1887

Abstract

SUMMARY

We have investigated whether herpes simplex virus (HSV) contains structural polypeptides which are modified by myristic acid. We demonstrate that herpes simplex virions contain a family of myristylated proteins, approximately 13000 to 16000. These were mapped, using HSV-1/HSV-2 intertypic recombinants, to 0·130 to 0·204 map units on the virus genome. Using anti-peptide sera, raised against the carboxy-terminus of the predicted UL11 gene product, we have established that the myristylated virion polypeptides are products of the viral gene UL11.

Keyword(s): gene UL11 , HSV-1 and myristylation
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1989-12-01
2024-12-02
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References

  1. Atherton E., Gait M. J., Sheppard R. C., Williams B. J. 1979; The polyamide method of solid phase peptide and oligonucleotide synthesis. Bioorganic Chemistry 8:351–370
    [Google Scholar]
  2. Baer R., Bankier A. T., Biggin M. D., Deininger P. L., Farrell P. J., Gibson T. J., Hatfull G., Hudson G. S., Satchwell S. C., Seguin C, Tuffnell P. S., Barrell B. G. 1984; DNA sequence and expression of the B95-8 Epstein-Barr virus genome. Nature, London 310:207–211
    [Google Scholar]
  3. Bassiri R. M., Dvorak J., Utiger R. D. 1979; Thyrotropin-releasing hormone. In Methods of Hormone Radioimmunoassay46–47 Juffe B. H., Behrman H. R. New York: Academic Press;
    [Google Scholar]
  4. Bradac J. A., Hunter E. 1986; Polypeptides of Mason-Pfizer monkey virus. III. Translational order of proteins on the gag and env gene specified precursor polypeptides. Virology 150:503–508
    [Google Scholar]
  5. Brown S. M., Ritchie D. A., Subak-Sharpe I. H. 1973; Genetic studies with herpes simplex virus type 1. The isolation of temperature-sensitive mutants, their arrangement into complementation groups and recombination analysis leading to a linkage map. Journal of General Virology 18:329–346
    [Google Scholar]
  6. Buss J. E., Mumby S. M., Casey P. J., Gilman A. G., Sefton B. M. 1987; Myristoylated a subunits of guanine nucleotide-binding regulatory proteins. Proceedings of the National Academy of SciencesU.S.A 84:7493–7497
    [Google Scholar]
  7. Carr S. A., Biemann K., Shoji S., Parmelee D. C., Titani K. 1982; n-Tetradecanoyl is the NH2-terminal blocking group of the catalytic subunit of cyclic AMP-dependent protein kinase from bovine cardiac muscle. Proceedings of the National Academy of SciencesU.S.A 79:6128–6131
    [Google Scholar]
  8. Chartrand P., Wilkie N. M., Timbury M. C. 1981; Physical mapping of temperature-sensitive mutations of herpes simplex virus type 2 by marker rescue. Journal of General Virology 52:121–133
    [Google Scholar]
  9. Chen Z. Q., Ulsh L. S., Dubols G., shih T. Y. 1985; Post-translational processing of p21 ras proteins involves palmitylation of the C-terminal tetrapeptide containing cysteine-186. Journal of Virology 56:607–612
    [Google Scholar]
  10. Chow M., Newman J. F. E., Filman D., Hogle J. M., Rowlands D. J., Brown F. 1987; Myristylation of picornavirus capsid protein VP4 and its structural significance. Nature, London 327:482–486
    [Google Scholar]
  11. Clark B., Desselberger U. 1988; Myristylation of rotavirus proteins. Journal of General Virology 69:2681–2686
    [Google Scholar]
  12. Cohen G. H., Ponce De Leon M., Diggelmann H., Lawrence W. C., Vernon S. K., Eisenberg R. J. 1980; Structural analysis of the capsid polypeptides of HSV types 1 and 2. Journal of Virology 34:521–531
    [Google Scholar]
  13. Costa R. H., Draper K. G., Banks L., Powell K. L., Cohen G., Eisenberg R., Wagner E. K. 1983; High resolution characterization of herpes simplex virus type 1 transcripts encoding alkaline exonuclease and a 50000-dalton protein tentatively identified as a capsid protein. Journal of Virology 48:591–603
    [Google Scholar]
  14. Cross F. R., Garber E. A., Pellman D., Hanafusa H. 1984; A short sequence in the p60src N terminus is required for p60src myristylation and membrane association and for cell transformation. Molecular and Cellular Biology 4:1834–1842
    [Google Scholar]
  15. Cross G. A. M. 1987; Eukaryotic protein modification and membrane attachment via phosphatidylinositol. Cell 48:179–181
    [Google Scholar]
  16. Davison A. J., Scott J. E. 1986; The complete DNA sequence of varicella-zoster virus. Journal of General Virology 67:1759–1816
