Alternative splicing of SYK regulates mitosis and cell survival

Nature Structural and Molecular Biology

Volumn 18, Issue 6, 2011, Pages 673-679

  Prinos, Panagiotis ^a   Garneau, Daniel ^a   Lucier, Jean François ^a   Gendron, Daniel ^a   Couture, Sonia ^a   Boivin, Marianne ^a   Brosseau, Jean Philippe ^a,b   Lapointe, Elvy ^a   Thibault, Philippe ^a   Durand, Mathieu ^a   Tremblay, Karine ^a   Gervais Bird, Julien ^a   Nwilati, Hanad ^a   Klinck, Roscoe ^a   Chabot, Benoit ^a   Perreault, Jean Pierre ^b   Wellinger, Raymund J ^a   Elela, Sherif Abou ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

^b UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

JANUS KINASE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE SYK;

APOPTOSIS; ARTICLE; CELL CYCLE REGULATION; CELL GROWTH; CELL SURVIVAL; CELL VIABILITY; GENE EXPRESSION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; MITOSIS; PRIORITY JOURNAL; SPLICING DEFECT;

ALTERNATIVE SPLICING; APOPTOSIS; CELL LINE, TUMOR; CELL SURVIVAL; EPIDERMAL GROWTH FACTOR; GENE EXPRESSION REGULATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MITOSIS; PROTEIN-TYROSINE KINASES;

EID: 79958812227     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2040     Document Type: Article

References (51)

