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Genetic Variability and Antigenic Diversity of Foot-and-Mouth Disease Virus

  • Esteban Domingo
  • Mauricio G. Mateu
  • Miguel A. Martínez
  • Joaquín Dopazo
  • Andrés Moya
  • Francisco Sobrino
Part of the Applied Virology Research book series (AVIR, volume 2)

Abstract

Foot-and-mouth disease (FMD) is an acute systemic disease of cloven-hooved animals, including cattle, swine, sheep, and goats. Despite mortality rates being generally below 5%, FMD severely decreases livestock productivity and trade. It is considered the economically most important disease of farm animals. Near two thousand million doses of vaccine are used annually to try to control FMD, which, nevertheless, is enzootic in most South American and African countries, parts of Asia, the Middle East, and the south of Europe. The causative agent, foot-and-mouth disease virus (FMDV), is an aphthovirus of the family Picornaviridae, a historically important virus as it was the first recognized viral agent (Loeffler and Frosch, 1898). In this chapter we review briefly the structure of FMDV and the organization and expression of its genome (Section II) and, in more detail, recent results on genetic variability (Section III) and antigenic diversity (Section V), reflected in several serotypes and subtypes of the virus. Such a diversity has implications for vaccine design and disease control, as discussed in Section V. Finally, we propose a model of evolution of FMDV and discuss its implications (Sections VI and VII).

Keywords

Cold Spring Harbor Laboratory Antigenic Site Antigenic Diversity Involve Amino Acid Synthetic Vaccine 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Acharya, R., Fry, F., Stuart, D., Fox, G., Rowlands, D., and Brown, F. (1989). Nature 337, 709–716.PubMedGoogle Scholar
  2. Adam, K. H., Kaaden, V. R., and Strohmaier, K. (1978). Biochem. Biophys. Res. Commun. 84, 677–683.PubMedGoogle Scholar
  3. Anderer, F. A., and Schlumberger, H. D. (1965). Biochim. Biophys. Acta 97, 503–509.PubMedGoogle Scholar
  4. Arrowsmith, A. E. M. (1977). In Developments in Biological Standardization, Vol. 35 (C. MacKowiak and R. H. Regamey, eds.), pp. 221–230, Karger, Basel.Google Scholar
  5. Augé de Mello, P., Honigman, M. H., Fernández, M. V., and Gomes, I. (1970). Bull. Off Int. Epizoot. 73, 489505.Google Scholar
  6. Bachrach, H. L. (1968). Annu. Rev. Microbiol. 22, 201–244.PubMedGoogle Scholar
  7. Bachrach, H. L. (1977). In Betsville Symposia in Agricultural Research. I. Virology in Agriculture (J. A. Romberger, ed.), pp. 3–22, Allanheld, Osmun, Montclair, NJ.Google Scholar
  8. Bachrach, H. L., Moore, D. M., McKercher, P. A., and Polatnick, J. (1975). J. Immunol. 115, 1636–1641.PubMedGoogle Scholar
  9. Bachrach, H. L., Morgan, D. O., and Moore, D. M. (1979). Intervirology 12, 65–72.PubMedGoogle Scholar
  10. Barnett, P. V., Ouldridge, E. J., Rowlands, D. J., Brown, J., and Parry, N. R. (1989). J. Gen. Virol. 70, 1483–1491.PubMedGoogle Scholar
  11. Batschelet, E., Domingo, E., and Weissmann, C. (1976). Gene 1, 27–32.PubMedGoogle Scholar
  12. Baxt, B., Morgan, D. O., Robertson, B. H., and Timpone, C. A. (1984). J. Virol. 51, 298–305.PubMedGoogle Scholar
  13. Baxt, B., Vakharia, V., Moore, D. M., Franke, A. J., and Morgan, D. O. (1989a). J. Virol. 63, 2143–2151.PubMedGoogle Scholar
  14. Baxt, B., Garmendia, A. E., and Morgan, D. O. (1989b). Viral Immunol. 2, 103–113.PubMedGoogle Scholar
  15. Beale, J. (1982). Nature 298, 14–15.PubMedGoogle Scholar
  16. Beck, E., and Strohmaier, K. (1987). J. Virol. 61, 1621–1629.PubMedGoogle Scholar
  17. Beck, E., Feil, G., and Strohmaier, K. (1983a). EMBO J. 2, 555–559.PubMedGoogle Scholar
  18. Beck, E., Forss, S., Strebel, K., Cattaneo, R., and Feil, G. (1983b). Nucleic Acids Res. 11, 7873–7885.PubMedGoogle Scholar
  19. Belsham, G. J., and Bostock, C. J. (1988). J. Gen. Virol. 69, 265–274.PubMedGoogle Scholar
  20. Bittle, J. L., Houghten, R. H., Alexander, H., Shinnick, T. M., Sutcliffe, J. G., Lerner, R. A., Rowlands, D. J., and Brown, F. (1982). Nature 298, 30–34.PubMedGoogle Scholar
  21. Boothroyd, J. C., Highfield, P. E., Cross, G. A. M., Rowlands, D. J., Lowe, P. A., Brown, F., and Harris, T. J. R. (1981). Nature 290, 800–802.PubMedGoogle Scholar
  22. Boothroyd, J. C., Harris, T. J. R., Rowlands, D. J., and Lowe, P. A. (1982). Gene 17, 153–161.PubMedGoogle Scholar
