Chapter 23 : Error Frequencies of Picornavirus RNA Polymerases: Evolutionary Implications for Virus Populations

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Error Frequencies of Picornavirus RNA Polymerases: Evolutionary Implications for Virus Populations, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817916/9781555812102_Chap23-1.gif /docserver/preview/fulltext/10.1128/9781555817916/9781555812102_Chap23-2.gif


This chapter examines key features of the three main stages in virus evolution with examples drawn from several virus groups. It then reviews specific results with picornaviruses, as well as implications of high mutation rates and quasispecies dynamics for this important and diverse group of pathogens. With the levels of heterogeneity and viral load often seen in infected individuals, RNA virus populations include potentially all possible single mutants and decreasing amounts of multiple mutants. There are probably many routes to drug resistance, including amino acid replacements in the wall of the pocket preventing accommodation of the drug into the pocket (termed "exclusion" mutants), and replacements elsewhere in the capsid that affect viral uncoating. Resistant mutants display decreased affinity for the drug or increased affinity for the receptor, and often show low fitness values relative to their parental counterparts. Studies with picornaviral RNA-dependent RNA polymerases (replicases) face limitations derived from the difficulties in obtaining purified enzymes capable of sustaining multiple rounds of template-dependent copying. Viral quasispecies show features of complex adaptive systems such as mobilization of minority components (individual genomes from the mutant spectrum) in response to external stimuli. New developments in biochemistry and structural biology, and a deeper understanding of the principles governing viral evolution can now be combined to produce practical developments following an extensive (and necessary) accumulation of results from basic research.

Citation: Domingo E, Baranowski E, Escarmís C, Sobrino F, Holland J. 2002. Error Frequencies of Picornavirus RNA Polymerases: Evolutionary Implications for Virus Populations, p 285-298. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch23
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


1. Ahmad, A., L, A. B. Dowsett,, and D. A. Tyrrell. 1987. Studies of rhinovirus resistant to an antiviral chalcone. Antiviral Res. 8: 27 39.
2. Albiach-Marti, M. R.,, M. Mawassi,, S. Gowda,, T. Satyanarayana,, M. E. Hilf,, S. Shanker,, E. C. Almira,, M. C. Vives,, C. Lopez,, J. Guerri,, R. Flores,, P. Moreno,, S. M. Garnsey,, and W. O. Dawson. 2000. Sequences of Citrus Tristeza Virus separated in time and space are essentially identical. J. Virol. 74: 6856 6865.
3. Anderson-Sillman, K.,, S. Bartal,, and D. R. Tershak. 1984. Guanidine-resistant poliovirus mutants produce modified 37-kilodalton proteins. J. Virol. 50: 922 928.
3a. Arias, A. E. Lázaro,, C. Escarmís,, and E. Domingo. 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.
4. Arion, D.,, N. Kaushik,, S. McCormick,, G. Borkow,, and M. A. Parniak. 1998. Phenotypic mechanism of HIV-1 resistance to 3'-azido-3'-deoxythymidine (AZT): increased polymerization processivity and enhanced sensitivity to pyrophosphate of the mutant viral reverse transcriptase. Biochemistry 37: 15908 15917.
5. Arnold, J. J.,, and C. E. Cameron. 2000. Poliovirus RNA-dependent RNA polymerase 3D pol). Assembly of stable, elongation-competent complexes by using a symmetrical primer-template substrate (sym/sub). J. Biol. Chem. 275: 5329 5336.
6. Arnold, J. J.,, S. K. Ghosh,, and C. E. Cameron. 1999. Poliovirus RNA-dependent RNA polymerase (3Dpol). Divalent cation modulation of primer, template, and nucleotide selection. J. Biol. Chem. 274: 37060 37069.
7. Arts, E. J.,, and S. F. Le Grice. 1998. Interaction of retroviral reverse transcriptase with template-primer duplexes during replication. Prog. Nucleic Acid Res. Mol. Biol. 58: 339 393.
8. Bae, Y. S.,, and J. W. Yoon. 1993. Determination of diabetogenicity attributable to a single amino acid, Ala776, on the polyprotein of encephalomyocarditis virus. Diabetes 42: 435 443.
9. Bailly, J. L.,, M. Chambon,, C. Henquell,, J. Icart,, and H. Peigue-Lafeuille. 2000. Genomic variations in echovirus 30 persistent isolates recovered from a chronically infected immunodeficient child and comparison with the reference strain. J. Clin. Microbiol. 38: 552 557.
9a. Baranowski, E.,, C. M. Ruiz-Jarabo,, and E. Domingo. 2001. Evolution of cell recognition by viruses. Science 292: 1102 1105.
10. Baranowski, E.,, C. M. Ruíz-Jarabo,, N. Sevilla,, D. Andreu,, E. Beck,, and E. Domingo. 2000. Cell recognition by foot-and-mouth disease virus that lacks the RGD integrin-binding motif: flexibility in aphthovirus receptor usage. J. Virol. 74: 1641 1647.
11. Batschelet, E.,, E. Domingo,, and C. Weissmann. 1976. The proportion of revertant and mutant phage in a growing population, as a function of mutation and growth rate. Gene 1: 27 32.
12. Beard, C. W.,, and P. W. Mason. 2000. Genetic determinants of altered virulence of Taiwanese foot-and-mouth disease virus. J. Virol. 74: 987 991.
13. Bebenek, K.,, and T. A. Kunkel,. 1993. The fidelity ofretroviral reverse transcriptases, p. 85 102. In A. M. Skalka, and S. P. Goff (ed.), Reverse Transcriptase. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
14. Beck, E.,, and K. Strohmaier. 1987. Subtyping of European foot-and-mouth disease virus strains by nucleotide sequence determination. J. Virol. 61: 1621 1629.
15. Beck, M. A.,, and O. A. Levander. 1997. Effects of nutritional antioxidants and other dietary constituents on coxsackievirus-induced myocarditis. Curr. Top. Microbiol. Immunol. 223: 81 96.
16. Beck, M. A.,, and O. A. Levander. 1995. Rapid genomic evolution of a non-virulent coxsackievirus B3 in selenium-deficient mice results in selection of identical virulent isolates. Nat. Med. 1: 433 436.
17. Bellmunt, A.,, G. May,, R. Zell,, P. Pring-Akerblom,, W. Verhagen,, and A. Heim. 1999. Evolution of poliovirus type I during 5.5 years of prolonged enteral replication in an immunodeficient patient. Virology 265: 178 184.
18. Belnap, D.M.,, B. M. McDermott, Jr.,, D. J. Filman,, N. Cheng,, B. L. Trus,, H. J. Zuccola,, V. R. Racaniello,, J. M. Hogle,, and A. C. Steven. 2000. Three-dimensional structure of poliovirus receptor bound to poliovirus. Proc. Natl. Acad. Sci. USA 97: 73 78.
