Characterization of a putative ancestor of coxsackievirus B5

Journal of Virology

Volumn 84, Issue 19, 2010, Pages 9695-9708

  Gullberg, Maria ^a   Tolf, Conny ^a   Jonsson, Nina ^a   Mulders, Mick N ^b   Savolainen Kopra, Carita ^c   Hovi, Tapani ^c   Van Ranst, Marc ^d   Lemey, Philippe ^d   Hafenstein, Susan ^e   Lindberg, A Michael ^a  

^a LINNAEUS UNIVERSITY   (Sweden)

^b NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^c NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^d REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^e PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; PROTEIN VP1; VIRUS RNA; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; BAYES THEOREM; CELL GROWTH; COXSACKIE VIRUS; COXSACKIE VIRUS B5; FLOW CYTOMETRY; GENE AMPLIFICATION; GENE SEQUENCE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MOLECULAR CLONING; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; RNA EXTRACTION; VIRAL GENETICS; VIRUS INFECTION; VIRUS ISOLATION; VIRUS PARTICLE; VIRUS RECOMBINANT; ANIMAL; BIOLOGICAL MODEL; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; COMPARATIVE STUDY; COXSACKIE VIRUS INFECTION; ENTEROVIRUS; GENETICS; ISOLATION AND PURIFICATION; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYSIOLOGY; STRUCTURAL HOMOLOGY; TIME; VIROLOGY; VIRUS GENOME;

COXSACKIEVIRUS; MIRIDAE; PICORNAVIRIDAE; RNA VIRUSES;

ANIMALS; BAYES THEOREM; CELL LINE; COXSACKIEVIRUS INFECTIONS; ENTEROVIRUS B, HUMAN; EVOLUTION, MOLECULAR; GENOME, VIRAL; HUMANS; MODELS, GENETIC; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; STRUCTURAL HOMOLOGY, PROTEIN; TIME FACTORS; VIRAL STRUCTURAL PROTEINS;

EID: 77956827656     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00071-10     Document Type: Article

References (110)

1. Adey, N. B., T. O. Tollefsbol, A. B. Sparks, M. H. Edgell, and C. A. Hutchison III. 1994. Molecular resurrection of an extinct ancestral promoter for mouse L1. Proc. Natl. Acad. Sci. U. S. A. 91:1569-1573.
2. Arnberg, N., K. Edlund, A. H. Kidd, and G. Wadell. 2000. Adenovirus type 37 uses sialic acid as a cellular receptor. J. Virol. 74:42-48. (Pubitemid 30002881)
3. Baranowski, E., N. Sevilla, N. Verdaguer, C. M. Ruiz-Jarabo, E. Beck, and E. Domingo. 1998. Multiple virulence determinants of foot-and-mouth disease virus in cell culture. J. Virol. 72:6362-6372.
4. Bedard, K. M., and B. L. Semler. 2004. Regulation of picornavirus gene expression. Microbes Infect. 6:702-713.
5. Bergelson, J. M., J. A. Cunningham, G. Droguett, E. A. Kurt-Jones, A. Krithivas, J. S. Hong, M. S. Horwitz, R. L. Crowell, and R. W. Finberg. 1997. Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320-1323.
6. Bergelson, J. M., J. F. Modlin, W. Wieland-Alter, J. A. Cunningham, R. L. Crowell, and R. W. Finberg. 1997. Clinical coxsackievirus B isolates differ from laboratory strains in their interaction with two cell surface receptors. J. Infect. Dis. 175:697-700.
7. Bergelson, J. M., J. G. Mohanty, R. L. Crowell, N. F. St. John, D. M. Lublin, and R. W. Finberg. 1995. Coxsackievirus B3 adapted to growth in RD cells binds to decay-accelerating factor (CD55). J. Virol. 69:1903-1906.
8. Bergelson, J. M., N. St. John, S. Kawaguchi, M. Chan, H. Stubdal, J. Modlin, and R. W. Finberg. 1993. Infection by echoviruses 1 and 8 depends on the alpha 2 subunit of human VLA-2. J. Virol. 67:6847-6852.
9. Borrego, B., E. Carra, J. A. Garcia-Ranea, and E. Brocchi. 2002. Characterization of neutralization sites on the circulating variant of swine vesicular disease virus (SVDV): a new site is shared by SVDV and the related coxsackie B5 virus. J. Gen. Virol. 83:35-44.
