Efficient NES-dependent protein nuclear export requires ongoing synthesis and export of mRNAs

Experimental Cell Research

Volumn 297, Issue 2, 2004, Pages 548-559

  O'Hagan, Heather M ^a,b   Ljungman, Mats ^a,b,c  

^a UNIVERSITY OF MICHIGAN COMPREHENSIVE CANCER CENTER   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

CRM1; mRNA nuclear export; NES GFP reporter protein; Nuclear microinjection; NUP160; Protein nuclear export; TAP; Transcription

Indexed keywords

MESSENGER RNA; RIBONUCLEASE; RNA;

ARTICLE; CONTROLLED STUDY; FIBROBLAST; FLUORESCENCE ANALYSIS; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MICROINJECTION; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN NUCLEIC ACID INTERACTION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REPORTER GENE; SCORING SYSTEM; SIGNAL TRANSDUCTION; STATISTICAL SIGNIFICANCE; TECHNIQUE;

NES;

EID: 2942744364     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2004.03.051     Document Type: Article

References (82)

1. Gorlich D., Kutay U. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol. 15:1999;607-660
2. Nakielny S., Dreyfuss G. Transport of proteins and RNAs in and out of the nucleus. Cell. 99:1999;677-690
3. Ohno M., Fornerod M., Mattaj I.W. Nucleocytoplasmic transport: the last 200 nanometers. Cell. 92:1998;327-336
4. Fischer U., Huber J., Boelens W.C., Mattaj I.W., Luhrmann R. The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell. 82:1995;475-483
5. Fornerod M., Ohno M., Yoshida M., Mattaj I.W. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell. 90:1997;1051-1060
6. Kudo N., Khochbin S., Nishi K., Kitano K., Yanagida M., Yoshida M., Horinouchi S. Molecular cloning and cell cycle-dependent expression of mammalian CRM1, a protein involved in nuclear export of proteins. J. Biol. Chem. 272:1997;29742-29751
7. Mattaj I.W., Englmeier L. Nucleocytoplasmic transport: the soluble phase. Annu. Rev. Biochem. 67:1998;265-306
8. Stade K., Ford C.S., Guthrie C., Weis K. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell. 90:1997;1041-1050
9. Izaurralde E., Kutay U., von Kobbe C., Mattaj I.W., Gorlich D. The asymmetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus. EMBO J. 16:1997;6535-6547
10. Quimby B.B., Corbett A.H. Nuclear transport mechanisms. Cell. Mol. Life Sci. 58:2001;1766-1773
11. Weis K. Nucleocytoplasmic transport: cargo trafficking across the border. Curr. Opin. Cell Biol. 14:2002;328-335
12. Yang J., Bogerd H.P., Wang P.J., Page D.C., Cullen B.R. Two closely related human nuclear export factors utilize entirely distinct export pathways. Mol. Cell. 8:2001;397-406
13. Brennan C.M., Gallouzi I.E., Steitz J.A. Protein ligands to HuR modulate its interaction with target mRNAs in vivo. J. Cell Biol. 151:2000;1-14
14. Zenklusen D., Stutz F. Nuclear export of mRNA. FEBS Lett. 498:2001;150-156
15. Johnson A.W., Lund E., Dahlberg J. Nuclear export of ribosomal subunits. Trends Biochem. Sci. 27:2002;580-585
16. Cullen B.R. Nuclear mRNA export: insights from virology. Trends Biochem. Sci. 28:2003;419-424
17. Clouse K.N., Luo M.J., Zhou Z., Reed R. A Ran-independent pathway for export of spliced mRNA. Nat. Cell Biol. 3:2001;97-99
18. Reed R., Hurt E. A conserved mRNA export machinery coupled to pre-mRNA splicing. Cell. 108:2002;523-531
19. Luo M.J., Reed R. Splicing is required for rapid and efficient mRNA export in metazoans. Proc. Natl. Acad. Sci. U. S. A. 96:1999;14937-14942
20. Brodsky A.S., Silver P.A. Pre-mRNA processing factors are required for nuclear export. RNA. 6:2000;1737-1749
21. Le Hir H., Moore M.J., Maquat L.E. Pre-mRNA splicing alters mRNP composition: evidence for stable association of proteins at exon-exon junctions. Genes Dev. 14:2000;1098-1108
