The gene encoding the splicing factor SF2/ASF is a proto-oncogene

Nature Structural and Molecular Biology

Volumn 14, Issue 3, 2007, Pages 185-193

  Karni, Rotem ^a   De Stanchina, Elisa ^a   Lowe, Scott W ^a   Sinha, Rahul ^a   Mu, David ^a   Krainer, Adrian R ^a  

^a Cold Spring Harbor Laboratory ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 4E; ISOPROTEIN; ONCOPROTEIN; S6 KINASE; S6 KINASE 1; SPLICING FACTOR SF2; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; CANCER GENETICS; CANCER THERAPY; CELL TRANSFORMATION; CONTROLLED STUDY; DRUG TARGETING; FIBROBLAST; GENE ACTIVITY; GENE AMPLIFICATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTO ONCOGENE; RAT; RODENT; SARCOMA; TUMOR SUPPRESSOR GENE; UPREGULATION;

ALTERNATIVE SPLICING; ANIMALS; APOPTOSIS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; EUKARYOTIC INITIATION FACTOR-4E; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HELA CELLS; HUMANS; MICE; MICE, NUDE; NEOPLASMS; NIH 3T3 CELLS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTO-ONCOGENES; RATS; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; UP-REGULATION;

MUS MUSCULUS; RODENTIA;

EID: 33847630730     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb1209     Document Type: Article

References (50)

