A Multi-Step Process of Viral Adaptation to a Mutagenic Nucleoside Analogue by Modulation of Transition Types Leads to Extinction-Escape

1. DomingoE

2006 Quasispecies: Concepts and Implications for Virology. In Curr Top Microbiol Immunol Vol, 299

2. ScheidelLM

DurbinRK

StollarV

1987 Sindbis virus mutants resistant to mycophenolic acid and ribavirin. Virology 158 1 7

3. RichmanDD

1996 Antiviral Drug Resistance New York John Wiley and Sons Inc

4. DomingoE

1989 RNA virus evolution and the control of viral disease. Prog Drug Res 33 93 133

5. DomingoE

2003 Quasispecies and the development of new antiviral strategies. Progress in Drug Res 60 133 158

6. DomingoE

ParrishC

HollandJJE

2008 Origin and Evolution of Viruses. 2nd edition Oxford Elsevier

7. MasA

López-GalíndezC

CachoI

GómezJ

MartinezMA

2010 Unfinished stories on viral quasispecies and Darwinian views of evolution. J Mol Biol 397 865 877

8. SwetinaJ

SchusterP

1982 Self-replication with errors. A model for polynucleotide replication. Biophys Chem 16 329 345

9. EigenM

2002 Error catastrophe and antiviral strategy. Proc Natl Acad Sci USA 99 13374 13376

10. BiebricherCK

EigenM

2005 The error threshold. Virus Res 107 117 127

11. EigenM

BiebricherCK

1988 Sequence space and quasispecies distribution.

DomingoE

AhlquistP

HollandJJ

RNA Genetics Boca Raton, FL CRC Press 211 245

12. SchusterP

StadlerPF

2008 Early Replicons: Origin and Evolution. Origin and Evolution of Viruses 2nd edition.

DomingoE

ParrishCR

HollandJJ

Oxford Elsevier 1 42

13. OchoaG

2006 Error thresholds in genetic algorithms. Evol Comput 14 157 182

14. HarrisKS

BrabantW

StyrchakS

GallA

DaifukuR

2005 KP-1212/1461, a nucleoside designed for the treatment of HIV by viral mutagenesis. Antiviral Res 67 1 9

15. AndersonJP

DaifukuR

LoebLA

2004 Viral error catastrophe by mutagenic nucleosides. Annu Rev Microbiol 58 183 205

16. DomingoE

ParienteN

AiraksinenA

Gonzalez-LopezC

SierraS

2005 Foot-and-mouth disease virus evolution: exploring pathways towards virus extinction. Curr Top Microbiol Immunol 288 149 173

17. GraciJD

CameronCE

2002 Quasispecies, error catastrophe, and the antiviral activity of ribavirin. Virology 298 175 180

18. HarkiDA

GraciJD

EdathilJP

CastroC

CameronCE

2007 Synthesis of a universal 5-nitroindole ribonucleotide and incorporation into RNA by a viral RNA-dependent RNA polymerase. Chembiochem 8 1359 1362

19. GraciJD

TooK

SmidanskyED

EdathilJP

BarrEW

2008 Lethal mutagenesis of picornaviruses with N-6-modified purine nucleoside analogues. Antimicrob Agents Chemother 52 971 979

20. Ruiz-JaraboCM

LyC

DomingoE

de la TorreJC

2003 Lethal mutagenesis of the prototypic arenavirus lymphocytic choriomeningitis virus (LCMV). Virology 308 37 47

21. CrottyS

CameronCE

AndinoR

2001 RNA virus error catastrophe: direct molecular test by using ribavirin. Proc Natl Acad Sci USA 98 6895 6900

22. HollandJJ

DomingoE

de la TorreJC

SteinhauerDA

1990 Mutation frequencies at defined single codon sites in vesicular stomatitis virus and poliovirus can be increased only slightly by chemical mutagenesis. J Virol 64 3960 3962

23. HofmannWP

PoltaA

HerrmannE

MihmU

KronenbergerB

2007 Mutagenic effect of ribavirin on hepatitis C nonstructural 5B quasispecies in vitro and during antiviral therapy. Gastroenterology 132 921 930

24. LoebLA

EssigmannJM

KazaziF

ZhangJ

RoseKD

1999 Lethal mutagenesis of HIV with mutagenic nucleoside analogs. Proc Natl Acad Sci USA 96 1492 1497

25. LoebLA

MullinsJI

2000 Lethal mutagenesis of HIV by mutagenic ribonucleoside analogs. AIDS Res Hum Retroviruses 13 1 3

26. TapiaN

FernandezG

PareraM

Gomez-MarianoG

ClotetB

2005 Combination of a mutagenic agent with a reverse transcriptase inhibitor results in systematic inhibition of HIV-1 infection. Virology 338 1 8

