The apoptosis modulator and tumour suppressor protein RBM5 is a phosphoprotein

Cell Biochemistry and Function

Volumn 25, Issue 6, 2007, Pages 643-653

  Shu, Yanjun ^a,e   Rintala Maki, Nina D ^a   Wall, Vanessa E ^a   Wang, Ke ^a   Goard, Carolyn A ^a   Langdon, Colleen E ^a   Sutherland, Leslie C ^a,b,c,d  

^a SUDBURY REGIONAL HOSPITAL   (Canada)

^b NORTHERN ONTARIO SCHOOL OF MEDICINE   (Canada)

^c LAURENTIAN UNIVERSITY   (Canada)

^d Princess Margaret Hospital ^*  (Canada)

^e PRINCESS MARGARET HOSPITAL   (Canada)

Author keywords

Apoptosis; LUCA 15; Phosphorylation; RBM5; Tumour suppressor

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; PHOSPHOPROTEIN; PHOSPHOTYROSINE; RNA BINDING PROTEIN; TUMOR SUPPRESSOR PROTEIN; TUMOR SUPPRESSOR PROTEIN RBM5; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DEPENDENT PROTEIN KINASE; DNA BINDING PROTEIN; PROTEIN KINASE C; RBM5 PROTEIN, HUMAN; RECOMBINANT GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; SERINE;

APOPTOSIS; ARTICLE; CELL CULTURE; CELL CYCLE REGULATION; CELL LYSATE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MODULATION; MOLECULAR WEIGHT; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; AMINO ACID SEQUENCE; BINDING SITE; DRUG EFFECT; GENETIC TRANSFECTION; GENETICS; LEUKEMIA CELL LINE; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PHYSIOLOGY; SITE DIRECTED MUTAGENESIS; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE; WESTERN BLOTTING;

AMINO ACID SEQUENCE; APOPTOSIS; BINDING SITES; BLOTTING, WESTERN; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLIC GMP-DEPENDENT PROTEIN KINASES; DNA-BINDING PROTEINS; GENES, TUMOR SUPPRESSOR; GRANULOCYTE MACROPHAGE COLONY-STIMULATING FACTORS, RECOMBINANT; HUMANS; JURKAT CELLS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASE C; RNA-BINDING PROTEINS; SERINE; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS;

EID: 38449115065     PISSN: 02636484     EISSN: 10990844     Source Type: Journal    
DOI: 10.1002/cbf.1366     Document Type: Article

References (55)