  23. Bolwell, C., Brown, A. L., Barnett, P. V., Campbell, R. O., Clarke, B. E., Parry, N. R., Ouldrige, E. J., Brown, F., and Rowlands, D. J. (1989a). J. Gen. Virol. 70, 45–57.PubMedGoogle Scholar
  24. Bolwell, C., Clarke, B. E., Parry, N. R., Ouldridge, E. J., Brown, F., and Rowlands, D. J. (1989b). J. Gen. Virol. 70, 59–68.PubMedGoogle Scholar
  25. Borca, M. V., Fernandez, F. M., Sadir, A. M., Braun, M., and Schudel, A. A. (1986). Immunology 59, 261–267.PubMedGoogle Scholar
  26. Britten, R. J. (1986). Science 231, 1393–1398.PubMedGoogle Scholar
  27. Broekhuijsen, M. P., Blom, T., Van Rijn, J., Pouwels, P. H., Klasen, E. A., Fasbender, M. J., and Enger-Valk, B. E. (1986). Gene 49, 189–197.PubMedGoogle Scholar
  28. Broekhuijsen, M. P., Van Rijn, J. M. M., Blom, A. J. M., Pouwels, P. H., Enger-Valk, B. E., Brown, F., and Francis, M. J. (1987). J. Gen. Virol. 68, 3137–3143.PubMedGoogle Scholar
  29. Brooksby, J. B. (1958). Adv. Virus Res. 5, 1–37.PubMedGoogle Scholar
  30. Brooksby, J. B. (1981a). In Virus diseases of food animals, Vol. 1 (E. P. J. Gibbs, ed.), pp. 69–78, Academic Press, London.Google Scholar
  31. Brooksby, J. B. (1981b). Nature 289, 535.PubMedGoogle Scholar
  32. Brooksby, J. B., and Rogers, J. (1957). In Methods of Typing and Cultivation of Foot-and-Mouth Disease Viruses,OEEC, Paris.Google Scholar
  33. Brown, A. L., Campbell, R. O., and Clarke, B. E. (1989). Gene 75, 225–234.PubMedGoogle Scholar
  34. Brown, F. (1979). In The Molecular Biology of Picornaviruses (R. Perez-Bercoff, ed.), pp. 49–72, Plenum Press, New York.Google Scholar
  35. Brown, F. (1988). Vaccine 8, 180–182.Google Scholar
  36. Brown, F. (1989). In Molecular Aspects of Picornavirus Infection and Detection (B. L. Semler and E. Ehrenfeld, eds.), pp. 179–191, ASM, Washington, DC.Google Scholar
  37. Brown, F., Newman, J. F. E., Stott, J., Porter, A., Frisby, D., Newton, C., Carey, N., and Fellner, P. (1974). Nature 251, 342–344.PubMedGoogle Scholar
  38. Burrows, R. (1966). J. Hyg. 64, 81–90.PubMedGoogle Scholar
  39. Burrows, R., Mann, J. A., Garland, A. J. M., Greig, A., and Goodridge, D. (1981). J. Comp. Pathol. 91, 599–609.PubMedGoogle Scholar
  40. Callis, J. J. (1979). Foot-and-mouth disease. A world problem. Proceedings of the 83rd Annual Meeting of the United States Animal Health Association, pp. 261–269.Google Scholar
  41. Callis, J. J., and McKercher, P. D. (1985). In Fiebre aftosa, Bovis, Vol. 3 ( J. M. Sanchez-Vizcaíno, ed.), Luzân S. A. de Ediciones, Madrid.Google Scholar
  42. Capel-Edwards, M. (1971). J. Comp. Path. 81, 433–438.PubMedGoogle Scholar
  43. Carrillo, C., Dopazo, J., Moya, A., Gonzalez, M., Martínez, M. A., Saiz, J. C., and Sobrino, F. (1990). Virus Res. 15, 45–56.PubMedGoogle Scholar
  44. Carroll, A. R., Rowlands, D. J., and Clarke, B. E. (1984). Nucleic Acids Res. 12, 2461–2472.PubMedGoogle Scholar
  45. Cheung, A. K., and Upper, H. (1984). Biotechnol. Genetic Engineering Rev. 1, 223–259.Google Scholar
  46. Cheung, A., DeLaMarter, J., Weiss, S., and Upper, H. (1983). J. Virol. 48, 451–459.PubMedGoogle Scholar
  47. Cheung, A. K., Whitehead, P., Weiss, S., and Upper, H. (1984). Gene 30, 241–245.PubMedGoogle Scholar
  48. Chow, M., Newman, J. F. E., Felman, D., Hogle, J. M., Rowlands, D. J., and Brown, F. (1987). Nature 327, 482–486.PubMedGoogle Scholar
  49. Ciaccio, G. (1963). Ann. Inst. Pasteur 104, 529–534.Google Scholar
  50. Clarke, B. E., and Sangar, D. V. (1988). J. Gen. Virol. 69, 2313–2325.PubMedGoogle Scholar
  51. Clarke, B. E., Carroll, A. P., Rowlands, D. J., Nicholson, B. H., Houghten, R. A., Lerner, R. A., and Brown, F. (1983). FEBS Lett. 157, 261–264.PubMedGoogle Scholar
  52. Clarke, B. E., Brown, A. L., Currey, R. M., Newton, S. E., Rowlands, D. J., and Carroll, A. R. (1987a). Nucleic Acids Res. 15, 7067–7079.PubMedGoogle Scholar
  53. Clarke, B. E., Newton, S. E., Carroll, A. R., Francis, M. J., Appleyard, G., Syred, A. D., Highfield, P. E., Rowlands, D. J., and Brown, F. (19876). Nature 330, 381–384.Google Scholar
  54. Clarke, B. E., Carroll, A. R., Francis, M. J., Appleyard, G., Syred, A. D., Highfield, P. E., Rowlands, D. J., and Brown, F. (1988). In Vaccines 88 (H. Ginsberg, F. Brown, R. A. Lerner, and R. M. Chanock, eds.), pp. 127–131, Cold Spring Harbor Laboratory, New York.Google Scholar
