Ceramide modulates pre-mRNA splicing to restore the expression of wild-type tumor suppressor p53 in deletion-mutant cancer cells

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1841, Issue 11, 2014, Pages 1571-1580

  Patwardhan, Gauri A ^a   Hosain, Salman B ^a   Liu, David X ^a,d   Khiste, Sachin K ^a   Zhao, Yunfeng ^b   Bielawski, Jacek ^c   Jazwinski, S Michal ^d   Liu, Yong Yu ^a  

^a UNIVERSITY OF LOUISIANA AT MONROE   (United States)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^d TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer; Ceramide; p53 mutant; Pre mRNA splicing; Restoration; SRSF1

Indexed keywords

CERAMIDE; MESSENGER RNA; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN BAX; PROTEIN P21; PROTEIN P53; SERINE ARGININE RICH PROTEIN; SERINE ARGININE RICH SPLICING FACTOR 1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL DEATH; CELL GROWTH; CELL NUCLEUS; CELL SURVIVAL; CELL VIABILITY; CODON; CONTROLLED STUDY; CYTOTOXICITY; DELETION MUTANT; DNA DAMAGE; ENZYME ACTIVATION; EPIGENETICS; EXON; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SILENCING; GENE TRANSLOCATION; GLYCOSYLATION; HETEROZYGOSITY; HUMAN; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; OVARIAN CANCER CELL LINE; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; RNA SPLICING;

EID: 84907789796     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2014.08.017     Document Type: Article

References (63)

