Cell cycle-dependent phosphorylation of human CDC5 regulates RNA processing

Cell Cycle

Volumn 7, Issue 12, 2008, Pages 1795-1803

  Gräub, Remo ^a   Lancero, Hope ^a   Pedersen, Anissa ^a   Chu, Meihua ^a   Padmanabhan, Krishnan ^a   Xu, Xiao Qin ^a   Spitz, Paul ^a   Chalkley, Robert ^a   Burlingame, Alma L ^a   Stokoe, David ^b   Bernstein, Harold S ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CDC5L; Cell cycle; Mitotic entry; Phosphorylation; Spliceosome

Indexed keywords

2 BIS(2 HYDROXYETHYL)AMINO 9 ISOPROPYL 6 (4 METHOXYBENZYLAMINO)PURINE; CELL CYCLE PROTEIN; CELL CYCLE PROTEIN 5; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 2; PHOSPHOPEPTIDE; THREONINE;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL CYCLE; ELECTROSPRAY MASS SPECTROMETRY; GENE MAPPING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; ISOTOPE LABELING; MOLECULAR RECOGNITION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; PROTEIN PHOSPHORYLATION; RNA PROCESSING; RNA SPLICING; SPLICEOSOME;

MAMMALIA;

EID: 47249110708     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.7.12.6017     Document Type: Article

References (49)