  55. Cloyd, M. W., and Holt, M. J. (1987). Virology 161, 286–292.PubMedGoogle Scholar
  56. Collen, T., Pullen, L., and Doel, T. R. (1989). J. Gen. Virol. 70, 395–403.PubMedGoogle Scholar
  57. Condy, J. B., Hedger, R. S., Hamblin, C., and Barnett, I. T. R. (1985). Comp. Immunol. Microbial. Infect. Dis. 8, 259–265.Google Scholar
  58. Cosby, S. L., McQuaid, S., Duffy, N., Lyons, C., Rima, B. K., Allan, G. M., McCullough, S. J., Kennedy, S., Smyth, J. A., and McNeilly, F. (1988). Nature 36, 115–116.Google Scholar
  59. Costa Giorni, M. P., Bergmann, 1. E., Scodeller, E. A., Augé de Mello, P., Gomes, I., and La Torre, J. L. (1984). J. Viro!. 51, 799–805.Google Scholar
  60. Costa Giorni, M. P., Gomes, I., Tiraboschi, B., Auge de Mello, P., Bergmann, I. E., Scodeller, E. A., and La Torre, J. L. (1988). Virology 162, 58–64.Google Scholar
  61. Dawe, P. S., and King, A. M. Q. (1983). Arch. Virol. 76, 117–126.PubMedGoogle Scholar
  62. Dayhoff, M. O., Eck, R. V., and Park, C. M. (1972). In Atlas of Protein Sequence and Structure, Vol. 5 (M. O. Dayhoff, ed.), pp. 89–99, National Biomedical Research Foundation, Washington, DC.Google Scholar
  63. de la Torre, J. C., and Domingo, E. (1988). Microbial. SEM 4, 161–166.Google Scholar
  64. de la Torre, J. C., Davila, M., Sobrino, F., Ortín, J., and Domingo, E. (1985). Virology 145, 24–35.PubMedGoogle Scholar
  65. de la Torre, J. C., Alarcón, B., Martínez-Salas, E., Carrasco, L., and Domingo, E. (1987). J. Viro!. 61, 233–235.Google Scholar
  66. de la Torre, J. C., Martínez-Salas, E., Díez, J., Villaverde, A., Gebauer, F., Rocha, E., Davila, M., and Domingo, E. (1988). J. Virol. 62, 2050–2058.PubMedGoogle Scholar
  67. de la Torre, J. C., de la Luna, S., Díez, J., and Domingo, E. (1989a). J. Viral. 63, 2385–2387.Google Scholar
  68. de la Torre, J. C., Martínez-Salas, E., Díez, J., and Domingo, E. (19896). J. Virol. 63, 59–63.Google Scholar
  69. DePolo, N. J., Giachetti, C., and Holland, J. J. (1987). J. Viral. 61, 454–464.Google Scholar
  70. Devaney, M. A., Vakharia, V. N., Lloyd, R. E., Ehrenfeld, E., and Grubman, M. J. (1988). J. Viro!. 62, 4407–4409.Google Scholar
  71. Di Girolamo, W., Salas, M., and Laguens, R. P. (1985). Arch. Viro!. 83, 331–336.Google Scholar
  72. Di Marchi, R., Brooke, G., Gale, C., Cracknell, V., Doel, T., and Mowat, N. (1986). Science 232, 639–641.Google Scholar
  73. Dietzshold, B., Kaaden, O. R., Tokui, T., and Bohm, H. C. (1971). J. Gen. Viro!. 13, 1–7.Google Scholar
  74. Díez, J., Mateu, M. G., and Domingo, E. (1989). J. Gen. Viro!. 70, 3281–3289.Google Scholar
  75. Dinter, Z., Philipson, L., and Wesslen, T. (1959). Virology 8, 542–544.PubMedGoogle Scholar
  76. Doel, T. R., Gale, C., Brooke, G., and Di Marchi, R. (1988). J. Gen. Viral. 69, 2403–2406.Google Scholar
  77. Domier, L., Shaw, J. G., and Rhoads, R. E. (1987). Virology 158, 20–27.PubMedGoogle Scholar
  78. Domingo, E. (1989). In Progress in Drug Research, Vol. 33 (E. Jucker, ed.), pp. 93–13. 3, Birkhüuser Verlag, Basel.Google Scholar
  79. Domingo, E., and Holland, J. J. (1988). In RNA Genetics, Vol. III. Variability of RNA Genomes (E. Domingo, J. J. Holland, and P. Ahlquist, eds.), pp. 3–36, CRC Press, Boca Raton, FL.Google Scholar
  80. Domingo, E., Flavell, R. A., and Weissmann, C. (1976). Gene 1, 3–25.PubMedGoogle Scholar
  81. Domingo, E., Sabo, D., Taniguchi, T., and Weissmann, C. (1978). Cell 13, 735–744.PubMedGoogle Scholar
  82. Domingo, E., Davila, M., and Ortín, J. (1980). Gene 11, 333–346.PubMedGoogle Scholar
  83. Domingo, E., Martínez-Salas, E., Sobrino, F., de la Torre, J. C., Portela, A., Ortín, J., López-Galindez, C., Pérez-Brefia, P., Villanueva, N., Nâjera, R., VandePol, S., Steinhauer, D., De Polo, N., and Holland, J. J. (1985). Gene 40, 1–8.PubMedGoogle Scholar
  84. Donaldson, A. (1987). Irish Vet. J. 41, 325–327.Google Scholar
  85. Donaldson, A. I., Gibson, C. F., Oliver, R., Hamlin, C., and Kitching, R. P. (1987). Res. Vet. Sci. 43, 339–346.PubMedGoogle Scholar
  86. Dopazo, J., Sobrino, F., Palma, E. L., Domingo, E., and Moya, A. (1988). Proc. Natl. Acad. Sci. USA 85, 6811–6815.PubMedGoogle Scholar
  87. Duchesne, M., Cartwright, T., Crespo, A., Boucher, F., and Fallourd, A. (1984). J. Gen. Virol. 65, 1559–1566.PubMedGoogle Scholar
  88. Eigen, M. (1971). Naturwissenschaften 58, 465–523.PubMedGoogle Scholar
  89. Eigen, M. (1987). Cold Spring Harbor Symp. Quant. Biol. 52, 307–320.PubMedGoogle Scholar
