SR protein kinases promote splicing of nonconsensus introns

Nature Structural and Molecular Biology

Volumn 22, Issue 8, 2015, Pages 611-617

  Lipp, Jesse J ^a   Marvin, Michael C ^b   Shokat, Kevan M ^a   Guthrie, Christine ^b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; BRANCHPOINT BINDING PROTEIN 1; DSK1 PROTEIN KINASE; PROTEIN KINASE; RNA HELICASE; SERINE ARGININE RICH PROTEIN; UNCLASSIFIED DRUG; PROTEIN SERINE THREONINE KINASE; PRP4 PROTEIN, S POMBE; RNA SPLICING; SCHIZOSACCHAROMYCES POMBE PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SUBSTRATE; FEMALE; GENE EXPRESSION; HELA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRON; INTRON RETENTION; MICROARRAY ANALYSIS; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE; SIGNAL TRANSDUCTION; SPLICING DEFECT; TRANSLATION INITIATION; AMINO ACID SEQUENCE; DNA MICROARRAY; DRUG EFFECTS; ENZYME SPECIFICITY; GENETICS; METABOLISM; MUTATION; PHOSPHORYLATION; WESTERN BLOTTING;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BLOTTING, WESTERN; INTRONS; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBONUCLEOPROTEIN, U4-U6 SMALL NUCLEAR; RNA SPLICE SITES; RNA SPLICING; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84938701492     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3057     Document Type: Article

References (55)

