Genetic divergence with emergence of novel phenotypic variants of equine arteritis virus during persistent infection of stallions

Journal of Virology

Volumn 73, Issue 5, 1999, Pages 3672-3681

  Hedges, Jodi F ^a   Balasuriya, Udeni B R ^a   Timoney, Peter J ^b   McCollum, William H ^b   Maclachlan, N James ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS PROTEIN;

AMINO ACID SEQUENCE; ANIMAL MODEL; ARTICLE; BIODIVERSITY; EQUINE VIRAL ARTERITIS VIRUS; HORSE; HORSE DISEASE; MALE; NONHUMAN; OPEN READING FRAME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; VIRUS NEUTRALIZATION; VIRUS VIRULENCE;

EID: 0032958431     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.5.3672-3681.1999     Document Type: Article

References (65)

1. Archambault, D., G. Laganiere, S. Carman, and G. St-Laurent. 1997. Comparison of nucleic and amino acid sequences and phylogenetic analysis of open reading frames 3 and 4 of various equine arteritis virus isolates. Vet. Res. 28:505-516.
2. Balasuriya, U. B. R., J. F. Evermann, J. F. Hedges, A. J. McKeirnan, J. Q. Mitten, J. C. Beyer, W. H. McCollum, P. J. Timoney, and N. J. MacLachlan. 1998. Serologic and molecular characterization of an abortigenic strain of equine arteritis virus derived from infective frozen semen and an aborted equine fetus. J. Am. Vet. Med. Assoc. 213:1586-1589.
3. Balasuriya, U. B. R., J. F. Hedges, P. J. Timoney, W. H. McCollum, and N. J. MacLachlan. Genetic stability of equine arteritis virus during horizontal and vertical transmission in an outbreak of equine viral arteritis. Submitted for publication.
4. L) of equine arteritis virus. Virology 297:518-527.
5. L envelope glycoprotein. Virology 232:114-128.
6. Balasuriya, U. B. R., P. V. Rossitto, C. D. DeMaula, and N. J. MacLachlan. 1993. A 29K envelope glycoprotein of equine arteritis virus expresses neutralization determinants recognized by murine monoclonal antibodies. J. Gen. Virol. 74:2525-2529.
7. L envelope glycoprotein. Virology 214:690-697.
8. Cavanagh, D. 1997. Nidovirales: a new order comprising Coronaviridae and Arteriviridae. Arch. Virol. 142:629-633.
9. Chao, L. 1990. Fitness of RNA virus decreased by Muller's ratchet. Nature 348:454-455.
10. Chirnside, E. D., C. M. Wearing, M. M. Binns, and J. A. Mumford. 1994. Comparison of M and N gene sequences distinguishes variation amongst equine arteritis virus isolates. J. Gen. Virol. 75:1491-1497.
11. Clarke, D. K., E. A. Duarte, A. Moya, S. F. Elena, E. Domingo, and J. J. Holland. 1993. Genetic bottlenecks and population passages cause profound fitness differences in RNA viruses. J. Virol. 67:222-228.
12. den Boon, J. A., E. J. Snijder, E. D. Chirnside, A. A. F. de Vries, M. C. Horzinek, and W. J. M. Spaan. 1991. Equine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily. J. Virol. 65:2910-2920.
13. de Vries, A. A. F., E. D. Chirnside, M. C. Horzinek, and P. J. M. Rottier. 1992. Structural proteins of equine arteritis virus. J. Virol. 66:6294-6303.
14. Domingo, E., J. Diez, M. A. Martinez, J. Hernandez, A. Holguin, 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. (Erratum, 75:949, 1994.)
15. Domingo, E., C. Escarmis, N. Sevilla, A. Moya, S. F. Elena, J. Quer, I. S. Novella, and J. J. Holland. 1996. Basic concepts in RNA virus evolution. FASEB J. 10:859-864.
16. Domingo, E., and J. J. Holland. 1997. RNA virus mutations and fitness for survival. Annu. Rev. Microbiol. 51:151-178.
17. Drew, T. W., J. P. Lowings, and F. Yapp. 1997. Variation in open reading frames 3, 4 and 7 among porcine reproductive and respiratory syndrome virus isolates in the UK. Vet. Microbiol. 55:209-221.
18. Duarte, E. A., D. K. Clarke, A. Moya, S. F. Elena, E. Domingo, and J. J. Holland. 1993. Many-trillionfold amplification of single RNA virus particles fails to overcome the Muller's ratchet effect. J. Virol. 67:3620-3623.
19. Eigen, M. 1993. Viral quasispecies. Sci. Am. 269:42-49.
20. Escarmis, C., M. Davila, 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.
21. Faaberg, K. S., and P. G. W. Plagemann. 1997. ORF3 of lactate dehydrogenase-elevating virus encodes a soluble, nonstructural, highly glycosylated, and antigenic protein. Virology 227:245-251.
22. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using bootstrap. Evolution 39:783-791.
