Elucidation of Hepatitis C Virus Transmission and Early Diversification by Single Genome Sequencing

PLoS Pathogens

Volumn 8, Issue 8, 2012, Pages

  Li, Hui ^a   Stoddard, Mark B ^a   Wang, Shuyi ^a   Blair, Lily M ^b   Giorgi, Elena E ^c,d   Parrish, Erica H ^a   Learn, Gerald H ^a   Hraber, Peter ^c   Goepfert, Paul A ^e   Saag, Michael S ^e   Denny, Thomas N ^f   Haynes, Barton F ^f   Hahn, Beatrice H ^a   Ribeiro, Ruy M ^c   Perelson, Alan S ^c   Korber, Bette T ^b,c   Bhattacharya, Tanmoy ^b,c   Shaw, George M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b SANTA FE INSTITUTE   (United States)

^c LOS ALAMOS NATIONAL LABORATORY   (United States)

^d CENTER FOR NONLINEAR STUDIES   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^f DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; VIRUS RNA;

ARTICLE; BOTTLENECK POPULATION; CLINICAL ARTICLE; CONTROLLED STUDY; GENE IDENTIFICATION; GENETIC VARIABILITY; GENOME ANALYSIS; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; IMMUNOPATHOGENESIS; MATHEMATICAL MODEL; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEOMICS; SEQUENCE ANALYSIS; SINGLE GENOME SEQUENCING; UNINDEXED SEQUENCE; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS LOAD; VIRUS MUTATION; VIRUS REPLICATION; VIRUS RESISTANCE; VIRUS TRANSMISSION;

ACUTE DISEASE; FEMALE; GENOME, VIRAL; HEPACIVIRUS; HEPATITIS C; HOST-PATHOGEN INTERACTIONS; HUMANS; MALE; RNA, VIRAL; SEQUENCE ANALYSIS, RNA;

HEPATITIS C VIRUS;

EID: 84866144158     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002880     Document Type: Article

References (87)