1. D.P. Lane Cancer. p53, guardian of the genome Nature 358 1992 15 16
2. R. Brosh, and V. Rotter When mutants gain new powers: news from the mutant p53 field Nat. Rev. Cancer 9 2009 701 713
3. M. Hollstein, D. Sidransky, B. Vogelstein, and C.C. Harris p53 mutations in human cancers Science 253 1991 49 53
4. M.S. Greenblatt, W.P. Bennett, M. Hollstein, and C.C. Harris Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis Cancer Res. 54 1994 4855 4878
5. A. Petitjean, M.I. Achatz, A.L. Borresen-Dale, P. Hainaut, and M. Olivier TP53 mutations in human cancers: functional selection and impact on cancer prognosis and outcomes Oncogene 26 2007 2157 2165
6. K.G. Wiman Pharmacological reactivation of mutant p53: from protein structure to the cancer patient Oncogene 29 2010 4245 4252
7. F. Chen, W. Wang, and W.S. El-Deiry Current strategies to target p53 in cancer Biochem. Pharmacol. 80 2010 724 730
8. Y.Y. Liu Resuscitating wild-type p53 expression by disrupting ceramide glycosylation: a novel approach to target mutant p53 tumors Cancer Res. 71 2011 6295 6299
9. A.G. Zeimet, and C. Marth Why did p53 gene therapy fail in ovarian cancer? Lancet Oncol. 4 2003 415 422
10. Y.A. Hannun, and L.M. Obeid Principles of bioactive lipid signalling: lessons from sphingolipids Nat. Rev. Mol. Cell Biol. 9 2008 139 150
11. E. Alesse, F. Zazzeroni, A. Angelucci, G. Giannini, L. Di Marcotullio, and A. Gulino The growth arrest and downregulation of c-myc transcription induced by ceramide are related events dependent on p21 induction, Rb underphosphorylation and E2F sequestering Cell Death Differ. 5 1998 381 389
12. W.H. Kim, K.H. Kang, M.Y. Kim, and K.H. Choi Induction of p53-independent p21 during ceramide-induced G1 arrest in human hepatocarcinoma cells Biochem. Cell Biol. 78 2000 127 135
13. G.A. Patwardhan, and Y.Y. Liu Sphingolipids and expression regulation of genes in cancer Prog. Lipid Res. 50 2011 104 114
14. Y.Y. Liu, J.Y. Yu, D. Yin, G.A. Patwardhan, V. Gupta, Y. Hirabayashi, W.M. Holleran, A.E. Giuliano, S.M. Jazwinski, V. Gouaze-Andersson, D.P. Consoli, and M.C. Cabot A role for ceramide in driving cancer cell resistance to doxorubicin FASEB J. 22 2008 2541 2551
15. D. Wu, M. Marko, K. Claycombe, K.E. Paulson, and S.N. Meydani Ceramide-induced and age-associated increase in macrophage COX-2 expression is mediated through up-regulation of NF-kappa B activity J. Biol. Chem. 278 2003 10983 10992
16. B. Ogretmen, J.M. Kraveka, D. Schady, J. Usta, Y.A. Hannun, and L.M. Obeid Molecular mechanisms of ceramide-mediated telomerase inhibition in the A549 human lung adenocarcinoma cell line J. Biol. Chem. 276 2001 32506 32514
17. C.E. Chalfant, K. Rathman, R.L. Pinkerman, R.E. Wood, L.M. Obeid, B. Ogretmen, and Y.A. Hannun De novo ceramide regulates the alternative splicing of caspase 9 and Bcl-x in A549 lung adenocarcinoma cells. Dependence on protein phosphatase-1 J. Biol. Chem. 277 2002 12587 12595
18. A. Massiello, and C.E. Chalfant SRp30a (ASF/SF2) regulates the alternative splicing of caspase-9 pre-mRNA and is required for ceramide-responsiveness J. Lipid Res. 47 2006 892 897
19. Y.Y. Liu, G.A. Patwardhan, K. Bhinge, V. Gupta, X. Gu, and S.M. Jazwinski Suppression of glucosylceramide synthase restores p53-dependent apoptosis in mutant p53 cancer cells Cancer Res. 71 2011 2276 2285
20. B. Ogretmen, and A.R. Safa Expression of the mutated p53 tumor suppressor protein and its molecular and biochemical characterization in multidrug resistant MCF-7/Adr human breast cancer cells Oncogene 14 1997 499 506
21. G.A. Patwardhan, Q.J. Zhang, D. Yin, V. Gupta, J. Bao, C.E. Senkal, B. Ogretmen, M.C. Cabot, G.V. Shah, P.W. Sylvester, S.M. Jazwinski, and Y.Y. Liu A new mixed-backbone oligonucleotide against glucosylceramide synthase sensitizes multidrug-resistant tumors to apoptosis PLoS ONE 4 2009 e6938