  90. Eigen, M., and Biebricher, C. K. (1988). In RNA Genetics. Vol. III. Variability of RNA Genomes (E. Domingo, J. J. Holland, and P. Ahlquist, eds.), pp. 211–245, CRC Press, Boca Raton, FL.Google Scholar
  91. Eigen, M., and Schuster, P. (1979). The Hypercycle, Springer, Berlin.Google Scholar
  92. Fagg, R. M., and Hyslop, N. S. G. (1966). J. Hyg. 64, 397–404.PubMedGoogle Scholar
  93. Forss, S., and Schaller, H. (1982). Nucleic Acids Res. 10, 6441–6450.PubMedGoogle Scholar
  94. Forss, S., Strebel, K., Beck, E., and Schaller, H. (1984). Nucleic Acids Res. 12, 6587–6601.PubMedGoogle Scholar
  95. Fox, G., Stuart, D., Acharya, K. R., Fry, E., Rowlands, D., and Brown, F. (1987). J. Mol. Biol. 196, 591–597.PubMedGoogle Scholar
  96. Fox, G., Parry, N. R., Barnett, P. V., McGinn, B., Rowlands, D. J., and Brown, F. (1989). J. Gen. Virol. 70, 625–637.PubMedGoogle Scholar
  97. Francis, M. J., Fry, C. M., Rowlands, D. J., Bittle, J. L., Houghten, R. A., Lerner, R. A., and Brown, F. (1987a). Immunology 61, 1–6.PubMedGoogle Scholar
  98. Francis, M. J., Fry, C. M., Clarke, B. E., Rowlands, D. J., Brown, F., Bittle, J. L., Houghten, R. A., and Lerner, R. A. (1987b). In Vaccines 87 (R. M. Channock, H. Ginsberg, R. A. Lerner, and F. Brown, eds.), pp. 60–67, Cold Spring Harbor Laboratory, New York.Google Scholar
  99. Francis, M. J., Hastings, G. Z., Syred, A. D., McGinn, B., Brown, F., and Rowlands, D. J. (1987c). Nature 330, 168–170.PubMedGoogle Scholar
  100. Francis, M. J., Hastings, G. Z., Syred, A. D., McGinn, B., Brown, F., and Rowlands, D. J. (1988). In Vaccines 88 (H. Ginsberg, F. Brown, R. A. Lerner, and R. M. Chanock, eds.), pp. 1–7, Cold Spring Harbor Laboratory, New York.Google Scholar
  101. Gailiunas, P. (1968). Arch. ges. Virusforsch. 25, 188–200.PubMedGoogle Scholar
  102. Gaschutz, S., Hess, G., and Wittmann, G. (1986). In Report of the Session of the Research Group of the Standing Technical Committee of the European Commission for the Control of Foot-and-Mouth Disease, Madrid, pp. 9–11, FAO, Rome.Google Scholar
  103. Gebauer, F., de la Torre, J. C., Gomes, I., Mateu, M. G., Barahona, H., Tiraboschi, B., Bergmann, 1., Auge de Mello, P., and Domingo, E. (1988). J. Virol. 62, 2041–2049.PubMedGoogle Scholar
  104. Geysen, H. M., Meloen, R. H., and Barteling, S. J. (1984). Proc. Natl. Acad. Sci. USA 81, 3998–4002.PubMedGoogle Scholar
  105. Geysen, H. M., Barteling, S. J., and Meloen, R. H. (1985). Proc. Natl. Acad. Sci. USA 82, 178–182.PubMedGoogle Scholar
  106. Geysen, H. M., Rodda, S. J., Mason, T. J., Tribbick, G., and Schoofs, P. G. (1987). J. Immunol. Methods 102, 259–274.PubMedGoogle Scholar
  107. Gibson, C. F., and Donaldson, A. I. (1986). Res. Vet. Sci. 41, 45–49.PubMedGoogle Scholar
  108. Gomes, I., and Rosenberg, F. J. (1984). Preventive Vet. Med. 3, 197–205.Google Scholar
  109. Grubman, M. J., and Morgan, D. O. (1986). Virus Res. 6, 33–43.PubMedGoogle Scholar
  110. Harrison, S. C. (1989). Nature 338, 205–206.PubMedGoogle Scholar
  111. Hedger, R. S., and Condy, J. B. (1985). Vet. Rec. 117, 205.PubMedGoogle Scholar
  112. Hedger, R. S., and Stubbins, A. G. J. (1971). State Vet. J. 26, 45–50.Google Scholar
  113. Holland, J. J., Grabau, E. A., Jones, C. L., and Semler, B. L. (1979). Cell 16, 495–504.PubMedGoogle Scholar
  114. Holland, J. J., Spindler, K., Horodyski, F., Grabau, E., Nichol, S., and VandePol, S. (1982). Science 215, 1577–1585.PubMedGoogle Scholar
  115. Horodyski, F. M., Nichol, S. T., Spindler, K. R., and Holland, J. J. (1983). Cell 33, 801–810. Hyslop, N. St. G. (1965). J. Gen. Microbiol. 41, 135–142.Google Scholar
  116. Hyslop, N. St. G. (1970). Adv. Vet. Sci. Comp. Med. 14, 261–307.PubMedGoogle Scholar
  117. Jackson, R. J. (1989). In Molecular Aspects of Picornavirus Infection and Detection (B. L. Semler and E. Ehrenfeld, eds.), pp. 51–71, ASM, Washington, DC.Google Scholar
  118. Joubert, L., and Mackowiak, C. (1968). La Fievre Aphteuse, Expansion Scientifique Française. Kaaden, O. R., Adam, K. H., and Strohmaier, K. (1977). J. Gen. Virol. 34, 397–400.Google Scholar
  119. King, A. M. Q. (1988). In RNA Genetics. Vol. II. Retroviruses, Viroids, and RNA Recombination (E. Domingo, J. J. Holland, and P. Ahlquist, eds.), pp. 149–165, CRC Press, Boca Raton, FL.Google Scholar
  120. King. A. M. Q., Underwood, B. O., McCahon, D., Newman, J. W. I., and Brown, F. (1981). Nature 293, 479–480.Google Scholar
