SRSF2 promotes splicing and transcription of exon 11 included isoform in Ron proto-oncogene

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1839, Issue 11, 2014, Pages 1132-1140

  Moon, Heegyum ^a   Cho, Sunghee ^a   Loh, Tiing Jen ^a   Oh, Hyun Kyung ^a   Jang, Ha Na ^a   Zhou, Jianhua ^b   Kwon, Young Soo ^c   Liao, D Joshua ^d   Jun, Youngsoo ^a   Eom, Soohyun ^a   Ghigna, Claudia ^e   Biamonti, Giuseppe ^e   Green, Michael R ^f   Zheng, Xuexiu ^a   Shen, Haihong ^a  

^a Gwangju Institute of Science and Technology (GIST)   (South Korea)

^b NANTONG UNIVERSITY   (China)

^c Sejong University   (South Korea)

^d UNIVERSITY OF MINNESOTA   (United States)

^e CNR   (Italy)

^f UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Exon 11 inclusion; Pre mRNA splicing; Proto oncogene; Ron; SRSF2; Transcription

Indexed keywords

MESSENGER RNA PRECURSOR; ISOENZYME; NUCLEAR PROTEIN; PROTEIN TYROSINE KINASE; RIBONUCLEOPROTEIN; RON PROTEIN; SRSF2 PROTEIN, HUMAN;

ARTICLE; EXON; GENE; GENE EXPRESSION; INTRON; MOLECULAR INTERACTION; MUTATIONAL ANALYSIS; PROTO ONCOGENE; RON PROTO ONCOGENE; SEQUENCE ANALYSIS; SRSF2 GENE; TRANSCRIPTION INITIATION; CELL CULTURE; GENETIC TRANSCRIPTION; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; PHYSIOLOGY; RNA SPLICING;

CELLS, CULTURED; EXONS; HELA CELLS; HUMANS; ISOENZYMES; NUCLEAR PROTEINS; PROTO-ONCOGENES; RECEPTOR PROTEIN-TYROSINE KINASES; RIBONUCLEOPROTEINS; RNA SPLICING; TRANSCRIPTION, GENETIC;

EID: 84907494747     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2014.09.003     Document Type: Article

References (43)