1. Nasmyth K, Nurse P. Cell division cycle mutants altered in DNA replication and mitosis in the fission yeast Schizosaccharomyces pombe. Mol Gen Genet 1981; 182:119-24.
2. + gene encodes an essential protein with homology to c-Myb. EMBO J 1994; 13:471-83.
3. 2 progression and mitotic entry. J Biol Chem 1998; 273:4666-71.
4. Bernstein HS, Coughlin SR. Pombe Cdc5-related protein. A putative human transcription factor implicated in mitogen-activated signaling. J Biol Chem 1997; 272:5833-7.
5. Lei XH, Shen X, Xu XQ, Bernstein HS. Human Cdc5, a regulator of mitotic entry, can act as a site-specific DNA binding protein. J Cell Sci 2000; 113:4523-31.
6. Johnson LM, Too CK. Prolactin, interleukin-2 and FGF-2 stimulate expression, nuclear distribution and DNA-binding of rat homolog of pombe Cdc5 in Nb2 T lymphoma cells. Mol Cell Endocrinol 2001; 184:151-61.
7. Tsai WY, Chow YT, Chen HR, Huang KT, Hong RI, Jan SP, Kuo NY, Tsao TY, Chen CH, Cheng SC. Cef1p is a component of the Prp19p-associated complex and essential for pre-mRNA splicing. J Biol Chem 1999; 274:9455-62.
8. McDonald WH, Ohi R, Smelkova N, Frendewey D, Gould KL. Myb-related fission yeast cdc5p is a component of a 40S snRNP-containing complex and is essential for pre-mRNA splicing. Mol Cell Biol 1999; 19:5352-62.
9. Ajuh P, Kuster B, Panov K, Zomerdijk JC, Mann M, Lamond AI. Functional analysis of the human CDC5L complex and identification of its components by mass spectrometry. EMBO J 2000; 19:6569-81.
10. Ohi MD, Link AJ, Ren L, Jennings JL, McDonald WH, Gould KL. Proteomics analysis reveals stable multiprotein complexes in both fission and budding yeasts containing Myb-related Cdc5p/Cef1p, novel pre-mRNA splicing factors, and snRNAs. Mol Cell Biol 2002; 22:2011-24.
11. Zhou Z, Licklider LJ, Gygi SP, Reed R. Comprehensive proteomic analysis of the human spliceosome. Nature 2002; 419:182-5.
12. Makarov EM, Makarova OV, Urlaub H, Gentzel M, Will CL, Wilm M, Luhrmann R. Small nuclear ribonucleoprotein remodeling during catalytic activation of the spliceosome. Science 2002; 298:2205-8.
13. Liu L, Graub R, Hlaing M, Epting CL, Turck CW, Xu XQ, Zhang L, Bernstein HS. Distinct domains of human CDC5 direct its nuclear import and association with the spliceosome. Cell Biochem Biophys 2003; 39:119-32.
14. Burns CG, Ohi R, Krainer AR, Gould KL. Evidence that Myb-related CDC5 proteins are required for pre-mRNA splicing. Proc Natl Acad Sci USA 1999; 96:13789-94.
15. Boudrez A, Beullens M, Groenen P, Van Eynde A, Vulsteke V, Jagiello I, Murray M, Krainer AR, Stalmans W, Bollen M. NIPP1-mediated interaction of protein phosphatase-1 with CDC5L, a regulator of pre-mRNA splicing and mitotic entry. J Biol Chem 2000; 275:25411-7.
16. Ajuh P, Sleeman J, Chusainow J, Lamond AI. A direct interaction between the carboxyl-terminal region of CDC5L and the WD40 domain of PLRG1 is essential for pre-mRNA splicing. J Biol Chem 2001; 276:42370-81.
17. Burns CG, Ohi R, Mehta S, O'Toole ET, Winey M, Clark TA, Sugnet CW, Ares M Jr, Gould KL. Removal of a single alpha-tubulin gene intron suppresses cell cycle arrest phenotypes of splicing factor mutations in Saccharomyces cerevisiae. Mol Cell Biol 2002; 22:801-15.
18. Morgan DO. Cyclin-dependent kinases: engines, clocks and microprocessors. Ann Rev Cell Dev Biol 1997; 13:261-91.
19. Soret J, Tazi J. Phosphorylation-dependent control of the pre-mRNA splicing machinery. Prog Mol Subcell Biol 2003; 31:89-126.
20. Mermoud JE, Cohen P, Lamond AI. Ser/Thr-specific protein phosphatases are required for both catalytic steps of pre-mRNA splicing. Nuc Acids Res 1992; 20:5263-9.
21. Tazi J, Daugeron MC, Cathala G, Brunel C, Jeanteur P. Adenosine phosphorothioates (ATP alpha S and ATP tau S) differentially affect the two steps of mammalian pre-mRNA splicing. J Biol Chem 1992; 267:4322-6.
22. Lai MC, Lin RI, Huang SY, Tsai CW, Tarn WY. A human importin-beta family protein, transportin-SR2, interacts with the phosphorylated RS domain of SR proteins. J Biol Chem 2000; 275:7950-7.
23. Misteli T, Caceres JF, Clement JQ, Krainer AR, Wilkinson MF, Spector DL. Serine phosphorylation of SR proteins is required for their recruitment to sites of transcription in vivo. J Cell Biol 1998; 143:297-307.
