CYR61 controls p53 and NF-κB expression through PI3K/Akt/mTOR pathways in carboplatin-induced ovarian cancer cells

Cancer Letters

Volumn 315, Issue 1, 2012, Pages 86-95

  Lee, Kwang Beom ^a   Byun, Hyun Jung ^b   Park, Sung Ho ^c   Park, Chan Yong ^a   Lee, Seung Hoon ^d   Rho, Seung Bae ^b  

^a Gachon University College of Medicine   (South Korea)

^b National Cancer Center   (South Korea)

^c Hallym University   (South Korea)

^d Yongin University   (South Korea)

Author keywords

Apoptosis; Carboplatin; CCN1 (CYR61); NF B; Ovarian carcinoma cells; PI3K Akt

Indexed keywords

CARBOPLATIN; CYSTEINE RICH PROTEIN 61; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN KINASE B; PROTEIN MCL 1; PROTEIN P21; PROTEIN P53; RAPAMYCIN; VASCULOTROPIN;

APOPTOSIS; ARTICLE; CANCER CELL; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG INHIBITION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; HUMAN; HUMAN CELL; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TREATMENT RESPONSE;

APOPTOSIS; CARBOPLATIN; CELL LINE, TUMOR; CYSTEINE-RICH PROTEIN 61; FEMALE; HUMANS; NF-KAPPA B; OVARIAN NEOPLASMS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 81955167355     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.10.016     Document Type: Article

References (55)

