J. 2000. Sequence, expression and reconstitution of an HCV genome from a British isolate derived from a single blood donation. J Viral Hepat 7:459–465.http://dx.doi.org/10.1046/j.1365-2893.2000.00259.x.
54. Timm J, Neukamm M, Kuntzen T, Kim AY, Chung RT, Brander C, Lauer GM, Walker BD, Allen TM. 2007. Characterization of full-length hepatitis C virus genotype 4 sequences. J Viral Hepat 14:330–337.http://dx.doi.org/10.1111/j.1365-2893.2006.00792.x.
55. Yamada N, Tanihara K, Mizokami M, Ohba K, Takada A, Tsutsumi M, Date T. 1994. Full-length sequence of the genome of hepatitis C virus type 3a: comparative study with different genotypes. J Gen Virol 75: 3279–3284.http://dx.doi.org/10.1099/0022-1317-75-11-3279.
56. Wei X, Decker JM, Wang S, Hui H, Kappes JC, Wu X, Salazar- Gonzalez JF, Salazar MG, Kilby JM, Saag MS, Komarova NL, Nowak MA, Hahn BH, Kwong PD, Shaw GM. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307–312.http://dx.doi.org/10.1038/nature01470.
57. Moore PL, Gray ES, Wibmer CK, Bhiman JN, Nonyane M, Sheward DJ, Hermanus T, Bajimaya S, Tumba NL, Abrahams M-R, Lambson BE, Ranchobe N, Ping L, Ngandu N, Abdool Karim Q, Abdool Karim SS, Swanstrom RI, Seaman MS, Williamson C, Morris L. 2012. Evolution of an HIV glycan-dependent broadly neutralizing antibody epitope through immune escape. Nat Med 18:1688–1692.http://dx.doi.org/10.1038/nm.2985.
58. Brown RJ, Hudson N, Wilson G, Rehman SU, Jabbari S, Hu K, Tarr AW, Borrow P, Joyce M, Lewis J, Zhu LF, Law M, Kneteman N, Tyrrell DL, McKeating JA, Ball JK. 2012. Hepatitis C virus envelope glycoprotein fitness defines virus population composition following transmission to a new host. J Virol 86:11956–11966.http://dx.doi.org/10.1128/JVI.01079-12.
59. Yi M, Lemon SM. 2003. 3= nontranslated RNA signals required for replication of hepatitis C virus RNA. J Virol 77:3557–3568.http://dx.doi.org/10.1128/JVI.77.6.3557-3568.2003.
60. Tanaka T, Kato N, Cho MJ, Sugiyama K, Shimotohno K. 1996. Structure of the 3= terminus of the hepatitis C virus genome. J Virol 70: 3307–3312.
61. Harrison GP, Mayo MS, Hunter E, Lever AM. 1998. Pausing of reverse transcriptase on retroviral RNA templates is influenced by secondary structures both 5= and 3= of the catalytic site. Nucleic Acids Res 26: 3433–3442.http://dx.doi.org/10.1093/nar/26.14.3433.
62. Quiñones-Mateu ME, Gao Y, Ball SC, Marozsan AJ, Abraha A, Arts EJ. 2002. In vitro intersubtype recombinants of human immunodeficiency virus type 1: comparison to recent and circulating in vivo recombinant forms. J Virol 76:9600–9613.http://dx.doi.org/10.1128/JVI.76.19.9600-9613.2002.
63. Lanciault C, Champoux JJ. 2006. Pausing during reverse transcription increases the rate of retroviral recombination. J Virol 80:2483–2494.http://dx.doi.org/10.1128/JVI.80.5.2483-2494.2006.
64. Riepsamen AH, Gibson T, Rowe J, Chitwood DJ, Subbotin SA, Dowton M. 2011. Poly(T) variation in heteroderid nematode mitochondrial genomes is predominantly an artefact of amplification. J Mol Evol 72: 182–192.http://dx.doi.org/10.1007/s00239-010-9414-3.
65. Behrens SE, Tomei L, De Francesco R. 1996. Identification and properties of the RNA-dependent RNA polymerase of hepatitis C virus. EMBO J 15:12–22.