1. Wahl, M. C., Will, C. L. & Lührmann, R. The spliceosome: design principles of a dynamic RNP machine. Cell 136, 701-718 (2009).
2. Mermoud, J. E., Cohen, P. & Lamond, A. I. Ser/Thr-specific protein phosphatases are required for both catalytic steps of pre-mRNA splicing. Nucleic Acids Res. 20, 5263-5269 (1992).
3. Mermoud, J. E., Cohen, P. T. & Lamond, A. I. Regulation of mammalian spliceosome assembly by a protein phosphorylation mechanism. EMBO J. 13, 5679-5688 (1994).
4. Tazi, J. et al. Thiophosphorylation of U1-70K protein inhibits pre-mRNA splicing. Nature 363, 283-286 (1993).
5. Gui, J. F., Lane, W. S. & Fu, X. D. A serine kinase regulates intracellular localization of splicing factors in the cell cycle. Nature 369, 678-682 (1994).
6. Ghosh, G. & Adams, J. A. Phosphorylation mechanism and structure of serine-arginine protein kinases. FEBS J. 278, 587-597 (2011).
7. Giannakouros, T., Nikolakaki, E., Mylonis, I. & Georgatsou, E. Serine-arginine protein kinases: a small protein kinase family with a large cellular presence. FEBS J. 278, 570-586 (2011).
8. Colwill, K. et al. The Clk/Sty protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution. EMBO J. 15, 265-275 (1996).
9. Duncan, P. I., Stojdl, D. F., Marius, R. M., Scheit, K. H. & Bell, J. C. The Clk2 and Clk3 dual-specificity protein kinases regulate the intranuclear distribution of SR proteins and influence pre-mRNA splicing. Exp. Cell Res. 241, 300-308 (1998).
10. Gross, T. et al. Functional analysis of the fission yeast Prp4 protein kinase involved in pre-mRNA splicing and isolation of a putative mammalian homologue. Nucleic Acids Res. 25, 1028-1035 (1997).
11. Roth, M. B., Zahler, A. M. & Stolk, J. A. A conserved family of nuclear phosphoproteins localized to sites of polymerase II transcription. J. Cell Biol. 115, 587-596 (1991).
12. Graveley, B. R. Sorting out the complexity of SR protein functions. RNA 6, 1197-1211 (2000).
13. Zhou, Z. & Fu, X.-D. Regulation of splicing by SR proteins and SR protein-specific kinases. Chromosoma 122, 191-207 (2013).
14. Cao, D.-S. et al. Large-scale prediction of human kinase-inhibitor interactions using protein sequences and molecular topological structures. Anal. Chim. Acta 792, 10-18 (2013).
15. Xiao, S. H. & Manley, J. L. Phosphorylation of the ASF/SF2 RS domain affects both protein-protein and protein-RNA interactions and is necessary for splicing. Genes Dev. 11, 334-344 (1997).
16. Xiao, S. H. & Manley, J. L. Phosphorylation-dephosphorylation differentially affects activities of splicing factor ASF/SF2. EMBO J. 17, 6359-6367 (1998).
17. Cao, W., Jamison, S. F. & Garcia-Blanco, M. A. Both phosphorylation and dephosphorylation of ASF/SF2 are required for pre-mRNA splicing in vitro. RNA 3, 1456-1467 (1997).
18. Tacke, R., Chen, Y. & Manley, J. L. Sequence-specific RNA binding by an SR protein requires RS domain phosphorylation: creation of an SRp40-specific splicing enhancer. Proc. Natl. Acad. Sci. USA 94, 1148-1153 (1997).
19. Yeakley, J. M. et al. Phosphorylation regulates in vivo interaction and molecular targeting of serine/arginine-rich pre-mRNA splicing factors. J. Cell Biol. 145, 447-455 (1999).
20. Roscigno, R. F. & Garcia-Blanco, M. A. SR proteins escort the U4/U6. U5 tri-snRNP to the spliceosome. RNA 1, 692-706 (1995).
21. Boutz, P. L., Bhutkar, A. & Sharp, P. A. Detained introns are a novel, widespread class of post-transcriptionally spliced introns. Genes Dev. 29, 63-80 (2015).
22. Zhou, Z. et al. 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 (2012).
23. Bishop, A. C. et al. A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 407, 395-401 (2000).
24. Inada, M. & Pleiss, J. A. Genome-wide approaches to monitor pre-mRNA splicing. Methods Enzymol. 470, 51-75 (2010).
25. Hertz, N. T. et al. Chemical genetic approach for kinase-substrate mapping by covalent capture of thiophosphopeptides and analysis by mass spectrometry. Curr. Protoc. Chem. Biol. 2, 15-36 (2010).
26. Colwill, K. et al. SRPK1 and Clk/Sty protein kinases show distinct substrate specificities for serine/arginine-rich splicing factors. J. Biol. Chem. 271, 24569-24575 (1996).
27. Aubol, B. E. et al. Partitioning RS domain phosphorylation in an SR protein through the CLK and SRPK protein kinases. J. Mol. Biol. 425, 2894-2909 (2013).
