HIV-1 Rev protein specifies the viral RNA export pathway by suppressing TAP/NXF1 recruitment

Nucleic Acids Research

Volumn 42, Issue 10, 2014, Pages 6645-6658

  Taniguchi, Ichiro ^a   Mabuchi, Naoto ^a   Ohno, Mutsuhito ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EXPORTIN 1; MULTIPROTEIN COMPLEX; REV PROTEIN; RNA BINDING PROTEIN; TAP PROTEIN; TRANSCRIPTION EXPORT COMPLEX; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EXON; EXON JUNCTION COMPLEX; FEMALE; GENE EXPRESSION; HUMAN IMMUNODEFICIENCY VIRUS 1; INHIBITION KINETICS; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN RNA BINDING; RNA EXPORT PATHWAY; RNA SPLICING; RNA TRANSCRIPTION; RNA TRANSPORT; VIRAL GENETICS; VIRUS EXPRESSION; XENOPUS;

ANIMALS; DROSOPHILA PROTEINS; FUSHI TARAZU TRANSCRIPTION FACTORS; HIV-1; KARYOPHERINS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; OOCYTES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; REV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; RNA CAP-BINDING PROTEINS; RNA SPLICING; RNA TRANSPORT; RNA, VIRAL; RNA-BINDING PROTEINS; XENOPUS;

EID: 84903128169     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku304     Document Type: Article

References (65)

