Complications of RNA Heterogeneity for the Engineering of Virus Vaccines and Antiviral Agents

  • Esteban Domingo
  • John J. Holland
Part of the Genetic Engineering book series (GEPM, volume 14)

Abstract

The most abundant viruses infecting plants, animals and humans are the RNA viruses (riboviruses and retroviruses). These elemental life forms are hypervariable to a degree that is difficult to comprehend fully. The genetics of RNA viruses is a strange, unfamiliar, and often counterintuitive genetics.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Theiler, M. and Smith, H.H. (1937) J. Exp. Med. 65, 787–800.PubMedCrossRefGoogle Scholar
  2. 2.
    Burnet, F.M. and Bull, D.R. (1943) Aust. J. Exp. Biol. Med. Sci. 21, 55–69.CrossRefGoogle Scholar
  3. 3.
    Kunkel, L.O. (1947) Annu. Rev. Microbiol. 1, 85–100.CrossRefGoogle Scholar
  4. 4.
    McClain, M.E., Hackett, A.J. and Madin, S.H. (1958) Science 127, 1391–1392.PubMedCrossRefGoogle Scholar
  5. 5.
    Mundry, K.W. and Gierer, A. (1958) Zeitschrift für Vererbungslehre 89, 614–630.PubMedGoogle Scholar
  6. 6.
    Granoff, A. (1964) in Newcastle Disease Virus, an Evolving Pathogen (Hanson, R.P., ed.) pp. 107–118, University of Wisconsin Press, Madison, WI.Google Scholar
  7. 7.
    Eggers, H.J. and Tamm, I. (1965) Science 148, 97–98.PubMedCrossRefGoogle Scholar
  8. 8.
    McCormick, K.J. and Murphy, W.H. (1969) Nature 221, 286.PubMedCrossRefGoogle Scholar
  9. 9.
    Lafay, F. (1969) C.R. Acad. Sci. Paris 268(D), 2385–2388.Google Scholar
  10. 10.
    Fields, B.N. and Joklik, W.K. (1969) Virology 37, 335–342.PubMedCrossRefGoogle Scholar
  11. 11.
    Valentine, R.C., Ward, R. and Strant, M. (1969) Adv. Virus Res. 15, 1–59.PubMedCrossRefGoogle Scholar
  12. 12.
    Holland, J.J., Spindler, K., Horodyski, F., Grabau, E., Nichol, S. and VandePol, S. (1982) Science 215, 1577–1585.PubMedCrossRefGoogle Scholar
  13. 13.
    Domingo, E., Martínez-Salas, E., Sobrino, F., de la Torre, J.C., Portela, A., Ortín, J., López-Galíndez, C., Pérez-Breña, P., Villanueva, N., Nájera, R., VandePol, S., Steinhauer, D., De Polo, N. and Holland, J.J. (1985) Gene 40, 1–8.PubMedCrossRefGoogle Scholar
  14. 14.
    Coffin, J. (1986) Cell 46, 1–4.PubMedCrossRefGoogle Scholar
  15. 15.
    Smith, D.B. and Inglis, S.C. (1987) J. Gen. Virol. 68, 2729–2740.PubMedCrossRefGoogle Scholar
  16. 16.
    Steinhauer, D. and Holland, J.J. (1987) Annu. Rev. Microbiol. 41, 409–433.PubMedCrossRefGoogle Scholar
  17. 17.
    Domingo, E. and Holland, J.J. (1988) in RNA Genetics, Vol. III, Variability of RNA Genomes (Domingo, E., Holland, J.J. and Ahlquist, P., eds.) pp. 3–36, CRC Press Inc., FL.Google Scholar
  18. 18.
    vanVloten-Doting, L. and Bol, J.F. (1988) in RNA Genetics, Vol. III, Variability of RNA Genomes (Domingo, E., Holland, J.J. and Ahlquist, P., eds.) pp. 37–51, CRC Press Inc., FL.Google Scholar
  19. 19.
    Smith, F.I. and Palese, P. (1988) in RNA Genetics, Vol. III, Variability of RNA Genomes (Domingo, E., Holland, J.J. and Ahlquist, P., eds.) pp. 123–135, CRC Press Inc., FL.Google Scholar
  20. 20.
    Southern, P.J. and Oldstone, M.B.A. (1988) in RNA Genetics, Vol. III, Variability of RNA Genomes (Domingo, E., Holland, J.J. and Ahlquist, P., eds.) pp. 159–170, CRC Press Inc., FL.Google Scholar
  21. 21.