22. Strasser K., Hurt E. Yra1p, a conserved nuclear RNA-binding protein, interacts directly with Mex67p and is required for mRNA export. EMBO J. 19:2000;410-420
23. Zenklusen D., Vinciguerra P., Wyss J.C., Stutz F. Stable mRNP formation and export require cotranscriptional recruitment of the mRNA export factors Yra1p and Sub2p by Hpr1p. Mol. Cell. Biol. 22:2002;8241-8253
24. Hammell C.M., Gross S., Zenklusen D., Heath C.V., Stutz F., Moore C., Cole C.N. Coupling of termination, 3′ processing, and mRNA export. Mol. Cell. Biol. 22:2002;6441-6457
25. Maniatis T., Reed R. An extensive network of coupling among gene expression machines. Nature. 416:2002;499-506
26. Zhou Z., Luo M.J., Straesser K., Katahira J., Hurt E., Reed R. The protein Aly links pre-messenger-RNA splicing to nuclear export in metazoans. Nature. 407:2000;401-405
27. Luo M.L., Zhou Z., Magni K., Christoforides C., Rappsilber J., Mann M., Reed R. Pre-mRNA splicing and mRNA export linked by direct interactions between UAP56 and Aly. Nature. 413:2001;644-647
28. Rodrigues J.P., Rode M., Gatfield D., Blencowe B.J., Carmo-Fonseca M., Izaurralde E. REF proteins mediate the export of spliced and unspliced mRNAs from the nucleus. Proc. Natl. Acad. Sci. U. S. A. 98:2001;1030-1035
29. Gatfield D., Izaurralde E. REF1/Aly and the additional exon junction complex proteins are dispensable for nuclear mRNA export. J. Cell Biol. 159:2002;579-588
30. Ohno M., Segref A., Kuersten S., Mattaj I.W. Identity elements used in export of mRNAs. Mol. Cell. 9:2002;659-671
31. Caceres J.F., Screaton G.R., Krainer A.R. A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev. 12:1998;55-66
32. Gallouzi I.E., Steitz J.A. Delineation of mRNA export pathways by the use of cell-permeable peptides. Science. 294:2001;1895-1901
33. Huang Y., Gattoni R., Stevenin J., Steitz J.A. SR splicing factors serve as adapter proteins for TAP-dependent mRNA export. Mol. Cell. 11:2003;837-843
34. Michael W.M., Eder P.S., Dreyfuss G. The K nuclear shuttling domain: a novel signal for nuclear import and nuclear export in the hnRNP K protein. EMBO J. 16:1997;3587-3598
35. Black B.E., Holaska J.M., Levesque L., Ossareh-Nazari B., Gwizdek C., Dargemont C., Paschal B.M. NXT1 is necessary for the terminal step of Crm1-mediated nuclear export. J. Cell Biol. 152:2001;141-155
36. Englmeier L., Olivo J.C., Mattaj I.W. Receptor-mediated substrate translocation through the nuclear pore complex without nucleotide triphosphate hydrolysis. Curr. Biol. 9:1999;30-41
37. Kehlenbach R.H., Dickmanns A., Gerace L. Nucleocytoplasmic shuttling factors including Ran and CRM1 mediate nuclear export of NFAT in vitro. J. Cell Biol. 141:1998;863-874
38. Siebrasse J.P., Coutavas E., Peters R. Reconstitution of nuclear protein export in isolated nuclear envelopes. J. Cell Biol. 158:2002;849-854
39. Calado A., Treichel N., Muller E.C., Otto A., Kutay U. Exportin-5-mediated nuclear export of eukaryotic elongation factor 1A and tRNA. EMBO J. 21:2002;6216-6224
40. Bohnsack M.T., Regener K., Schwappach B., Saffrich R., Paraskeva E., Hartmann E., Gorlich D. Exp5 exports eEF1A via tRNA from nuclei and synergizes with other transport pathways to confine translation to the cytoplasm. EMBO J. 21:2002;6205-6215
41. Rosorius O., Heger P., Stelz G., Hirschmann N., Hauber J., Stauber R.H. Direct observation of nucleocytoplasmic transport by microinjection of GFP-tagged proteins in living cells. BioTechniques. 27:1999;350-355
42. Vasu S., Shah S., Orjalo A., Park M., Fischer W.H., Forbes D.J. Novel vertebrate nucleoporins Nup133 and Nup160 play a role in mRNA export. J. Cell Biol. 155:2001;339-354
43. Kudo N., Matsumori N., Taoka H., Fujiwara D., Schreiner E.P., Wolff B., Yoshida M., Horinouchi S. Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc. Natl. Acad. Sci. U. S. A. 96:1999;9112-9117