19. Bernad, A.,, L. Blanco,, J. M. Lazaro,, G. Martin,, and M. Salas. 1989. A conserved 3' → 5' exonuclease active site in prokaryotic and eukaryotic DNA polymerases. Cell 59: 219 228.
20. Biebricher, C.K., 1999. Mutation, competition and selectionas measured with small RNA molecules, p. 65 85. In E. Domingo,, R. G. Webster,, and J. J. Holland (ed.), Origin and Evolution of Viruses. Academic Press, San Diego, Calif.
21. Boege, U.,, D. Kobasa,, S. Onodera,, G. D. Parks,, A. C. Palmenberg,, and D. G. Scraba. 1991. Characterization of mengo virus neutralization epitopes. Virology 181: 1 13.
22. Borrego, B.,, I. S. Novella,, E. Giralt,, D. Andreu,, and E. Domingo. 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.
23. Boyer, J. C.,, K. Bebenek,, and T. A. Kunkel. 1996. Analyzing the fidelity of reverse transcription and transcription. Methods Enzymol. 275: 523 537.
24. Brown, B.A.,, M. S. Oberste,, J. P. Alexander, Jr.,, M. L. Kennett,, and M. A. Pallansch. 1999. Molecular epidemiology and evolution of enterovirus 71 strains isolated from 1970 to 1998. J. Virol. 73: 9969 9975.
25. Caggana, M.,, P. Chan,, and A. Ramsingh. 1993. Identification of a single amino acid residue in the capsid protein VP1 of coxsackievirus B4 that determines the virulent phenotype. J. Virol. 67: 4797 4803.
26. Carrillo, C.,, M. Borca,, D. M. Moore,, D. O. Morgan,, and F. Sobrino. 1998. In vivo analysis of the stability and fitness of variants recovered from foot-and-mouth disease virus quasispecies. J. Gen. Virol. 79: 1699 1706.
27. Carrillo, C.,, J. Plana,, R. Mascarella,, J. Bergada,, and F. Sobrino. 1990. Genetic and phenotypic variability during replication of foot-and-mouth disease virus in swine. Virology 179: 890 892.
28. Chao, L. 1990. Fitness of RNA virus decreased by Muller's ratchet. Nature 348: 454 455.
29. Chapman, N. M.,, A. I. Ramsingh,, and S. Tracy. 1997. Genetics of coxsackievirus virulence. Curr. Top. Microbiol. Immunol. 223: 227 258.
30. Chumakov, K. M.,, L. B. Powers,, K. E. Noonan,, I. B. Roninson,, and I. S. Levenbook. 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.
31. Clarke, D. K.,, E. A. Duarte,, A. Moya,, S. F. Elena,, E. Domingo,, and J. Holland. 1993. Genetic bottlenecks and population passages cause profound fitness differences in RNA viruses. J. Virol. 67: 222 228.
32. Cowan, G. A.,, D. Pines,, and D. Meitzer (ed.). 1994. Complexity. Metaphors, Models and Reality. Addison-Wesley Publishing Company, Reading, Mass.
32a.. Crotty, S.,, C. E. Cameron,, and R. Andino. 2001. RNA virus error catastrophe: direct molecular test by using ribavirin. Proc. Natl. Acad. Sci. USA 98: 6895 6900.
33. Crotty, S.,, D. Maag,, J. J. Arnold,, W. Zhong,, J. Y,. N. Lau,, Z. Hong,, R. Andino,, and C. E. Cameron. The broad-spectrum antiviral ribonucleotide, ribavirin, is an RNA virus mutagen. Nat. Med., in press.
34. Dasgupta, A.,, M. H. Baron,, and D. Baltimore. 1979. Poliovirus replicase: a soluble enzyme able to initiate copying of poliovirus RNA. Proc. Natl. Acad. Sci. USA 76: 2679 2683.
35. Dearden, C.,, W. al-Nakib,, K. Andries,, R. Woestenborghs,, and D. A. Tyrrell. 1989. Drug resistant rhinoviruses from the nose of experimentally treated volunteers. Arch. Virol. 109: 71 81.
36. de la Torre, J. C.,, M. Davila,, F. Sobrino,, J. Ortín,, and E. Domingo. 1985. Establishment of cell lines persistently infected with foot-and-mouth disease virus. Virology 145: 24 35.
37. de la Torre, J. C.,, C. Giachetti,, B. L. Semler,, and J. J. Holland. 1992. High frequency of single-base transitions and extreme frequency of precise multiple-base reversion mutations in poliovirus. Proc. Natl. Acad. Sci. USA 89: 2531 2535.
38. de la Torre, J. C.,, E. Martínez-Salas,, J. Diez,, A. Villaverde,, F. Gebauer,, E. Rocha,, M. Dávila,, and E. Domingo. 1988. Coevolution of cells and viruses in a persistent infection of foot-and-mouth disease virus in cell culture. J. Virol. 62: 2050 2058.
39. de la Torre, J. C.,, E. Wimmer,, and J. J. Holland. 1990. Very high frequency of reversion to guanidine resistance in clonal pools of guanidine-dependent type 1 poliovirus. J. Virol. 64: 664 671.
40. Díez, J.,, M. Dávila,, C. Escarmís,, M. G. Mateu,, J. Dominguez,, J. J. Pérez,, E. Giralt,, J. A. Melero,, and E. Domingo. 1990. Unique amino acid substitutions in the capsid proteins of foot-and-mouth disease virus from a persistent infection in cell culture. J. Virol. 64: 5519 5528.
41. Díez, J.,, M. G. Mateu,, and E. Domingo. 1989. Selection of antigenic variants of foot-and-mouth disease virus in the absence of antibodies, as revealed by an in situ assay. J. Gen. Virol. 70: 3281 3289.
42. Domingo, E., 1999. Quasispecies, p. 1431 1436. In A. Granoff, and R. G. Webster (ed.), Encyclopedia of Virology. Academic Press, London, United Kingdom.
43. Domingo, E. 1989. RNA virus evolution and the control of viral disease. Prog. Drug Res. 33: 93 133.
44. Domingo, E., 1999. RNA virus quasispecies as models of biological complexity, p. 79 90. In R. A. Dixon,, M. J. Harrison,, and M. J. Roossinck (ed.), Proceedings 10th Anniversary Symposium. The Samuel Roberts Noble Foundation, Plant Biology Division. The Samuel Roberts Foundation, Ardmore, Okla.
45. Domingo, E.,, C. Biebricher,, M. Eigen,, and J. J. Holland. 2001. Quasispecies and RNA Virus Evolution: Principles and Consequences. Landes Bioscience, Austin, Tex.
46. Domingo, E.,, J. Díez,, M. A. Martínez,, J. Hernández,, A. Holguín,, B. Borrego,, and M. G. Mateu. 1993. New observations on antigenic diversification of RNA viruses. Antigenic variation is not dependent on immune selection. J. Gen. Virol. 74: 2039 2045.