10. Bridgham, J. T., E. A. Ortlund, and J. W. Thornton. 2009. An epistatic ratchet constrains the direction of glucocorticoid receptor evolution. Nature 461:515-519.
11. 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.
12. Bruen, T. C., H. Philippe, and D. Bryant. 2006. A simple and robust statistical test for detecting the presence of recombination. Genetics 172:2665-2681.
13. Caro, V., S. Guillot, F. Delpeyroux, and R. Crainic. 2001. Molecular strategy for 'serotyping' of human enteroviruses. J. Gen. Virol. 82:79-91.
14. Casas, I., G. F. Palacios, G. Trallero, D. Cisterna, M. C. Freire, and A. Tenorio. 2001. Molecular characterization of human enteroviruses in clinical samples: comparison between VP2, VP1, and RNA polymerase regions using RT nested PCR assays and direct sequencing of products. J. Med. Virol. 65:138-148.
15. Chang, B. S., K. Jonsson, M. A. Kazmi, M. J. Donoghue, and T. P. Sakmar. 2002. Recreating a functional ancestral archosaur visual pigment. Mol. Biol. Evol. 19:1483-1489.
16. Crowell, R. L., and J. T. Syverton. 1961. The mammalian cell-virus relationship. VI. Sustained infection of HeLa cells by coxsackie B3 virus and effect on superinfection. J. Exp. Med. 113:419-435.
17. Diallo, A. B., V. Makarenkov, and M. Blanchette. 2010. Ancestors 1.0: a Web server for ancestral sequence reconstruction. Bioinformatics 26:130-131.
18. Dobos, P. 1976. Use of gum tragacanth overlay, applied at room temperature, in the plaque assay of fish and other animal viruses. J. Clin. Microbiol. 3:373-375.
19. Domingo, E., C. Escarmis, E. Baranowski, C. M. Ruiz-Jarabo, E. Carrillo, J. I. Nunez, and F. Sobrino. 2003. Evolution of foot-and-mouth disease virus. Virus Res. 91:47-63.
20. Domingo, E., V. Martin, C. Perales, and C. Escarmis. 2008. Coxsackieviruses and quasispecies theory: evolution of enteroviruses. Curr. Top. Microbiol. Immunol. 323:3-32.
21. Doria-Rose, N. A., G. H. Learn, A. G. Rodrigo, D. C. Nickle, F. Li, M. Mahalanabis, M. T. Hensel, S. McLaughlin, P. F. Edmonson, D. Montefiori, S. W. Barnett, N. L. Haigwood, and J. I. Mullins. 2005. Human immunodeficiency virus type 1 subtype B ancestral envelope protein is functional and elicits neutralizing antibodies in rabbits similar to those elicited by a circulating subtype B envelope. J. Virol. 79:11214-11224.
22. Drake, J. W., and J. J. Holland. 1999. Mutation rates among RNA viruses. Proc. Natl. Acad. Sci. U. S. A. 96:13910-13913.
23. Drummond, A. J., S. Y. Ho, M. J. Phillips, and A. Rambaut. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4:e88.
24. Drummond, A. J., G. K. Nicholls, A. G. Rodrigo, and W. Solomon. 2002. Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161:1307-1320.
25. Drummond, A. J., and A. Rambaut. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7:214.
26. Drummond, A. J., A. Rambaut, B. Shapiro, and O. G. Pybus. 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol. Biol. Evol. 22:1185-1192.
27. Escribano-Romero, E., M. A. Jimenez-Clavero, and V. Ley. 2000. Swine vesicular disease virus. Pathology of the disease and molecular characteristics of the virion. Anim. Health Res. Rev. 1:119-126.
28. Fares, M. A., E. Barrio, N. Becerra, C. Escarmis, E. Domingo, and A. Moya. 1998. The foot-and-mouth disease RNA virus as a model in experimental phylogenetics. Int. Microbiol. 1:311-318.
29. Faria, N. R., M. de Vries, F. J. van Hemert, K. Benschop, and L. van der Hoek. 2009. Rooting human parechovirus evolution in time. BMC Evol. Biol. 9:164.
30. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791.
