Hepatitis C quasispecies adaptation in the setting of a variable fidelity polymerase

References

• Choo QL, Kuo G, Weiner AJ, Overby LR, Bradley DW, Houghton M. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science. 1989;244(4902):359–362.
   PubMed Web of Science ®Google Scholar
• Alter MJ. Epidemiology of hepatitis C virus infection. World J Gastroenterol. 2007;13(17):2436–2441.
   PubMed Web of Science ®Google Scholar
• Pockros PJ. Developments in the treatment of chronic hepatitis C. Expert Opin Investig Drugs. 2002;11(4):515–528.
   PubMed Web of Science ®Google Scholar
• Steinhauer DA, Domingo E, Holland JJ. Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. Gene. 1992;122(2):281–288.
   PubMed Web of Science ®Google Scholar
• Eigen M. Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften. 1971;58(10):465–523.
   PubMedGoogle Scholar
• Gause GF. The Struggle for Existence. New York, Dover; 1971.
   Google Scholar
• Kimura M. The Neutral Theory of Molecular Evolution. Cambridge: Cambridge University Press; 1983.
   Google Scholar
• Nelson CW, Sanford JC. The effects of low-impact mutations in digital organisms. Theor Biol Med Model. 2011;8:9.
   Web of Science ®Google Scholar
• Van Valen L. A new evolutionary law. Evol Theory. 1973;1(1):1–30.
   Google Scholar
• Sole RV Ferrer R, Gonzalez-Garcia I, Quer J, Domingo E. Red queen dynamics, competition and critical points in a model of RNA virus quasispecies. J Theor Biol. 1999;198(1):47–59.
   Web of Science ®Google Scholar
• Furio V Moya A, Sanjuan R. The cost of replication fidelity in an RNA virus. Proc Nat Acad Sci U S A. 2005;102(29):10233–10237.
   Web of Science ®Google Scholar
• Muller HJ. The relation of recombination to mutational advance. Mutat Res. 1964;106:2–9.
   PubMed Web of Science ®Google Scholar
• Worobey M, Holmes EC. Evolutionary aspects of recombination in RNA viruses. J Gen Virol. 1999;80(Pt 10):2535–2543.
   PubMedGoogle Scholar
• Koonin EV Dolja VV Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit Rev Biochem Mol Biol. 1993;28(5):375–430.
   Web of Science ®Google Scholar
• Gerrish PJ, Lenski RE. The fate of competing beneficial mutations in an asexual population. Genetica. 1998;102–103(1–6):127–144.
   Web of Science ®Google Scholar
• Miralles R, Gerrish PJ, Moya A, Elena SF. Clonal interference and the evolution of RNA viruses. Science. 1999;285(5434):1745–1747.
   Web of Science ®Google Scholar
• de la Torre JC, Holland JJ. RNA virus quasispecies populations can suppress vastly superior mutant progeny. J Virol. 1990;64(12):6278–6281.
   Web of Science ®Google Scholar
• Miralles R, Moya A, Elena SF. Diminishing returns of population size in the rate of RNA virus adaptation. J Virol. 2000;74(8):3566–3571.
   Web of Science ®Google Scholar
• Imhof M, Schlotterer C. Fitness effects of advantageous mutations in evolving Escherichia coli populations. Proc Nat Acad Sci U S A. 2001;98(3):1113–1117.
   Web of Science ®Google Scholar
• Miller CR, Joyce P, Wichman HA. Mutational effects and population dynamics during viral adaptation challenge current models. Genetics. 2011;187(1):185–202.
   Web of Science ®Google Scholar
• Verbinnen T, Van Marck H, Vandenbroucke I, et al. Tracking the evolution of multiple in vitro hepatitis C virus replicon variants under protease inhibitor selection pressure by 454 deep sequencing. J Virol. 2010;84(21):11124–11133.
   Web of Science ®Google Scholar
• Bantel-Schaal U, zur Hausen H. Characterization of the DNA of a defective human parvovirus isolated from a genital site. Virology. 1984;134(1):52–63.