23. Felsenstein, J. 1993. PHYLIP (Phylogeny Inference Package) 3.5c manual. University of Washington, Seattle, Wash.
24. Fitch, W. M., and E. Margoliash. 1967. Construction of phylogenetic trees. Science 155:279-384.
25. Gebauer, F., J. C. de la Torre, I. Gomes, M. G. Mateu, H. Barahona, B. Tiraboschi, I. Bergmann, P. Auge 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.
26. Gerone, P. J., R. B. Couch, G. V. Keefer, R. G. Douglas, E. B. Derrenbacher, and V. Knight. 1966. Assessment of experimental and natural viral aerosols. Bacteriol. Rev. 30:576-584.
27. Glaser, A. L., E. D. Chirnside, M. C. Horzinek, and A. A. F. de Vries. 1997. Equine arteritis virus. Theriogenology 47:1275-1295.
28. Glaser, A. L., P. J. M. Rottier, M. C. Horzinek, and B. Colenbrander. 1996. Equine arteritis virus: a review of clinical features and management aspects. Vet. Q. 18:95-99.
29. Godeny, E. K., L. Chen, S. N. Kumar, S. L. Methven, E. V. Koonin, and M. A. Brinton. 1993. Complete genomic sequence and phylogenetic analysis of the lactate dehydrogenase-elevating virus (LDV). Virology 194:585-596.
30. Hedges, J. F., U. B. R. Balasuriya, S. Ahmad, P. J. Timoney, W. H. McCollum, T. D. Yilma, and N. J. MacLachlan. 1998. Detection of antibodies to equine arteritis virus by enzyme linked immunosorbant assays utilizing GL, M and N proteins expressed from recombinant baculoviruses. J. Virol. Methods 76:127-137.
31. Hedges, J. F., U. B. R. Balasuriya, P. J. Timoney, W. H. McCollum, and N. J. MacLachlan. 1996. Genetic variation in open reading frame 2 of field isolates and laboratory strains of equine arteritis virus. Virus Res. 42:41-52.
32. Hillis, D. M., and J. J. Bull. 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst. Biol. 42:182-192.
33. 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.
34. Holyoak, G. R., R. C. Giles, W. H. McCollum, T. V. Little, and P. J. Timoney. 1993. Pathological changes associated with equine arteritis virus infection of the reproductive tract in prepubertal and peripubertal colts. J. Comp. Pathol. 109:281-293.
35. Hullinger, P. J., W. D. Wilson, P. V. Rossitto, J. F. Patton, M. C. Thurmond, and N. J. MacLachlan. 1998. Passive transfer, decay and protein specificity of equine arteritis virus antibodies in an endemically-infected standardbred herd. J. Am. Vet. Med. Assoc. 213:839-842.
36. Katz, J. B., A. L. Shafer, K. A. Eernisse, J. G. Landgraf, and E. A. Nelson. 1995. Antigenic differences between European and American isolates of porcine reproductive and respiratory syndrome virus (PRRSV) are encoded by the carboxy terminal portion of viral open reading frame 3. Vet. Microbiol. 44:65-76.
37. Kimura, M. 1980. A simple model for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120.
38. Kumar, S., K. Tamura, and M. Nei. 1993. MEGA: molecular evolutionary genetics analysis, version 1.01. The Pennsylvania State University, University Park, Pa.
39. Leroux, C., C. J. Issel, and R. C. Montelaro. 1997. Novel and dynamic evolution of equine infectious anemia virus genomic quasispecies associated with sequential disease cycles in an experimentally infected pony. J. Virol. 71:9627-9639.
40. Li, W. H. 1997. Molecular evolution. Sinauer Associates Inc., Sunderland, Mass.
41. Little, T. V., G. R. Holyoak, W. H. McCollum, and P. J. Timoney. 1992. Output of equine arteritis virus from persistently infected stallions is testosterone dependent, p. 225-229. In W. Plowright, P. D. Rossdale, and J. F. Wade (ed.), Proceedings of the 6th International Conference on Equine Infectious Diseases, Cambridge, 1991. R & W Publications, Newmarket, England.
42. Manzin, A., L. Solforosi, E. Petrelli, G. Macarri, G. Tosone, M. Piazza, and M. Clementi. 1998. Evolution of hypervariable region 1 of hepatitis C virus in primary infection. J. Virol. 72:6271-6276.
43. Mardassi, H., P. Gonin, C. A. Gagnon, B. Massie, and S. Dea. 1998. A subset of porcine reproductive and respiratory syndrome virus GP3 glycoprotein is released into the culture medium of cells as a non-virion-associated and membrane-free (soluble) form. J. Virol. 72:6298-6306.