1. Cullen, B.R. (2003) Nuclear mRNA export: insights from virology. Trends Biochem. Sci., 28, 419-424.
2. Kohler, A. and Hurt, E. (2007) Exporting RNA from the nucleus to the cytoplasm. Nat. Rev. Mol. Cell Biol., 8, 761-773.
3. Strasser, K., Masuda, S., Mason, P., Pfannstiel, J., Oppizzi, M., Rodriguez-Navarro, S., Rondon, A.G., Aguilera, A., Struhl, K., Reed, R. et al. (2002) TREX is a conserved complex coupling transcription with messenger RNA export. Nature, 417, 304-308.
4. Cheng, H., Dufu, K., Lee, C.S., Hsu, J.L., Dias, A. and Reed, R. (2006) Human mRNA export machinery recruited to the 5′ end of mRNA. Cell, 127, 1389-1400.
5. Nojima, T., Hirose, T., Kimura, H. and Hagiwara, M. (2007) The interaction between cap-binding complex and RNA export factor is required for intronless mRNA export. J. Biol. Chem., 282, 15645-15651.
6. Gruter, P., Tabernero, C., von Kobbe, C., Schmitt, C., Saavedra, C., Bachi, A., Wilm, M., Felber, B.K. and Izaurralde, E. (1998) TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol. Cell, 1, 649-659.
7. Katahira, J., Strasser, K., Podtelejnikov, A., Mann, M., Jung, J.U. and Hurt, E. (1999) The Mex67p-mediated nuclear mRNA export pathway is conserved from yeast to human. EMBO J., 18, 2593-2609.
8. Santos-Rosa, H., Moreno, H., Simos, G., Segref, A., Fahrenkrog, B., Pante, N. and Hurt, E. (1998) Nuclear mRNA export requires complex formation between Mex67p and Mtr2p at the nuclear pores. Mol. Cell. Biol., 18, 6826-6838.
9. Segref, A., Sharma, K., Doye, V., Hellwig, A., Huber, J., Luhrmann, R. and Hurt, E. (1997) Mex67p, a novel factor for nuclear mRNA export, binds to both poly(A)+ RNA and nuclear pores. EMBO J., 16, 3256-3271.
10. Rodrigues, J.P., Rode, M., Gatfield, D., Blencowe, B.J., Carmo-Fonseca, M. and Izaurralde, E. (2001) REF proteins mediate the export of spliced and unspliced mRNAs from the nucleus. Proc. Natl. Acad. Sci. U.S.A., 98, 1030-1035.
11. Strasser, K. and Hurt, E. (2000) Yra1p, a conserved nuclear RNA-binding protein, interacts directly with Mex67p and is required for mRNA export. EMBO J., 19, 410-420.
12. Stutz, F., Bachi, A., Doerks, T., Braun, I.C., Seraphin, B., Wilm, M., Bork, P. and Izaurralde, E. (2000) REF, an evolutionary conserved family of hnRNP-like proteins, interacts with TAP/Mex67p and participates in mRNA nuclear export. RNA, 6, 638-650.
13. Jensen, T.H., Dower, K., Libri, D. and Rosbash, M. (2003) Early formation of mRNP: license for export or quality control? Mol. Cell, 11, 1129-1138.
14. Sommer, P. and Nehrbass, U. (2005) Quality control of messenger ribonucleoprotein particles in the nucleus and at the pore. Curr. Opin. Cell Biol., 17, 294-301.
15. Kjems, J. and Askjaer, P. (2000) Rev protein and its cellular partners. Adv. Pharmacol., 48, 251-298.
16. Pollard, V.W. and Malim, M.H. (1998) The HIV-1 Rev protein. Annu. Rev. Microbiol., 52, 491-532.
17. Arnold, M., Nath, A., Hauber, J. and Kehlenbach, R.H. (2006) Multiple importins function as nuclear transport receptors for the Rev protein of human immunodeficiency virus type 1. J. Biol. Chem., 281, 20883-20890.
18. Henderson, B.R. and Percipalle, P. (1997) Interactions between HIV Rev and nuclear import and export factors: the Rev nuclear localisation signal mediates specific binding to human importin-beta. J. Mol. Biol., 274, 693-707.
19. Fischer, U., Huber, J., Boelens, W.C., Mattaj, I.W. and Luhrmann, R. (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.
20. Fornerod, M., Ohno, M., Yoshida, M. and Mattaj, I.W. (1997) CRM1 is an export receptor for leucine-rich nuclear export signals. Cell, 90, 1051-1060.
21. Fukuda, M., Asano, S., Nakamura, T., Adachi, M., Yoshida, M., Yanagida, M. and Nishida, E. (1997) CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature, 390, 308-311.
22. Ossareh-Nazari, B., Bachelerie, F. and Dargemont, C. (1997) Evidence for a role of CRM1 in signal-mediated nuclear protein export. Science, 278, 141-144.
23. Stade, K., Ford, C.S., Guthrie, C. and Weis, K. (1997) Exportin 1 (Crm1p) is an essential nuclear export factor. Cell, 90, 1041-1050.