  121. King, A. M. Q., McCahon, D., Slade, W. R., and Newman, J. W. I. (1982). Cell 29, 921–928.PubMedGoogle Scholar
  122. King, A. M. Q., Underwood, B. O., McCahon, D., Newman. J. W. I., and Slade, W. R. (1985). Virus Res. 3, 373–384.PubMedGoogle Scholar
  123. Kitching, R. P., Rendlc, R., and Ferris, N. P. (1988). Vaccine 6, 1–6.Google Scholar
  124. Kitching, R. P., Knowles, N. J., Samuel. A. R., and Donaldson, A. 1. (1989). Trop. Animal Health Production 21, 153–166.Google Scholar
  125. Kitson, J. D. A., Belsham, G. J., Burke, K. L., and Almond, J. W. (1989). Abstracts of the 6th Meeting of the European Group of Molecular Biology of Picornaviruses, Bruges, Belgium, Abstract E12.Google Scholar
  126. Kleid, D. G., Yansura, D., Small, B., Dowbenko, D., Moore, D. M., Grubman, M. J., McKercher, P. D., Morgan, D. O., Robertson, B. H., and Bachrach, H. L. (1981). Science 214, 1125–1129.PubMedGoogle Scholar
  127. Köpper, H., Keller, W., Kurz, C., Forss, S., Schaller, H., Franze, R., Strohmaier, K., Marquardt, O., Zaslaysky, V. G., and Hofschneider, H. (1981). Nature 289, 555–559.Google Scholar
  128. Kurz, C., Forss, S., Küpper, H., Strohmaier, K., and Schaller, H. (1981). Nucleic Acids Res. 9, 1919–1931.PubMedGoogle Scholar
  129. La Torre, J. L., Grubmann, M. J., Baxt, B., and Bachrach, H. L. (1980). Proc. Natl. Acad. Sci. USA 77, 7444–7447.PubMedGoogle Scholar
  130. Laplace, E., Rey-Senelonge, A., Kohen, G., and Rivière, M. (1987). In Report of the Session of the Research Group of the Standing Technical Committee of the European Commission for the Control of Foot-andMouth Disease, Lyons, pp. 117–119, FAO, Rome.Google Scholar
  131. Laporte, J., Grosclaude, J., Wantyghem, J., Bernard, S., and Rouze, P. (1973). Co. r. hebdorna. seeinces Acad. Sci. Paris 276, 3390–3401.Google Scholar
  132. Loeffler, F., and Frosch, P. (1898). Zentralbl. Bacterial. Parasitenkunde Infektionskrankh. 23, 371–391.Google Scholar
  133. Luo, M., Vriend, G., Kamer, G., Minor, 1., Arnold, E., Rossmann, M. G., Boege, U., Scraha, D. G.. Duke, G. M., and Palmenberg, A. C. (1987). Science 235, 182–191.PubMedGoogle Scholar
  134. Luo, M., Rossmann, M. G., and Palmenberg, A. C. (1988). Virology 166, 503–514.PubMedGoogle Scholar
  135. Mahy, B. W. J., Barrett, T., Evans, S., Anderson, E. C., and Bostock, C. J. (1988). Nature 336, 115.Google Scholar
  136. Makoff, A. J., Poynter, C. A., Rowlands, D. J., and Boothroyd, J. C. (1982). Nucleic Acids Res. 10, 8285–8295.PubMedGoogle Scholar
  137. Marquardt, O., and Adam, K. H. (1988). Virus Genes 2, 283–291.Google Scholar
  138. Martínez, M. A., Carrillo, C., Plana, J., Mascarella, R., Bergadâ, J., Palma, E. L., Domingo, E., and Sabrina, F. (1988). Gene 62, 75–84.PubMedGoogle Scholar
  139. Martínez-Salas, E., Ortín, J., and Domingo, E. (1985). Gene 35, 55–61.PubMedGoogle Scholar
  140. Matou, M. G., Rocha, E., Vicente, O., Vayreda, F., Navalpotro. C., Andreu, O., Pedrosa, E., Giralt, E., Enjuanes, L., and Domingo, E. (1987). Virus Res. 8, 261–274.Google Scholar
  141. Mateu, M. G., da Silva, J. L., Rocha, E., de Brum, D. I.., Alonso, A., Enjuanes, L., Domingo, E., and Barahona, H. (1988). Virology 167, 113–124.Google Scholar
  142. Mateu, M. G., Martínez, M. A., Rocha, E., Andreu, D., Parejo, J., Giralt, E., Sobrino, F., and Domingo, E. (1989). Proc. Natl. Acad. Sci. USA 86, 5883–5887.PubMedGoogle Scholar
  143. Mateu, M. G., Martínez, M. A., Capucci, L., Andreu, D., Giralt, E., Sobrino, F., Bracchi, E., and Domingo, E. (1990). J. Gen. Viral. (in press).Google Scholar
  144. McCahon, D., King, A. M. Q., Roe, D. S., Slade, W. R., Newman, J. W. I., and Cleary, A. M. (1985). Virus Res. 3, 87–100.PubMedGoogle Scholar
  145. McCahon, D., Crowther, J. R., Belsham, G. J., Kitson, J. D. A., Duchesne, M., Have, P., Meloen, R. H., Morgan, D. O., and De Simone, F. (1989). J. Gen. Viral. 70, 639–645.Google Scholar
  146. McCullough, K. C., Crowther, J. R., Butcher, R. N., Carpenter, W. C., Brocchi, E., Capucci, L., and De Simone, F. (1986). Immunology 58, 421–428.PubMedGoogle Scholar
  147. McCullough, K. C., Crowther, J. R., Carpenter, W. C., Bracchi, E., Capucci, L., De Simone, F., Xie, Q., and McCahon, D. (1987). Virology 157, 516–525.PubMedGoogle Scholar
  148. McVicar, J. W., and Sutmoller, P. (1976). J. Hvg. 76, 467–481.Google Scholar