    Zimmern, D. (1988) in RNA Genetics, Vol. II, Retroviruses, Viroids and RNA Recombination (Domingo, E., Holland, J.J. and Ahlquist, P., eds.) pp. 221–240, CRC Press Inc., FL.Google Scholar
  22. 22.
    Strauss, J.H. and Strauss, E.G. (1988) Annu. Rev. Microbiol. 42, 657–683.PubMedCrossRefGoogle Scholar
  23. 23.
    Domingo, E. (1989) in Progress in Drug Research, Vol. 33 (Jucker, E., ed.) pp. 93–133, Birkhäuser Verlag, Basel.CrossRefGoogle Scholar
  24. 24.
    Heinz, B.A., Rueckert, R.R., Shepard, D.A., Dutko, F.J., McKinlay, M.A., Fancher, M., Rosmann, M.G., Badger, J. and Smith, T.J. (1989) J. Virol. 63, 2476–2485.PubMedGoogle Scholar
  25. 25.
    Temin, H. (1989) J. AIDS 2, 1–9.Google Scholar
  26. 26.
    Steinhauer, D.A., de la Torre, J.C. and Holland, J.J. (1989) J. Virol. 63, 2063–2071.PubMedGoogle Scholar
  27. 27.
    Steinhauer, D.A., de la Torre, J.C., Meier, E. and Holland, J.J. (1989) J. Virol. 63, 2072–2080.PubMedGoogle Scholar
  28. 28.
    Mateu, M.G., Martínez, M.A., Rocha, E., Andreu, D., Parejo, J., Giralt, E., Sobrino, F. and Domingo, E. (1989) Proc. Nat. Acad. Sci. U.S.A. 86, 5883–5887.CrossRefGoogle Scholar
  29. 29.
    Meyerhans, A., Cheynier, R., Albert, J., Seth, M., Kwok, S., Sminsky, J., Morfeldt-Manson, L., Asjö, B. and Wain-Hobson, S. (1989) Cell 58, 901–910.PubMedCrossRefGoogle Scholar
  30. 30.
    Domingo, E., Mateu, M.G., Martínez, M.A., Dopazo, J., Moya, A. and Sobrino, F. (1990) in Applied Virology Research, Vol. 2, Virus Variability, Epidemiology and Control (Kurstak, E., Marusyk, R.G., Murphy, F.A. and Van Regenmortel, M.H.V., eds.) pp. 233–266, Plenum Press, New York, NY.Google Scholar
  31. 31.
    Coffin, J.M. (1990) in Applied Virology Research, Vol. 2, Virus Variability, Epidemiology and Control (Kurstak, E., Marusyk, R.G., Murphy, F.A. and Van Regenmortel, M.H.V., eds.) pp. 11–33, Plenum Press, New York, NY.Google Scholar
  32. 32.
    Kew, O.M., Nottay, B.K., Rico-Hesse, R. and Pallansch, M.A. (1990) in Applied Virology Research, Vol. 2, Virus Variability, Epidemiology and Control (Kurstak, E., Marusyk, R.G., Murphy, F.A. and Van Regenmortel, M.H.V., eds.) pp. 199–221, Plenum Press, New York, NY.Google Scholar
  33. 33.
    Carpenter, S., Evans, L.H., Sevoian, M. and Chesebro, M. (1990) in Applied Virology Research, Vol. 2, Virus Variability, Epidemiology and Control (Kurstak, E., Marusyk, R.G., Murphy, F.A. and Van Regenmortel, M.H.V., eds.) pp. 99–115, Plenum Press, New York, NY.Google Scholar
  34. 34.
    Kinnunen, L., Huovilainen, A., Pöyry and Hovi, T. (1990) J. Gen. Virol. 71, 317–324.PubMedCrossRefGoogle Scholar
  35. 35.
    Holland, J., Domingo, E., de la Torre, J.C. and Steinhauer, D.A. (1990) J. Virol. 64, 3960–3962.PubMedGoogle Scholar
  36. 36.
    Chao, L. (1990) Nature 348, 454–455.PubMedCrossRefGoogle Scholar
  37. 37.
    Imazeki, F., Omata, M., Ohto, M. (1990) J. Virol, 64, 5594–5599.PubMedGoogle Scholar
  38. 38.
