The cellular RNA export receptor TAP/NXF1 is required for ICP27-mediated export of herpes simplex virus 1 RNA, but the TREX complex adaptor protein Aly/REF appears to be dispensable

Journal of Virology

Volumn 83, Issue 13, 2009, Pages 6335-6346

  Johnson, Lisa A ^a   Li, Ling ^a,b   Sandri Goldin, Rozanne M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Verdezyne Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN ALY; ADAPTOR PROTEIN REF; ADAPTOR PROTEIN TREX; CELL RECEPTOR; INFECTED CELL PROTEIN 27; POLYADENYLIC ACID; RNA EXPORT RECEPTOR NXF1; RNA EXPORT RECEPTOR TAP; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA; YELLOW FLUORESCENT PROTEIN; ICP27 PROTEIN, HUMAN HERPESVIRUS 1; IMMEDIATE EARLY PROTEIN; NUCLEAR PROTEIN; NUCLEOCYTOPLASMIC TRANSPORT PROTEIN; NXF1 PROTEIN, HUMAN; RNA BINDING PROTEIN; THOC4 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DEFECTIVE VIRUS; GENE EXPRESSION REGULATION; HERPES SIMPLEX VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA TRANSPORT; TRANSPORT KINETICS; VIRUS RECOMBINANT; VIRUS REPLICATION; ANIMAL; CERCOPITHECUS; GENE SILENCING; GENETICS; HELA CELL; HUMAN; METABOLISM; PHYSIOLOGY; RABBIT; VERO CELL;

HUMAN HERPESVIRUS 1;

ANIMALS; CERCOPITHECUS AETHIOPS; GENE EXPRESSION REGULATION, VIRAL; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HERPESVIRUS 1, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; NUCLEAR PROTEINS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; RABBITS; RNA TRANSPORT; RNA, SMALL INTERFERING; RNA, VIRAL; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS; VERO CELLS; VIRUS REPLICATION;

EID: 67449086121     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00375-09     Document Type: Article

References (52)

