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Population dynamics of RNA viruses: the essential contribution of mutant spectra

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Infectious Diseases from Nature: Mechanisms of Viral Emergence and Persistence

Summary

Cells and their viral and cellular parasites are genetically highly diverse, and their genomes contain signs of past and present variation and mobility. The great adaptive potential of viruses, conferred on them by high mutation rates and quasispecies dynamics, demands new strategies for viral disease prevention and control. This necessitates a more detailed knowledge of viral population structure and dynamics. Here we review studies with the important animal pathogen Foot-and-mouth disease virus (FMDV) that document modulating effects of the mutant spectra that compose viral populations. As a consequence of interactions within mutant spectra, enhanced mutagenesis may lead to viral extinction, and this is currently investigated as a new antiviral strategy, termed virus entry into error catastrophe.

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References

  1. Agol VI (2002) Picornavirus genetics: an overview. In: Semler BL, Wimmer E (eds) Molecular biology of picornaviruses. American Society for Microbiology, Washington DC, pp 269–284

    Google Scholar 

  2. Airaksinen A, Pariente N, Menendez-Arias L, Domingo E (2003) Curing of foot-and-mouth disease virus from persistently infected cells by ribavirin involves enhanced mutagenesis. Virology 311: 339–349

    Article  PubMed  CAS  Google Scholar 

  3. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Molecular biology of the cell. Garland Science, New York, NY

    Google Scholar 

  4. Alves D, Fontanari JF (1998) Error threshold in finite populations. Phys Rev E 57: 7008–7013

    Article  CAS  Google Scholar 

  5. Arias A, Lázaro E, Escarmís C, Domingo E (2001) Molecular intermediates of fitness gain of an RNA virus: characterization of a mutant spectrum by biological and molecular cloning. J Gen Virol 82: 1049–1060

    PubMed  CAS  Google Scholar 

  6. Arias A, Ruiz-Jarabo CM, Escarmis C, Domingo E (2004) Fitness increase of memory genomes in a viral quasispecies. J Mol Biol 339: 405–412

    Article  PubMed  CAS  Google Scholar 

  7. Baranowski E, Ruíz-Jarabo CM, Pariente N, Verdaguer N, Domingo E (2003) Evolution of cell recognition by viruses: a source of biological novelty with medical implications. Adv Virus Res 62: 19–111

    Article  PubMed  CAS  Google Scholar 

  8. Batschelet E, Domingo E, Weissmann C (1976) The proportion of revertant and mutant phage in a growing population, as a function of mutation and growth rate. Gene 1: 27–32

    Article  PubMed  CAS  Google Scholar 

  9. Borrego B, Novella IS, Giralt E, Andreu D, Domingo E (1993) Distinct repertoire of antigenic variants of foot-and-mouth disease virus in the presence or absence of immune selection. J Virol 67: 6071–6079

    PubMed  CAS  Google Scholar 

  10. Bushman F (2002) Lateral DNA transfer. Mechanisms and consequences. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  11. Chao L (1990) Fitness of RNA virus decreased by Muller’s ratchet. Nature 348: 454–455

    Article  PubMed  CAS  Google Scholar 

  12. Chumakov KM, Powers LB, Noonan KE, Roninson IB, Levenbook IS (1991) Correlation between amount of virus with altered nucleotide sequence and the monkey test for acceptability of oral poliovirus vaccine. Proc Natl Acad Sci USA 88: 199–203

    Article  PubMed  CAS  Google Scholar 

  13. Coffin JM, Hughes SH, Varmus HE (1997) Retroviruses. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  14. Condit RC (2001) Principles of Virology. In: Knipe DM, Howley PM (eds) Fields virology. Lippincott Williams and Wilkins, Philadelphia, vol 1, pp 19–51

    Google Scholar 

  15. Contreras AM, Hiasa Y, He W, Terella A, Schmidt EV, Chung RT (2002) Viral RNA mutations are region specific and increased by ribavirin in a full-length hepatitis C virus replication system. J Virol 76: 8505–8517

