1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Virology
  4. Volume 8, 2021
  5. Article

Annual Review of Virology

Volume 8, 2021

Historical Perspective on the Discovery of the Quasispecies Concept

Abstract

Viral quasispecies are dynamic distributions of nonidentical but closely related mutant and recombinant viral genomes subjected to a continuous process of genetic variation, competition, and selection that may act as a unit of selection. The quasispecies concept owes its theoretical origins to a model for the origin of life as a collection of mutant RNA replicators. Independently, experimental evidence for the quasispecies concept was obtained from sampling of bacteriophage clones, which revealed that the viral populations consisted of many mutant genomes whose frequency varied with time of replication. Similar findings were made in animal and plant RNA viruses. Quasispecies became a theoretical framework to understand viral population dynamics and adaptability. The evidence came at a time when mutations were considered rare events in genetics, a perception that was to change dramatically in subsequent decades. Indeed, viral quasispecies was the conceptual forefront of a remarkable degree of biological diversity, now evident for cell populations and organisms, not only for viruses. Quasispecies dynamics unveiled complexities in the behavior of viral populations,with consequences for disease mechanisms and control strategies. This review addresses the origin of the quasispecies concept, its major implications on both viral evolution and antiviral strategies, and current and future prospects.

Keyword(s): adaptation, antiviral strategies, lethal mutagenesis, mutation, mutation rate, population dynamics, residue conservation, sequence space
Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-091919-105900
2021-09-29
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/virology/8/1/annurev-virology-091919-105900.html?itemId=/content/journals/10.1146/annurev-virology-091919-105900&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Domingo E. 2020. Virus as Populations Amsterdam: Elsevier, 2nd ed..
  2. 2. 
    Holland JJ, Spindler K, Horodyski F, Grabau E, Nichol S, VandePol S 1982. Rapid evolution of RNA genomes. Science 215:1577–85
     [Google Scholar]
  3. 3. 
    Eigen M. 1971. Self-organization of matter and the evolution of biological macromolecules. Naturwissenschaften 58:465–523
     [Google Scholar]
  4. 4. 
    Eigen M, Schuster P. 1979. The Hypercycle: A Principle of Natural Self-Organization Berlin: Springer
  5. 5. 
    Mills DR, Peterson RL Spiegelman S. 1967. An extracellular Darwinian experiment with a self-duplicating nucleic acid molecule italicPNAS 58:217–24
     [Google Scholar]
  6. 6. 
    Bull JJ, Meyers LA, Lachmann M. 2005. Quasispecies made simple. PLOS Comput. Biol. 1:e61
     [Google Scholar]
  7. 7. 
    Tejero H, Montero F, Nuno JC. 2016. Theories of lethal mutagenesis: from error catastrophe to lethal defection. Curr. Top. Microbiol. Immunol. 392:161–79
     [Google Scholar]
  8. 8. 
    Domingo E, Schuster P. 2016. Quasispecies: From Theory to Experimental Systems Cham, Switz: Springer
  9. 9. 
    Szostak N, Wasik S, Blazewicz J. 2016. Hypercycle. PLOS Comput. Biol 12:e1004853
     [Google Scholar]
  10. 10. 
    Eigen M. 2002. Error catastrophe and antiviral strategy. PNAS 99:13374–76
     [Google Scholar]
  11. 11. 
    Eigen M. 2013. From Strange Simplicity to Complex Familiarity Oxford, UK: Oxford Univ. Press
  12. 12. 
    Weissmann C, Billeter MA, Goodman HM, Hindley J, Weber H. 1973. Structure and function of phage RNA. Annu. Rev. Biochem. 42:303–28
     [Google Scholar]
  13. 13. 
    Weissmann C. 1974. The making of a phage. FEBS Lett 40:S1S3–9
     [Google Scholar]
  14. 14. 
    Takeshita D, Yamashita S, Tomita K. 2014. Molecular insights into replication initiation by Qβ replicase using ribosomal protein S1. Nucleic Acids Res 42:10809–22
     [Google Scholar]
  15. 15. 
    Flavell RA, Sabo DL, Bandle EF, Weissmann C. 1974. Site-directed mutagenesis: generation of an extracistronic mutation in bacteriophage Qβ RNA. J. Mol. Biol. 89:255–72
     [Google Scholar]
  16. 16. 
