Exceptional Heterogeneity in Viral Evolutionary Dynamics Characterises Chronic Hepatitis C Virus Infection

PLoS Pathogens

Volumn 12, Issue 9, 2016, Pages

  Raghwani, Jayna ^a   Rose, Rebecca ^b   Sheridan, Isabelle ^c   Lemey, Philippe ^d   Suchard, Marc A ^e   Santantonio, Teresa ^f   Farci, Patrizia ^g   Klenerman, Paul ^c   Pybus, Oliver G ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b BIOINFOEXPERTS LLC   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF FOGGIA   (Italy)

^g NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CHRONIC HEPATITIS C; CONTROLLED STUDY; DYNAMICS; EVOLUTIONARY ADAPTATION; FREQUENCY ANALYSIS; GENETIC HETEROGENEITY; GENETIC VARIABILITY; MOLECULAR EVOLUTION; MONTE CARLO METHOD; NONHUMAN; PHYLOGENY; SEQUENCE ANALYSIS; VIRUS LOAD; VIRUS TRANSMISSION; COMPARATIVE STUDY; FEMALE; FOLLOW UP; GENETICS; HEPACIVIRUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MALE; PHYSIOLOGY; VIRUS REPLICATION;

EVOLUTION, MOLECULAR; FEMALE; FOLLOW-UP STUDIES; HEPACIVIRUS; HEPATITIS C, CHRONIC; HIV INFECTIONS; HIV-1; HUMANS; MALE; VIRUS REPLICATION;

EID: 84989823202     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005894     Document Type: Article

References (78)

1. Smith DB, Pathirana S, Davidson F, Lawlor E, Power J, Yap PL, et al. The origin of hepatitis C virus genotypes. J Gen Virol. 1997;78 (Pt 2):321–8. 9018053
2. Kato T, Date T, Miyamoto M, Furusaka A, Tokushige K, Mizokami M, et al. Efficient replication of the genotype 2a hepatitis C virus subgenomic replicon. Gastroenterology. 2003;125(6):1808–17. 14724833
3. Hezode C, Forestier N, Dusheiko G, Ferenci P, Pol S, Goeser T, et al. Telaprevir and peginterferon with or without ribavirin for chronic HCV infection. N Engl J Med. 2009;360(18):1839–50. doi: 10.1056/NEJMoa080765019403903
4. Poordad F, McCone J, Jr.Bacon BR, u S, Manns MP, Sulkowski MS, et al. Boceprevir for untreated chronic HCV genotype 1 infection. N Engl J Med. 2011;364(13):1195–206. doi: 10.1056/NEJMoa101049421449783
5. Kohli A, Kapoor R, Sims Z, Nelson A, Sidharthan S, Lam B, et al. Ledipasvir and sofosbuvir for hepatitis C genotype 4: a proof-of-concept, single-centre, open-label phase 2a cohort study. Lancet Infect Dis. 2015;15(9):1049–54. doi: 10.1016/S1473-3099(15)00157-726187031
6. Kohli A, Osinusi A, Sims Z, Nelson A, Meissner EG, Barrett LL, et al. Virological response after 6 week triple-drug regimens for hepatitis C: a proof-of-concept phase 2A cohort study. Lancet. 2015;385(9973):1107–13. doi: 10.1016/S0140-6736(14)61228-925591505
7. Sulkowski M, Hezode C, Gerstoft J, Vierling JM, Mallolas J, Pol S, et al. Efficacy and safety of 8 weeks versus 12 weeks of treatment with grazoprevir (MK-5172) and elbasvir (MK-8742) with or without ribavirin in patients with hepatitis C virus genotype 1 mono-infection and HIV/hepatitis C virus co-infection (C-WORTHY): a randomised, open-label phase 2 trial. Lancet. 2015;385(9973):1087–97. doi: 10.1016/S0140-6736(14)61793-125467560
8. Nowak MA, May RM, Virus dynamics: mathematical principles of immunology and virology. Oxford; New York: Oxford University Press; 2000. xii, 237 p. p.