44. Kudo N., Wolff B., Sekimoto T., Schreiner E.P., Yoneda Y., Yanagida M., Horinouchi S., Yoshida M. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp. Cell Res. 242:1998;540-547
45. Sauerbier W., Hercules K. Gene and transcription mapping by radiation effects. Annu. Rev. Genet. 12:1978;329-363
46. Selby C., Sancar A. Transcription preferentially inhibits nucleotide excision repair of the template DNA strand in vitro. J. Biol. Chem. 265:1990;21330-21336
47. Donahue B.A., Yin S., Taylor J.S., Reines D., Hanawalt P.C. Transcript cleavage by RNA polymerase II arrested by a cyclobutane pyrimidine dimer in the DNA template. Proc. Natl. Acad. Sci. U. S. A. 91:1994;8502-8506
48. Sobell H. Actinomycin and DNA transcription. Proc. Natl. Acad. Sci. U. S. A. 82:1985;5328-5331
49. Dubois M.F., Nguyen V.T., Bellier S., Bensaude O. Inhibitors of transcription such as 5, 6-dichloro-1-beta-D- ribofuranosylbenzimidazole and isoquinoline sulfonamide derivatives (H-8 and H-7*) promote dephosphorylation of the carboxyl-terminal domain of RNA polymerase II largest subunit. J. Biol. Chem. 269:1994;13331-13336
50. Ljungman M., Zhang F.F., Chen F., Rainbow A.J., McKay B.C. Inhibition of RNA polymerase II as a trigger for the p53 response. Oncogene. 18:1999;583-592
51. Schlegel R.A., Miller L.S., Rose K.M. Reduction in RNA synthesis following red cell-mediated microinjection of antibodies to RNA polymerase I. Cell Biol. Int. Rep. 9:1985;341-350
52. Scheer U. Injection of antibodies into the nucleus of amphibian oocytes: an experimental means of interfering with gene expression in the living cell. J. Embryol. Exp. Morphol. 97:1986;223-242
53. Stutz F., Bachi A., Doerks T., Braun I.C., Seraphin B., Wilm M., Bork P., Izaurralde E. REF, an evolutionary conserved family of hnRNP-like proteins, interacts with TAP/Mex67p and participates in mRNA nuclear export. RNA. 6:2000;638-650
54. Kang Y., Cullen B.R. The human Tap protein is a nuclear mRNA export factor that contains novel RNA-binding and nucleocytoplasmic transport sequences. Genes Dev. 13:1999;1126-1139
55. Katahira J., Strasser K., Podtelejnikov A., Mann M., Jung J.U., Hurt E. The Mex67p-mediated nuclear mRNA export pathway is conserved from yeast to human. EMBO J. 18:1999;2593-2609
56. Gruter P., Tabernero C., von Kobbe C., Schmitt C., Saavedra C., Bachi A., Wilm M., Felber B.K., Izaurralde E. TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol. Cell. 1:1998;649-659
57. Pasquinelli A.E., Ernst R.K., Lund E., Grimm C., Zapp M.L., Rekosh D., Hammarskjold M.L., Dahlberg J.E. The constitutive transport element (CTE) of Mason-Pfizer monkey virus (MPMV) accesses a cellular mRNA export pathway. EMBO J. 16:1997;7500-7510
58. Saavedra C., Felber B., Izaurralde E. The simian retrovirus-1 constitutive transport element, unlike the HIV-1 RRE, uses factors required for cellular mRNA export. Curr. Biol. 7:1997;619-628
59. Vasu S.K., Forbes D.J. Nuclear pores and nuclear assembly. Curr. Opin. Cell Biol. 13:2001;363-375
60. Pinol-Roma S., Dreyfuss G. Transcription-dependent and transcription-independent nuclear transport of hnRNP proteins. Science. 253:1991;312-314
61. Meyer B.E., Malim M.H. The HIV-1 Rev trans-activator shuttles between the nucleus and the cytoplasm. Genes Dev. 8:1994;1538-1547
62. Kamath R.V., Leary D.J., Huang S. Nucleocytoplasmic shuttling of polypyrimidine tract-binding protein is uncoupled from RNA export. Mol. Biol. Cell. 12:2001;3808-3820
63. Kawamura H., Tomozoe Y., Akagi T., Kamei D., Ochiai M., Yamada M. Identification of the nucleocytoplasmic shuttling sequence of heterogeneous nuclear ribonucleoprotein D-like protein JKTBP and its interaction with mRNA. J. Biol. Chem. 277:2002;2732-2739
