High-resolution genetic profile of viral genomes: Why it matters

Current Opinion in Virology

Volumn 14, Issue , 2015, Pages 62-

  Qi, Hangfei ^a   Wu, Nicholas C ^b,c   Du, Yushen ^a   Wu, Ting Ting ^a   Sun, Ren ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; ANTIVIRAL RESISTANCE; DNA SEQUENCE; DRUG DESIGN; DRUG RESISTANCE; DRUG SENSITIVITY; GENETIC SELECTION; HAPLOTYPE; HEALTH HAZARD; HEPATITIS C VIRUS; MOLECULAR DOCKING; NONHUMAN; PERSONALIZED MEDICINE; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; VIRAL GENETICS; VIRUS GENOME; VIRUS LOAD; VIRUS REPLICATION; VIRUS RESISTANCE; VIRUS STRAIN; DRUG EFFECTS; GENETICS; HEPACIVIRUS; HUMAN; METABOLISM; MUTATION;

ANTIVIRAL AGENTS; DRUG RESISTANCE, VIRAL; GENOME, VIRAL; HEPACIVIRUS; HUMANS; MUTATION; VIRAL PROTEINS;

EID: 84941204245     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2015.08.005     Document Type: Review

References (88)

1. V. Lohmann, F. Körner, J.-O. Koch, U. Herian, L. Theilmann, and R. Bartenschlager Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line Science 285 1999 110 113
2. K.J. Blight, A.A. Kolykhalov, and C.M. Rice Efficient initiation of HCV RNA replication in cell culture Science 290 2000 1972 1974
3. B.D. Lindenbach, M.J. Evans, A.J. Syder, B. Wolk, T.L. Tellinghuisen, C.C. Liu, T. Maruyama, R.O. Hynes, D.R. Burton, J.A. McKeating, and et al. Complete replication of hepatitis C virus in cell culture Science 309 2005 623 626
4. T. Wakita, T. Pietschmann, T. Kato, T. Date, M. Miyamoto, Z. Zhao, K. Murthy, A. Habermann, H.G. Krausslich, M. Mizokami, and et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome Nat Med 11 2005 791 796
5. M. Yi, R.A. Villanueva, D.L. Thomas, T. Wakita, and S.M. Lemon Production of infectious genotype 1a hepatitis C virus (Hutchinson strain) in cultured human hepatoma cells Proc Natl Acad Sci U S A 103 2006 2310 2315
6. A.S. deLemos, and R.T. Chung Hepatitis C treatment: an incipient therapeutic revolution Trends Mol Med 20 2014 315 321
7. V. Soriano, E. Vispo, E. Poveda, P. Labarga, L. Martin-Carbonero, J.V. Fernandez-Montero, and P. Barreiro Directly acting antivirals against hepatitis C virus J Antimicrob Chemother 66 2011 1673 1686
8. B.R. Bacon, S.C. Gordon, E. Lawitz, P. Marcellin, J.M. Vierling, S. Zeuzem, F. Poordad, Z.D. Goodman, H.L. Sings, N. Boparai, and et al. Boceprevir for previously treated chronic HCV genotype 1 infection N Engl J Med 364 2011 1207 1217
9. F. Poordad, J. McCone Jr., B.R. Bacon, S. Bruno, M.P. Manns, M.S. Sulkowski, I.M. Jacobson, K.R. Reddy, Z.D. Goodman, N. Boparai, and et al. Boceprevir for untreated chronic HCV genotype 1 infection N Engl J Med 364 2011 1195 1206
10. I.M. Jacobson, J.G. McHutchison, G. Dusheiko, A.M. Di Bisceglie, K.R. Reddy, N.H. Bzowej, P. Marcellin, A.J. Muir, P. Ferenci, R. Flisiak, and et al. Telaprevir for previously untreated chronic hepatitis C virus infection N Engl J Med 364 2011 2405 2416
11. S. Zeuzem, P. Andreone, S. Pol, E. Lawitz, M. Diago, S. Roberts, R. Focaccia, Z. Younossi, G.R. Foster, A. Horban, and et al. Telaprevir for retreatment of HCV infection N Engl J Med 364 2011 2417 2428
12. T.L. Kieffer, and S. George Resistance to hepatitis C virus protease inhibitors Curr Opin Virol 8 2014 16 21