9. Neumann AU, Lam NP, Dahari H, Gretch DR, Wiley TE, Layden TJ, et al. Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-alpha therapy. Science. 1998;282(5386):103–7. 9756471
10. Dahari H, Feliu A, Garcia-Retortillo M, Forns X, Neumann AU, Second hepatitis C replication compartment indicated by viral dynamics during liver transplantation. J Hepatol. 2005;42(4):491–8. 15763335
11. Dahari H, Major M, Zhang X, Mihalik K, Rice CM, Perelson AS, et al. Mathematical modeling of primary hepatitis C infection: noncytolytic clearance and early blockage of virion production. Gastroenterology. 2005;128(4):1056–66. 15825086
12. Dahari H, Lo A, Ribeiro RM, Perelson AS, Modeling hepatitis C virus dynamics: liver regeneration and critical drug efficacy. J Theor Biol. 2007;247(2):371–81. 17451750
13. Macdonald RA, "Lifespan" of liver cells. Autoradio-graphic study using tritiated thymidine in normal, cirrhotic, and partially hepatectomized rats. Arch Intern Med. 1961;107:335–43. 13764742
14. Timpe JM, Stamataki Z, Jennings A, Hu K, Farquhar MJ, Harris HJ, et al. Hepatitis C virus cell-cell transmission in hepatoma cells in the presence of neutralizing antibodies. Hepatology. 2008;47(1):17–24. 17941058
15. Meredith LW, Harris HJ, Wilson GK, Fletcher NF, Balfe P, McKeating JA, Early infection events highlight the limited transmissibility of hepatitis C virus in vitro. J Hepatol. 2013;58(6):1074–80. doi: 10.1016/j.jhep.2013.01.01923353869
16. Xiao S, Wang Q, Si L, Shi Y, Wang H, Yu F, et al. Synthesis and anti-HCV entry activity studies of beta-cyclodextrin-pentacyclic triterpene conjugates. ChemMedChem. 2014;9(5):1060–70. doi: 10.1002/cmdc.20130054524623716
17. Lau DT, Fish PM, Sinha M, Owen DM, Lemon SM, Gale M, Jr. Interferon regulatory factor-3 activation, hepatic interferon-stimulated gene expression, and immune cell infiltration in hepatitis C virus patients. Hepatology. 2008;47(3):799–809. doi: 10.1002/hep.2207618203148
18. Liang YQ, Shilagard T, Xiao SY, Snyder N, Lau D, Cicalese L, et al. Visualizing Hepatitis C Virus Infections in Human Liver by Two-Photon Microscopy. Gastroenterology. 2009;137(4):1448–58. doi: 10.1053/j.gastro.2009.07.05019632233
19. Stiffler JD, Nguyen M, Sohn JA, Liu C, Kaplan D, Seeger C, Focal distribution of hepatitis C virus RNA in infected livers. PloS One. 2009;4(8):e6661. doi: 10.1371/journal.pone.000666119688046
20. Kandathil AJ, Graw F, Quinn J, Hwang HS, Torbenson M, Perelson AS, et al. Use of laser capture microdissection to map hepatitis C virus-positive hepatocytes in human liver. Gastroenterology. 2013;145(6):1404–13 e1-10. doi: 10.1053/j.gastro.2013.08.03423973767
21. Wieland S, Makowska Z, Campana B, Calabrese D, Dill MT, Chung J, et al. Simultaneous detection of hepatitis C virus and interferon stimulated gene expression in infected human liver. Hepatology. 2014;59(6):2121–30. doi: 10.1002/hep.2677024122862
22. Gray RR, Strickland SL, Veras NM, Goodenow MM, Pybus OG, Lemon SM, et al. Unexpected Maintenance of Hepatitis C Viral Diversity following Liver Transplantation. J Virol. 2012;86(16):8432–9. doi: 10.1128/JVI.00749-1222623804
23. Lawitz E, Poordad F, Kowdley KV, Cohen DE, Podsadecki T, Siggelkow S, et al. A phase 2a trial of 12-week interferon-free therapy with two direct-acting antivirals (ABT-450/r, ABT-072) and ribavirin in IL28B C/C patients with chronic hepatitis C genotype 1. J Hepatol. 2013;59(1):18–23. doi: 10.1016/j.jhep.2013.02.00923439262
24. Soriano V, Vispo E, de Mendoza C, Labarga P, Plaza Z, Fernandez-Montero JV, et al. Very late relapse after discontinuation of antiviral therapy for chronic hepatitis C. Antivir Ther. 2013;18(8):1033–5. doi: 10.3851/IMP265923804629
25. Barreiro P, Vispo E, Maida I, Aguilera A, Fernandez-Montero JV, de Mendoza C, et al. Very late HCV relapse following triple therapy for hepatitis C. Antivir Ther. 2014;19(7):723–4. doi: 10.3851/IMP275324535551
26. Ho DD, Neumann AU, Perelson AS, Chen W, Leonard JM, Markowitz M, Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature. 1995;373(6510):123–6. 7816094
27. Wei X, Ghosh SK, Taylor ME, Johnson VA, Emini EA, Deutsch P, et al. Viral dynamics in human immunodeficiency virus type 1 infection. Nature. 1995;373(6510):117–22. 7529365