27. SierraM

AiraksinenA

González-LópezC

AgudoR

AriasA

2007 Foot-and-mouth disease virus mutant with decreased sensitivity to ribavirin: implications for error catastrophe. J Virol 81 2012 2024

28. VignuzziM

StoneJK

AndinoR

2005 Ribavirin and lethal mutagenesis of poliovirus: molecular mechanisms, resistance and biological implications. Virus Res 107 173 181

29. VignuzziM

StoneJK

ArnoldJJ

CameronCE

AndinoR

2006 Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439 344 348

30. PfeifferJK

KirkegaardK

2003 A single mutation in poliovirus RNA-dependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity. Proc Natl Acad Sci USA 100 7289 7294

31. PfeifferJK

KirkegaardK

2005 Increased fidelity reduces poliovirus fitness under selective pressure in mice. PLoS Pathogens 1 102 110

32. DavisGL

Esteban-MurR

RustgiV

HoefsJ

GordonSC

1998 Interferon alfa-2b alone or in combination with ribavirin for the treatment of relapse of chronic hepatitis C. International Hepatitis Interventional Therapy Group. N Engl J Med 339 1493 1499

33. McHutchisonJG

GordonSC

SchiffER

ShiffmanML

LeeWM

1998 Interferon alfa-2b alone or in combination with ribavirin as initial treatment for chronic hepatitis C. Hepatitis Interventional Therapy Group. N Engl J Med 339 1485 1492

34. CummingsKJ

LeeSM

WestES

Cid-RuzafaJ

FeinSG

2001 Interferon and ribavirin vs interferon alone in the re-treatment of chronic hepatitis C previously nonresponsive to interferon: A meta-analysis of randomized trials. Jama 285 193 199

35. Di BisceglieAM

ThompsonJ

Smith-WilkaitisN

BruntEM

BaconBR

2001 Combination of interferon and ribavirin in chronic hepatitis C: re-treatment of nonresponders to interferon. Hepatology 33 704 707

36. CrottyS

MaagD

ArnoldJJ

ZhongW

LauJYN

2000 The broad-spectrum antiviral ribonucleotide, ribavirin, is an RNA virus mutagen. Nature Medicine 6 1375 1379

37. DayCW

SmeeDF

JulanderJG

YamshchikovVF

SidwellRW

2005 Error-prone replication of West Nile virus caused by ribavirin. Antiviral Res 67 38 45

38. SeversonWE

SchmaljohnCS

JavadianA

JonssonCB

2003 Ribavirin causes error catastrophe during Hantaan virus replication. J Virol 77 481 488

39. MaagD

CastroC

HongZ

CameronCE

2001 Hepatitis C virus RNA-dependent RNA polymerase (NS5B) as a mediator of the antiviral activity of ribavirin. J Biol Chem 276 46094 46098

40. LanfordRE

ChavezD

GuerraB

LauJY

HongZ

2001 Ribavirin induces error-prone replication of GB virus B in primary tamarin hepatocytes. J Virol 75 8074 8081

41. FreistadtMS

MeadesGD

CameronCE

2004 Lethal mutagens: broad-spectrum antivirals with limited potential for development of resistance? Drug Resist Updat 7 19 24

42. AiraksinenA

ParienteN

Menendez-AriasL

DomingoE

2003 Curing of foot-and-mouth disease virus from persistently infected cells by ribavirin involves enhanced mutagenesis. Virology 311 339 349

43. ParkerWB

2005 Metabolism and antiviral activity of ribavirin. Virus Res 107 165 171

44. GraciJD

CameronCE

2006 Mechanisms of action of ribavirin against distinct viruses. Rev Med Virol 16 37 48

45. AsahinaY

IzumiN

EnomotoN

UchiharaM

KurosakiM

2005 Mutagenic effects of ribavirin and response to interferon/ribavirin combination therapy in chronic hepatitis C. J Hepatol 43 623 629

46. ChevaliezS

BrilletR

LazaroE

HezodeC

PawlotskyJM

2007 Analysis of ribavirin mutagenicity in human hepatitis C virus infection. J Virol 81 7732 7741

47. PerelsonAS

LaydenTJ

2007 Ribavirin: is it a mutagen for hepatitis C virus? Gastroenterology 132 2050 2052

48. HongZ

2003 The role of ribavirin-induced mutagenesis in HCV therapy: a concept or a fact? Hepatology 38 807 810

49. CuevasJM

Gonzalez-CandelasF

MoyaA

SanjuanR

2009 Effect of ribavirin on the mutation rate and spectrum of hepatitis C virus in vivo. J Virol 83 5760 5764

50. AriasA

ArnoldJJ

SierraM

SmidanskyED

DomingoE

2008 Determinants of RNA-dependent RNA polymerase (in)fidelity revealed by kinetic analysis of the polymerase encoded by a foot-and-mouth disease virus mutant with reduced sensitivity to ribavirin. J Virol 82 12346 12355