1. Mourtada-Maarabouni M, Sutherland LC, Meredith JM, Williams GT. Simultaneous acceleration of the cell cycle and suppression of apoptosis by splice variant delta-6 of the candidate tumour suppressor LUCA-15/RBM5. Genes Cells 2003; 8: 109-119.
2. Rintala-Maki ND, Sutherland LC. LUCA-15/RBM5, a putative tumour suppressor, enhances multiple receptor-initiated death signals. Apoptosis 2004; 9: 475-484.
3. Rintala-Maki ND, Abrasonis V, Burd M, Sutherland LC. Genetic instability of RBM5/LUCA-15/H37 in MCF-7 breast carcinoma sublines may affect susceptibility to apoptosis. Cell Biochem Funct 2004; 22: 307-313.
4. Mourtada-Maarabouni M, Williams GT. RBM5/LUCA-15 - Tumour suppression by control of apoptosis and the cell cycle? Sci World J 2002; 2: 1885-1890.
5. Oh JJ, West AR, Fishbein MC, Slamon DJ. A candidate tumor suppressor gene, H37, from the human lung cancer tumor suppressor locus 3p21.3. Cancer Res 2002; 62: 3207-3213.
6. Sutherland LC, Lerman M, Williams GT, Miller BA. LUCA-15 suppresses CD95-mediated apoptosis in Jurkat T cells. Oncogene 2001; 20: 2713-2719.
7. Sutherland LC, Lerman M, Williams GT, Miller BA. LUCA-15 suppresses CD95-mediated apoptosis in Jurkat T cells. Oncogene 2004; 23: 629.
8. Mourtada-Maarabouni M, Sutherland LC, Williams GT. Candidate tumour suppressor LUCA-15 can regulate multiple apoptotic pathways. Apoptosis 2002; 7: 421-432.
9. Kok K, van den BA, Veldhuis PM, et al. A homozygous deletion in a small cell lung cancer cell line involving a 3p21 region with a marked instability in yeast artificial chromosomes. Cancer Res 1994; 54: 4183-4187.
10. Wei MH, Latif F, Bader S, et al. Construction of a 600-kilobase cosmid clone contig and generation of a transcriptional map surrounding the lung cancer tumor suppressor gene (TSG) locus on human chromosome 3p21.3: progress toward the isolation of a lung cancer TSG. Cancer Res 1996; 56: 1487-1492.
11. Sekido Y, Ahmadian M, Wistuba II, et al. Cloning of a breast cancer homozygous deletion junction narrows the region of search for a 3p21.3 tumor suppressor gene. Oncogene 1998; 16: 3151-3157.
12. Kok K, Naylor SL, Buys CH. Deletions of the short arm of chromosome 3 in solid tumors and the search for suppressor genes. Adv Cancer Res 1997; 71: 27-92.
13. Lerman MI, Minna JD. The 630-kb lung cancer homozygous deletion region on human chromosome 3p21.3: identification and evaluation of the resident candidate tumor suppressor genes. The International Lung Cancer Chromosome 3p21.3 Tumor Suppressor Gene Consortium. Cancer Res 2000; 60: 6116-6133.
14. Senchenko VN, Liu J, Loginov W, et al. Discovery of frequent homozygous deletions in chromosome 3p21.3 LUCA and AP20 regions in renal, lung and breast carcinomas. Oncogene 2004; 23: 5719-5728.
15. Timmer T, Terpstra P, van den BA. et al. A comparison of genomic structures and expression patterns of two closely related flanking genes in a critical lung cancer region at 3p21.3. Eur J Hum Genet 1999; 7: 478-486.
16. Oh JJ, Grosshans DR, Wong SG, Slamon DJ. Identification of differentially expressed genes associated with HER- 2/neu overexpression in human breast cancer cells. Nucleic Acids Res 1999; 27: 4008-4017.
17. Valcarcel J, Green MR. The SR protein family: pleiotropic functions in pre-mRNA splicing. Trends Biochem Sci 1996; 21: 296-301.
18. Manley JL, Tacke R. SR proteins and splicing control. Genes Dev 1996; 10: 1569-1579.
19. Blencowe BJ, Bowman JA, McCracken S, Rosonina E. SR-related proteins and the processing of messenger RNA precursors. Biochem Cell Biol 1999; 77: 277-291.
20. Burd CG, Dreyfuss G. Conserved structures and diversity of functions of RNA-binding proteins. Science 1994; 265: 615-621.
21. Wu JY, Maniatis T. Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell 1993; 75: 1061-1070.
22. Kohtz JD, Jamison SF, Will CL, et al. Protein-protein interactions and 5′-splice-site recognition in mammalian mRNA precursors. Nature 1994; 368: 119-124.
23. Graveley BR. Sorting out the complexity of SR protein functions. RNA 2000; 6: 1197-1211.
24. Colwill K, Pawson T, Andrews B, et al. The Clk/Sty protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution. EMBO J 1996; 15: 265-275.
25. Bubulya PA, Prasanth KV, Deerinck TJ, et al. Hypophosphorylated SR splicing factors transiently localize around active nucleolar organizing regions in telophase daughter nuclei. J Cell Biol 2004; 167: 51-63.
26. 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.
27. Duncan PI, Stojdl DF, Marius RM, Scheit KH, Bell JC. The Clk2 and Clk3 dual-specificity protein kinases regulate the intranuclear distribution of SR proteins and influence pre-mRNA splicing. Exp Cell Res 1998; 241: 300-308.
