Intra-domain cross-talk regulates serine-arginine protein kinase 1-dependent phosphorylation and splicing function of transformer 2β1

Journal of Biological Chemistry

Volumn 290, Issue 28, 2015, Pages 17269-17281

  Jamros, Michael A ^a   Aubol, Brandon E ^a   Keshwani, Malik M ^a   Zhang, Zhaiyi ^b   Stamm, Stefan ^b   Adams, Joseph A ^a  

^a University of California San Diego   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CROSSTALK; ENZYMES; MASS SPECTROMETRY; NEURONS; PHOSPHORYLATION; PROTEINS; RNA;

KINETIC EXPERIMENT; LIGAND EXCHANGES; NOVEL FUNCTIONS; RNA-RECOGNITION MOTIFS; SPLICE VARIANTS; SPLICING ENHANCER; SPLICING FACTORS; SURVIVAL MOTOR NEURONS;

AMINO ACIDS;

PROTEIN SRPK1; PROTEIN TRA2 BETA1; RNA; SERINE ARGININE RICH PROTEIN; SURVIVAL MOTOR NEURON PROTEIN 2; TRANSFORMING PROTEIN; UNCLASSIFIED DRUG; NERVE PROTEIN; PROTEIN SERINE THREONINE KINASE; RECOMBINANT PROTEIN; RNA BINDING PROTEIN; SERINE; SMN2 PROTEIN, HUMAN; SRPK1 PROTEIN, HUMAN; TRA2B PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; EXON; GENE; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MOLECULAR DOCKING; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; RNA BINDING; RNA SPLICING; SMN2 GENE; BINDING SITE; CHEMISTRY; GENETICS; HEK293 CELL LINE; KINETICS; METABOLISM; PHOSPHORYLATION; SITE DIRECTED MUTAGENESIS;

BINDING SITES; EXONS; HEK293 CELLS; HUMANS; KINETICS; MUTAGENESIS, SITE-DIRECTED; NERVE TISSUE PROTEINS; PHOSPHORYLATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT PROTEINS; RNA; RNA SPLICING; RNA-BINDING PROTEINS; SERINE; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SURVIVAL OF MOTOR NEURON 2 PROTEIN;

EID: 84940094447     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.656579     Document Type: Article

References (52)