    Domingo E, Flavell RA, Weissmann C. 1976. In vitro site-directed mutagenesis: generation and properties of an infectious extracistronic mutant of bacteriophage Qβ. Gene 1:3–25
     [Google Scholar]
  17. 17. 
    Sheahan TP, Sims AC, Zhou S, Graham RL, Pruijssers AJ et al. 2020. An orally bioavailable broad-spectrum antiviral inhibits SARS-CoV-2 in human airway epithelial cell cultures and multiple coronaviruses in mice. Sci. Transl. Med. 12:eabb5883
     [Google Scholar]
  18. 18. 
    Agostini ML, Pruijssers AJ, Chappell JD, Gribble J, Lu X et al. 2019. Small-molecule antiviral β-d-N4-hydroxycytidine inhibits a proofreading-intact coronavirus with a high genetic barrier to resistance. J. Virol. 93:e01348-19
     [Google Scholar]
  19. 19. 
    de Wachter R, Fiers W. 1972. Preparative two-dimensional polyacrylamide gel electrophoresis of 32P-labeled RNA. Anal. Biochem. 49:184–97
     [Google Scholar]
  20. 20. 
    Billeter MA. 1978. Sequence and location of large RNase T1 oligonucleotides in bacteriophage Qbeta RNA. J. Biol. Chem. 253:8381–89
     [Google Scholar]
  21. 21. 
    Weissmann C, Tanaguchi T, Domingo E, Sabo D, Flavell RA 1977. Site-directed mutagenesis as a tool in genetics. Genetic Manipulation as It Affects the Cancer Problem J Schultz, Z Brada 11–36 New York: Academic
     [Google Scholar]
  22. 22. 
    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
     [Google Scholar]
  23. 23. 
    Drake JW. 1969. Comparative rates of spontaneous mutation. Nature 221:1132
     [Google Scholar]
  24. 24. 
    Drake JW, Charlesworth B, Charlesworth D, Crow JF. 1998. Rates of spontaneous mutation. Genetics 148:1667–86
     [Google Scholar]
  25. 25. 
    Drake JW, Holland JJ 1999. Mutation rates among RNA viruses. PNAS 96:13910–13
     [Google Scholar]
  26. 26. 
    Sanjuan R, Nebot MR, Chirico N, Mansky LM, Belshaw R. 2010. Viral mutation rates. J. Virol. 84:9733–48
     [Google Scholar]
  27. 27. 
    Domingo E, Sabo D, Taniguchi T, Weissmann C. 1978. Nucleotide sequence heterogeneity of an RNA phage population. Cell 13:735–44
     [Google Scholar]
  28. 28. 
    Biebricher CK, Eigen M, Gardiner WC Jr. 1985. Kinetics of RNA replication: competition and selection among self-replicating RNA species. Biochemistry 24:6550–60
     [Google Scholar]
  29. 29. 
    Domingo E, Holland JJ, Ahlquist P. 1988. RNA Genetics Boca Raton, FL: CRC
  30. 30. 
    Holmes EC, Moya A. 2002. Is the quasispecies concept relevant to RNA viruses?. J. Virol. 76:1460–62
     [Google Scholar]
  31. 31. 
    Domingo E. 2002. Quasispecies theory in virology. J. Virol. 76:463–65
     [Google Scholar]
  32. 32. 
    de la Torre JC, Holland JJ. 1990. RNA virus quasispecies populations can suppress vastly superior mutant progeny. J. Virol. 64:6278–81
     [Google Scholar]
  33. 33. 
    Domingo E, Perales C. 2019. Viral quasispecies. PLOS Genet 15:e1008271
     [Google Scholar]
  34. 34. 
    Domingo E, Schuster P. 2016. What is a quasispecies? Historical origins and current scope. Curr. Top. Microbiol. Immunol. 392:1–22
     [Google Scholar]
  35. 35. 
    Briones C, Domingo E 2008. Minority report: hidden memory genomes in HIV-1 quasispecies and possible clinical implications. AIDS Rev 10:93–109
     [Google Scholar]
  36. 36. 
    Sukkaew A, Thanagith M, Thongsakulprasert T, Mutso M, Mahalingam S et al. 2018. Heterogeneity of clinical isolates of chikungunya virus and its impact on the responses of primary human fibroblast-like synoviocytes. J. Gen. Virol. 99:525–35
     [Google Scholar]
  37. 37. 