    Article  PubMed  CAS  Google Scholar 

  16. Crotty S, Maag D, Arnold JJ, Zhong W, Lau JYN, Hong Z, Andino R, Cameron CE (2000) The broad-spectrum antiviral ribonucleotide, ribavirin, is an RNA virus mutagen. Nat Med 6: 1375–1379

    Article  PubMed  CAS  Google Scholar 

  17. Crotty S, Cameron CE, Andino R (2001) RNA virus error catastrophe: direct molecular test by using ribavirin. Proc Natl Acad Sci USA 98: 6895–6900

    Article  PubMed  CAS  Google Scholar 

  18. Crotty S, Cameron C, Andino R (2002) Ribavirin’s antiviral mechanism of action: lethal mutagenesis? J Mol Med 80: 86–95

    Article  PubMed  CAS  Google Scholar 

  19. de la Torre JC, Alarcón B, Martínez-Salas E, Carrasco L, Domingo E (1987) Ribavirin cures cells of a persistent infection with foot-and-mouth disease virus in vitro. J Virol 61: 233–235

    PubMed  Google Scholar 

  20. de la Torre JC, Holland JJ (1990) RNA virus quasispecies populations can suppress vastly superior mutant progeny. J Virol 64: 6278–6281

    PubMed  Google Scholar 

  21. de Visser JA (2002) The fate of microbial mutators. Microbiology 148: 1247–1252

    PubMed  Google Scholar 

  22. Domingo E, Sabo D, Taniguchi T, Weissmann C (1978) Nucleotide sequence heterogeneity of an RNA phage population. Cell 13: 735–744

    Article  PubMed  CAS  Google Scholar 

  23. Domingo E (1989) RNA virus evolution and the control of viral disease. Prog Drug Res 33: 93–133

    PubMed  CAS  Google Scholar 

  24. Domingo E, Biebricher C, Eigen M, Holland JJ (2001) Quasispecies and RNA virus evolution: principles and consequences. Landes Bioscience, Austin

    Google Scholar 

  25. Domingo E (2003) Quasispecies and the development of new antiviral strategies. Prog Drug Res 60: 133–158

    PubMed  CAS  Google Scholar 

  26. Domingo E (2005) Virus entry into error catastrophe as a new antiviral strategy. Virus Res 107: 115–228

    Article  CAS  Google Scholar 

  27. Domingo E (2005) Viruses as quasispecies: biological implications. Current Topics in Microbiology and Immunology (in press)

    Google Scholar 

  28. Drake JW, Holland JJ (1999) Mutation rates among RNA viruses. Proc Natl Acad Sci USA 96: 13910–13913

    Article  PubMed  CAS  Google Scholar 

  29. Duarte E, Clarke D, Moya A, Domingo E, Holland J (1992) Rapid fitness losses in mammalian RNA virus clones due to Muller’s ratchet. Proc Natl Acad Sci USA 89: 6015–6019

    Article  PubMed  CAS  Google Scholar 

  30. Eigen M (1971) Self-organization of matter and the evolution of biological macromolecules. Naturwissenschaften 58: 465–523

    Article  PubMed  CAS  Google Scholar 

  31. Eigen M, Schuster P (1979) The hypercycle. A principle of natural self-organization. Springer, Berlin Heidelberg New York Tokyo

    Google Scholar 

  32. Eigen M, Biebricher CK (1988) Sequence space and quasispecies distribution. In: Domingo E, Ahlquist P, Holland JJ (eds) RNA Genetics. CRC Press, Boca Raton, FL, vol 3, pp 211–245

    Google Scholar 

  33. Eigen M (1996) On the nature of virus quasispecies. Trends Microbiol 4: 216–218

    Article  PubMed  CAS  Google Scholar 

  34. Eigen M (2000) Natural selection: a phase transition? Biophys Chem 85: 101–123

    Article  PubMed  CAS  Google Scholar 

  35. Eigen M (2002) Error catastrophe and antiviral strategy. Proc Natl Acad Sci USA 99: 13374–13376

    Article  PubMed  CAS  Google Scholar 

  36. Escarmís C, Dávila M, Charpentier N, Bracho A, Moya A, Domingo E (1996) Genetic lesions associated with Muller’s ratchet in an RNA virus. J Mol Biol 264: 255–267

