The proto-oncogene PKCι regulates the alternative splicing of Bcl-x Pre-mRNA

Molecular Cancer Research

Volumn 10, Issue 5, 2012, Pages 660-669

  Shultz, Jacqueline C ^a   Vu, Ngoc ^a   Shultz, Michael D ^a   Mba, Mba Uzoma U ^a   Shapiro, Brian A ^a   Chalfant, Charles E ^a,b,c  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 5 METHOXY 1H INDOL 3 YL] 3 (1H INDOL 3 YL)MALEIMIDE; 2 MORPHOLINO 8 PHENYLCHROMONE; CERAMIDE; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL X; PROTEIN KINASE C; PROTEIN KINASE C ZETA; TRANS ACTING FACTOR;

ALTERNATIVE RNA SPLICING; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CELL SURVIVAL; CONTROLLED STUDY; CORRELATION ANALYSIS; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTO ONCOGENE; RECEPTOR DOWN REGULATION;

ALTERNATIVE SPLICING; APOPTOSIS; BCL-X PROTEIN; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL SURVIVAL; CERAMIDES; CHROMONES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INDOLES; ISOENZYMES; MALEIMIDES; MORPHOLINES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHOPROTEINS; PROTEIN KINASE C; RIBONUCLEOPROTEIN, U2 SMALL NUCLEAR; RNA SPLICE SITES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84861110352     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-11-0363     Document Type: Article

References (51)

