A role for TREX components in the release of spliced mRNA from nuclear speckle domains

Nature Communications

Volumn 1, Issue 7, 2010, Pages

  Dias, Anusha P ^a   Dufu, Kobina ^a   Lei, Haixin ^a   Reed, Robin ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLOBIN; COMPLEMENTARY DNA; DNA; MESSENGER RNA; RNA; VIRUS DNA; BAT1 PROTEIN, HUMAN; DEAD BOX PROTEIN; NUCLEAR PROTEIN; RNA BINDING PROTEIN; RNA PRECURSOR; THOC4 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ALY GENE; ARTICLE; CELL NUCLEUS; CYTOMEGALOVIRUS; CYTOPLASM; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; INFRARED SPECTROSCOPY; MICROINJECTION; PROTEIN FUNCTION; TREX GENE; UAO56 GENE; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; HELA CELL; RNA INTERFERENCE; RNA SPLICING;

DEAD-BOX RNA HELICASES; HELA CELLS; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; NUCLEAR PROTEINS; RNA INTERFERENCE; RNA PRECURSORS; RNA SPLICING; RNA, MESSENGER; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS;

EID: 84880317039     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms1103     Document Type: Article

References (58)

1. Maniatis, T. &Reed, R. An extensive network of coupling among gene expression machines. Nature 416, 499-506 (2002). (Pubitemid 34288845)
2. Reed, R. Coupling transcription, splicing and mRNA export. Curr. Opin. Cell Biol. 15, 326-331 (2003). (Pubitemid 36638651)
3. Pandit, S., Wang, D. &Fu, X.D. Functional integration of transcriptional and RNA processing machineries. Curr. Opin. Cell Biol. 20, 260-265 (2008).
4. Zhong, X.Y., Wang, P., Han, J., Rosenfeld, M.G. &Fu, X.D. SR proteins in vertical integration of gene expression from transcription to RNA processing to translation. Mol. Cell 35, 1-10 (2009).
5. Hall, L.L., Smith, K.P., Byron, M. &Lawrence, J.B. Molecular anatomy of a speckle. Anat. Rec. A Discov. Mol. Cell Evol. Biol. 288, 664-675 (2006). (Pubitemid 44015467)
6. Lawrence, J.B. &Clemson, C.M. Gene associations: True romance or chance meeting in a nuclear neighborhood? J. Cell Biol. 182, 1035-1038 (2008).
7. Jensen, T.H., Dower, K., Libri, D. &Rosbash, M. Early formation of mRNP: License for export or quality control? Mol. Cell 11, 1129-1138 (2003). (Pubitemid 36645134)
8. Olesen, J.R., Libri, D. &Jensen, T.H. A link between transcription and mRNP quality in Saccharomyces cerevisiae. RNA Biol. 2, 45-48 (2005). (Pubitemid 41359798)
9. Vanacova, S. &Stefl, R. The exosome and RNA quality control in the nucleus. EMBO Rep. 8, 651-657 (2007). (Pubitemid 47033796)
10. Rougemaille, M., Villa, T., Gudipati, R.K. &Libri, D. mRNA journey to the cytoplasm: Attire required. Biol. Cell 100, 327-342 (2008). (Pubitemid 351803963)
11. Xing, Y., Johnson, C.V., Dobner, P.R. &Lawrence, J.B. Higher level organization of individual gene transcription and RNA splicing. Science 259, 1326-1330 (1993). (Pubitemid 23100272)
12. Xing, Y., Johnson, C.V., Moen, P.T. Jr, McNeil, J.A. &Lawrence, J. Nonrandom gene organization: Structural arrangements of specific pre-mRNA transcription and splicing with SC-35 domains.J. Cell Biol. 131, 1635-1647 (1995). (Pubitemid 26007964)
13. Hattinger, C.M., Jochemsen, A.G., Tanke, H.J. &Dirks, R.W. Induction of p21 mRNA synthesis after short-wavelength UV light visualized in individual cells by RNA FISH.J. Histochem. Cytochem. 50, 81-89 (2002). (Pubitemid 34074625)
14. Shopland, L.S., Johnson, C.V. &Lawrence, J.B. Evidence that all SC-35 domains contain mRNAs and that transcripts can be structurally constrained within these domains.J. Struct. Biol. 140, 131-139 (2002). (Pubitemid 36139854)
15. Smith, K.P., Moen, P.T., Wydner, K.L., Coleman, J.R. &Lawrence, J.B. Processing of endogenous pre-mRNAs in association with SC-35 domains is gene specific.J. Cell Biol. 144, 617-629 (1999). (Pubitemid 29234542)