66. Lohmann V, Körner F, Herian U, Bartenschlager R. 1997. Biochemical properties of hepatitis C virus NS5B RNA-dependent RNA polymerase and identification of amino acid sequence motifs essential for enzymatic activity. J Virol 71:8416–8428.
67. Ago H, Adachi T, Yoshida A, Yamamoto M, Habuka N, Yatsunami K, Miyano M. 1999. Crystal structure of the RNA-dependent RNA polymerase of hepatitis C virus. Structure 7:1417–1426.http://dx.doi.org/10.1016/S0969-2126(00)80031-3.
68. Mosley RT, Edwards TE, Murakami E, Lam AM, Grice RL, Du J, Sofia MJ, Furman PA, Otto MJ. 2012. Structure of hepatitis C virus polymerase in complex with primer-template RNA. J Virol 86:6503–6511.http://dx.doi.org/10.1128/JVI.00386-12.
69. Odelberg SJ, Weiss RB, Hata A, White R. 1995. Template-switching during DNA synthesis by Thermus aquaticus DNA polymerase I. Nucleic Acids Res 23:2049–2057.http://dx.doi.org/10.1093/nar/23.11.2049.
70. Pfeiffer JK, Topping RS, Shin NH, Telesnitsky A. 1999. Altering the intracellular environment increases the frequency of tandem repeat deletion during Moloney murine leukemia virus reverse transcription. J Virol 73:8441–8447.
71. Mader RM, Schmidt WM, Sedivy R, Rizovski B, Braun J, Kalipciyan M, Exner M, Steger GG, Mueller MW. 2001. Reverse transcriptase template switching during reverse transcriptase-polymerase chain reaction: artificial generation of deletions in ribonucleotide reductase mRNA. J Lab Clin Med 137:422–428.http://dx.doi.org/10.1067/mlc.2001.115452.
72. Viguera E, Canceill D, Ehrlich SD. 2001. In vitro replication slippage by DNA polymerases from thermophilic organisms. J Mol Biol 312: 323–333.http://dx.doi.org/10.1006/jmbi.2001.4943.
73. Li Y, Korolev S, Waksman G. 1998. Crystal structures of open and closed forms of binary and ternary complexes of the large fragment of Thermus aquaticus DNA polymerase I: structural basis for nucleotide incorporation. EMBO J 17:7514–7525.http://dx.doi.org/10.1093/emboj/17.24.7514.
74. Shinde D, Lai Y, Sun F, Arnheim N. 2003. Taq DNA polymerase slippage mutation rates measured by PCR and quasi-likelihood analysis: (CA/GT)n and (A/T)n microsatellites. Nucleic Acids Res 31:974–980.http://dx.doi.org/10.1093/nar/gkg178.
75. Svarovskaia ES, Cheslock SR, Zhang W-H, Hu W-S, Pathak VK. 2003. Retroviral mutation rates and reverse transcriptase fidelity. Front Biosci 8:d117–d134.http://dx.doi.org/10.2741/957.
76. Das D, Georgiadis MM. 2004. The crystal structure of the monomeric reverse transcriptase from Moloney murine leukemia virus. Structure 12:819–829.http://dx.doi.org/10.1016/j.str.2004.02.032.
77. Menéndez-Arias L. 2009. Mutation rates and intrinsic fidelity of retroviral reverse transcriptases. Viruses 1:1137–1165.http://dx.doi.org/10.3390/v1031137.
78. Boyer JC, Bebenek K, Kunkel TA. 1992. Unequal human immunodeficiency virus type 1 reverse transcriptase error rates with RNA and DNA templates. Proc Natl Acad Sci U S A 89:6919–6923.http://dx.doi.org/10.1073/pnas.89.15.6919.
79. Klarmann GJ, Schauber CA, Preston BD. 1993. Template-directed pausing of DNA synthesis by HIV-1 reverse transcriptase during polymerization of HIV-1 sequences in vitro. J Biol Chem 268:9793–9802.
