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Volume 79, Issue 7

Distinct domains in herpes simplex virus type 1 US11 protein mediate post-transcriptional transactivation of human T-lymphotropic virus type I envelope glycoprotein gene expression and specific binding to the Rex responsive element. Free

Abstract

Herpes simplexvirustype 1 (HSV-1)US11 protein is an RNA-binding protein which is able to mediate post-transcriptional transactivation of human T-lymphotropic virus type I (HTLV-I) envelope glycoprotein gene expression by interacting with the Rex responsive element (XRE) located at the 3′ end of the mRNA. In view of this functional activity, and because US11 protein is capable of substituting for HTLV-I Rex protein, it was hypothesized that US11 protein should exhibit at least two functional domains, an RNA-binding domain for specific interaction with the target RNA, and an effector domain involved in transport and translation of this mRNA. Recombinant US11 wild-type and deleted proteins were tested for their ability (i) to bind to the XRE and to HSV-1 UL34 RNA, the natural target of US11 protein, and (ii) to transactivate HTLV-I gene expression. The C-terminal half of US11 protein, consisting of 20–24 XPR repeats, was necessary and sufficient to mediate RNA-binding with a high affinity and specificity. Structure prediction analyses showed the likely conformation of this domain to be that of a polyproline type II helix. Localized within the first 40 amino acids of the N-terminal region of US11 protein was the effector domain, deletion of which created US11(Δ1–40), a -dominant negative mutant. These results demonstrate structural differences between US11 protein and proteins like Rex and Rev, despite their functional similarities.

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© Society for General Microbiology 1998
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1998-07-01
2024-04-27
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References