1. Ray SC, Thomas DL (2010) Hepatitis C. In: Mandell GL, Bennett JE, Dolan R, editors. Principles and practice of infectious diseases. 7th edition. Churchill Livingstone Elsevier Publishers. pp. 2157-2185.
2. Lindenbach BD, Thiel H-J, Rice CM (2007) Flaviviridae: the viruses and their replication. In: Knipe DM, Howley PM, editors. Fields Virology Lippincott. Williams & Williams Publishers. pp. 1101-1152.
3. Moradpour D, Penin F, Rice CM, (2007) Replication of hepatitis C virus. Nat Rev Microbiol 5: 453-463.
4. Simmonds P, (2004) Genetic diversity and evolution of hepatitis C virus-15 years on. J Gen Virol 85: 3173-3188.
5. Murray CL, Rice CM, (2011) Turning hepatitis C into a real virus. Annu Rev Microbiol 65: 307-327.
6. Hoofnagle JH, (2009) A step forward in therapy for hepatitis C. N Engl J Med 360: 1899-1901.
7. Pawlotsky JM, (2011) Treatment failure and resistance with direct-acting antiviral drugs against hepatitis C virus. Hepatology 53: 1742-1751.
8. Yusim K, Fischer W, Yoon H, Thurmond J, Fenimore PW, et al. (2010) Genotype 1 and global hepatitis C T-cell vaccines designed to optimize coverage of genetic diversity. J Gen Virol 91: 1194-1206.
9. Bowen DG, Walker CM, (2005) Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature 436: 946-952.
10. Rehermann B, (2009) Hepatitis C virus versus innate and adaptive immune responses: a tale of coevolution and coexistence. J Clin Invest 119: 1745-1754.
11. Abrahams MR, Anderson JA, Giorgi EE, Seoighe C, Mlisana K, et al. (2009) Quantitating the multiplicity of infection with human immunodeficiency virus type 1 subtype C reveals a non-poisson distribution of transmitted variants. J Virol 83: 3556-3567.
12. Bar KJ, Li H, Chamberland A, Tremblay C, Routy JP, et al. (2010) Wide variation in the multiplicity of HIV-1 infection among injection drug users. J Virol 84: 6241-6247.
13. Goonetilleke N, Liu MK, Salazar-Gonzalez JF, Ferrari G, Giorgi E, et al. (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.
14. Haaland RE, Hawkins PA, Salazar-Gonzalez J, Johnson A, Tichacek A, et al. (2009) Inflammatory genital infections mitigate a severe genetic bottleneck in heterosexual transmission of subtype A and C HIV-1. PLoS Pathog 5: e1000274.
15. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, et al. (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.
16. Li H, Bar KJ, Wang S, Decker JM, Chen Y, et al. (2010) High multiplicity infection by HIV-1 in men who have sex with men. PLoS Pathog 6: e1000890.
17. Palmer S, Kearney M, Maldarelli F, Halvas EK, Bixby CJ, et al. (2005) Multiple, linked human immunodeficiency virus type 1 drug resistance mutations in treatment-experienced patients are missed by standard genotype analysis. J Clin Microbiol 43: 406-413.
18. Salazar-Gonzalez JF, Salazar MG, Keele BF, Learn GH, Giorgi EE, et al. (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.
19. Bull RA, Luciani F, McElroy K, Gaudieri S, Pham ST, et al. (2011) Sequential bottlenecks drive viral evolution in early acute hepatitis C virus infection. PLoS Pathog 7: e1002243.
20. Cox AL, Mosbruger T, Mao Q, Liu Z, Wang XH, et al. (2005) Cellular immune selection with hepatitis C virus persistence in humans. J Exp Med 201: 1741-1752.
21. Farci P, Shimoda A, Coiana A, Diaz G, Peddis G, et al. (2000) The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 288: 339-344.
22. Glynn SA, Wright DJ, Kleinman SH, Hirschkorn D, Tu Y, et al. (2005) Dynamics of viremia in early hepatitis C virus infection. Transfusion 45: 994-1002.
23. Herring BL, Tsui R, Peddada L, Busch M, Delwart EL, (2005) Wide range of quasispecies diversity during primary hepatitis C virus infection. J Virol 79: 4340-4346.
24. Irving WL, Brown RJ, (2010) Acute hepatitis C virus infection: a dynamic and challenging concept. J Infect Dis 202: 1765-1767.
25. Kuntzen T, Timm J, Berical A, Lewis-Ximenez LL, Jones A, et al. (2007) Viral sequence evolution in acute hepatitis C virus infection. J Virol 81: 11658-11668.
26. Maheshwari A, Ray S, Thuluvath PJ, (2008) Acute hepatitis C. Lancet 372: 321-332.
27. Page K, Hahn JA, Evans J, Shiboski S, Lum P, et al. (2009) Acute hepatitis C virus infection in young adult injection drug users: a prospective study of incident infection, resolution, and reinfection. J Infect Dis 200: 1216-1226.
28. Smith JA, Aberle JH, Fleming VM, Ferenci P, Thomson EC, et al. (2010) Dynamic coinfection with multiple viral subtypes in acute hepatitis C. J Infect Dis 202: 1770-1779.
29. Thimme R, Oldach D, Chang KM, Steiger C, Ray SC, et al. (2001) Determinants of viral clearance and persistence during acute hepatitis C virus infection. J Exp Med 194: 1395-1406.
30. Thomson EC, Fleming VM, Main J, Klenerman P, Weber J, et al. (2011) Predicting spontaneous clearance of acute hepatitis C virus in a large cohort of HIV-1-infected men. Gut 60: 837-845.
31. Balagopal A, Thomas DL, Thio CL, (2010) IL28B and the control of hepatitis C virus infection. Gastroenterology 139: 1865-1876.