80. Owsianka AM, Timms JM, Tarr AW, Brown RJ, Hickling TP, Szwejk A, Bienkowska-Szewczyk K, Thomson BJ, Patel AH, Ball JK. 2006. Identification of conserved residues in the E2 envelope glycoprotein of the hepatitis C virus that are critical for CD81 binding. J Virol 80: 8695–8704.http://dx.doi.org/10.1128/JVI.00271-06.
81. Kato N, Ootsuyama Y, Ohkoshi S, Nakazawa T, Sekiya H, Hijikata M, Shimotohno K. 1992. Characterization of hypervariable regions in the putative envelope protein of hepatitis C virus. Biochem Biophys Res Commun 189:119–127.http://dx.doi.org/10.1016/0006-291X(92)91533-V.
82. Gray RR, Parker J, Lemey P, Salemi M, Katzourakis A, Pybus OG. 2011. The mode and tempo of hepatitis C virus evolution within and among hosts. BMC Evol Biol 11:131.http://dx.doi.org/10.1186/1471-2148-11-131.
83. Friebe P, Bartenschlager R. 2002. Genetic analysis of sequences in the 3= nontranslated region of hepatitis C virus that are important for RNA replication. J Virol 76:5326–5338.http://dx.doi.org/10.1128/JVI.76.11.5326-5338.2002.
84. Yanagi M, St. Claire M, Emerson SU, Purcell RH, Bukh J. 1999. In vivo analysis of the 3= untranslated region of the hepatitis C virus after in vitro mutagenesis of an infectious cDNA clone. Proc Natl Acad Sci U S A 96:2291–2295.http://dx.doi.org/10.1073/pnas.96.5.2291.
85. Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. 2005. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 309:1577–1581.http://dx.doi.org/10.1126/science.1113329.
86. You S, Rice CM. 2008. 3= RNA elements in hepatitis C virus replication: kissing partners and long poly(U). J Virol 82:184–195.http://dx.doi.org/10.1128/JVI.01796-07.
87. Ito T, Lai MM. 1997. Determination of the secondary structure of and cellular protein binding to the 3=-untranslated region of the hepatitis C virus RNA genome. J Virol 71:8698–8706.
88. Mitchell AM, Stone AEL, Cheng L, Ballinger K, Edwards MG, Stoddard M, Li H, Golden-Mason L, Shaw GM, Khetani S, Rosen HR. 2015. Transmitted/founder hepatitis C viruses induce cell-type- and genotypespecific differences in innate signaling within the liver. MBio 6(1): e02510-14.http://dx.doi.org/10.1128/mBio.02510-14.
89. Giugliano S, Kriss M, Golden-Mason L, Dobrinskikh E, Stone AE, Soto-Gutierrez A, Mitchell A, Khetani SR, Yamane D, Stoddard M, Li H, Shaw GM, Edwards MG, Lemon SM, Gale M, Shah VH, Rosen HR. 4 November 2014. Hepatitis C virus infection induces autocrine interferon signaling by human liver endothelial cell and release of exosomes, which inhibits viral replication. Gastroenterology http://dx.doi.org/10.1053/j.gastro.2014.10.040.
90. Jones CT, Catanese MT, Law LM, Khetani SR, Syder AJ, Ploss A, Oh TS, Schoggins JW, MacDonald MR, Bhatia SN, Rice CM. 2010. Realtime imaging of hepatitis C virus infection using a fluorescent cell-based reporter system. Nat Biotechnol 28:167–171.http://dx.doi.org/10.1038/nbt.1604.
91. Carroll SS, Tomassini JE, Bosserman M, Getty K, Stahlhut MW, Eldrup AB, Bhat B, Hall D, Simcoe AL, LaFemina R, Rutkowski CA, Wolanski B, Yang Z, Migliaccio G, De Francesco R, Kuo LC, MacCoss M, Olsen DB. 2003. Inhibition of hepatitis C virus RNA replication by 2=-modified nucleoside analogs. J Biol Chem 278:11979–11984.http://dx.doi.org/10.1074/jbc.M210914200.