1. Boise LH, Gonzalez-Garcia M, Postema CE, Ding L, Lindsten T, Turka LA, et al. bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 1993;74:597-608. (Pubitemid 23259741)
2. Boise LH, Thompson CB. Bcl-x(L) can inhibit apoptosis in cells that have undergone Fas-induced protease activation. Proc Natl Acad Sci U S A 1997;94:3759-64.
3. Coluccia AM, Perego S, Cleris L, Gunby RH, Passoni L, Marchesi E, et al. Bcl-XL down-regulation suppresses the tumorigenic potential of NPM/ALK in vitro and in vivo. Blood 2004;103: 2787-94. (Pubitemid 38393038)
4. Datta R, Manome Y, Taneja N, Boise LH, Weichselbaum R, Thompson CB, et al. Overexpression of Bcl-XL by cytotoxic drug exposure confers resistance to ionizing radiation-induced internucleosomal DNA fragmentation. Cell Growth Differ 1995;6:363-70.
5. Dole MG, Jasty R, Cooper MJ, Thompson CB, Nunez G, Castle VP. Bcl-xL is expressed in neuroblastoma cells and modulates chemotherapy-induced apoptosis. Cancer Res 1995;55:2576-82.
6. Finch A, Prescott J, Shchors K, Hunt A, Soucek L, Dansen TB, et al. Bcl-xL gain of function and p19 ARF loss of function cooperate oncogenically with Myc in vivo by distinct mechanisms. Cancer Cell 2006;10:113-20. (Pubitemid 44175905)
7. Johnson BW, Cepero E, Boise LH. Bcl-xL inhibits cytochrome c release but not mitochondrial depolarization during the activation of multiple death pathways by tumor necrosis factor-alpha. J Biol Chem 2000;275:31546-53.
8. Meyn RE, Stephens LC, Hunter NR, Milas L. Apoptosis in murine tumors treated with chemotherapy agents. Anti-cancer drugs 1995;6:443-50.
9. Minn AJ, Boise LH, Thompson CB. Bcl-x(S) anatagonizes the protective effects of Bcl-x(L). J Biol Chem 1996;271:6306-12.
10. Minn AJ, Rudin CM, Boise LH, Thompson CB. Expression of bcl-xL can confer a multidrug resistance phenotype. Blood 1995;86: 1903-10.
11. Kuhl JS, Krajewski S, Duran GE, Reed JC, Sikic BI. Spontaneous overexpression of the long form of the Bcl-X protein in a highly resistant P388 leukaemia. Br J Cancer 1997;75:268-74. (Pubitemid 27019573)
12. Liu JR, Fletcher B, Page C, Hu C, Nunez G, Baker V. Bcl-xL is expressed in ovarian carcinoma and modulates chemotherapy-induced apoptosis. Gynecol Oncol 1998;70:398-403. (Pubitemid 28473641)
13. Luo D, Cheng SC, Xie H, Xie Y. Effects of Bcl-2 and Bcl-XL protein levels on chemoresistance of hepatoblastoma HepG2 cell line. Biochem Cell Biol 2000;78:119-26. (Pubitemid 30353769)
14. Olopade OI, Adeyanju MO, Safa AR, Hagos F, Mick R, Thompson CB, et al. Overexpression of BCL-x protein in primary breast cancer is associated with high tumor grade and nodal metastases. Cancer J Sci Am 1997;3:230-7.
15. Schmitt E, Sane AT, Steyaert A, Cimoli G, Bertrand R. The Bcl-xL and Bax-alpha control points: modulation of apoptosis induced by cancer chemotherapy and relation to TPCK-sensitive protease and caspase activation. Biochem Cell Bio 1997;75:301-14. (Pubitemid 127733181)
16. Van Houten N, Blake SF, Li EJ, Hallam TA, Chilton DG, Gourley WK, et al. Elevated expression of Bcl-2 and Bcl-x by intestinal intraepithelial lymphocytes: resistance to apoptosis by glucocorticoids and irradiation. Int Immunol 1997;9:945-53. (Pubitemid 27277739)
17. Ban J, Eckhart L, Weninger W, Mildner M, Tschachler E. Identification of a human cDNA encoding a novel Bcl-x isoform. Biochem Biophys Res Commun 1998;248:147-52. (Pubitemid 28418202)
18. Fang W, Rivard JJ, Mueller DL, Behrens TW. Cloning and molecular characterization of mouse bcl-x in B and T lymphocytes. J Immunol 1994;153:4388-98. (Pubitemid 24346833)
19. Shiraiwa N, Inohara N, Okada S, Yuzaki M, Shoji S, Ohta S. An additional formof rat Bcl-x, Bcl-xbeta, generated by an unspliced RNA, promotes apoptosis in promyeloid cells. J Biol Chem 1996;271:13258-65. (Pubitemid 26175910)
20. Yang XF, Weber GF, Cantor H. A novel Bcl-x isoform connected to the T cell receptor regulates apoptosis in T cells. Immunity 1997;7:629-39. (Pubitemid 28156631)
21. Taylor JK, Zhang QQ, Wyatt JR, Dean NM. Induction of endogenous Bcl-xS through the control of Bcl-x pre-mRNA splicing by antisense oligonucleotides. Nat Biotechnol 1999;17:1097-100. (Pubitemid 29533549)
22. Mercatante DR, Bortner CD, Cidlowski JA, Kole R. Modification of alternative splicing of Bcl-x pre-mRNA in prostate and breast cancer cells. analysis of apoptosis and cell death. J Biol Chem 2001;276: 16411-7.
23. Deng G, Lane C, Kornblau S, Goodacre A, Snell V, Andreeff M, et al. Ratio of bcl-xshort to bcl-xlong is different in good- and poor-prognosis subsets of acute myeloid leukemia. Mol Med 1998;4:158-64. (Pubitemid 28223967)
24. Mercatante DR, Mohler JL, Kole R. Cellular response to an antisense-mediated shift of Bcl-x pre-mRNA splicing and antineoplastic agents. J Biol Chem 2002;277:49374-82. (Pubitemid 36014369)
25. Sumantran VN, Ealovega MW, Nunez G, Clarke MF, Wicha MS. Overexpression of Bcl-XS sensitizes MCF-7 cells to chemotherapy-induced apoptosis. Cancer Res 1995;55:2507-10.
26. Chalfant CE, Ogretmen B, Galadari S, Kroesen BJ, Pettus BJ, Hannun YA. FAS activation induces dephosphorylation of SR proteins; dependence on the de novo generation of ceramide and activation of protein phosphatase 1. J Biol Chem 2001;276:44848-55.
