Herpes simplex virus 1 induces cytoplasmic accumulation of TIA-1/TIAR and both synthesis and cytoplasmic accumulation of tristetraprolin, two cellular proteins that bind and destabilize AU-Rich RNAs

Journal of Virology

Volumn 78, Issue 16, 2004, Pages 8582-8592

  Esclatine, Audrey ^a   Taddeo, Brunella ^a   Roizman, Bernard ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; RIBOSOME RNA;

ADENYLATION; ANIMAL CELL; ARTICLE; CELL STRUCTURE; DNA DEGRADATION; FIBROBLAST; GENETIC CODE; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN RNA BINDING; PROTEIN SECRETION; PROTEIN SYNTHESIS INHIBITION; RNA DEGRADATION; RNA STABILITY; VIRUS INDUCTION;

CELL LINE, TUMOR; CELLS, CULTURED; CYTOPLASM; DNA-BINDING PROTEINS; FIBROBLASTS; HELA CELLS; HERPESVIRUS 1, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; POLY(A)-BINDING PROTEINS; PROTEINS; RNA, MESSENGER; RNA-BINDING PROTEINS; TRISTETRAPROLIN; UP-REGULATION; VIRAL PROTEINS;

EID: 3543058093     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.16.8582-8592.2004     Document Type: Article

References (46)

