N-terminus of the protein kinase CLK1 induces SR protein hyperphosphorylation

Biochemical Journal

Volumn 462, Issue 1, 2014, Pages 143-152

  Aubol, Brandon E ^a   Plocinik, Ryan M ^a   Keshwani, Malik M ^a   Mcglone, Maria L ^a   Hagopian, Jonathan C ^a   Ghosh, Gourisankar ^b   Fu, Xiang Dong ^c   Adams, Joseph A ^a  

^a University of California San Diego   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cdc2 like kinase 1 (CLK1); Docking; Kinase; Kinetics; Phosphorylation; Splicing

Indexed keywords

CDC2 LIKE KINASE 1; PROTEIN KINASE; SERINE ARGININE RICH PROTEIN; SERINE ARGININE RICH PROTEIN PROTEIN SPLICING FACTOR 1; SERINE ARGININE RICH PROTEIN PROTEIN SPLICING FACTOR 2; SERINE ARGININE RICH PROTEIN PROTEIN SPLICING FACTOR 5; TRANSFORMER 2BETA1; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING;

ANIMALS; ARGININE; HUMANS; MICE; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; RNA SPLICING; RNA-BINDING PROTEINS; SERINE; SUBSTRATE SPECIFICITY;

EID: 84904640566     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20140494     Document Type: Article

References (30)