13. M.W. Fried, M. Buti, G.J. Dore, R. Flisiak, P. Ferenci, I. Jacobson, P. Marcellin, M. Manns, I. Nikitin, F. Poordad, and et al. Once-daily simeprevir (TMC435) with pegylated interferon and ribavirin in treatment-naive genotype 1 hepatitis C: the randomized PILLAR study Hepatology 58 2013 1918 1929
14. O. Lenz, L. Vijgen, J.M. Berke, M.D. Cummings, B. Fevery, M. Peeters, G. De Smedt, C. Moreno, and G. Picchio Virologic response and characterisation of HCV genotype 2-6 in patients receiving TMC435 monotherapy (study TMC435-C202) J Hepatol 58 2013 445 451
15. A.M. Lam, C. Espiritu, S. Bansal, H.M. Micolochick Steuer, C. Niu, V. Zennou, M. Keilman, Y. Zhu, S. Lan, M.J. Otto, and et al. Genotype and subtype profiling of PSI-7977 as a nucleotide inhibitor of hepatitis C virus Antimicrob Agents Chemother 56 2012 3359 3368
16. J.A. Lemm, D. O'Boyle, M. Liu, P.T. Nower, R. Colonno, M.S. Deshpande, L.B. Snyder, S.W. Martin, St. Laurent, M.H. Serrano-Wu DR, and et al. Identification of Hepatitis C virus NS5A inhibitors J Virol 84 2010 482 491
17. M. Gao, R.E. Nettles, M. Belema, L.B. Snyder, V.N. Nguyen, R.A. Fridell, M.H. Serrano-Wu, D.R. Langley, J.-H. Sun, O. ÄôBoyle Ii D.R., and et al. Chemical genetics strategy identifies an HCV NS5A inhibitor with a potent clinical effect Nature 465 2010 96 100
18. R.A. Fridell, D. Qiu, C. Wang, L. Valera, and M. Gao Resistance analysis of the hepatitis C virus NS5A inhibitor BMS-790052 in an in vitro replicon system Antimicrob Agents Chemother 54 2010 3641 3650
19. C. Wang, H. Huang, L. Valera, J.-H. Sun, D.R. O'Boyle, P.T. Nower, L. Jia, D. Qiu, X. Huang, A. Altaf, and et al. Hepatitis C virus RNA elimination and development of resistance in replicon cells treated with BMS-790052 Antimicrob Agents Chemother 56 2012 1350 1358
20. C. Wang, L. Jia, H. Huang, D. Qiu, L. Valera, X. Huang, J.H. Sun, P.T. Nower, D.R. O'Boyle 2nd, M. Gao, and et al. In vitro activity of BMS-790052 on hepatitis C virus genotype 4 NS5A Antimicrob Agents Chemother 56 2012 1588 1590
21. P. Ferenci Treatment of hepatitis C in difficult-to-treat patients Nat Rev Gastroenterol Hepatol 12 2015 284 292
22. K.V. Kowdley, S.C. Gordon, K.R. Reddy, L. Rossaro, D.E. Bernstein, E. Lawitz, M.L. Shiffman, E. Schiff, R. Ghalib, M. Ryan, and et al. Ledipasvir and sofosbuvir for 8 or 12 weeks for chronic HCV without cirrhosis N Engl J Med 370 2014 1879 1888
23. N. Afdhal, K.R. Reddy, D.R. Nelson, E. Lawitz, S.C. Gordon, E. Schiff, R. Nahass, R. Ghalib, N. Gitlin, R. Herring, and et al. Ledipasvir and sofosbuvir for previously treated HCV genotype 1 infection N Engl J Med 370 2014 1483 1493
24. N. Afdhal, S. Zeuzem, P. Kwo, M. Chojkier, N. Gitlin, M. Puoti, M. Romero-Gomez, J.P. Zarski, K. Agarwal, P. Buggisch, and et al. Ledipasvir and sofosbuvir for untreated HCV genotype 1 infection N Engl J Med 370 2014 1889 1898
25. P. Ferenci, D. Bernstein, J. Lalezari, D. Cohen, Y. Luo, C. Cooper, E. Tam, R.T. Marinho, N. Tsai, A. Nyberg, and et al. ABT-450/r-ombitasvir and dasabuvir with or without ribavirin for HCV N Engl J Med 370 2014 1983 1992
26. E. Lawitz, F.F. Poordad, P.S. Pang, R.H. Hyland, X. Ding, H. Mo, W.T. Symonds, J.G. McHutchison, and F.E. Membreno Sofosbuvir and ledipasvir fixed-dose combination with and without ribavirin in treatment-naive and previously treated patients with genotype 1 hepatitis C virus infection (LONESTAR): an open-label, randomised, phase 2 trial Lancet 383 2014 515 523