  149. Mellor, E. J. C., Brown, F., and Harris, T. J. R. (1985). J. Gen. Viral. 66, 1919–1929.Google Scholar
  150. Meloen. R. H., and Barteling, S. J. (1986a). Virology 149, 55–63.Google Scholar
  151. Meloen, R. H., and Barteling, S. J. (1986b). J. Gen. Virol. 67, 289–294.PubMedGoogle Scholar
  152. Meloen, R. H., Rowlands, D. J., and Brown, F. (1979). J. Gen. Virol. 45, 761–763.PubMedGoogle Scholar
  153. Meloen, R. H., Briaire, J., Woortmeyer, R. J., and Van Zaane, D. (1983). J. Gen. Virol. 64, 1193–1198.PubMedGoogle Scholar
  154. Meloen, R. H., Puyk, W. C., Meijer, D. J. A., Lankhof, H., Posthumus, W. P. A., and Schaaper, W. M. M. (1986). Protides Biol. Fluids Proc. Colloq. 34, 103–106.Google Scholar
  155. Meloen, R. H., Puyk, W. C., Meijer, D. J. A., Lankhof, H., Posthumus, W. P. A., and Schaaper, W. M. M. (1987). J. Gen. Virol. 68, 305–314.PubMedGoogle Scholar
  156. Meloen, R. H., Puyk, W. C., Posthumus, W. P. A., Lankhof, H., Thomas, A., and Schaaper, W. M. M. (1988). In Vaccines 88 (H. Ginsberg, F. Brown, R. A. Lerner, and R. M. Chanock, eds.), pp. 35–40, Cold Spring Harbor Laboratory, New York.Google Scholar
  157. Meyerhans, A., Cheynier, R., Albert, J., Seth, M., Kwok, S., Sninsky, J., Morfeldt-Manson, L., Asjö, B., and Wain-Hobson, S. (1989). Cell 58, 901–910.PubMedGoogle Scholar
  158. Newton, S. E., Carroll, A. R., Campbell, R. D., Clarke, B. E., and Rowlands, D. J. (1985). Gene 40, 331–336.PubMedGoogle Scholar
  159. Newton, S. E., Francis, M. J., Brown, F., Appleyard, G., and Mackett, M. (1986). In Vaccines 86 (F. Brown, R. M. Chanock, and R. A. Lerner, eds.), pp. 303–309, Cold Spring Harbor Laboratory, New York. Newton, S. E., Clarke, B. E., Appleyard, G., Francis, M. J., Carroll, A. R., Rowlands, D. J., Skehel, J., and Brown, F. (1987). In Vaccines 87 ( R. M. Chanock, R. A. Lemer, F. Brown and H. Ginsberg, eds.), pp. 12–21. Cold Spring Harbor Laboratory, New York.Google Scholar
  160. O’Hara, P. J., Horodyski, F. M., Nichol, S. J., and Holland, J. J. (1984a). J. Virol. 49, 793–798.PubMedGoogle Scholar
  161. O’Hara, P. J., Nichol, S. T., Horodyski, F. M., and Holland, J. J. (1984b). Cell 36, 915–924.PubMedGoogle Scholar
  162. Onishchenko, A. M., Petrova, N. A., Blinov, V. M., Vassilenko, S. K., Sandakhchiev, L. S., Burdov, A. N., Ivanyushchenkov, V. N., and Perevozchikova, N. A. (1986). Bioorganicheskóya Khimiya 12, 416–419.Google Scholar
  163. Ouldridge, E. J., Barnett, P. V., Parry, N. R., Syred, A. D., Head, M., and Rweyemamu, M. M. (1984). J. Gen. Virol. 65, 203–207.PubMedGoogle Scholar
  164. Palmenberg, A. (1989). In Molecular Aspects of Picornavirus Infection and Detection (B. L. Semler and E. Ehrenfeld, eds.), pp. 211–241, ASM, Washington, DC.Google Scholar
  165. Parry, N. R. (1982). Ph.D. thesis. Studies on plaque variation of foot-and-mouth disease virus, University of London.Google Scholar
  166. Parry, N. R., Ouldridge, E. J., Barnett, P. V., Rowlands, D. J., Brown, F., Bittle, J. L., Houghten, R. A., and Lerner, R. A. (1985). In Vaccines 85 (R. A. Lerner, R. M. Chanock, and F. Brown, eds.), pp. 211–216, Cold Spring Harbor Laboratory, New York.Google Scholar
  167. Parry, N. R., Barnett, P. V., Ouldridge, E. J., Rowlands, D. J., and Brown, F. (1989a). J. Gen. Virol. 70, 1493–1503.PubMedGoogle Scholar
  168. Parry, N. R., Ouldridge, E. J., Barnett, P. V., Fox, J. D., Francis, M. J., Rowlands, D. J., and Brown, F. (1989b). Abstracts of the 6th Meeting of the European Group of Molecular Biology of Picornaviruses, Bruges, Belgium, Abstract D13.Google Scholar
  169. Pereira, H. G. (1977). In Developments in Biological Standardization, Vol. 35 (C. MacKowiak and R. H. Regamey, eds.), pp. 167–174, Karger, Basel.Google Scholar
  170. Pereira, H. G. (1981). In Virus Diseases of Food Animals, Vol. 2 (E. P. J. Gibbs, ed.), pp. 333–363, Academic Press, London.Google Scholar
  171. Pfaff, E., Mussgay, M., Böhm, H. O., Schultz, G. E., and Schaller, H. (1982). EMBO J. 1, 869–874.PubMedGoogle Scholar
  172. Pfaff, E., Kuhn, C., Schaller, H., Leban, J., Thiel, H. J. and Böhm, H. O. (1985). In Vaccines 85 ( R. A. LernerGoogle Scholar
  173. R. M. Chanock, and F. Brown, eds.), pp. 199–202, Cold Spring Harbor Laboratory, New York. Pfaff, E., Thiel, H-J., Beck, E., Strohmaier, K., and Schaller, H. (1988). J. Virol. 62, 2033–2040.Google Scholar