    Carrillo, C., Plana, J., Mascarella, R., Bergadá, J. and Sobrino, F. (1990) Virology 179, 890–892.PubMedCrossRefGoogle Scholar
  39. 39.
    de la Torre, J.C., Wimmer, E. and Holland, J.J. (1990) J. Virol. 64, 664–671.PubMedGoogle Scholar
  40. 40.
    Groenink, M., Fouchier, R.A.M., de Goede, R.E.Y., De Wolf, F., Cruters, R.A., Cuypers, H.T.M., Huisman, H.G. and Tersmette, M. (1991) J. Virol. 65, 1968–1975.PubMedGoogle Scholar
  41. 41.
    Holland, J.J., de la Torre, J.C., Clarke, D.K. and Duarte, E. (1991) J. Virol. 65, 2960–2967.PubMedGoogle Scholar
  42. 42.
    Gonzalez, M.J., Saiz, J.C., Laor, O. and Moore, D.M. (1991) J. Virol. 65, 3949–3953.PubMedGoogle Scholar
  43. 43.
    Martínez, M.A., Carrillo, C., González-Candelas, F., Moya, A., Domingo, E. and Sobrino, F. (1991) J. Virol. 65, 3954–3957.PubMedGoogle Scholar
  44. 44.
    Rocha, E., Cox, N.J., Black, R.A., Harmon, M.W., Harrison, C.J. and Kendal, A.P. (1991) J. Virol. 65, 2340–2350.PubMedGoogle Scholar
  45. 45.
    Burns, D.P.W. and Desrosiers, R.C. (1991) J. Virol. 65, 1843–1854.PubMedGoogle Scholar
  46. 46.
    Holland, J.J., de la Torre, J.C. and Steinhauer, D.A. (1992) in Current Topics in Microbiology and Immunology, Vol. 176, Genetic Diversity of RNA Viruses (Holland, J.J., ed.) Springer-Verlag, Berlin (in press).CrossRefGoogle Scholar
  47. 47.
    Domingo, E., Escarmis, C., Martínez, M.A., Martínez-Salas, E. and Mateu, M.G. (1992) in Current Topics in Microbiology and Immunology, Vol. 176, Genetic Diversity of RNA Viruses (Holland, J.J., ed.) Springer-Verlag, Berlin (in press).Google Scholar
  48. 48.
    Eigen, M. (1971) Naturwissenschaften 58, 465–523.PubMedCrossRefGoogle Scholar
  49. 49.
    Eigen, M. and Schuster, P. (1977) Naturwissenschaften 64, 541–565.PubMedCrossRefGoogle Scholar
  50. 50.
    Eigen, M. and Schuster, P. (1978) Naturwissenschaften 65, 7–41.CrossRefGoogle Scholar
  51. 51.
    Eigen, M. and Schuster, P. (1978) Naturwissenschaften 65, 341–369.CrossRefGoogle Scholar
  52. 52.
    Eigen, M. and Biebricher (1988) in RNA Genetics, Vol. III. Variability of RNA Genomes (Domingo, E., Holland, J.J. and Ahlquist, P., eds.) pp 211–245, CRC Press Inc., FL.Google Scholar
  53. 53.
    de la Torre, J.C. and Holland, J.J. (1990) J. Virol. 64, 6278–6281.PubMedGoogle Scholar
  54. 54.
    Sobrino, F., Dávila, M., Ortín, J. and Domingo, E. (1983) Virology 128, 310–318.PubMedCrossRefGoogle Scholar
  55. 55.
    Batschelet, E., Domingo, E. and Weissmann, C (1976) Gene 1, 27–32.PubMedCrossRefGoogle Scholar
  56. 56.
    King, A.M.Q., McCahon, D., Slade, W.R. and Newman, J.W.I. (1982) Cell 29, 921–928.PubMedCrossRefGoogle Scholar
  57. 57.
    Minor, P.D., John, A., Ferguson, M. and Icenogle, J.P. (1986) J. Gen. Virol. 67, 693–706.PubMedCrossRefGoogle Scholar
  58. 58.
    Makino, S., Keck, J.G., Stohlman, S.A. and Lai, M.M. (1986) J. Virol. 57, 729–737.PubMedGoogle Scholar
  59. 59.
    Keck, J.G., Matsushima, G.K., Makino, S., Fleming, J.O., Vannier, D. M., Stohlman, S.A. and Lai, M.M.C. (1988) J. Virol. 62, 1810–1813.PubMedGoogle Scholar
  60. 60.