31. Fry, E. E., N. J. Knowles, J. W. Newman, G. Wilsden, Z. Rao, A. M. King, and D. I. Stuart. 2003. Crystal structure of swine vesicular disease virus and implications for host adaptation. J. Virol. 77:5475-5486.
32. Gaucher, E. A., J. M. Thomson, M. F. Burgan, and S. A. Benner. 2003. Inferring the palaeoenvironment of ancient bacteria on the basis of resurrected proteins. Nature 425:285-288.
33. Gifford, R., and G. Dalldorf. 1951. The morbid anatomy of experimental coxsackie virus infection. Am. J. Pathol. 27:1047-1063.
34. Goldman, N., and Z. Yang. 1994. A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol. Biol. Evol. 11:725-736.
35. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
36. Hafenstein, S., V. D. Bowman, P. R. Chipman, C. M. B. Kelly, F. Lin, M. E. Medof, and M. G. Rossmann. 2007. Interaction of decay-accelerating factor with coxsackievirus B3. J. Virol. 81:12927-12935.
37. Hammerle, T., C. U. Hellen, and E. Wimmer. 1991. Site-directed mutagenesis of the putative catalytic triad of poliovirus 3C proteinase. J. Biol. Chem. 266:5412-5416.
38. Harvala, H., and P. Simmonds. 2009. Human parechoviruses: biology, epidemiology and clinical significance. J. Clin. Virol. 45:1-9.
39. He, Y., P. R. Chipman, J. Howitt, C. M. Bator, M. A. Whitt, T. S. Baker, R. J. Kuhn, C. W. Anderson, P. Freimuth, and M. G. Rossmann. 2001. Interaction of coxsackievirus B3 with the full length coxsackievirus-adenovirus receptor. Nat. Struct. Biol. 8:874-878.
40. Hellen, C. U., M. Facke, H. G. Krausslich, C. K. Lee, and E. Wimmer. 1991. Characterization of poliovirus 2A proteinase by mutational analysis: residues required for autocatalytic activity are essential for induction of cleavage of eukaryotic initiation factor 4F polypeptide p220. J. Virol. 65:4226-4231.
41. Hierholzer, J. C., and R. A. Killinton. 1996. Quantitation of virus, p. 35-37. In B. W. J. Mahy and R. A. Kangro (ed.), Virology methods manual. Academic Press, London, United Kingdom.
42. Hovi, T., and M. Roivainen. 1993. Peptide antisera targeted to a conserved sequence in poliovirus capsid VP1 cross-react widely with members of the genus Enterovirus. J. Clin. Microbiol. 31:1083-1087.
43. Hsu, K. H., K. Lonberg-Holm, B. Alstein, and R. L. Crowell. 1988. A monoclonal antibody specific for the cellular receptor for the group B coxsackieviruses. J. Virol. 62:1647-1652.
44. Hughes, A. L. 2004. Phylogeny of the Picornaviridae and differential evolutionary divergence of picornavirus proteins. Infect. Genet. Evol. 4:143-152.
45. Ivics, Z., P. B. Hackett, R. H. Plasterk, and Z. Izsvak. 1997. Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 91:501-510.
46. Jermann, T. M., J. G. Opitz, J. Stackhouse, and S. A. Benner. 1995. Reconstructing the evolutionary history of the artiodactyl ribonuclease superfamily. Nature 374:57-59.
47. Jonsson, N., M. Gullberg, and A. M. Lindberg. 2009. Real-time polymerase chain reaction as a rapid and efficient alternative to estimation of picornavirus titers by tissue culture infectious dose 50% or plaque forming units. Microbiol. Immunol. 53:149-154.
48. Kanno, T., T. Inoue, Y. Wang, A. Sarai, and S. Yamaguchi. 1995. Identification of the location of antigenic sites of swine vesicular disease virus with neutralization-resistant mutants. J. Gen. Virol. 76(Pt. 12):3099-3106.
49. Konno, A., T. Ogawa, T. Shirai, and K. Muramoto. 2007. Reconstruction of a probable ancestral form of conger eel galectins revealed their rapid adaptive evolution process for specific carbohydrate recognition. Mol. Biol. Evol. 24:2504-2514.
50. Kopecka, H., B. Brown, and M. Pallansch. 1995. Genotypic variation in coxsackievirus B5 isolates from three different outbreaks in the United States. Virus Res. 38:125-136.