92. Andrus L, Marukian S, Jones CT, Catanese MT, Sheahan TP, Schoggins JW, Barry WT, Dustin LB, Trehan K, Ploss A, Bhatia SN, Rice CM. 2011. Expression of paramyxovirusVproteins promotes replication and spread of hepatitis C virus in cultures of primary human fetal liver cells. Hepatology 54:1901–1912.http://dx.doi.org/10.1002/hep.24557.
93. Ogawa S, Surapisitchat J, Virtanen C, Ogawa M, Niapour M, Sugamori KS, Wang S, Tamblyn L, Guillemette C, Hoffmann E, Zhao B, Strom S, Laposa RR, Tyndale RF, Grant DM, Keller G. 2013. Threedimensional culture and cAMP signaling promote the maturation of human pluripotent stem cell-derived hepatocytes. Development 140: 3285–3296.http://dx.doi.org/10.1242/dev.090266.
94. Lee HY, Giorgi EE, Keele BF, Gaschen B, Athreya GS, Salazar- Gonzalez JF, Pham KT, Goepfert PA, Kilby JM, Saag MS, Delwart EL, Busch MP, Hahn BH, Shaw GM, Korber BT, Bhattacharya T, Perelson AS. 2009. Modeling sequence evolution in acute HIV-1 infection. J Theor Biol 261:341–360.http://dx.doi.org/10.1016/j.jtbi.2009.07.038.
95. Liu J, Keele BF, Li H, Keating S, Norris PJ, Carville A, Mansfield KG, Tomaras GD, Haynes BF, Kolodkin-Gal D, Letvin NL, Hahn BH, Shaw GM, Barouch DH. 2010. Low-dose mucosal simian immunodeficiency virus infection restricts early replication kinetics and transmitted virus variants in rhesus monkeys. J Virol 84:10406–10412.http://dx.doi.org/10.1128/JVI.01155-10.
96. Cristina J, Colina R. 2006. Evidence of structural genomic region recombination in hepatitis C virus. Virol J 3:53.http://dx.doi.org/10.1186/1743-422X-3-53.
97. González-Candelas F, López-Labrador FX, Bracho MA. 2011. Recombination in hepatitis C virus. Viruses 3:2006–2024.http://dx.doi.org/10.3390/v3102006.
98. Galli A, Bukh J. 2014. Comparative analysis of the molecular mechanisms of recombination in hepatitis C virus. Trends Microbiol 22: 354–364.http://dx.doi.org/10.1016/j.tim.2014.02.005.
99. Glynn SA, Wright DJ, Kleinman SH, Hirschkorn D, Tu Y, Heldebrant C, Smith R, Giachetti C, Gallarda J, Busch MP. 2005. Dynamics of viremia in early hepatitis C virus infection. Transfusion 45:994–1002.http://dx.doi.org/10.1111/j.1537-2995.2005.04390.x.
100. Busch MP, Murthy KK, Kleinman SH, Hirschkorn DF, Herring BL, Delwart EL, Racanelli V, Yoon JC, Rehermann B, Alter HJ. 2012. Infectivity in chimpanzees (Pan troglodytes) of plasma collected before HCV RNA detectability by FDA-licensed assays: implications for trans-fusion safety and HCV infection outcomes. Blood 119:6326–6334.http://dx.doi.org/10.1182/blood-2011-12-393637.
101. Sentandreu V, Jiménez-Hernández N, Torres-Puente M, Bracho MA, Valero A, Gosalbes MJ, Ortega E, Moya A, González-Candelas F. 2008. Evidence of recombination in intrapatient populations of hepatitis Cvirus. PLoS One 3: e3239. http://dx.doi.org/10.1371/journal.pone.0003239.
102. Barnes E, Folgori A, Capone S, Swadling L, Aston S, Kurioka A, Meyer J, Huddart R, Smith K, Townsend R, Brown A, Antrobus R, Ammendola V, Naddeo M, O’Hara G, Willberg C, Harrison A, Grazioli F, Esposito ML, Siani L, Traboni C, Oo Y, Adams D, Hill A, Colloca S, Nicosia A, Cortese R, Klenerman P. 2012. Novel adenovirus-based vaccines induce broad and sustained T cell responses to HCV in man. Sci Transl Med 4:115ra111.http://dx.doi.org/10.1126/scitranslmed.3003155.