    King, A.M.Q. (1988) in RNA Genetics, Vol. II, Retroviruses, Viroids and RNA Recombination (Domingo, E., Holland, J.J. and Ahlquist, P., eds.) pp. 149–156, CRC Press Inc., FL.Google Scholar
  61. 61.
    Webster, R.G., Laver, W.G., Air, G.M. and Schild, G.C. (1982) Nature 296, 115–121.PubMedCrossRefGoogle Scholar
  62. 62.
    Hundley, F., Biryahwaho, B., Gow, M. and Desselberger, U. (1985) Virology 143, 88–103.PubMedCrossRefGoogle Scholar
  63. 63.
    O’Hara, P.J., Nichol, S.T., Horodyski, F.M. and Holland, J.J. (1984) Cell 36, 915–924.CrossRefGoogle Scholar
  64. 64.
    Cattaneo, R., Schmid, A., Eschle, D., Baczko, K., ter Meulen, V. and Billeter, M.A. (1988) Cell 55, 255–265.PubMedCrossRefGoogle Scholar
  65. 65.
    Bass, B.L., Weintraub, H., Cattaneo, R. and Billeter, M.A.(1989) Cell 56, 331.PubMedCrossRefGoogle Scholar
  66. 66.
    Holland, J.J. (1990) in Virology (Fields, B.N., Knipe, D.M., et al., eds.) pp. 151–165, Raven Press, Ltd., New York, NY.Google Scholar
  67. 67.
    Buonagurio, D.A., Nakada, S., Parvin, J.D., Krystal, M., Palese, P. and Fitch, W.M. (1986) Sciences 232, 980–982.CrossRefGoogle Scholar
  68. 68.
    Gorman, O.T., Bean, W.J., Kawaoka, Y., Donatelli, I., Guo, Y. and Webster, R.G. (1991) J. Virol. 65, 3704–3714.PubMedGoogle Scholar
  69. 69.
    Sobrino, D., Palma, E.L., Beck, E., Dávila, M., de la Torre, J.C., Negro, P., Villanueva, N., Ortin, J. and Domingo, E. (1986) Gene 50, 149–159.PubMedCrossRefGoogle Scholar
  70. 70.
    Villaverde, A., Martínez-Salas, E. and Domingo, E. (1988) J. Mol. Biol. 204, 771–776.PubMedCrossRefGoogle Scholar
  71. 71.
    Villaverde, A., Martínez, M.A., Sobrino, F., Dopazo, J., Moya, A. and Domingo, E. (1991) Gene 103, 147–153.PubMedCrossRefGoogle Scholar
  72. 72.
    Weaver, S.C., Scott, T.W. and Rico-Hesse, R. (1991) Virology 182, 774–784.PubMedCrossRefGoogle Scholar
  73. 73.
    Domingo, E., Dávila, M. and Ortín, J. (1980) Gene 11, 333–346.PubMedCrossRefGoogle Scholar
  74. 74.
    Clements, J.E., Pedersen, F.S., Narayan, O. and Haseltine, W.A. (1980) Proc. Nat. Acad. Sci. U.S.A. 77, 4454–4458.CrossRefGoogle Scholar
  75. 75.
    Gebauer, F., delaTorre, J.C., Gomes, I., Mateau, M.G., Barahona, H., Tiraboschi, B., Bergmann, I., Augé de Mello, P. and Domingo, E. (1988) J. Virol. 62, 2041–2049.PubMedGoogle Scholar
  76. 76.
    Domingo, E., Sabo, D., Taniguchi, T. and Weissmann, C. (1978) Cell 13, 735–744.PubMedCrossRefGoogle Scholar
  77. 77.
    Rutgers, T.,. Cabezón, T. and De Wilde, M. (1990) in Immunochemistry of Viruses II. The Basis for Serodiagnosis and Vaccines (Van Regenmortel, M.H.V. and Neurath, A.R., eds.) pp. 103–124, Elsevier, Amsterdam.Google Scholar
  78. 78.
    Liew, F.Y. (1990) In Biotechnology and Genetic Engineering Reviews, Vol. 8 (Tombs, M.P., ed.) pp. 53–95, Intercept, Andover, MA.Google Scholar
  79. 79.
    Urakawa, T., Ferguson, M., Minor, P.D., Cooper, J., Sullivan, M., Almond, J.W. and Bishop, D.H.L. (1989) J. Gen Virol. 70, 1453–1563.PubMedCrossRefGoogle Scholar
  80. 80.