    Yin J. 1993. Evolution of bacteriophage T7 in a growing plaque. J. Bacteriol. 175:1272–77
     [Google Scholar]
  38. 38. 
    Voorhees IEH, Lee H, Allison AB, Lopez-Astacio R, Goodman LB et al. 2019. Limited intrahost diversity and background evolution accompany 40 years of canine parvovirus host adaptation and spread. J. Virol. 94:e01162-19
     [Google Scholar]
  39. 39. 
    Jordan-Paiz A, Nevot M, Lamkiewicz K, Lataretu M, Franco S et al. 2020. HIV-1 lethality and loss of Env protein expression induced by single synonymous substitutions in the virus genome intronic-splicing silencer. J. Virol. 94:e01108-20
     [Google Scholar]
  40. 40. 
    Nam B, Mekuria Z, Carossino M, Li G, Zheng Y et al. 2019. Intrahost selection pressure drives equine arteritis virus evolution during persistent infection in the stallion reproductive tract. J. Virol. 93:e00045-19
     [Google Scholar]
  41. 41. 
    Honce R, Schultz-Cherry S. 2020. They are what you eat: shaping of viral populations through nutrition and consequences for virulence. PLOS Pathog 16:e1008711
     [Google Scholar]
  42. 42. 
    Mira A, Martin-Cuadrado AB, D'Auria G, Rodriguez-Valera F 2010. The bacterial pan-genome: a new paradigm in microbiology. Int. Microbiol. 13:45–57
     [Google Scholar]
  43. 43. 
    Acevedo A, Brodsky L, Andino R. 2014. Mutational and fitness landscapes of an RNA virus revealed through population sequencing. Nature 505:686–90
     [Google Scholar]
  44. 44. 
    Riaz N, Leung P, Barton K, Smith MA, Carswell S et al. 2021. Adaptation of Oxford Nanopore technology for hepatitis C whole genome sequencing and identification of within-host viral variants. BMC Genom. 22:1148
     [Google Scholar]
  45. 45. 
    Borrow P, Lewicki H, Wei X, Horwitz MS, Peffer N et al. 1997. Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat. Med. 3:205–11
     [Google Scholar]
  46. 46. 
    Young DF, Wignall-Fleming EB, Busse DC, Pickin MJ, Hankinson J et al. 2019. The switch between acute and persistent paramyxovirus infection caused by single amino acid substitutions in the RNA polymerase P subunit. PLOS Pathog 15:e1007561
     [Google Scholar]
  47. 47. 
    Oldstone MB. 2006. Viral persistence: parameters, mechanisms and future predictions. Virology 344:111–18
     [Google Scholar]
  48. 48. 
    Marcus PI, Rodriguez LL, Sekellick MJ. 1998. Interferon induction as a quasispecies marker of vesicular stomatitis virus populations. J. Virol. 72:542–49
     [Google Scholar]
  49. 49. 
    Garcin D, Itoh M, Kolakofsky D. 1997. A point mutation in the Sendai virus accessory C proteins attenuates virulence for mice, but not virus growth in cell culture. Virology 238:424–31
     [Google Scholar]
  50. 50. 
    Young DF, Chatziandreou N, He B, Goodbourn S, Lamb RA, Randall RE. 2001. Single amino acid substitution in the V protein of simian virus 5 differentiates its ability to block interferon signaling in human and murine cells. J. Virol. 75:3363–70
     [Google Scholar]
  51. 51. 
    Ghorbani A, Abundo MC, Ji H, Taylor KJM, Ngunjiri JM, Lee CW 2020. Viral subpopulation screening guides in designing a high interferon inducing live attenuated influenza vaccine by targeting rare mutations in NS1 and PB2 proteins. J. Virol. 95:2e01722-20
     [Google Scholar]
  52. 52. 
    Baranowski E, Ruiz-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
     [Google Scholar]
  53. 53. 
    Ringelhan M, McKeating JA, Protzer U. 2017. Viral hepatitis and liver cancer. Philos. Trans. R. Soc. B 372:20160274
     [Google Scholar]
  54. 54. 
    Koizumi K, Enomoto N, Kurosaki M, Murakami T, Izumi N et al. 1995. Diversity of quasispecies in various disease stages of chronic hepatitis C virus infection and its significance in interferon treatment. Hepatology 22:30–35
     [Google Scholar]
  55. 55. 