51. Kothe, D. L., Y. Li, J. M. Decker, F. Bibollet-Ruche, K. P. Zammit, M. G. Salazar, Y. Chen, Z. Weng, E. A. Weaver, F. Gao, B. F. Haynes, G. M. Shaw, B. T. Korber, and B. H. Hahn. 2006. Ancestral and consensus envelope immunogens for HIV-1 subtype C. Virology 352:438-449.
52. Kuang, D., Y. Yao, D. Maclean, M. Wang, D. R. Hampson, and B. S. Chang. 2006. Ancestral reconstruction of the ligand-binding pocket of family C G protein-coupled receptors. Proc. Natl. Acad. Sci. U. S. A. 103:14050-14055.
53. Lanave, C., G. Preparata, C. Saccone, and G. Serio. 1984. A new method for calculating evolutionary substitution rates. J. Mol. Evol. 20:86-93.
54. Lin, F., and R. P. Kitching. 2000. Swine vesicular disease: an overview. Vet. J. 160:192-201.
55. Lindberg, A. M., and C. Polacek. 2000. Molecular analysis of the prototype coxsackievirus B5 genome. Arch. Virol. 145:205-221.
56. Lindberg, A. M., C. Polacek, and S. Johansson. 1997. Amplification and cloning of complete enterovirus genomes by long distance PCR. J. Virol. Methods 65:191-199.
57. Lukashev, A. N. 2005. Role of recombination in evolution of enteroviruses. Rev. Med. Virol. 15:157-167.
58. Marc, D., G. Drugeon, A. L. Haenni, M. Girard, and S. van der Werf. 1989. Role of myristoylation of poliovirus capsid protein VP4 as determined by site-directed mutagenesis of its N-terminal sequence. EMBO J. 8:2661-2668. (Pubitemid 19273351)
59. Martino, T. A., M. Petric, M. Brown, K. Aitken, C. J. Gauntt, C. D. Richardson, L. H. Chow, and P. P. Liu. 1998. Cardiovirulent coxsackieviruses and the decay-accelerating factor (CD55) receptor. Virology 244:302-314.
60. Martino, T. A., M. Petric, H. Weingartl, J. M. Bergelson, M. A. Opavsky, C. D. Richardson, J. F. Modlin, R. W. Finberg, K. C. Kain, N. Willis, C. J. Gauntt, and P. P. Liu. 2000. The coxsackie-adenovirus receptor (CAR) is used by reference strains and clinical isolates representing all six serotypes of coxsackievirus group B and by swine vesicular disease virus. Virology 271:99-108.
61. Melnick, J. L., E. W. Shaw, and E. C. Curnen. 1949. A virus isolated from patients diagnosed as non-paralytic poliomyelitis or aseptic meningitis. Proc. Soc. Exp. Biol. Med. 71:344-349.
62. Milstone, A. M., J. Petrella, M. D. Sanchez, M. Mahmud, J. C. Whitbeck, and J. M. Bergelson. 2005. Interaction with coxsackievirus and adenovirus receptor, but not with decay-accelerating factor (DAF), induces A-particle formation in a DAF-binding coxsackievirus B3 isolate. J. Virol. 79:655-660.
63. Minor, P. 1985. Growth, assay and purification of picornaviruses, p. 25-41. In B. Mahy (ed.), Virology, a practical approach. IRL Press, Oxford, United Kingdom.
64. Muckelbauer, J. K., M. Kremer, I. Minor, G. Diana, F. J. Dutko, J. Groarke, D. C. Pevear, and M. G. Rossmann. 1995. The structure of coxsackievirus B3 at 3.5 Å resolution. Structure 3:653-667.
65. Mulders, M. N., M. Salminen, N. Kalkkinen, and T. Hovi. 2000. Molecular epidemiology of coxsackievirus B4 and disclosure of the correct VP1/2A(pro) cleavage site: evidence for high genomic diversity and long-term endemicity of distinct genotypes. J. Gen. Virol. 81:803-812.
66. Mullins, J. I., D. C. Nickle, L. Heath, A. G. Rodrigo, and G. H. Learn. 2004. Immunogen sequence: the fourth tier of AIDS vaccine design. Expert Rev. Vaccines 3:S151-S159.
67. Nardelli, L., E. Lodetti, G. L. Gualandi, R. Burrows, D. Goodridge, F. Brown, and B. Cartwright. 1968. A foot and mouth disease syndrome in pigs caused by an enterovirus. Nature 219:1275-1276.