    Tartaglia, J., Pincus, S. and Paoletti (1990) in Critical Reviews in Immunology, Vol. 10, Issue 1 (Atassi, M.Z., ed.) pp. 13–30, CRC Press, Inc., FL.Google Scholar
  81. 81.
    Fenner, F., Wittek, R. and Dumbell, K.R. (1989) The Orthopoxviruses, pp. 353–376, Academic Press, Inc., San Diego, CA.Google Scholar
  82. 82.
    Fuerst, T.R., Fernandez, M.P. and Moss, B. (1989) Proc. Nat. Acad. Sci. U.S.A. 86, 2549–2553.CrossRefGoogle Scholar
  83. 83.
    Rodriguez, J.F. and Smith, G.L. (1990) Nucl. Acids Res. 18, 5347–5351.PubMedCrossRefGoogle Scholar
  84. 84.
    Burke, K.L., Dunn, G., Ferguson, M., Minor, P.D. and Almond, J.W. (1988) Nature 332, 81–83.PubMedCrossRefGoogle Scholar
  85. 85.
    Arnon, R. (1991) Molecular Immunology 28, 209–215.PubMedCrossRefGoogle Scholar
  86. 86.
    Lerner, R.A. (1982) Nature 299, 595–596.CrossRefGoogle Scholar
  87. 87.
    Di Marchi, R., Brooke, G., Gale, C., Cracknell, W., Doel, T. and Mowat, N. (1986) Science 232, 639–641.CrossRefGoogle Scholar
  88. 88.
    Brown, F. (1989) in Synthetic Peptides: Approaches to Biological Problems (Tarn, J.P. and Kaiser, E.T., eds.) pp. 127–142, Alan R. Liss, Inc., New York, NY.Google Scholar
  89. 89.
    Dalgleish, A.G. and Kennedy, R.C. (1988) Vaccine 6, 215–220.PubMedCrossRefGoogle Scholar
  90. 90.
    Zaghouani, H., Goldstein, D., Shah, H., Anderson, S., Lacroix, M., Dionne, G., Kennedy, R. and Bona, C. (1991) Proc. Nat. Acad. Sci. U.S.A. 88, 5645–5649.CrossRefGoogle Scholar
  91. 91.
    Schwartz, R.H. (1986) Current Topics in Microbiology and Immunology 130, 79–85.PubMedCrossRefGoogle Scholar
  92. 92.
    Celada, F. and Sercarz, E.E. (1988) Vaccine 6, 94–98.PubMedCrossRefGoogle Scholar
  93. 93.
    Whitton, J.L. and Oldstone, M.B.A. (1990) in Virology (Fields, B.N., Knipe, D.M., et al., eds.) pp. 369–381, Raven Press, Ltd., New York, NY.Google Scholar
  94. 94.
    Virelizier, J.L. (1989) in Special Publications of the Society for General Microbiology, Vol. 27, Immune Responses, Virus Infections and Disease (Dimmock, N.J. and Minor, P.D., eds.) pp. 1–14, IRL Press, Oxford.Google Scholar
  95. 95.
    Bjorkman, P.J. and Davis, M.M. (1990) in Use of X-ray Crystallography in the Design of Antiviral Agents (Laver, W.G. and Air, G.M., eds.) pp. 19–34, Academic Press, Inc., San Diego, CA.Google Scholar
  96. 96.
    Martínez, M.A., Hernández, J., Piccone, M.E., Palma, E.L., Domingo, E., Knowles, N. and Mateu, M.G. (1991) Virology 184, 695–706.PubMedCrossRefGoogle Scholar
  97. 97.
    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.PubMedCrossRefGoogle Scholar
  98. 98.
    Bolwell, C., Brown, A.L., Barnett, P.V., Campbell, R.O., Clarke, B.E., Parry, N.R., Ouldridge, E.J., Brown, F. and Rowlands, D.J. (1989) J. Gen. Virol. 62, 2050–2058.Google Scholar
  99. 99.
    Cloyd, M.W. and Holt, M.J. (1987) Virology 161, 286–292.PubMedCrossRefGoogle Scholar
  100. 100.
    Díez, J., Mateu, M.G. and Domingo, E. (1989) J. Gen. Virol. 70, 3281–3289.PubMedCrossRefGoogle Scholar
  101. 101.