27. Chalfant CE, Rathman K, Pinkerman RL, Wood RE, Obeid LM, Ogretmen B, et al. 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 2002;277:12587-95. (Pubitemid 34952617)
28. Boon-Unge K, Yu Q, Zou T, Zhou A, Govitrapong P, Zhou J. Emetine regulates the alternative splicing of Bcl-x through a protein phosphatase 1-dependent mechanism. Chem Biol 2007;14:1386-92. (Pubitemid 350262840)
29. Chang WH, Liu TC, Yang WK, LeeCC, Lin YH, Chen TY, et al. Amiloride modulates alternative splicing in leukemic cells and resensitizes Bcr-AblT315I mutant cells to imatinib. Cancer Res 2011;71:383-92.
30. Massiello A, Salas A, Pinkerman RL, Roddy P, Roesser JR, Chalfant CE. Identification of two RNA cis-elements that function to regulate the 5′ splice site selection of Bcl-x pre-mRNA in response to ceramide. J Biol Chem 2004;279:15799-804. (Pubitemid 38509266)
31. Massiello A, Roesser JR, Chalfant CE. SAP155 Binds to ceramide-responsive RNA cis-element 1 and regulates the alternative 5′ splice site selection of Bcl-x pre-mRNA. FASEB J 2006;20:1680-2.
32. Revil T, Toutant J, Shkreta L, Garneau D, Cloutier P, Chabot B. Protein kinase C-dependent control of Bcl-x alternative splicing. Mol Cell Biol 2007;27:8431-41.
33. Goehe RW, Shultz JC, Murudkar C, Usanovic S, Lamour NF, Massey DH, et al. hnRNP L regulates the tumorigenic capacity of lung cancer xenografts in mice via caspase-9 pre-mRNA processing. J Clin Invest 2010;120:3923-39.
34. Lamour NF, Wijesinghe DS, Mietla JA, Ward KE, Stahelin RV, Chalfant CE. Ceramide kinase regulates the production of tumor necrosis factor alpha (TNFalpha) via inhibition of TNFalpha-converting enzyme. J Biol Chem 2011;286:42808-17.
35. Shkreta L, Michelle L, Toutant J, Tremblay ML, Chabot B. The DNA damage response pathway regulates the alternative splicing of the apoptotic mediator Bcl-x. J Biol Chem 2011;286:331-40.
36. Shultz JC, Goehe RW, Murudkar CS, Wijesinghe DS, Mayton EK, Massiello A, et al. 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 2011;9:889-900.
37. Pettus BJ, Chalfant CE, Hannun YA. Ceramide in apoptosis: an overview and current perspectives. Biochim Biophys Acta 2002; 1585:114-25. (Pubitemid 36092075)
38. Bauman JA, Li SD, Yang A, Huang L, Kole R. Anti-tumor activity of splice-switching oligonucleotides. Nucleic Acids Res 2010;38: 8348-56.
39. Shultz JC, Goehe RW, Wijesinghe DS, Murudkar C, Hawkins AJ, Shay JW, et al. Alternative splicing of caspase 9 is modulated by the phosphoinositide 3-kinase/Akt pathway via phosphorylation of SRp30a. Cancer Res 2010;70:9185-96.
40. Revil T, Pelletier J, Toutant J, Cloutier A, Chabot B. Heterogeneous nuclear ribonucleoprotein K represses the production of pro-apoptotic Bcl-xS splice isoform. J Biol Chem 2009;284:21458-67.
41. Paronetto MP, Achsel T, Massiello A, Chalfant CE, Sette C. The RNA-binding protein Sam68 modulates the alternative splicing of Bcl-x. J Cell Biol 2007;176:929-39. (Pubitemid 46506967)
42. Garneau D, Revil T, Fisette JF, Chabot B. Heterogeneous nuclear ribonucleoprotein F/H proteins modulate the alternative splicing of the apoptotic mediator Bcl-x. J Biol Chem 2005;280:22641-50. (Pubitemid 40853168)
43. Regala RP, Weems C, Jamieson L, Copland JA, Thompson EA, Fields AP. Atypical protein kinase Ciota plays a critical role in human lung cancer cell growth and tumorigenicity. J Biol Chem 2005;280:31109-15. (Pubitemid 41291846)
44. Solier S, De Cian MC, Bettaieb A, Desoche L, Solary E, Corcos L. PKC zeta controls DNA topoisomerase-dependent human caspase-2 pre-mRNA splicing. FEBS Lett 2008;582:372-8.
45. Moore MJ, Wang Q, Kennedy CJ, Silver PA. An alternative splicing network links cell-cycle control to apoptosis. Cell 2010;142: 625-36.
46. Litherland GJ, Elias MS, Hui W, Macdonald CD, Catterall JB, Barter MJ, et al. Protein kinase C isoforms zeta and iota mediate collagenase expression and cartilage destruction via STAT3- and ERK-dependent c-fos induction. J Biol Chem 2010;285:22414-25.
47. Munoz MJ, Perez Santangelo MS, Paronetto MP, de la Mata M, Pelisch F, Boireau S, et al. DNA damage regulates alternative splicing through inhibition of RNA polymerase II elongation. Cell 2009;137:708-20.
48. Pecci A, Viegas LR, Baranao JL, Beato M. Promoter choice influences alternative splicing and determines the balance of isoforms expressed from the mouse bcl-X gene. J Biol Chem 2001;276:21062-9.
49. Standaert ML, Bandyopadhyay G, SajanMP, Cong L, Quon MJ, Farese RV. Okadaic acid activates atypical protein kinase C (zeta/lambda) in rat and 3T3/L1 adipocytes. An apparent requirement for activation of Glut4 translocation and glucose transport. J Biol Chem 1999;274: 14074-8.
50. Wang YM, Seibenhener ML, Vandenplas ML, Wooten MW. Atypical PKC zeta is activated by ceramide, resulting in coactivation of NFkappaB/JNK kinase and cell survival. J Neurosci Res 1999;55:293-302. (Pubitemid 29055179)
51. Regala RP, Weems C, Jamieson L, Khoor A, Edell ES, Lohse CM, et al. Atypical protein kinase C iota is an oncogene in human non-small cell lung cancer. Cancer Res 2005;65:8905-11. (Pubitemid 41377380)