Characterization of nuclear localization signals (NLSs) and function of NLSs and phosphorylation of serine residues in subcellular and subnuclear localization of Transformer-2α (Tra2β)

Journal of Biological Chemistry

Volumn 288, Issue 13, 2013, Pages 8898-8909

  Li, Shu Jing ^a   Qi, Yao ^a   Zhao, Jing Jing ^a   Li, Ya ^a   Liu, Xiao Yan ^a   Chen, Xian Hua ^a   Xu, Ping ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASMIC LOCALIZATION; MUTATION ANALYSIS; NUCLEAR LOCALIZATION; NUCLEAR LOCALIZATION SIGNAL; PRE-MRNA SPLICING; SPATIAL ORGANIZATION; SUBCELLULAR DISTRIBUTION; SUBNUCLEAR LOCALIZATION;

AMINO ACIDS; MAMMALS; PHOSPHORYLATION; SOFTWARE TESTING; SPECKLE;

PROTEINS;

SERINE; SERINE ARGININE RICH PROTEIN; TRANSFORMER 2BETA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; GENE DELETION; HUMAN; HUMAN CELL; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR SPECKLE; NUCLEOTIDE SEQUENCE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SERINE ARGININE RICH DOMAIN 1; SERINE ARGININE RICH DOMAIN 2;

ANIMALS; BRAIN; CELL LINE, TUMOR; CELL NUCLEUS; CYTOPLASM; GENE EXPRESSION REGULATION; HUMANS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; NERVE TISSUE PROTEINS; NUCLEAR LOCALIZATION SIGNALS; PHOSPHORYLATION; PLASMIDS; POINT MUTATION; PROTEIN STRUCTURE, TERTIARY; RNA SPLICING; RNA, MESSENGER; RNA-BINDING PROTEINS; SERINE; SUBCELLULAR FRACTIONS;

MAMMALIA;

EID: 84875999513     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.456715     Document Type: Article

References (50)