    Article  PubMed  Google Scholar 

  37. Escarmís C, Dávila M, Domingo E (1999) Multiple molecular pathways for fitness recovery of an RNA virus debilitated by operation of Muller’s ratchet. J Mol Biol 285: 495–505

    Article  PubMed  Google Scholar 

  38. Escarmís C, Gómez-Mariano G, Dávila M, Lázaro E, Domingo E (2002) Resistance to extinction of low fitness virus subjected to plaque-to-plaque transfers: diversification by mutation clustering. J Mol Biol 315: 647–661

    Article  PubMed  CAS  Google Scholar 

  39. Ferrer-Orta C, Arias A, Perez-Luque R, Escarmis C, Domingo E, Verdaguer N (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

    Article  PubMed  CAS  Google Scholar 

  40. Flint SJ, Enquist LW, Racaniello VR, Skalka AM (2004) Principles of virology. Molecular biology, pathogenesis, and control of animal viruses, 2nd edn. ASM Press, Washington, DC

    Google Scholar 

  41. García-Arriaza J, Domingo E, Escarmís C (2005) A segmented form of foot-and-mouth disease virus interferes with standard virus: a link between interference and competitive fitness. Virology 335: 155–164

    Article  PubMed  CAS  Google Scholar 

  42. Giraud A, Matic I, Radman M, Fons M, Taddei F (2002) Mutator bacteria as a risk factor in treatment of infectious diseases. Antimicrob Agents Chemother 46: 863–865

    Article  PubMed  CAS  Google Scholar 

  43. González-López C, Arias A, Pariente N, Gómez-Mariano G, Domingo E (2004) Preextinction viral RNA can interfere with infectivity. J Virol 78: 3319–3324

    Article  PubMed  CAS  Google Scholar 

  44. González-López C, Gómez-Mariano G, Escarmís C, Domingo E (2005) Invariant aphthovirus consensus nucleotide sequence in the transition to error catastrophe. Infection, Geneticas and Evolution (in press)

    Google Scholar 

  45. Graci JD, Cameron CE (2002) Quasispecies, error catastrophe, and the antiviral activity of ribavirin. Virology 298: 175–180

    Article  PubMed  CAS  Google Scholar 

  46. Grande-Pérez A, Sierra S, Castro MG, Domingo E, Lowenstein PR (2002) Molecular indetermination in the transition to error catastrophe: systematic elimination of lymphocytic choriomeningitis virus through mutagenesis does not correlate linearly with large increases in mutant spectrum complexity. Proc Natl Acad Sci USA 99: 12938–12943

    Article  PubMed  CAS  Google Scholar 

  47. Holland JJ, Domingo E, de la Torre JC, Steinhauer DA (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

    PubMed  CAS  Google Scholar 

  48. Lanford RE, Chavez D, Guerra B, Lau JY, Hong Z, Brasky KM, Beames B (2001) Ribavirin induces error-prone replication of GB virus B in primary tamarin hepatocytes. J Virol 75: 8074–8081

    Article  PubMed  CAS  Google Scholar 

  49. Lazaro E, Escarmis C, Perez-Mercader J, Manrubia SC, Domingo E (2003) Resistance of virus to extinction on bottleneck passages: study of a decaying and fluctuating pattern of fitness loss. Proc Natl Acad Sci USA 100: 10830–10835

    Article  PubMed  CAS  Google Scholar 

  50. Lázaro E, Escarmís C, Domingo E, Manrubia SC (2002) Modeling viral genome fitness evolution associated with serial bottleneck events: evidence of stationary states of fitness. J Virol 76: 8675–8681

