Poly(A)-binding protein 1 partially relocalizes to the nucleus during herpes simplex virus type 1 infection in an ICP27-independent manner and does not inhibit virus replication

Journal of Virology

Volumn 84, Issue 17, 2010, Pages 8539-8548

  Salaun, C ^a,e   MacDonald, A I ^a   Larralde, O ^a,c   Howard, L ^a   Lochtie, K ^a   Burgess, H M ^b   Brook, M ^b   Malik, P ^a,d   Gray, N K ^b   Graham, S V ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c SCOTTISH NATIONAL BLOOD TRANSFUSION SERVICE   (United Kingdom)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ICP27 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; POLYADENYLIC ACID BINDING PROTEIN; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; VIRUS PROTEIN; CARRIER PROTEIN; ICP27 PROTEIN, HUMAN HERPESVIRUS 1; IMMEDIATE EARLY PROTEIN;

ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; ENZYME ACTIVATION; FEMALE; HELA CELL; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; VERO CELL; VIRUS REPLICATION; ANIMAL; CERCOPITHECUS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; VIROLOGY;

HUMAN HERPESVIRUS 1; SIMPLEXVIRUS;

ANIMALS; CARRIER PROTEINS; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; GENE EXPRESSION REGULATION, VIRAL; HELA CELLS; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; OXIDATIVE STRESS; POLY(A)-BINDING PROTEIN I; PROTEIN TRANSPORT; VERO CELLS; VIRUS REPLICATION;

EID: 77956642791     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00668-10     Document Type: Article

References (59)