1. Kohtz, J. D., Jamison, S. F., Will, C. L., Zuo, P., Lührmann, R., Garcia-Blanco, M. A., and Manley, J. L. (1994) Protein-protein interactions and 5″-splice-site recognition in mammalian mRNA precursors. Nature 368, 119-124
2. Wu, J. Y., and Maniatis, T. (1993) Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell 75, 1061-1070
3. Roscigno, R. F., and Garcia-Blanco, M. A. (1995) SR proteins escort the U4/U6.U5 tri-snRNP to the spliceosome. RNA 1, 692-706
4. Mermoud, J. E., Cohen, P. T., and Lamond, A. I. (1994) Regulation of mammalian spliceosome assembly by a protein phosphorylation mechanism. EMBO J. 13, 5679-5688
5. Haynes, C., and Iakoucheva, L. M. (2006) Serine/arginine-rich splicing factors belong to a class of intrinsically disordered proteins. Nucleic Acids Res. 34, 305-312
6. Xiang, S., Gapsys, V., Kim, H. Y., Bessonov, S., Hsiao, H. H., Möhlmann, S., Klaukien, V., Ficner, R., Becker, S., Urlaub, H., Lührmann, R., de Groot, B., and Zweckstetter, M. (2013) Phosphorylation drives a dynamic switch in serine/arginine-rich proteins. Structure 21, 2162-2174
7. Cho, S., Hoang, A., Sinha, R., Zhong, X. Y., Fu, X. D., Krainer, A. R., and Ghosh, G. (2011) Interaction between the RNA binding domains of Ser-Arg splicing factor 1 and U1-70K snRNP protein determines early spliceosome assembly. Proc. Natl. Acad. Sci. U.S.A. 108, 8233-8238
8. Keshwani, M. M., Aubol, B. E., Fattet, L., Ma, C. T., Qiu, J., Jennings, P. A., Fu, X. D., and Adams, J. A. (2015) Conserved proline-directed phosphorylation regulates SR protein conformation and splicing function. Biochem. J. 466, 311-322
9. Zhou, Z., Qiu, J., Liu, W., Zhou, Y., Plocinik, R. M., Li, H., Hu, Q., Ghosh, G., Adams, J. A., Rosenfeld, M. G., and Fu, X. D. (2012) The Akt-SRPK-SR axis constitutes a major pathway in transducing EGF signaling to regulate alternative splicing in the nucleus. Mol. Cell 47, 422-433
10. Sumanasekera, C., Kelemen, O., Beullens, M., Aubol, B. E., Adams, J. A., Sunkara, M., Morris, A., Bollen, M., Andreadis, A., and Stamm, S. (2012) C6 pyridinium ceramide influences alternative pre-mRNA splicing by inhibiting protein phosphatase-1. Nucleic Acids Res. 40, 4025-4039
11. Chalfant, C. E., Rathman, K., Pinkerman, R. L., Wood, R. E., Obeid, L. M., Ogretmen, B., and Hannun, Y. A. (2002) De novo ceramide regulates the alternative splicing of caspase 9 and Bcl-x in A549 lung adenocarcinoma cells. Dependence on protein phosphatase-1. J. Biol. Chem. 277, 12587-12595
12. 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
13. 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 τ exon 10 and its regulatory proteins CLK2 and TRA2-β1 changes in sporadic Alzheimer's disease. J. Neurochem. 96, 635-644
14. Ma, C. T., Velazquez-Dones, A., Hagopian, J. C., Ghosh, G., Fu, X. D., and Adams, J. A. (2008) Ordered multi-site phosphorylation of the splicing factor ASF/SF2 by SRPK1. J. Mol. Biol. 376, 55-68
15. Ma, C. T., Hagopian, J. C., Ghosh, G., Fu, X. D., and Adams, J. A. (2009) Regiospecific phosphorylation control of the SR protein ASF/SF2 by SRPK1. J. Mol. Biol. 390, 618-634
16. Ngo, J. C., Giang, K., Chakrabarti, S., Ma, C. T., Huynh, N., Hagopian, J. C., Dorrestein, P. C., Fu, X. D., Adams, J. A., and Ghosh, G. (2008) A sliding docking interaction is essential for sequential and processive phosphorylation of an SR protein by SRPK1. Mol. Cell 29, 563-576
17. Ngo, J. C., Chakrabarti, S., Ding, J. H., Velazquez-Dones, A., Nolen, B., Aubol, B. E., Adams, J. A., Fu, X. D., and Ghosh, G. (2005) Interplay between SRPK and Clk/Sty kinases in phosphorylation of the splicing factor ASF/SF2 is regulated by a docking motif in ASF/SF2. Mol. Cell 20, 77-89
18. 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
19. Stojdl, D. F., and Bell, J. C. (1999) SR protein kinases: the splice of life. Biochem. Cell Biol. 77, 293-298
20. Tacke, R., Tohyama, M., Ogawa, S., and Manley, J. L. (1998) Human Tra2 proteins are sequence-specific activators of pre-mRNA splicing. Cell 93, 139-148
21. Cowper, A. E., Cáceres, J. F., Mayeda, A., and Screaton, G. R. (2001) Serine-arginine (SR) protein-like factors that antagonize authentic SR proteins and regulate alternative splicing. J. Biol. Chem. 276, 48908-48914
22. Hoshijima, K., Inoue, K., Higuchi, I., Sakamoto, H., and Shimura, Y. (1991) Control of doublesex alternative splicing by transformer and transformer-2 in Drosophila. Science 252, 833-836
23. Lynch, K. W., and Maniatis, T. (1995) Synergistic interactions between two distinct elements of a regulated splicing enhancer. Genes Dev. 9, 284-293
24. Singh, N. N., Androphy, E. J., and Singh, R. N. (2004) The regulation and regulatory activities of alternative splicing of the SMN gene. Crit. Rev. Eukaryot. Gene Expr. 14, 271-285
25. Jiang, Z., Tang, H., Havlioglu, N., Zhang, X., Stamm, S., Yan, R., and Wu, J. Y. (2003) Mutations in τ 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
26. Ward, A. J., and Cooper, T. A. (2010) The pathobiology of splicing. J. Pathol. 220, 152-163
