ICP27 interacts with the RNA export factor Aly/REF to direct herpes simplex virus type 1 intronless mRNAs to the TAP export pathway

Journal of Virology

Volumn 76, Issue 24, 2002, Pages 12877-12889

  Chen, I Hsiung Brandon ^a   Sciabica, Kathryn S ^a   Sandri Goldin, Rozanne M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LEPTOMYCIN B; NUCLEOPORIN; PROTEIN ALY; PROTEIN ICP 27; PROTEIN REF; PROTEIN SC 35; PROTEIN TAP; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CROSS LINKING; CYTOPLASM; EMBRYO; GENE DELETION; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRON; MAMMAL CELL; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RNA SPLICING; SPLICEOSOME; VIRUS MUTANT; XENOPUS;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CELL LINE; DACTINOMYCIN; FATTY ACIDS, UNSATURATED; HERPESVIRUS 1, HUMAN; IMMEDIATE-EARLY PROTEINS; INTRONS; RABBITS; RNA, MESSENGER; RNA, VIRAL; TRANSCRIPTION FACTORS;

EID: 0036892520     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.76.24.12877-12889.2002     Document Type: Article

References (62)

1. Bachi, A., I. C. Braun, J. P. Rodrigues, N. Pante, K. Ribbeck, C. von Kobbe, U. Kutay, M. Wilm, D. Gorlich, M. Carmo-Fonseca, and E. Izaurralde. 2000. The C-terminal domain of TAP interacts with the nuclear pore complex and promotes export of specific CTE-bearing RNA substrates. RNA 6:136-158.
2. Bear, J., W. Tan, A. S. Zolotukhin, C. Tabernero, E. A. Hudson, and B. K. Felber. 1999. Identification of novel import and export signals of human TAP, the protein that binds to the Constitutive Transport Element of the type D retrovirus mRNAs. Mol. Cell. Biol. 19:6306-6317.
3. Braun, I. C., A. Herold, M. Rode, E. Conti, and E. Izaurralde. 2001. Overexpression of TAP/p15 heterodimers bypasses nuclear retention and stimulates nuclear mRNA export. J. Biol. Chem. 276:20536-20543.
4. Bryant, H. E., S. Wadd, A. I. Lamond, S. J. Silverstein, and J. B. Clements. 2001. Herpes simplex virus IE63 (ICP27) protein interacts with spliceosomeassociated protein 145 and inhibits splicing prior to the first catalytic step. J. Virol. 75:4376-4385.
5. Cullen, B. R. 2000. Connections between the processing and nuclear export of mRNA: Evidence for an export license? Proc. Natl. Acad. Sci. USA 97:4-6.
6. Cullen, B. R. 2000. Nuclear RNA export pathways. Mol. Cell. Biol. 20:4181-4187.
7. Fischer, U., J. Huber, W. C. Boelens, I. W. Mattaj, and R. Luhrmann. 1995. The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell 82:475-483.
8. Fornerod, M., M. Ohno, M. Yoshida, and I. W. Mattaj. 1997. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90:1051-1060.
9. Freisen, W. J., S. Paushkin, A. Wyce, S. Massenet, G. S. Pesiridis, G. Van Duyne, J. Rappsilber, M. Mann, and G. Dreyfuss. 2001. The methylosome, a 20S complex containing JBP1 and pICln, produces dimethylarginine-modified Sm proteins. Mol. Cell. Biol. 21:8289-8300.
10. Garfield, D., H. LeHir, C. Schmitt, I. C. Braun, T. Kocher, M. Wilm, and E. Izaurralde. 2001. The DexH/D box protein HEL/UAP56 is essential for mRNA export in Drosophila. Curr. Biol. 11:1716-1721.
11. Gruter, P., C. Tabernero, C. von Kobbe, C. Schmitt, C. Saavedra, A. Bacchi, M. Wilm, B. K. Felber, and E. Izaurralde. 1998. TAP, the human homologue of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol. Cell 1:649-659.
12. Hardwicke, M. A., and R. M. Sandri-Goldin. 1994. The herpes simplex virus regulatory protein ICP27 can cause a decrease in cellular mRNA levels during infection. J. Virol. 68:4797-4810.
13. 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.
14. Herold, A., M. Suyama, J. P. Rodrigues, I. C. Braun, U. Kutay, M. Carmo-Fonseca, P. Bork, and E. Izaurralde. 2000. TAP (NXF1) belongs to a multigene family of putative RNA export factors with a conserved modular architecture. Mol. Cell. Biol. 20:8996-9008.
15. Hibbard, M. K., and R. M. Sandri-Goldin. 1995. Arginine-rich regions succeeding the nuclear localization region of the HSV-1 regulatory protein ICP27 are required for efficient nuclear localization and late gene expression. J. Virol. 69:4656-4667.
16. Kang, Y., and B. R. Cullen. 1999. The human Tap protein is a nuclear mRNA export factor that contains novel RNA-binding and nucleocytoplasmic transport sequences. Genes Dev. 13:1126-1139.