    [Google Scholar]
  17. Davison A. J., Marsden H. S., Wilkie N. M. 1981; One functional copy of the long terminal repeat gene specifying the immediate-early polypeptide IE 110 suffices for a productive infection of human foetal lung cells by herpes simplex virus. Journal of General Virology 55:179–191
    [Google Scholar]
  18. Draper K. G., Devi-Rao G., Costa R. H., Blair E. D., Thompson R. L., Wagner E. K. 1986; Characterization of the genes encoding herpes simplex virus type 1 and type 2 alkaline exonucleases and overlapping proteins. Journal of Virology 57:1023–1036
    [Google Scholar]
  19. Gibson W., Roizman B. 1972; Proteins specified by herpes simplex virus. VIII. Characterisation and composition of multiple capsid forms of subtypes 1 and 2. Journal of Virology 10:1044–1052
    [Google Scholar]
  20. Heilman C. J., Zweig M., Stephenson J. R., Hampar B. 1979; Isolation of a nucleocapsid polypeptide of HSV types 1 and 2 possessing immunologically type-specific and cross-reactive determinants. Journal of Virology 29:34–42
    [Google Scholar]
  21. Henderson L. E., Krutzsch H. C., Oroszlan S. 1983; Myristyl amino-terminal acylation of murine retrovirus proteins: an unusual post-translational protein modification. Proceedings of the National Academy of SciencesU.S.A 80:339–343
    [Google Scholar]
  22. Hope R. G., Palfreyman J., Suh M., Marsden H. S. 1982; Sulphated glycoproteins induced by herpes simplex virus. Journal of General Virology 58:399–415
    [Google Scholar]
  23. Johnson D. C., Spear P. G. 1983; O-linked oligosaccharides are acquired by herpes simplex virus glycoproteins in the Golgi apparatus. Cell 32:987–997
    [Google Scholar]
  24. Kaufman J. F., Krangel M. S., Strominger J. L. 1984; Cysteines in the transmembrane region of major histocompatibility complex antigens are fatty acylated via thioester bonds. Journal of Biological Chemistry 259:7230–7238
    [Google Scholar]
  25. Mcgeoch D. J., Dolan A., Donald S., Rixon F. J. 1985; Sequence determination and genetic content of the short unique region of the genome of herpes simplex virus type 1. Journal of Molecular Biology 181:1–13
    [Google Scholar]
  26. Mcgeoch D. J., Dolan A., Frame M. C. 1986; DNA sequence of the region in the genome of herpes simplex virus type 1 containing the exonuclease gene and neighbouring genes. Nucleic Acids Research 14:3435–3448
    [Google Scholar]
  27. Mcgeoch D. J., Dalrymple M. A., Davison A. J., Dolan A., Frame M. C., Mcnab D., Perry L. J., Scott J. E., Taylor P. 1988; The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. Journal of General Virology 69:1531–1574
    [Google Scholar]
  28. Macpherson I., Stoker M. 1962; Polyoma transformation of hamster cell clones - an investigation of genetic factors affecting cell competence. Virology 16:147–151
    [Google Scholar]
  29. Magee A. I., Courtneidge S. A. 1985; Two classes of fatty acid acylated proteins exist in eukaryotic cells. EMBO Journal 4:1137–1144
    [Google Scholar]
  30. Marsden H. S., Crombie I. K., Subak-Sharpe J. H. 1976; Control of protein synthesis in herpesvirus-infected cells: analysis of the polypeptides induced by wild-type and 16 temperature-sensitive mutants of HSV strain 17. Journal of General Virology 31:347–372
    [Google Scholar]
  31. Marsden H. S., Stow N. D., Preston V. G., Timbury M. C., Wilkie N. M. 1978; Physical mapping of herpes simplex virus-induced polypeptides. Journal of Virology 28:624–642
    [Google Scholar]
  32. Marsden H. S., Lang J., Davison A. J., Hope R. G., Macdonald D. M. 1982; Genomic location and lack of phosphorylation of the HSV immediate-early polypeptide IE 12. Journal of General Virology 62:17–27
    [Google Scholar]
  33. Olson E. N., Towler D. A., Glaser L. 1985; Specificity of fatty acid acylation of cellular proteins. Journal of Biological Chemistry 260:3784–3790
    [Google Scholar]
  34. Ozols J., Carr S. A., Strittmatter P. 1984; Identification of the NH2-terminal blocking group of NADH- cytochrome b5 reductase as myristic acid and the complete amino acid sequence of the membrane-binding domain. Journal of Biological Chemistry 259:13349–13354
    [Google Scholar]
  35. Paul A. V., Schultz A., Pincus S. E., Oroszlan S., Wimmer E. 1987; Capsid protein VP4 of poliovirus is N-myristylated. Proceedings of the National Academy of SciencesU.S.A 84:7827–7831