  1. Bayliss G. J., Marsden H. S., Hay J. 1975; Herpes simplex virus proteins: DNA binding proteins in infected cells and in the virus structure. Virology 68:124–134
     [Google Scholar]
  2. Bogerd H., Greene W. C. 1993; Dominant negative mutants of human T-cell leukemia virus type I rex and human immunodeficiency virus type 1 rev fail to multimerize in vivo. Journal of Virology 67:2496–2502
     [Google Scholar]
  3. Bogerd H. P., Tiley L. S., Cullen B. R. 1992; Specific binding of human T-cell leukemia virus type I Rex protein to a short RNA sequence located within the Rex-response element. Journal of Virology 66:7572–7575
     [Google Scholar]
  4. Bogerd H. P., Fridell R. A., Benson R. E., Hua J., Cullen B. R. 1996; Protein sequence requirements for function of the human T-cell leukemia virus type I Rex nuclear export signal delineated by a novel in vivo randomization-selection assay. Molecular and Cellular Biology 16:4207–42l4
     [Google Scholar]
  5. Burd C. G., Dreyfuss G. 1994; Conserved structures and diversity of functions of RNA-binding proteins. Science 265:615–621
     [Google Scholar]
  6. Cochrane A. W., Pekkins A., Rosen C. A. 1990; Identification of sequences important in the nucleolar localization of human immuno-deficiency virus Rev: relevance of nucleolar localization to function. Journal of Virology 64:881–885
     [Google Scholar]
  7. Cullen B. R. 1992; Mechanism of action of regulatory proteins encoded by complex retroviruses. Microbiological Reviews 56:375–394
     [Google Scholar]
  8. Daly T. J., Cook K. S., Gray G. S., Maione T. E., Rusche J. R. 1989; Specific binding of HIV-1 recombinant Rev protein to the Rev-responsive element in vitro. Nature 342:816–819
     [Google Scholar]
  9. Dalziel R. G., Marsden H. S. 1984; Identification of two herpes simplex virus type 1-induced proteins (21K and 22K) which interact specifically with the a sequence of herpes simplex virus DNA. Journal of General Virology 65:1467–1475
     [Google Scholar]
  10. Diaz J.-J., Simonin D., Massé T., Deviller P., Kindbeiter K., Denoroy L., Madjar J.-J. 1993; The herpes simplex virus type l US11 gene product is a phosphorylated protein found to be non-specifically associated with both ribosomal subunits. Journal of General Virology 74:397–406
     [Google Scholar]
  11. Diaz J.-J., Duc Dodon M., Schaerer-Uthurralt N., Simonin D., Kindbeiter K., Gazzolo L., Madjar J.-J. 1996; Post-transcriptional transactivation of human retroviral envelope glycoprotein expression by herpes simplex virus USll protein. Nature 379:273–277
     [Google Scholar]
  12. Diaz-Latoud C., Diaz J.-J., Fabre-Jonca N., Kindbeiter K., Madjar J.-J., Arrigo A.-P. 1997; Herpes simplex virus USll protein enhances recovery of protein synthesis and survival in heat shock treated HeLa cells. Cell Stress and Chaperones 2:119–131
     [Google Scholar]
  13. Fischer U., Meyer S., Teufel M., Heckel C., Lûhrmann R., Rautmann G. 1994; Evidence that HIV-l Rev directly promotes the nuclear export of unspliced RNA. EMBO Journal 13:4105–4112
     [Google Scholar]
  14. Ghisolfi-Nieto L., Joseph G., Puvion-Dutilleul F., Amalric F., Bouvet P. 1996; Nucleolin is a sequence-specific RNA-binding protein: characterization of targets on pre-ribosomal RNA. Journal of Molecular Biology 260:34–53
     [Google Scholar]
  15. Goldin A. L., Sandri-Goldin R. M., Levine M., Glorioso J. C. 1981; Cloning of herpes simplex virus type l sequences representing the whole genome. Journal of Virology 38:50–58
     [Google Scholar]
  16. Grate D., Wilson C. 1997; Role REVersal : understanding how RRE RNA binds its peptide ligand. Structure 5:7–11
     [Google Scholar]
  17. Greco A., Simonin D., Diaz J.-J., Barjhoux L., Kindbeiter K., Madjar J.-J., Massé T. 1994; The DNA sequence coding for the 5′ untranslated region of herpes simplex virus type 1 ICP22 mRNA mediates a high level of gene expression. Journal of General Virology 75:1693–1702
     [Google Scholar]
  18. Heaphy S., Dingwal I., Gait M. J., Green S. M., Karn J., Lowe A. D., Singh M., Skinner M. A. 1990; HIV-1 regulator of virion expression (Rev) protein binds to an RNA stem-loop structure located within the Rev response element region. Cell 60:685–693
     [Google Scholar]
  19. Herschlag D. 1995; RNA chaperones and the RNA folding problem. Journal of Biological Chemistry 270:20871–20874
     [Google Scholar]
  20. Hope T. J., Klein N. P., Elder M. E., Parslow T. G. 1992; Transdominant inhibition of human immunodeficiency virus type 1 Rev occurs through formation of inactive protein complexes. Journal of Virology 66:1849–1855
     [Google Scholar]
  21. Johnson P. A., MacLean C., Marsden H. S., Dalziel R. G., Everett R. D. 1986; The product of gene US11 of herpes simplex virus type 1 is expressed as a true late gene. Journal of General Virology 67:871–883
     [Google Scholar]
  22. Kim F. J., Beeche A. A., Hunter J. J., Chin D. J., Hope T. J. 1996; Characterization of the nuclear export signal of human T-cell lympho- tropic virus type I Rex reveals that nuclear export is mediated by position-variable hydrophobic interactions. Molecular and Cellular Biology 16:5147–5155
     [Google Scholar]
  23. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
     [Google Scholar]
  24. Longnecker R., Roizman B. 1987; Clustering of genes dispensable for growth in culture in the S component of the HSVl genome. Science 236:573–576
     [Google Scholar]