68. Nijhar, S. K., D. K. Mackay, E. Brocchi, N. P. Ferris, R. P. Kitching, and N. J. Knowles. 1999. Identification of neutralizing epitopes on a European strain of swine vesicular disease virus. J. Gen. Virol. 80(Pt. 2):277-282.
69. Norder, H., L. Bjerregaard, and L. O. Magnius. 2001. Homotypic echoviruses share aminoterminal VP1 sequence homology applicable for typing. J. Med. Virol. 63:35-44.
70. Oberste, M. S., K. Maher, M. L. Kennett, J. J. Campbell, M. S. Carpenter, D. Schnurr, and M. A. Pallansch. 1999. Molecular epidemiology and genetic diversity of echovirus type 30 (E30): genotypes correlate with temporal dynamics of E30 isolation. J. Clin. Microbiol. 37:3928-3933.
71. Oberste, M. S., K. Maher, D. R. Kilpatrick, M. R. Flemister, B. A. Brown, and M. A. Pallansch. 1999. Typing of human enteroviruses by partial sequencing of VP1. J. Clin. Microbiol. 37:1288-1293.
72. Oberste, M. S., K. Maher, D. R. Kilpatrick, and M. A. Pallansch. 1999. Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J. Virol. 73:1941-1948.
73. Pauling, L., and E. Zuckerkandl. 1963. Chemical paleogenetics: molecular restoration studies of extinct forms of life. Acta Chem. Scand. 17:S9-S16.
74. Percy, N., W. S. Barclay, M. Sullivan, and J. W. Almond. 1992. A poliovirus replicon containing the chloramphenicol acetyltransferase gene can be used to study the replication and encapsidation of poliovirus RNA. J. Virol. 66:5040-5046.
75. Pettersen, E. F., T. D. Goddard, C. C. Huang, G. S. Couch, D. M. Greenblatt, E. C. Meng, and T. E. Ferrin. 2004. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.
76. Pfeiffer, J. K., and K. Kirkegaard. 2005. Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLoS Pathog. 1:e11.
77. Polacek, C., J. O. Ekstrom, A. Lundgren, and A. M. Lindberg. 2005. Cytolytic replication of coxsackievirus B2 in CAR-deficient rhabdomyosarcoma cells. Virus Res. 113:107-115.
78. Pupko, T., I. Pe'er, R. Shamir, and D. Graur. 2000. A fast algorithm for joint reconstruction of ancestral amino acid sequences. Mol. Biol. Evol. 17:890-896.
79. Reagan, K. J., B. Goldberg, and R. L. Crowell. 1984. Altered receptor specificity of coxsackievirus B3 after growth in rhabdomyosarcoma cells. J. Virol. 49:635-640.
80. Rezig, D., A. Ben Yahia, H. Ben Abdallah, O. Bahri, and H. Triki. 2004. Molecular characterization of coxsackievirus B5 isolates. J. Med. Virol. 72:268-274.
81. Rolland, M., M. A. Jensen, D. C. Nickle, J. Yan, G. H. Learn, L. Heath, D. Weiner, and J. I. Mullins. 2007. Reconstruction and function of ancestral center-of-tree human immunodeficiency virus type 1 proteins. J. Virol. 81:8507-8514.
82. Rossmann, M. G. 2002. Picornavirus structure overview, p. 27-38. In B. L. Semler and E. Wimmer (ed.), Molecular biology of picornaviruses. ASM Press, Washington, DC.
83. Sanner, M. F., A. J. Olson, and J. C. Spehner. 1996. Reduced surface: an efficient way to compute molecular surfaces. Biopolymers 38:305-320.
84. Selinka, H. C., A. Wolde, A. Pasch, K. Klingel, J. J. Schnorr, J. H. Kupper, A. M. Lindberg, and R. Kandolf. 2002. Comparative analysis of two coxsackievirus B3 strains: putative influence of virus-receptor interactions on pathogenesis. J. Med. Virol. 67:224-233.
85. Shafren, D. R., R. C. Bates, M. V. Agrez, R. L. Herd, G. F. Burns, and R. D. Barry. 1995. Coxsackieviruses B1, B3, and B5 use decay accelerating factor as a receptor for cell attachment. J. Virol. 69:3873-3877.