    [Google Scholar]
  36. Persing D. H., Varmus H. E., Ganem D. 1987; The preSl protein of hepatitis B virus is acylated at its amino terminus with myristic acid. Journal of Virology 61:1672–1677
    [Google Scholar]
  37. Pillai S., Baltimore D. 1987; Myristoylation and the post-translational acquisition of hydrophobicity by the membrane immunoglobulin heavy-chain polypeptide in B lymphocytes. Proceedings of the National Academy of SciencesU.S.A 84:7654–7658
    [Google Scholar]
  38. Preston V. G., Davison A. J., Marsden H. S., Timbury M. C., Subak-Sharpe J. H., Wilkie N. M. 1978; Recombinants between herpes simplex virus types 1 and 2: analysis of genome structures and expression of immediate early polypeptides. Journal of Virology 28:499–517
    [Google Scholar]
  39. Rein A., Mcclure M. R., Rice N. R., Luftig R. B., Schultz A. M. 1986; Myristylation site in Pr65gag is essential for virus particle formation by Moloney murine leukemia virus. Proceedings of the National Academy of SciencesU.S.A 83:7246–7250
    [Google Scholar]
  40. Rhee S. S., Hunter E. 1987; Myristylation is required for intracellular transport but not for assembly of D-type retrovirus capsids. Journal of Virology 61:1045–1053
    [Google Scholar]
  41. Rose J. K., Adams G. A., Gallione C. J. 1984; The presence of cysteine in the cytoplasmic domain of the vesicular stomatitis virus glycoprotein is required for palmitate addition. Proceedings of the National Academy of SciencesU.S.A 81:2050–2054
    [Google Scholar]
  42. Schmidt M. F. G. 1982a; Acylation of viral spike glycoproteins: a feature of enveloped RNA viruses. Virology 116:327–338
    [Google Scholar]
  43. Schmidt M. F. G. 1982b; Acylation of proteins - a new type of modification of membrane glycoproteins. Trends in Biochemical Sciences 7:322–324
    [Google Scholar]
  44. Schmidt M. F. G. 1984; The transfer of myristic and other fatty acids on lipid and viral protein acceptors in cultured cells infected with Semliki Forest and influenza virus. EMBO Journal 3:2295–2300
    [Google Scholar]
  45. Schmidt M. F. G., Bracha M., Schlesinger M. J. 1979; Evidence for covalent attachment of fatty acids to Sindbis virus glycoproteins. Proceedings of the National Academy of SciencesU.S.A 76:1687–1691
    [Google Scholar]
  46. Schultz A. M., Oroszlan S. 1983; In vivo modification of retroviral gag gene-encoded polyproteins by myristic acid. Journal of Virology 46:355–361
    [Google Scholar]
  47. Schultz A. M., Henderson L. E., Oroszlan S., Garber E. A., Hanafusa H. 1985; Amino terminal myristylation of the protein kinase p60src, a retroviral transforming protein. Science 227:427–429
    [Google Scholar]
  48. Sefton B. M., Buss J. E. 1987; The covalent modification of eukaryotic proteins with lipid. Journal of Cell Biology 104:1449–1453
    [Google Scholar]
  49. Sefton B. M., Trowbridge I. S., Cooper J. A. 1982; The transforming proteins of Rous sarcoma virus, Harvey sarcoma virus and Abelson virus contain tightly bound lipid. Cell 31:465–474
    [Google Scholar]
  50. Sheppard R. C. 1983; Continuous flow methods in organic synthesis. Chemistry in Britain 19:402–413
    [Google Scholar]
  51. Staufenbiel M., Lazarides E. 1986; Ankyrin is fatty acid acylated in erythrocytes. Proceedings of the National Academy of SciencesU.S.A 83:318–322
    [Google Scholar]
  52. Streuli C. H., Griffin B. E. 1987; Myristic acid is coupled to a structural protein of polyoma virus and SV40. Nature, London 326:619–622
    [Google Scholar]
  53. Timbury M. C. 1971; Temperature-sensitive mutants of herpes simplex virus type 2. Journal of General Virology 13:373–376
    [Google Scholar]
  54. Towler D. A., Adams S. P., Eubanks S. R., Towery D. S., Jackson-Machelski E., Glaser L., Gordon J. I. 1987; Purification and characterization of yeast myristoyl CoA: protein N-myristoyl-transferase. Proceedings of the National Academy of SciencesU.S.A 84:2708–2712
    [Google Scholar]
  55. Wilcox C, Hu J.-S., Olson E. N. 1987; Acylation of proteins with myristic acid occurs cotranslationally. Science 238:1275–1278
    [Google Scholar]
  56. Zweig M., Heilman C. J., Rabin H., Hampar B. 1980; Shared antigenic determinants between two distinct classes of proteins in cells infected with herpes simplex virus. Journal of Virology 35:644–652
    [Google Scholar]
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