Disturbed expression of splicing factors in renal cancer affects alternative splicing of apoptosis regulators, oncogenes, and tumor suppressors

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Piekielko Witkowska, Agnieszka ^a   Wiszomirska, Hanna ^a   Wojcicka, Anna ^a   Poplawski, Piotr ^a   Boguslawska, Joanna ^a   Tanski, Zbigniew ^b   Nauman, Alicja ^a  

^a MEDICAL CENTER FOR POSTGRADUATE EDUCATION   (Poland)

^b Regional Hospital   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS REGULATORY PROTEIN; CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 1; CASPASE 9; CELL PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A1; MESSENGER RNA; PROTEIN 9G8; PROTEIN ASF; PROTEIN RON; PROTEIN SC35; PROTEIN SF2; PROTEIN SRP20; PROTEIN SRP40; PROTEIN SRP55; PROTEIN SRP75; RAC1 PROTEIN; SERINE ARGININE RICH PROTEIN; SPLICING FACTOR; TRANSCRIPTION FACTOR GLI1; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; CANCER GROWTH; CANCER TISSUE; CARCINOGENESIS; CLINICAL ARTICLE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE FUNCTION; HUMAN; HUMAN TISSUE; KIDNEY CARCINOMA; ONCOGENE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SPLICING DEFECT; WESTERN BLOTTING; APOPTOSIS; GENETICS; KIDNEY TUMOR; PATHOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TUMOR SUPPRESSOR GENE;

ALTERNATIVE SPLICING; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, RENAL CELL; GENES, TUMOR SUPPRESSOR; HUMANS; KIDNEY NEOPLASMS; ONCOGENES; POLYMERASE CHAIN REACTION;

EID: 78149455880     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013690     Document Type: Article

References (72)