    Emini, E.A., Kao, S., Lewis, A.J., Crainic, R. and Wimmer, E. (1983) J. Virol. 46, 466–474.PubMedGoogle Scholar
  102. 102.
    Lubeck, M.D., Schulman, J.L. and Palese, P. (1980) Virology 102, 458–462.PubMedCrossRefGoogle Scholar
  103. 103.
    Portner, A., Webster, R.G. and Bean, W. (1980) Virology 104, 235–238.PubMedCrossRefGoogle Scholar
  104. 104.
    Stec, D.S., Waddel, A., Schmaljohn, C.S., Cole, G.A. and Schmaljohn, A.L. (1986) J. Virol. 57, 715–720.PubMedGoogle Scholar
  105. 105.
    Sherry, B., Mosser, A.G., Colonno, R.J. and Rueckert, R.R. (1986) J. Virol. 57, 246–257.PubMedGoogle Scholar
  106. 106.
    Holland, J.J., de laTorre, J.C., Steinhauer, D.A., Clarke, D., Durate, E. and Domingo, E. (1989) J. Virol. 63, 5030–5036.PubMedGoogle Scholar
  107. 107.
    Boege, U., Kobasa, D., Onodera, S., Parks, G.D., Palmenberg, A.C. and Scraba, D.G. (1991) Virology 181, 1–13.PubMedCrossRefGoogle Scholar
  108. 108.
    Valcarcel, J. and Ortin, J. (1989) J. Virol. 63, 4107–4109.PubMedGoogle Scholar
  109. 109.
    Lemon, S.M., Binn, L.N., Marchwicki, R., Murphy, P.C., Ping, L.H., Stapleton, J.T., Taylor, D.G. and LeDuc, J.W. (1990) J. Infect. Dis. 161, 7–13.PubMedCrossRefGoogle Scholar
  110. 110.
    Martínez, M.A., Carrillo, C., Plana, J., Mascarella, R., Bergadá, J., Palma, E.L., Domingo, E. and Sobrino, F. (1988) Gene 62, 75–84.PubMedCrossRefGoogle Scholar
  111. 111.
    Magrath, D.I., Evans, D.M.A., Ferguson, M., Schild, G.C., Minor, P.D., Horaud, F., Grainic, R., Stenvik, M. and Hovi, T. (1986) J. Gen. Virol. 67, 899–906.PubMedCrossRefGoogle Scholar
  112. 112.
    Carman, W.F., Zanetti, A.R., Karayiannis, P., Waters, J. Manzillo, G., Tanzi, E., Zuckerman, A.J. and Thomas, H.C. (1990) Lancet 336, 325–329.PubMedCrossRefGoogle Scholar
  113. 113.
    Echevarria, J.M., León, P., Domingo, C.J., López, J.A., Echevarria, J.E., Contreras, G. and Fuertes, A. (1991) J. Med. Virol. 33, 240–247.PubMedCrossRefGoogle Scholar
  114. 114.
    Kurth, R., Binninger, D., Ennen, J., Denner, J., Hartung, S. and Norley, S. (1991) AIDS Research and Human Retroviruses 7, 425–433.PubMedCrossRefGoogle Scholar
  115. 115.
    Gardner, M.B. (1991) Antiviral Res. 15, 267–286.PubMedCrossRefGoogle Scholar
  116. 116.
    Couch, R.B. (1990) in Virology (Fields, B.N., Knipe, D.M., et al., eds.) pp. 607–629, Raven Press, Ltd., New York, NY.Google Scholar
  117. 117.
    Kew, O.M., Nottay, B.K., Hatch, M.H., Nakano, J.H., and Obijeski, J.F. (1981) J. Gen Virol. 56, 337–347.PubMedCrossRefGoogle Scholar
  118. 118.
    Evans, D.M.A., Dunn, G., Minor, P.D., Schild, G.C., Cann, A.J., Stanway, G., Almond, J.W., Currey, K. and Maizel, J.V. (1985) Nature 314, 548–550.PubMedCrossRefGoogle Scholar
  119. 119.
    WHO Bulletin (1976) 53, 319-331.Google Scholar
  120. 120.
    Díez, J., Hofner, M., Domingo, E. and Donaldson, A.I. (1990) Virus Research 18, 3–8.PubMedCrossRefGoogle Scholar
  121. 121.