1. Pan, Q., Shai, O., Lee, L.J., Frey, B.J. & Blencowe, B.J. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat. Genet. 40, 1413-1415 (2008).
2. Wang, E.T. et al. Alternative isoform regulation in human tissue transcriptomes. Nature 456, 470-476 (2008). (Pubitemid 352759009)
3. Matlin, A.J., Clark, F. & Smith, C.W. Understanding alternative splicing: towards a cellular code. Nat. Rev. Mol. Cell Biol. 6, 386-398 (2005). (Pubitemid 40637856)
4. Castle, J.C. et al. Expression of 24,426 human alternative splicing events and predicted cis regulation in 48 tissues and cell lines. Nat. Genet. 40, 1416-1425 (2008).
5. Venables, J.P. et al. Cancer-associated regulation of alternative splicing. Nat. Struct. Mol. Biol. 16, 670-676 (2009).
6. Venables, J.P. Aberrant and alternative splicing in cancer. Cancer Res. 64, 7647-7654 (2004). (Pubitemid 39446889)
7. Cooper, D.L. & Dougherty, G.J. To metastasize or not? Selection of CD44 splice sites. Nat. Med. 1, 635-637 (1995).
8. Christofk, H.R. et al. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452, 230-233 (2008). (Pubitemid 351380249)
9. Levanon, E.Y. & Sorek, R. The importance of alternative splicing in the drug discovery process. Targets 2, 109-114 (2003). (Pubitemid 40418169)
10. Iorns, E., Lord, C.J., Turner, N. & Ashworth, A. Utilizing RNA interference to enhance cancer drug discovery. Nat. Rev. Drug Discov. 6, 556-568 (2007). (Pubitemid 47019444)
11. Klinck, R. et al. Multiple alternative splicing markers for ovarian cancer. Cancer Res. 68, 657-663 (2008). (Pubitemid 351206740)
12. Venables, J.P. et al. Identification of alternative splicing markers for breast cancer. Cancer Res. 68, 9525-9531 (2008).
13. Celotto, A.M. & Graveley, B.R. Exon-specific RNAi: a tool for dissecting the functional relevance of alternative splicing. RNA 8, 718-724 (2002). (Pubitemid 34620449)
14. Villemaire, J., Dion, I., Elela, S.A. & Chabot, B. Reprogramming alternative pre-messenger RNA splicing through the use of protein-binding antisense oligonucleotides. J. Biol. Chem. 278, 50031-50039 (2003). (Pubitemid 37548839)
15. Baudot, A.D. et al. The tyrosine kinase Syk regulates the survival of chronic lymphocytic leukemia B cells through PKCdelta and proteasome-dependent regulation of Mcl-1 expression. Oncogene 28, 3261-3273 (2009).
16. Gobessi, S. et al. Inhibition of constitutive and BCR-induced Syk activation downregulates Mcl-1 and induces apoptosis in chronic lymphocytic leukemia B cells. Leukemia 23, 686-697 (2009).
17. Adams, K.W. & Cooper, G.M. Rapid turnover of mcl-1 couples translation to cell survival and apoptosis. J. Biol. Chem. 282, 6192-6200 (2007). (Pubitemid 47100899)
18. Bingle, C.D. et al. Exon skipping in Mcl-1 results in a bcl-2 homology domain 3 only gene product that promotes cell death. J. Biol. Chem. 275, 22136-22146 (2000). (Pubitemid 30621794)
19. Wang, L. et al. Alternative splicing disrupts a nuclear localization signal in spleen tyrosine kinase that is required for invasion suppression in breast cancer. Cancer Res. 63, 4724-4730 (2003). (Pubitemid 36951053)
20. Zhou, F., Hu, J., Ma, H., Harrison, M.L. & Geahlen, R.L. Nucleocytoplasmic trafficking of the Syk protein tyrosine kinase. Mol. Cell. Biol. 26, 3478-3491 (2006).
21. Shaulian, E. AP-1-the Jun proteins: oncogenes or tumor suppressors in disguise? Cell. Signal. 22, 894-899 (2010).
22. Wisdom, R., Johnson, R.S. & Moore, C. c-Jun regulates cell cycle progression and apoptosis by distinct mechanisms. EMBO J. 18, 188-197 (1999). (Pubitemid 29005035)
23. Bennett, B.L. et al. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. USA 98, 13681-13686 (2001). (Pubitemid 33115958)
24. Akgul, C. Mcl-1 is a potential therapeutic target in multiple types of cancer. Cell. Mol. Life Sci. 66, 1326-1336 (2009).
25. Michels, J., Johnson, P.W. & Packham, G. Mcl-1. Int. J. Biochem. Cell Biol. 37, 267-271 (2005). (Pubitemid 39330187)
26. Bae, J., Leo, C.P., Hsu, S.Y. & Hsueh, A.J. MCL-1S, a splicing variant of the antiapoptotic BCL-2 family member MCL-1, encodes a proapoptotic protein possessing only the BH3 domain. J. Biol. Chem. 275, 25255-25261 (2000).
27. Shieh, J.J., Liu, K.T., Huang, S.W., Chen, Y.J. & Hsieh, T.Y. Modification of alternative splicing of Mcl-1 pre-mRNA using antisense morpholino oligonucleotides induces apoptosis in basal cell carcinoma cells. J. Invest. Dermatol. 129, 2497-2506 (2009).
28. Mócsai, A., Ruland, J. & Tybulewicz, V.L. The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat. Rev. Immunol. 10, 387-402 (2010).
29. Coopman, P.J. et al. The Syk tyrosine kinase suppresses malignant growth of human breast cancer cells. Nature 406, 742-747 (2000).
30. Moroni, M. et al. Progressive loss of Syk and abnormal proliferation in breast cancer cells. Cancer Res. 64, 7346-7354 (2004). (Pubitemid 39372073)
31. Zyss, D. et al. The Syk tyrosine kinase localizes to the centrosomes and negatively affects mitotic progression. Cancer Res. 65, 10872-10880 (2005). (Pubitemid 41713355)
32. Faruki, S., Geahlen, R.L. & Asai, D.J. Syk-dependent phosphorylation of microtubules in activated B-lymphocytes. J. Cell Sci. 113, 2557-2565 (2000). (Pubitemid 30601377)
33. Peters, J.D., Furlong, M.T., Asai, D.J., Harrison, M.L. & Geahlen, R.L. Syk, activated by cross-linking the B-cell antigen receptor, localizes to the cytosol where it interacts with and phosphorylates alpha-tubulin on tyrosine. J. Biol. Chem. 271, 4755-4762 (1996). (Pubitemid 26074958)
34. Feldman, A.L. et al. Overexpression of Syk tyrosine kinase in peripheral T-cell lymphomas. Leukemia 22, 1139-1143 (2008). (Pubitemid 351833780)
35. Buchner, M. et al. Spleen tyrosine kinase is overexpressed and represents a potential therapeutic target in chronic lymphocytic leukemia. Cancer Res. 69, 5424-5432 (2009).
36. Nakashima, H. et al. Clinical significance of nuclear expression of spleen tyrosine kinase (Syk) in gastric cancer. Cancer Lett. 236, 89-94 (2006).
37. Luangdilok, S. et al. Syk tyrosine kinase is linked to cell motility and progression in squamous cell carcinomas of the head and neck. Cancer Res. 67, 7907-7916 (2007). (Pubitemid 47281387)
38. Goodman, P.A., Wood, C.M., Vassilev, A., Mao, C. & Uckun, F.M. Spleen tyrosine kinase (Syk) deficiency in childhood pro-B cell acute lymphoblastic leukemia. Oncogene 20, 3969-3978 (2001). (Pubitemid 32681602)
39. Blaustein, M. et al. Concerted regulation of nuclear and cytoplasmic activities of SR proteins by AKT. Nat. Struct. Mol. Biol. 12, 1037-1044 (2005). (Pubitemid 41746773)
40. Shin, C. & Manley, J.L. Cell signalling and the control of pre-mRNA splicing. Nat. Rev. Mol. Cell Biol. 5, 727-738 (2004). (Pubitemid 39208182)
41. Mandal, M. et al. Growth factors regulate heterogeneous nuclear ribonucleoprotein K expression and function. J. Biol. Chem. 276, 9699-9704 (2001).
42. Ashton-Beaucage, D. et al. The exon junction complex controls the splicing of MAPK and other long intron-containing transcripts in Drosophila. Cell 143, 251-262 (2010).
43. Roignant, J.Y. & Treisman, J.E. Exon junction complex subunits are required to splice Drosophila MAP kinase, a large heterochromatic gene. Cell 143, 238-250 (2010).
44. Nicke, B. et al. Involvement of MINK, a Ste20 family kinase, in Ras oncogene-induced growth arrest in human ovarian surface epithelial cells. Mol. Cell 20, 673-685 (2005). (Pubitemid 41740690)
45. Hendzel, M.J. et al. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106, 348-360 (1997). (Pubitemid 27510848)
46. Brosseau, J.P. et al. High-throughput quantification of splicing isoforms. RNA 16, 442-449 (2010).
47. Hellemans, J., Mortier, G., De Paepe, A., Speleman, F. & Vandesompele, J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8, R19 (2007).
48. Venables, J.P. et al. Multiple and specific mRNA processing targets for the major human hnRNP proteins. Mol. Cell. Biol. 28, 6033-6043 (2008).
49. Zhang, J.H., Chung, T.D. & Oldenburg, K.R. A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J. Biomol. Screen. 4, 67-73 (1999). (Pubitemid 29278954)
50. Birmingham, A. et al. Statistical methods for analysis of high-throughput RNA interference screens. Nat. Methods 6, 569-575 (2009).
51. Chung, N. et al. Median absolute deviation to improve hit selection for genome-scale RNAi screens. J. Biomol. Screen. 13, 149-158 (2008). (Pubitemid 351248688)