Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-27T10:37:35.544Z Has data issue: false hasContentIssue false

From Quasispecies Theory to Viral Quasispecies: How Complexityhas Permeated Virology

Published online by Cambridge University Press:  17 October 2012

E. Domingo*
Affiliation:
Centro de Biología Molecular “Severo Ochoa” (CSIC-UAM) Campus de Cantoblanco 28049, Madrid, Spain Centro de Astrobiología (CSIC-INTA), Instituto Nacional de Técnica Aeroespacial Ctra. de Torrejón a Ajalvir, Km 4, 28850 Torrejón de Ardoz, Madrid, Spain Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), 08036 Barcelona, Spain
C. Perales
Affiliation:
Centro de Biología Molecular “Severo Ochoa” (CSIC-UAM) Campus de Cantoblanco 28049, Madrid, Spain Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), 08036 Barcelona, Spain
*
Corresponding author. E-mail: edomingo@cbm.uam.es
Get access

Abstract

RNA viruses replicate as complex and dynamic mutant distributions. They are termed viralquasispecies, in recognition of the fundamental contribution of quasispecies theory in ourunderstanding of error-prone replicative entities. Viral quasispecies have launched afertile field of transdiciplinary research, both experimental and theoretical. Here wereview the origin and some implications of the quasispecies concept, with emphasis oninternal interactions among components of the same mutant virus ensemble, a critical factto design new antiviral strategies. We make the distinction between “intrinsic” and“extrinsic” properties of mutant distributions, and emphasize that there are severallevels of complexity that can influence viral quasispecies behavior.

Type
Research Article
Copyright
© EDP Sciences, 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Références

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.
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, 311 (2003), 339349. CrossRefGoogle ScholarPubMed
Antia, R., Regoes, R.R., Koella, J.C., Bergstrom, C.T.. The role of evolution in the emergence of infectious diseases. Nature, 426 (2003), 658661. CrossRefGoogle ScholarPubMed
Arias, A., Agudo, R., Ferrer-Orta, C., Perez-Luque, R., Airaksinen, A., Brocchi, E., Domingo, E., Verdaguer, N., Escarmis, C.. Mutant viral polymerase in the transition of virus to error catastrophe identifies a critical site for RNA binding. J. Mol. Biol., 353 (2005), 10211032. CrossRefGoogle ScholarPubMed
Batschelet, E., Domingo, E., Weissmann, C.. The proportion of revertant and mutant phage in a growing population, as a function of mutation and growth rate. Gene, 1 (1976), 2732. CrossRefGoogle Scholar
Bernad, A., Blanco, L., Lazaro, J.M., Martin, G., Salas, M.. A conserved 3’ 5’ exonuclease active site in prokaryotic and eukaryotic DNA polymerases. Cell, 59 (1989), 219228. CrossRefGoogle ScholarPubMed
Biebricher, C.K., Eigen, M.. The error threshold. Virus Res., 107 (2005), 117127. CrossRefGoogle ScholarPubMed
Borrego, B., Novella, I.S., Giralt, E., Andreu, D., Domingo, E.. Distinct repertoire of antigenic variants of foot-and-mouth disease virus in the presence or absence of immune selection. J. Virol., 67 (1993), 60716079. Google Scholar
Buzon, M.J., Wrin, T., Codoner, F.M., Dalmau, J., Phung, P., Bonjoch, A., Coakley, E., Clotet, B., Martinez-Picado, J.. 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), 109117. CrossRefGoogle Scholar
Clementi, M.. Perspectives and opportunities for novel antiviral treatments targeting virus fitness. Clin Microbiol Infect, 14 (2008), 629631. CrossRefGoogle ScholarPubMed
Coffey, L.L., Beeharry, Y., Borderia, A.V., Blanc, H., Vignuzzi, M.. Arbovirus high fidelity variant loses fitness in mosquitoes and mice. Proc Natl Acad Sci U S A, 108 (2011), 1603816043. CrossRefGoogle ScholarPubMed
Crowder, S., Kirkegaard, K.. Trans-dominant inhibition of RNA viral replication can slow growth of drug-resistant viruses. Nature Genetics, 37 (2005), 701709. CrossRefGoogle Scholar
Chumakov, K.M., Powers, L.B., Noonan, K.E., Roninson, I.B., Levenbook, I.S.. 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), 199203. CrossRefGoogle ScholarPubMed
de la Torre, J.C., Holland, J.J.. RNA virus quasispecies populations can suppress vastly superior mutant progeny. J. Virol., 64 (1990), 62786281. Google ScholarPubMed
Denison, M.R., Graham, R.L., Donaldson, E.F., Eckerle, L.D., Baric, R.S.. Coronaviruses : an RNA proofreading machine regulates replication fidelity and diversity. RNA biology, 8 (2011), 270279. CrossRefGoogle ScholarPubMed
Domingo, E.. Mechanisms of viral emergence. Vet Res, 41 (2010), 38. CrossRefGoogle ScholarPubMed
E. Domingo, C. Biebricher, M. Eigen, J.J. Holland. Quasispecies and RNA Virus Evolution : Principles and Consequences. Landes Bioscience, Austin, 2001.