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. (Pubitemid 30069044)
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. Boyne, J. R., K. J. Colgan, and A. Whitehouse. 2008. Recruitment of the complete hTREX complex is required for Kaposi's sarcoma-associated herpesvirus intronless mRNA nuclear export and virus replication. PLoS Pathog. 4:e1000194.
4. 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.
5. Caceres, J. F., G. R. Screaton, and A. R. Krainer. 1998. A specific subset of SR proteins shuttles continuously between the nucleus and cytoplasm. Genes Dev. 12:55-66. (Pubitemid 28083658)
6. Chen, I. B., L. Li, L. Silva, and R. M. Sandri-Goldin. 2005. ICP27 recruits Aly/REF but not TAP/NXF1 to herpes simplex virus type 1 transcription sites although TAP/NXF1 is required for ICP27 export. J. Virol. 79:3949-3961. (Pubitemid 40388335)
7. Chen, I. B., K. S. Sciabica, and R. M. Sandri-Goldin. 2002. ICP27 interacts with the export factor Aly/REF to direct herpes simplex virus 1 intronless RNAs to the TAP export pathway. J. Virol. 76:12877-12889. (Pubitemid 35386971)
8. Cheng, H., K. Dufu, C. S. Lee, J. L. Hsu, A. Dias, and R. Reed. 2006. Human mRNA export machinery recruited to the 5′ end of mRNA. Cell 127:1389-1400.
9. Custodio, N., C. Carvalho, I. Condado, M. Antoniou, B. J. Blencowe, and M. Carmo-Fonseca. 2004. In vivo recruitment of exon junction complex proteins to transcription sites in mammalian cell nuclei. RNA 10:622-633.
10. Dai-Ju, J. Q., L. Li, L. A. Johnson, and R. M. Sandri-Goldin. 2006. ICP27 interacts with the C-terminal domain of RNA polymerase II and facilitates its recruitment to herpes simplex virus-1 transcription sites, where it undergoes proteasomal degradation during infection. J. Virol. 80:3567-3581.
11. Fribourg, S., I. C. Braun, E. Izaurralde, and E. Conti. 2001. Structural basis for the recognition of a nucleoporin FG repeat by the NTF2-like domain of the TAP/p15 mRNA nuclear export factor. Mol. Cell 8:645-656. (Pubitemid 32946941)
12. Gatfield, D., and E. Izaurralde. 2002. REF/Aly and the additional exon junction complex proteins are dispensable for nuclear mRNA export. J. Cell Biol. 159:579-588.
13. Gatfield, 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.
14. 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. (Pubitemid 128379243)
15. Hardwicke, M. A., P. J. Vaughan, R. E. Sekulovich, R. O'Conner, and R. M. Sandri-Goldin. 1989. The regions important for the activator and repressor functions of the HSV-1 alpha protein ICP27 map to the C-terminal half of the molecule. J. Virol. 63:4590-4602. (Pubitemid 19257833)
16. 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.
17. Hiriart, E., G. Farjot, H. Gruffat, M. V. C. Nguyen, A. Sergeant, and E. Manet. 2003. A novel nuclear export signal and a REF interaction domain both promote mRNA export by the Epstein-Barr virus EB2 protein. J. Biol. Chem. 278:335-342.
18. Hurt, E., K. Straber, A. Segref, S. Bailer, N. Schlaich, C. Presutti, D. Tollervey, and R. Jansen. 2000. Mex67p mediates nuclear export of a variety of RNA polymerase II transcripts. J. Biol. Chem. 275:8361-8368.
19. 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.
20. 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. (Pubitemid 29233144)
21. Katahira, J., K. Straesser, T. Saiwaki, Y. Yoneda, and E. Hurt. 2002. Complex formation between Tap and p15 affects binding to FG-repeat nucleoporins and nucleocytoplasmic shuttling. J. Biol. Chem. 277:9242-9246.
22. 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 to the cellular mRNA export pathway. EMBO J. 20:5769-5778. (Pubitemid 33010052)
23. Larsen, J. K., P. O. Jensen, and J. Larsen. 2001. Flow cytometric analysis of RNA synthesis by detection of bromouridine incorporation. Curr. Protoc. Cytom. doi:10.1002/0471142956.cy0712s12.
24. Le Hir, 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. (Pubitemid 32848650)
25. Le Hir, 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. (Pubitemid 32011679)
26. Le Hir, H., M. J. Moore, and L. E. Maquat. 2000. Pre-mRNA splicing alters mRNP composition: evidence for stable association of proteins at exon-exon junctions. Genes Dev. 14:1098-1108. (Pubitemid 30324423)
27. Li, L., L. A. Johnson, J. Q. Dai-Ju, and R. M. Sandri-Goldin. 2008. Hsc70 focus formation at the periphery of HSV-1 transcription sites requires ICP27. PLoS ONE 3:e1491. (Pubitemid 351827207)
28. Lischka, P., Z. Toth, M. Thomas, R. Mueller, and T. Stamminger. 2006. The UL69 transactivator protein of human cytomegalovirus interacts with DEXD/H-box RNA helicase UAP56 to promote cytoplasmic accumulation of unspliced RNA. Mol. Cell. Biol. 26:1631-1643.
29. Longman, D., I. L. Johnstone, and J. F. Caceres. 2003. The Ref/Aly proteins are dispensable for mRNA export and development in Caenorhabditis elegans. RNA 9:881-891.
30. 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.
31. MacMorris, M., C. Brocker, and T. Blumenthal. 2003. UAP56 levels affects viability and mRNA export in Caenorbditis elegans. RNA 9:847-857.
32. Malik, P., D. J. Blackbourn, and J. B. Clements. 2004. The evolutionarily conserved Kaposi's sarcoma-associated ORF57 protein interacts with REF protein and acts as an RNA export factor. J. Biol. Chem. 279:33001-33011.
33. Masuda, S., R. Das, H. Cheng, E. Hurt, N. Dorman, and R. Reed. 2005. Recruitment of the human TREX complex to mRNA during splicing. Genes Dev. 19:1512-1517.
34. Reed, R. 2003. Coupling transcription, splicing and mRNA export. Curr. Opinion Cell Biol. 15:326-331.
35. Reichert, V. L., H. LeHir, M. S. Jurica, and M. J. Moore. 2002. 5′ Exon interactions within the human spliceosome establish a framework for exon junction complex structure and assembly. Genes Dev. 16:2778-2791. (Pubitemid 35253146)
36. Rice, S. A., M. C. Long, V. Lam, and C. A. Spencer. 1994. RNA polymerase II is aberrantly phosphorylated and localized to viral replication compartments following herpes simplex virus infection. J. Virol. 68:988-1001. (Pubitemid 24022203)
37. 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.
38. 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. (Pubitemid 28150887)
39. 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. (Pubitemid 126508775)
40. 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.
41. Sciabica, K. S., Q. J. Dai, and R. M. Sandri-Goldin. 2003. ICP27 interacts with SRPK1 to mediate HSV-1 inhibition of pre-mRNA splicing by altering SR protein phosphorylation. EMBO J. 22:1608-1619. (Pubitemid 36417409)
42. + RNA and nuclear pores. EMBO J. 16:3256-3271.
43. 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.
44. 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. (Pubitemid 27492360)
45. Strasser, K., J. Bassler, and E. Hurt. 2000. Binding of the Mex67p/Mtr2p heterodimer to FXFG, GLFG and FG repeat nucleoporins is essential for nuclear mRNA export. J. Cell Biol. 150:695-706. (Pubitemid 30663408)
46. Strasser, K., S. Masuda, P. Mason, J. Pfannstiel, M. Oppizzi, S. Rodriguez- Navarro, A. G. Rondon, A. Aguilera, K. Struhl, R. Reed, and E. Hurt. 2002. TREX is a conserved complex coupling transcription with messenger RNA export. Nature 417:304-308. (Pubitemid 34534714)
47. 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. (Pubitemid 30212241)
48. Toth, Z., and T. Stamminger. 2008. The human cytomegalovirus regulatory protein UL69 and its effect on mRNA export. Front. Biosci. 13:2939-2949.
49. Wiegand, 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.
50. Wiegand, H. L., S. Lu, and B. R. Cullen. 2003. Exon junction complexes the enhancing effect of splicing on mRNA expression. Proc. Natl. Acad. Sci. USA 100:11327-11332.
51. 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.
52. Zhou, Z., M. J. Luo, K. Straesser, J. Katahira, E. Hurt, and R. Reed. 2000. The protein Aly links pre-messenger-RNA splicing to nuclear export in metazoans. Nature 407:401-405.