47. Domingo, E.,, C. Escarmís,, L. Menéndez-Arias,, and J. J. Holland,. 1999. Viral quasispecies and fitness variations, p. 141 161. In E. Domingo,, R. G. Webster,, and J. J. Holland (ed.), Origin and Evolution of Viruses. Academic Press, San Diego, Calif.
48. Domingo, E.,, and J. J. Holland,. 1994. Mutation rates and rapid evolution of RNA viruses, p. 161 184. In S. S. Morse (ed.), Evolutionary Biology of Viruses. Raven Press, New York, N.Y.
49. Domingo, E.,, D. Sabo,, T. Taniguchi,, and C. Weissmann. 1978. Nucleotide sequence heterogeneity of an RNA phage population. Cell 13: 735 744.
50. Domingo, E.,, R. G. Webster,, and J. J. Holland (ed.). 1999. Origin and Evolution of Viruses. Academic Press, San Diego, Calif.
51. Drake, J. W. 1969. Comparative rates of spontaneous mutation. Nature 221: 1132.
52. Drake, J. W. 1991. A constant rate of spontaneous mutation in DNA-based microbes. Proc. Natl. Acad. Sci. USA 88: 7160 7164.
53. Drake, J. W.,, and J. J. Holland. 1999. Mutation rates among RNA viruses. Proc. Natl. Acad. Sci. USA 96: 13910 13913.
54. Duarte, E.,, D. Clarke,, A. Moya,, E. Domingo,, and J. Holland. 1992. Rapid fitness losses in mammalian RNA virus clones due to Muller's ratchet. Proc. Natl. Acad. Sci. USA 89: 6015 6019.
55. Duarte, E. A.,, D. K. Clarke,, A. Moya,, S. F. Elena,, E. Domingo,, and J. Holland. 1993. Many-trillionfold amplification of single RNA virus particles fails to overcome the Muller's ratchet effect. J. Virol. 67: 3620 3623.
56. Eggers, H. J.,, and I. Tamm. 1965. Coxsackie A9 virus: mutation from drug dependence to drug independence. Science 148: 97 98.
57. Eigen, M. 1996. On the nature of virus quasispecies. Trends Microbiol. 4: 216 218.
58. Eigen, M. 1971. Self-organization of matter and the evolution of biological macromolecules. Naturwissenschaften 58: 465 523.
59. Eigen, M.,, and C. K. Biebricher,. 1988. Sequence space and quasispecies distribution, p. 211 245. In E. Domingo,, P. Ahlquist,, and J. J. Holland (ed.), RNA Genetics, vol. 3. CRC Press, Boca Raton, Fla.
60. Elena, S. F.,, F. González-Candelas,, I. S. Novella,, E. A. Duarte,, D. K. Clarke,, E. Domingo,, J. J. Holland,, and A. Moya. 1996. Evolution of fitness in experimental populations of vesicular stomatitis virus. Genetics 142: 673 679.
61. Emini, E. A.,, B. A. Jameson,, A. J. Lewis,, G. R. Larsen,, and E. Wimmer. 1982. Poliovirus neutralization epitopes: analysis and localization with neutralizing monoclonal antibodies. J. Virol. 43: 997 1005.
62. Escarmís, C.,, E. C. Carrillo,, M. Ferrer,, J. F. Arriaza,, N. Lopez,, C. Tami,, N. Verdaguer,, E. Domingo,, and M. T. Franze-Fernández. 1998. Rapid selection in modified BHK-21 cells of a foot-and-mouth disease virus variant showing alterations in cell tropism. J. Virol. 72: 10171 10179.
63. Escarmís, C.,, M. Dávila,, N. Charpentier,, A. Bracho,, A. Moya,, and E. Domingo. 1996. Genetic lesions associated with Muller's ratchet in an RNA virus. J. Mol. Biol. 264: 255 267.
64. Escarmís, C.,, M. Dávila,, and E. Domingo. 1999. Multiple molecular pathways for fitness recovery of an RNA virus debilitated by operation of Muller's ratchet. J. Mol. Biol. 285: 495 505.
65. Evans, D. J.,, and J. W. Almond. 1998. Cell receptors for picornaviruses as determinants of cell tropism and pathogenesis. Trends Microbiol. 6: 198 202.
66. Farci, P.,, A. Shimoda,, A. Coiana,, G. Diaz,, G. Peddis,, J. C. Melpolder,, A. Strazzera,, D. Y. Chien,, S. J. Munoz,, A. Balestrieri,, R. H. Purcell,, and H. J. Alter. 2000. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 288: 339 344.
67. Flanegan, J. B.,, and D. Baltimore. 1977. Poliovirus-specific primer-dependent RNA polymerase able to copy poly(A). Proc. Natl. Acad. Sci. USA 74: 3677 3680.
68. Flanegan, J. B.,, and T. A. Van Dyke. 1979. Isolation of a soluble and template-dependent poliovirus RNA polymerase that copies virion RNA in vitro. J. Virol. 32: 155 161.
69. Flint, S. J.,, L. W. Enquist,, R. M. Krug,, V. R. Racaniello,, and A. M. Skalka. 2000. Virology. Molecular Biology, Pathogenesis and Control. ASM Press, Washington, D.C.
70. Forns, X.,, R. H. Purcell,, and J. Bukh. 1999. Quasispecies in viral persistence and pathogenesis of hepatitis C virus. Trends Microbiol. 7: 402 410.
71. Fox, M. P.,, M. J. Otto,, and M. A. McKinlay. 1986. The prevention of rhinovirus and poliovirus uncoating by WIN 51711: a new antiviral drug. Antimicrob. Agents Chemother. 30: 110 116.
72. Fry, E. E.,, S. M. Lea,, T. Jackson,, J. W. Newman,, F. M. Ellard,, W. E. Blakemore,, R. Abu-Ghazaleh,, A. Samuel,, A. M. King,, and D. I. Stuart. 1999. The structure and function of a foot-and-mouth disease virus-oligosaccharide receptor complex. EMBO J. 18: 543 554.
73. Gauntt, C. J. 1997. Roles of the humoral response in coxsackievirus B-induced disease. Curr. Top. Microbiol. Immunol. 223: 259 282.
74. Gavrilin, G. V.,, E. A. Cherkasova,, G. Y. Lipskaya,, O. M. Kew,, and V. I. Agol. 2000. Evolution of circulating wild poliovirus and of vaccine-derived poliovirus in an immunodeficient patient: a unifying model. J. Virol. 74: 7381 7390.
75. Gebauer, F.,, J. C. de la Torre,, I. Gomes,, M. G. Mateu,, H. Barahona,, B. Tiraboschi,, I. Bergmann,, P. A. de Mello,, and E. Domingo. 1988. Rapid selection of genetic and antigenic variants of foot-and-mouth disease virus during persistence in cattle. J. Virol. 62: 2041 2049.
