From quasispecies theory to viral quasispecies: How complexity has permeated virology

Mathematical Modelling of Natural Phenomena

Volumn 7, Issue 5, 2012, Pages 105-122

  Domingo, E ^a,b,c   Perales, C ^a,c  

^a CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^b INSTITUTO NACIONAL DE TÉCNICA AEROESPACIAL   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Lethal mutagenesis; Mutation rate; RNA viruses; Viral fitness; Viral quasispecies

Indexed keywords

ERROR PRONES; FERTILE FIELDS; MUTANT DISTRIBUTION; MUTATION RATES; QUASISPECIES; QUASISPECIES THEORY; RNA VIRUS; VIRAL FITNESS;

RNA;

VIRUSES;

EID: 84867696469     PISSN: 09735348     EISSN: 17606101     Source Type: Journal    
DOI: 10.1051/mmnp/20127508     Document Type: Review

References (100)

1. V.I. Agol. Picornaviruses as a model for studying the nature of RNA recombination. In: The Picornaviruses. E. Ehrenfeld, E. Domingo and R.P. Roos, eds, ASM Press, Washington DC. pp. 239-252, 2010.
2. A. Airaksinen, N. Pariente, L. Menendez-Arias, E. Domingo. Curing of foot-and-mouth disease virus from persistently infected cells by ribavirin involves enhanced mutagenesis. Virology, 311 (2003), 339-349. (Pubitemid 36808775)
3. R. Antia, R.R. Regoes, J.C. Koella, C.T. Bergstrom. The role of evolution in the emergence of infectious diseases. Nature, 426 (2003), 658-661. (Pubitemid 38009372)
4. A. Arias, R. Agudo, C. Ferrer-Orta, R. Perez-Luque, A. Airaksinen, E. Brocchi, E. Domingo, N. Verdaguer, C. Escarmis. Mutant viral polymerase in the transition of virus to error catastrophe identifies a critical site for RNA binding. J. Mol. Biol., 353 (2005), 1021-1032. (Pubitemid 41503270)
5. E. Batschelet, E. Domingo, C. Weissmann. The proportion of revertant and mutant phage in a growing population, as a function of mutation and growth rate. Gene, 1 (1976), 27-32.
6. A. Bernad, L. Blanco, J.M. Lazaro, G. Martin, M. Salas. A conserved 3' 5' exonuclease active site in prokaryotic and eukaryotic DNA polymerases. Cell, 59 (1989), 219-228. (Pubitemid 19248571)
7. C.K. Biebricher, M. Eigen. The error threshold. Virus Res., 107 (2005), 117-127. (Pubitemid 40093085)
8. B. Borrego, I.S. Novella, E. Giralt, D. Andreu, E. Domingo. Distinct repertoire of antigenic variants of foot-and-mouth disease virus in the presence or absence of immune selection. J. Virol., 67 (1993), 6071-6079. (Pubitemid 23277518)
9. M.J. Buzon, T. Wrin, F.M. Codoner, J. Dalmau, P. Phung, A. Bonjoch, E. Coakley, B. Clotet, J. Martinez-Picado. Combined antiretroviral therapy and immune pressure lead to in vivo HIV-1 recombination with ancestral viral genomes. Journal of acquired immune deficiency syndromes (1999), 57 (2011), 109-117.
10. M. Clementi. Perspectives and opportunities for novel antiviral treatments targeting virus fitness. Clin Microbiol Infect, 14 (2008), 629-631. (Pubitemid 351837022)
11. L.L. Coffey, Y. Beeharry, A.V. Borderia, H. Blanc, M. Vignuzzi. Arbovirus high fidelity variant loses fitness in mosquitoes and mice. Proc Natl Acad Sci U S A, 108 (2011), 16038-16043.
12. S. Crowder, K. Kirkegaard. Trans-dominant inhibition of RNA viral replication can slow growth of drug-resistant viruses. Nature Genetics, 37 (2005), 701-709. (Pubitemid 41754886)
13. K.M. Chumakov, L.B. Powers, K.E. Noonan, I.B. Roninson, I.S. Levenbook. 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 (1991), 199-203. (Pubitemid 21914454)
14. J.C. de la Torre, J.J. Holland. RNA virus quasispecies populations can suppress vastly superior mutant progeny. J. Virol., 64 (1990), 6278-6281.