22. U. Munoz, J.E. Puche, R. Hannivoort, U.E. Lang, M. Cohen-Naftaly, and S.L. Friedman Hepatocyte growth factor enhances alternative splicing of the Kruppel-like factor 6 (KLF6) tumor suppressor to promote growth through SRSF1 Mol. Cancer Res. 10 2012 1216 1227
23. R.D. Phair, and T. Misteli High mobility of proteins in the mammalian cell nucleus Nature 404 2000 604 609
24. J. Bielawski, Z.M. Szulc, Y.A. Hannun, and A. Bielawska Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry Methods 39 2006 82 91
25. J. Bielawski, J.S. Pierce, J. Snider, B. Rembiesa, Z.M. Szulc, and A. Bielawska Comprehensive quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry Methods Mol. Biol. 579 2009 443 467
26. Y.Y. Liu, V. Gupta, G.A. Patwardhan, K. Bhinge, Y. Zhao, J. Bao, H. Mehendale, M.C. Cabot, Y.T. Li, and S.M. Jazwinski Glucosylceramide synthase upregulates MDR1 expression in the regulation of cancer drug resistance through cSrc and beta-catenin signaling Mol. Cancer 9 2010 145
27. E. Klenova, I. Chernukhin, T. Inoue, S. Shamsuddin, and J. Norton Immunoprecipitation techniques for the analysis of transcription factor complexes Methods 26 2002 254 259
28. C.M. Diaz-Montero, and B.W. McIntyre Acquisition of anoikis resistance in human osteosarcoma cells does not alter sensitivity to chemotherapeutic agents BMC Cancer 5 2005 39
29. T.D. King, J.C. Gandy, and G.N. Bijur The protein phosphatase-1/inhibitor-2 complex differentially regulates GSK3 dephosphorylation and increases sarcoplasmic/endoplasmic reticulum calcium ATPase 2 levels Exp. Cell Res. 312 2006 3693 3700
30. A.H. Merrill Jr. Sphingolipid and glycosphingolipid metabolic pathways in the era of sphingolipidomics Chem. Rev. 111 2011 6387 6422
31. Y.Y. Liu, R.A. Hill, and Y.T. Li Ceramide glycosylation catalyzed by glucosylceramide synthase and cancer drug resistance Adv. Cancer Res. 117 2013 59 89
32. Y.A. Hannun, and L.M. Obeid Many ceramides J. Biol. Chem. 286 2011 27855 27862
33. Y. Pewzner-Jung, S. Ben-Dor, and A.H. Futerman When do Lasses (longevity assurance genes) become CerS (ceramide synthases)?: insights into the regulation of ceramide synthesis J. Biol. Chem. 281 2006 25001 25005
34. N. Andrieu-Abadie, and T. Levade Sphingomyelin hydrolysis during apoptosis Biochim. Biophys. Acta 1585 2002 126 134
35. R. Bose, M. Verheij, A. Haimovitz-Friedman, K. Scotto, Z. Fuks, and R. Kolesnick Ceramide synthase mediates daunorubicin-induced apoptosis: an alternative mechanism for generating death signals Cell 82 1995 405 414
36. A. Yang, and F. McKeon P63 and P73: P53 mimics, menaces and more Nat. Rev. Mol. Cell Biol. 1 2000 199 207
37. E.R. Flores, K.Y. Tsai, D. Crowley, S. Sengupta, A. Yang, F. McKeon, and T. Jacks p63 and p73 are required for p53-dependent apoptosis in response to DNA damage Nature 416 2002 560 564
38. M.P. Deyoung, and L.W. Ellisen p63 and p73 in human cancer: defining the network Oncogene 26 2007 5169 5183
39. B.D. Rowland, R. Bernards, and D.S. Peeper The KLF4 tumour suppressor is a transcriptional repressor of p53 that acts as a context-dependent oncogene Nat. Cell Biol. 7 2005 1074 1082
40. P.P. Ruvolo Ceramide regulates cellular homeostasis via diverse stress signaling pathways Leukemia 15 2001 1153 1160
41. C.E. Chalfant, K. Kishikawa, M.C. Mumby, C. Kamibayashi, A. Bielawska, and Y.A. Hannun Long chain ceramides activate protein phosphatase-1 and protein phosphatase-2A. Activation is stereospecific and regulated by phosphatidic acid J. Biol. Chem. 274 1999 20313 20317
42. C.E. Chalfant, B. Ogretmen, S. Galadari, B.J. Kroesen, B.J. Pettus, and Y.A. Hannun FAS activation induces dephosphorylation of SR proteins; dependence on the de novo generation of ceramide and activation of protein phosphatase 1 J. Biol. Chem. 276 2001 44848 44855
43. S. Stamm Regulation of alternative splicing by reversible protein phosphorylation J. Biol. Chem. 283 2008 1223 1227
44. K. Kishikawa, C.E. Chalfant, D.K. Perry, A. Bielawska, and Y.A. Hannun Phosphatidic acid is a potent and selective inhibitor of protein phosphatase 1 and an inhibitor of ceramide-mediated responses J. Biol. Chem. 274 1999 21335 21341