28. Graw F, Balagopal A, Kandathil AJ, Ray SC, Thomas DL, Ribeiro RM, et al. Inferring viral dynamics in chronically HCV infected patients from the spatial distribution of infected hepatocytes. PLoS Comput Biol. 2014;10(11):e1003934. doi: 10.1371/journal.pcbi.100393425393308
29. Maggi F, Fornai C, Vatteroni ML, Giorgi M, Morrica A, Pistello M, et al. Differences in hepatitis C virus quasispecies composition between liver, peripheral blood mononuclear cells and plasma. J Gen Virol. 1997;78:1521–5. 9225024
30. Navas S, Martin J, Quiroga JA, Castillo I, Carreno V, Genetic diversity and tissue compartmentalization of the hepatitis C virus genome in blood mononuclear cells, liver, and serum from chronic hepatitis C patients. J Virol. 1998;72(2):1640–6. 9445070
31. Maggi F, Fornai C, Morrica A, Vatteroni ML, Giorgi M, Marchi S, et al. Divergent evolution of hepatitis C virus in liver and peripheral blood mononuclear cells of infected patients. J Med Virol. 1999;57(1):57–63. 9890422
32. Sobesky R, Feray C, Rimlinger F, Derian N, Dos Santos A, Roque-Afonso AM, et al. Distinct hepatitis C virus core and F protein quasispecies in tumoral and nontumoral hepatocytes isolated via microdissection. Hepatology. 2007;46(6):1704–12. 17935229
33. Bauhofer O, Ruggieri A, Schmid B, Schirmacher P, Bartenschlager R, Persistence of HCV in quiescent hepatic cells under conditions of an interferon-induced antiviral response. Gastroenterology. 2012;143(2):429–38 e8. doi: 10.1053/j.gastro.2012.04.01822522091
34. Cuevas JM, 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(11):5760–4. doi: 10.1128/JVI.00201-0919321623
35. Ribeiro RM, Li H, Wang S, Stoddard MB, Learn GH, Korber BT, et al. Quantifying the diversification of hepatitis C virus (HCV) during primary infection: estimates of the in vivo mutation rate. Plos Pathog. 2012;8(8):e1002881. doi: 10.1371/journal.ppat.100288122927817
36. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, Salazar MG, et al. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A. 2008;105(21):7552–7. doi: 10.1073/pnas.080220310518490657
37. Frater AJ, Edwards CT, McCarthy N, Fox J, Brown H, Milicic A, et al. Passive sexual transmission of human immunodeficiency virus type 1 variants and adaptation in new hosts. J Virol. 2006;80(14):7226–34. 16809328
38. Abrahams MR, Anderson JA, Giorgi EE, Seoighe C, Mlisana K, Ping LH, et al. Quantitating the multiplicity of infection with human immunodeficiency virus type 1 subtype C reveals a non-poisson distribution of transmitted variants. J Virol. 2009;83(8):3556–67. doi: 10.1128/JVI.02132-0819193811
39. Ross HA, Rodrigo AG, Immune-mediated positive selection drives human immunodeficiency virus type 1 molecular variation and predicts disease duration. J Virol. 2002;76(22):11715–20. 12388731
40. Lemey P, Kosakovsky Pond SL, Drummond AJ, Pybus OG, Shapiro B, Barroso H, et al. Synonymous substitution rates predict HIV disease progression as a result of underlying replication dynamics. PLoS Comput Biol. 2007;3(2):e29. 17305421
41. Vrancken B, Rambaut A, Suchard MA, Drummond A, Baele G, Derdelinckx I, et al. The genealogical population dynamics of HIV-1 in a large transmission chain: bridging within and among host evolutionary rates. PLoS Comput Biol. 2014;10(4):e1003505. doi: 10.1371/journal.pcbi.100350524699231
42. Farci P, Shimoda A, Coiana A, Diaz G, Peddis G, Melpolder JC, et al. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science. 2000;288(5464):339–44. 10764648
43. Farci P, Wollenberg K, Diaz G, Engle RE, Lai ME, Klenerman P, et al. Profibrogenic chemokines and viral evolution predict rapid progression of hepatitis C to cirrhosis. Proc Natl Acad Sci U S A. 2012;109(36):14562–7. doi: 10.1073/pnas.121059210922829669
44. Williamson S, Adaptation in the env gene of HIV-1 and evolutionary theories of disease progression. Mol Biol Evol. 2003;20(8):1318–25. 12777505
45. Frost SD, Wrin T, Smith DM, Kosakovsky Pond SL, Liu Y, Paxinos E, et al. Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proc Natl Acad Sci U S A. 2005;102(51):18514–9. 16339909
46. Gray RR, Salemi M, Klenerman P, Pybus OG, A New Evolutionary Model for Hepatitis C Virus Chronic Infection. Plos Pathog. 2012;8(5).