1. Sampath D., Winneker R.C., Zhang Z. Cyr61, a member of the CCN family, is required for MCF-7 cell proliferation: regulation by 17 beta-estradiol and overexpression in human breast cancer. Endocrinology 2001, 142:2540-2548.
2. Tsai M.S., Bogart D.F., Castaneda J.M., Li P., Lupu R. Cyr61 promotes breast tumorigenesis and cancer progression. Oncogene 2001, 21:8178-8185.
3. Menéndez J.A., Mehmi I., Griggs D.W., Lupu R. International congress on hormonal steroids and hormones and cancer. The angiogenic factor CYR61 in breast cancer: molecular pathology and therapeutic perspectives. Endocr. Relat. Cancer 2003, 10:141-152.
4. Jiang W.G., Watkins G., Fodstad O., Douglas-Jones A., Mokbel K., Mansel R.E. Differential expression of the CCN family members Cyr61, CTGF and Nov in human breast cancer. Endocr. Relat. Cancer 2004, 11:781-791.
5. Gery S., Xie D., Yin D., Gabra H., Miller C., Wang H., Scott D., Yi W.S., Popoviciu M.L., Said J.W., Koeffler H.P. Ovarian carcinomas: CCN genes are aberrantly expressed and CCN1 promotes proliferation of these cells. Clin. Cancer Res. 2005, 11:7243-7254.
6. Chen C.-C., Lau L.F. Functions and mechanisms of action of CCN multicellular proteins. Int. J. Biochem. Cell Biol. 2009, 41:771-783.
7. Watari H., Xiong Y., Hassan M.K., Sakuragi N. Cyr61, a member of CCN (connective tissue growth factor/cysteine-rich 61/nephroblastoma overexpressed) family predicts survival of patients with endometrial cancer of endometrioid subtype. Gynecol. Oncol. 2009, 112:229-234.
8. Chen Y., Du X.-Y. Functional properties and intracellular signaling of CCN/Cyr61. J. Cell. Biochem. 2007, 100:1337-1345.
9. Babic A.M., Kireeva M.L., Kolesnikova T.V., Lau L.F. CYR61, product of a growth factor-inducible immediate-early gene, promotes angiogenesis and tumor growth. Proc. Natl. Acad. Sci. USA. 1998, 95:6355-6360.
10. Mo F.E., Muntean A.G., Chen C.-C., Stolz D.B., Watkins S.C., Lau L.F. CYR61 (CCN1) is essential for placental development and vascular integrity. Mol. Cell. Biol. 2002, 22:8709-8720.
11. Mo F.E., Lau L.F. The matricellular protein CCN1 is essential for cardiac development. Circ. Res. 2006, 99:961-969.
12. Dhar A., Ray A. The CCN family proteins in carcinogenesis. Exp. Oncol. 2010, 32:2-9.
13. Wesierska-Gadek J., Schloffer D., Kotala V., Horky M. Escape of p53 protein from E6-mediated degradation in HeLa cells after cisplatin therapy. Int. J. Cancer 2002, 101:128-136.
14. Rho S.B., Byun H.-J., Park S.-Y., Chun T. Cysteine 61 (CYR61) inhibits cisplatin-induced apoptosis in ovarian carcinomas cells. Biotechnol. Lett. 2009, 31:23-28.
15. Kireeva M.L., Mo F.E., Yang G.P., Lau L.F. Cyr61, a product of a growth factor-inducible immediate-early gene, promotes cell proliferation, migration, and adhesion. Mol. Cell. Biol. 1996, 16:1326-1334.
16. Leu S.J., Lam S.C., Lau L.F. Pro-angiogenic activities of CYR61 (CCN1) mediated through integrins alphavbeta3 and alpha6beta1 in human umbilical vein endothelial cells. J. Biol. Chem. 2002, 277:46248-46255.
17. Pivot X., Cals L., Cupissol D., Guardiola E., Tchiknavorian X., Guerrier P., Merad L., Wendling J.L., Barnouin L., Savary J., Thyss A., Schneider M. Phase II trial of a paclitaxel-carboplatin combination in recurrent squamous cell carcinoma of head and neck. Oncology 2001, 60:66-71.
18. Fujiwara K., Sakuragi N., Suzuki S., Yoshida N., Maehata K., Nishiya M., Koshida T., Sawai H., Aotani E., Kohno I. First-line intraperitoneal carboplatin-based chemotherapy for 165 patients with epithelial ovarian carcinoma: results of long term follow up. Gynecol. Oncol. 2003, 90:637-643.
19. Cheng C.F., Juan S.H., Chen J.J., Chao Y.C., Chen H.H., Lian W.S., Lu C.Y., Chang C.I., Chiu T.H., Lin H. Pravastatin attenuates carboplatin-induced cardiotoxicity via inhibition of oxidative stress associated apoptosis. Apoptosis 2008, 13:883-894.
20. Alberts D.S. Carboplatin versus cisplatin in ovarian cancer. Semin. Oncol. 1995, 22:88-90.
21. Ndinguri M.W., Solipuram R., Gambrell R.P., Aggarwal S., Hansel W., Hammer R.P. Peptide targeting of platinum anti-cancer drugs. Bioconjug. Chem. 2009, 20:1869-1878.
22. Boulikas T., Vougiouka M. Cisplatin and platinum drugs at the molecular level (Review). Oncol. Rep. 2003, 10:1663-1682.
23. Lee C.S., Kim Y.J., Jang E.R., Myung S.C., Kim W. Akt inhibitor enhances apoptotic effect of carboplatin on human epithelial ovarian carcinoma cell lines. Eur. J. Pharmacol. 2010, 632:7-13.
24. Adams J.M., Cory S. The Bcl-2 protein family: arbiters of cell survival. Science 1998, 281:1322-1326.
25. Antonsson B., Martinou J.C. The Bcl-2 protein family. Exp. Cell Res. 2000, 256:50-57.
26. Yin X.M., Oltvai Z.N., Korsmeyer S.J. BH1 and BH2 domain of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature 1994, 369:321-323.
27. Reed J.C. Bcl-2 family proteins: regulators of apoptosis and chemoresistance in hematologic malignancies. Semin. Hematol. 1997, 34:9-19.
28. Johnstone R.W., Ruefli A.A., Lowe S.W. Apoptosis: a link between cancer genetics and chemotherapy. Cell 2002, 108:153-164.