17. Katahira, J., K. Straber, A. Podtelejnikov, M. Mann, J. U. Jung, and E. Hurt. 1999. The Mex-67p-mediated nuclear mRNA export pathway is conserved from yeast to human. EMBO J. 18:2593-2609.
18. Kataoka, N., J. Yong, V. N. Kim, F. Velazquez, R. A. Perkinson, F. Wang, and G. Dreyfuss. 2000. Pre-mRNA splicing imprints mRNA in the nucleus with a novel RNA-binding protein that persists in the cytoplasm. Mol. Cell 6:673-682.
19. Kehlenbach, R. H., A. Dickmanns, and L. Gerace. 1998. Nucleocytoplasmic shuttling factors including Ran and CRM1 mediate nuclear export of NFAT in vitro. J. Cell Biol. 141:863-874.
20. Koffa, M. D., J. B. Clements, E. Izaurralde, S. Wadd, S. A. Wilson, I. W. Mattaj, and S. Kuersten. 2001. Herpes simplex virus ICP27 protein provides viral mRNAs with access tot he cellular mRNA export pathway. EMBO J. 20:5769-5778.
21. Komeili, A., and E. K. O'Shea. 2001. New perspectives on nuclear transport. Annu. Rev. Genet. 35:341-364.
22. Kudo, N., B. Wolff, T. Sekimoto, E. P. Schreiner, Y. Yoneda, M. Yanagida, S. Horinouchi, and M. Yoshida. 1998. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRMI. Exp. Cell Res. 242:540-547.
23. LeHir, H., D. Gatfield, E. Izaurralde, and M. J. Moore. 2001. The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J. 20:4987-4997.
24. LeHir, H., E. Izaurralde, L. E. Maquat, and M. J. Moore. 2000. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 19:6860-6869.
25. Liu, X., and J. E. Mertz. 1995. HnRNP L binds a cis-acting RNA sequence element that enables intron-independent gene expression. Genes Dev. 9:1766-1780.
26. Love, D. C., T. D. Sweitzer, and J. A. Hanover. 1998. Reconstitution of HIV-1 Rev nuclear export: Independent requirements for nuclear import and export. Proc. Natl. Acad. Sci. USA 95:10608-10613.
27. Luo, M. J., and R. Reed. 1999. Splicing is required for rapid and efficient mRNA export in metazoans. Proc. Natl. Acad. Sci. USA 96:14937-14942.
28. Luo, M. J., Z. Zhou, K. Magni, C. Christoforides, J. Rappsilber, M. Mann, and R. Reed. 2001. Pre-mRNA splicing and mRNA export linked by direct interactions between UAP56 and Aly. Nature 413:644-647.
29. Mears, W. E., V. Lam, and S. A. Rice. 1995. Identification of nuclear and nucleolar localization signals in the herpes simplex virus regulatory protein ICP27. J. Virol. 69:935-947.
30. Mears, W. E., and S. A. Rice. 1996. The RGG box motif of the herpes simplex virus ICP27 protein mediates an RNA-binding activity and determines in vivo methylation. J. Virol. 70:7445-7453.
31. Mears, W. E., and S. A. Rice. 1998. The herpes simplex virus immediate-early protein ICP27 shuttles between the nucleus and cytoplasm. Virology 242:128-137.
32. Meister, G., C. Eggert, D. Buhler, H. Brahms, C. Kambach, and U. Fischer. 2001. Methylation of Sm proteins by a complex containing PRMT5 and the putative U snRNP assembly factor pICln. Curr. Biol. 11:1990-1994.
33. Michael, W. M., M. Choi, and G. Dreyfuss. 1995. A nuclear export signal in hnRNP A1: A signal-mediated, temperature-dependent nuclear protein export pathway. Cell 83:415-422.
34. Neubauer, G., A. King, J. Rappsilber, C. Calvio, M. Watson, P. Ajuh, J. Sleeman, A. Lamond, and M. Mann. 1998. Mass spectrometry and ESTdatabase searching allows characterization of the multi-protein spliceosome complex. Nat. Genet. 20:46-50.
35. Neville, M., and M. Rosbash. 1999. The NES-Crm1 export pathway is not a major mRNA export route in Saccharomyces cerevisiae. EMBO J. 18:3746-3756.
36. Otero, G. C., and T. J. Hope. 1998. Splicing-independent expression of the herpes simplex virus type 1 thymidine kinase gene is mediated by three cis-acting RNA subelements. J. Virol. 72:9889-9896.
37. Phelan, A., M. Carmo-Fonseca, J. McLauchlan, A. I. Lamond, and J. B. Clements. 1993. A herpes simplex virus type 1 immediate-early gene product, IE63, regulates small nuclear ribonucleoprotein distribution. Proc. Natl. Acad. Sci. USA 90:9056-9060.
38. Phelan, A., and J. B. Clements. 1997. Herpes simplex virus type 1 immediate early protein IE63 shuttles between nuclear compartments and the cytoplasm. J. Gen. Virol. 78:3327-3331.