76. Gell-Mann, M. 1994. The Quark and the Jaguar. Freeman, New York, N.Y.
77. Gibbs, A.,, C. Calisher,, and F. García-Arenal (ed.). 1995. Molecular Basis of Virus Evolution. Cambridge University Press, Cambridge, United Kingdom.
78. Giraudo, A. T.,, E. Beck,, K. Strebel,, P. A. de Mello,, J. L. La Torre,, E. A. Scodeller,, and I. E. Bergmann. 1990. Identification of a nucleotide deletion in parts of polypeptide 3A in two independent attenuated aphthovirus strains. Virology 177: 780 783.
79. Gohara, D. W.,, S. Crotty,, J. J. Arnold,, J. D. Yoder,, R. Andino,, and C. E. Cameron. 2000. Poliovirus RNA-dependent RNA polymerase (3D pol). Structural, biochemical, and biological analysis of conserved structural motifs A and B. J. Biol. Chem. 275: 25523 25532.
80. González, M. J.,, J. C. Sáiz,, O. Laor,, and D. M. Moore. 1981. Antigenic stability of foot-and-mouth disease virus variants on serial passage in cell culture. J. Virol. 65: 3949 3953.
81. Goodman, M. F.,, and K. D. Fygenson. 1998. DNA polymerase fidelity: from Genetics toward a biochemical understanding. Genetics 148: 1475 1482.
82. Gromeier, M.,, E. Wimmer,, and A. E. Gorbalenya,. 1999. Genetics, pathogenesis and evolution of picornaviruses, p. 287 343. In E. Domingo,, R. G. Webster,, and J. J. Holland (ed.), Origin and Evolution of Viruses. Academic Press, San Diego, Calif.
83. Hadfield, A. T.,, M. A. Oliveira,, K. H. Kim,, P. Minor,, M. Kremer,, B. A. Heinz,, D. Shepard,, D. C. Pevear,, R. R. Rueckert,, and M. G. Rossmann. 1995. Structural studies on human rhinovirus 14 drug-resistant compensation mutants. J. Mol. Biol. 253: 61 73.
84. Hansen, J.,, A. M. Long,, and S. Schultz. 1997. Structure of the RNA-dependent RNA polymerase of poliovirus. Structure 15: 1109 1122.
85. Harber, J.,, G. Bernhardt,, H. H. Lu,, J. Y. Sgro,, and E. Wimmer. 1995. Canyon rim residues, including antigenic determinants, modulate serotype-specific binding of polioviruses to mutants of the poliovirus receptor. Virology 214: 559 570.
86. He, Y.,, V. D. Bowman,, S. Mueller,, C. M. Bator,, J. Bella,, X. Peng,, T. S. Baker,, E. Wimmer,, R. J. Kuhn,, and M. G. Rossmann. 2000. Interaction of the poliovirus receptor with poliovirus. Proc. Natl. Acad. Sci. USA 97: 79 84.
87. Heinz, B. A.,, R. R. Rueckert,, D. A. Shepard,, F. J. Dutko,, M. A. McKinlay,, M. Fancher,, M. G. Rossmann,, J. Badger,, and T. J. Smith. 1989. Genetic and molecular analyses of spontaneous mutants of human rhinovirus 14 that are resistant to an antiviral compound. J. Virol. 63: 2476 2485.
88. Hernández, J.,, M. A. Martínez,, E. Rocha,, E. Domingo,, and M. G. Mateu. 1992. Generation of a subtype-specific neutralization epitope in foot-and-mouth disease virus of a different subtype. J. Gen. Virol. 73: 213 216.
89. Hewat, E. A.,, N. Verdaguer,, I. Fita,, W. Blakemore,, S. Brookes,, A. King,, J. Newman,, E. Domingo,, M. G. Mateu,, and D. I. Stuart. 1997. Structure of the complex of an Fab fragment of a neutralizing antibody with foot-and-mouth disease virus: positioning of a highly mobile antigenic loop. EMBO J. 16: 1492 1500.
90. Hirasawa, K.,, H. S. Jun,, H. S. Han,, M. L. Zhang,, M. D. Hollenberg,, and J. W. Yoon. 1999. Prevention of encephalomyocarditis virus-induced diabetes in mice by inhibition of the tyrosine kinase signalling pathway and subsequent suppression of nitric oxide production in macrophages. J. Virol. 73: 8541 8548.
91. Holland, J.,, K. Spindler,, F. Horodyski,, E. Grabau,, S. Nichol,, and S. VandePol. 1982. Rapid evolution of RNA genomes. Science 215: 1577 1585.
92. Holland, J. J. (ed.). 1992. Genetic diversity of RNA viruses. Curr. Top. Microbiol. Immunol., vol. 176.
93. Holland, J. J.,, J. C. de la Torre,, D. K. Clarke,, and E. Duarte. 1991. Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses. J. Virol. 65: 2960 2967.
94. Holland, J. J.,, J. C. de La Torre,, and D. A. Steinhauer. 1992. RNA virus populations as quasispecies. Curr. Top. Microbiol. Immunol. 176: 1 20.
95. Holland, J. J.,, J. C. de la Torre,, D. A. Steinhauer,, D. Clarke,, E. Duarte,, and E. Domingo. 1989. Virus mutation frequencies can be greatly underestimated by monoclonal antibody neutralization of virions. J. Virol. 63: 5030 5036.
96. Holland, J. J.,, E. Domingo,, J. C. de la Torre,, and D. A. Steinhauer. 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.
97. Hyypiä, T.,, T. Hovi,, N. J. Knowles,, and G. Stanway. 1997. Classification of enteroviruses based on molecular and biological properties. J. Gen. Virol. 78: 1 11.
98. Jackson, T.,, F. M. Ellard,, R. A. Ghazaleh,, S. M. Brookes,, W. E. Blakemore,, A. H. Corteyn,, D. I. Stuart,, J. W. Newman,, and A. M. King. 1996. Efficient infection of cells in culture by type O foot-and-mouth disease virus requires binding to cell surface heparan sulfate. J. Virol. 70: 5282 5287.
99. Jnaoui, K.,, and T. Middels. 1998. Adaptation of Theiler's virus to L929 cells: mutations in the putative receptor binding site on the capsid map to neutralization sites and modulate viral persistence. Virology 244: 397 404.
100. Kew, O. M.,, R. W. Sutter,, B. K. Nottay,, M. J. McDenough,, R. Prevots,, L. Quick,, and M. A. Pallansch. 1995. Molecular epidemiology of poliovirus. Semin. Virol. 6: 401 414.
100a.. Kew, O.,, V. Morris-Glasgow,, M. Landaverde,, C. Burns,, J. Shaw,, Z. Garib,, J. Andre,, E. Blackman,, C. J. Freeman,, J. Jorba,, R. Sutter,, G. Tambini,, L. Venczel,, C. Perdreira,, F. Laender,, H. Shimizu,, T. Yoneyama,, T. Miyamura,, H. van der Avoort,, M. S. Oberste,, D. Kilpatrick,, S. Cochi,, M. Pallansch,, and C. de Quadros. 2002. Outbreak of poliomyelitis in Hispaniola associated with circulating type 1 vaccine-derived poliovirus. Science 296: 356 359.