    Farci P, Shimoda A, Coiana A, Diaz G, Peddis G et al. 2000. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 288:339–44
     [Google Scholar]
  56. 56. 
    Kumar D, Malik A, Asim M, Chakravarti A, Das RH, Kar P. 2008. Influence of quasispecies on virological responses and disease severity in patients with chronic hepatitis C. World J. Gastroenterol 14:701–8
     [Google Scholar]
  57. 57. 
    Hamdane N, Juhling F, Crouchet E, El Saghire H, Thumann C et al. 2019. HCV-induced epigenetic changes associated with liver cancer risk persist after sustained virologic response. Gastroenterology 156:2313–29.e7
     [Google Scholar]
  58. 58. 
    Horie C, Iwahana H, Horie T, Shimizu I, Yoshimoto K et al. 1996. Detection of different quasispecies of hepatitis C virus core region in cancerous and noncancerous lesions. Biochem. Biophys. Res. Commun. 218:674–81
     [Google Scholar]
  59. 59. 
    Zhang AY, Lai CL, Huang FY, Seto WK, Fung J et al. 2017. Deep sequencing analysis of quasispecies in the HBV pre-S region and its association with hepatocellular carcinoma. J. Gastroenterol. 52:1064–74
     [Google Scholar]
  60. 60. 
    Fang X, Wu HH, Ren JJ, Liu HZ, Li KZ et al. 2017. Associations between serum HBX quasispecies and their integration in hepatocellular carcinoma. Int. J. Clin. Exp. Pathol. 10:11857–66
     [Google Scholar]
  61. 61. 
    Perelygina L, Chen MH, Suppiah S, Adebayo A, Abernathy E et al. 2019. Infectious vaccine-derived rubella viruses emerge, persist, and evolve in cutaneous granulomas of children with primary immunodeficiencies. PLOS Pathog 15:e1008080
     [Google Scholar]
  62. 62. 
    Agudelo-Romero P, Carbonell P, de la Iglesia F, Carrera J, Rodrigo G et al. 2008. Changes in the gene expression profile of Arabidopsis thaliana after infection with Tobacco etch virus. Virol. J. 5:92
     [Google Scholar]
  63. 63. 
    Hillung J, Garcia-Garcia F, Dopazo J, Cuevas JM, Elena SF. 2016. The transcriptomics of an experimentally evolved plant-virus interaction. Sci. Rep. 6:24901
     [Google Scholar]
  64. 64. 
    Cervera H, Ambros S, Bernet GP, Rodrigo G, Elena SF 2018. Viral fitness correlates with the magnitude and direction of the perturbation induced in the host's transcriptome: the tobacco etch potyvirus—tobacco case study. Mol. Biol. Evol. 35:1599–615
     [Google Scholar]
  65. 65. 
    Correa RL, Sanz-Carbonell A, Kogej Z, Muller SY, Ambros S et al. 2020. Viral fitness determines the magnitude of transcriptomic and epigenomic reprograming of defense responses in plants. Mol. Biol. Evol. 37:1866–81
     [Google Scholar]
  66. 66. 
    Vignuzzi M, Lopez CB. 2019. Defective viral genomes are key drivers of the virus-host interaction. Nat. Microbiol. 4:1075–87
     [Google Scholar]
  67. 67. 
    Ahmed R, Oldstone MB. 1988. Organ-specific selection of viral variants during chronic infection. J. Exp. Med. 167:1719–24
     [Google Scholar]
  68. 68. 
    Wong JK, Ignacio CC, Torriani F, Havlir D, Fitch NJ, Richman DD. 1997. In vivo compartmentalization of human immunodeficiency virus: evidence from the examination of pol sequences from autopsy tissues. J. Virol. 71:2059–71
     [Google Scholar]
  69. 69. 
    Shapshak P, Segal DM, Crandall KA, Fujimura RK, Zhang BT et al. 1999. Independent evolution of HIV type 1 in different brain regions. AIDS Res. Hum. Retroviruses 15:811–20
     [Google Scholar]
  70. 70. 
    van't Wout AB, Ran LJ, Kuiken CL, Kootstra NA, Pals ST, Schuitemaker H. 1998. Analysis of the temporal relationship between human immunodeficiency virus type 1 quasispecies in sequential blood samples and various organs obtained at autopsy. J. Virol. 72:488–96
     [Google Scholar]
  71. 71. 