27. C. Bock, and T. Lengauer Managing drug resistance in cancer: lessons from HIV therapy Nat Rev Cancer 12 2012 494 501
28. R.M. Ribeiro, H. Li, S. Wang, M.B. Stoddard, G.H. Learn, B.T. Korber, T. Bhattacharya, J. Guedj, E.H. Parrish, B.H. Hahn, and et al. Quantifying the diversification of hepatitis C virus (HCV) during primary infection: estimates of the in vivo mutation rate PLoS Pathog 8 2012 e1002881
29. J.M. Cuevas, F. Gonzalez-Candelas, A. Moya, and R. Sanjuan Effect of ribavirin on the mutation rate and spectrum of hepatitis C virus in vivo J Virol 83 2009 5760 5764
30. A.U. Neumann, N.P. Lam, H. Dahari, D.R. Gretch, T.E. Wiley, T.J. Layden, and A.S. Perelson Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-alpha therapy Science 282 1998 103 107
31. L. Rong, H. Dahari, R.M. Ribeiro, and A.S. Perelson Rapid emergence of protease inhibitor resistance in hepatitis C virus Sci Transl Med 2 2010 ra3230
32. M. Robinson, Y. Tian, Delaney WEt, and A.E. Greenstein Preexisting drug-resistance mutations reveal unique barriers to resistance for distinct antivirals Proc Natl Acad Sci U S A 108 2011 10290 10295
33. A.J. Thompson, S.A. Locarnini, and M.R. Beard Resistance to anti-HCV protease inhibitors Curr Opin Virol 1 2011 599 606
34. D.M. Fowler, and S. Fields Deep mutational scanning: a new style of protein science Nat Methods 11 2014 801 807
35. D.M. Fowler, J.J. Stephany, and S. Fields Measuring the activity of protein variants on a large scale using deep mutational scanning Nat Protoc 9 2014 2267 2284
36. B.C. Cunningham, and J.A. Wells High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis Science 244 1989 1081 1085
37. C.L. Murray, C.T. Jones, J. Tassello, and C.M. Rice Alanine scanning of the hepatitis C virus core protein reveals numerous residues essential for production of infectious virus J Virol 81 2007 10220 10231
38. T. Kekarainen, H. Savilahti, and J.P. Valkonen Functional genomics on potato virus A: virus genome-wide map of sites essential for virus propagation Genome Res 12 2002 584 594
39. V. Arumugaswami, R. Remenyi, V. Kanagavel, E.Y. Sue, T. Ngoc Ho, C. Liu, V. Fontanes, A. Dasgupta, and R. Sun High-resolution functional profiling of hepatitis C virus genome PLoS Pathog 4 2008 e1000182
40. B.F. Beitzel, R.R. Bakken, J.M. Smith, and C.S. Schmaljohn High-resolution functional mapping of the Venezuelan equine encephalitis virus genome by insertional mutagenesis and massively parallel sequencing PLoS Pathog 6 2010 e1001146
41. L. Thorne, D. Bailey, and I. Goodfellow High-resolution functional profiling of the norovirus genome J Virol 86 2012 11441 11456
42. N.S. Heaton, D. Sachs, C.J. Chen, R. Hai, and P. Palese Genome-wide mutagenesis of influenza virus reveals unique plasticity of the hemagglutinin and NS1 proteins Proc Natl Acad Sci U S A 110 2013 20248 20253
43. R. Remenyi, H. Qi, S.-Y. Su, Z. Chen, N.C. Wu, V. Arumugaswami, S. Truong, V. Chu, T. Stokelman, H.-H. Lo, and et al. A comprehensive functional map of the hepatitis C virus genome provides a resource for probing viral proteins mBio 2014 5
44. L.Q. Al-Mawsawi, N.C. Wu, C.A. Olson, V.C. Shi, H. Qi, X. Zheng, T.T. Wu, and R. Sun High-throughput profiling of point mutations across the HIV-1 genome Retrovirology 11 2014 124