24. Coyle, J.H., Bor, Y.C., Rekosh, D. and Hammarskjold, M.L. (2011) The Tpr protein regulates export of mRNAs with retained introns that traffic through the Nxf1 pathway. RNA, 17, 1344-1356.
25. Jin, L., Guzik, B.W., Bor, Y.C., Rekosh, D. and Hammarskjold, M.L. (2003) Tap and NXT promote translation of unspliced mRNA. Genes Dev., 17, 3075-3086.
26. Kuersten, S., Segal, S.P., Verheyden, J., LaMartina, S.M. and Goodwin, E.B. (2004) NXF-2, REF-1, and REF-2 affect the choice of nuclear export pathway for tra-2 mRNA in C. elegans. Mol. Cell, 14, 599-610.
27. McCloskey, A., Taniguchi, I., Shinmyozu, K. and Ohno, M. (2012) hnRNP C tetramer measures RNA length to classify RNA polymerase II transcripts for export. Science, 335, 1643-1646.
28. Nott, A., Le Hir, H. and Moore, M.J. (2004) Splicing enhances translation in mammalian cells: an additional function of the exon junction complex. Genes Dev., 18, 210-222.
29. Ohno, M., Segref, A., Kuersten, S. and Mattaj, I.W. (2002) Identity elements used in export of mRNAs. Mol. Cell, 9, 659-671.
30. Swanson, C.M., Puffer, B.A., Ahmad, K.M., Doms, R.W. and Malim, M.H. (2004) Retroviral mRNA nuclear export elements regulate protein function and virion assembly. EMBO J., 23, 2632-2640.
31. Wiegand, H.L., Lu, S. and Cullen, B.R. (2003) Exon junction complexes mediate the enhancing effect of splicing on mRNA expression. Proc. Natl. Acad. Sci. U.S.A., 100, 11327-11332.
32. Askjaer, P., Jensen, T.H., Nilsson, J., Englmeier, L. and Kjems, J. (1998) The specificity of the CRM1-Rev nuclear export signal interaction is mediated by RanGTP. J. Biol. Chem., 273, 33414-33422.
33. Rio, D.C. (1988) Accurate and efficient pre-mRNA splicing in Drosophila cell-free extracts. Proc. Natl. Acad. Sci. U.S.A., 85, 2904-2908.
34. Fischer, U., Pollard, V.W., Luhrmann, R., Teufel, M., Michael, M.W., Dreyfuss, G. and Malim, M.H. (1999) Rev-mediated nuclear export of RNA is dominant over nuclear retention and is coupled to the Ran-GTPase cycle. Nucleic Acids Res., 27, 4128-4134.
35. Sawa, H., Ohno, M., Sakamoto, H. and Shimura, Y. (1988) Requirement of ATP in the second step of the pre-mRNA splicing reaction. Nucleic Acids Res., 16, 3157-3164.
36. Krainer, A.R., Maniatis, T., Ruskin, B. and Green, M.R. (1984) Normal and mutant human beta-globin pre-mRNAs are faithfully and efficiently spliced in vitro. Cell, 36, 993-1005.
37. Taniguchi, I. and Ohno, M. (2008) ATP-dependent recruitment of export factor Aly/REF onto intronless mRNAs by RNA helicase UAP56. Mol. Cell. Biol., 28, 601-608.
38. Ohno, M., Segref, A., Bachi, A., Wilm, M. and Mattaj, I.W. (2000) PHAX, a mediator of U snRNA nuclear export whose activity is regulated by phosphorylation. Cell, 101, 187-198.
39. Jarmolowski, A., Boelens, W.C., Izaurralde, E. and Mattaj, I.W. (1994) Nuclear export of different classes of RNA is mediated by specific factors. J. Cell Biol., 124, 627-635.
40. Mabuchi, N., Masuyama, K. and Ohno, M. (2008) Immunoprecipitation analysis to study RNA-protein interactions in Xenopus oocytes. Methods Mol. Biol., 488, 257-265.
41. Masuyama, K., Taniguchi, I., Kataoka, N. and Ohno, M. (2004) RNA length defines RNA export pathway. Genes Dev., 18, 2074-2085.
42. Le Hir, H., Izaurralde, E., Maquat, L.E. and Moore, M.J. (2000) The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J., 19, 6860-6869.
43. Huang, Y., Gattoni, R., Stevenin, J. and Steitz, J.A. (2003) SR splicing factors serve as adapter proteins for TAP-dependent mRNA export. Mol. Cell, 11, 837-843.
44. Shimane, K., Kodama, E.N., Nakase, I., Futaki, S., Sakurai, Y., Sakagami, Y., Li, X., Hattori, T., Sarafianos, S.G. and Matsuoka, M. (2010) Rev-derived peptides inhibit HIV-1 replication by antagonism of Rev and a co-receptor, CXCR4. Int. J. Biochem. Cell Biol., 42, 1482-1488.
45. Takemura, R., Takeiwa, T., Taniguchi, I., McCloskey, A. and Ohno, M. (2011) Multiple factors in the early splicing complex are involved in the nuclear retention of pre-mRNAs in mammalian cells. Genes Cells, 16, 1035-1049.