    Hightower GK, Wong JK, Letendre SL, Umlauf AA, Ellis RJ et al. 2012. Higher HIV-1 genetic diversity is associated with AIDS and neuropsychological impairment. Virology 433:498–505
     [Google Scholar]
  72. 72. 
    Ciota AT, Ngo KA, Lovelace AO, Payne AF, Zhou Y et al. 2007. Role of the mutant spectrum in adaptation and replication of West Nile virus. J. Gen. Virol. 88:865–74
     [Google Scholar]
  73. 73. 
    Pfeiffer JK, Kirkegaard K 2006. Bottleneck-mediated quasispecies restriction during spread of an RNA virus from inoculation site to brain. PNAS 103:5520–25
     [Google Scholar]
  74. 74. 
    Bull RA, Luciani F, McElroy K, Gaudieri S, Pham ST et al. 2011. Sequential bottlenecks drive viral evolution in early acute hepatitis C virus infection. PLOS Pathog 7:e1002243
     [Google Scholar]
  75. 75. 
    Jerzak GV, Bernard K, Kramer LD, Shi PY, Ebel GD. 2007. The West Nile virus mutant spectrum is host-dependant and a determinant of mortality in mice. Virology 360:469–76
     [Google Scholar]
  76. 76. 
    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. PNAS 88:199–203
     [Google Scholar]
  77. 77. 
    Marcus PI, Ngunjiri JM, Sekellick MJ, Wang L, Lee CW 2010. In vitro analysis of virus particle subpopulations in candidate live-attenuated influenza vaccines distinguishes effective from ineffective vaccines. J. Virol. 84:10974–81
     [Google Scholar]
  78. 78. 
    Sanz-Ramos M, Diaz-San Segundo F, Escarmis C, Domingo E, Sevilla N 2008. Hidden virulence determinants in a viral quasispecies in vivo. J. Virol. 82:10465–76
     [Google Scholar]
  79. 79. 
    Moreno E, Gallego I, Gregori J, Lucia-Sanz A, Soria ME et al. 2017. Internal disequilibria and phenotypic diversification during replication of hepatitis C virus in a noncoevolving cellular environment. J. Virol. 91:e02505-16
     [Google Scholar]
  80. 80. 
    Braun T, Borderia AV, Barbezange C, Vignuzzi M, Louzoun Y. 2019. Long-term context-dependent genetic adaptation of the viral genetic cloud. Bioinformatics 35:1907–15
     [Google Scholar]
  81. 81. 
    Gallego I, Soria ME, Garcia-Crespo C, Chen Q, Martinez-Barragan P et al. 2020. Broad and dynamic diversification of infectious hepatitis C virus in a cell culture environment. J. Virol. 94:e01856-19
     [Google Scholar]
  82. 82. 
    Baccam P, Thompson RJ, Fedrigo O, Carpenter S, Cornette JL. 2001. PAQ: partition analysis of quasispecies. Bioinformatics 17:16–22
     [Google Scholar]
  83. 83. 
    Skums P, Zelikovsky A, Singh R, Gussler W, Dimitrova Z et al. 2018. QUENTIN: reconstruction of disease transmissions from viral quasispecies genomic data. Bioinformatics 34:163–70
     [Google Scholar]
  84. 84. 
    Ahn S, Ke Z, Vikalo H. 2018. Viral quasispecies reconstruction via tensor factorization with successive read removal. Bioinformatics 34:i23–31
     [Google Scholar]
  85. 85. 
    Henningsson R, Moratorio G, Borderia AV, Vignuzzi M, Fontes M. 2019. DISSEQT—DIStribution-based modeling of SEQuence space Time dynamics. Virus Evol 5:vez028
     [Google Scholar]
  86. 86. 
    Jee J, Rasouly A, Shamovsky I, Akivis Y, Steinman SR et al. 2016. Rates and mechanisms of bacterial mutagenesis from maximum-depth sequencing. Nature 534:693–96
     [Google Scholar]
  87. 87. 
    Garcia-Crespo C, Soria ME, Gallego I, Avila AI, Martinez-Gonzalez B et al. 2020. Dissimilar conservation pattern in hepatitis C virus mutant spectra, consensus sequences, and data banks. J. Clin. Med. 9:3450
     [Google Scholar]
  88. 88. 