1. Schöffski P, Dumez H, Clement P, Hoeben A, Prenen H, et al. (2006) Emerging role of tyrosine kinase inhibitors in the treatment of advanced renal cell cancer: a review. Ann Oncol 17: 1185-1196.
2. Ljungberg B, Hanbury DC, Kuczyk MA, Merseburger AS, Mulders PFA, et al. (2009), on behalf of the European Association of Urology (EAU) (2009) Guidelines on renal cell carcinoma. Available on the website of the European Association of Urology (accessed 2010) http://www.uroweb.org/fileadmin/tx_eauguidelines/2009/Full/RCC.pdf.
3. Fackenthal JD, Godley LA (2008) Aberrant RNA splicing and its functional consequences in cancer cells. Dis Model Mech 1: 37-42.
4. Piekielko-Witkowska A, Master A, Wojcicka A, Boguslawska J, Brozda I, et al. (2009) Disturbed expression of type 1 iodothyronine deiodinase splice variants in human renal cancer. Thyroid 19: 1105-1113.
5. Gereben B, Bianco AC (2009) Covering the base-pairs in iodothyronine deiodinase-1 biology: holes remain in the lineup. Thyroid 19: 1027-1029.
6. Master A, Wójcicka A, Piekiełko-Witkowska A, Bogusławska J, Popławski P, et al. (2010) Untranslated regions of thyroid hormone receptor beta 1 mRNA are impaired in human clear cell renal cell carcinoma. Biochim Biophys Acta 1802: pp 995-1005.
7. Kempkensteffen C, Hinz S, Johannsen M, Krause H, Magheli A, et al. (2009) Expression of Mcl-1 splicing variants in clear-cell renal cancer and their correlation with histopathological parameters and prognosis. Tumour Biol 30: 73-79.
8. Shiina H, Igawa M, Breault J, Ribeiro-Filho L, Pookot D, et al. (2003) The human T-cell factor-4 gene splicing isoforms, Wnt signal pathway, and apoptosis in renal cell carcinoma. Clin Cancer Res 9: 2121-2132.
9. Mahotka C, Krieg T, Krieg A, Wenzel M, Suschek CV, et al. (2002) Distinct in vivo expression patterns of survivin splice variants in renal cell carcinomas. Int J Cancer 100: 30-36.
10. Audebert M, Chevillard S, Levalois C, Gyapay G, Vieillefond A, et al. (2000) Alterations of the DNA repair gene OGG1 in human clear cell carcinomas of the kidney. Cancer Res 60: 4740-4744.
11. Long JC, Caceres JF (2009) The SR protein family of splicing factors: master regulators of gene expression. Biochem J 417: 15-27.
12. He Y, Smith R (2009) Nuclear functions of heterogeneous nuclear ribonucleo-proteins A/B. Cel Mol Life Sci 66: 1239-1256.
13. Ca ́ceres JF, Stamm S, Helfman DM, Krainer AR (1994) Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science 265: 1706-1709.
14. Goncalves V, Matos P, Jordan P (2009) Antagonistic SR proteins regulate alternative splicing of tumor-related Rac1b downstream of the PI3-kinase and Wnt pathways. Hum Mol Genet 18: 3696-3707.
15. Expert-Bezancon A, Sureau A, Durosay P, Salesse R, Groeneveld H, et al. (2004) hnRNP A1 and the SR proteins ASF/SF2 and SC35 have antagonistic functions in splicing of beta-tropomyosin exon 6B. J Biol Chem 279: 38249-38259.
16. Venables JP (2006) Unbalanced alternative splicing and its significance in cancer. Bioessays 28: 378-386.
17. Brinkman BM (2004) Splice variants as cancer biomarkers. Clin Biochem 37: 584-594.
18. Karni R, de Stanchina E, Lowe SW, Sinha R, Mu D, et al. (2007) The gene encoding the splicing factor SF2/ASF is a proto-oncogene. Nat Struct Mol Biol 14: 185-193.
19. Ghigna C, Giordano S, Shen H, Benvenuto F, Castiglioni F, et al. (2005) Cell motility is controlled by SF2/ASF through alternative splicing of the Ron protooncogene. Mol Cell 20: 881-890.
20. Schwerk C, Schulze-Osthoff K (2005) Regulation of apoptosis by alternative pre-mRNA splicing. Mol Cell 19: 1-13.
21. Lopez-Beltran A, Scarpelli M, Montironi R, Kirkali Z (2006) 2004 WHO classification of the renal tumors of the adults. Eur Urol 49: 798-805.
22. Massiello A, Chalfant CE (2006) SRp30a (ASF/SF2) regulates the alternative splicing of Caspase-9 pre-mRNA and is required for ceramide-responsiveness. J Lipid Res 47: 892-897.
23. Gaur S, Shively JE, Yen Y, Gaur RK (2008) Altered splicing of CEACAM1 in breast cancer: identification of regulatory sequences that control splicing of CEACAM1 into long or short cytoplasmic domain isoforms. Mol Cancer 28: 7:46.
24. Jordan P, Brazåo R, Boavida MG, Gespach C, Chastre E (1999) Cloning of a novel human Rac1b splice variant with increased expression in colorectal tumors. Oncogene 18: 6835-6839.
25. Shimokawa T, Tostar U, Lauth M, Palaniswamy R, Kasper M, et al. (2008) Novel human glioma-associated oncogene 1 (GLI1) splice variants reveal distinct mechanisms in the terminal transduction of the hedgehog signal. J Biol Chem 283: 14345-14354.