44. McCollum, W. H., T. V. Little, P. J. Timoney, and T. W. Swerczek. 1994. Resistance of castrated male horses to attempted establishment of the carrier state with equine arteritis virus. J. Comp. Pathol. 111:383-388.
45. McCollum, W. H., and P. J. Timoney. 1984. The pathogenic qualities of the 1984 strain of equine arteritis virus, p. 34-84. In Proceedings of the Grayson Foundation International Conference of Thoroughbred Breeders Organizations, Ireland 1984.
46. McDonald, L. E., and N. H. Pineda. 1989. Veterinary endocrinology and reproduction, p. 5, 272-280. Lea & Febiger, Philadelphia, Pa.
47. Murphy, T. W., W. H. McCollum, and P. J. Timoney. 1992. Variation in the genomic RNA of equine arteritis virus during long term persistence in the stallion, p. 327. In W. Plowright, P. D. Rossdale, and J. F. Wade (ed.), Proceedings of the 6th International Conference on Equine Infectious Diseases, Cambridge 1991. R & W Publications, Newmarket, England.
48. Nei, M., and T. Gojobori. 1986. Simple methods for estimating the numbers of synonymous and non-synonymous nucleotide substitutions. Mol. Biol. Evol. 3:418-426.
49. Neu, S. M., P. J. Timoney, and W. H. McCollum. 1988. Persistent infection of the reproductive tract in stallions persistently infected with equine arteritis virus, p. 149-154. In D. G. Powell (ed.), Proceedings of the 5th International Conference of Equine Infectious Diseases, Lexington 1987. The University Press of Kentucky, Lexington, Ky.
50. Patton, J. F., U. B. R. Balasuriya, J. F. Hedges, T. M. Schweidler, P. J. Hullinger, and N. J. MacLachlan. Phylogenetic characterization of a highly attenuated strain of equine arteritis virus from the semen of a persistently infected standardbred stallion. Arch. Virol., in press.
51. Plana-Duran, J., I. Climent, A. Sarraseca, E. Urniza, E. Cortes, C. Vela, and J. I. Casal. 1998. Baculovirus expression of proteins of porcine reproductive and respiratory syndrome virus strain Olo/91. Involvement of ORF3 and ORF5 proteins in protection. Virus Genes 14:19-29.
52. Reed, L. J., and H. Muench. 1938. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 27:493-497.
53. 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.
54. Shivaji, S., K. H. Scheit, and P. M. Bhargava. 1990. Immunosupressive factors in seminal plasma, p. 375-389. In Proteins of seminal plasma and secretions of the male reproductive tract. John Wiley & Sons, New York, N.Y.
55. Smith, D. B., J. McAllister, C. Casino, and P. Simmonds. 1997. Virus 'quasispecies': making a mountain out of a molehill? J. Gen. Virol. 78:1511-1519.
56. Snijder, E. J., and H. van Tol. 1998. Personal communication.
57. Spindler, K., F. Horodyski, E. Grabau, S. Nichol, and S. Vandepol. 1982. Rapid evolution of RNA genomes. Science 215:1577-1585.
58. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
59. Timoney, P. J. 1984. Clinical, virological, and epidemiological features of the 1984 outbreak of equine viral arteritis in the Thoroughbred population in Kentucky, USA, p. 24-33. In Proceedings of the Grayson Foundation International Conference of Thoroughbred Breeders Organizations, Ireland 1984.
60. Timoney, P. J., and W. H. McCollum. 1988. Equine viral arteritis: epidemiology and control. J. Equine Vet. Sci. 8:54-59.
61. Timoney, P. J., and W. H. McCollum. 1993. Equine viral arteritis. Vet. Clin. North Am. Equine Pract. 9:295-309.
62. Timoney, P. J., W. H. McCollum, T. W. Murphy, A. W. Roberts, J. G. Willard, and G. D. Carswell. 1987. The carrier state in equine arteritis virus infection in the stallion with specific emphasis on the venereal mode of virus transmission. J. Reprod. Fertil. Suppl. 35:95-102.
63. Timoney, P. J., W. H. McCollum, A. W. Roberts, and T. W. Murphy. 1986. Demonstration of the carrier state in naturally acquired equine arteritis virus infection in the stallion. Res. Vet. Sci. 41:279-280.
64. van Berlo, M. F., P. J. M. Rottier, M. C. Horzinek, and B. A. M. van der Zeijst. 1986. Intracellular equine arteritis virus (EAV)-specific RNAs contain common sequences. Virology 152:492-496.
65. van Dinten, L. C., J. A. den Boon, A. L. M. Wassenaar, W. J. M. Spaan, and E. J. Snijder. 1997. An infectious arterivirus cDNA clone: identification of a replicase point mutation that abolishes discontinuous mRNA transcription. Proc. Natl. Acad. Sci. USA 94:991-996.