1. Ronsin C., Muscatelli F., Mattei M.G., Breathnach R. A novel putative receptor protein tyrosine kinase of the met family. Oncogene 1993, 8:1195-1202.
2. Gaudino G., Follenzi A., Naldini L., Collesi C., Santoro M., Gallo K.A., Godowski P.J., Comoglio P.M. RON is a heterodimeric tyrosine kinase receptor activated by the HGF homologue MSP. EMBO J. 1994, 13:3524-3532.
3. Angeloni D., Danilkovitch-Miagkova A., Ivanov S.V., Breathnach R., Johnson B.E., Leonard E.J., Lerman M.I. Gene structure of the human receptor tyrosine kinase RON and mutation analysis in lung cancer samples. Gene Chromosome Cancer 2000, 29:147-156.
4. Danilkovitch A., Leonard E.J. Kinases involved in MSP/RON signaling. J. Leukoc. Biol. 1999, 65:345-348.
5. Longati P., Bardelli A., Ponzetto C., Naldini L., Comoglio P.M. Tyrosines1234-1235 are critical for activation of the tyrosine kinase encoded by the MET proto-oncogene (HGF receptor). Oncogene 1994, 9:49-57.
6. Iwama A., Yamaguchi N., Suda T. STK/RON receptor tyrosine kinase mediates both apoptotic and growth signals via the multifunctional docking site conserved among the HGF receptor family. EMBO J. 1996, 15:5866-5875.
7. Logan-Collins J., Thomas R.M., Yu P., Jaquish D., Mose E., French R., Stuart W., McClaine R., Aronow B., Hoffman R.M., Waltz S.E., Lowy A.M. Silencing of RON receptor signaling promotes apoptosis and gemcitabine sensitivity in pancreatic cancers. Cancer Res. 2010, 70:1130-1140.
8. Maggiora P., Marchio S., Stella M.C., Giai M., Belfiore A., De Bortoli M., Di Renzo M.F., Costantino A., Sismondi P., Comoglio P.M. Overexpression of the RON gene in human breast carcinoma. Oncogene 1998, 16:2927-2933.
9. Wang M.H., Yao H.P., Zhou Y.Q. Oncogenesis of RON receptor tyrosine kinase: a molecular target for malignant epithelial cancers. Acta Pharmacol. Sin. 2006, 27:641-650.
10. Lu Y., Yao H.P., Wang M.H. Multiple variants of the RON receptor tyrosine kinase: biochemical properties, tumorigenic activities, and potential drug targets. Cancer Lett. 2007, 257:157-164.
11. Collesi C., Santoro M.M., Gaudino G., Comoglio P.M. A splicing variant of the RON transcript induces constitutive tyrosine kinase activity and an invasive phenotype. Mol. Cell. Biol. 1996, 16:5518-5526.
12. Ghigna C., Giordano S., Shen H., Benvenuto F., Castiglioni F., Comoglio P.M., Green M.R., Riva S., Biamonti G. Cell motility is controlled by SF2/ASF through alternative splicing of the Ron protooncogene. Mol. Cell 2005, 20:881-890.
13. Bonomi S., di Matteo A., Buratti E., Cabianca D.S., Baralle F.E., Ghigna C., Biamonti G. HnRNP A1 controls a splicing regulatory circuit promoting mesenchymal-to-epithelial transition. Nucleic Acids Res. 2013, 41:8665-8679.
14. Golan-Gerstl R., Cohen M., Shilo A., Suh S.S., Bakacs A., Coppola L., Karni R. Splicing factor hnRNP A2/B1 regulates tumor suppressor gene splicing and is an oncogenic driver in glioblastoma. Cancer Res. 2011, 71:4464-4472.
15. Lefave C.V., Squatrito M., Vorlova S., Rocco G.L., Brennan C.W., Holland E.C., Pan Y.X., Cartegni L. Splicing factor hnRNPH drives an oncogenic splicing switch in gliomas. EMBO J. 2011, 30:4084-4097.
16. Keren H., Lev-Maor G., Ast G. Alternative splicing and evolution: diversification, exon definition and function. Nat. Rev. Genet. 2010, 11:345-355.
17. Grabowski P.J., Black D.L. Alternative RNA splicing in the nervous system. Prog. Neurobiol. 2001, 65:289-308.
18. David C.J., Manley J.L. Alternative pre-mRNA splicing regulation in cancer: pathways and programs unhinged. Genes Dev. 2010, 24:2343-2364.
19. Lee J., Zhou J., Zheng X., Cho S., Moon H., Loh T.J., Jo K., Shen H. Identification of a novel cis-element that regulates alternative splicing of Bcl-x pre-mRNA. Biochem. Biophys. Res. Commun. 2012, 420:467-472.
20. Cho S., Moon H., Yang X., Zhou J., Kim H.R., Shin M.G., Loh T.J., Zheng X., Shen H. Validation of trans-acting elements that promote exon 7 skipping of SMN2 in SMN2-GFP stable cell line. Biochem. Biophys. Res. Commun. 2012, 423:531-535.
21. Busch A., Hertel K.J. Evolution of SR protein and hnRNP splicing regulatory factors. Wiley Interdiscip. Rev. RNA 2012, 3:1-12.