   Web of Science ®Google Scholar
• Laughlin CA, Myers MW, Risin DL, Carter BJ. Defective-interfering particles of the human parvovirus adeno-associated virus. Virology. 1979;94(1):162–174.
   Web of Science ®Google Scholar
• Palma EL, Huang A. Cyclic production of vesicular stomatitis virus caused by defective interfering particles. J Infect Dis. 1974;129(4):402–410.
   PubMed Web of Science ®Google Scholar
• Prince AM, Huima-Byron T, Parker TS, Levine DM. Visualization of hepatitis C virions and putative defective interfering particles isolated from low density lipoproteins. J Viral Hepat. 1996;3(1):11–17.
   Google Scholar
• Horikami SM, Curran J, Kolakofsky D, Moyer SA. Complexes of Sendai virus NP-P and PL proteins are required for defective interfering particle genome replication in vitro. J Virol. 1992;66(8):4901–4908.
   Google Scholar
• Perrault J. Origin and replication of defective interfering particles. Curr Top Microbiol Immunol. 1981;93:151–207.
   PubMedGoogle Scholar
• Kirkwood TB, Bangham CR. Cycles, chaos, and evolution in virus cultures: a model of defective interfering particles. Proc Nat Acad Sci U S A. 1994;91(18):8685–8689.
   Web of Science ®Google Scholar
• Marriott AC, Dimmock NJ. Defective interfering viruses and their potential as antiviral agents. Rev Med Virol. 2010;20(1):51–62.
   Web of Science ®Google Scholar
• Rao DD, Huang AS. Interference among defective interfering particles of vesicular stomatitis virus. J Virol. 1982;41(1):210–221.
   Web of Science ®Google Scholar
• Stumpf MP, Zitzmann N. RNA replication kinetics, genetic polymorphism and selection in the case of the hepatitis C virus. Proc Biol Sci. 2001;268(1480):1993–1999.
   Web of Science ®Google Scholar
• Navas S, Martín J, Quiroga JA, Castillo I, Carreño 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):1640–1646.
   Web of Science ®Google Scholar
• Gretch DR, Polyak SJ. The quasispecies nature of Hepatitis C Virus: research methods and biological implications. In: Groupe Français d’études molécularies des hépatites (GEMHEP), Hepatitis C Virus: 2; Genetic Heterogeneity and Viral Load. Paris: John Libbey Eurotext; 1997:57–69. [English].
   Google Scholar
• Cabot B, Martell M, Esteban JI, et al. Nucleotide and amino acid complexity of hepatitis C virus quasispecies in serum and liver. J Virol. 2000;74(2):805–811.
   Web of Science ®Google Scholar
• Wilke CO, Wang JL, Ofria C, Lenski RE, Adami C. Evolution of digital organisms at high mutation rates leads to survival of the flattest. Nature. 2001;412(6844):331–333.
   PubMed Web of Science ®Google Scholar
• Wilke CO. Adaptive evolution on neutral networks. Bull Math Biol. 2001;63(4):715–730.
   Web of Science ®Google Scholar
• Codoñer FM, Darós JA, Solé RV, Elena SF. The fittest versus the flattest: experimental confirmation of the quasispecies effect with subviral pathogens. PLoS Pathog. 2006;2(12):e136.
   Web of Science ®Google Scholar
• Campo D, Dimitrova Z, Mitchell R, Lara J, Khudyakov Y. Coordinated evolution of the hepatitis C virus. Proc Nat Acad Sci U S A. 2008;105(28):9685–9690.
   Web of Science ®Google Scholar
• Sanjuán R, Moya A, Elena SF. The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. Proc Nat Acad Sci USA. 2004;101(22):8396–8401.
   Web of Science ®Google Scholar
• Aguirre J, Lázaro E, Manrubia SC. A trade-off between neutrality and adaptability limits the optimization of viral quasispecies. J Theor Biol. 2009;261(1):148–155.
   Web of Science ®Google Scholar
• Earl DJ, Deem MW. Evolvability is a selectable trait. Proc Nat Acad Sci USA. 2004;101(32):11531–11536.
   PubMed Web of Science ®Google Scholar
• Schuster P, Swetina J. Stationary mutant distributions and evolutionary optimization. Bull Math Biol. 1988;50(6):635–660.