26. Cartegni L, Wang J, Zhu Z, Zhang MQ, Krainer AR (2003) ESEfinder: A web resource to identify exonic splicing enhancers. Nucleic Acids Res 31: 3568-3571.
27. Smith P J, Zhang C, Wang J, Chew S L, Zhang M Q, et al. (2006) An increased specificity score matrix for the prediction of SF2/ASF-specific exonic splicing enhancers. Hum Mol Genet 15: 2490-2508.
28. Wei T Corrplot: visualization of a correlation matrix. R package version 0.2-0. Available on Comprehensive R Archive Network website (accessed 2010): http://CRAN.R-project.org/package=corrplot 2010.
29. Chandradas S, Deikus G, Tardos JG, Bogdanov VY (2010) Antagonistic roles of four SR proteins in the biosynthesis of alternatively spliced tissue factor transcripts in monocytic cells. J Leukoc Biol 87: 147-152.
30. Hanamura A, Ca ́ceres JF, Mayeda A, Franza BR Jr., Krainer AR (1998) Regulated tissue-specific expression of antagonistic pre-mRNA splicing factors. RNA 4: 430-444.
31. Takahashi M, Rhodes DR, Furge KA, Kanayama H, Kagawa S, et al. (2001) Gene expression profiling of clear cell renal cell carcinoma: gene identification and prognostic classification. Proc Natl Acad Sci USA 98: 9754-9759.
32. Sültmann H, von Heydebreck A, Huber W, Kuner R, Buness A, et al. (2005) Gene expression in kidney cancer is associated with cytogenetic abnormalities, metastasis formation, and patient survival. Clin Cancer Res 11: 646-655.
33. Zhao H, Ljungberg B, Grankvist K, Rasmuson T, Tibshirani R, et al. (2006) Gene expression profiling predicts survival in conventional renal cell carcinoma. PLoS Med 3(1): e13.
34. Klein CA, Blankenstein TJ, Schmidt-Kittler O, Petronio M, Polzer B, et al. (2002) Genetic heterogeneity of single disseminated tumour cells in minimal residual cancer. Lancet 360: 683-689.
35. Perou CM, Sørlie T, Eisen MB, van de Rijn M, Jeffrey SS, et al. (2000) Molecular portraits of human breast tumours. Nature 406: 747-752.
36. Ahram M, Best CJ, Flaig MJ, Gillespie JW, Leiva IM, et al. (2002) Proteomic analysis of human prostate cancer. Mol Carcinog 33: 9-15.
37. Chen X, Cheung ST, So S, Fan ST, Barry C, et al. (2002) Gene expression patterns in human liver cancers. Mol Biol Cell 13: 1929-1939.
38. Warrenfeltz S, Pavlik S, Datta S, Kraemer ET, Benigno B, et al. (2004) Gene expression profiling of epithelial ovarian tumours correlated with malignant potential. Mol Cancer 7: 3: 27.
39. Mole S, McFarlane M, Chuen-Im T, Milligan SG, Millan D, et al. (2009) RNA splicing factors regulated by HPV16 during cervical tumour progression. J Pathol 219: 383-391.
40. Tun HW, Marlow LA, von Roemeling CA, Cooper SJ, Kreinest P, et al. (2010) Pathway signature and cellular differentiation in clear cell renal cell carcinoma. PLoS One 5(5): e10696.
41. Piekiełko-Witkowska A (2006) Phosphorylation of serine-arginine rich proteins- pleiotropic effect of one type posttranslational modification. Advances in Biochemistry (Poste {ogonek}py Biochemii, Polish; abstract in English) 52: 383-389.
42. Patel NA, Kaneko S, Apostolatos HS, Bae SS, Watson JE, et al. (2005) Molecular and genetic studies imply Akt-mediated signaling promotes protein kinase CbetaII alternative splicing via phosphorylation of serine/arginine-rich splicing factor SRp40. J Biol Chem 280: 14302-14309.
43. Porta C, Figlin RA (2009) Phosphatidylinositol-3-kinase/Akt signaling pathway and kidney cancer, and the therapeutic potential of phosphatidylinositol-3-kinase/Akt inhibitors. J Urol 182: 2569-2577.
44. Gagne ́ JP, Hunter JM, Labrecque B, Chabot B, Poirier GG (2003) A proteomic approach to the identification of heterogeneous nuclear ribonucleoproteins as a new family of poly(ADP-ribose)-binding proteins. Biochem J 371: 331-340.
45. Malanga M, Czubaty A, Girstun A, Staron K, Althaus FR (2008) Poly(ADP-ribose) binds to the splicing factor ASF/SF2 and regulates its phosphorylation by DNA topoisomerase I. J Biol Chem 283: 19991-19998.
46. Ji Y, Tulin AV (2009) Poly(ADP-ribosyl)ation of heterogeneous nuclear ribonucleoproteins modulates splicing. Nucleic Acids Res 37: 3501-3513.
47. McLaren J, Boulikas T, Vamvakas S (1994) Induction of poly(ADP-ribosyl)ation in the kidney after in vivo application of renal carcinogens. Toxicology 88: 101-12.
48. Matafora V, D'Amato A, Mori S, Blasi F, Bachi A (2009) Proteomics analysis of nucleolar SUMO-1 target proteins upon proteasome inhibition. Mol Cell Proteomics 8: 2243-2255.