15. M.R. Denison, R.L. Graham, E.F. Donaldson, L.D. Eckerle, R.S. Baric. Coronaviruses: an RNA proofreading machine regulates replication fidelity and diversity. RNA biology, 8 (2011), 270-279.
16. E. Domingo. Mechanisms of viral emergence. Vet Res, 41 (2010), 38.
17. E. Domingo, C. Biebricher, M. Eigen, J.J. Holland. Quasispecies and RNA Virus Evolution: Principles and Consequences. Landes Bioscience, Austin, 2001.
18. E. Domingo, M. Davila, J. Ortin. Nucleotide sequence heterogeneity of the RNA from a natural population of foot-and-mouth-disease virus. Gene, 11 (1980), 333-346. (Pubitemid 11215356)
19. E. Domingo, R.A. Flavell, C. Weissmann. In vitro site-directed mutagenesis: generation and properties of an infectious extracistronic mutant of bacteriophage Q. Gene, 1 (1976), 3-25.
20. E. Domingo, J.J. Holland, P. Ahlquist. RNA Genetics, CRC Press, Boca Raton, 1988.
21. E. Domingo, D. Sabo, T. Taniguchi, C. Weissmann. Nucleotide sequence heterogeneity of an RNA phage population. Cell, 13 (1978), 735-744. (Pubitemid 8312229)
22. E. Domingo, J. Sheldon, C. Perales. Viral quasispecies evolution. Microbiology and Molecular Biology Reviews, 76 (2012), 159-216.
23. E. Domingo, S. Wain-Hobson. The 30th anniversary of quasispecies. Meeting on 'Quasispecies: past, present and future'. EMBO Rep, 10 (2009), 444-448.
24. J.W. Drake. Comparative rates of spontaneous mutation. Nature, 221 (1969), 1132.
25. J.W. Drake, J.J. Holland. Mutation rates among RNA viruses. Proc. Natl. Acad. Sci. USA, 96 (1999), 13910-13913.
26. E.A. Duarte, I.S. Novella, S. Ledesma, D.K. Clarke, A. Moya, S.F. Elena, E. Domingo, J.J. Holland. Subclonal components of consensus fitness in an RNA virus clone. J. Virol., 68 (1994), 4295-4301. (Pubitemid 24183022)
27. L.D. Eckerle, M.M. Becker, R.A. Halpin, K. Li, E. Venter, X. Lu, S. Scherbakova, R.L. Graham, R.S. Baric, T.B. Stockwell, D.J. Spiro, M.R. Denison. Infidelity of SARS-CoV Nsp14-exonuclease mutant virus replication is revealed by complete genome sequencing. PLoS Pathog, 6 (2010), e1000896.
28. L.D. Eckerle, X. Lu, S.M. Sperry, L. Choi, M.R. Denison. High fidelity of murine hepatitis virus replication is decreased in nsp14 exoribonuclease mutants. J Virol, 81 (2007), 12135-12144. (Pubitemid 350085829)
29. M. Eigen. Natural selection: a phase transition ? Biophys. Chem., 85 (2000), 101-123.
30. M. Eigen. Self-organization of matter and the evolution of biological macromolecules. Naturwissenschaften, 58 (1971), 465-523.
31. M. Eigen. Steps towards life, Oxford University Press, 1992.
32. M. Eigen, J. McCaskill, P. Schuster. Molecular quasi-species. J. Phys. Chem., 92 (1988), 6881-6891.
33. M. Eigen, P. Schuster. The hypercycle. A principle of natural self-organization. Springer, Berlin, 1979.
34. C. Escarmis, E. Lazaro, A. Arias, E. Domingo. Repeated bottleneck transfers can lead to non-cytocidal forms of a cytopathic virus: implications for viral extinction. J. Mol. Biol., 376 (2008), 367-379.
35. G. Feix, R. Pollet, C. Weissmann. Replication of viral RNA, XVI. Enzymatic synthesis of infectious viral RNA with noninfectious Q-beta minus strands as template. Proc Natl Acad Sci U S A, 59 (1968), 145-152.
36. C. Ferrer-Orta, R. Agudo, E. Domingo, N. Verdaguer. Structural insights into replication initiation and elongation processes by the FMDV RNA-dependent RNA polymerase. Current Opinion in Structural Biology, 19 (2009), 752-758.
37. C. Ferrer-Orta, A. Arias, R. Agudo, R. Perez-Luque, C. Escarmis, E. Domingo, N. Verdaguer. The structure of a protein primer-polymerase complex in the initiation of genome replication. EMBO J, 25 (2006), 880-888. (Pubitemid 43292448)