45. N.C. Wu, A.P. Young, S. Dandekar, H. Wijersuriya, L.Q. Al-Mawsawi, T.-T. Wu, and R. Sun Systematic identification of H274Y compensatory mutations in influenza A virus neuraminidase by high-throughput screening J Virol 87 2013 1193 1199
46. N.C. Wu, A.P. Young, L.Q. Al-Mawsawi, C.A. Olson, J. Feng, H. Qi, S.H. Chen, I.H. Lu, C.Y. Lin, R.G. Chin, and et al. High-throughput profiling of influenza A virus hemagglutinin gene at single-nucleotide resolution Sci Rep 4 2014 4942
47. J.D. Bloom An experimentally determined evolutionary model dramatically improves phylogenetic fit Mol Biol Evol 31 2014 1956 1978
48. B. Thyagarajan, and J.D. Bloom The inherent mutational tolerance and antigenic evolvability of influenza hemagglutinin Elife 2014 3
49. K. Das, J.M. Aramini, L.C. Ma, R.M. Krug, and E. Arnold Structures of influenza A proteins and insights into antiviral drug targets Nat Struct Mol Biol 17 2010 530 538
50. A. Engelman, and P. Cherepanov The structural biology of HIV-1: mechanistic and therapeutic insights Nat Rev Microbiol 10 2012 279 290
51. D. Moradpour, and F. Penin Hepatitis C virus proteins: from structure to function Curr Top Microbiol Immunol 369 2013 113 142
52. D.C. Ekiert, G. Bhabha, M.A. Elsliger, R.H. Friesen, M. Jongeneelen, M. Throsby, J. Goudsmit, and I.A. Wilson Antibody recognition of a highly conserved influenza virus epitope Science 324 2009 246 251
53. M. Throsby, E. van den Brink, M. Jongeneelen, L.L. Poon, P. Alard, L. Cornelissen, A. Bakker, F. Cox, E. van Deventer, Y. Guan, and et al. Heterosubtypic neutralizing monoclonal antibodies cross-protective against H5N1 and H1N1 recovered from human IgM+ memory B cells PLoS One 3 2008 e3942
54. S.J. Fleishman, T.A. Whitehead, D.C. Ekiert, C. Dreyfus, J.E. Corn, E.M. Strauch, I.A. Wilson, and D. Baker Computational design of proteins targeting the conserved stem region of influenza hemagglutinin Science 332 2011 816 821
55. H. Qi, C.A. Olson, N.C. Wu, R. Ke, C. Loverdo, V. Chu, S. Truong, R. Remenyi, Z. Chen, Y. Du, and et al. A quantitative high-resolution genetic profile rapidly identifies sequence determinants of hepatitis C viral fitness and drug sensitivity PLoS Pathog 10 2014 e1004064
56. R.A. Fridell, C. Wang, J.H. Sun, D.R. O'Boyle 2nd, P. Nower, L. Valera, D. Qiu, S. Roberts, X. Huang, B. Kienzle, and et al. Genotypic and phenotypic analysis of variants resistant to hepatitis C virus nonstructural protein 5A replication complex inhibitor BMS-790052 in humans: in vitro and in vivo correlations Hepatology 54 2011 1924 1935
57. Y. Suzuki, K. Ikeda, F. Suzuki, J. Toyota, Y. Karino, K. Chayama, Y. Kawakami, H. Ishikawa, H. Watanabe, W. Hu, and et al. Dual oral therapy with daclatasvir and asunaprevir for patients with HCV genotype 1b infection and limited treatment options J Hepatol 58 2013 655 662
58. G.T. Everson, K.D. Sims, M. Rodriguez-Torres, C. Hezode, E. Lawitz, M. Bourliere, V. Loustaud-Ratti, V. Rustgi, H. Schwartz, H. Tatum, and et al. Efficacy of an interferon- and ribavirin-free regimen of daclatasvir, asunaprevir, and BMS-791325 in treatment-naive patients with HCV genotype 1 infection Gastroenterology 146 2014 420 429
59. M. Manns, S. Pol, I.M. Jacobson, P. Marcellin, S.C. Gordon, C.Y. Peng, T.T. Chang, G.T. Everson, J. Heo, G. Gerken, and et al. All-oral daclatasvir plus asunaprevir for hepatitis C virus genotype 1b: a multinational, phase 3, multicohort study Lancet 384 2014 1597 1605