    Domingo E. 2006. Quasispecies: concepts and implications for virology. Curr. Top. Microbiol. Immunol. 299:1–31
     [Google Scholar]
  89. 89. 
    Caldwell HS, Lasek-Nesselquist E, Follano P, Kramer LD, Ciota AT. 2020. Divergent mutational landscapes of consensus and minority genotypes of West Nile virus demonstrate host and gene-specific evolutionary pressures. Genes 11:1299
     [Google Scholar]
  90. 90. 
    Knyazev S, Hughes L, Skums P, Zelikovsky A. 2020. Epidemiological data analysis of viral quasispecies in the next-generation sequencing era. Briefings Bioinform. 22:96–108
     [Google Scholar]
  91. 91. 
    Kennedy DA, Read AF. 2020. Monitor for COVID-19 vaccine resistance evolution during clinical trials. PLOS Biol 18:e3001000
     [Google Scholar]
  92. 92. 
    Holland JJ, Domingo E, de la Torre JC, Steinhauer DA. 1990. Mutation frequencies at defined single codón sites in vesicular stomatitis virus and poliovirus can be increased only slightly by chemical mutagenesis. J. Virol. 64:3960–62
     [Google Scholar]
  93. 93. 
    Loeb LA, Essigmann JM, Kazazi F, Zhang J, Rose KD, Mullins JI 1999. Lethal mutagenesis of HIV with mutagenic nucleoside analogs. PNAS 96:1492–97
     [Google Scholar]
  94. 94. 
    Mullins JI, Heath L, Hughes JP, Kicha J, Styrchak S et al. 2011. Mutation of HIV-1 genomes in a clinical population treated with the mutagenic nucleoside KP1461. PLOS ONE 6:e15135
     [Google Scholar]
  95. 95. 
    Loeb LA. 2011. Human cancers express mutator phenotypes: origin, consequences and targeting. Nat. Rev. Cancer 11:450–57
     [Google Scholar]
  96. 96. 
    Perales C, Gallego I, de Avila AI, Soria ME, Gregori J et al. 2019. The increasing impact of lethal mutagenesis of viruses. Future Med. Chem. 11:1645–57
     [Google Scholar]
  97. 97. 
    Geoghegan JL, Holmes EC. 2018. Evolutionary virology at 40. Genetics 210:1151–62
     [Google Scholar]
  98. 98. 
    Domingo E, Soria ME, Gallego I, de Avila AI, Garcia-Crespo C et al. 2020. A new implication of quasispecies dynamics: broad virus diversification in absence of external perturbations. Infect. Genet. Evol. 82:104278
     [Google Scholar]
  99. 99. 
    Glebova O, Knyazev S, Melnyk A, Artyomenko A, Khudyakov Y et al. 2017. Inference of genetic relatedness between viral quasispecies from sequencing data. BMC Genom 18:918
     [Google Scholar]
  100. 100. 
    Denison MR, Graham RL, Donaldson EF, Eckerle LD, Baric RS. 2011. Coronaviruses: An RNA proofreading machine regulates replication fidelity and diversity. RNA Biol. 8:2270–79
     [Google Scholar]
  101. 101. 
    Trypsteen W, Van Cleemput J, Snippenberg WV, Gerlo S, Vandekerckhove L. 2020. On the whereabouts of SARS-CoV-2 in the human body: a systematic review. PLOS Pathog 16:e1009037
     [Google Scholar]
  102. 102. 
    Weisblum Y, Schmidt F, Zhang F, DaSilva J, Poston D et al. 2020. Escape from neutralizing antibodies by SARS-CoV-2 spike protein variants. eLife 9:e61312
     [Google Scholar]
  103. 103. 
    Karamitros T, Papadopoulou G, Bousali M, Mexias A, Tsiodras S, Mentis A. 2020. SARS-CoV-2 exhibits intra-host genomic plasticity and low-frequency polymorphic quasispecies. J. Clin. Virol. 131:104585
     [Google Scholar]
  104. 104. 
    Capobianchi MR, Rueca M, Messina F, Giombini E, Carletti F et al. 2020. Molecular characterization of SARS-CoV-2 from the first case of COVID-19 in Italy. Clin. Microbiol. Infect. 26:954–56
     [Google Scholar]
  105. 105. 