Domingo, E., Davila, M., Ortin, J.. Nucleotide sequence heterogeneity of the RNA from a natural population of foot-and-mouth-disease virus. Gene, 11 (1980), 333346. CrossRefGoogle ScholarPubMed
Domingo, E., Flavell, R.A., Weissmann, C.. In vitro site-directed mutagenesis : generation and properties of an infectious extracistronic mutant of bacteriophage Q . Gene, 1 (1976), 325. CrossRefGoogle Scholar
E. Domingo, J.J. Holland, P. Ahlquist. RNA Genetics, CRC Press, Boca Raton, 1988.
Domingo, E., Sabo, D., Taniguchi, T., Weissmann, C.. Nucleotide sequence heterogeneity of an RNA phage population. Cell, 13 (1978), 735744. CrossRefGoogle Scholar
Domingo, E., Sheldon, J., Perales, C.. Viral quasispecies evolution. Microbiology and Molecular Biology Reviews, 76 (2012), 159216. CrossRefGoogle ScholarPubMed
Domingo, E., Wain-Hobson, S.. The 30th anniversary of quasispecies. Meeting on ’Quasispecies : past, present and future’. EMBO Rep, 10 (2009), 444448. CrossRefGoogle ScholarPubMed
Drake, J.W.. Comparative rates of spontaneous mutation. Nature, 221 (1969), 1132. CrossRefGoogle ScholarPubMed
Drake, J.W., Holland, J.J.. Mutation rates among RNA viruses. Proc. Natl. Acad. Sci. USA, 96 (1999), 1391013913. CrossRefGoogle ScholarPubMed
Duarte, E.A., Novella, I.S., Ledesma, S., Clarke, D.K., Moya, A., Elena, S.F., Domingo, E., Holland, J.J.. Subclonal components of consensus fitness in an RNA virus clone. J. Virol., 68 (1994), 42954301. Google Scholar
Eckerle, L.D., Becker, M.M., Halpin, R.A., Li, K., Venter, E., Lu, X., Scherbakova, S., Graham, R.L., Baric, R.S., Stockwell, T.B., Spiro, D.J., Denison, M.R.. Infidelity of SARS-CoV Nsp14-exonuclease mutant virus replication is revealed by complete genome sequencing. PLoS Pathog, 6 (2010), e1000896. CrossRefGoogle ScholarPubMed
Eckerle, L.D., Lu, X., Sperry, S.M., Choi, L., Denison, M.R.. High fidelity of murine hepatitis virus replication is decreased in nsp14 exoribonuclease mutants. J Virol, 81 (2007), 1213512144. CrossRefGoogle ScholarPubMed
Eigen, M.. Natural selection : a phase transition? Biophys. Chem., 85 (2000), 101123. CrossRefGoogle ScholarPubMed
Eigen, M.. Self-organization of matter and the evolution of biological macromolecules. Naturwissenschaften, 58 (1971), 465523. CrossRefGoogle Scholar
M. Eigen. Steps towards life, Oxford University Press, 1992.
Eigen, M., McCaskill, J., Schuster, P.. Molecular quasi-species. J. Phys. Chem., 92 (1988), 68816891. CrossRefGoogle Scholar