60. E. Murakami, M. Imamura, C.N. Hayes, H. Abe, N. Hiraga, Y. Honda, A. Ono, K. Kosaka, T. Kawaoka, M. Tsuge, and et al. Ultradeep sequencing study of chronic hepatitis C virus genotype 1 infection in patients treated with daclatasvir, peginterferon, and ribavirin Antimicrob Agents Chemother 58 2014 2105 2112
61. M.S. Sulkowski, D.F. Gardiner, M. Rodriguez-Torres, K.R. Reddy, T. Hassanein, I. Jacobson, E. Lawitz, A.S. Lok, F. Hinestrosa, P.J. Thuluvath, and et al. Daclatasvir plus sofosbuvir for previously treated or untreated chronic HCV infection N Engl J Med 370 2014 211 221
62. C. Hezode, G.M. Hirschfield, W. Ghesquiere, W. Sievert, M. Rodriguez-Torres, S.D. Shafran, P.J. Thuluvath, H.A. Tatum, I. Waked, G. Esmat, and et al. Daclatasvir plus peginterferon alfa and ribavirin for treatment-naive chronic hepatitis C genotype 1 or 4 infection: a randomised study Gut 64 2015 948 956
63. A.J. Muir, F. Poordad, J. Lalezari, G. Everson, G.J. Dore, R. Herring, A. Sheikh, P. Kwo, C. Hezode, P.J. Pockros, and et al. Daclatasvir in combination with asunaprevir and beclabuvir for hepatitis C virus genotype 1 infection with compensated cirrhosis JAMA 313 2015 1736 1744
64. S. Yoshimi, M. Imamura, E. Murakami, N. Hiraga, M. Tsuge, Y. Kawakami, H. Aikata, H. Abe, C.N. Hayes, T. Sasaki, and et al. Long term persistence of NS5A inhibitor-resistant hepatitis C virus in patients who failed daclatasvir and asunaprevir therapy J Med Virol 87 2015 1913 1920
65. S. Harper, J.A. McCauley, M.T. Rudd, M. Ferrara, M. DiFilippo, B. Crescenzi, U. Koch, A. Petrocchi, M.K. Holloway, J.W. Butcher, and et al. Discovery of MK-5172, a macrocyclic hepatitis C virus NS3/4a protease inhibitor ACS Med Chem Lett 3 2012 332 336
66. B. Moreau, J.A. O'Meara, J. Bordeleau, M. Garneau, C. Godbout, V. Gorys, M. Leblanc, E. Villemure, P.W. White, and M. Llinàs-Brunet Discovery of hepatitis C virus NS3-4A protease inhibitors with improved barrier to resistance and favorable liver distribution J Med Chem 57 2014 1770 1776
67. V. Summa, S.W. Ludmerer, J.A. McCauley, C. Fandozzi, C. Burlein, G. Claudio, P.J. Coleman, J.M. Dimuzio, M. Ferrara, M. Di Filippo, and et al. MK-5172, a selective inhibitor of hepatitis C virus NS3/4a protease with broad activity across genotypes and resistant variants Antimicrob Agents Chemother 56 2012 4161 4167
68. A.M. Wensing, N.M. van Maarseveen, and M. Nijhuis Fifteen years of HIV protease inhibitors: raising the barrier to resistance Antiviral Res 85 2010 59 74
69. A.K. Ghosh, Z.L. Dawson, and H. Mitsuya Darunavir, a conceptually new HIV-1 protease inhibitor for the treatment of drug-resistant HIV Bioorg Med Chem 15 2007 7576 7580
70. J.V. Madruga, D. Berger, M. McMurchie, F. Suter, D. Banhegyi, K. Ruxrungtham, D. Norris, E. Lefebvre, M.P. de Bethune, F. Tomaka, and et al. Efficacy and safety of darunavir-ritonavir compared with that of lopinavir-ritonavir at 48 weeks in treatment-experienced. HIV-infected patients in TITAN: a randomised controlled phase III trial Lancet 370 2007 49 58
71. E. Fumero, and D. Podzamczer New patterns of HIV-1 resistance during HAART Clin Microbiol Infect 9 2003 1077 1084
72. J. Liu, M.D. Miller, R.M. Danovich, N. Vandergrift, F. Cai, C.B. Hicks, D.J. Hazuda, and F. Gao Analysis of low-frequency mutations associated with drug resistance to raltegravir before antiretroviral treatment Antimicrob Agents Chemother 55 2011 1114 1119