  25. McGeoch D. J., Dolan A., Donald S., Rixon F. J. 1985; Sequence determination and genetic content of the short unique region in the genome of herpes simplex type 1 virus. Journal of Molecular Biology 181:1–13
     [Google Scholar]
  26. MacLean C. A., Rixon F. J., Marsden H. S. 1987; The products of gene US11 of herpes simplex virus type 1 are DNA-binding and localize to the nucleoli of infected cells. Journal of General Virology 68:1921–1937
     [Google Scholar]
  27. Malim M. H., Cullen B. R. 1991; HIV-1 structural gene expression requires the binding of multiple Rev monomers to the viral RRE: implications for HIV-1 latency. Cell 65:241–248
     [Google Scholar]
  28. Malim M. H., Böhnlein S., Hauber J., Cullen B. R. 1989; Functional dissection of the HIV-1 Rev trans-activator - derivation of a transdominant repressor of Rev function. Cell 58:205–214
     [Google Scholar]
  29. Massé T., Garcin D., Jacquemont B., Madjar J.-J. 1990; Ribosome and protein synthesis modifications after infection of human epidermoid carcinoma cells with herpes simplex virus type 1. Molecular and General Genetics 220:1–12
     [Google Scholar]
  30. Meyer B., Meinkoth J. L., Malim M. H. 1996; Nuclear transport of human immunodeficiency virus type 1, visna virus, and equine infectious anemia virus Rev proteins: identification of a family of transferable nuclear export signals. Journal of Virology 70:2350–2359
     [Google Scholar]
  31. Puvion-Dutilleul F. 1987; Localization of viral-specific 21 kDa protein in nucleoli of herpes simplex infected cells. European Journal of Cell Biology 43:487–498
     [Google Scholar]
  32. Rimsky L., Hauber J., Dukovich M., Malim M. H., Langlois A., Cullen B. R., Greene W. C. 1988; Functional replacement of the HIV-1 Rev protein by the HTLV-I Rex protein. Nature 335:738–740
     [Google Scholar]
  33. Rimsky L., Duc Dodon M., Dixon E. P., Greene W. C. 1989; Trans-dominant inactivation of HTLV-I and HIV-1 gene expression by mutation of the HTLV-I Rex transactivator. Nature 341:453–456
     [Google Scholar]
  34. Roizman B., Sears A. E. 1993; Herpes simplex viruses and their replication. In The Human Herpesviruses chapter 2 pp. 11–68 Roizman B., Whitley R. J., Lopez C. Edited by New York: Lippincott-Raven;
     [Google Scholar]
  35. Roller R. J., Roizman B. 1990; The herpes simplex virus US11 open reading frame encodes a sequence-specific RNA-binding protein. Journal of Virology 64:3463–3470
     [Google Scholar]
  36. Roller R. J., Roizman B. 1991; Herpes simplex virus 1 RNA-binding protein US11 negatively regulates the accumulation of a truncated viral mRNA. Journal of Virology 65:5873–5879
     [Google Scholar]
  37. Roller R. J., Roizman B. 1992; The herpes simplex virus 1 RNA binding protein US11 is a virion component and associates with ribosomal 60S subunits. Journal of Virology 66:3624–3632
     [Google Scholar]
  38. Roller R. J., Roizman B. 1994; A herpes simplex virus 1 US11- expressing cell line is resistant to herpes simplex virus infection at a step in viral entry mediated by glycoprotein D. Journal of Virology 68:2830–2839
     [Google Scholar]
  39. Roller R. J., Monk L. L., Stuart D., Roizman B. 1996; Structure and function in the herpes simplex virus 1 RNA-binding protein US11 : mapping of the domain required for ribosomal and nucleolar association and RNA binding in vitro. Journal of Virology 70:2842–2851
     [Google Scholar]
  40. Seiki M., Hattori S., Hirayama Y., Yoshida M. C. 1983; Human adult T-cell leukemia virus : complete nucleotide sequence of the provirus genome integrated in leukemia cell DNA. Proceedings of the National Academy of Sciences, USA 80:3618–3622
     [Google Scholar]
  41. Shimoni L., Glusker J. 1995; Hydrogen bonding motifs of protein side chains : descriptions of binding of arginine and amide groups. Protein Science 4:65–74
     [Google Scholar]
  42. Simonin D., Diaz J.-J., Kindbeiter K., Pernas P., Madjar J.-J. 1995; Phosphorylation of herpes simplex virus type 1 US11 protein is independent of viral genome expression. Electrophoresis 16:1317–1322
     [Google Scholar]
  43. Siomi H., Shida H., Nam S. H., Nosaka T., Maki M., Hatanaka M. 1988; Sequence requirements for nucleolar localization of human T-cell leukemia virus type I pX protein, which regulates viral RNA processing. Cell 55:197–209
     [Google Scholar]
  44. Vartikar J. V., Draper E. D. 1989; S4-16S ribosomal RNA complex. Binding constant measurements and specific recognition of a 460-nucleotide region. Journal of Molecular Biology 209:221–234
     [Google Scholar]
  45. Ward P. L., Roizman B. 1994; Herpes simplex genes: the blueprint of a successful human pathogen. Trends in Genetics 10:267–274
     [Google Scholar]
  46. Wen W., Meinkoth J. L., Tsien R. Y., Taylor S. S. 1995; Identification of a signal for rapid export of proteins from the nucleus. Cell 82:463–473
     [Google Scholar]
  47. Williamson M. 1994; The structure and function of proline-rich regions in proteins. Biochemical Journal 297:249–260
     [Google Scholar]
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Distinct domains in herpes simplex virus type 1 US11 protein mediate post-transcriptional transactivation of human T-lymphotropic virus type I envelope glycoprotein gene expression and specific binding to the Rex responsive element.
J. Gen. Virol. 79, 1593 (1998); https://doi.org/10.1099/0022-1317-79-7-1593
/content/journal/jgv/10.1099/0022-1317-79-7-1593
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