49. Liu Q, Dreyfuss G (1995) In vivo and in vitro arginine methylation of RNA-binding proteins. Mol Cell Biol 15: 2800-2808.
50. Sinha R, Allemand E, Zhang Z, Karni R, Myers MP, et al. (2010) Arginine methylation controls the subcellular localization and functions of the oncoprotein splicing factor SF2/ASF. Mol Cell Biol 30: 2762-2774.
51. Hartmann B, Valcárcel J (2009) Decrypting the genome's alternative messages. Curr Opin Cell Biol 21: 377-386.
52. Merdzhanova G, Edmond V, De Seranno S, Van den Broeck A, Corcos L, et al. (2008) E2F1 controls alternative splicing pattern of genes involved in apoptosis through upregulation of the splicing factor SC35. Cell Death Differ 15: 1815-1823.
53. Turowska O, Nauman A, Pietrzak M, Popławski P, Master A, et al. (2007) Overexpression of E2F1 in clear cell renal cell carcinoma: a potential impact of erroneous regulation by thyroid hormone nuclear receptors. Thyroid 17: 1039-1048.
54. Zhou MI, Foy RL, Chitalia VC, Zhao J, Panchenko MV, et al. (2005) Jade-1, a candidate renal tumor suppressor that promotes apoptosis. Proc Natl Acad Sci U S A 102: 11035-11040.
55. Mizutani Y, Nakanishi H, Li YN, Matsubara H, Yamamoto K, et al. (2007) Overexpression of XIAP expression in renal cell carcinoma predicts a worse prognosis. Int J Oncol 30: 919-925.
56. Fernández-Zapico ME (2008) Primers on molecular pathways GLI: more than just Hedgehog? Pancreatology 8: 227-229.
57. Dormoy V, Danilin S, Lindner V, Thomas L, Rothhut S, et al. (2009) The sonic hedgehog signaling pathway is reactivated in human renal cell carcinoma and plays orchestral role in tumor growth. Mol Cancer 16: 8:123.
58. Obrink B (2008) On the role of CEACAM1 in cancer. Lung Cancer 60: 309-312.
59. Kleinerman DI, Troncoso P, Lin S-H, Pister LL, Sherwood ER, et al. (1995) Consistent expression of an epithelial cell adhesion molecule (C-CAM) during prostate development and loss of expression in prostate cancer: implication as a tumor supressor. Cancer Res 55: 1215-1220.
60. Kleinerman DI, Dinney CP, Zhang WW, Lin SH, Van NT, et al. (1996) Suppression of human bladder cancer growth by increased expression of C-CAM1 gene in an orthotopic model. Cancer Res 56: 3431-3435.
61. Luo W, Wood CG, Earley K, Hung MC, Lin SH (1997) Suppression of tumorigenicity of breast cancer cells by an epithelial cell adhesion molecule (C-CAM1): the adhesion and growth suppression are mediated by different domains. Oncogene 14: 1697-1704.
62. Müller MM, Klaile E, Vorontsova O, Singer BB, Obrink B (2009) Homophilic adhesion and CEACAM1-S regulate dimerization of CEACAM1-L and recruitment of SHP-2 and c-Src. J Cell Biol 187: 569-581.
63. Kammerer R, Riesenberg R, Weiler C, Lohrmann J, Schleypen J, et al. (2004) The tumour suppressor gene CEACAM1 is completely but reversibly downregulated in renal cell carcinoma. J Pathol 204: 258-267.
64. Benvenuti S, Comoglio PM (2007) The MET receptor tyrosine kinase in invasion and metastasis. J Cell Physiol 213: 316-325.
65. Bardella C, Costa B, Maggiora P, Patane' S, Olivero M, et al. (2004) Truncated RON tyrosine kinase drives tumor cell progression and abrogates cell-cell adhesion through E-cadherin transcriptional repression. Cancer Res 64: 5154-5161.
66. Novara G, Martignoni G, Artibani W, Ficarra V (2007) Grading systems in renal cell carcinoma. J Urol 177: 430-436.
67. Zhou YQ, He C, Chen YQ, Wang D, Wang MH (2003) Altered expression of the RON receptor tyrosine kinase in primary human colorectal adenocarcino-mas: generation of different splicing RON variants and their oncogenic potential. Oncogene 2: 186-197.
68. Bosco EE, Mulloy JC, Zheng Y (2009) Rac1 GTPase: a ''Rac'' of all trades. Cell Mol Life Sci 66: 370-374.
69. Singh A, Karnoub AE, Palmby TR, Lengyel E, Sondek J, et al. (2004) Rac1b, a tumor associated, constitutively active Rac1 splice variant, promotes cellular transformation. Oncogene 23: 9369-9380.
70. Matos P, Jordan P (2008) Increased Rac1b expression sustains colorectal tumor cell survival. Mol Cancer Res 6: 1178-1184.
71. Engers R, Springer E, Michiels F, Collard JG, Gabbert HE (2001) Rac affects invasion of human renal cell carcinomas by up-regulating tissue inhibitor of metalloproteinases (TIMP)-1 and TIMP-2 expression. J Biol Chem 276: 41889-41897.
72. Patry C, Bouchard L, Labrecque P, Gendron D, Lemieux B, et al. (2003) Small interfering RNA-mediated reduction in heterogeneous nuclear ribonucleoparti-cule A1/A2 proteins induces apoptosis in human cancer cells but not in normal mortal cell lines. Cancer Res 63: 7679-7688.