1887

Abstract

Foot-and-mouth disease virus (FMDV) capsids are inherently labile under mildly acidic conditions, dissociating to pentamers at pH values in the region of 6·5, with the release of protein 1A and the viral RNA. This acid-induced disassembly is thought to be required for the entry of the virus genome into the host cell. Previous work has highlighted a histidine–α-helix charge-dipole interaction at the twofold axes of symmetry between pentamers and has suggested that this interaction plays a role in acid-induced disassembly. The validity of this theory has now been tested by converting the implicated residue, His-142 of protein 1C, to Arg, Phe and Asp. The effects of such changes were studied by using a previously described vaccinia virus expression system, in which synthesis and processing of FMDV capsid proteins results in the self-assembly of capsids. In agreement with the histidine–α-helix charge-dipole theory, assembly in the arginine mutant was found to be greatly reduced, while capsids of the aspartic acid mutant were considerably more stable under acidic conditions than the wild-type. Aberrant but acid-stable complexes were obtained in the phenylalanine mutant.

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1999-08-01
2024-03-28
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References

  1. Abrams C. C., King A. M. Q., Belsham G. J. 1995; Assembly of foot-and-mouth disease virus empty capsids synthesized by a vaccinia virus expression system. Journal of General Virology 76:3089–3098
    [Google Scholar]
  2. Acharya R., Fry E., Stuart D., Fox G., Rowlands D., Brown F. 1989; The three-dimensional structure of foot-and-mouth disease virus at 2·9 Å resolution. Nature 337:709–716
    [Google Scholar]
  3. Almela M. J., Gonzalez M. E., Carrasco L. 1991; Inhibitors of poliovirus uncoating efficiently block the early membrane permeabilization induced by virus particles. Journal of Virology 65:2572–2577
    [Google Scholar]
  4. Baxt B. 1987; Effect of lysosomotropic compounds on early events in foot-and-mouth disease virus replication. Virus Research 7:257–271
    [Google Scholar]
  5. Carrillo E. C., Giachetti C., Campos R. H. 1984; Effect of lysosomotropic agents on the foot-and-mouth disease virus replication. Virology 135:542–545
    [Google Scholar]
  6. Carrillo E. C., Giachetti C., Campos R. H. 1985; Early steps in FMDV replication: further analysis on the effects of chloroquine. Virology 147:118–125
    [Google Scholar]
  7. Carroll A. R., Rowlands D. J., Clarke B. E. 1984; The complete nucleotide sequence of the RNA coding for the primary translation product of foot and mouth disease virus. Nucleic Acids Research 12:2461–2472
    [Google Scholar]
  8. Chu G., Hayakawa H., Berg P. 1987; Electroporation for the efficient transfection of mammalian cells with DNA. Nucleic Acids Research 15:1311–1326
    [Google Scholar]
  9. Curry S., Abrams C. C., Fry E., Crowther J. C., Belsham G. J., Stuart D. I., King A. M. Q. 1995; Viral RNA modulates the acid sensitivity of foot-and-mouth disease virus capsids. Journal of Virology 69:430–438
    [Google Scholar]
  10. Curry S., Fry E., Blakemore W., Abu-Ghazaleh R., Jackson T., King A., Lea S., Newman J., Stuart D. 1997; Dissecting the roles of VP0 cleavage and RNA packaging in picornavirus capsid stabilization: the structure of empty capsids of foot-and-mouth disease virus. Journal of Virology 71:9743–9752
    [Google Scholar]
  11. Dawson R. M., Elliott D. C., Elliott W. H., Jones K. M. 1969 Data for Biochemical Research pp 484–485 London: Oxford University Press;
  12. Firestone G. L., Winguth S. D. 1990; Immunoprecipitation of proteins. Methods in Enzymology 182:688–700
    [Google Scholar]
  13. Fricks C. E., Hogle J. M. 1990; Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. Journal of Virology 64:1934–1945