16. Johnson, C. et al. Tracking COL1A1 RNA in osteogenesis imperfecta. Splice-defective transcripts initiate transport from the gene but are retained within the SC35 domain.J. Cell Biol. 150, 417-432 (2000).
17. Melcak, I., Melcakova, S., Kopsky, V., Vecerova, J. &Raska, I. Prespliceosomal assembly on microinjected precursor mRNA takes place in nuclear speckles. Mol. Biol. Cell 12, 393-406 (2001). (Pubitemid 33051583)
18. Tokunaga, K. et al. Nucleocytoplasmic transport of fluorescent mRNA in living mammalian cells: Nuclear mRNA export is coupled to ongoing gene transcription. Genes Cells 11, 305-317 (2006).
19. Ishihama, Y., Tadakuma, H., Tani, T. &Funatsu, T. The dynamics of pre-mRNAs and poly(A)+ RNA at speckles in living cells revealed by iFRAP studies. Exp. Cell Res. 314, 748-762 (2008). (Pubitemid 351191904)
20. Funatsu, T. [Single-molecule imaging and quantification of mRNAs in a living cell]. Yakugaku Zasshi 129, 265-272 (2009).
21. Brown, J.M. et al. Association between active genes occurs at nuclear speckles and is modulated by chromatin environment.J. Cell Biol. 182, 1083-1097 (2008).
22. Hu, Q. et al. Enhancing nuclear receptor-induced transcription requires nuclear motor and LSD1-dependent gene networking in interchromatin granules. Proc. Natl Acad. Sci. USA 105, 19199-19204 (2008).
23. Takizawa, T., Gudla, P.R., Guo, L., Lockett, S. &Misteli, T. Allele-specific nuclear positioning of the monoallelically expressed astrocyte marker GFAP. Genes Dev. 22, 489-498 (2008). (Pubitemid 351272756)
24. Lamond, A.I. &Spector, D.L. Nuclear speckles: A model for nuclear organelles. Nat. Rev. Mol. Cell Biol. 4, 605-612 (2003). (Pubitemid 36934962)
25. Prasanth, K.V. et al. Regulating gene expression through RNA nuclear retention. Cell 123, 249-263 (2005). (Pubitemid 41457215)
26. Pawlicki, J.M. &Steitz, J.A. Primary microRNA transcript retention at sites of transcription leads to enhanced microRNA production.J. Cell Biol. 182, 61-76 (2008). (Pubitemid 352008622)
27. Pawlicki, J.M. &Steitz, J.A. Subnuclear compartmentalization of transiently expressed polyadenylated pri-microRNAs: Processing at transcription sites or accumulation in SC35 foci. Cell Cycle 8, 345-356 (2009).
28. Zhao, R., Bodnar, M.S. &Spector, D.L. Nuclear neighborhoods and gene expression. Curr. Opin. Genet. Dev. 19, 172-179 (2009).
29. Reed, R. &Cheng, H. TREX, SR proteins and export of mRNA. Curr. Opin. Cell Biol. 17, 269-273 (2005). (Pubitemid 40719916)
30. Moore, M.J. &Proudfoot, N.J. Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 136, 688-700 (2009).
31. Reed, R. &Hurt, E. A conserved mRNA export machinery coupled to pre-mRNA splicing. Cell 108, 523-531 (2002). (Pubitemid 34260877)
32. Kohler, A. &Hurt, E. Exporting RNA from the nucleus to the cytoplasm. Nat. Rev. Mol. Cell Biol. 8, 761-773 (2007). (Pubitemid 47462133)
33. Saguez, C., Olesen, J.R. &Jensen, T.H. Formation of export-competent mRNP: Escaping nuclear destruction. Curr. Opin. Cell Biol. 17, 287-293 (2005). (Pubitemid 40719919)
34. Sommer, P. &Nehrbass, U. Quality control of messenger ribonucleoprotein particles in the nucleus and at the pore. Curr. Opin. Cell Biol. 17, 294-301 (2005). (Pubitemid 40719920)
35. Rougemaille, M. et al. THO/Sub2p functions to coordinate 3'-end processing with gene-nuclear pore association. Cell 135, 308-321 (2008).
36. Carmody, S.R. &Wente, S.R. mRNA nuclear export at a glance.J. Cell Sci. 122, 1933-1937 (2009).
37. Zhou, Z. et al. The protein Aly links pre-messenger-RNA splicing to nuclear export in metazoans. Nature 407, 401-405 (2000).
38. Luo, M.J. et al. Pre-mRNA splicing and mRNA export linked by direct interactions between UAP56 and Aly. Nature 413, 644-647 (2001).