38. R.A. Flavell, D.L. Sabo, E.F. Bandle, C. Weissmann. Site-directed mutagenesis: generation of an extracistronic mutation in bacteriophage Q beta RNA. J Mol Biol, 89 (1974), 255-272.
39. E.C. Friedberg, G.C. Walker, W. Siede, R.D. Wood, R.A. Schultz, T. Ellenberger. DNA repair and mutagenesis. American Society for Microbiology, Washington, DC, 2006.
40. M. Gell-Mann. Complex adaptive systems, in: G.A. Cowan, D. Pines, D. Meltzer (Eds.). Complexity. Metaphors, models and reality, Wesley Publishing Co., Reading, MA, 1994, pp. 17-45.
41. R.F. Gesteland, T.R. Cech, J.F. Atkins. The RNA World. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 2006.
42. W. Gilbert. The RNA world. Nature, 319 (1986), 618.
43. C. Gonzalez-Lopez, A. Arias, N. Pariente, G. Gomez-Mariano, E. Domingo. Preextinction viral RNA can interfere with infectivity. J. Virol., 78 (2004), 3319-3324. (Pubitemid 38568272)
44. A. Grande-Perez, E. Lazaro, P. Lowenstein, E. Domingo, S.C. Manrubia. Suppression of viral infectivity through lethal defection. Proc. Natl. Acad. Sci. USA, 102 (2005), 4448-4452. (Pubitemid 40397132)
45. A. Grande-Perez, S. Sierra, M.G. Castro, E. Domingo, P.R. Lowenstein. 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 (2002), 12938-12943.
46. B.L. Haagmans, A.C. Andeweg, A.D. Osterhaus. The application of genomics to emerging zoonotic viral diseases. PLoS Pathog, 5 (2009), e1000557.
47. G.Z. Han, M. Worobey. Homologous recombination in negative sense RNA viruses. Viruses, 3 (2011), 1358-1373.
48. J.J. Holland. Continuum of change in RNA virus genomes. In: A.L. Notkins, M.B.A. Oldstone (Eds.). Concepts in Viral Pathogenesis, Springer-Verlag, New York, 1984.
49. J.J. Holland. Genetic diversity of RNA viruses. Current Topics in Microbiology and Immunology, Springer-Verlag, Berlin, 1992.
50. J.J. Holland, E.A. Grabau, C.L. Jones, B.L. Semler. Evolution of multiple genome mutations during long-term persistent infection by vesicular stomatitis virus. Cell, 16 (1979), 495-504. (Pubitemid 9140454)
51. J.J. Holland, K. Spindler, F. Horodyski, E. Grabau, S. Nichol, S. VandePol. Rapid evolution of RNA genomes. Science, 215 (1982), 1577-1585. (Pubitemid 12102984)
52. K. Horiuchi. Genetic studies of RNA phages, in: N.D. Zinder (Ed.) RNA Phages, Cold Spring Harbor laboratory, Cold Spring Harbor, New York, 1975, pp. 29-50.
53. J. Iranzo, S.C. Manrubia. Stochastic extinction of viral infectivity through the action of defectors. Europhys. Lett., 85 (2009), 18001.
54. J. Iranzo, C. Perales, E. Domingo, S.C. Manrubia. Tempo and mode of inhibitor-mutagen antiviral therapies: A multidisciplinary approach. Proc Natl Acad Sci U S A, 108 (2011), 16008-16013.
55. K.S. Kemal, C.M. Kitchen, H. Burger, B. Foley, D. Mayers, T. Klimkait, F. Hamy, K. Anastos, K. Petrovic, V.N. Minin, M.A. Suchard, B. Weiser. Recombination Between Variants from Genital Tract and Plasma: Evolution of Multidrug-Resistant HIV Type 1. AIDS research and human retroviruses, (2012), in press.
56. G.M. Li. Mechanisms and functions of DNA mismatch repair. Cell research, 18 (2008), 85-98.
57. T. Loeb, N.D. Zinder. A bacteriophage containing RNA. Proc Natl Acad Sci U S A, 47 (1961), 282-289.
58. R. Mateo, A. Diaz, E. Baranowski, M.G. Mateu. Complete alanine scanning of intersubunit interfaces in a foot-and-mouth disease virus capsid reveals critical contributions of many side chains to particle stability and viral function. J Biol Chem, 278 (2003), 41019-41027. (Pubitemid 37280925)