   PubMed Web of Science ®Google Scholar
• Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature. 2005;439(7074):344–348.
   Web of Science ®Google Scholar
• Arbiza J, Mirazo S, Fort H. Viral quasispecies profiles as the result of the interplay of competition and cooperation. BMCEvolBiol. 2010;10:137.
   Google Scholar
• de Visser JA, Rozen DE. Limits to adaptation in asexual populations. J Evol Biol. 2005;18(4):779–788.
   Web of Science ®Google Scholar
• Jain K, Krug J. Deterministic and stochastic regimes of asexual evolution on rugged fitness landscapes. Genetics. 2007;175(3):1275–1288.
   Web of Science ®Google Scholar
• Saakian DB, Biebricher CK, Hu CK. Phase diagram for the Eigen quasispecies theory with a truncated fitness landscape. Phys Rev E Stat Nonlin Soft Matter Phys. 2009;79(4 Pt 1):041905.
   Web of Science ®Google Scholar
• Crotty S, Cameron CE, Andino R. RNA virus error catastrophe: direct molecular test by using ribavirin. Proc Nat Acad Sci U S A. 2001 ;98(12): 6895–6900.
   Google Scholar
• Biebricher CK, Eigen M. The error threshold. Virus Res. 2005;107(2):117–127.
   PubMed Web of Science ®Google Scholar
• Orr HA. The rate of adaptation in asexuals. Genetics. 2000;155(2):961–968.
   Web of Science ®Google Scholar
• Stich M, Briones C, Manrubia SC. Collective properties of evolving molecular quasispecies. BMC Evol Biol. 2007;7:110.
   Web of Science ®Google Scholar
• Johnson T, Barton NH. The effect of deleterious alleles on adaptation in asexual populations. Genetics. 2002;162(1):395–411.
   Web of Science ®Google Scholar
• Arjan JA, de Visser M, Zeyl CW, Gerrish PJ, Blanchard JL, Lenski RE. Diminishing returns from mutation supply rate in asexual populations. Science. 1999;283(5400):404–406.
   Web of Science ®Google Scholar
• Elena SF, Lenski RE. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet. 2003;4(6):457–469.
   PubMed Web of Science ®Google Scholar
• Clune J, Misevic D, Ofria C, Lenski RE, Elena SF, Sanjuán R. Natural selection fails to optimize mutation rates for long-term adaptation on rugged fitness landscapes. PLoS Comput Biol. 2008;4(9):e1000187.
   Web of Science ®Google Scholar
• Springman R, Keller T, Molineux IJ, Bull JJ. Evolution at a high imposed mutation rate: adaptation obscures the load in phage T7. Genetics. 2010;184(1):221–232.
   Web of Science ®Google Scholar
• Foster PL. Adaptive mutation: implications for evolution. Bioessays. 2000;22(12):1067–1074.
   Web of Science ®Google Scholar
• Cases-González C, Arribas M, Domingo E, Lázaro E. Beneficial effects of population bottlenecks in an RNA virus evolving at increased error rate. J Mol Biol. 2008;384(5):1120–1129.
   PubMed Web of Science ®Google Scholar
• Wainberg MA, Drosopoulos WC, Salomon H, et al. Enhanced fidelity of 3TC-selected mutant HIV-1 reverse transcriptase. Science. 1996;271(5253):1282–1285.
   Web of Science ®Google Scholar
• Metzgar D, Wills C. Evidence for the adaptive evolution of mutation rates. Cell. 2000;101(6):581–584.
   Web of Science ®Google Scholar
• Drake JW, Charlesworth B, Charlesworth D, Crow JF. Rates of spontaneous mutation. Genetics. 1998;148(4):1667–1686.
   PubMed Web of Science ®Google Scholar
• 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):5760–5764.
   PubMed Web of Science ®Google Scholar
• Drake JW, Holland JJ. Mutation rates among RNA viruses. Proc Nat Acad Sci USA. 1999;96(24):13910–13913.