    Article  PubMed  CAS  Google Scholar 

  51. Loeb LA, Essigmann JM, Kazazi F, Zhang J, Rose KD, Mullins JI (1999) Lethal mutagenesis of HIV with mutagenic nucleoside analogs. Proc Natl Acad Sci USA 96: 1492–1497

    Article  PubMed  CAS  Google Scholar 

  52. Loeb LA, Mullins JI (2000) Lethal mutagenesis of HIV by mutagenic ribonucleoside analogs. AIDS Res Hum Retroviruses 13: 1–3

    Article  Google Scholar 

  53. Maag D, Castro C, Hong Z, Cameron CE (2001) Hepatitis C virus RNA-dependent RNA polymerase (NS5B) as a mediator of the antiviral activity of ribavirin. J Biol Chem 276: 46094–46098

    Article  PubMed  CAS  Google Scholar 

  54. McClure MA (1999) The retroid agents: disease, function and evolution. In: Domingo E, Webster RG, Holland JJ (eds) Origin and evolution of viruses. Academic Press, San Diego, pp 163–195

    Google Scholar 

  55. Menéndez-Arias L (2002) Targeting HIV: antiretroviral therapy and development of drug resistance. Trends Pharmacol Sci 23: 381–388

    Article  PubMed  Google Scholar 

  56. Mount DW(2004) Bioinformatics. Sequence and genome analysis. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  57. Muller HJ (1964) The relation of recombination to mutational advance. Mut Res 1: 2–9

    Google Scholar 

  58. Nowak M, Schuster P (1989) Error thresholds of replication in finite populations mutation frequencies and the onset of Muller’s ratchet. J Theor Biol 137: 375–395

    PubMed  CAS  Google Scholar 

  59. Page KM, Nowak MA (2002) Unifying evolutionary dynamics. J Theor Biol 219: 93–98

    PubMed  Google Scholar 

  60. Pariente N, Sierra S, Lowenstein PR, Domingo E (2001) Efficient virus extinction by combinations of a mutagen and antiviral inhibitors. J Virol 75: 9723–9730

    Article  PubMed  CAS  Google Scholar 

  61. Pariente N, Airaksinen A, Domingo E (2003) Mutagenesis versus inhibition in the efficiency of extinction of foot-and-mouth disease virus. J Virol 77: 7131–7138

    Article  PubMed  CAS  Google Scholar 

  62. Pfeiffer JK, Kirkegaard K (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

    Article  PubMed  CAS  Google Scholar 

  63. Richman DD (1996) Antiviral drug resistance. JohnWiley and Sons Inc., New York

    Google Scholar 

  64. Rowlands DJ (ed) (2003) Foot-and-mouth disease. Virus Res 91: 1–161

    Google Scholar 

  65. Ruiz-Jarabo CM, Ly C, Domingo E, de la Torre JC (2003) Lethal mutagenesis of the prototypic arenavirus lymphocytic choriomeningitis virus (LCMV). Virology 308: 37–47

    Article  PubMed  CAS  Google Scholar 

  66. Severson WE, Schmaljohn CS, Javadian A, Jonsson CB (2003) Ribavirin causes error catastrophe during Hantaan virus replication. J Virol 77: 481–488

    Article  PubMed  CAS  Google Scholar 

  67. Sierra S, Dávila M, Lowenstein PR, Domingo E (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

    Article  PubMed  CAS  Google Scholar 

  68. Sierra S (2001) Caracterización de la respuesta del virus de la fiebre aftosa a mutagénesis química. Universidad Autónoma de Madrid, Madrid, Spain

    Google Scholar 

  69. Snell NJ (2001) Ribavirin-current status of a broad spectrum antiviral agent. Expert Opin Pharmacother 2: 1317–1324

    Article  PubMed  CAS  Google Scholar 

  70. Sobrino F, Domingo E (2004) Foot-and-mouth disease: current perspectives. Horizon Bioscience, Wymondham, England

    Google Scholar 

  71. Streeter DG, Witkowski JT, Khare GP, Sidwell RW, Bauer RJ, Robins RK, Simon LN (1973) Mechanism of action of 1-D-ribofuranosyl-1,2,4-triazole-3-carboxamide (Virazole), a new broad-spectrum antiviral agent. Proc Natl Acad Sci USA 70:1174–1178