59. L. Menendez-Arias. Mutation rates and intrinsic fidelity of retroviral reverse transcriptases. Viruses, 1 (2009), 1137-1165.
60. A. Meyerhans, R. Cheynier, J. Albert, M. Seth, S. Kwok, J. Sninsky, L. Morfeldt-Manson, B. Asjo, S. Wain-Hobson. Temporal fluctuations in HIV quasispecies in vivo are not reflected by sequential HIV isolations. Cell, 58 (1989), 901-910. (Pubitemid 19227898)
61. D.R. Mills, R.L. Peterson, S. Spiegelman. An extracellular Darwinian experiment with a self-duplicating nucleic acid molecule. Proc. Natl. Acad. Sci. USA, 58 (1967), 217-224.
62. E. Minskaia, T. Hertzig, A.E. Gorbalenya, V. Campanacci, C. Cambillau, B. Canard, J. Ziebuhr. Discovery of an RNA virus 3'-> 5' exoribonuclease that is critically involved in coronavirus RNA synthesis. Proc. Natl. Acad. Sci. USA, 103 (2006), 5108-5113.
63. L. Moutouh, J. Corbeil, D.D. Richman. Recombination leads to the rapid emergence of HIV-1 dually resistant mutants under selective drug pressure. Proc Natl Acad Sci U S A, 93 (1996), 6106-6111. (Pubitemid 26190811)
64. H. Naegeli. Mechanisms of DNA damage recognition in mammalian cells. Landes Bioscience, Austin, Texas, 1997.
65. M.A. Nowak, P. Schuster. Error thresholds of replication in finite populations mutation frequencies and the onset of Muller's ratchet. J. Theor. Biol., 137 (1989), 375-395.
66. S. Ojosnegros, N. Beerenwinkel, T. Antal, M.A. Nowak, C. Escarmis, E. Domingo. Competition-colonization dynamics in an RNA virus. Proc Natl Acad Sci U S A, 107 (2010), 2108-2112.
67. K.M. Page, M.A. Nowak. Unifying evolutionary dynamics. J. Theor. Biol., 219 (2002), 93-98. (Pubitemid 35304434)
68. N. Pariente, A. Airaksinen, E. Domingo. Mutagenesis versus inhibition in the efficiency of extinction of foot-and-mouth disease virus. J. Virol., 77 (2003), 7131-7138. (Pubitemid 36666908)
69. N. Pariente, S. Sierra, P.R. Lowenstein, E. Domingo. Efficient virus extinction by combinations of a mutagen and antiviral inhibitors. J. Virol., 75 (2001), 9723-9730. (Pubitemid 32900107)
70. C. Perales, R. Agudo, S.C. Manrubia, E. Domingo. Influence of mutagenesis and viral load on the sustained low-level replication of an RNA virus. J Mol Biol, 407 (2011), 60-78.
71. C. Perales, R. Agudo, H. Tejero, S.C. Manrubia, E. Domingo. Potential benefits of sequential inhibitor-mutagen treatments of RNA virus infections. PLoS Pathog, 5 (2009), e1000658.
72. C. Perales, M. Henry, E. Domingo, S. Wain-Hobson, J.P. Vartanian. Lethal mutagenesis of foot-and-mouth disease virus involves shifts in sequence space. J Virol, (2011), 12227-12240.
73. C. Perales, R. Lorenzo-Redondo, C. Lopez-Galandez, M.A. Martinez, E. Domingo. Mutant spectra in virus behavior. Future Virology, 5 (2010), 679-698.
74. C. Perales, R. Mateo, M.G. Mateu, E. Domingo. Insights into RNA virus mutant spectrum and lethal mutagenesis events: replicative interference and complementation by multiple point mutants. J. Mol. Biol., 369 (2007), 985-1000. (Pubitemid 46754065)
75. J.K. Pfeiffer, K. Kirkegaard. Increased fidelity reduces poliovirus fitness under selective pressure in mice. PLoS Pathogens, 1 (2005), 102-110.
76. M.E. Quinones-Mateu, E. Arts. Virus fitness: concept, quantification, and application to HIV population dynamics. Current Topics in Microbiol. and Immunol., 299 (2006), 83-140. (Pubitemid 43086562)
77. D.B. Saakian, C.K. Biebricher, C.K. Hu. Phase diagram for the Eigen quasispecies theory with a truncated fitness landscape. Physical review, 79 (2009), 041905.
78. D.B. Saakian, E. Munoz, C.K. Hu, M.W. Deem. Quasispecies theory for multiple-peak fitness landscapes. Physical Review E, 73 (2006), 041913.