1. Advani, S. J., R. R. Weichselbaum, and B. Rolzman. 2000. E2F proteins are posttranslationally modified concomitantly with a reduction in nuclear binding activity in cells infected with herpes simplex virus 1. J. Virol. 74:7842-7850.
2. Anderson, P., and N. Kedersha. 2002. Stressful initiations. J. Cell Sci. 115:3227-3234.
3. Anderson, P., and N. Kedersha. 2002. Visibly stressed: the role of eIF2, TIA-1, and stress granules in protein translation. Cell Stress Chaperones 7:213-221.
4. Arlt, A., O. Grobe, A. Sieke, M. L. Kruse, U. R. Folsch, W. E. Schmidt, and H. Schafer. 2001. Expression of the NF-kappa B target gene IEX-1 (p22/ PRG1) does not prevent cell death but instead triggers apoptosis in HeLa cells. Oncogene 20:69-76.
5. Bevilacqua, A., M. C. Ceriani, S. Capaccioli, and A. Nicolin. 2003. Posttranscriptional regulation of gene expression by degradation of messenger RNAs. J. Cell Physiol. 195:356-372.
6. Blackshear, P. J. 2002. Tristetraprolin and other CCCH tandem zinc-finger proteins in the regulation of mRNA turnover. Biochem. Soc. Trans. 30:945-952.
7. Bresnahan, W. A., G. E. Hultman, and T. Shenk. 2000. Replication of wild-type and mutant human cytomegalovirus in life-extended human diploid fibroblasts. J. Virol. 74:10816-10818.
8. Carballo, E., W. S. Lai, and P. J. Blackshear. 1998. Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin. Science 281:1001-1005.
9. Chee, A. V., P. Lopez, P. P. Pandolfi, and B. Roizman. 2003. Promyelocytic leukemia protein mediates interferon-based anti-herpes simplex virus 1 effects. J. Virol. 77:7101-7105.
10. Chen, C. Y., R. Gherzi, S. E. Ong, E. L. Chan, R. Raijmakers, G. J. Pruijn, G. Stoecklin, C. Moroni, M. Mann, and M. Karin. 2001. AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107:451-464.
11. Chen, C. Y., N. Xu, and A. B. Shyu, 1995. mRNA decay mediated by two distinct AU-rich elements from c-fos and granulocyte-macrophage colony-stimulating factor transcripts: different deadenylation kinetics and uncoupling from translation. Mol. Cell. Biol. 15:5777-5788.
12. Chou, J., J. J. Chen, M. Gross, and B. Roizman. 1995. Association of a M(r) 90,000 phosphoprotein with protein kinase PKR in cells exhibiting enhanced phosphorylation of translation initiation factor eIF-2 alpha and premature shutoff of protein synthesis after infection with gamma 134.5- mutants of herpes simplex virus 1. Proc. Natl. Acad. Sci. USA 92:10516-10520.
13. Ejercito, P. M., E. D. Kieff, and B. Roizman. 1968. Characterization of herpes simplex virus strains differing in their effects on social behaviour of infected cells. J. Gen. Virol. 2:357-364.
14. Ellison, K. S., S. A. Rice, R. Verity, and J. R. Smiley. 2000. Processing of alpha-globin and ICP0 mRNA in cells infected with herpes simplex virus type 1 ICP27 mutants. J. Virol. 74:7307-7319.
15. Esclatine, A., B. Taddeo, L. Evans, and B. Roizman. 2004. The herpes simplex virus 1 UL41 gene-dependent destabilization of cellular RNAs is selective and may be sequence-specific. Proc. Natl. Acad. Sci. USA 101:3603-3608.
16. Fairhurst, A. M., J. E. Connolly, K. A. Hintz, N. J. Goulding, A. J. Rassias, M. P. Yeager, W. Rigby, and P. K. Wallace. 2003. Regulation and localization of endogenous human tristetraprolin. Arthritis Res. Ther. 5:R214-R225.
17. Feng, P., D. N. Everly, Jr., and G. S. Read. 2001. mRNA decay during herpesvirus infections: interaction between a putative viral nuclease and a cellular translation factor. J. Virol. 75:10272-10280.
18. Gao, M., C. J. Wilusz, S. W. Peltz, and J. Wilusz. 2001. A novel mRNA-decapping activity in HeLa cytoplasmic extracts is regulated by AU-rich elements. EMBO J. 20:1134-1143.
19. Gu, H., and B. Roizman. 2003. The degradation of promyelocytic leukemia and Sp100 proteins by herpes simplex virus 1 is mediated by the ubiquitin-conjugating enzyme UbcH5a. Proc. Natl. Acad. Sci. USA 100:8963-8968.
20. Gueydan, C., L. Droogmans, P. Chalon, G. Huez, D. Caput, and V. Kruys. 1999. Identification of TIAR as a protein binding to the translational regulatory AU-rich element of tumor necrosis factor alpha mRNA. J. Biol. Chem. 274:2322-2326.
21. He, B., M. Gross, and B. Roizman. 1997. The gamma(1)34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1alpha to dephosphorylate the alpha subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNA-activated protein kinase. Proc. Natl. Acad. Sci. USA 94:843-848.
22. Hrdlickova, R., J. Nehyba, A. Roy, E. H. Humphries, and H. R. Bose, Jr. 1995. The relocalization of v-Rel from the nucleus to the cytoplasm coincides with induction of expression of IκBα and NF-κB1 and stabilization of IκBα. J. Virol. 69:403-413.
23. Karr, B. M., and G. S. Read. 1999. The virion host shutoff function of herpes simplex virus degrades the 5′ end of a target mRNA before the 3′ end. Virology 264:195-204.