47. Sanjuan R, Nebot MR, Chirico N, Mansky LM, Belshaw R, Viral mutation rates. J Virol. 2010;84(19):9733–48. doi: 10.1128/JVI.00694-1020660197
48. Jang SJ, Wang LF, Radkowski M, Rakela J, Laskus T, Differences between hepatitis C virus 5 ' untranslated region quasispecies in serum and liver. J Gen Virol. 1999;80:711–6. 10092011
49. Okuda M, Hino K, Korenaga M, Yamaguchi Y, Katoh Y, Okita K, Differences in hypervariable region 1 quasispecies of hepatitis C virus in human serum, peripheral blood mono-nuclear cells, and liver. Hepatology. 1999;29(1):217–22. 9862869
50. Sakai A, Kaneko S, Honda M, Matsushita E, Kobayashi K, Quasispecies of hepatitis C virus in serum and in three different parts of the liver of patients with chronic hepatitis. Hepatology. 1999;30(2):556–61. 10421668
51. Cabot B, Martell M, Esteban JI, Sauleda S, Otero T, Esteban R, et al. Nucleotide and amino acid complexity of hepatitis C virus quasispecies in serum and liver. J Virol. 2000;74(2):805–11. 10623742
52. Jouvencel AC, Neau D, Faure M, Neau M, Martinaud C, Legrand E, et al. Plasma and liver hepatitis C virus variability in patients coinfected with human immunodeficiency virus. J Clin Microbiol. 2006;44(5):1877–80. 16672429
53. Ramirez S, Perez-Del-Pulgar S, Carrion JA, Costa J, Gonzalez P, Massaguer A, et al. Hepatitis C Virus Compartmentalization and Infection Recurrence after Liver Transplantation. Am J Transplant. 2009;9(7):1591–601. doi: 10.1111/j.1600-6143.2009.02666.x19459796
54. Ruster B, Zeuzem S, Krump-Konvalinkova V, Berg T, Jonas S, Severin K, et al. Comparative sequence analysis of the core- and NSS-region of hepatitis C virus from tumor and adjacent non-tumor tissue. J Med Virol. 2001;63(2):128–34. 11170049
55. Alam SS, Nakamura T, Naganuma A, Nozaki A, Nouso K, Shimomura H, et al. Hepatitis C virus quasispecies in cancerous and noncancerous hepatic lesions: The core protein-encoding region. Acta Med Okayama. 2002;56(3):141–7. 12108585
56. Pavio N, Battaglia S, Boucreux D, Arnulf B, Sobesky R, Hermine O, et al. Hepatitis C virus core variants isolated from liver tumor but not from adjacent non-tumor tissue interact with Smad3 and inhibit the TGF-beta pathway. Oncogene. 2005;24(40):6119–32. 16007207
57. Harouaka D, Engle RE, Wollenberg K, Diaz G, Tice AB, Zamboni F, et al. Diminished viral replication and compartmentalization of hepatitis C virus in hepatocellular carcinoma tissue. Proc Natl Acad Sci U S A. 2016;113(5):1375–80. doi: 10.1073/pnas.151687911326787866
58. Brimacombe CL, Grove J, Meredith LW, Hu K, Syder AJ, Flores MV, et al. Neutralizing Antibody-Resistant Hepatitis C Virus Cell-to-Cell Transmission. J Virol. 2011;85(1):596–605. doi: 10.1128/JVI.01592-1020962076
59. Roque-Afonso AM, Ducoulombier D, Di Liberto G, Kara R, Gigou M, Dussaix E, et al. Compartmentalization of hepatitis C virus genotypes between plasma and peripheral blood mononuclear cells. J Virol. 2005;79(10):6349–57. 15858018
60. Roque-Afonso AM, Jiang JJ, Penin F, Tareau C, Samuel D, Petit MA, et al. Nonrandom distribution of hepatitis C virus quasispecies in plasma and peripheral blood mononuclear cell subsets. J Virol. 1999;73(11):9213–21. 10516029
61. Zehender G, De Maddalena C, Bernini F, Ebranati E, Monti G, Pioltelli P, et al. Compartmentalization of hepatitis C virus quasispecies in blood mononuclear cells of patients with mixed cryoglobulinemic syndrome. J Virol. 2005;79(14):9145–56. 15994809