    [Google Scholar]
  14. Fuerst T. R., Niles E. G., Studier F. W., Moss B. 1986; Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proceedings of the National Academy of Sciences, USA 83:8122–8126
    [Google Scholar]
  15. Gauss G. H., Lieber M. R. 1992; DEAE–dextran enhances electroporation of mammalian cells. Nucleic Acids Research 20:6739–6740
    [Google Scholar]
  16. Giranda V. L., Heinz B. A., Oliveira M. A., Minor I., Kim K. H., Kolatkar P. R., Rossmann M. G., Rueckert R. R. 1992; Acid-induced structural changes in human rhinovirus 14: possible role in uncoating. Proceedings of the National Academy of Sciences, USA 89:10213–10217
    [Google Scholar]
  17. Higuchi R., Krummel B., Saiki R. K. 1988; A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Research 16:7351–7367
    [Google Scholar]
  18. Kim S., Boege U., Krishnaswamy S., Minor I., Smith T. J., Luo M., Scraba D. G., Rossmann M. G. 1990; Conformational variability of a picornavirus capsid: pH-dependent structural change of Mengo virus related to its host receptor attachment site and disassembly. Virology 175:176–190
    [Google Scholar]
  19. Knipe T., Rieder E., Baxt B., Ward G., Mason P. W. 1997; Characterization of synthetic foot-and-mouth disease virus provirions separates acid-mediated disassembly from infectivity. Journal of Virology 71:2851–2856
    [Google Scholar]
  20. Mason P. W., Baxt B., Brown F., Harber J., Murdin A., Wimmer E. 1993; Antibody-complexed foot-and-mouth disease virus, but not poliovirus, can infect normally insusceptible cells via the Fc receptor. Virology 192:568–577
    [Google Scholar]
  21. Mosser A. G., Sgro J. Y., Rueckert R. R. 1994; Distribution of drug resistance mutations in type 3 poliovirus identifies three regions involved in uncoating functions. Journal of Virology 68:8193–8201
    [Google Scholar]
  22. Prchla E., Kuechler E., Blaas D., Fuchs R. 1994; Uncoating of human rhinovirus serotype 2 from late endosomes. Journal of Virology 68:3713–3723
    [Google Scholar]
  23. Rossmann M. G. 1994; Viral cell recognition and entry. Protein Science 3:1712–1725
    [Google Scholar]
  24. Ryan M. D., Belsham G. J., King A. M. Q. 1989; Specificity of enzyme–substrate interactions in foot-and-mouth disease virus polyprotein processing. Virology 173:35–45
    [Google Scholar]
  25. Ryan M. D., King A. M. Q., Thomas G. P. 1991; Cleavage of foot-and-mouth disease virus polyprotein is mediated by residues located within a 19 amino acid sequence. Journal of General Virology 72:2727–2732
    [Google Scholar]
  26. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  27. Sayle R. A., Milner-White E. J. 1995; RASMOL: biomolecular graphics for all. Trends in Biochemical Sciences 20:374–376
    [Google Scholar]
  28. Skern T., Torgersen H., Auer H., Kuechler E., Blaas D. 1991; Human rhinovirus mutants resistant to low pH. Virology 183:757–763
    [Google Scholar]
  29. Twomey T., France L. L., Hassard S., Burrage T. G., Newman J. F. E., Brown F. 1995; Characterization of an acid-resistant mutant of foot-and-mouth disease virus. Virology 206:69–75
    [Google Scholar]
  30. van Vlijmen H. W., Curry S., Schaefer M., Karplus M. 1998; Titration calculations of foot-and-mouth disease virus capsids and their stabilities as a function of pH. Journal of Molecular Biology 275:295–308
    [Google Scholar]
  31. Ypma-Wong M. F., Semler B. L. 1987; Processing determinants required for in vitro cleavage of the poliovirus P1 precursor to capsid proteins. Journal of Virology 61:3181–3189
    [Google Scholar]
  32. Zibert A., Maass G., Strebel K., Falk M. M., Beck E. 1990; Infectious foot-and-mouth disease virus derived from a cloned full-length cDNA. Journal of Virology 64:2467–2473
    [Google Scholar]
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