64. Michael W.M., Choi M., Dreyfuss G. A nuclear export signal in hnRNP A1: a signal-mediated, temperature-dependent nuclear protein export pathway. Cell. 83:1995;415-422
65. Weighardt F., Biamonti G., Riva S. Nucleo-cytoplasmic distribution of human hnRNP proteins: a search for the targeting domains in hnRNP A1. J. Cell Sci. 108:1995;545-555
66. Hamilton B.J., Burns C.M., Nichols R.C., Rigby W.F. Modulation of AUUUA response element binding by heterogeneous nuclear ribonucleoprotein A1 in human T lymphocytes. The roles of cytoplasmic location, transcription, and phosphorylation. J. Biol. Chem. 272:1997;28732-28741
67. Vautier D., Chesne P., Cunha C., Calado A., Renard J.P., Carmo-Fonseca M. Transcription-dependent nucleocytoplasmic distribution of hnRNP A1 protein in early mouse embryos. J. Cell Sci. 114:2001;1521-1531
68. Pollard V.W., Michael W.M., Nakielny S., Siomi M.C., Wang F., Dreyfuss G. A novel receptor-mediated nuclear protein import pathway. Cell. 86:1996;985-994
69. Siomi M.C., Eder P.S., Kataoka N., Wan L., Liu Q., Dreyfuss G. Transportin-mediated nuclear import of heterogeneous nuclear RNP proteins. J. Cell Biol. 138:1997;1181-1192
70. Stauber R.H., Kratzer F., Schneider G., Hirschmann N., Hauber J., Rosorius O. Investigation of nucleo-cytoplasmic transport using UV-guided microinjection. J. Cell. Biochem. 80:2001;388-396
71. Henderson B.R., Percipalle P. 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. 274:1997;693-707
72. Truant R., Cullen B.R. The arginine-rich domains present in human immunodeficiency virus type 1 Tat and Rev function as direct importin beta-dependent nuclear localization signals. Mol. Cell. Biol. 19:1999;1210-1217
73. Gerber D.A., Souquere-Besse S., Puvion F., Dubois M.F., Bensaude O., Cochet C. Heat-induced relocalization of protein kinase CK2. Implication of CK2 in the context of cellular stress. J. Biol. Chem. 275:2000;23919-23926
74. Lee S., Neumann M., Stearman R., Stauber R., Pause A., Pavlakis G.N., Klausner R.D. Transcription-dependent nuclear-cytoplasmic trafficking is required for the function of the von Hippel-Lindau tumor suppressor protein. Mol. Cell. Biol. 19:1999;1486-1497
75. Groulx I., Lee S. Oxygen-dependent ubiquitination and degradation of hypoxia-inducible factor requires nuclear-cytoplasmic trafficking of the von Hippel-Lindau tumor suppressor protein. Mol. Cell. Biol. 22:2002;5319-5336
76. Brokstad K.A., Kalland K.H., Russell W.C., Matthews D.A. Mitochondrial protein p32 can accumulate in the nucleus. Biochem. Biophys. Res. Commun. 281:2001;1161-1169
77. Ljungman M., O'Hagan H.M., Paulsen M.T. Induction of ser15 and lys382 modifications of p53 by blockage of transcription elongation. Oncogene. 20:2001;5964-5971
78. Ljungman M., Zhang F. Blockage of RNA polymerase as a possible trigger for uv light-induced apoptosis. Oncogene. 13:1996;823-831
79. Koumenis C., Giaccia A. Transformed cells require continuous activity of RNA polymerase II to resist oncogene-induced apoptosis. Mol. Cell. Biol. 17:1997;7306-7316
80. Porter L.A., Cukier I.H., Lee J.M. Nuclear localization of cyclin B1 regulates DNA damage-induced apoptosis. Blood. 101:2003;1928-1933
81. Aoyama T., Takemura G., Maruyama R., Kosai K., Takahashi T., Koda M., Hayakawa K., Kawase Y., Minatoguchi S., Fujiwara H. Molecular mechanisms of non-apoptosis by Fas stimulation alone versus apoptosis with an additional actinomycin D in cultured cardiomyocytes. Cardiovasc. Res. 55:2002;787-798
82. Ng C.P., Zisman A., Bonavida B. Synergy is achieved by complementation with Apo2L/TRAIL and actinomycin D in Apo2L/TRAIL-mediated apoptosis of prostate cancer cells: role of XIAP in resistance. Prostate. 53:2002;286-299