    Xu D, Zhang Z, Wang FS. 2004. SARS-associated coronavirus quasispecies in individual patients. N. Engl. J. Med. 350:1366–67
     [Google Scholar]
  106. 106. 
    Park D, Huh HJ, Kim YJ, Son DS, Jeon HJ et al. 2016. Analysis of intrapatient heterogeneity uncovers the microevolution of Middle East respiratory syndrome coronavirus. Cold Spring Harb. Mol. Case Stud. 2:a001214
     [Google Scholar]
  107. 107. 
    Jary A, Leducq V, Malet I, Marot S, Klement-Frutos E et al. 2020. Evolution of viral quasispecies during SARS-CoV-2 infection. Clin. Microbiol. Infect. 26:1560.e1–4
     [Google Scholar]
  108. 108. 
    Rueca M, Bartolini B, Gruber CEM, Piralla A, Baldanti F et al. 2020. Compartmentalized replication of SARS-Cov-2 in upper versus lower respiratory tract assessed by whole genome quasispecies analysis. Microorganisms 8:1302
     [Google Scholar]
  109. 109. 
    Shannon A, Selisko B, Le NT, Huchting J, Touret F et al. 2020. Rapid incorporation of favipiravir by the fast and permissive viral RNA polymerase complex results in SARS-CoV-2 lethal mutagenesis. Nat. Commun. 11:4682
     [Google Scholar]
  110. 110. 
    Dong L, Hu S, Gao J. 2020. Discovering drugs to treat coronavirus disease 2019 (COVID-19). Drug Discov. Ther. 14:58–60
     [Google Scholar]
  111. 111. 
    Takahashi H, Iwasaki Y, Watanabe T, Ichinose N, Okada Y et al. 2020. Case studies of SARS-CoV-2 treated with favipiravir among patients in critical or severe condition. Int. J. Infect. Dis. 100:283–85
     [Google Scholar]
  112. 112. 
    Dietzschold B, Wunner WH, Wiktor TJ, Lopes AD, Lafon M et al. 1983. Characterization of an antigenic determinant of the glycoprotein that correlates with pathogenicity of rabies virus. PNAS 80:70–74
     [Google Scholar]
  113. 113. 
    Salvato M, Borrow P, Shimomaye E, Oldstone MB. 1991. Molecular basis of viral persistence: A single amino acid change in the glycoprotein of lymphocytic choriomeningitis virus is associated with suppression of the antiviral cytotoxic T-lymphocyte response and establishment of persistence. J. Virol. 65:1863–69
     [Google Scholar]
  114. 114. 
    Sitbon M, d'Auriol L, Ellerbrok H, Andre C, Nishio J et al. 1991. Substitution of leucine for isoleucine in a sequence highly conserved among retroviral envelope surface glycoproteins attenuates the lytic effect of the Friend murine leukemia virus. PNAS 88:5932–36
     [Google Scholar]
  115. 115. 
    Bae YS, Yoon JW. 1993. Determination of diabetogenicity attributable to a single amino acid, Ala776, on the polyprotein of encephalomyocarditis virus. Diabetes 42:435–43
     [Google Scholar]
  116. 116. 
    Holzmann H, Stiasny K, Ecker M, Kunz C, Heinz FX. 1997. Characterization of monoclonal antibody-escape mutants of tick-borne encephalitis virus with reduced neuroinvasiveness in mice. J. Gen. Virol. 78:131–37
     [Google Scholar]
  117. 117. 
    Núñez JI, Baranowski E, Molina N, Ruiz-Jarabo CM, Sánchez C et al. 2001. A single amino acid substitution in nonstructural protein 3A can mediate adaptation of foot-and-mouth disease virus to the guinea pig. J. Virol. 75:3977–83
     [Google Scholar]
  118. 118. 
    Nakano Y, Yamamoto K, Ueda MT, Soper A, Konno Y et al. 2020. A role for gorilla APOBEC3G in shaping lentivirus evolution including transmission to humans. PLOS Pathog 16:e1008812
     [Google Scholar]
/content/journals/10.1146/annurev-virology-091919-105900
Loading
Historical Perspective on the Discovery of the Quasispecies Concept
Annual Review of Virology 8, 51 (2021); https://doi.org/10.1146/annurev-virology-091919-105900
/content/journals/10.1146/annurev-virology-091919-105900
/content/journals/10.1146/annurev-virology-091919-105900
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error