32. Khakoo SI, Thio CL, Martin MP, Brooks CR, Gao X, et al. (2004) HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 305: 872-874.
33. Thomas DL, Thio CL, Martin MP, Qi Y, Ge D, et al. (2009) Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 461: 798-801.
34. Jacobson IM, McHutchison JG, Dusheiko G, Di Bisceglie AM, Reddy KR, et al. (2011) Telaprevir for previously untreated chronic hepatitis C virus infection. N Engl J Med 364: 2405-2416.
35. Jensen DM, (2011) A new era of hepatitis C therapy begins. N Engl J Med 364: 1272-1274.
36. Poordad F, McCone J Jr, Bacon BR, Bruno S, Manns MP, et al. (2011) Boceprevir for untreated chronic HCV genotype 1 infection. N Engl J Med 364: 1195-1206.
37. Houghton M, Abrignani S, (2005) Prospects for a vaccine against the hepatitis C virus. Nature 436: 961-966.
38. Tester I, Smyk-Pearson S, Wang P, Wertheimer A, Yao E, et al. (2005) Immune evasion versus recovery after acute hepatitis C virus infection from a shared source. J Exp Med 201: 1725-1731.
39. Wang YM, Ray SC, Laeyendecker O, Ticehurst JR, Thomas DL, (1998) Assessment of hepatitis C virus sequence complexity by electrophoretic mobilities of both single-and double-stranded DNAs. J Clin Microbiol 36: 2982-2989.
40. Liu Z, Netski DM, Mao Q, Laeyendecker O, Ticehurst JR, et al. (2004) Accurate representation of the hepatitis C virus quasispecies in 5.2-kilobase amplicons. J Clin Microbiol 42: 4223-4229.
41. Dowd KA, Netski DM, Wang XH, Cox AL, Ray SC, (2009) Selection pressure from neutralizing antibodies drives sequence evolution during acute infection with hepatitis C virus. Gastroenterology 136: 2377-2386.
42. Liu L, Fisher BE, Dowd KA, Astemborski J, Cox AL, et al. (2010) Acceleration of hepatitis C virus envelope evolution in humans is consistent with progressive humoral immune selection during the transition from acute to chronic infection. J Virol 84: 5067-5077.
43. Wang GP, Sherrill-Mix SA, Chang KM, Quince C, Bushman FD, (2010) Hepatitis C virus transmission bottlenecks analyzed by deep sequencing. J Virol 84: 6218-6228.
44. Liu SL, Rodrigo AG, Shankarappa R, Learn GH, Hsu L, et al. (1996) HIV quasispecies and resampling. Science 273: 415-416.
45. Meyerhans A, Vartanian JP, Wain-Hobson S, (1990) DNA recombination during PCR. Nucleic Acids Res 18: 1687-1691.
46. Shriner D, Rodrigo AG, Nickle DC, Mullins JI, (2004) Pervasive genomic recombination of HIV-1 in vivo. Genetics 167: 1573-1583.
47. Simmonds P, Balfe P, Ludlam CA, Bishop JO, Brown AJ, (1990) Analysis of sequence diversity in hypervariable regions of the external glycoprotein of human immunodeficiency virus type 1. J Virol 64: 5840-5850.
48. Giorgi EE, Funkhouser B, Athreya G, Perelson AS, Korber BT, et al. (2010) Estimating time since infection in early homogeneous HIV-1 samples using a poisson model. BMC Bioinformatics 11: 532.
49. Lee HY, Giorgi EE, Keele BF, Gaschen B, Athreya GS, et al. (2009) Modeling sequence evolution in acute HIV-1 infection. J Theor Biol 261: 341-360.
50. Ribeiro RM, Li H, Wang S, Stoddard MB, Learn GH, et al. (2012) Quantifying the diversification of hepatitis C virus (HCV) during primary infection: estimates of the in vivo mutataion rate. PLoS Pathog 8: e1002881.
51. Keele BF, Li H, Learn GH, Hraber P, Giorgi EE, et al. (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.
52. Perelson AS, Neumann AU, Markowitz M, Leonard JM, Ho DD, (1996) HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 271: 1582-1586.
53. Quinkert D, Bartenschlager R, Lohmann V, (2005) Quantitative analysis of the hepatitis C virus replication complex. J Virol 79: 13594-13605.
54. Macdonald RA, (1961) "Lifespan" of liver cells. Autoradio-graphic study using tritiated thymidine in normal, cirrhotic, and partially hepatectomized rats. Arch Intern Med 107: 335-343.
55. Shin EC, Park SH, Demino M, Nascimbeni M, Mihalik K, et al. (2011) Delayed induction, not impaired recruitment, of specific CD8(+) T cells causes the late onset of acute hepatitis C. Gastroenterology 141: 686-695, 686-695, e681.
56. Cuevas JM, Gonzalez-Candelas F, Moya A, Sanjuan R, (2009) Effect of ribavirin on the mutation rate and spectrum of hepatitis C virus in vivo. J Virol 83: 5760-5764.
57. Sanjuan R, Nebot MR, Chirico N, Mansky LM, Belshaw R, (2010) Viral mutation rates. J Virol 84: 9733-9748.
58. Wertheimer AM, Miner C, Lewinsohn DM, Sasaki AW, Kaufman E, et al. (2003) Novel CD4(+) and CD8(+) T-cell determinants within the NS3 protein in subjects with spontaneously resolved HCV infection. Hepatology 37: 577-589.
59. Kuntzen T, Timm J, Berical A, Lennon N, Berlin AM, et al. (2008) Naturally occurring dominant resistance mutations to hepatitis C virus protease and polymerase inhibitors in treatment-naive patients. Hepatology 48: 1769-1778.