45. S.C. Wright, H. Zheng, and J. Zhong Tumor cell resistance to apoptosis due to a defect in the activation of sphingomyelinase and the 24 kDa apoptotic protease (AP24) FASEB J. 10 1996 325 332
46. C.E. Chalfant, Z. Szulc, P. Roddy, A. Bielawska, and Y.A. Hannun The structural requirements for ceramide activation of serine-threonine protein phosphatases J. Lipid Res. 45 2004 496 506
47. L.M. Leoni, H.C. Shih, L. Deng, C. Tuey, G. Walter, D.A. Carson, and H.B. Cottam Modulation of ceramide-activated protein phosphatase 2A activity by low molecular weight aromatic compounds Biochem. Pharmacol. 55 1998 1105 1111
48. R.A. Wolff, R.T. Dobrowsky, A. Bielawska, L.M. Obeid, and Y.A. Hannun Role of ceramide-activated protein phosphatase in ceramide-mediated signal transduction J. Biol. Chem. 269 1994 19605 19609
49. S. Cho, A. Hoang, R. Sinha, X.Y. Zhong, X.D. Fu, A.R. Krainer, and G. Ghosh Interaction between the RNA binding domains of Ser-Arg splicing factor 1 and U1-70K snRNP protein determines early spliceosome assembly Proc. Natl. Acad. Sci. U. S. A. 108 2011 8233 8238
50. S.H. Xiao, and J.L. Manley Phosphorylation-dephosphorylation differentially affects activities of splicing factor ASF/SF2 EMBO J. 17 1998 6359 6367
51. R. Das, J. Yu, Z. Zhang, M.P. Gygi, A.R. Krainer, S.P. Gygi, and R. Reed SR proteins function in coupling RNAP II transcription to pre-mRNA splicing Mol. Cell 26 2007 867 881
52. G. Michlewski, J.R. Sanford, and J.F. Caceres The splicing factor SF2/ASF regulates translation initiation by enhancing phosphorylation of 4E-BP1 Mol. Cell 30 2008 179 189
53. J.C. Ngo, S. Chakrabarti, J.H. Ding, A. Velazquez-Dones, B. Nolen, B.E. Aubol, J.A. Adams, X.D. Fu, and G. Ghosh Interplay between SRPK and Clk/Sty kinases in phosphorylation of the splicing factor ASF/SF2 is regulated by a docking motif in ASF/SF2 Mol. Cell 20 2005 77 89
54. C.T. Ma, G. Ghosh, X.D. Fu, and J.A. Adams Mechanism of dephosphorylation of the SR protein ASF/SF2 by protein phosphatase 1 J. Mol. Biol. 403 2010 386 404
55. T. Misteli, and D.L. Spector Serine/threonine phosphatase 1 modulates the subnuclear distribution of pre-mRNA splicing factors Mol. Biol. Cell 7 1996 1559 1572
56. J.R. Sanford, and J.P. Bruzik Regulation of SR protein localization during development Proc. Natl. Acad. Sci. U. S. A. 98 2001 10184 10189
57. S. Lin, R. Xiao, P. Sun, X. Xu, and X.D. Fu Dephosphorylation-dependent sorting of SR splicing factors during mRNP maturation Mol. Cell 20 2005 413 425
58. S.A. Tenenbaum, and J. Aguirre-Ghiso Dephosphorylation shows SR proteins the way out Mol. Cell 20 2005 499 501
59. R. Karni, E. de Stanchina, S.W. Lowe, R. Sinha, D. Mu, and A.R. Krainer The gene encoding the splicing factor SF2/ASF is a proto-oncogene Nat. Struct. Mol. Biol. 14 2007 185 193
60. O. Anczukow, A.Z. Rosenberg, M. Akerman, S. Das, L. Zhan, R. Karni, S.K. Muthuswamy, and A.R. Krainer The splicing factor SRSF1 regulates apoptosis and proliferation to promote mammary epithelial cell transformation Nat. Struct. Mol. Biol. 19 2012 220 228
61. J.C. Shultz, R.W. Goehe, C.S. Murudkar, D.S. Wijesinghe, E.K. Mayton, A. Massiello, A.J. Hawkins, P. Mukerjee, R.L. Pinkerman, M.A. Park, and C.E. Chalfant SRSF1 regulates the alternative splicing of caspase 9 via a novel intronic splicing enhancer affecting the chemotherapeutic sensitivity of non-small cell lung cancer cells Mol. Cancer Res. 9 2011 889 900
62. R.W. Goehe, J.C. Shultz, C. Murudkar, S. Usanovic, N.F. Lamour, D.H. Massey, L. Zhang, D.R. Camidge, J.W. Shay, J.D. Minna, and C.E. Chalfant hnRNP L regulates the tumorigenic capacity of lung cancer xenografts in mice via caspase-9 pre-mRNA processing J. Clin. Invest. 120 2010 3923 3939
63. O.I. Fregoso, S. Das, M. Akerman, and A.R. Krainer Splicing-factor oncoprotein SRSF1 stabilizes p53 via RPL5 and induces cellular senescence Mol. Cell 50 2013 56 66