101. Kew, O. M.,, R. W. Sutter,, B. K Nottay,, M. J. McDonough,, D. R. Prevots,, L. Quick,, and M. A. Pallansch. 1998. Prolonged replication of a type 1 vaccine-derived poliovirus in an immunodeficient patient. J. Clin. Microbiol. 36: 2893 2899.
102. Kilbourne, E. D., 1994. Host determination of viral evolution: a variable tautology, p. 253 271. In S. S. Morse (ed.), The Evolutionary Biology of Viruses. Raven Press, New York, N.Y.
103. King, A. M.,, D. McCahon,, W. R. Slade,, and J. W. Newman. 1982. Recombination in RNA. Cell 29: 921 928.
104. Kolatkar, P. R.,, J. Bella,, N. H. Olson,, C. M. Bator,, T. S. Baker,, and M. G. Rossmann. 1999. Structural studies of two rhinovirus serotypes complexed with fragments of their cellular receptor. EMBO J. 18: 6249 6259.
105. Kuge, S.,, N. Kawamura,, and A. Nomoto. 1989. Strong inclination toward transition mutation in nucleotide substitutions by poliovirus replicase. J. Mol. Biol. 207: 175 182.
106. Lai, M. M. C., 1995. Recombination and its evolutionary effects on viruses with RNA genomes, p. 119 132. In A. Gibbs (ed.), Molecular Basis of Virus Evolution. Cambridge University Press, Cambridge, United Kingdom.
107. Lea, S.,, J. Hernández,, W. Blakemore,, E. Brocchi,, S. Curry,, E. Domingo,, E. Fry,, R. Abu-Ghazaleh,, A. King,, J. Newman,, D. Stuart,, and M. G. Mateu. 1994. The structure and antigenicity of a type C foot-and-mouth disease virus. Structure 2: 123 139.
108. Ledinko, N. 1963. Genetic recombination with poliovirus type 1. Studies of crosses between a normal horse serum-resistant mutant and several guanidine-resistant mutants of the same strain. Virology 20: 107 119.
109. Lemon, S. M.,, L. Whetter,, K. H. Chang,, and E. A. Brown. 1992. Why do human hepatitis viruses replicate so poorly in cell cultures? FEMS Microbiol. Lett. 79: 455 459.
110. Li, F.,, G. F. Browning,, M. J. Studdert,, and B. S. Crabb. 1996. Equine rhinovirus 1 is more closely related to foot-and-mouth disease virus than to other picornaviruses. Proc. Natl. Acad. Sci. USA 93: 990 995.
111. Liao, S.,, and V. Racaniello. 1997. Allele-specific adaptation of poliovirus VP1 B-C loop variants to mutant cell receptors. J. Virol. 71: 9770 9777.
112. Loeb, L. A., , J. M. Essigmann,, F. Kazazi,, J. Zhang,, K. D. Rose,, and J. I. Mullins. 1999. Lethal mutagenesis of HIV with mutagenic nucleoside analogs. Proc. Natl. Acad. Sci. USA 96: 1492 1497.
113. Loeb, L. A., , and J. I. Mullins. 2000. Lethal mutagenesis of HIV by mutagenic ribonucleoside analogs. AIDS Res. Hum. Retrovir. 13: 1 3.
114. Mansky, L. M. 1996. The mutation rate of human immunodeficiency virus type 1 is influenced by the vpr gene. Virology 222: 391 400.
115. Mansky, L. M.,, S. Preveral,, L. Selig,, R. Benarous,, and S. Benichou. 2000. The interaction of Vpr with uracil DNA glycosylase modulates the human immunodeficiency virus type 1 in vivo mutation rate. J. Virol. 74: 7039 7047.
116. Martin, B., 1994 The schema, p. 263 285. In G. A. Cowan,, D. Pines,, and D. Meitzer (ed.), Complexity. Metaphors, Models and Reality. Addison Wesley Publishing Co., Reading, Mass.
117. Martin, J.,, G. Dunn,, R. Hull,, V. Patel,, and P. D. Minor. 2000. Evolution of the Sabin strain of type 3 poliovirus in an immunodeficient patient during the entire 637-day period of virus excretion. J. Virol. 74: 3001 3010.
118. Martínez, M. A.,, C. Carrillo,, F. González-Candelas,, A. Moya,, E. Domingo,, and F. Sobrino. 1991. Fitness alteration of foot-and-mouth disease virus mutants: measurement of adaptability of viral quasispecies. J. Virol. 65: 3954 3957.
119. Martínez, M. A.,, N. Verdaguer,, M. G. Mateu,, and E. Domingo. 1997. Evolution subverting essentiality: dispensability of the cell attachment Arg-Gly-Asp motif in multiply passaged foot-and-mouth disease virus. Proc. Natl. Acad. Sci. USA 94: 6798 6802.
120. Martínez-Salas, E.,, J. Ortín,, and E. Domingo. 1985. Sequence of the viral replicase gene from foot-and-mouth disease virus Cl-Santa Pau (C-S8). Gene 35: 55 61.
121. Martin-Hernández, A. M.,, E. Domingo,, and L. Menéndez-Arias. 1996. Human immunodeficiency virus type 1 reverse transcriptase: role of Tyr115 in deoxynucleotide binding and misinsertion fidelity of DNA synthesis. EMBO J. 15: 4434 4442.
122. Marvil, P.,, N. J. Knowles,, A. P. Mockett,, P. Britton,, T. D. Brown,, and D. Cavanagh. 1999. Avian encephalomyelitis virus is a Picornavirus and is most closely related to hepatitis A virus. J. Gen. Virol. 80: 653 662.
123. Mas, A.,, M. Parera,, C. Briones,, V. Soriano,, M. A. Martínez,, E. Domingo,, and L. Menéndez-Arias. 2000. Role of a dipeptide insertion between codons 69-70 of HIV-1 reverse transcriptase in the mechanism of AZT resistance. EMBO J. 19: 5752 5761.
124. Mateu, M. G. 1995. Antibody recognition of picornaviruses and escape from neutralization: a structural view. Virus Res. 38: 1 24.
125. Mateu, M. G.,, C. Escarmís,, and E. Domingo. 1998. Mutational analysis of discontinuous epitopes of foot-and-mouth disease virus using an unprocessed capsid pro-tomer precursor. Virus Res. 53: 27 37.
126. Melnick, J. L.,, D. Crowther,, and J. Barrera-Oro. 1961. Rapid development of drug-resistant mutants of poliovirus. Science 134: 557.
127. Meyer, P. R.,, S. E. Matsuura,, A. M. Mian,, A. G. So,, and W. A. Scott. 1999. A mechanism of AZT resistance: an increase in nucleotide-dependent primer unblocking by mutant HIV-1 reverse transcriptase. Mol. Cell 4: 35 43.