29. Malaguarnera L. Implications of apoptosis regulators in tumorigenesis. Cancer Metastasis Rev. 2004, 23:367-387.
30. Khwaja A. Akt is more than just a Bad kinase. Nature 1999, 401:33-34.
31. McCormick F. Cancer: survival pathways meet their end. Nature 2004, 428:267-269.
32. Westfall S.D., Skinner M.K. Inhibition of phosphatidylinositol 3-kinase sensitizes ovarian cancer cells to carboplatin and allows adjunct chemotherapy treatment. Mol. Cancer Ther. 2005, 4:1764-1771.
33. Yuan Z.Q., Sun N., Feldman R.I., Wang G., Ma X., Jiang C., Coppola D., Nicosia S.V., Cheng J.Q. Frequent activation of AKT2 and induction of apoptosis by inhibition of phosphoinositide-3-OH kinase/Akt pathway in human ovarian cancer. Oncogene 2000, 19:2324-2330.
34. Bjornsti M.A., Houghton P.J. The mTOR pathways: a target for cancer therapy. Nat. Rev. Cancer 2004, 4:335-348.
35. Bjornsti M.A., Houghton P.J. Lost in translation: dysregulation of cap-dependent translation and cancer. Cancer Cell 2004, 5:519-523.
36. Fruman D.A., Mauvais-Jarvis F., Pollard D.A., Yballe C.M., Brazil D., Bronson R.T., Kahn C.R., Cantley L.C. Hypoglycaemia, liver necrosis and perinatal death in mice lacking all isoforms of phosphoinositide 3-kinase p85 alpha. Nat. Genet. 2000, 26:379-382.
37. Karin M., Cao Y., Greten F.R., Li Z.W. NF-kappaB in cancer: from innocent bystander to major culprit. Nat. Rev. Cancer 2002, 2:301-310.
38. Oren M. Decision making by p53: life, death and cancer. Cell Death Differ. 2003, 10:431-442.
39. Steele R.J., Lane D.P. P53 in cancer: a paradigm for modern management of cancer. Surgeon 2005, 3:197-205.
40. Haldar S., Negrini M., Monne M., Sabbioni S., Croce C.M. Down-regulation of Bcl-2 by p53 in breast cancer cells. Cancer Res. 1994, 54:2095-2097.
41. Miyashita T., Reed J.C. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 1995, 80:293-299.
42. Bentires-Alj M., Dejardin E., Viatour P., Van Lint C., Froesch B., Reed J.C., Merville M.P., Bours V. Inhibition of the NF-kappaB transcription factor increases Bax expression in cancer cell lines. Oncogene 2001, 20:2805-2813.
43. Heckman C.A., Mehew J.W., Boxer L.M. NF-kappaB activates Bcl-2 expression in t(14:18) lymphoma cells. Oncogene 2002, 21:3898-3908.
44. Lin M.T., Chang C.C., Chen S.T., Chang H.L., Su J.L., Chau Y.P., Kuo M.L. Cyr61 expression confers resistance to apoptosis in breast cancer MCF-7 cells by a mechanism of NF-kappaB-dependent XIAP up-regulation. J. Biol. Chem. 2004, 279:24015-24023.
45. Chien W., Kumagai T., Miller C.W., Desmond J.C., Frank J.M., Said J.W., Koeffler H.P. Cyr61 suppresses growth of human endometrial cancer cells. J. Biol. Chem. 2004, 279:53087-53096.
46. Croci S., Landuzzi L., Astolfi A., Nicoletti G., Rosolen A., Sartori F., Follo M.Y., Oliver N., De Giovanni C., Nanni P., Lollini P.L. Inhibition of connective tissue growth factor (CTGF/CCN2) expression decreases the survival and myogenic differentiation of human rhabdomyosarcoma cells. Cancer Res. 2004, 64:1730-1736.
47. Fujisawa T., Hattori T., Ono M., Uehara J., Kubota S., Kuboki T., Takigawa M. CCN family 2/connective tissue growth factor (CCN2/CTGF) stimulates proliferation and differentiation of auricular chondrocytes. Osteoarth. Cartilage 2008, 16:787-795.
48. Perbal B. NOV (nephroblastoma overexpressed) and the CCN family of genes: structural and functional issues. Mol. Pathol. 2001, 54:57-79.
49. Schmidt U., Fiedler U., Pilarsky C.P., Ehlers W., Füssel S., Haase M., Faller G., Sauter G., Wirth M.P. Expression of the extracellular matrix signaling molecule Cyr61 is downregulated in prostate cancer. Prostate 1998, 36:85-91.
50. Tong X., Xie D., O'Kelly J., Miller C.W., Muller-Tidow C., Koeffler H.P. Cyr61, a member of CCN family, is a tumor suppressor in non-small-cell lung cancer. J. Biol. Chem. 2001, 276:47709-47714.
51. Guo R.X., Qiao Y.H., Zhou Y., Li L.X., Shi H.R., Chen K.S. Increased staining for phosphorylated AKT and nuclear factor-κB p65 and their relationship with prognosis in epithelial ovarian cancer. Pathol. Int. 2008, 58:749-756.
52. Marra M., Abbruzzese A., Addeo R., Del Prete S., Tassone P., Tonini G., Tagliaferri P., Santini D., Caraglia M. Cutting the limits of aminobisphosphonates: new strategies for the potentiation of their anti-tumour effects. Curr. Cancer Drug Targets 2009, 9:791-800.
53. Marra M., Santini D., Meo G., Vincenzi B., Zappavigna S., Baldi A., Rosolowski M., Tonini G., Loeffler M., Lupu R., Addeo S.R., Abbruzzese A., Budillon A., Caraglia M. Cyr61 downmodulation potentiates the anticancer effects of zoledronic acid in androgen-independent prostate cancer cells. Int. J. Cancer 2009, 125:2004-2013.
54. Vitale G., Gentilini D., Abbruzzese A., Caraglia M. Pyk2 and Cyr61 at the cross-road of cAMP-dependent signalling in invasiveness and neuroendocrine differentiation of prostate cancer. Cancer Biol. Ther. 2009, 8:243-244.
55. Suvasini R., Somasundaram K. Essential role of PI3K-kinase pathway in p53-mediated transcription: implications in cancer chemotherapy. Oncogene 2010, 29:3605-3618.