  174. Piccone, M. E., Kaplan, G., Giavedoni, L., Domingo, E., and Palma, E. L. (1988). J. Virol. 62, 1469–1473.PubMedGoogle Scholar
  175. Pincus, S. E., Rohl, H., and Wimmer, E. (1987). Virology 157, 83–88.PubMedGoogle Scholar
  176. Polatnick, J. (1980). J. Virol. 33, 774–779.PubMedGoogle Scholar
  177. Polatnick, J., Arlinghaus, R. B., Graves, J. H., and Cowan, K. M. (1967). Virology 31, 609–615.PubMedGoogle Scholar
  178. Porter, A. G., Fellner, P., Black, D. N., Rowlands, D. J., Harris, T. J. R., and Brown, F. (1978). Nature 276, 298–301.PubMedGoogle Scholar
  179. Prabhakar, B. S., Haspel, M. V., McClintock, P. R., and Notkins, A. L. (1982). Nature 300, 374–376.PubMedGoogle Scholar
  180. Prabhakar, B. S., Menegus, M. A., and Notkins, A. L. (1985). Virology 146, 302–306.PubMedGoogle Scholar
  181. Reanney, D. C. (1984). In The Microbe, Part I (B. W. J. Mahy and J. R. Pattison, eds.), pp. 175–196, Cambridge University Press, Cambridge, MA.Google Scholar
  182. Robertson, B. H., Morgan, D. 0., and Moore, D. M. (1984). Virus Res. 1, 489–500.PubMedGoogle Scholar
  183. Robertson, B. H., Grubman, M. J., Wendell, G. N., Moore, D. H., Welsh, J. D., Fischer, T., Dowbenko, D. J., Yansura, D. G., Small, B., and Kleid, D. G. (1985). J. Virol. 54, 651–660.PubMedGoogle Scholar
  184. Robson, K. J. H., Harris, T. J. R., and Brown, F. (1977). J. Gen. Virol. 37, 271–276.Google Scholar
  185. Robson, K. J. H., Crowther, J. R., King, A. M. Q., and Brown, F. (1979). J. Gen. Virol. 45, 579–590.PubMedGoogle Scholar
  186. Rossmann, M. G., and Rueckert, R. R. (1987). Microbiol. Sci. 4, 206–214.PubMedGoogle Scholar
  187. Rowlands, D. J., Harris, T. J. R., and Brown, F. (1978). J. Virol. 26, 335–343.PubMedGoogle Scholar
  188. Rowlands, D. J.. Clarke, B. E., Carroll, A. R., Brown, F., Nicholson, B. H., Bittle, J. L., Houghten, R. A., and Lerner, R. A. (1983). Nature 306, 694–697.PubMedGoogle Scholar
  189. Rweyemamu, M. M. (1984). J. Biol. Stand. 12, 323–337.PubMedGoogle Scholar
  190. Saiz, J. C., Gonzalez, M. J., Morgan, D. O., Card, J. L., Sobrino, F., and Moore, D. M. (1989). VirusRes. 13, 45–60.Google Scholar
  191. Sangar, D. V. (1979). J. Gen. Viro!. 45, I - 13.Google Scholar
  192. Sangar, D. V., Black, D. N., Rowlands, D. J., Harris, T. J. R., and Brown, F. (1980). J. Viro!. 33, 59–68.Google Scholar
  193. Sangar. D. V., Newton, S. E., Rowlands, D. J., and Clarke, B. E. (1987). Nucleic Acids Res. 15, 3305–3315.Google Scholar
  194. Sangar, D. V., Clark, R. P., Carroll, A. R., Rowlands, D. J., and Clarke, B. E. (1988). J. Gen. Virol. 69, 2327–2333.PubMedGoogle Scholar
  195. Saunders, K., King, A. M. Q., McCahon, D., Newman, J. W. I., Slade, W. R., and Forss, S. (1985). J. Viral. 56, 921–929.Google Scholar
  196. Schwartz, R. H. (1986). Curr. Topics Microbiol. Imrnunol. 130, 79–85.Google Scholar
  197. Seibold, H. R., Cottral, G. E., Patty, R. E., and Gailiunas, P. (1964). Am. J. Vet. Re.s. 25, 806–814. Sellers, R. F. (1971). Vet. Bull. 41, 431–439.Google Scholar
  198. Sellers, R. F. (1981). In Virus Diseases of Food Animals, Vol. 1 (E. P. J. Gibbs, ed.), pp. 19–29, Academic Press, London.Google Scholar
  199. Semler, B. L., Kuhn, R. J., and Wimmer, E. (1988). In RNA Genetics. Vol. I. RNA-Directed Virus Replication (E. Domingo, J. J. Holland, and P. Ahlquist, eds.), pp. 23–48, CRC Press, Boca Raton, FL.Google Scholar
  200. Shahan, M. S. (1962). Ann. NY Acad. Sci. 101, 445–454.Google Scholar
  201. Singh, B. S. (1969). NZ Vet. J. 17, 173–177.Google Scholar
  202. Smith, D. B., and Inglis, S. C. (1987). J. Gen. Viral. 68, 2729–2740.Google Scholar
  203. Smith, F. I., and Palese, P. (1988). In RNA Genetics. Vol. III. Variability of RNA Genomes (E. Domingo, J. J. Holland, and P. Ah]quist, eds.), pp. 123–135. CRC Press, Boca Raton, FL.Google Scholar
  204. Sobrino, F., Davila, M., Ort(n, J., and Domingo, E. (1983). Virology 128, 310–318.PubMedGoogle Scholar
  205. Sobrino, F., Palma, E. L., Beck, E., Davila, M., de la Torre, J. C., Negro, P., Villanueva, N., Ortín, J., and Domingo, E. (1986). Gene 50, 149–159.PubMedGoogle Scholar
  206. Sobrino, F., Martínez, M. A., Carrillo, C., and Beck, E. (1989). Virus Res. 14, 273–280.PubMedGoogle Scholar
  207. Spindler, K. R., Horodyski, F. M., and Holland, J. J. (1982). Virology 119, 96–108.PubMedGoogle Scholar
  208. Stave, J. W., Card, J. L., and Morgan, D. O. (1986). J. Gen. Viral. 67, 2083–2092.Google Scholar