M. Eigen, P. Schuster. The hypercycle. A principle of natural self-organization. Springer, Berlin, 1979.
Escarmis, C., Lazaro, E., Arias, A., Domingo, E.. Repeated bottleneck transfers can lead to non-cytocidal forms of a cytopathic virus : implications for viral extinction. J. Mol. Biol., 376 (2008), 367379. CrossRefGoogle ScholarPubMed
Feix, G., Pollet, R., Weissmann, C.. 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), 145152. CrossRefGoogle ScholarPubMed
Ferrer-Orta, C., Agudo, R., Domingo, E., Verdaguer, N.. Structural insights into replication initiation and elongation processes by the FMDV RNA-dependent RNA polymerase. Current Opinion in Structural Biology, 19 (2009), 752758. CrossRefGoogle ScholarPubMed
Ferrer-Orta, C., Arias, A., Agudo, R., Perez-Luque, R., Escarmis, C., Domingo, E., Verdaguer, N.. The structure of a protein primer-polymerase complex in the initiation of genome replication. EMBO J, 25 (2006), 880888. CrossRefGoogle ScholarPubMed
Flavell, R.A., Sabo, D.L., Bandle, E.F., Weissmann, C.. Site-directed mutagenesis : generation of an extracistronic mutation in bacteriophage Q beta RNA. J Mol Biol, 89 (1974), 255272. CrossRefGoogle ScholarPubMed
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.
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.
R.F. Gesteland, T.R. Cech, J.F. Atkins. The RNA World. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 2006.
Gilbert, W.. The RNA world. Nature, 319 (1986), 618. CrossRefGoogle Scholar
Gonzalez-Lopez, C., Arias, A., Pariente, N., Gomez-Mariano, G., Domingo, E.. Preextinction viral RNA can interfere with infectivity. J. Virol., 78 (2004), 33193324. CrossRefGoogle ScholarPubMed
Grande-Perez, A., Lazaro, E., Lowenstein, P., Domingo, E., Manrubia, S.C.. Suppression of viral infectivity through lethal defection. Proc. Natl. Acad. Sci. USA, 102 (2005), 44484452. CrossRefGoogle ScholarPubMed
Grande-Perez, A., Sierra, S., Castro, M.G., Domingo, E., Lowenstein, P.R.. 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), 1293812943. CrossRefGoogle Scholar
Haagmans, B.L., Andeweg, A.C., Osterhaus, A.D.. The application of genomics to emerging zoonotic viral diseases. PLoS Pathog, 5 (2009), e1000557. CrossRefGoogle Scholar
Han, G.Z., Worobey, M.. Homologous recombination in negative sense RNA viruses. Viruses, 3 (2011), 13581373. CrossRefGoogle Scholar
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.
J.J. Holland. Genetic diversity of RNA viruses. Current Topics in Microbiology and Immunology, Springer-Verlag, Berlin, 1992.
Holland, J.J., Grabau, E.A., Jones, C.L., Semler, B.L.. Evolution of multiple genome mutations during long-term persistent infection by vesicular stomatitis virus. Cell, 16 (1979), 495504. CrossRefGoogle ScholarPubMed
Holland, J.J., Spindler, K., Horodyski, F., Grabau, E., Nichol, S., VandePol, S.. Rapid evolution of RNA genomes. Science, 215 (1982), 15771585. CrossRefGoogle ScholarPubMed
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.
Iranzo, J., Manrubia, S.C.. Stochastic extinction of viral infectivity through the action of defectors. Europhys. Lett., 85 (2009), 18001. CrossRefGoogle Scholar
Iranzo, J., Perales, C., Domingo, E., Manrubia, S.C.. Tempo and mode of inhibitor-mutagen antiviral therapies : A multidisciplinary approach. Proc Natl Acad Sci U S A, 108 (2011), 1600816013. CrossRefGoogle ScholarPubMed
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.