128. Meyerhans, A.,, and J.-P. Vartanian,. 1999. The fidelity of cellular and viral polymerases and its manipulation for hypermutagenesis, p. 87 114. In E. Domingo,, R. G. Webster,, and J. J. Holland (ed.), Origin and Evolution of Viruses. Academic Press, San Diego, Calif.
129. Minor, P. D. 1992. The molecular biology of poliovaccines. J. Gen. Virol. 73: 3065 3077.
130. Minor, P. D.,, M. Ferguson,, D. M. Evans,, J. W. Almond,, and J. P. Icenogle. 1986. Antigenic structure of polioviruses of serotypes 1, 2 and 3. J. Gen. Virol. 67: 1283 1291.
131. Minor, P. D.,, G. C. Schild,, J. Bootman,, D. M. Evans,, M. Ferguson,, P. Reeve,, M. Spitz,, G. Stanway,, A. J. Cann,, R. Hauptmann,, L. D. Clarke,, R. C. Mountford,, and J. W. Almond. 1983. Location and primary structure of a major antigenic site for poliovirus neutralization. Nature 301: 674 679.
132. Misbah, S. A., , G. P. Spickett,, P. C. Ryba,, J. M. Hockaday,, J. S. Kroll,, C. Sherwood,, J. B. Kurtz,, E. R. Moxon,, and H. M. Chapel. 1992. Chronic enteroviral meningoencephalitis in agammaglobulinemia: case report and literature review. J. Clin. Immunol. 12: 266 270.
133. Morse, S. S. (ed.). 1993. Emerging Viruses. Oxford University Press, Oxford, United Kingdom.
134. Morse, S. S. (ed.). 1994. The Evolutionary Biology of Viruses. Raven Press, New York, N.Y.
135. Mosser, A. G.,, and R. R. Rueckert,. 1996. Capsid-binding agents, p. 13 40. In D. D. Richman (ed.), Antiviral Drug Resistance. John Wiley and Sons Ltd., Chichester, United Kingdom.
136. Mosser, A. G.,, J. Y. Sgro,, and R. R. Rueckert. 1994. Distribution of drug resistance mutations in type 3 poliovirus identifies three regions involved in uncoating functions. J. Virol. 68: 8193 8201.
137. Murphy, F. A.,, and N. Nathanson. 1994. The emergence of new virus diseases: an overview. Semin. Virol. 5: 87 102.
138. Nagy, P. D.,, and A. E. Simon. 1997. New insights into the mechanisms of RNA recombination. Virology 235: 1 9.
139. Nájera, I.,, A. Holguín,, M. E. Quiñones-Mateu,, M. A. Muñoz-Fernández,, R. Nájera,, C. López-Galíndez,, and E. Domingo. 1995. Pol gene quasispecies of human immunodeficiency virus: mutations associated with drug resistance in virus from patients undergoing no drug therapy. J. Virol. 69: 23 31.
140. Nomoto, A.,, T. Omata,, H. Toyoda,, S. Kuge,, H. Horie,, Y. Kataoka,, Y. Genba,, Y. Nakano,, and N. Imura. 1982. Complete nucleotide sequence of the attenuated poliovirus Sabin 1 strain genome. Proc. Natl. Acad. Sci. USA 79: 5793 5797.
141. Novella, I. S.,, E. A. Duarte,, S. F. Elena,, A. Moya,, E. Domingo,, and J. J. Holland. 1995. Exponential increases of RNA virus fitness during large population transmissions. Proc. Natl. Acad. Sci. USA 92: 5841 5844.
142. Novella, I. S.,, S. F. Elena,, A. Moya,, E. Domingo,, and J. J. Holland. 1995. Size of genetic bottlenecks leading to virus fitness loss is determined by mean initial population fitness. J. Virol. 69: 2869 2872.
143. Novella, I. S.,, C. L. Hershey,, C. Escarmís,, E. Domingo,, and J. J. Holland. 1999. Lack of evolutionary stasis during alternating replication of an arbovirus in insect and mammalian cells. J. Mol. Biol. 287: 459 465.
144. Novella, I. S.,, J. Quer,, E. Domingo,, and J. J. Holland. 1999. Exponential fitness gains of RNA virus populations are limited by bottleneck effects. J. Virol. 73: 1668 1671.
145. Nowak, M. A. 1992. What is a quasispecies? Trends Ecol. Evol. 4: 118 121.
145a.. Núñez, J. L.,, E. Baranowski,, N. Molina,, C. M. Ruíz-Jarabo,, C. Sanchez,, E. Domingo,, and F. Sobrino. 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 3983.
145b.. Pariente, N.,, S. Sierra,, P. R. Lowenstein,, and E. Domingo. 2001. Efficient vims extinction by combinations of a mutagen and antiviral inhibitors. J. Virol. 75: 9723 9730.
146. Parvin, J. D.,, A. Moscona,, W. T. Pan,, J. M. Leider,, and P. Palese. 1986. Measurement of the mutation rates of animal viruses: influenza A virus and poliovirus type 1. J. Virol. 59: 377 383.
147. Pathak, V. K.,, and H. M. Temin. 1992. 5-Azacytidine and RNA secondary structure increase the retrovirus mutation rate. J. Virol. 66: 3093 3100.
148. Patterson, L. J.,, and V. V. Hamparian. 1997. Hyperantigenic variation occurs with human rhinovirus type 17. J. Virol. 71: 1370 1374.
149. Paul, A. V.,, J. H. van Boom,, D. Filippov,, and E. Wimmer. 1998. Protein-primed RNA synthesis by purified poliovirus RNA polymerase. Nature 393: 280 284.
149a.. Pawlotsky, J. M. 2000. Hepatitis C. Virus Resistance to antiviral therapy. Hepatology 32: 889 896.
150. Pawlotsky, J. M.,, G. Germanidis,, A. U. Neumann,, M. Pellerin,, P. O. Frainais,, and D. Dhumeaux. 1998. Interferon resistance of hepatitis C virus genotype lb: relationship to nonstructural 5A gene quasispecies mutations. J. Virol 72: 2795 2805.
151. Pfister, T.,, and E. Wimmer. 1999. Characterization of the nucleoside triphosphatase activity of poliovirus protein 2C reveals a mechanism by which guanidine inhibits poliovirus replication. J. Biol. Chem. 274: 6992 7001.
152. Pincus, S. E.,, and E. Wimmer. 1986. Production of guanidine-resistant and -dependent poliovirus mutants from cloned cDNA: mutations in polypeptide 2C are directly responsible for altered guanidine sensitivity. J. Virol. 60: 793 796.
153. Prabhakar, B. S.,, V. M. Haspel,, P. R. McClintock,, and A. L. Notkins. 1982. High frequency of antigenic variants among naturally occurring human coxsackie B4 virus isolates identified by monoclonal antibodies. Nature 300: 374 376.