28. Kanopka A, Muhlemann O, Petersen-Mahrt S, Estmer C, Ohrmalm C, Akusjarvi G. Regulation of adenovirus alternative RNA splicing by dephosphorylation of SR proteins. Nature 1998; 393: 185-187.
29. Tazi J, Kornstadt U, Rossi F, et al. Thiophosphorylation of U1-70K protein inhibits pre-mRNA splicing. Nature 1993; 363: 283-286.
30. Xiao SH, Manley JL. Phosphorylation of the ASF/SF2 RS domain affects both protein-protein and protein-RNA interactions and is necessary for splicing. Genes Dev 1997; 11: 334-344.
31. Xiao SH, Manley JL. Phosphorylation-dephosphorylation differentially affects activities of splicing factor ASF/SF2. EMBO J 1998; 17: 6359-6367.
32. Mermoud JE, Cohen PT, Lamond AI. Regulation of mammalian spliceosome assembly by a protein phosphorylation mechanism. EMBO J 1994; 13: 5679-5688.
33. Murray MV, Kobayashi R, Krainer AR. The type 2C Ser/Thr phosphatase PP2Cgamma is a pre-mRNA splicing factor. Genes Dev 1999; 13: 87-97.
34. Wang HY, Lin W, Dyck JA, et al. SRPK2: a differentially expressed SR protein-specific kinase involved in mediating the interaction and localization of pre-mRNA splicing factors in mammalian cells. J Cell Biol 1998; 140: 737-750.
35. Papoutsopoulou S, Nikolakaki E, Giannakouros T. SRPK1 and LBR protein kinases show identical substrate specificities. Biochem Biophys Res Commun 1999; 255: 602-607.
36. Stojdl DF, Bell JC. SR protein kinases: the splice of life. Biochem Cell Biol 1999; 77: 293-298.
37. Sutherland LC, Rintala-Maki ND, White RD, Morin CD. RNA binding motif (RBM) proteins: a novel family of apoptosis modulators? J Cell Biochem 2005; 94: 5-24.
38. Holmstrom TH, Eriksson JE. Phosphorylation-Based signaling in Fas receptor-mediated apoptosis. Crit Rev Immunol 2000; 20: 121-152.
39. Ruvolo PP, Deng X, May WS. Phosphorylation of Bcl2 and regulation of apoptosis. Leukemia 2001; 15: 515-522.
40. Lew DJ, Kornbluth S. Regulatory roles of cyclin dependent kinase phosphorylation in cell cycle control. Curr Opin Cell Biol 1996; 8: 795-804.
41. Morgan DO, Fisher RP, Espinoza FH, et al. Control of eukaryotic cell cycle progression by phosphorylation of cyclin-dependent kinases. Cancer J Sci Am 1998; 4Suppl 1:S77-S83.
42. Sutherland LC, Edwards SE, Cable HC, et al. LUCA-15-encoded sequence variants regulate CD95-mediated apoptosis. Oncogene 2000; 19: 3774-3781.
43. Rintala-Maki ND, Abrasonis V, Burd M, Sutherland LC. Genetic instability of RBM5/LUCA-15/H37 in MCF-7 breast carcinoma sublines may affect susceptibility to apoptosis. Cell Biochem Funct 2004; 22: 307-313.
44. Datta SR, Brunet A, Greenberg ME. Cellular survival: a play in three Akts. Genes Dev 1999; 13: 2905-2927.
45. Kitamura T, Tange T, Terasawa T, et al. Establishment and characterization of a unique human cell line that proliferates dependently on GM-CSF, IL-3, or erythropoietin. J Cell Physiol 1989; 140: 323-334.
46. Marshall RD. Glycoproteins Annu Rev Biochem 1972; 41: 673-702.
47. Treigyte G, Savickiene J, Navakauskiene R. Identification of O-and N-glycosylated nuclear proteins of HL-60 cells induced to granulocytic differentiation. Biologija 2004; 2: 49-51.
48. Saito S, Sidis Y, Mukherjee A, Xia Y, Schneyer A. Differential biosynthesis and intracellular transport of follistatin isoforms and follistatin-like-3. Endocrinology 2005; 146: 5052-5062.
49. Rondanino C, Bousser MT, Monsigny M, Roche AC. Sugar-dependent nuclear import of glycosylated proteins in living cells. Glycobiology 2003; 13: 509-519.
50. Zhen Y, Caprioli RM, Staros JV. Characterization of glycosylation sites of the epidermal growth factor receptor. Biochemistry 2003; 42: 5478-5492.
51. Guan KL, Figueroa C, Brtva TR, et al. Negative regulation of the serine/threonine kinase B-Raf by Akt. J Biol Chem 2000; 275: 27354-27359.
52. Basu S, Totty NF, Irwin MS, Sudol M, Downward J. Akt phosphorylates the Yes-associated protein, YAP, to induce interaction with 14-3-3 and attenuation of p73-mediated apoptosis. Mol Cell 2003; 11: 11-23.
53. Vellenga E, Biesma B, Meyer C, Wagteveld L, Esselink M, de Vries EG. The effects of five hematopoietic growth factors on human small cell lung carcinoma cell lines: interleukin 3 enhances the proliferation in one of the eleven cell lines. Cancer Res 1991; 51: 73-76.
54. Chalfant CE, Ogretmen B, Galadari S, Kroesen BJ, Pettus BJ, Hannun YA. FAS activation induces dephosphorylation of SR proteins; dependence on the de novo generation of ceramide and activation of protein phosphatase 1. J Biol Chem 2001; 276: 44848-44855.
55. Yang H, Sadda MR, Li M, et al. S-adenosylmethionine and its metabolite induce apoptosis in HepG2 cells: role of protein phosphatase 1 and Bcl-x(S). Hepatology 2004; 40: 221-231.