86. Shapiro, B., A. Rambaut, and A. J. Drummond. 2006. Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol. Biol. Evol. 23:7-9.
87. Smit, A. F., and A. D. Riggs. 1996. Tiggers and DNA transposon fossils in the human genome. Proc. Natl. Acad. Sci. U. S. A. 93:1443-1448.
88. Stackhouse, J., S. R. Presnell, G. M. McGeehan, K. P. Nambiar, and S. A. Benner. 1990. The ribonuclease from an extinct bovid ruminant. FEBS Lett. 262:104-106.
89. Stanway, G., F. Brown, P. Christian, T. Hovi, T. Hyypia, A. M. Q. King, N. J. Knowles, S. M. Lemon, P. D. Minor, M. A. Pallansch, A. C. Palmenberg, and T. Skern. 2005. Family Picornaviridae, p. 757-778. In C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger, and L. A. Ball (ed.), Virus taxonomy: eighth report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, London, United Kingdom.
90. Strimmer, K., and A. von Haeseler. 1997. Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proc. Natl. Acad. Sci. U. S. A. 94:6815-6819.
91. Takeda, N., M. Tanimura, and K. Miyamura. 1994. Molecular evolution of the major capsid protein VP1 of enterovirus 70. J. Virol. 68:854-862.
92. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
93. Thoelen, I., P. Lemey, I. Van Der Donck, K. Beuselinck, A. M. Lindberg, and M. Van Ranst. 2003. Molecular typing and epidemiology of enteroviruses identified from an outbreak of aseptic meningitis in Belgium during the summer of 2000. J. Med. Virol. 70:420-429.
94. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
95. Thomson, J. M., E. A. Gaucher, M. F. Burgan, D. W. De Kee, T. Li, J. P. Aris, and S. A. Benner. 2005. Resurrecting ancestral alcohol dehydrogenases from yeast. Nat. Genet. 37:630-635.
96. Thornton, J. W. 2004. Resurrecting ancient genes: experimental analysis of extinct molecules. Nat. Rev. Genet. 5:366-375.
97. Thornton, J. W., E. Need, and D. Crews. 2003. Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 301:1714-1717.
98. Tomko, R. P., R. Xu, and L. Philipson. 1997. HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc. Natl. Acad. Sci. U. S. A. 94:3352-3356.
99. Tracy, S., and C. Gauntt. 2008. Group B coxsackievirus virulence. Curr. Top. Microbiol. Immunol. 323:49-63.
100. Vance, L. M., N. Moscufo, M. Chow, and B. A. Heinz. 1997. Poliovirus 2C region functions during encapsidation of viral RNA. J. Virol. 71:8759-8765.
101. Verdaguer, N., M. A. Jimenez-Clavero, I. Fita, and V. Ley. 2003. Structure of swine vesicular disease virus: mapping of changes occurring during adaptation of human coxsackie B5 virus to infect swine. J. Virol. 77:9780-9789. (Pubitemid 37122058)
102. Vignuzzi, M., J. K. Stone, J. J. Arnold, C. E. Cameron, and R. Andino. 2006. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439:344-348.
103. Whitton, J. L., C. T. Cornell, and R. Feuer. 2005. Host and virus determinants of picornavirus pathogenesis and tropism. Nat. Rev. Microbiol. 3:765-776.
104. Xia, X., Z. Xie, M. Salemi, L. Chen, and Y. Wang. 2003. An index of substitution saturation and its application. Mol. Phylogenet. Evol. 26:1-7.
105. Yang, Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13:555-556.
106. Yang, Z., S. Kumar, and M. Nei. 1995. A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 141:1641-1650.
107. Yu, S. F., and R. E. Lloyd. 1991. Identification of essential amino acid residues in the functional activity of poliovirus 2A protease. Virology 182:615-625.
108. Zhang, G., D. T. Haydon, N. J. Knowles, and J. W. McCauley. 1999. Molecular evolution of swine vesicular disease virus. J. Gen. Virol. 80(Pt. 3):639-651.
109. 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(Pt. 5):845-853.
110. Zhang, J., and H. F. Rosenberg. 2002. Complementary advantageous substitutions in the evolution of an antiviral RNase of higher primates. Proc. Natl. Acad. Sci. U. S. A. 99:5486-5491.