1. Black, D. L. (2000) Protein diversity from alternative splicing: a challenge for bioinformatics and post-genome biology. Cell 103, 367-370
2. Graveley, B. R. (2001) Alternative splicing: increasing diversity in the proteomic world. Trends Genet. 17, 100-107
3. Faustino, N. A., and Cooper, T. A. (2003) Pre-mRNA splicing and human disease. Genes Dev. 17, 419-437
4. Fu, X. D. (1995) The superfamily of arginine/serine-rich splicing factors. RNA 1, 663-680
5. Manley, J. L., and Tacke, R. (1996) SR proteins and splicing control. Genes Dev. 10, 1569-1579
6. Spector, D. L. (1993) Macromolecular domains within the cell nucleus. Annu. Rev. Cell Biol. 9, 265-315
7. O'Keefe, R. T., Mayeda, A., Sadowski, C. L., Krainer, A. R., and Spector, D. L. (1994) Disruption of pre-mRNA splicing in vivo results in reorganization of splicing factors. J. Cell Biol. 124, 249-260
8. Jiménez-Garcia, L. F., and Spector, D. L. (1993) In vivo evidence that transcription and splicing are coordinated by a recruiting mechanism. Cell 73, 47-59
9. Huang, S., and Spector, D. L. (1996) Intron-dependent recruitment of pre-mRNA splicing factors to sites of transcription. J. Cell Biol. 133, 719-732
10. Misteli, T., and Spector, D. L. (1997) Protein phosphorylation and the nuclear organization of pre-mRNA splicing. Trends Cell Biol. 7, 135-138
11. Cáceres, J. F., Screaton, G. R., and Krainer, A. R. (1998) A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev. 12, 55-66
12. Huang, Y., Gattoni, R., Stévenin, J., and Steitz, J. A. (2003) SR splicing factors serve as adapter proteins for TAP-dependent mRNA export. Mol. Cell 11, 837-843
13. Lemaire, R., Prasad, J., Kashima, T., Gustafson, J., Manley, J. L., and Lafyatis, R. (2002) Stability of a PKCI-1-related mRNA is controlled by the splicing factor ASF/SF2: a novel function for SR proteins. Genes Dev. 16, 594-607
14. Sanford, J. R., Gray, N. K., Beckmann, K., and Cáceres, J. F. (2004) A novel role for shuttling SR proteins in mRNA translation. Genes Dev. 18, 755-768
15. Li, H., and Bingham, P. M. (1991) Arginine/serine-rich domains of the su(wa) and tra RNA processing regulators target proteins to a subnuclear compartment implicated in splicing. Cell 67, 335-342
16. Hedley, M. L., Amrein, H., and Maniatis, T. (1995) An amino acid sequence motif sufficient for subnuclear localization of an arginine/serinerich splicing factor. Proc. Natl. Acad. Sci. U.S.A. 92, 11524-11528
17. Gui, J. F., Lane, W. S., and Fu, X. D. (1994) A serine kinase regulates intracellular localization of splicing factors in the cell cycle. Nature 369, 678-682
18. Colwill, K., Pawson, T., Andrews, B., Prasad, J., Manley, J. L., Bell, J. C., and Duncan, P. I. (1996) The Clk/Sty protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution. EMBO J. 15, 265-275
19. Wang, H. Y., Lin, W., Dyck, J. A., Yeakley, J. M., Songyang, Z., Cantley, L. C., and Fu, X. D. (1998) SRPK2: a differentially expressed SR proteinspecific kinase involved in mediating the interaction and localization of pre-mRNA splicing factors in mammalian cells. J. Cell Biol. 140, 737-750
20. Misteli, T., and Spector, D. L. (1996) Serine/threonine phosphatase 1 modulates the subnuclear distribution of pre-mRNA splicing factors. Mol. Biol. Cell 7, 1559-1572
21. Cáceres, J. F., Misteli, T., Screaton, G. R., Spector, D. L., and Krainer, A. R. (1997) Role of the modular domains of SR proteins in subnuclear localization and alternative splicing specificity. J. Cell Biol. 138, 225-238
22. Beil, B., Screaton, G., and Stamm, S. (1997) Molecular cloning of htra2-β-1 and htra2-β-2, two human homologs of tra-2 generated by alternative splicing. DNA Cell Biol. 16, 679-690
23. Nayler, O., Cap, C., and Stamm, S. (1998) Human transformer-2-β gene (SFRS10): complete nucleotide sequence, chromosomal localization, and generation of a tissue-specific isoform. Genomics 53, 191-202
24. Chen, X., Guo, L., Lin, W., and Xu, P. (2003) Expression of Tra2β isoforms is developmentally regulated in a tissue- and temporal-specific pattern. Cell Biol. Int. 27, 491-496
25. Hofmann, Y., Lorson, C. L., Stamm, S., Androphy, E. J., and Wirth, B. (2000) Htra2-β1 stimulates an exonic splicing enhancer and can restore full-length SMN expression to survival motor neuron 2 (SMN2). Proc. Natl. Acad. Sci. U.S.A. 97, 9618-9623
26. Glatz, D. C., Rujescu, D., Tang, Y., Berendt, F. J., Hartmann, A. M., Faltraco, F., Rosenberg, C., Hulette, C., Jellinger, K., Hampel, H., Riederer, P., Möller, H. J., Andreadis, A., Henkel, K., and Stamm, S. (2006) The alternative splicing of tau exon 10 and its regulatory proteins CLK2 and TRA2-β1 changes in sporadic Alzheimer's disease. J. Neurochem. 96, 635-644
27. D'Souza, I., and Schellenberg, G. D. (2006) Arginine/serine-rich protein interaction domain-dependent modulation of a tau exon 10 splicing enhancer: altered interactions and mechanisms for functionally antagonistic FTDP-17 mutations Δ280K AND N279K. J. Biol. Chem. 281, 2460-2469