Li, G.M.. Mechanisms and functions of DNA mismatch repair. Cell research, 18 (2008), 8598. CrossRefGoogle Scholar
Loeb, T., Zinder, N.D.. A bacteriophage containing RNA. Proc Natl Acad Sci U S A, 47 (1961), 282289. CrossRefGoogle ScholarPubMed
Mateo, R., Diaz, A., Baranowski, E., Mateu, M.G.. 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), 4101941027. CrossRefGoogle Scholar
Menendez-Arias, L.. Mutation rates and intrinsic fidelity of retroviral reverse transcriptases. Viruses, 1 (2009), 11371165. CrossRefGoogle ScholarPubMed
Meyerhans, A., Cheynier, R., Albert, J., Seth, M., Kwok, S., Sninsky, J., Morfeldt-Manson, L., Asjo, B., Wain-Hobson, S.. Temporal fluctuations in HIV quasispecies in vivo are not reflected by sequential HIV isolations. Cell, 58 (1989), 901910. CrossRefGoogle Scholar
Mills, D.R., Peterson, R.L., Spiegelman, S.. An extracellular Darwinian experiment with a self-duplicating nucleic acid molecule. Proc. Natl. Acad. Sci. USA, 58 (1967), 217224. CrossRefGoogle ScholarPubMed
Minskaia, E., Hertzig, T., Gorbalenya, A.E., Campanacci, V., Cambillau, C., Canard, B., Ziebuhr, J.. Discovery of an RNA virus 3’ −  > 5’ exoribonuclease that is critically involved in coronavirus RNA synthesis. Proc. Natl. Acad. Sci. USA, 103 (2006), 51085113. CrossRefGoogle ScholarPubMed
Moutouh, L., Corbeil, J., Richman, D.D.. 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), 61066111. CrossRefGoogle Scholar
H. Naegeli. Mechanisms of DNA damage recognition in mammalian cells. Landes Bioscience, Austin, Texas, 1997.
Nowak, M.A., Schuster, P.. Error thresholds of replication in finite populations mutation frequencies and the onset of Muller’s ratchet. J. Theor. Biol., 137 (1989), 375395. CrossRefGoogle Scholar
Ojosnegros, S., Beerenwinkel, N., Antal, T., Nowak, M.A., Escarmis, C., Domingo, E.. Competition-colonization dynamics in an RNA virus. Proc Natl Acad Sci U S A, 107 (2010), 21082112. CrossRefGoogle Scholar
Page, K.M., Nowak, M.A.. Unifying evolutionary dynamics. J. Theor. Biol., 219 (2002), 9398. CrossRefGoogle ScholarPubMed
Pariente, N., Airaksinen, A., Domingo, E.. Mutagenesis versus inhibition in the efficiency of extinction of foot-and-mouth disease virus. J. Virol., 77 (2003), 71317138. CrossRefGoogle Scholar
Pariente, N., Sierra, S., Lowenstein, P.R., Domingo, E.. Efficient virus extinction by combinations of a mutagen and antiviral inhibitors. J. Virol., 75 (2001), 97239730. CrossRefGoogle ScholarPubMed
Perales, C., Agudo, R., Manrubia, S.C., Domingo, E.. Influence of mutagenesis and viral load on the sustained low-level replication of an RNA virus. J Mol Biol, 407 (2011), 6078. CrossRefGoogle ScholarPubMed
Perales, C., Agudo, R., Tejero, H., Manrubia, S.C., Domingo, E.. Potential benefits of sequential inhibitor-mutagen treatments of RNA virus infections. PLoS Pathog, 5 (2009), e1000658. CrossRefGoogle ScholarPubMed
Perales, C., Henry, M., Domingo, E., Wain-Hobson, S., Vartanian, J.P.. Lethal mutagenesis of foot-and-mouth disease virus involves shifts in sequence space. J Virol, (2011), 1222712240. CrossRefGoogle ScholarPubMed
Perales, C., Lorenzo-Redondo, R., Lopez-Galandez, C., Martinez, M.A., Domingo, E.. Mutant spectra in virus behavior. Future Virology, 5 (2010), 679698. CrossRefGoogle Scholar
Perales, C., Mateo, R., Mateu, M.G., Domingo, E.. Insights into RNA virus mutant spectrum and lethal mutagenesis events : replicative interference and complementation by multiple point mutants. J. Mol. Biol., 369 (2007), 9851000. CrossRefGoogle ScholarPubMed
Pfeiffer, J.K., Kirkegaard, K.. Increased fidelity reduces poliovirus fitness under selective pressure in mice. PLoS Pathogens, 1 (2005), 102110. CrossRefGoogle ScholarPubMed
Quinones-Mateu, M.E., Arts, E.. Virus fitness : concept, quantification, and application to HIV population dynamics. Current Topics in Microbiol. and Immunol., 299 (2006), 83140. Google ScholarPubMed
Saakian, D.B., Biebricher, C.K., Hu, C.K.. Phase diagram for the Eigen quasispecies theory with a truncated fitness landscape. Physical review, 79 (2009), 041905. Google ScholarPubMed
Saakian, D.B., Munoz, E., Hu, C.K., Deem, M.W.. Quasispecies theory for multiple-peak fitness landscapes. Physical Review E, 73 (2006), 041913. CrossRefGoogle ScholarPubMed
Sanjuan, R., Nebot, M.R., Chirico, N., Mansky, L.M., Belshaw, R.. Viral mutation rates. J Virol, 84 (2010), 97339748. CrossRefGoogle ScholarPubMed
Shriner, D., Rodrigo, A.G., Nickle, D.C., Mullins, J.I.. Pervasive genomic recombination of HIV-1 in vivo. Genetics, 167 (2004), 15731583. CrossRefGoogle ScholarPubMed
Sierra, S., Davila, M., Lowenstein, P.R., Domingo, E.. Response of foot-and-mouth disease virus to increased mutagenesis. Influence of viral load and fitness in loss of infectivity. J. Virol., 74 (2000), 83168323. CrossRefGoogle ScholarPubMed
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.