    Article  PubMed  CAS  Google Scholar 

  72. Sun C, Skaletsky H, Rozen S, Gromoll J, Nieschlag E, Oates R, Page DC (2000) Deletion of azoospermia factor a (AZFa) region of human Y chromosome caused by recombination between HERV15 proviruses. Hum Mol Genet 9: 2291–2296

    Article  PubMed  CAS  Google Scholar 

  73. Swetina J, Schuster P (1982) Self-replication with errors. A model for polynucleotide replication. Biophys Chem 16: 329–345

    Article  PubMed  CAS  Google Scholar 

  74. Teng MN, Oldstone MB, de la Torre JC (1996) Suppression of lymphocytic choriomeningitis virus-induced growth hormone deficiency syndrome by diseasenegative virus variants. Virology 223: 113–119

    Article  PubMed  CAS  Google Scholar 

  75. Vo NV, Young KC, Lai MMC (2003) Mutagenic and inhibitory effects of ribavirin on hepatitis C virus RNA polymerase. Biochemistry 42: 10462–10471

    Article  PubMed  CAS  Google Scholar 

  76. Wilke CO, Ronnewinkel C, Martinetz T (2001) Dynamic fitness landscapes in molecular evolution. Phys Rep 349: 395–446

    Article  CAS  Google Scholar 

  77. Young KC, Lindsay KL, Lee KJ, Liu WC, He JW, Milstein SL, Lai MM (2003) Identification of a ribavirin-resistant NS5B mutation of hepatitis C virus during ribavirin monotherapy. Hepatology 38: 869–878

    Article  PubMed  CAS  Google Scholar 

  78. Youngner JS, Whitaker-Dowling P (1999) Interference. In: Granoff A, Webster RG (eds) Encyclopedia of virology. Academic Press, San Diego, California, vol 2, pp 850–854

    Google Scholar 

  79. Yuste E, Sánchez-Palomino S, Casado C, Domingo E, López-Galíndez C (1999) Drastic fitness loss in human immunodeficiency virus type 1 upon serial bottleneck events. J Virol 73: 2745–2751

    PubMed  CAS  Google Scholar 

  80. Yuste E, López-Galíndez C, Domingo E (2000) Unusual distribution of mutations associated with serial bottleneck passages of human immunodeficiency virus type 1. J Virol 74: 9546–9552

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Centro de Biología Molecular “Severo Ochoa” (CSIC-UAM), Universidad Autónoma de Madrid, Cantoblanco, Madrid, 28049, Spain

    E. Domingo, C. Gonzalez-Lopez, N. Pariente, A. Airaksinen & C. Escarmís

  2. Centro de Investigación en Sanidad Animal (CISA-INIA), Universidad Autónoma de Madrid, Cantoblanco, Madrid, Spain

    E. Domingo

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  1. E. Domingo
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  2. C. Gonzalez-Lopez
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  3. N. Pariente
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  4. A. Airaksinen
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  5. C. Escarmís
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Editors and Affiliations

  1. Department of Pathology, WHO Collaborating Center for Tropical Diseases, University of Texas, Galveston, USA

    C. J. Peters

  2. Arthropod-borne and Infectious Diseases Laboratory, Department of Microbiology, Immunology and Pathology, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, USA

    Charles H. Calisher

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Domingo, E., Gonzalez-Lopez, C., Pariente, N., Airaksinen, A., Escarmís, C. (2005). Population dynamics of RNA viruses: the essential contribution of mutant spectra. In: Peters, C.J., Calisher, C.H. (eds) Infectious Diseases from Nature: Mechanisms of Viral Emergence and Persistence. Springer, Vienna. https://doi.org/10.1007/3-211-29981-5_6

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