28. Jiang, Z., Tang, H., Havlioglu, N., Zhang, X., Stamm, S., Yan, R., and Wu, J. Y. (2003) Mutations in tau gene exon 10 associated with FTDP-17 alter the activity of an exonic splicing enhancer to interact with Tra2β. J. Biol. Chem. 278, 18997-19007
29. Watermann, D. O., Tang, Y., Zur Hausen, A., Jäger, M., Stamm, S., and Stickeler, E. (2006) Splicing factor Tra2-β1 is specifically induced in breast cancer and regulates alternative splicing of the CD44 gene. Cancer Res. 66, 4774-4780
30. Daoud, R., Mies, G., Smialowska, A., Oláh, L., Hossmann, K. A., and Stamm, S. (2002) Ischemia induces a translocation of the splicing factor tra2-β1 and changes alternative splicing patterns in the brain. J. Neurosci. 22, 5889-5899
31. Shukla, S., and Fisher, S. A. (2008) Tra2β as a novel mediator of vascular smooth muscle diversification. Circ. Res. 103, 485-492
32. Han, Y., Chen, X., Shi, F., Li, S., Huang, J., Xie, M., Hu, L., Hoidal, J. R., and Xu, P. (2007) CPG15, a new factor upregulated after ischemic brain injury, contributes to neuronal network re-establishment after glutamate-induced injury. J. Neurotrauma 24, 722-731
33. Segade, F., Hurlé, B., Claudio, E., Ramos, S., and Lazo, P. S. (1996) Molecular cloning of a mouse homologue for the Drosophila splicing regulator Tra2. FEBS Lett. 387, 152-156
34. Kalderon, D., Roberts, B. L., Richardson, W. D., and Smith, A. E. (1984) A short amino acid sequence able to specify nuclear location. Cell 39, 499-509
35. Dingwall, C., Robbins, J., Dilworth, S. M., Roberts, B., and Richardson, W. D. (1988) The nucleoplasmin nuclear location sequence is larger and more complex than that of SV-40 large T antigen. J. Cell Biol. 107, 841-849
36. Zahler, A. M., Lane, W. S., Stolk, J. A., and Roth, M. B. (1992) SR proteins: a conserved family of pre-mRNA splicing factors. Genes Dev. 6, 837-847
37. Daub, H., Olsen, J. V., Bairlein, M., Gnad, F., Oppermann, F. S., Körner, R., Greff, Z., Kéri, G., Stemmann, O., and Mann, M. (2008) Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol. Cell 31, 438-448
38. Dephoure, N., Zhou, C., Villén, J., Beausoleil, S. A., Bakalarski, C. E., Elledge, S. J., and Gygi, S. P. (2008) A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 105, 10762-10767
39. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P., and Mann, M. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648
40. Wang, B., Malik, R., Nigg, E. A., and Körner, R. (2008) Evaluation of the low-specificity protease elastase for large-scale phosphoproteome analysis. Anal. Chem. 80, 9526-9533
41. Rikova, K., Guo, A., Zeng, Q., Possemato, A., Yu, J., Haack, H., Nardone, J., Lee, K., Reeves, C., Li, Y., Hu, Y., Tan, Z., Stokes, M., Sullivan, L., Mitchell, J., Wetzel, R., Macneill, J., Ren, J. M., Yuan, J., Bakalarski, C. E., Villen, J., Kornhauser, J. M., Smith, B., Li, D., Zhou, X., Gygi, S. P., Gu, T. L., Polakiewicz, R. D., Rush, J., and Comb, M. J. (2007) Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 131, 1190-1203
42. van der Houven van Oordt, W., Diaz-Meco, M. T., Lozano, J., Krainer, A. R., Moscat, J., and Cáceres, J. F. (2000) The MKK(3/6)-p38-signaling cascade alters the subcellular distribution of hnRNP A1 and modulates alternative splicing regulation. J. Cell Biol. 149, 307-316
43. Kataoka, N., Bachorik, J. L., and Dreyfuss, G. (1999) Transportin-SR, a nuclear import receptor for SR proteins. J. Cell Biol. 145, 1145-1152
44. Lai, M. C., Lin, R. I., Huang, S. Y., Tsai, C. W., and Tarn, W. Y. (2000) A human importin-beta family protein, transportin-SR2, interacts with the phosphorylated RS domain of SR proteins. J. Biol. Chem. 275, 7950-7957
45. Lai, M. C., Lin, R. I., and Tarn, W. Y. (2001) Transportin-SR2 mediates nuclear import of phosphorylated SR proteins. Proc. Natl. Acad. Sci. U.S.A. 98, 10154-10159
46. Yun, C. Y., Velazquez-Dones, A. L., Lyman, S. K., and Fu, X. D. (2003) Phosphorylation-dependent and -independent nuclear import of RS domain-containing splicing factors and regulators. J. Biol. Chem. 278, 18050-18055
47. Grellscheid, S., Dalgliesh, C., Storbeck, M., Best, A., Liu, Y., Jakubik, M., Mende, Y., Ehrmann, I., Curk, T., Rossbach, K., Bourgeois, C. F., Stévenin, J., Grellscheid, D., Jackson, M. S., Wirth, B., and Elliott, D. J. (2011) Identification of evolutionarily conserved exons as regulated targets for the splicing activator tra2β in development. PLoS Genet. 7, e1002390
48. Daoud, R., Da Penha Berzaghi, M., Siedler, F., Hübener, M., and Stamm, S. (1999) Activity-dependent regulation of alternative splicing patterns in the rat brain. Eur. J. Neurosci. 11, 788-802
49. Mattox, W., Palmer, M. J., and Baker, B. S. (1990) Alternative splicing of the sex determination gene transformer-2 is sex-specific in the germ line but not in the soma. Genes Dev. 4, 789-805
50. Stoilov, P., Daoud, R., Nayler, O., and Stamm, S. (2004) Human tra2-β1 autoregulates its protein concentration by influencing alternative splicing of its pre-mRNA. Hum. Mol. Genet. 13, 509-524