1. Johnson, J.M. et al. Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 302, 2141-2144 (2003).
2. Black, D.L. Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 72, 291-336 (2003).
3. Mayeda, A. & Krainer, A.R. Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell 68, 365-375 (1992).
4. Cáceres, J.F., Stamm, S., Helfman, D.M. & Krainer, A.R. Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science 265, 1706-1709 (1994).
5. Xu, Q. & Lee, C. Discovery of novel splice forms and functional analysis of cancer-specific alternative splicing in human expressed sequences. Nucleic Acids Res. 31, 5635-5643 (2003).
6. Wang, Z. et al. Computational analysis and experimental validation of tumor-associated alternative RNA splicing in human cancer. Cancer Res. 63, 655-657 (2003).
7. Venables, J.P. Aberrant and alternative splicing in cancer. Cancer Res. 64, 7647-7654 (2004).
8. Venkitaraman, A.R. Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell 108, 171-182 (2002).
9. Hammes, A. et al. Two splice variants of the Wilms' tumor 1 gene have distinct functions during sex determination and nephron formation. Cell 106, 319-329 (2001).
10. Wu, J.Y., Tang, H. & Havlioglu, N. Alternative pre-mRNA splicing and regulation of programmed cell death. Prog. Mol. Subcell. Biol. 31, 153-185 (2003).
11. Ge, K. et al. Mechanism for elimination of a tumor suppressor: aberrant splicing of a brain-specific exon causes loss of function of Bin1 in melanoma. Proc. Natl. Acad. Sci. USA 96, 9689-9694 (1999).
12. Kumar, A., Baker, S.J., Lee, C.M. & Reddy, E.P. Molecular mechanisms associated with the regulation of apoptosis by the two alternatively spliced products of c-Myb. Mol. Cell. Biol. 23, 6631-6645 (2003).
13. Tennenbaum, T. et al. A splice variant of alpha 6 integrin is associated with malignant conversion in mouse skin tumorigenesis. Proc. Natl. Acad. Sci. USA 92, 7041-7045 (1995).
14. Steinman, H.A. et al. An alternative splice form of Mdm2 induces p53-independent cell growth and tumorigenesis. J. Biol. Chem. 279, 4877-4886 (2004).
15. Tockman, M.S. et al. Prospective detection of preclinical lung cancer: results from two studies of heterogeneous nuclear ribonucleoprotein A2/B1 overexpression. Clin. Cancer Res. 3, 2237-2246 (1997).
16. Ghigna, C., Moroni, M., Porta, C., Riva, S. & Biamonti, G. Altered expression of heterogenous nuclear ribonucleoproteins and SR factors in human colon adenocarcinomas. Cancer Res. 58, 5818-5824 (1998).
17. Patry, C. et al. Small interfering RNA-mediated reduction in heterogeneous nuclear ribonucleoparticule A1/A2 proteins induces apoptosis in human cancer cells but not in normal mortal cell lines. Cancer Res. 63, 7679-7688 (2003).
18. He, X., Ee, P.L., Coon, J.S. & Beck, W.T. Alternative splicing of the multidrug resistance protein 1/ATP binding cassette transporter subfamily gene in ovarian cancer creates functional splice variants and is associated with increased expression of the splicing factors PTB and SRp20. Clin. Cancer Res. 10, 4652-4660 (2004).
19. Fischer, D.C. et al. Expression of splicing factors in human ovarian cancer. Oncol. Rep. 11, 1085-1090 (2004).
20. Ghigna, C. et al. Cell motility is controlled by SF2/ASF through alternative splicing of the Ron protooncogene. Mol. Cell 20, 881-890 (2005).
21. Sinclair, C.S., Rowley, M., Naderi, A. & Couch, F.J. The 17q23 amplicon and breast cancer. Breast Cancer Res. Treat. 78, 313-322 (2003).
22. Cáceres, J.F., Screaton, G.R. & Krainer, A.R. A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev. 12, 55-66 (1998).
23. Sanford, J.R., Gray, N.K., Beckmann, K. & Cáceres, J.F. A novel role for shuttling SR proteins in mRNA translation. Genes Dev. 18, 755-768 (2004).
24. de Stanchina, E. et al. E1A signaling to p53 involves the p19(ARF) tumor suppressor. Genes Dev. 12, 2434-2442 (1998).
25. Huang, Y. & Steitz, J.A. SRprises along a messenger's journey. Mol. Cell 17, 613-615 (2005).
26. Mixon, M., Kittrell, F. & Medina, D. Expression of Brca1 and splice variant Brca1-delta11 RNA levels in mouse mammary gland during normal development and tumorigenesis. Oncogene 19, 5237-5243 (2000).
27. Sakamuro, D., Elliott, K.J., Wechsler-Reya, R. & Prendergast, G.C. BIN1 is a novel MYC-interacting protein with features of a tumour suppressor. Nat. Genet. 14, 69-77 (1996).
28. Hanahan, D. & Weinberg, R.A. The hallmarks of cancer. Cell 100, 57-70 (2000).
29. Holz, M.K., Ballif, B.A., Gygi, S.P. & Blenis, J. mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123, 569-580 (2005).
30. Waskiewicz, A.J. et al. Phosphorylation of the cap-binding protein eukaryotic translation initiation factor 4E by protein kinase Mnk1 in vivo. Mol. Cell. Biol. 19, 1871-1880 (1999).
31. Scheper, G.C. et al. The N and C termini of the splice variants of the human mitogen-activated protein kinase-interacting kinase Mnk2 determine activity and localization. Mol. Cell. Biol. 23, 5692-5705 (2003).
32. Harada, H., Andersen, J.S., Mann, M., Terada, N. & Korsmeyer, S.J. p70S6 kinase signals cell survival as well as growth, inactivating the pro-apoptotic molecule BAD. Proc. Natl. Acad. Sci. USA 98, 9666-9670 (2001).
33. Scheper, G.C., Morrice, N.A., Kleijn, M. & Proud, C.G. The mitogen-activated protein kinase signal-integrating kinase Mnk2 is a eukaryotic initiation factor 4E kinase with high levels of basal activity in mammalian cells. Mol. Cell. Biol. 21, 743-754 (2001).
34. Sjöblom, T. et al. The consensus coding sequences of human breast and colorectal cancers. Science 314, 268-274 (2006).
35. Kim, S., Shi, H., Lee, D.K. & Lis, J.T. Specific SR protein-dependent splicing substrates identified through genomic SELEX. Nucleic Acids Res. 31, 1955-1961 (2003).
36. Xu, X. et al. ASF/SF2-regulated CaMKIIdelta alternative splicing temporally reprograms excitation-contraction coupling in cardiac muscle. Cell 120, 59-72 (2005).
37. Wang, H.Y., Xu, X., Ding, J.H., Bermingham, J.R., Jr. & Fu, X.D. SC35 plays a role in T cell development and alternative splicing of CD45. Mol. Cell 7, 331-342 (2001).
38. Blanchette, M., Green, R.E., Brenner, S.E. & Rio, D.C. Global analysis of positive and negative pre-mRNA splicing regulators in Drosophila. Genes Dev. 19, 1306-1314 (2005).
39. Bjornsti, M.A. & Houghton, P.J. Lost in translation: dysregulation of cap-dependent translation and cancer. Cancer Cell 5, 519-523 (2004).
40. Topisirovic, I., Ruiz-Gutierrez, M. & Borden, K.L. Phosphorylation of the eukaryotic translation initiation factor eIF4E contributes to its transformation and mRNA transport activities. Cancer Res. 64, 8639-8642 (2004).
41. Schalm, S.S. & Blenis, J. Identification of a conserved motif required for mTOR signaling. Curr. Biol. 12, 632-639 (2002).
42. Hanks, S.K. & Hunter, T. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 9, 576-596 (1995).
43. Zender, L. et al. Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach. Cell 125, 1253-1267 (2006).
44. Kim, M. et al. Comparative oncogenomics identifies NEDD9 as a melanoma metastasis gene. Cell 125, 1269-1281 (2006).
45. DuHadaway, J.B., Sakamuro, D., Ewert, D.L. & Prendergast, G.C. Bin1 mediates apoptosis by c-Myc in transformed primary cells. Cancer Res. 61, 3151-3156 (2001).
46. Bourgeois, C.F., Lejeune, F. & Stévenin, J. Broad specificity of SR (serine/arginine) proteins in the regulation of alternative splicing of pre-messenger RNA. Prog. Nucleic Acid Res. Mol. Biol. 78, 37-88 (2004).
47. Li, X. & Manley, J.L. Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability. Cell 122, 365-378 (2005).
48. McCurrach, M.E. & Lowe, S.W. Methods for studying pro- and antiapoptotic genes in nonimmortal cells. Methods Cell Biol. 66, 197-227 (2001).
49. Stolarov, J. et al. Design of a retroviral-mediated ecdysone-inducible system and its application to the expression profiling of the PTEN tumor suppressor. Proc. Natl. Acad. Sci. USA 98, 13043-13048 (2001).
50. Karni, R., Jove, R. & Levitzki, A. Inhibition of pp60c-Src reduces Bcl-XL expression and reverses the transformed phenotype of cells overexpressing EGF and HER-2 receptors. Oncogene 18, 4654-4662 (1999).