154. Prabhakar, B. S.,, M. A. Menegus,, and A. L. Notkins. 1985. Detection of conserved and nonconserved epitopes on coxsackievirus B4: frequency of antigenic change. Virology 146: 302 306.
155. Racaniello, V. R.,, and D. Baltimore. 1981. Cloned poliovirus complementary DNA is infectious in mammalian cells. Science 214: 916 919.
156. Ramsingh, A. I.,, and D. N. Collins. 1995. A point mutation in the VP4 coding sequence of coxsackievirus B4 influences virulence. J. Virol. 69: 7278 7281.
157. Ramsingh, A. I., , W. T. Lee,, D. N. Collins,, and L. E. Armstrong. 1999. T cells contribute to disease severity during coxsackievirus B4 infection. J. Virol. 73: 3080 3086.
158. Rodrigo, M. J.,, and J. Dopazo. 1995. Evolutionary analysis of the Picornavirus family. J. Mol. Evol. 40: 362 371.
159. Rossmann, M. G.,, J. Bella,, P. R. Kolatkar,, Y. He,, E. Wimmer,, R. Kuhn,, and T. S. Baker. 2000. Cell recognition and entry by rhino- and enteroviruses. Virology 269: 239 247.
160. Ruiz-Jarabo, C. M.,, A. Arias,, E. Baranowski,, C. Escarmís,, and E. Domingo. 2000. Memory in viral quasispecies. J. Virol. 74: 3543 3547.
160a.. Ruiz-Jarabo, C. M.,, A. Arias,, C. Molina-Paris,, C. Briones,, E. Baranowski,, C. Escarmís,, and E. Domingo. 2002. Duration and fitness dependence of quasispecies memory. J. Mol. Biol. 315: 285 296.
161. Ruiz-Jarabo, C. M.,, N. Sevilla,, M. Davila,, G. Gomez-Mariano,, E. Baranowski,, and E. Domingo. 1999. Antigenic properties and population stability of a foot-and-mouth disease virus with an altered Arg-Gly-Asp receptor-recognition motif. J. Gen. Virol. 80: 1899 1909.
162. Sa-Carvalho, D.,, E. Rieder,, B. Baxt,, R. Rodarte,, A. Tanuri,, and P. W. Mason. 1997. Tissue culture adaptation of foot-and-mouth disease virus selects viruses that bind to heparin and are attenuated in cattle. J. Virol. 71: 5115 5123.
163. Sáiz, J. C., and E. Domingo. 1996. Virulence as a positive trait in viral persistence. J. Virol. 70: 6410 6413.
164. Sankar, S.,, and A. G. Porter. 1992. Point mutations which drastically affect the polymerization activity of encephalomyocarditis virus RNA-dependent RNA polymerase correspond to the active site of Escherichia coli DNA polymerase I. J. Biol. Chem. 267: 10168 10176.
165. Saunders, K.,, and A. M. King. 1982. Guanidine-resistant mutants of aphthovirus induce the synthesis of an altered nonstructural polypeptide, P34. J. Virol. 42: 389 394.
166. Schrag, S. J.,, P. A. Rota,, and W. J. Bellini. 1999. Spontaneous mutation rate of measles virus: direct estimation based on mutations conferring monoclonal antibody resistance. J. Virol. 73: 51 54.
167. Schwimmbeck, P. L.,, S. A. Huber,, and H. P. Schultheiss. 1997. Roles of T cells in coxsackievirus B-induced disease. Curr. Top. Microbiol. Immunol. 223: 283 303.
168. Sedivy, J. M.,, J. P. Capone,, U. L. RajBhandary,, and P. A. Sharp. 1987. An inducible mammalian amber suppressor: propagation of a poliovirus mutant. Cell 50: 379 389.
169. Sevilla, N.,, and E. Domingo. 1996. Evolution of a persistent aphthovirus in cytolytic infections: partial reversion of phenotypic traits accompanied by genetic diversification. J. Virol. 70: 6617 6624.
170. Sevilla, N.,, C. M. Ruiz-Jarabo,, G. Gómez-Mariano,, E. Baranowski,, and E. Domingo. 1998. An RNA virus can adapt to the multiplicity of infection. J. Gen. Virol. 79: 2971 2980.
171. Sevilla, N.,, N. Verdaguer,, and E. Domingo. 1996. Antigenically profound amino acid substitutions occur during large population passages of foot-and-mouth disease virus. Virology 225: 400 405.
172. Sherry, B.,, A. G. Mosser,, R. J. Colonno,, and R. R. Rueckert. 1986. Use of monoclonal antibodies to identify four neutralization immunogens on a common cold Picornavirus, human rhinovirus 14. J. Virol. 57: 246 257.
173. Sierra, S.,, M. Dávila,, P. R. Lowenstein,, and E. Domingo. 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.
174. Smith, T. J.,, and T. Baker. 1999. Picornaviruses: epitopes, canyons, and pockets. Adv. Virus Res. 52: 1 23.
175. Smith, T. J.,, E. S. Chase,, T. J. Schmidt,, N. H. Olson,, and T. S. Baker. 1996. Neutralizing antibody to human rhinovirus 14 penetrates the receptor-binding canyon. Nature 383: 350 354.
176. Smith, T. J.,, M. J. Kremer,, M. Luo,, G. Vriend,, E. Arnold,, G. Kamer,, M. G. Rossmann,, M. A. McKinlay,, G. D. Diana,, and M. J. Otto. 1986. The site of attachment in human rhinovirus 14 for antiviral agents that inhibit uncoating. Science 233: 1286 1293.
177. Sousa, R. 1996. Structural and mechanistic relationships between nucleic acid polymerases. Trends Biochem. Sci. 21: 186 190.
178. Stanway, G.,, P. J. Hughes,, R. C. Mountford,, P. Reeve,, P. D. Minor,, G. C. Schild,, and J. W. Almond. 1984. Comparison of the complete nucleotide sequences of the genomes of the neurovirulent poliovirus P3/Leon/37 and its attenuated Sabin vaccine derivative P3/Leon 12alb. Proc. Natl. Acad. Sci. USA 81: 1539 1543.
179. Stapleton, J. T.,, and S. M. Lemon. 1987. Neutralization escape mutants define a dominant immunogenic neutralization site on hepatitis A virus. J. Virol. 61: 491 498.
180. Steinhauer, D. A.,, J. C. de la Torre,, and J. J. Holland. 1989. High nucleotide substitution error frequencies in clonal pools of vesicular stomatitis virus. J. Virol. 63: 2063 2071.
181. Steinhauer, D. A., , E. Domingo,, and J. J. Holland. 1992. Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. Gene 122: 281 288.
182. Steinhauer, D. A., , and J. J. Holland. 1986. Direct method for quantitation of extreme polymerase error frequencies at selected single base sites in viral RNA. J. Virol. 57: 219 228.