73. S. Palmer, V. Boltz, F. Maldarelli, M. Kearney, E.K. Halvas, D. Rock, J. Falloon, R.T. Davey Jr., R.L. Dewar, J.A. Metcalf, and et al. Selection and persistence of non-nucleoside reverse transcriptase inhibitor-resistant HIV-1 in patients starting and stopping non-nucleoside therapy AIDS 20 2006 701 710
74. B. Clotet Strategies for overcoming resistance in HIV-1 infected patients receiving HAART AIDS Rev 6 2004 123 130
75. I. Kinde, J. Wu, N. Papadopoulos, K.W. Kinzler, and B. Vogelstein Detection and quantification of rare mutations with massively parallel sequencing Proc Natl Acad Sci U S A 108 2011 9530 9535
76. D.I. Lou, J.A. Hussmann, R.M. McBee, A. Acevedo, R. Andino, W.H. Press, and S.L. Sawyer High-throughput DNA sequencing errors are reduced by orders of magnitude using circle sequencing Proc Natl Acad Sci U S A 110 2013 19872 19877
77. L.Q. Al-Mawsawi, N.C. Wu, J. De La Cruz, V.C. Shi, T.T. Wu, E.S. Daar, M.J. Lewis, O.O. Yang, and R. Sun Short communication: HIV-1 gag genetic variation in a single acutely infected participant defined by high-resolution deep sequencing AIDS Res Hum Retroviruses 30 2014 806 811
78. N.C. Wu, J. De La Cruz, L.Q. Al-Mawsawi, C.A. Olson, H. Qi, H.H. Luan, N. Nguyen, Y. Du, S. Le, T.T. Wu, and et al. HIV-1 quasispecies delineation by tag linkage deep sequencing PLoS One 9 2014 e97505
79. L.Z. Hong, S. Hong, H.T. Wong, P.P. Aw, Y. Cheng, A. Wilm, P.F. de Sessions, S.G. Lim, N. Nagarajan, M.L. Hibberd, and et al. BAsE-Seq: a method for obtaining long viral haplotypes from short sequence reads Genome Biol 15 2014 517
80. S. Mangul, N.C. Wu, N. Mancuso, A. Zelikovsky, R. Sun, and E. Eskin Accurate viral population assembly from ultra-deep sequencing data Bioinformatics 30 2014 i329 i337
81. O. Zagordi, A. Bhattacharya, N. Eriksson, and N. Beerenwinkel ShoRAH: estimating the genetic diversity of a mixed sample from next-generation sequencing data BMC Bioinformatics 12 2011 119
82. N. Eriksson, L. Pachter, Y. Mitsuya, S.Y. Rhee, C. Wang, B. Gharizadeh, M. Ronaghi, R.W. Shafer, and N. Beerenwinkel Viral population estimation using pyrosequencing PLoS Comput Biol 4 2008 e1000074
83. O. Zagordi, R. Klein, M. Daumer, and N. Beerenwinkel Error correction of next-generation sequencing data and reliable estimation of HIV quasispecies Nucleic Acids Res 38 2010 7400 7409
84. P. Skums, N. Mancuso, A. Artyomenko, B. Tork, I. Mandoiu, Y. Khudyakov, and A. Zelikovsky Reconstruction of viral population structure from next-generation sequencing data using multicommodity flows BMC Bioinformatics 14 Suppl. 9 2013 S2
85. M.C. Prosperi, and M. Salemi QuRe: software for viral quasispecies reconstruction from next-generation sequencing data Bioinformatics 28 2012 132 133
86. I. Astrovskaya, B. Tork, S. Mangul, K. Westbrooks, I. Mandoiu, P. Balfe, and A. Zelikovsky Inferring viral quasispecies spectra from 454 pyrosequencing reads BMC Bioinformatics 12 Suppl. 6 2011 S1
87. R. Ke, C. Loverdo, H. Qi, R. Sun, and J.O. Lloyd-Smith Rational design and adaptive management of combination therapies for hepatitis C virus infection PLoS Comput Biol 11 2015 e1004040
88. E. Poveda, D.L. Wyles, A. Mena, J.D. Pedreira, A. Castro-Iglesias, and E. Cachay Update on hepatitis C virus resistance to direct-acting antiviral agents Antiviral Res 108 2014 181 191