  209. Stave, J. W., Card, J. L., Morgan, D. O., and Vakharia, V. N. (1988). Virology 162, 21–29.PubMedGoogle Scholar
  210. Steinhauer, D., and Holland, J. J. (1986). J. Viral. 57, 219–228.Google Scholar
  211. Steinhauer, D., and Holland, J. J. (1987). Annu. Rev. Microbial. 41, 409–433.Google Scholar
  212. Steinhauer, D., de la Torre, J. C., and Holland, J. J. (1989a). J. Viral. 63, 2063–2071.Google Scholar
  213. Steinhauer, D., de la Torre, J. C., Meier, E., and Holland, J. J. (1989b). J. Virol. 63, 2072–2080.PubMedGoogle Scholar
  214. Strauss, J. H., and Strauss, E. G. (1988). Annu. Rev. Microbial. 42, 657–668.Google Scholar
  215. Strebe], K., and Beck, E. (1986). J. Virol. 58, 893–899.Google Scholar
  216. Strohmaier, K., Franze, R., and Adam, K. H. (1982). J. Gen. Virol. 59, 295–306.PubMedGoogle Scholar
  217. Sutcliffe, J. G., Shinnick, T. M., Green, N., and Lerner, R. (1983). Science 219, 660–666. Sutmoller, P., and Gaggero, A. (1965). Vet. Ree. 77, 968–969.Google Scholar
  218. Sutmoller, P., and McVicar, J. W. (1976). J. Hyg. 77, 235–243.Google Scholar
  219. Sutmoller, P., McVicar, J. W., and Cottral, G. E. (1968). Arch. Ges. Virusfarsch. 23, 227–235.Google Scholar
  220. Takeda, N., Miyamura, K., Ogino, T., Natori, K., Yamazaki, S., Sakwiai, N., Nakazono, N., Ishii, K., and Kono, R. (1984). Virology 134, 375–388.PubMedGoogle Scholar
  221. Thomas, A. A. M., Woortmeijer, R. J., Puijk, W., and Barteling, S. J. (1988). J. Viral. 62, 2782–2789.Google Scholar
  222. Timoney, J. F., Gillespie, J. H., Scott, F. W., and Barlough, J. E. (1988). Hagan and Bruner’.s Microbiology and Infectious Diseases of Domestic Animals, pp. 647–667, Comstock Publishing Associates, Cornell University Press, Ithaca, London.Google Scholar
  223. Vakharia, V. N., Devaney, M. A., Moore, D. M., Dunn, J. J., and Grubman, M. J. (1987). J. Viro!. 61, 3199–3207.Google Scholar
  224. Vallée, H., and Carré, H. (1922). C. r. hebdom. séances Acad. Sci. Paris 174, 207–208.Google Scholar
  225. van Bekkum, J. G., Frenkel, H. S., Frederiks, H. H. J., and Frenkel, S. (1959). Tijdschr. Diergeneeskd. 84, 1159–1164.Google Scholar
  226. Villanueva, N., Davila, M., Ortin, J., and Domingo, E. (1983). Gene 23, 185–194.PubMedGoogle Scholar
  227. Villaverde, A., Martínez-Salas, E., and Domingo, E. (1988). J. Mol. Biot 204, 771–776.Google Scholar
  228. Waldmann, O., and Trautwein, K. (1926). Berl. Munch. tierarztliche Wochenschr. 42, 569–570.Google Scholar
  229. Webb, S. R., Kearse, K. P., Foulke, C. L., Hartig, P. C., and Prabhakar, B. S. (1986). J. Med. Virol. 12, 9–15.Google Scholar
  230. Weddell, G. N., Yansura, D. G., Dowbenko, D. J., Hoatlin, M. E., Grubman, M. J., Moore, D. M., and Kleid, D. G. (1985). Proc. Natl. Acad. Sci. USA 82, 2618–2622.PubMedGoogle Scholar
  231. Weissmann, C., and Weber, H. (1986). Prog. Nucleic Acid Res. Mol. Biol. 33, 251–300.PubMedGoogle Scholar
  232. Wiesmüller, K. H., Jung, G., and Hess, G. (1989). Vaccine 7, 29–33.PubMedGoogle Scholar
  233. Wild, T. F., Burroughs, J. N., and Brown, F. (1969). J. Gen. Virol. 4, 313–320.PubMedGoogle Scholar
  234. Wilson, V., Taylor, P., and Desselberger, U. (1988). Arch. Virol. 102, 131–139.PubMedGoogle Scholar
  235. Winther, M. D., Allen, G., Bomford, R. H., and Brown, F. (1986). J. Immunol. 136, 1835–1840.PubMedGoogle Scholar
  236. Xie, Q. C., McCahon, D., Crowther, J. R., Belsham, G. J., and McCullough, K. C. (1987). J. Gen. Virol. 68, 1637–1647.PubMedGoogle Scholar
  237. Yilma, T. (1980). Am. J. Vet. Res. 41, 1537–1542.PubMedGoogle Scholar
  238. Youngner, J., and Preble, O. T. (1980). In Comprehensive Virology, Vol. 16 (H. Fraenkel-Conrat and R. R. Wagner, eds.), pp. 73–135, Plenum Press, New York.Google Scholar
  239. Zibert, A., Maas, G., Strebel, K., Falk, M. M., and Beck, E. (1990). J. Virol. in press.Google Scholar

Copyright information

© Springer Science+Business Media New York 1990

Authors and Affiliations

  • Esteban Domingo
    • 1
  • Mauricio G. Mateu
    • 1
  • Miguel A. Martínez
    • 2
  • Joaquín Dopazo
    • 3
  • Andrés Moya
    • 3
  • Francisco Sobrino
    • 2
  1. 1.Centro de Biología MolecularUniversidad Autónoma de MadridMadridSpain
  2. 2.Departamento de Sanidad AnimalInstituto Nacional de Investigaciones AgrariasMadridSpain
  3. 3.Laboratorio de GenéticaUniversidad de ValenciaBurjassot, ValenciaSpain

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