51. Ferrer-OrtaC

SierraM

AgudoR

de la HigueraI

AriasA

2010 Structure of foot-and-mouth disease virus mutant polymerases with reduced sensitivity to ribavirin. J Virol 84 6188 6199

52. PeralesC

AgudoR

DomingoE

2009 Counteracting quasispecies adaptability: extinction of a ribavirin-resistant virus mutant by an alternative mutagenic treatment. PLoS ONE 4 e5554

53. PeralesC

AgudoR

TejeroH

ManrubiaSC

DomingoE

2009 Potential benefits of sequential inhibitor-mutagen treatments of RNA virus infections. PLoS Pathog 5 e1000658

54. SobrinoF

DávilaM

OrtínJ

DomingoE

1983 Multiple genetic variants arise in the course of replication of foot-and-mouth disease virus in cell culture. Virology 128 310 318

55. CharpentierN

DavilaM

DomingoE

EscarmisC

1996 Long-term, large-population passage of aphthovirus can generate and amplify defective noninterfering particles deleted in the leader protease gene. Virology 223 10 18

56. SierraM

2007 Bases moleculares de la resistencia a ribavirina en el virus de la fiebre aftosa. Implicaciones para la mutagénesis letal de virus. [Ph. D. Thesis]. Madrid (Spain): Universidad Autónoma de Madrid

57. TojaM

EscarmisC

DomingoE

1999 Genomic nucleotide sequence of a foot-and-mouth disease virus clone and its persistent derivatives. Implications for the evolution of viral quasispecies during a persistent infection. Virus Res 64 161 171

58. SierraS

DávilaM

LowensteinPR

DomingoE

2000 Response of foot-and-mouth disease virus to increased mutagenesis. Influence of viral load and fitness in loss of infectivity. J Virol 74 8316 8323

59. ParienteN

SierraS

LowensteinPR

DomingoE

2001 Efficient virus extinction by combinations of a mutagen and antiviral inhibitors. J Virol 75 9723 9730

60. OjosnegrosS

AgudoR

SierraM

BrionesC

SierraS

2008 Topology of evolving, mutagenized viral populations: quasispecies expansion, compression, and operation of negative selection. BMC Evol Biol 8 207

61. SnellNJ

2001 Ribavirin–current status of a broad spectrum antiviral agent. Expert Opin Pharmacother 2 1317 1324

62. ArnoldJJ

CameronCE

2000 Poliovirus RNA-dependent RNA polymerase (3Dpol). Assembly of stable, elongation-competent complexes by using a symmetrical primer-template substrate (sym/sub). J Biol Chem 275 5329 5336

63. Ferrer-OrtaC

AriasA

Perez-LuqueR

EscarmisC

DomingoE

2004 Structure of foot-and-mouth disease virus RNA-dependent RNA polymerase and its complex with a template-primer RNA. J Biol Chem 279 47212 47221

64. Ferrer-OrtaC

AgudoR

DomingoE

VerdaguerN

2009 Structural insights into replication initiation and elongation processes by the FMDV RNA-dependent RNA polymerase. Current Opinion in Structural Biology 19 752 758

65. Ferrer-OrtaC

AriasA

Perez-LuqueR

EscarmisC

DomingoE

2007 Sequential structures provide insights into the fidelity of RNA replication. Proc Natl Acad Sci U S A 104 9463 9468

66. Ferrer-OrtaC

AgudoR

DomingoE

VerdaguerN

2009 Structural insights into replication initiation and elongation processes by the FMDV RNA-dependent RNA polymerase. Curr Opin Struct Biol 19 752 758

67. AriasA

AgudoR

Ferrer-OrtaC

Perez-LuqueR

AiraksinenA

2005 Mutant viral polymerase in the transition of virus to error catastrophe identifies a critical site for RNA binding. J Mol Biol 353 1021 1032