46. Jablonski, J.A. and Caputi, M. (2009) Role of cellular RNA processing factors in human immunodeficiency virus type 1 mRNA metabolism, replication, and infectivity. J. Virol., 83, 981-992.
47. Fischer, U., Meyer, S., Teufel, M., Heckel, C., Luhrmann, R. and Rautmann, G. (1994) Evidence that HIV-1 Rev directly promotes the nuclear export of unspliced RNA. EMBO J., 13, 4105-4112.
48. Stutz, F., Izaurralde, E., Mattaj, I.W. and Rosbash, M. (1996) A role for nucleoporin FG repeat domains in export of human immunodeficiency virus type 1 Rev protein and RNA from the nucleus. Mol. Cell. Biol., 16, 7144-7150.
49. Tokunaga, K., Shibuya, T., Ishihama, Y., Tadakuma, H., Ide, M., Yoshida, M., Funatsu, T., Ohshima, Y. and Tani, T. (2006) Nucleocytoplasmic transport of fluorescent mRNA in living mammalian cells: nuclear mRNA export is coupled to ongoing gene transcription. Genes Cells, 11, 305-317.
50. Pasquinelli, A.E., Ernst, R.K., Lund, E., Grimm, C., Zapp, M.L., Rekosh, D., Hammarskjold, M.L. and Dahlberg, J.E. (1997) The constitutive transport element (CTE) of Mason-Pfizer monkey virus (MPMV) accesses a cellular mRNA export pathway. EMBO J., 16, 7500-7510.
51. Saavedra, C., Felber, B. and Izaurralde, E. (1997) The simian retrovirus-1 constitutive transport element, unlike the HIV-1 RRE, uses factors required for cellular mRNA export. Curr. Biol., 7, 619-628.
52. Emerman, M., Vazeux, R. and Peden, K. (1989) The rev gene product of the human immunodeficiency virus affects envelope-specific RNA localization. Cell, 57, 1155-1165.
53. Malim, M.H., Hauber, J., Le, S.Y., Maizel, J.V. and Cullen, B.R. (1989) The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature, 338, 254-257.
54. Malim, M.H., Bohnlein, S., Hauber, J. and Cullen, B.R. (1989) Functional dissection of the HIV-1 Rev trans-activator-derivation of a trans-dominant repressor of Rev function. Cell, 58, 205-214.
55. Luo, M.L., Zhou, Z., Magni, K., Christoforides, C., Rappsilber, J., Mann, M. and Reed, R. (2001) Pre-mRNA splicing and mRNA export linked by direct interactions between UAP56 and Aly. Nature, 413, 644-647.
56. Strasser, K. and Hurt, E. (2001) Splicing factor Sub2p is required for nuclear mRNA export through its interaction with Yra1p. Nature, 413, 648-652.
57. Kim, V.N., Yong, J., Kataoka, N., Abel, L., Diem, M.D. and Dreyfuss, G. (2001) The Y14 protein communicates to the cytoplasm the position of exon-exon junctions. EMBO J., 20, 2062-2068.
58. Lei, H., Dias, A.P. and Reed, R. (2011) Export and stability of naturally intronless mRNAs require specific coding region sequences and the TREX mRNA export complex. Proc. Natl. Acad. Sci. U.S.A., 108, 17985-17990.
59. Palazzo, A.F., Springer, M., Shibata, Y., Lee, C.S., Dias, A.P. and Rapoport, T.A. (2007) The signal sequence coding region promotes nuclear export of mRNA. PLoS Biol., 5, e322.
60. Kaida, D., Motoyoshi, H., Tashiro, E., Nojima, T., Hagiwara, M., Ishigami, K., Watanabe, H., Kitahara, T., Yoshida, T., Nakajima, H. et al. (2007) Spliceostatin A targets SF3b and inhibits both splicing and nuclear retention of pre-mRNA. Nat. Chem. Biol., 3, 576-583.
61. Gallie, D.R. (1991) The cap and poly(a) tail function synergistically to regulate messenger-RNA translational efficiency. Gene Dev., 5, 2108-2116.
62. Hakata, Y., Yamada, M., Mabuchi, N. and Shida, H. (2002) The carboxy-terminal region of the human immunodeficiency virus type 1 protein Rev has multiple roles in mediating CRM1-related Rev functions. J. Virol., 76, 8079-8089.
63. Yedavalli, V.S.R.K., Neuveut, C., Chi, Y.H., Kleiman, L. and Jeang, K.T. (2004) Requirement of DDX3 DEAD box RNA helicase for HIV-1 Rev-RRE export function. Cell, 119, 381-392.
64. Masuyama, K., Taniguchi, I., Kataoka, N. and Ohno, M. (2004) SR proteins preferentially associate with mRNAs in the nucleus and facilitate their export to the cytoplasm. Genes Cells, 9, 959-965.
65. Schumann, S., Jackson, B.R., Baquero-Perez, B. and Whitehouse, A. (2013) Kaposi's sarcoma-associated herpesvirus ORF57 protein: exploiting all stages of viral mRNA processing. Viruses, 5, 1901-1923. Technology