103. Goffard A, Callens N, Bartosch B, Wychowski C, Cosset F-L, Montpellier C, Dubuisson J. 2005. Role of N-linked glycans in the functions of hepatitis C virus envelope glycoproteins. J Virol 79:8400–8409.http://dx.doi.org/10.1128/JVI.79.13.8400-8409.2005.
104. McCaffrey K, Boo I, Poumbourios P, Drummer HE. 2007. Expression and characterization of a minimal hepatitis C virus glycoprotein E2 core domain that retains CD81 binding. J Virol 81:9584–9590.http://dx.doi.org/10.1128/JVI.02782-06.
105. Goffard A, Dubuisson J. 2003. Glycosylation of hepatitis C virus envelope proteins. Biochimie 85:295–301.http://dx.doi.org/10.1016/S0300-9084(03)00004-X.
106. Helle F, Vieyres G, Elkrief L, Popescu C-I, Wychowski C, Descamps V, Castelain S, Roingeard P, Duverlie G, Dubuisson J. 2010. Role of N-linked glycans in the functions of hepatitis C virus envelope proteins incorporated into infectious virions. J Virol 84:11905–11915.http://dx.doi.org/10.1128/JVI.01548-10.
107. Saito T, Owen DM, Jiang F, Marcotrigiano J, Gale M. 2008. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454:523–527.http://dx.doi.org/10.1038/nature07106.
108. Schnell G, Loo Y-M, Marcotrigiano J, Gale M. 2012. Uridine composition of the poly-U/UC tract of HCV RNA defines non-self recognition by RIG-I. PLoS Pathog 8:e1002839.http://dx.doi.org/10.1371/journal.ppat.1002839.
109. Li T, Zhang J. 2000. Determination of the frequency of retroviral recombination between two identical sequences within a provirus. J Virol 74: 7646–7650.http://dx.doi.org/10.1128/JVI.74.16.7646-7650.2000.
110. Sumpter R, Loo Y-M, Foy E, Li K, Yoneyama M, Fujita T, Lemon SM, Gale M. 2005. Regulating intracellular antiviral defense and permissiveness to hepatitisCvirusRNAreplication through a cellularRNAhelicase, RIG-I. J Virol 79:2689–2699.http://dx.doi.org/10.1128/JVI.79.5.2689-2699.2005.
111. Li K, Chen Z, Kato N, Gale M, Lemon SM. 2005. Distinct poly(I-C) and virus-activated signaling pathways leading to interferon-beta production in hepatocytes. J Biol Chem 280:16739–16747.http://dx.doi.org/10.1074/jbc.M414139200.
112. Pietschmann T, Zayas M, Meuleman P, Long G, Appel N, Koutsoudakis G, Kallis S, Leroux-Roels G, Lohmann V, Bartenschlager R. 2009. Production of infectious genotype 1b virus particles in cell culture and impairment by replication enhancing mutations. PLoS Pathog 5:e1000475.http://dx.doi.org/10.1371/journal.ppat.1000475.
113. Marukian S, Andrus L, Sheahan TP, Jones CT, Charles ED, Ploss A, Rice CM, Dustin LB. 2011. Hepatitis C virus induces interferon-_ and interferon-stimulated genes in primary liver cultures. Hepatology 54: 1913–1923.http://dx.doi.org/10.1002/hep.24580.
114. Helle F, Brochot E, Fournier C, Descamps V, Izquierdo L, Hoffmann TW, Morel V, Herpe Y-E, Bengrine A, Belouzard S, Wychowski C, Dubuisson J, Francois C, Regimbeau J-M, Castelain S, Duverlie G. 2013. Permissivity of primary human hepatocytes and different hepatoma cell lines to cell culture adapted hepatitis C virus. PLoS One 8:e70809.http://dx.doi.org/10.1371/journal.pone.0070809.