28. Tang, Z. et al. Interacting factors and cellular localization of SR protein-specific kinase Dsk1. Exp. Cell Res. 318, 2071-2084 (2012).
29. Tang, Z., Yanagida, M. & Lin, R. J. Fission yeast mitotic regulator Dsk1 is an SR protein-specific kinase. J. Biol. Chem. 273, 5963-5969 (1998).
30. Zhang, Y. et al. Structure, phosphorylation and U2AF65 binding of the N-terminal domain of splicing factor 1 during 3-splice site recognition. Nucleic Acids Res. 41, 1343-1354 (2013).
31. Krämer, A. & Utans, U. Three protein factors (SF1, SF3 and U2AF) function in pre-splicing complex formation in addition to snRNPs. EMBO J. 10, 1503-1509 (1991).
32. Rain, J. C., Rafi, Z., Rhani, Z., Legrain, P. & Krämer, A. Conservation of functional domains involved in RNA binding and protein-protein interactions in human and Saccharomyces cerevisiae pre-mRNA splicing factor SF1. RNA 4, 551-565 (1998).
33. Berglund, J. A., Abovich, N. & Rosbash, M. A cooperative interaction between U2AF65 and mBBP/SF1 facilitates branchpoint region recognition. Genes Dev. 12, 858-867 (1998).
34. Berglund, J. A., Chua, K., Abovich, N., Reed, R. & Rosbash, M. The splicing factor BBP interacts specifically with the pre-mRNA branchpoint sequence UACUAAC. Cell 89, 781-787 (1997).
35. Berglund, J. A., Fleming, M. L. & Rosbash, M. The KH domain of the branchpoint sequence binding protein determines specificity for the pre-mRNA branchpoint sequence. RNA 4, 998-1006 (1998).
36. Huang, T., Vilardell, J. & Query, C. C. Pre-spliceosome formation in S. pombe requires a stable complex of SF1-U2AF(59)-U2AF(23). EMBO J. 21, 5516-5526 (2002).
37. Liu, Z. et al. Structural basis for recognition of the intron branch site RNA by splicing factor 1. Science 294, 1098-1102 (2001).
38. Jacewicz, A., Chico, L., Smith, P., Schwer, B. & Shuman, S. Structural basis for recognition of intron branchpoint RNA by yeast Msl5 and selective effects of interfacial mutations on splicing of yeast pre-mRNAs. RNA 21, 401-414 (2015).
39. Manceau, V. et al. Major phosphorylation of SF1 on adjacent Ser-Pro motifs enhances interaction with U2AF65. FEBS J. 273, 577-587 (2006).
40. Wang, W. et al. Structure of phosphorylated SF1 bound to U2AF65 in an essential splicing factor complex. Structure 21, 197-208 (2013).
41. Stamm, S. Regulation of alternative splicing by reversible protein phosphorylation. J. Biol. Chem. 283, 1223-1227 (2008).
42. Aubol, B. E. et al. Processive phosphorylation of alternative splicing factor/splicing factor 2. Proc. Natl. Acad. Sci. USA 100, 12601-12606 (2003).
43. Ngo, J. C. K. et al. A sliding docking interaction is essential for sequential and processive phosphorylation of an SR protein by SRPK1. Mol. Cell 29, 563-576 (2008).
44. Cho, S. et al. 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. USA 108, 8233-8238 (2011).
45. Shin, C., Feng, Y. & Manley, J. L. Dephosphorylated SRp38 acts as a splicing repressor in response to heat shock. Nature 427, 553-558 (2004).
46. Huang, Y., Gattoni, R., Stévenin, J. & Steitz, J. A. SR splicing factors serve as adapter proteins for TAP-dependent mRNA export. Mol. Cell 11, 837-843 (2003).
47. Gao, Q. et al. Evaluation of cancer dependence and druggability of PRP4 kinase using cellular, biochemical, and structural approaches. J. Biol. Chem. 288, 30125-30138 (2013).
48. Rutz, B. & Séraphin, B. Transient interaction of BBP/ScSF1 and Mud2 with the splicing machinery affects the kinetics of spliceosome assembly. RNA 5, 819-831 (1999).
49. Rutz, B. & Séraphin, B. A dual role for BBP/ScSF1 in nuclear pre-mRNA retention and splicing. EMBO J. 19, 1873-1886 (2000).
50. Jang, S.-W. et al. Interaction of Akt-phosphorylated SRPK2 with 14-3-3 mediates cell cycle and cell death in neurons. J. Biol. Chem. 284, 24512-24525 (2009).
51. Potashkin, J., Naik, K. & Wentz-Hunter, K. U2AF homolog required for splicing in vivo. Science 262, 573-575 (1993).
52. Smyth, G. K. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. App. Genet. Mol. Biol. 3, Article3 (2004).
53. Durinck, S. et al. BioMart and Bioconductor: a powerful link between biological databases and microarray data analysis. Bioinformatics 21, 3439-3440 (2005).
54. Lorenz, R. et al. ViennaRNA Package 2. 0. Algorithms Mol. Biol. 6, 26 (2011).
55. Plass, M., Agirre, E., Reyes, D., Camara, F. & Eyras, E. Co-evolution of the branch site and SR proteins in eukaryotes. Trends Genet. 24, 590-594 (2008).