    Parrish, C.R., O’Connell, P.H., Evermann, J.F. and Carmichael, L.F. (1985) Science 230, 1046–1048.PubMedCrossRefGoogle Scholar
  122. 122.
    Evans, A.S. (1984) Viral Infections of Humans: Epidemiology and Control. Plenum Press, New York, NY.CrossRefGoogle Scholar
  123. 123.
    Zinkernagel, R.M. (1988) in Immunology and Pathogenesis of Persistent Virus Infections (López, C., ed.) pp. 54–59, American Society for Microbiology, Washington, D.C.Google Scholar
  124. 124.
    Oehen, S., Hengartner, H. and Zinkernagel, R.M. (1991) Science 251, 195–198.PubMedCrossRefGoogle Scholar
  125. 125.
    Kapikian, A.Z., Mitchell, R.H., Chanock, R.M., Shvedoff, R.A. and Stewart, C.E. (1969) Amer. J. Epidemiol. 89, 405–421.Google Scholar
  126. 126.
    Prince, G.A., Jenson, A.B., Hemming, V.G., Murphy, B.R., Walsh, E.E., Horswood, R.L. and Chanock, R.M. (1986) J. Virol. 57, 721–728.PubMedGoogle Scholar
  127. 127.
    Southern, P.J. and Oldstone, P.J. (1988) in RNA Genetics, Vol. III, Variability of RNA Genomes (Domingo, E., Holland, J.J. and Ahlquist, P., eds.) pp. 159–170, CRC Press, Inc., FL.Google Scholar
  128. 128.
    de laTorre, J.C., Martínez-Salas, E., Díez, J., Villaverde, A., Gebauer, F., Rocha, E., Dávila, M. and Domingo, E. (1988) J. Virol. 62, 2050–2058.PubMedGoogle Scholar
  129. 129.
    Johnson, R.T. (1982) Viral Infections of the Nervous System, Raven Press, New York, NY.Google Scholar
  130. 130.
    Fujinami, R.S. and Oldstone, M.B.A. (1985) Science 230, 1043–1045.PubMedCrossRefGoogle Scholar
  131. 131.
    Fujinami, R.S. (1990) in Immunochemistry of Viruses II. The Basis for Serodiag-nosis and Vaccines (Van Regenmortel, M.H.V. and Neurath, A.R., eds.) pp. 75–82, Elsevier, Amsterdam.Google Scholar
  132. 132.
    Mateu, M.G., Martínez, M.A., Capucci, L., Andreu, D., Giralt, E., Sobrino, F., Brocchi, E. and Domingo, E. (1990) J. Gen. Virol. 71, 629–637.PubMedCrossRefGoogle Scholar
  133. 133.
    Heinz, B.A., Rueckert, R.R., Shepard, D.A., Dutko, F.J., McKinlay, M.A., Fancher, M., Rossmann, M.G., Badger, J. and Smith, T.J. (1989) J. Virol. 63, 2476–2485.PubMedGoogle Scholar
  134. 134.
    Heinz, B.A., Shepard, D.A. and Rueckert, R.R. (1990) in Use of X-ray Crystallography in the Design of Antiviral Agents (Laver, W.G. and Air, G.M., eds.) pp. 173–186, Academic Press Inc., San Diego, CA.Google Scholar
  135. 135.
    Colonno, R.J., Condra, J.H., Mizutani, S., Callahan, P.L., Davies, M.E. and Murko, M.A. (1988) Proc. Nat. Acad. Sci. U.S.A. 85, 5449–5453.CrossRefGoogle Scholar
  136. 136.
    Appleyard, G. (1977) J. Gen. Virol. 36, 249–255.PubMedCrossRefGoogle Scholar
  137. 137.
    Lubeck, M.D., Schulman, J.L. and Palese, P. (1978) J. Virol. 28, 710–716.PubMedGoogle Scholar
  138. 138.
    Belshe, R.B., Hall-Smith, M., Hall, C.B., Betts, R. and Hay, A.J. (1988) J. Virol. 62, 1508–1512.PubMedGoogle Scholar
  139. 139.
    Hay, A.J. (1989) in Concepts of Viral Pathogenesis, Vol. III(Notkins, A.L. and Oldstone, M.B.A., eds.) pp. 361–367, Springer-Verlag, New York, NY.CrossRefGoogle Scholar
  140. 140.
    Hayden, F.G., Belshe, M.D., Clover, R.D., Hay, A.J., Oakes, M.G. and Soo, W. (1989) New Eng. J. Med. 321, 1696–1702.PubMedCrossRefGoogle Scholar
  141. 141.