1. Afonina, E., R. Stauber, and G. N. Pavlakis. 1998. The human poly(A)-binding protein 1 shuttles between the nucleus and the cytoplasm. J. Biol. Chem. 273:13015-13021.
2. Arias, C., D. Walsh, J. Harbell, A. C. Wilson, and I. Mohr. 2009. Activation of host translational control pathways by a viral developmental switch. PLoS Pathog. 5:1-12.
3. Beauchemin, C., and J.-F. Laliberté. 2007. The poly(A) binding protein is internalized in virus-induced vesicles or redistributed to the nucleolus during turnip mosaic virus infection. J. Virol. 81:10905-10913. (Pubitemid 47536065)
4. Boutell, C., and R. D. Everett. 2004. Herpes simplex virus type 1 infection induces the stabilization of p53 in a USP7- and ATM-independent manner. J. Virol. 78:8068-8077. (Pubitemid 38944291)
5. Deakin, N. O., and C. E. Turner. 2008. Paxillin comes of age. J. Cell Sci. 121:2435-2444.
6. Dobrikova, E., M. Shveygert, R. Walters, and M. Gromeier. 2010. Herpes simplex virus proteins ICP27 and UL47 associate with polyadenylate-binding protein and control its subcellular distribution. J. Virol. 84:270-279.
7. Dong, J.-M., L.-S. Lau, L. Lim, and E. Manser. 2009. Paxillin nuclearcytoplasmic localization is regulated by phosphorylation of the LD4 motif: evidence that nuclear paxillin promotes cell proliferation. Biochem. J. 418: 173-184.
8. Ellison, K. S., R. A. Maranchuk, K. L. Mottet, and J. R. Smiley. 2005. Control of VP16 translation by the herpes simplex virus type 1 immediate-early protein ICP27. J. Virol. 79:4120-4131. (Pubitemid 40388350)
9. Fontaine-Rodriguez, E. C., and D. M. Knipe. 2008. Herpes simplex virus ICP27 increases translation of a subset of viral late mRNAs. J. Virol. 82: 3538-3545.
10. Fontaine-Rodriguez, E. C., T. J. Taylor, M. Olesky, and D. M. Knipe. 2004. Proteomics of herpes simplex virus infected cell protein 27: association with translation initiation factors. Virology 330:487-492. (Pubitemid 39572854)
11. Gillis, P. A., L. H. Okagaki, and S. A. Rice. 2009. Herpes simplex virus type 1 ICP27 induces p38 mitogen-activated protein kinase signaling and apoptosis in HeLa cells. J. Virol. 83:1767-1777.
12. Gorgoni, B., and N. K. Gray. 2004. The roles of cytoplasmic poly(A)-binding proteins in regulating gene expression: a developmental perspective. Brief. Funct. Genomic. Proteomic. 3:125-141.
13. Harb, A., M. M. Becker, D. Vitour, C. H. Baron, P. Vende, S. C. Brown, S. Bolte, S. T. Arold, and D. Poncet. 2008. Nuclear localization of cytoplasmic poly(A)-binding protein upon rotavirus infection involves the interaction of NSP3 with eIF4G and RoXaN. J. Virol. 82:11283-11293.
14. Hardwicke, M., and R. M. Sandri-Goldin. 1994. The herpes simplex virus regulatory protein ICP27 contributes to the decrease in cellular mRNA levels during infection. J. Virol. 68:4797-4810. (Pubitemid 24226544)
15. Hardy, W. R., and R. M. Sandri-Goldin. 1994. Herpes simplex virus inhibits host cell splicing and regulatory protein ICP27 is required for this effect. J. Virol. 68:7790-7799.
16. Hargett, D., T. McLean, and S. L. Bachenheimer. 2005. Herpes simplex virus ICP27 activation of stress kinases JNK and p38. J. Virol. 79:8348-8360. (Pubitemid 40853538)
17. - herpes simplex virus 1: failure of activated RNA-dependent protein kinase to shut off protein synthesis is associated with a deletion in the domain of the α47 gene. J. Virol. 71:6049-6054.
18. Hosoda, N., F. Lejeune, and L. E. Maquat. 2006. Evidence that poly(A)-binding protein C1 binds nuclear pre-mRNA poly(A) tails. Mol. Cell. Biol. 26:3085-3097.
19. Huang, C., K. Jacobson, and M. D. Schaller. 2004. MAP kinases and cell migration. J. Cell Sci. 117:4619-4628.
20. Imataka, H., A. Gradi, and N. Sonenberg. 1998. A newly defined N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation. EMBO J. 17:7480-7489. (Pubitemid 29002714)
21. Jackson, R. J., C. U. T. Hellen, and T. V. Pestova. 2010. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol. 10:113-127.
22. Jean, S., K. M. LeVan, B. Song, M. Levine, and D. M. Knipe. 2010. Herpes simplex virus 1 ICP27 is required for transcription of two viral late (gamma2) genes in infected cells. Virology 283:273-284.