79. R. Sanjuan, M.R. Nebot, N. Chirico, L.M. Mansky, R. Belshaw. Viral mutation rates. J Virol, 84 (2010), 9733-9748.
80. D. Shriner, A.G. Rodrigo, D.C. Nickle, J.I. Mullins. Pervasive genomic recombination of HIV-1 in vivo. Genetics, 167 (2004), 1573-1583. (Pubitemid 39265897)
81. S. Sierra, M. Davila, P.R. Lowenstein, E. Domingo. Response of foot-and-mouth disease virus to increased mutagenesis. Influence of viral load and fitness in loss of infectivity. J. Virol., 74 (2000), 8316-8323. (Pubitemid 30666681)
82. P. Simmonds. Recombination in the Evolution of Picornaviruses. In: The Picornaviruses. E. Ehrenfeld, E. Domingo and R.P. Roos, eds, ASM Press, Washington, D.C. p.p. 229-238, 2010.
83. P. Simmonds, S. Midgley. Recombination in the genesis and evolution of hepatitis B virus genotypes. J Virol, 79 (2005), 15467-15476. (Pubitemid 43032329)
84. H.A. Simon. The Sciences of the Artificial (3rd edition). The MIT Press, Cambridge, Massachusetts, 1996.
85. F. Sobrino, M. Davila, J. Ortin, E. Domingo. Multiple genetic variants arise in the course of replication of foot-and-mouth disease virus in cell culture. Virology, 128 (1983), 310-318. (Pubitemid 13048816)
86. R. Solé, B. Goodwin. Signs of Life. How Complexity Pervades Biology. Basic Books, New York, 2000.
87. R. Sousa. Structural and mechanistic relationships between nucleic acid polymerases. Trends Biochem. Sci., 21 (1996), 186-190. (Pubitemid 26142569)
88. D.A. Steinhauer, E. Domingo, J.J. Holland. Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. Gene, 122 (1992), 281-288. (Pubitemid 23030332)
89. T.A. Steitz. DNA polymerases: structural diversity and common mechanisms. J. Biol. Chem., 274 (1999), 17395-17398.
90. J. Swetina, P. Schuster. Self-replication with errors. A model for polynucleotide replication. Biophys. Chem., 16 (1982), 329-345.
91. J. Sztuba-Solinska, A. Urbanowicz, M. Figlerowicz, J.J. Bujarski. RNA-RNA recombination in plant virus replication and evolution. Annual review of phytopathology, 49 (2011), 415-443.
92. M.N. Teng, M.B. Oldstone, J.C. de la Torre. Suppression of lymphocytic choriomeningitis virus-induced growth hormone deficiency syndrome by disease-negative virus variants. Virology, 223 (1996), 113-119. (Pubitemid 26302051)
93. R.C. Valentine, R. Ward, M. Strand. The replication cycle of RNA bacteriophages. Adv. Virus Res., 15 (1969), 1-59.
94. M. Vignuzzi, R. Andino. in: E. Ehrenfeld, E. Domingo, R.F. Roos (Eds.). The Picornaviruses. ASM Press, Washington DC, 2010, pp. 213-228.
95. M. Vignuzzi, J.K. Stone, J.J. Arnold, C.E. Cameron, R. Andino. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature, 439 (2006), 344-348. (Pubitemid 43128860)
96. C. Weissmann, M.A. Billeter, H.M. Goodman, J. Hindley, H. Weber. Structure and function of phage RNA. Annu Rev Biochem, 42 (1973), 303-328.
97. C. Weissmann, T. Tanaguchi, E. Domingo, D. Sabo, R.A. Flavell. Site-directed mutagenesis as a tool in genetics, in: J. Schultz, Z. Brada (Eds.). Genetic manipulation as it affects the cancer problem, Academic Press, New York, 1977, pp. 11-36.
98. C.O. Wilke, C. Ronnewinkel, T. Martinetz. Dynamic fitness landscapes in molecular evolution. Physics Reports, 349 (2001), 395-446. (Pubitemid 33402589)
99. S. Wright. The roles of mutation, inbreeding, crossbreading, and selection in evolution. Proc. of the VI International Congress of Genetics, 1 (1932), 356-366.
100. M. Yarus. Life from an RNA world. The ancestor within. Harvard University Press, Cambridge, Massachusetts and London, England, 2010.