183. Steitz, T. A. 1999. DNA polymerases: structural diversity and common mechanisms. J. Biol. Chem. 274: 17395 17398.
184. Taboga, O.,, C. Tami,, E. Carrillo,, J., I. Nuñez,, A. Rodriguez,, J. C. Saíz,, E. Blanco,, M. L. Valero,, X. Roig,, J. A. Camarero,, D. Andreu,, M. G. Mateu,, E. Giralt,, E. Domingo,, F. Sobrino,, and E. L. Palma. 1997. A large-scale evaluation of peptide vaccines against foot-and-mouth disease: lack of solid protection in cattle and isolation of escape mutants. J. Virol. 71: 2606 2614.
185. Tatem, J. M.,, C. Weeks-Levy,, A. Georgiu,, S. J. Di-Michele,, E. J. Gorgacz,, V. R. Racaniello,, F. R. Cano,, and S. J. Mento. 1992. A mutation present in the amino terminus of Sabin 3 poliovirus VP1 protein is attenuating. J. Virol. 66: 3194 3197.
186. Tu, Z.,, N. M. Chapman,, G. Hufnagel,, S. Tracy,, J. R. Romero,, W. H. Barry,, L. Zhao,, K. Currey,, and B. Shapiro. 1995. The cardiovirulent phenotype of coxsackievirus B3 is determined at a single site in the genomic 5' nontranslated region. J. Virol. 69: 4607 4618.
187. Tyrrell, D. A. 1988. Hot news on the common cold. Annu. Rev. Microbiol. 42: 35 47.
188. Usherwood, E. J.,, and A. A. Nash. 1995. Lymphocyte recognition of picornaviruses. J. Gen. Virol. 76: 499 508.
189. Valcarcel, J.,, and J. Ortin. 1989. Phenotypic hiding: the carryover of mutations in RNA viruses as shown by detection of mar mutants in influenza virus. J. Virol. 63: 4107 4109.
190. Verdaguer, N.,, M. G. Mateu,, D. Andreu,, E. Giralt,, E. Domingo,, and I. Fita. 1995. Structure of the major antigenic loop of foot-and-mouth disease virus complexed with a neutralizing antibody: direct involvement of the Arg-Gly-Asp motif in the interaction. EMBO J. 14: 1690 1696.
191. Verdaguer, N.,, M. G. Mateu,, J. Bravo,, E. Domingo,, and I. Fita. 1996. Induced pocket to accommodate the cell attachment Arg-Gly-Asp motif in a neutralizing antibody against foot-and-mouth-disease virus. J. Mol. Biol. 256: 364 376.
192. Verdaguer, N.,, N. Sevilla,, M. L. Valero,, D. Stuart,, E. Brocchi,, D. Andreu,, E. Giralt,, E. Domingo,, M. G. Mateu,, and I. Fita. 1998. A similar pattern of interaction for different antibodies with a major antigenic site of foot-and-mouth disease virus: implications for intratypic antigenic variation. J. Virol. 72: 739 748.
193. Villaverde, A.,, E. Martínez-Salas,, and E. Domingo. 1988. 3D gene of foot-and-mouth disease virus. Conservation by convergence of average sequences. J. Mol. Biol. 204: 771 776.
194. Volkenstein, M. V. 1994. Physical Approaches to Biological Evolution. Springer-Verlag, Berlin, Germany.
195. Wainberg, M. A.,, W. C. Drosopoulos,, H. Salomon,, M. Hsu,, G. Borkow,, M. Parniak,, Z. Gu,, Q. Song,, J. Manne,, S. Islam,, G. Castriota,, and V. R. Prasad. 1996. Enhanced fidelity of 3TC-selected mutant HIV-1 reverse transcriptase. Science 271: 1282 1285.
196. Ward, C. D.,, and J. B. Flanegan. 1992. Determination of the poliovirus RNA polymerase error frequency at eight sites in the viral genome. J. Virol. 66: 3784 3793.
197. Ward, C. D.,, M. A. Stokes,, and J. B. Flanegan. 1988. Direct measurement of the poliovirus RNA polymerase error frequency in vitro. J. Virol. 62: 558 562.
198. Weaver, S. C.,, A. C. Brauk,, W. Kang,, and J. J. Holland. 1999. Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J. Virol. 73: 4316 4326.
199. Webster, R. G., 1999. Antigenic variation in influenza viruses, p. 377 390. In E. Domingo,, R. G. Webster,, and J. J. Holland (ed.), Origin and Evolution of Viruses. Academic Press, San Diego, Calif.
199a.. Wells, V. R.,, S. J. Plotch,, and J. J. DeStefano. 2001. Determination of the mutation rate of poliovirus RNA-dependent RNA polymerase. Virus Res. 74: 119 132.
200. Wimmer, E.,, C. U. Hellen,, and X. Cao. 1993. Genetics of poliovirus. Annu. Rev. Genet. 27: 353 436.
201. Wutz, G.,, H. Auer,, N. Nowotny,, B. Grosse,, T. Skern,, and E. Kuechler. 1996. Equine rhinovirus serotypes 1 and 2: relationship to each other and to aphthoviruses and cardioviruses. J. Gen. Virol. 77: 1719 1730.
202. Xie, Q.-C.,, D. McCahon,, J. R. Crowther,, G. J. Belsham,, and K. C. McCullough. 1987. Neutralization of foot-and-mouth disease virus can be mediated through any of at least three separate antigenic sites. J. Gen. Virol. 68: 1637 1647.
203. Xing, L.,, K. Tjarnlund,, B. Lindqvist,, G. G. Kaplan,, D. Feigelstock,, R. H. Cheng,, and J. M. Casasnovas. 2000. Distinct cellular receptor interactions in poliovirus and rhinoviruses. EMBO J. 19: 1207 1216.
204. Yoon, J. W,, and H. S. Jun,. 1998. Insulin-dependent diabetes mellitus, p. 1390-1398. In I. M. Roitt, and P. J. Delves (ed.), Encyclopedia of Immunology, 2nd ed. Academic Press, London, United Kingdom.
205. Yuste, E.,, C. López-Galíndez,, and E. Domingo. 2000. Unusual distribution of mutations associated with serial bottleneck passages of human immunodeficiency virus type 1. J. Virol. 74: 9546 9552.
206. Yuste, E.,, S. Sánchez-Palomino,, C. Casado,, E. Domingo,, and C. López-Galíndez. 1999. Drastic fitness loss in human immunodeficiency virus type 1 upon serial bottleneck events. J. Virol. 73: 2745 2751.
207. Zhang, G.,, G. Wilsden,, N. J. Knowles,, and J. W. McCauley. 1993. Complete nucleotide sequence of a Coxsackie B5 virus and its relationship to swine vesicular disease virus. J. Gen. Virol. 74: 845 853.
208. Zhang,, Zimmern, D., 1988. Evolution of RNA viruses, p. 211 240. In E. Domingo,, J. J. Holland,, and P. Ahlquist (ed.), RNA Genetics, vol. 2. CRC Press Inc., Boca Raton, Fla.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error