68. AriasA

Ruiz-JaraboCM

EscarmisC

DomingoE

2004 Fitness increase of memory genomes in a viral quasispecies. J Mol Biol 339 405 412

69. EscarmísC

DávilaM

CharpentierN

BrachoA

MoyaA

1996 Genetic lesions associated with Muller's ratchet in an RNA virus. J Mol Biol 264 255 267

70. García-ArriazaJ

ManrubiaSC

TojaM

DomingoE

EscarmísC

2004 Evolutionary transition toward defective RNAs that are infectious by complementation. J Virol 78 11678 11685

71. PeralesC

MateoR

MateuMG

DomingoE

2007 Insights into RNA virus mutant spectrum and lethal mutagenesis events: replicative interference and complementation by multiple point mutants. J Mol Biol 369 985 1000

72. SmithRA

KirkpatrickW

1980 Ribavirin: a broad spectrum antiviral agent New York Academic Press, Inc

73. SidwellOW

SimonLN

WitkowskiJT

RobinsRK

1974 Antiviral activity of virazole: review and structure-activity relationships. Prog Chemotherapy 2 889 903

74. ConnorE

MorrisonS

LaneJ

OleskeJ

SonkeRL

1993 Safety, tolerance, and pharmacokinetics of systemic ribavirin in children with human immunodeficiency virus infection. Antimicrob Agents Chemother 37 532 539

75. JordanI

BrieseT

FischerN

LauJY

LipkinWI

2000 Ribavirin inhibits West Nile virus replication and cytopathic effect in neural cells. J Infect Dis 182 1214 1217

76. OgleJW

ToltzisP

ParkerWD

AlvarezN

McIntoshK

1989 Oral ribavirin therapy for subacute sclerosing panencephalitis. J Infect Dis 159 748 750

77. AndersonJF

RahalJJ

2002 Efficacy of interferon alpha-2b and ribavirin against West Nile virus in vitro. Emerg Infect Dis 8 107 108

78. CrumpackerC

BubleyG

LuceyD

HusseyS

ConnorJ

1986 Ribavirin enters cerebrospinal fluid. Lancet 2 45 46

79. EscarmísC

PeralesC

DomingoE

2009 Biological effect of Muller's Ratchet: distant capsid site can affect picornavirus protein processing. J Virol 83 6748 6756

80. ColemanJR

PapamichailD

SkienaS

FutcherB

WimmerE

2008 Virus attenuation by genome-scale changes in codon pair bias. Science 320 1784 1787

81. AragonesL

BoschA

PintoRM

2008 Hepatitis A virus mutant spectra under the selective pressure of monoclonal antibodies: codon usage constraints limit capsid variability. J Virol 82 1688 1700

82. FrankAC

LobryJR

1999 Asymmetric substitution patterns: a review of possible underlying mutational or selective mechanisms. Gene 238 65 77

83. GaltierN

LobryJR

1997 Relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature in prokaryotes. J Mol Evol 44 632 636

84. WangHC

HickeyDA

2002 Evidence for strong selective constraint acting on the nucleotide composition of 16S ribosomal RNA genes. Nucleic Acids Res 30 2501 2507

85. PintoRM

AragonesL

CostafredaMI

RibesE

BoschA

2007 Codon usage and replicative strategies of hepatitis A virus. Virus Res 127 158 163

86. OjosnegrosS

BeerenwinkelN

AntalT

NowakMA

EscarmísC

2010 Competition-colonization dynamics in an RNA virus. Proc Natl Acad Sci USA 107 2108 2112

87. Sanz-RamosM

Diaz-San SegundoF

EscarmisC

DomingoE

SevillaN

2008 Hidden virulence determinants in a viral quasispecies in vivo. J Virol 82 10465 10476

88. Ferrer-OrtaC

AriasA

EscarmisC

VerdaguerN

2006 A comparison of viral RNA-dependent RNA polymerases. Curr Opin Struct Biol 16 27 34

89. AgudoR

AriasA

ParienteN

PeralesC

EscarmisC

2008 Molecular characterization of a dual inhibitory and mutagenic activity of 5-fluorouridine triphosphate on viral RNA synthesis. Implications for lethal mutagenesis. J Mol Biol 382 652 666

90. OtwinowskiZ

MinorW

1997 Processing X-ray diffraction data collected in oscillation model. Methods Enzymol 276 307 326

91. RousselA

CambillauC

1989 Turbo-Frodo. Silicon Graphics Geometry Partners Directory Mountain View, Ca Silicon Graphics 77 79

92. García-ArriazaJ

OjosnegrosS

DávilaM

DomingoE

EscarmisC

2006 Dynamics of mutation and recombination in a replicating population of complementing, defective viral genomes. J Mol Biol 360 558 572

93. EscarmísC

DávilaM

DomingoE

1999 Multiple molecular pathways for fitness recovery of an RNA virus debilitated by operation of Muller's ratchet. J Mol Biol 285 495 505