62. Forton DM, Karayiannis P, Mahmud N, Taylor-Robinson SD, Thomas HC, Identification of unique hepatitis C virus quasispecies in the central nervous system and comparative analysis of internal translational efficiency of brain, liver, and serum variants. J Virol. 2004;78(10):5170–83. 15113899
63. Chang M, Marquardt AP, Wood BL, Williams O, Cotler SJ, Taylor SL, et al. In situ distribution of hepatitis C virus replicative-intermediate RNA in hepatic tissue and its correlation with liver disease. J Virol. 2000;74(2):944–55. 10623757
64. Alfonso V, Mbayed VA, Sookoian S, Campos RH, Intra-host evolutionary dynamics of hepatitis C virus E2 in treated patients. J Gen Virol. 2005;86(Pt 10):2781–6. 16186232
65. Li H, McMahon BJ, McArdle S, Bruden D, Sullivan DG, Shelton D, et al. Hepatitis C virus envelope glycoprotein co-evolutionary dynamics during chronic hepatitis C. Virology. 2008;375(2):580–91. doi: 10.1016/j.virol.2008.02.01218343477
66. Ramachandran S, Campo DS, Dimitrova ZE, Xia GL, Purdy MA, Khudyakov YE, Temporal variations in the hepatitis C virus intrahost population during chronic infection. J Virol. 2011;85(13):6369–80. doi: 10.1128/JVI.02204-1021525348
67. Simmonds P, Smith DB, McOmish F, Yap PL, Kolberg J, Urdea MS, et al. Identification of genotypes of hepatitis C virus by sequence comparisons in the core, E1 and NS-5 regions. J Gen Virol. 1994;75 (Pt 5):1053–61. 8176367
68. Miralles R, Gerrish PJ, Moya A, Elena SF, Clonal interference and the evolution of RNA viruses. Science. 1999;285(5434):1745–7. 10481012
69. Chen AY, Hoare M, Shankar AN, Allison M, Alexander GJ, Michalak TI, Persistence of Hepatitis C Virus Traces after Spontaneous Resolution of Hepatitis C. PloS One. 2015;10(10):e0140312. doi: 10.1371/journal.pone.014031226473969
70. Gray RR, Tanaka Y, Takebe Y, Magiorkinis G, Buskell Z, Seeff L, et al. Evolutionary analysis of hepatitis C virus gene sequences from 1953. Philos Trans R Soc Lond B Biol Sci. 2013;368(1626):20130168. doi: 10.1098/rstb.2013.016823938759
71. Farci P, Quinti I, Farci S, Alter HJ, Strazzera R, Palomba E, et al. Evolution of hepatitis C viral quasispecies and hepatic injury in perinatally infected children followed prospectively. Proc Natl Acad Sci U S A. 2006;103(22):8475–80. 16707577
72. Shankarappa R, Margolick JB, Gange SJ, Rodrigo AG, Upchurch D, Farzadegan H, et al. Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J Virol. 1999;73(12):10489–502. 10559367
73. 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(10):2731–9. doi: 10.1093/molbev/msr12121546353
74. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R, DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003;19(18):2496–7. 14668244
75. Drummond AJ, Suchard MA, Xie D, Rambaut A, Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29(8):1969–73. doi: 10.1093/molbev/mss07522367748
76. Zanini F, Brodin J, Thebo L, Lanz C, Bratt G, Albert J, et al. Population genomics of intrapatient HIV-1 evolution. Elife. 2015;4:e11282doi: 10.7554/eLife.1128226652000
77. Dialdestoro K, Sibbesen JA, Maretty L, Raghwani J, Gall A, Kellam P, et al. Coalescent Inference Using Serially Sampled, High-Throughput Sequencing Data from Intrahost HIV Infection. Genetics. 2016;202(4):1449–72. doi: 10.1534/genetics.115.17793126857628
78. Lu Y, Xu Y, Di Bisceglie AM, Fan X, Comprehensive cloning of patient-derived 9022-bp amplicons of hepatitis C virus. J Virol Methods. 2013;191(2):105–12. doi: 10.1016/j.jviromet.2013.04.01023602804