   PubMed Web of Science ®Google Scholar
• Vignuzzi M, Stone JK, Andino R. Ribavirin and lethal mutagenesis of poliovirus: molecular mechanisms, resistance and biological implications. Virus Res. 2005;107(2):173–181.
   PubMed Web of Science ®Google Scholar
• Airaksinen A, Pariente N, Menendez-Arias L, Domingo E. Curing of foot-and-mouth disease virus from persistently infected cells by ribavirin involves enhanced mutagenesis. Virology. 2003;311(2):339–349.
   PubMed Web of Science ®Google Scholar
• Pfeiffer JK, Kirkegaard K. Ribavirin resistance in hepatitis C virus replicon-containing cell lines conferred by changes in the cell line or mutations in the replicon RNA. J Virol. 2005;79(4):2346–2355.
   Web of Science ®Google Scholar
• Young KC, Lindsay KL, Lee KJ, et al. Identification of a ribavirin- resistant NS5B mutation of hepatitis C virus during ribavirin monotherapy. Hepatology. 2003;38(4):869–878.
   Web of Science ®Google Scholar
• Arnold JJ, Vignuzzi M, Stone JK, Andino R, Cameron CE. Remote site control of an active site fidelity checkpoint in a viral RNA-dependent RNA polymerase. J Biol Chem. 2005;280(27):25706–25716.
   PubMed Web of Science ®Google Scholar
• Sallie R. Replicative homeostasis III: implications for antiviral therapy and mechanisms of response and non-response. Virol J. 2007;4:29.
   PubMed Web of Science ®Google Scholar
• Sallie R. Replicative homeostasis: a fundamental mechanism mediating selective viral replication and escape mutation. Virol J. 2005;2:10.
   Web of Science ®Google Scholar
• Sallie R. Replicative homeostasis II: influence of polymerase fidelity on RNA virus quasispecies biology: implications for immune recognition, viral autoimmunity and other “virus receptor” diseases. Virol J. 2005;2:70.
   Web of Science ®Google Scholar
• Hopfield JJ. Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proc Nat Acad Sci U S A. 1974;71(10):4135–4139.
   Web of Science ®Google Scholar
• Simon B. A stochastic model of evolutionary dynamics with deterministic large-population asymptotics. J Theor Biol. 2008;254(4):719–730.
   Web of Science ®Google Scholar
• Bukh J, Pietschmann T, Lohmann V et al. Mutations that permit efficient replication of hepatitis C virus RNA in Huh-7 cells prevent productive replication in chimpanzees. Proc Nat Acad Sci U S A. 2002;99(22):14416–14421.
   PubMed Web of Science ®Google Scholar
• Mueller LD, Ayala FJ. Trade-off between r-selection and K-selection in Drosophila populations. Proc Nat Acad Sci U S A. 1981 ;78(2): 1303–1305.
   Google Scholar
• Giraud A, Matic I, Tenaillon O, et al. Costs and benefits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Science. 2001;291(5513):2606–2608.
   PubMed Web of Science ®Google Scholar
• Sevilla N, Ruiz-Jarabo CM, Gomez-Mariano G, Baranowski E, Domingo E. An RNA virus can adapt to the multiplicity of infection. J Gen Virol. 1998;79(Pt 12):2971–2980.
   Google Scholar
• Rosenberg SM, Thulin C, Harris RS. Transient and heritable mutators in adaptive evolution in the lab and in nature. Genetics. 1998;148(4):1559–1566.
   Web of Science ®Google Scholar
• Alter HJ, Conry-Cantilena C, Melpolder J, et al. Hepatitis C in asymptomatic blood donors. Hepatology. 1997;26(3 Suppl 1):29S-33S.
   Web of Science ®Google Scholar
• Alter HJ, Seeff LB. Recovery, persistence, and sequelae in hepatitis C virus infection: a perspective on long-term outcome. Semin Liver Dis. 2000;20(1):17–35.
   Web of Science ®Google Scholar
• Sanjuan R. Mutational fitness effects in RNA and single-stranded DNA viruses: common patterns revealed by site-directed mutagenesis studies. Philos Trans R Soc Lond B Biol Sci. 2010;365(1548):1975–1982.
   Web of Science ®Google Scholar