39. Pinol-Roma, S., and G. Dreyfuss. 1992. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 355:730-732.
40. Rodrigues, J. P., M. Rode, D. Gatfield, B. J. Blencowe, M. Carmo-Fonseca, and E. Izaurralde. 2001. REF proteins mediate the export of spliced and unspliced mRNAs from the nucleus. Proc. Natl. Acad. Sci. USA 98:1030-1035.
41. Sandri-Goldin, R. M. 1998. ICP27 mediates herpes simplex virus RNA export by shuttling through a leucine-rich nuclear export signal and binding viral intronless RNAs through an RGG motif. Genes Dev. 12:868-879.
42. Sandri-Goldin, R. M. 1998. Interactions between an HSV regulatory protein and cellular mRNA processing pathways. Methods 16:95-104.
43. Sandri-Goldin, R. M., and M. K. Hibbard. 1996. The herpes simplex virus type 1 regulatory protein ICP27 coimmunoprecipitates with anti-Sm antiserum and an the C terminus appears to be required for this interaction. J. Virol. 70:108-118.
44. Sandri-Goldin, R. M., M. K. Hibbard, and M. A. Hardwicke. 1995. The C-terminal repressor region of HSV-1 ICP27 is required for the redistribution of small nuclear ribonucleoprotein particles and splicing factor SC35; however, these alterations are not sufficient to inhibit host cell splicing. J. Virol. 69:6063-6076.
45. Santos-Rosa, H., H. Moreno, G. Simos, A. Segref, B. Fahrenkrog, N. Pante, and E. Hurt. 1998. Nuclear mRNA export requires complex formation between Mex67p and Mtr2p at the nuclear pores. Mol. Cell. Biol. 18:6826-6838.
46. Schmitt, I., and L. Gerace. 2001. In vitro analysis of nuclear transport mediated by the C-terminal shuttle domain of Tap. J. Biol. Chem. 276:42355-42363.
47. + RNA and nuclear pores. EMBO J. 16:3256-3271.
48. Shen, E. C., M. F. Henry, V. H. Weiss, S. R. Valentini, P. A. Silver, and M. S. Lee. 1998. Arginine methylation facilitates the nuclear export of hnRNP proteins. Genes Dev. 12:679-691.
49. Smith, I. L., M. A. 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. Soliman, T. M., R. M. Sandri-Goldin, and S. 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.
51. Soliman, T. M., and S. J. Silverstein. 2000. Herpesvirus mRNAs are sorted for export via CRM1-dependent and -independent pathways. J. Virol. 74:2814-2825.
52. Soliman, T. M., and S. J. Silverstein. 2000. Identification of an export control sequence and a requirement for the KH domains in ICP27 from herpes simplex virus type 1. J. Virol. 74:7600-7609.
53. Straber, K., and E. Hurt. 2000. Yra1p, a conserved nuclear RNA-binding protein, interacts directly with Mex67p and is required for mRNA export. EMBO J. 19:410-420.
54. Straber, K., and E. Hurt. 2001. Splicing factor Sub2p is required for nuclear mRNA export through its interaction with Yra1p. Nature 413:648-652.
55. Stutz, F., A. Bachi, T. Doerks, I. C. Braun, B. Seraphin, M. Wilm, P. Bork, and E. Izaurralde. 2000. REF, an evolutionary conserved family of hnRNP-like proteins, interacts with TAP/Mex67p and participates in mRNA nuclear export. RNA 6:638-650.
56. Tan, W., A. S. Zolotukhin, J. Bear, D. J. Patenaude, and B. Felber. 2000. The mRNA export of Caenorhabditis elegans is mediated by Ce-NFX-1, an ortholog of human TAP/NFX and Saccharomyces cerevisiae Mex67p. RNA 6:1762-1772.
57. Weigand, H. L., G. A. Coburn, Y. Zeng, Y. Kang, H. P. Bogerd, and B. R. Cullen. 2002. Formation of Tap/NXT1 heterodimers activates Tap-dependent nuclear mRNA export by enhancing recruitment to nuclear pore complexes. Mol. Cell. Biol. 22:245-256.
58. Zenklusen, D., and F. Stutz. 2001. Nuclear export of mRNA. FEBS Lett. 498:150-156.
59. Zenklusen, D., P. Vinciguerra, Y. Strahm, and F. Stutz. 2001. The yeast hnRNP-like proteins Yra1p and Tra2p participate in mRNA export through interaction with Mex67p. Mol. Cell. Biol. 21:4219-4232.
60. Zhi, Y., and R. M. Sandri-Goldin. 1999. Analysis of the phosphorylation sites of the herpes simplex virus type 1 regulatory protein ICP27. J. Virol. 73:3246-3257.
61. Zhi, Y., K. S. Sciabica, and R. M. Sandri-Goldin. 1999. Self interaction of the herpes simplex virus type 1 regulatory protein ICP27. Virology 257:341-351.
62. Zhou, Z., M. J. Luo, K. Straesser, J. Katahira, E. Hurt, and R. Reed. 2001. The protein Aly links pre-messenger-RNA splicing to nuclear export in metazoans. Nature 407:401-405.