39. Masuda, S. et al. Recruitment of the human TREX complex to mRNA during splicing. Genes Dev. 19, 1512-1517 (2005). (Pubitemid 41002995)
40. Cheng, H. et al. Human mRNA export machinery recruited to the 5' end of mRNA. Cell 127, 1389-1400 (2006). (Pubitemid 44960410)
41. Valencia, P., Dias, A.P. &Reed, R. Splicing promotes rapid and efficient mRNA export in mammalian cells. Proc. Natl Acad. Sci. USA 105, 3386-3391 (2008). (Pubitemid 351723562)
42. Luo, M. &Reed, R. Splicing is required for rapid and efficient mRNA export in metazoans. Proc. Natl Acad. Sci. USA 96, 14937-14942 (1999). (Pubitemid 30019743)
43. Misteli, T. Protein dynamics: Implications for nuclear architecture and gene expression. Science 291, 843-847 (2001). (Pubitemid 32120749)
44. Smith, K.P., Byron, M., Johnson, C., Xing, Y. &Lawrence, J.B. Defining early steps in mRNA transport: Mutant mRNA in myotonic dystrophy type I is blocked at entry into SC-35 domains.J. Cell Biol. 178, 951-964 (2007). (Pubitemid 47443319)
45. Lee, C.S. et al. Human DDX3 functions in translation and interacts with the translation initiation factor eIF3. Nucleic Acids Res. 36, 4708-4718 (2008).
46. Kapadia, F., Pryor, A., Chang, T.H. &Johnson, L.F. Nuclear localization of poly(A)+ mRNA following siRNA reduction of expression of the mammalian RNA helicases UAP56 and URH49. Gene 384, 37-44 (2006). (Pubitemid 44738327)
47. Fleckner, J., Zhang, M., Valcarcel, J. &Green, M.R. U2AF65 recruits a novel human DEAD box protein required for the U2 snRNP-branchpoint interaction. Genes Dev. 11, 1864-1872 (1997). (Pubitemid 27315215)
48. Shen, H. et al. Distinct activities of the DExD/H-box splicing factor hUAP56 facilitate stepwise assembly of the spliceosome. Genes Dev. 22, 1796-1803 (2008). (Pubitemid 351915504)
49. Carter, K.C., Taneja, K.L. &Lawrence, J.B. Discrete nuclear domains of poly(A) RNA and their relationship to the functional organization of the nucleus.J. Cell Biol. 115, 1191-1202 (1991). (Pubitemid 21909965)
50. Visa, N., Puvion-Dutilleul, F., Harper, F., Bachellerie, J.P. &Puvion, E. Intranuclear distribution of poly(A) RNA determined by electron microscope in situ hybridization. Exp. Cell Res. 208, 19-34 (1993). (Pubitemid 23274485)
51. Huang, S., Deerinck, T.J., Ellisman, M.H. &Spector, D.L. In vivo analysis of the stability and transport of nuclear poly(A)+ RNA.J. Cell Biol. 126, 877-899 (1994). (Pubitemid 24252136)
52. Melcak, I. et al. Nuclear pre-mRNA compartmentalization: Trafficking of released transcripts to splicing factor reservoirs. Mol. Biol. Cell 11, 497-510 (2000). (Pubitemid 30112160)
53. Molenaar, C., Abdulle, A., Gena, A., Tanke, H.J. &Dirks, R.W. Poly(A)+ RNAs roam the cell nucleus and pass through speckle domains in transcriptionally active and inactive cells.J. Cell Biol. 165, 191-202 (2004). (Pubitemid 38544522)
54. Kotake, Y. et al. Splicing factor SF3b as a target of the antitumor natural product pladienolide. Nat. Chem. Biol. 3, 570-575 (2007). (Pubitemid 47294394)
55. Okada, M., Jang, S.W. &Ye, K. Akt phosphorylation and nuclear phosphoinositide association mediate mRNA export and cell proliferation activities by ALY. Proc. Natl Acad. Sci. USA 105, 8649-8654 (2008). (Pubitemid 351987734)
56. Hautbergue, G.M. et al. UIF, a new mRNA export adaptor that works together with REF/ALY, requires FACT for recruitment to mRNA. Curr. Biol. 19, 1918-1924 (2009).
57. Custodio, N. et al. Inefficient processing impairs release of RNA from the site of transcription. EMBO J. 18, 2855-2866 (1999). (Pubitemid 29233957)
58. Das, R. &Reed, R. Resolution of the mammalian E complex and the ATP-dependent spliceosomal complexes on native agarose mini-gels. RNA 5, 1504-1508 (1999). (Pubitemid 29530495)