23. Johnson, L. A., and R. M. Sandri-Goldin. 2009. Efficient nuclear export of herpes simplex virus 1 transcripts requires both RNA binding by ICP27 and ICP27 interaction with TAP/NXF1. J. Virol. 83:1184-1192.
24. Kahvejian, A., G. Roy, and N. Sonenberg. 2001. The mRNA closed loop model: the function of PABP and PABP-interacting proteins in mRNA translation. Cold Spring Harbor Symp. Quant. Biol. 66:300.
25. Kanno, T., Y. Sato, T. Sata, and H. Katano. 2006. Expression of Kaposi's sarcoma-associated herpesvirus-encoded K10/10.1 protein in tissues and its interaction with poly(A)-binding protein. Virology 352:100-109. (Pubitemid 44142686)
26. Kavouras, J. H., E. Prandovszky, K. Valyi-Nagy, S. K. Kovacs, V. Tiwari, M. Kovacs, D. Shukla, and T. Valyi-Nagy. 2007. Herpes simplex virus type 1 infection induces oxidative stress and the release of bioactive lipid peroxidation by-products in mouse P19N neural cell cultures. J. Neurovirol. 13: 416-425.
27. Khaleghpour, K., Y. V. Svitkin, A. W. Craig, C. T. DeMaria, R. C. Deo, S. K. Burley, and N. Sonenberg. 2001. Translational repression by a novel partner of human poly(A) binding protein, Paip2. Mol. Cell 7:205-216. (Pubitemid 32162913)
28. Kuyumcu-Martinez, N. M., M. Joachims, and R. E. Lloyd. 2002. Efficient cleavage of ribosome-associated poly(A) binding protein by enterovirus 3C protease. J. Virol. 76:2062-2074.
29. Kuyumcu-Martinez, N. M., M. E. Van Eden, P. Youan, and R. E. Lloyd. 2004. Cleavage of poly(A)-binding protein by poliovirus 3C protease inhibits host cell translation: a novel mechanism for host translation shutoff. Mol. Cell. Biol. 24:1779-1790.
30. Larralde, O., R. W. P. Smith, G. S. Wilkie, P. Malik, N. K. Gray, and J. B. Clements. 2006. Direct stimulation of translation by the multifunctional herpesvirus ICP27 protein. J. Virol. 80:1588-1591. (Pubitemid 43134114)
31. Laurent, A.-M., J.-J. Madjar, and A. Greco. 1998. Translational control of viral and host protein synthesis during the course of herpes simplex virus type 1 infection: evidence that initiation of translation is the limiting step. J. Gen. Virol. 79:2765-2775.
32. Le, H., R. L. Tanguaym, M. L. Balasta, C. C. Wei, K. S. Browning, A. M. Metz, D. J. Goss, and D. R. Gallie. 1997. Translation initiation factors eIF-iso4G and eIF4B interact with the poly(A)-binding protein and increase its RNA binding activity. J. Biol. Chem. 272:16247-16255.
33. Lee, Y. J., and B. A. Glaunsinger. 2009. Aberrant herpesvirus-induced polyadenylation correlates with cellular messenger RNA destruction. PLoS Biol. 7:e1000107.
34. Lilley, C. E., C. T. Carson, A. R. Muotri, F. H. Gage, and M. D. Weitzman. 2005. DNA repair proteins affect the lifecycle of herpes simplex virus 1. Proc. Natl. Acad. Sci. U. S. A. 102:5844-5849.
35. McCarthy, A. M., L. McMahan, and P. A. Schaffer. 1989. Herpes simplex virus type 1 ICP27 deletion mutants exhibit altered patterns of transcription and are DNA deficient. J. Virol. 63:18-27.
36. Mulvey, M., C. Arias, and I. Mohr. 2006. Resistance of mRNA translation to acute endoplasmic reticulum stress-inducing agents in herpes simplex virus type 1-infected cells requires multiple virus-encoded functions. J. Virol. 80:7354-7363. (Pubitemid 44092558)
37. Mulvey, M., C. Arias, and I. Mohr. 2007. Maintenance of the endoplasmic reticulum (ER) homeostasis in herpes simplex virus type 1-infected cells through the association of a viral glycoprotein with PERK, a cellular ER stress sensor. J. Virol. 81:3377-3390. (Pubitemid 46456647)
38. Mulvey, M., J. Poppers, D. Sternberg, and I. Mohr. 2003. Regulation of eIF2α phosphorylation by different functions that act during discrete phases in the herpes simplex virus type 1 life cycle. J. Virol. 77:10917-10928. (Pubitemid 37204285)
39. Nguyen, M. L., and J. A. Blaho. 2007. Apoptosis during herpes simplex virus infection. Adv. Virus Res. 69:67-97.
40. Peters, G. A., D. Khoo, I. Mohr, and G. C. Sen. 2002. Inhibition of PACT-mediated activation of PKR by the herpes simplex virus type 1 Us11 protein. J. Virol. 76:11054-11064.