27. Lorson, C. L., Hahnen, E., Androphy, E. J., and Wirth, B. (1999) A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy. Proc. Natl. Acad. Sci. U.S.A. 96, 6307-6311
28. 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
29. 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
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. Li, S. J., Qi, Y., Zhao, J. J., Li, Y., Liu, X. Y., Chen, X. H., and Xu, P. (2013) Characterization of nuclear localization signals (NLSs) and function of NLSs and phosphorylation of serine residues in subcellular and subnuclear localization of transformer-2β (Tra2β). J. Biol. Chem. 288, 8898-8909
32. 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
33. Hagopian, J. C., Ma, C. T., Meade, B. R., Albuquerque, C. P., Ngo, J. C., Ghosh, G., Jennings, P. A., Fu, X. D., and Adams, J. A. (2008) Adaptable molecular interactions guide phosphorylation of the SR protein ASF/SF2 by SRPK1. J. Mol. Biol. 382, 894-909
34. Aubol, B. E., Jamros, M. A., McGlone, M. L., and Adams, J. A. (2013) Splicing kinase SRPK1 conforms to the landscape of its SR protein substrate. Biochemistry 52, 7595-7605
35. Stoss, O., Stoilov, P., Hartmann, A. M., Nayler, O., and Stamm, S. (1999) The in vivo minigene approach to analyze tissue-specific splicing. Brain Res. Brain Res. Protoc. 4, 383-394
36. Aubol, B. E., Plocinik, R. M., Keshwani, M. M., McGlone, M. L., Hagopian, J. C., Ghosh, G., Fu, X. D., and Adams, J. A. (2014) N terminus of the protein kinase CLK1 induces SR protein hyperphosphorylation. Biochem. J. 462, 143-152
37. Aubol, B. E., and Adams, J. A. (2011) Applying the brakes to multisite SR protein phosphorylation: substrate-induced effects on the splicing kinase SRPK1. Biochemistry 50, 6888-6900
38. Adams, J. A., and Taylor, S. S. (1992) Energetic limits of phosphotransfer in the catalytic subunit of cAMP-dependent protein kinase as measured by viscosity experiments. Biochemistry 31, 8516-8522
39. Grant, B. D., and Adams, J. A. (1996) Pre-steady-state kinetic analysis of cAMP-dependent protein kinase using rapid quench flow techniques. Biochemistry 35, 2022-2029
40. Yu, F. X., Zhang, Y., Park, H. W., Jewell, J. L., Chen, Q., Deng, Y., Pan, D., Taylor, S. S., Lai, Z. C., and Guan, K. L. (2013) Protein kinase A activates the Hippo pathway to modulate cell proliferation and differentiation. Genes Dev. 27, 1223-1232
41. Aubol, B. E., Chakrabarti, S., Ngo, J., Shaffer, J., Nolen, B., Fu, X. D., Ghosh, G., and Adams, J. A. (2003) Processive phosphorylation of alternative splicing factor/splicing factor 2. Proc. Natl. Acad. Sci. U.S.A. 100, 12601-12606
42. Velazquez-Dones, A., Hagopian, J. C., Ma, C. T., Zhong, X. Y., Zhou, H., Ghosh, G., Fu, X. D., and Adams, J. A. (2005) Mass spectrometric and kinetic analysis of ASF/SF2 phosphorylation by SRPK1 and Clk/Sty. J. Biol. Chem. 280, 41761-41768
43. Zhou, J., and Adams, J. A. (1997) Participation of ADP dissociation in the rate-determining step in cAMP-dependent protein kinase. Biochemistry 36, 15733-15738
44. Kuzmic, P. (1996) Program DYNAFIT for the analysis of enzyme kinetic data: application to HIV proteinase. Anal. Biochem. 237, 260-273
45. Cléry, A., Jayne, S., Benderska, N., Dominguez, C., Stamm, S., and Allain, F. H. (2011) Molecular basis of purine-rich RNA recognition by the human SR-like protein Tra2-β1. Nat. Struct. Mol. Biol. 18, 443-450
46. Novoyatleva, T., Heinrich, B., Tang, Y., Benderska, N., Butchbach, M. E., Lorson, C. L., Lorson, M. A., Ben-Dov, C., Fehlbaum, P., Bracco, L., Burghes, A. H., Bollen, M., and Stamm, S. (2008) Protein phosphatase 1 binds to the RNA recognition motif of several splicing factors and regulates alternative pre-mRNA processing. Hum. Mol. Genet. 17, 52-70
47. Allemand, E., Guil, S., Myers, M., Moscat, J., Cáceres, J. F., and Krainer, A. R. (2005) Regulation of heterogeneous nuclear ribonucleoprotein A1 transport by phosphorylation in cells stressed by osmotic shock. Proc. Natl. Acad. Sci. U.S.A. 102, 3605-3610
48. Tazi, J., Daugeron, M. C., Cathala, G., Brunel, C., and Jeanteur, P. (1992) Adenosine phosphorothioates (ATPαS and ATPτS) differentially affect the two steps of mammalian pre-mRNA splicing. J. Biol. Chem. 267, 4322-4326
49. Kataoka, N., Bachorik, J. L., and Dreyfuss, G. (1999) Transportin-SR, a nuclear import receptor for SR proteins. J. Cell Biol. 145, 1145-1152
50. Zhang, Z., Kelemen, O., van Santen, M. A., Yelton, S. M., Wendlandt, A. E., Sviripa, V. M., Bollen, M., Beullens, M., Urlaub, H., Lührmann, R., Watt, D. S., and Stamm, S. (2011) Synthesis and characterization of pseudocantharidins, novel phosphatase modulators that promote the inclusion of exon 7 into the SMN (survival of motoneuron) pre-mRNA. J. Biol. Chem. 286, 10126-10136
51. Aubol, B. E., and Adams, J. A. (2014) Recruiting a silent partner for activation of the protein kinase SRPK1. Biochemistry 53, 4625-4634
52. Aubol, B. E., Plocinik, R. M., McGlone, M. L., and Adams, J. A. (2012) Nucleotide release sequences in the protein kinase SRPK1 accelerate substrate phosphorylation. Biochemistry 51, 6584-6594