24. Obenauer JC, Cantley LC, Yaffe MB. Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nuc Acids Res 2003; 31:3635-41.
25. Fairall L, Chapman L, Moss H, de Lange T, Rhodes D. Structure of the TRFH dimerization domain of the human telomeric proteins TRF1 and TRF2. Mol Cell 2001; 8:351-61.
26. Spink KG, Evans RJ, Chambers A. Sequence-specific binding of Taz1p dimers to fission yeast telomeric DNA. Nuc Acids Res 2000; 28:527-33.
27. Neubauer G, King A, Rappsilber J, Calvio C, Watson M, Ajuh P, Sleeman J, Lamond A, Mann M. Mass spectrometry and EST-database searching allows characterization of the multi-protein spliceosome complex. Nature Genetics 1998; 20:46-50.
28. Rappsilber J, Ryder U, Lamond AI, Mann M. Large-scale proteomic analysis of the human spliceosome. Genome Res 2002; 12:1231-45.
29. Stryke D, Kawamoto M, Huang CC, Johns SJ, King LA, Harper CA, Meng EC, Lee RE, Yee A, L'Italien L, Chuang PT, Young SG, Skarnes WC, Babbitt PC, Ferrin TE. BayGenomics: a resource of insertional mutations in mouse embryonic stem cells. Nuc Acids Res 2003; 31:278-81.
30. Pearson RB, Kemp BE. Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol 1991; 200:62-81.
31. Gescher A. Analogs of staurosporine: potential anticancer drugs? Gen Pharm 1998; 31:721-8.
32. Kousidou O, Tzanakakis GN, Karamanos NK. Effects of the natural isoflavonoid genistein on growth, signaling pathways and gene expression of matrix macromolecules by breast cancer cells. Mini Rev Med Chem 2006; 6:331-7.
33. Cuenda A, Alessi DR. Use of kinase inhibitors to dissect signaling pathways. Methods Mol Biol 2000; 99:161-75.
34. 2+ and cyclic adenosine monophosphate-dependent signaling in endothelial exocytosis. Blood 1998; 91:118-27.
35. Bhattacharjee RN, Banks GC, Trotter KW, Lee HL, Archer TK. Histone H1 phosphorylation by Cdk2 selectively modulates mouse mammary tumor virus transcription through chromatin remodeling. Mol Cell Biol 2001; 21:5417-25.
36. Brooks EE, Gray NS, Joly A, Kerwar SS, Lum R, Mackman RL, Norman TC, Rosete J, Rowe M, Schow SR, Schultz PG, Wang X, Wick MM, Shiffman D. CVT-313, a specific and potent inhibitor of CDK2 that prevents neointimal proliferation. J Biol Chem 1997; 272:29207-11.
37. Olivero P, Stutzin A. Calcium modulates osmosensitive taurine efflux in HeLa cells. Neurochem Res 2004; 29:169-76.
38. Gray N, Detivaud L, Doerig C, Meijer L. ATP-site directed inhibitors of cyclin-dependent kinases. Curr Med Chem 1999; 6:859-75.
39. + homolog of a higher plant, Arabidopsis thaliana. Proc Natl Acad Sci USA 1996; 93:13371-6.
40. Hlaing M, Shen X, Dazin P, Bernstein HS. The hypertrophic response in C2C12 myoblasts recruits the G1 cell cycle machinery. J Biol Chem 2002; 277:23794-9.
41. INK4A correlates with Cdk4 association. J Biol Chem 2003; 278:6619-22.
42. Boyle WJ, van der Geer P, Hunter T. Phosphopeptide mapping and phosphoamino acid analysis by 2D separation on thin-layer cellulose plates. Methods Enzymol 1991; 201:110-49.
43. Stokoe D, Engel K, Campbell DG, Cohen P, Gaestel M. Identification of MAPKAP kinase 2 as a major enzyme responsible for the phosphorylation of the small mammalian heat shock proteins. FEBS Letters 1992; 313:307-13.
44. Medzihradszky KF, Leffler H, Baldwin MA, Burlingame AL. Protein identification by in-gel digestion, high-performance liquid chromatography, and mass spectrometry: peptide analysis by complementary ionization techniques. J Am Soc Mass Spectrom 2001; 12:215-21.
45. Maruyama E. Biochemical characterization of mouse brain necdin. Biochem J 1996; 314:895-901.
46. Lamond AI, Konarska MM, Sharp PA. A mutational analysis of spliceosome assembly: evidence for splice site collaboration during spliceosome formation. Genes Dev 1987; 1:532-43.
47. Enssle J, Kugler W, Hentze MW, Kulozik AE. Determination of mRNA fate by different RNA polymerase II promoters. Proc Natl Acad Sci USA 1993; 90:10091-5.
48. Franklin CC, Adler V, Kraft AS. Phosphorylation of transcription factors. Methods Enzymol 1995; 254:550-64.
49. Adler V, Franklin CC, Kraft AS. Phorbol esters stimulate the phosphorylation of c-Jun but not v-Jun: regulation by the N-terminal delta domain. Proc Natl Acad Sci USA 1992; 89:5341-5.