24. Kawakami, A., Q. Tian, M. Streuli, M. Poe, S. Edelhoff, C. M. Disteche, and P. Anderson. 1994. Intron-exon organization and chromosomal localization of the human TIA-1 gene. J. Immunol. 152:4937-4945.
25. Kedersha, N., and P. Anderson. 2002. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30:963-969.
26. Kedersha, N. L., M. Gupta, W. Li, I. Miller, and P. Anderson. 1999. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J. Cell Biol. 147:1431-1442.
27. Khodarev, N. N., S. J. Advani, N. Gupta, B. Roizman, and R. R. Weichselbaum. 1999. Accumulation of specific RNAs encoding transcriptional factors and stress response proteins against a background of severe depletion of cellular RNAs in cells infected with herpes simplex virus 1. Proc. Natl. Acad. Sci. USA 96:12062-12067.
28. Kwong, A. D., and N. Frenkel. 1987. Herpes simplex virus-infected cells contain a function(s) that destabilizes both host and viral mRNAs. Proc. Natl. Acad. Sci. USA 84:1926-1930.
29. Kwong, A. D., J. A. Kruper, and N. Frenkel. 1988. Herpes simplex virus virion host shutoff function. J. Virol. 62:912-921.
30. Lai, W. S., E. A. Kennington, and P. J. Blackshear. 2003. Tristetraprolin and its family members can promote the cell-free deadenylation of AU-rich element-containing mRNAs by poly(A) ribonuclease. Mol. Cell. Biol. 23:3798-3812.
31. Lai, W. S., D. J. Stumpo, and P. J. Blackshear. 1990. Rapid insulin-stimulated accumulation of an mRNA encoding a proline-rich protein. J. Biol. Chem. 265:16556-16563.
32. Lee, G. E., G. A. Church, and D. W. Wilson. 2003. A subpopulation of tegument protein Vhs localizes to detergent-insoluble lipid rafts in herpes simplex virus-infected cells. J. Virol. 77:2038-2045.
33. Ogawa, K., F. Chen, Y. J. Kim, and Y. Chen. 2003. Transcriptional regulation of tristetraprolin by transforming growth factor-beta in human T cells. J. Biol. Chem. 278:30373-30381.
34. Piecyk, M., S. Wax, A. R. Beck, N. Kedersha, M. Gupta, B. Maritim, S. Chen, C. Gueydan, V. Kruys, M. Streuli, and P. Anderson. 2000. TIA-1 is a translational silencer that selectively regulates the expression of TNF-alpha. EMBO J. 19:4154-4163.
35. Poon, A. P., and B. Roizman. 1997. Differentiation of the shutoff of protein synthesis by virion host shutoff and mutant gamma (1)34.5 genes of herpes simplex virus 1. Virology 229:98-105.
36. Read, G. S., and N. Frenkel. 1983. Herpes simplex virus mutants defective in the virion-associated shutoff of host polypeptide synthesis and exhibiting abnormal synthesis of alpha (immediate early) viral polypeptides. J. Virol. 46:498-512.
37. Sawaoka, H., D. A. Dixon, J. A. Oates, and O. Boutaud. 2003. Tristetraprolin binds to the 3′-untranslated region of cyclooxygenase-2 mRNA. A polyadenylation variant in a cancer cell line lacks the binding site. J. Biol. Chem. 278:13928-13935.
38. Smiley, J. R. 2004. Herpes simplex virus virion host shutoff protein: immune evasion mediated by a viral RNase? J. Virol. 78:1063-1068.
39. Soliman, T. M., R. M. Sandri-Goldin, and S. J. Silverstein. 1997. Shuttling of the herpes simplex virus type 1 regulatory protein ICP27 between the nucleus and cytoplasm mediates the expression of late proteins. J. Virol. 71:9188-9197.
40. Stoecklin, G., B. Gross, X. F. Ming, and C. Moroni. 2003. A novel mechanism of tumor suppression by destabilizing AU-rich growth factor mRNA. Oncogene 22:3554-3561.
41. Taddeo, B., A. Esclatine, and B. Roizman. 2002. The patterns of accumulation of cellular RNAs in cells infected with a wild-type and a mutant herpes simplex virus 1 lacking the virion host shutoff gene. Proc. Natl. Acad. Sci. USA 99:17031-17036.
42. Taddeo, B., A. Esclatine, W. Zhang, and B. Roizman. 2003. The stress-inducible immediate-early responsive gene IEX-1 is activated in cells infected with herpes simplex virus 1, but several viral mechanisms, including 3′ degradation of its RNA, preclude expression of the gene. J. Virol. 77:6178-6187.
43. Taddeo, B., T. R. Luo, W. Zhang, and B. Roizman. 2003. Activation of NF-kappaB in cells productively infected with HSV-1 depends on activated protein kinase R and plays no apparent role in blocking apoptosis. Proc. Natl. Acad. Sci. USA 100:12408-12413.
44. Taupin, J. L., Q. Tian, N. Kedersha, M. Robertson, and P. Anderson. 1995. The RNA-binding protein TIAR is translocated from the nucleus to the cytoplasm during Fas-mediated apoptotic cell death. Proc. Natl. Acad. Sci. USA 92:1629-1633.
45. Taylor, G. A., M. J. Thompson, W. S. Lai, and P. J. Blackshear. 1996. Mitogens stimulate the rapid nuclear to cytosolic translocation of tristetraprolin, a potential zinc-finger transcription factor. Mol. Endocrinol. 10:140-146.
46. Worthington, M. T., J. W. Pelo, M. A. Sachedina, J. L. Applegate, K. O. Arseneau, and T. T. Pizarro. 2002. RNA binding properties of the AU-rich element-binding recombinant Nup475/TIS11/tristetraprolin protein. J. Biol. Chem. 277:48558-48564.