60. Volkow P, Brouwer KC, Loza O, Ramos R, Lozada R, et al. (2009) Cross-border paid plasma donation among injection drug users in two Mexico-U.S. border cities. Int J Drug Policy 20: 409-412.
61. Timm J, Lauer GM, Kavanagh DG, Sheridan I, Kim AY, et al. (2004) CD8 epitope escape and reversion in acute HCV infection. J Exp Med 200: 1593-1604.
62. Cox AL, Mosbruger T, Lauer GM, Pardoll D, Thomas DL, et al. (2005) Comprehensive analyses of CD8+ T cell responses during longitudinal study of acute human hepatitis C. Hepatology 42: 104-112.
63. Smith DB, McAllister J, Casino C, Simmonds P, (1997) Virus 'quasispecies': making a mountain out of a molehill? J Gen Virol 78 (Pt 7) (): 1511-1519.
64. Duffy S, Shackelton LA, Holmes EC, (2008) Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9: 267-276.
65. Malet I, Belnard M, Agut H, Cahour A, (2003) From RNA to quasispecies: a DNA polymerase with proofreading activity is highly recommended for accurate assessment of viral diversity. J Virol Methods 109: 161-170.
66. Mansky LM, Temin HM, (1995) Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J Virol 69: 5087-5094.
67. Powdrill MH, Tchesnokov EP, Kozak RA, Russell RS, Martin R, et al. (2011) Contribution of a mutational bias in hepatitis C virus replication to the genetic barrier in the development of drug resistance. Proc Natl Acad Sci U S A 108: 20509-20513.
68. Kalinina O, Norder H, Magnius LO, (2004) Full-length open reading frame of a recombinant hepatitis C virus strain from St Petersburg: proposed mechanism for its formation. J Gen Virol 85: 1853-1857.
69. Noppornpanth S, Lien TX, Poovorawan Y, Smits SL, Osterhaus AD, et al. (2006) Identification of a naturally occurring recombinant genotype 2/6 hepatitis C virus. J Virol 80: 7569-7577.
70. Taucher C, Berger A, Mandl CW, (2010) A trans-complementing recombination trap demonstrates a low propensity of flaviviruses for intermolecular recombination. J Virol 84: 599-611.
71. Bernardin F, Herring B, Page-Shafer K, Kuiken C, Delwart E, (2006) Absence of HCV viral recombination following superinfection. J Viral Hepat 13: 532-537.
72. Klepper AL, Eng F, Walewski J, Schwartz M, Schiano TD, et al. (2011) HCV double-stranded RNA is abundant and may be an important viral resevoir in persistence and relapse. American Association for the Study of Liver Diseases, Hepatology Supplement pp. Oct; 54 (54), 1342A #2094.
73. Brenner BG, Roger M, Routy JP, Moisi D, Ntemgwa M, et al. (2007) High rates of forward transmission events after acute/early HIV-1 infection. J Infect Dis 195: 951-959.
74. Hollingsworth TD, Anderson RM, Fraser C, (2008) HIV-1 transmission, by stage of infection. J Infect Dis 198: 687-693.
75. Pilcher CD, Eron JJ Jr, Vemazza PL, Battegay M, Harr T, et al. (2001) Sexual transmission during the incubation period of primary HIV infection. Jama 286: 1713-1714.
76. Wawer MJ, Gray RH, Sewankambo NK, Serwadda D, Li X, et al. (2005) Rates of HIV-1 transmission per coital act, by stage of HIV-1 infection, in Rakai, Uganda. J Infect Dis 191: 1403-1409.
77. Ma ZM, Stone M, Piatak M Jr, Schweighardt B, Haigwood NL, et al. (2009) High specific infectivity of plasma virus from the pre-ramp-up and ramp-up stages of acute simian immunodeficiency virus infection. J Virol 83: 3288-3297.
78. Fierer DS, Factor SH, Uriel AJ, Carriero DC, Dieterich DT, et al. (2011) Sexual transmission of hepatitis C virus among HIV-infected men who have sex with men-New York City, 2005-2010. MMWR Morb Mortal Wkly Rep 60: 945-950.
79. van de Laar T, Pybus O, Bruisten S, Brown D, Nelson M, et al. (2009) Evidence of a large, international network of HCV transmission in HIV-positive men who have sex with men. Gastroenterology 136: 1609-1617.
80. Sack-Davis R, Daraganova G, Aitken C, Higgs P, Tracy L, et al. (2012) Hepatitis C virus phylogeny is associated with the social-injecting network in a cohort of people who inject drugs. PLos One In press.
81. Busch MP, Murthy KK, Kleinman SH, Hirschkorn DF, Herring BL, et al. (2012) Infectivity in chimpanzees (Pan troglodytes) of plasma collected before HCV RNA detectability by FDA-licensed assays: implications for transfusion safety and HCV infection outcomes. Blood 119: 6326-34.
82. Bar KJ, Tsao C-y, Iyer SS, Decker JM, Yang Y, et al. (2012) Early low-titer neutralizing antibodies impede HIV-1 replication and select for virus escape. PLoS Pathog 8: e1002721.
83. Ochsenbauer C, Edmonds TG, Ding H, Keele BF, Decker J, et al. (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.
84. Wilen CB, Parrish NF, Pfaff JM, Decker JM, Henning EA, et al. (2011) Phenotypic and immunologic comparison of clade B transmitted/founder and chronic HIV-1 envelope glycoproteins. J Virol 85: 8514-8527.
85. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
86. Stamatakis A, (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
87. Salazar-Gonzalez JF, Bailes E, Pham KT, Salazar MG, Guffey MB, et al. (2008) Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J Virol 82: 3952-3970.