Simmonds, P., Midgley, S.. Recombination in the genesis and evolution of hepatitis B virus genotypes. J Virol, 79 (2005), 1546715476. CrossRefGoogle ScholarPubMed
H.A. Simon. The Sciences of the Artificial (3rd edition). The MIT Press, Cambridge, Massachusetts, 1996.
Sobrino, F., Davila, M., Ortin, J., Domingo, E.. Multiple genetic variants arise in the course of replication of foot-and-mouth disease virus in cell culture. Virology, 128 (1983), 310318. CrossRefGoogle ScholarPubMed
R. Solé, B. Goodwin. Signs of Life. How Complexity Pervades Biology. Basic Books, New York, 2000.
Sousa, R.. Structural and mechanistic relationships between nucleic acid polymerases. Trends Biochem. Sci., 21 (1996), 186190. CrossRefGoogle Scholar
Steinhauer, D.A., Domingo, E., Holland, J.J.. Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. Gene, 122 (1992), 281288. CrossRefGoogle ScholarPubMed
Steitz, T.A.. DNA polymerases : structural diversity and common mechanisms. J. Biol. Chem., 274 (1999), 1739517398. CrossRefGoogle Scholar
Swetina, J., Schuster, P.. Self-replication with errors. A model for polynucleotide replication. Biophys. Chem., 16 (1982), 329345. CrossRefGoogle Scholar
Sztuba-Solinska, J., Urbanowicz, A., Figlerowicz, M., Bujarski, J.J.. RNA-RNA recombination in plant virus replication and evolution. Annual review of phytopathology, 49 (2011), 415443. CrossRefGoogle Scholar
Teng, M.N., Oldstone, M.B., de la Torre, J.C.. Suppression of lymphocytic choriomeningitis virus-induced growth hormone deficiency syndrome by disease-negative virus variants. Virology, 223 (1996), 113119. CrossRefGoogle ScholarPubMed
Valentine, R.C., Ward, R., Strand, M.. The replication cycle of RNA bacteriophages. Adv. Virus Res., 15 (1969), 159. CrossRefGoogle ScholarPubMed
M. Vignuzzi, R. Andino. in : E. Ehrenfeld, E. Domingo, R.F. Roos (Eds.). The Picornaviruses. ASM Press, Washington DC, 2010, pp. 213–228.
Vignuzzi, M., Stone, J.K., Arnold, J.J., Cameron, C.E., Andino, R.. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature, 439 (2006), 344348. CrossRefGoogle Scholar
Weissmann, C., Billeter, M.A., Goodman, H.M., Hindley, J., Weber, H.. Structure and function of phage RNA. Annu Rev Biochem, 42 (1973), 303328. CrossRefGoogle ScholarPubMed
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.
Wilke, C.O., Ronnewinkel, C., Martinetz, T.. Dynamic fitness landscapes in molecular evolution. Physics Reports, 349 (2001), 395446. CrossRefGoogle Scholar
Wright, S.. The roles of mutation, inbreeding, crossbreading, and selection in evolution. Proc. of the VI International Congress of Genetics, 1 (1932), 356366. Google Scholar
M. Yarus. Life from an RNA world. The ancestor within. Harvard University Press, Cambridge, Massachusetts and London, England, 2010.