41. Piron, M., P. Vende, J. Cohen, and D. Poncet. 1998. Rotavirus RNA-binding protein NSP3 interacts with eIF4G1 and evicts the poly(A)-binding protein from eIF4F. EMBO J. 17:5811-5821. (Pubitemid 28445992)
42. Poppers, J., M. Mulvey, D. Khoo, and I. Mohr. 2000. Inhibition of PKR activation by the proline-rich RNA binding domain of the herpes simplex virus type 1 US11 protein. J. Virol. 74:11215-112221. (Pubitemid 32223989)
43. Rice, S. A., and D. M. Knipe. 1990. Genetic evidence for two distinct transactivation functions of the herpes simplex virus alpha protein ICP27. J. Virol. 64:1704-1715.
44. Roizman, B., and D. M. Knipe. 2001. Herpes simplex viruses and their replication, p. 2399-2459. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 4th ed., vol. 2. Lippincott Williams & Wilkins, Philadelphia, PA.
45. Sandri-Goldin, R. M., and G. E. Mendoza. 1992. A herpesvirus regulatory protein appears to act post-transcriptionally by affecting mRNA processing. Genes Dev. 6:848-863.
46. Smiley, J. R. 2004. Herpes simplex virus host shutoff protein: immune evasion by a viral RNase? J. Virol. 78:1063-1068.
47. Smiley, J. R., B. Panning, and C. A. Smibert. 1991. Regulation of cellular genes by HSV products, p. 151-179. In E. K. Wagner (ed.), Herpesvirus transcription and its regulation. CRC Press, Boca Raton, FL.
48. Smith, R. W. P., P. Malik, and J. B. Clements. 2005. The herpes simplex virus ICP27 protein: a multifunctional post-transcriptional regulator of gene expression. Biochem. Soc. Trans. 33:499-501.
49. Smith, I. L., M. Hardwicke, and R. M. Sandri-Goldin. 1992. Evidence that the herpes simplex virus immediate early protein ICP27 acts post- transcriptionally during infection to regulate gene expression. Virology 186:74-86.
50. Spriggs, K. A., M. Stoneley, M. Bushell, and A. E. Willis. 2008. Re-programming of translation following cell stress allows IRES-mediated translation to predominate. Biol. Cell 100:27-38.
51. Tarun, S. Z., and A. B. Sachs. 1996. Association of the yeast poly(A) binding protein with translation initiation factor eIF4G. EMBO J. 15:7168-7177.
52. van der Vlies, D., M. Makkinje, A. Jansens, I. Braakman, A. J. Verkleij, K. W. A. Wirtz, and J. A. Post. 2004. Oxidation of ER resident proteins upon oxidative stress: effects of altering cellular redox/antioxidant status and implications for protein maturation. Antioxid. Redox Signal. 5:381-389.
53. Walsh, D., C. Arias, C. Perez, D. Halladin, M. Escandon, T. Ueda, R. Watanabe-Fukunaga, R. Fukunaga, and I. Mohr. 2008. Eukaryotic translation initiation factor 4F architectural alterations accompany translation initiation factor redistribution in poxvirus-infected cells. Mol. Cell. Biol. 28: 2648-2658.
54. Walsh, D., and I. Mohr. 2004. Phosphorylation of eIF4E by Mnk-1 enhances HSV-1 translation and replication in quiescent cells. Genes Dev. 18:660-672. (Pubitemid 38489934)
55. Walsh, D., and I. Mohr. 2006. Assembly of an active translation initiation factor complex by a viral protein. Genes Dev. 20:461-472. (Pubitemid 43244400)
56. Walsh, D., C. Perez, J. Notary, and I. Mohr. 2005. Regulation of the translation initiation factor eIF4F by multiple mechanisms in human cytomegalovirus-infected cells. J. Virol. 79:8057-8064. (Pubitemid 40853509)
57. Woods, A. J., T. Kantidakis, H. Sabe, D. R. Critchley, and J. C. Norman. 2005. Interaction of paxillin with poly(A)-binding protein 1 and its role in focal adhesion turnover and cell migration. Mol. Cell. Biol. 25:3763-3773.
58. Woods, A. J., M. S. Roberts, J. Choudhary, S. T. Barry, Y. MAzaki, H. Sabe, S. J. Morley, D. R. Critchley, and J. C. Norman. 2002. Paxillin associates with poly(A)-binding protein 1 at the dense endoplasmic reticulum and the leading edge of migrating cells. J. Biol. Chem. 277:6428-6437.
59. Zachos, G., J. B. Clements, and J. Conner. 1999. Herpes simplex virus type 1 infection stimulates p38/c-Jun N-terminal mitogen-activated protein kinase pathways and activates transcription factor AP-1. J. Biol. Chem. 274:5097-5103.