1. Adams, J. A. (2001) Kinetic and Catalytic Mechanisms of Protein Kinases. Chem. Rev. 101, 2271-2290 CrossRef PubMed
2. Goldsmith, E. J., Akella, R., Min, X., Zhou, T. and Humphreys, J. M. (2007) Substrate and docking interactions in serine/threonine protein kinases. Chem. Rev. 107, 5065-5081 CrossRef PubMed (Pubitemid 350225869)
3. Long, J. C. and Caceres, J. F. (2009) The SR protein family of splicing factors: master regulators of gene expression. Biochem. J. 417, 15-27 CrossRef PubMed
4. 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 CrossRef PubMed (Pubitemid 43160053)
5. Xiang, S., Gapsys, V., Kim, H. Y., Bessonov, S., Hsiao, H. H., Mohlmann, S., Klaukien, V., Ficner, R., Becker, S., Urlaub, H. et al. (2013) Phosphorylation drives a dynamic switch in serine/arginine-rich proteins. Structure 21, 2162-2174 CrossRef PubMed
6. Tintaru, A. M., Hautbergue, G. M., Hounslow, A. M., Hung, M. L., Lian, L. Y., Craven, C. J. and Wilson, S. A. (2007) Structural and functional analysis of RNA and TAP binding to SF2/ASF. EMBO Rep. 8, 756-762 CrossRef PubMed (Pubitemid 47202455)
7. Phelan, M. M., Goult, B. T., Clayton, J. C., Hautbergue, G. M., Wilson, S. A. and Lian, L. Y. (2012) The structure and selectivity of the SR protein SRSF2 RRM domain with RNA. Nucleic Acids Res. 40, 3232-3244 CrossRef PubMed
8. Clery, 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 CrossRef PubMed
9. Ghosh, G. and Adams, J. A. (2011) Phosphorylation mechanism and structure of serine-arginine protein kinases. FEBS J. 278, 587-597 CrossRef PubMed
10. 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 CrossRef PubMed (Pubitemid 351374682)
11. 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 CrossRef PubMed
12. 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 CrossRef PubMed (Pubitemid 41396564)
13. Glatz, D. C., Rujescu, D., Tang, Y., Berendt, F. J., Hartmann, A. M., Faltraco, F., Rosenberg, C., Hulette, C., Jellinger, K., Hampel, H. et al. (2006) The alternative splicing of tau exon 10 and its regulatory proteins CLK2 and TRA2-BETA1 changes in sporadic Alzheimer's disease. J. Neurochem. 96, 635-644 CrossRef PubMed
14. Aubol, B. E., Plocinik, R. M., Hagopian, J. C., Ma, C. T., McGlone, M. L., Bandyopadhyay, R., Fu, X. D. and Adams, J. A. (2013) Partitioning RS domain phosphorylation in an SR protein through the CLK and SRPK protein kinases. J. Mol. Biol. 425, 2894-2909 CrossRef PubMed
15. 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 CrossRef PubMed (Pubitemid 41832239)
16. 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 CrossRef PubMed
17. Aubol, B. E., Plocinik, R. M., Hagopian, J. C., Ma, C. T., McGlone, M. L., Bandyopadhyay, R., Fu, X. D. and Adams, J. A. (2013) Partitioning RS domain phosphorylation in an SR protein through the CLK and SRPK protein kinases. J. Mol. Biol. 425, 2894-2909 CrossRef PubMed
18. Bullock, A. N., Das, S., Debreczeni, J. E., Rellos, P., Fedorov, O., Niesen, F. H., Guo, K., Papagrigoriou, E., Amos, A. L., Cho, S. et al. (2009) Kinase domain insertions define distinct roles of CLK kinases in SR protein phosphorylation. Structure 17, 352-362 CrossRef PubMed
19. 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 PubMed (Pubitemid 26029629)
20. Huynh, N., Ma, C. T., Giang, N., Hagopian, J., Ngo, J., Adams, J. and Ghosh, G. (2009) Allosteric interactions direct binding and phosphorylation of ASF/SF2 by SRPK1. Biochemistry 48, 11432-11440 CrossRef PubMed
21. 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 CrossRef PubMed
22. Ma, C. T., Ghosh, G., Fu, X. D. and Adams, J. A. (2010) Mechanism of dephosphorylation of the SR protein ASF/SF2 by protein phosphatase 1. J. Mol. Biol. 403, 386-404 CrossRef PubMed
23. 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 CrossRef PubMed
24. Koizumi, J., Okamoto, Y., Onogi, H., Mayeda, A., Krainer, A. R. and Hagiwara, M. (1999) The subcellular localization of SF2/ASF is regulated by direct interaction with SR protein kinases (SRPKs). J. Biol. Chem. 274, 11125-11131 CrossRef PubMed
25. Biondi, R. M., Komander, D., Thomas, C. C., Lizcano, J. M., Deak, M., Alessi, D. R. and van Aalten, D. M. (2002) High resolution crystal structure of the human PDK1 catalytic domain defines the regulatory phosphopeptide docking site. EMBO J. 21, 4219-4228 CrossRef PubMed
26. Schulman, B. A., Lindstrom, D. L. and Harlow, E. (1998) Substrate recruitment to cyclin-dependent kinase 2 by a multipurpose docking site on cyclin A. Proc. Natl. Acad. Sci. U.S.A. 95, 10453-10458 CrossRef PubMed (Pubitemid 28413088)
27. Brown, N. R., Noble, M. E., Endicott, J. A. and Johnson, L. N. (1999) The structural basis for specificity of substrate and recruitment peptides for cyclin-dependent kinases. Nat. Cell Biol. 1, 438-443 CrossRef PubMed (Pubitemid 129502811)
28. Hawkins, J., Zheng, S., Frantz, B. and LoGrasso, P. (2000) p38 map kinase substrate specificity differs greatly for protein and peptide substrates. Arch. Biochem. Biophys. 382, 310-313 CrossRef PubMed
29. Plocinik, R. M., Li, S., Liu, T., Hailey, K. L., Whitesides, J., Ma, C. T., Fu, X. D., Gosh, G., Woods, Jr, V. L., Jennings, P. A. and Adams, J. A. (2011) Regulating SR protein phosphorylation through regions outside the kinase domain of SRPK1. J. Mol. Biol. 410, 131-145 CrossRef PubMed
30. Perutz, M. F., Staden, R., Moens, L. and De Baere, I. (1993) Polar zippers. Curr. Biol. 3, 249-253 CrossRef PubMed