22. Han S.P., Tang Y.H., Smith R. Functional diversity of the hnRNPs: past, present and perspectives. Biochem. J. 2010, 430:379-392.
23. Graveley B.R. Sorting out the complexity of SR protein functions. RNA 2000, 6:1197-1211.
24. Blencowe B.J., Bowman J.A., McCracken S., Rosonina E. SR-related proteins and the processing of messenger RNA precursors. Biochem. Cell Biol. 1999, 77:277-291.
25. Long J.C., Caceres J.F. The SR protein family of splicing factors: master regulators of gene expression. Biochem. J. 2009, 417:15-27.
26. Wu J.Y., Maniatis T. Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell 1993, 75:1061-1070.
27. Qian W., Liang H., Shi J., Jin N., Grundke-Iqbal I., Iqbal K., Gong C.X., Liu F. Regulation of the alternative splicing of tau exon 10 by SC35 and Dyrk1A. Nucleic Acids Res. 2011, 39:6161-6171.
28. Apostolatos H., Apostolatos A., Vickers T., Watson J.E., Song S., Vale F., Cooper D.R., Sanchez-Ramos J., Patel N.A. Vitamin A metabolite, all-trans-retinoic acid, mediates alternative splicing of protein kinase C deltaVIII (PKCdeltaVIII) isoform via splicing factor SC35. J. Biol. Chem. 2010, 285:25987-25995.
29. Meshorer E., Bryk B., Toiber D., Cohen J., Podoly E., Dori A., Soreq H. SC35 promotes sustainable stress-induced alternative splicing of neuronal acetylcholinesterase mRNA. Mol. Psychiatry 2005, 10:985-997.
30. Xiao R., Sun Y., Ding J.H., Lin S., Rose D.W., Rosenfeld M.G., Fu X.D., Li X. Splicing regulator SC35 is essential for genomic stability and cell proliferation during mammalian organogenesis. Mol. Cell. Biol. 2007, 27:5393-5402.
31. Lin S., Coutinho-Mansfield G., Wang D., Pandit S., Fu X.D. The splicing factor SC35 has an active role in transcriptional elongation. Nat. Struct. Mol. Biol. 2008, 15:819-826.
32. Sureau A., Gattoni R., Dooghe Y., Stevenin J., Soret J. SC35 autoregulates its expression by promoting splicing events that destabilize its mRNAs. EMBO J. 2001, 20:1785-1796.
33. Ji X., Zhou Y., Pandit S., Huang J., Li H., Lin C.Y., Xiao R., Burge C.B., Fu X.D. SR proteins collaborate with 7SK and promoter-associated nascent RNA to release paused polymerase. Cell 2013, 153:855-868.
34. Mo S., Ji X., Fu X.D. Unique role of SRSF2 in transcription activation and diverse functions of the SR and hnRNP proteins in gene expression regulation. Transcription 2013, 4.
35. Cartegni L., Wang J., Zhu Z., Zhang M.Q., Krainer A.R. ESEfinder: a web resource to identify exonic splicing enhancers. Nucleic Acids Res. 2003, 31:3568-3571.
36. Pandit S., Zhou Y., Shiue L., Coutinho-Mansfield G., Li H., Qiu J., Huang J., Yeo G.W., Ares M., Fu X.D. Genome-wide analysis reveals SR protein cooperation and competition in regulated splicing. Mol. Cell 2013, 50:223-235.
37. Daubner G.M., Clery A., Jayne S., Stevenin J., Allain F.H. A syn-anti conformational difference allows SRSF2 to recognize guanines and cytosines equally well. EMBO J. 2012, 31:162-174.
38. Qian W., Iqbal K., Grundke-Iqbal I., Gong C.X., Liu F. Splicing factor SC35 promotes tau expression through stabilization of its mRNA. FEBS Lett. 2011, 585:875-880.
39. Sharma S., Liao W., Zhou X., Wong D.T., Lichtenstein A. Exon 11 skipping of E-cadherin RNA downregulates its expression in head and neck cancer cells. Mol. Cancer Ther. 2011, 10:1751-1759.
40. Montes M., Cloutier A., Sanchez-Hernandez N., Michelle L., Lemieux B., Blanchette M., Hernandez-Munain C., Chabot B., Sune C. TCERG1 regulates alternative splicing of the Bcl-x gene by modulating the rate of RNA polymerase II transcription. Mol. Cell. Biol. 2012, 32:751-762.
41. Fischer D.C., Noack K., Runnebaum I.B., Watermann D.O., Kieback D.G., Stamm S., Stickeler E. Expression of splicing factors in human ovarian cancer. Oncol. Rep. 2004, 11:1085-1090.
42. Piekielko-Witkowska A., Wiszomirska H., Wojcicka A., Poplawski P., Boguslawska J., Tanski Z., Nauman A. Disturbed expression of splicing factors in renal cancer affects alternative splicing of apoptosis regulators, oncogenes, and tumor suppressors. PLoS ONE 2010, 5:e13690.
43. Yoshida K., Ogawa S. Splicing factor mutations and cancer. Wiley Interdiscip. Rev. RNA 2014, 5:445-459.