    Larder, B.A., Darby, G. and Richmann, D.D. (1989) Science 243, 1731–1734.PubMedCrossRefGoogle Scholar
  142. 142.
    Larder, B.A. and Kemp, S.D. (1989) Science 246, 1155–1158.PubMedCrossRefGoogle Scholar
  143. 143.
    McKinlay, M.A. and Rossmann, M.G. (1989) Annu. Rev. Pharmacol. Toxicol. 29, 111–122.PubMedCrossRefGoogle Scholar
  144. 144.
    Laver, W.G. and Air, G.M. (1990) Use of X-ray Crystallography in the Design of Antiviral Agents, Academic Press, Inc., San Diego, CA.Google Scholar
  145. 145.
    Goodford, P.J. (1985) J. Med. Chem. 28, 849–857.PubMedCrossRefGoogle Scholar
  146. 146.
    Boobbyer, D.N.A., Goodford, P.J., McWhinnie, P.W. and Wade, R.C. (1989) J. Med. Chem. 32, 1083–1094.PubMedCrossRefGoogle Scholar
  147. 147.
    Wade, R.C. (1990) in Use of X-ray Crystallography in the Design of Antiviral Agents (Laver, W.G. and Air, G.M., eds.) pp. 61–74, Academic Press, Inc., San Diego, CA.Google Scholar
  148. 148.
    Lu, S., Reyes, V.E., Torgerson, R.R., Lew, R.A. and Humphreys, R.E. (1991) Trends Biotechnol. 9, 238–242.PubMedCrossRefGoogle Scholar
  149. 149.
    Walsh, C. (1980) Tetrahedron 38, 871–909.CrossRefGoogle Scholar
  150. 150.
    Bartlett, P.A., Sampson, N.S., Reich, S.H., Drewry, D.H. and Lamden, L.A. (1990) in Use of X-ray Crystallography in the Design of Antiviral Agents (Laver, W.G. and Air, G.M., eds.) pp. 247–259, Academic Press, Inc., San Diego, CA.Google Scholar
  151. 151.
    Erickson, J., Neidhardt, D.J., VanDrie, J., Kempf, D.J., Wang, X.C., Norbeck, D.W., Plattner, J.J., Rittenhouse, J.W., Turon, M., Wideburg, N., Kohlbrenner, W.E., Simmer, R., Helfrich, R., Paul, D.A. and Knigge, M. (1990) Science 249, 527–532.PubMedCrossRefGoogle Scholar
  152. 152.
    Pain, R.H. (1983) Nature 305, 581–582.PubMedCrossRefGoogle Scholar
  153. 153.
    Doolittle, R.F., Feng, D.F., Johnson, M.S. and McClure, M.A. (1989) Quart. Rev. Biol. 64, 1–30.PubMedCrossRefGoogle Scholar
  154. 154.
    Steinhauer, D. and Holland, J.J. (1986) J. Virol. 57, 219–228.PubMedGoogle Scholar
  155. 155.
    Acharya, R., Fry, E., Stuart, D., Fox, G., Rowlands, D. and Brown, F. (1989) Nature 337, 709–716.PubMedCrossRefGoogle Scholar
  156. 156.
    Díez, J., Dávila, M., Escarmís, C., Mateu, M.G., Domínguez, J., Pérez, J.J., Giralt, E., Melero, J.A. and Domingo, E. (1990) J. Virol. 64, 5519–5528.PubMedGoogle Scholar
  157. 157.
    Pathak, V.K. and Temin, H.M. (1990) Proc. Nat. Acad. Sci. U.S.A. 87, 6019–6023.CrossRefGoogle Scholar
  158. 158.
    Roberts, J.D., Bebenek, K. and Kunkel, T.A. (1988) Science 242, 1171–1173.PubMedCrossRefGoogle Scholar
  159. 159.
    Vartanian, J.P., Meyerhans, A., Asjö, B. and Wain-Hobson, S. (1991) J. Virol. 65, 1779–1788.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1992

Authors and Affiliations

  • Esteban Domingo
    • 1
  • John J. Holland
    • 2
  1. 1.Centro de Biología Molecular (CSIC-UAM)Universidad Autónoma de MadridMadridSpain
  2. 2.Department of Biology, 0116University of California, San DiegoLa JollaUSA

Personalised recommendations