12-O-tetradecanoylphorbol-1,3-acetate induces the negative regulation of protein kinase B by protein kinase Calpha during gastric cancer cell apoptosis

• Autorzy: Zhang B , Xia C.
• Języki publikacji: EN

Abstrakty

EN

The PKB signaling pathway is essential for cell survival and the inhibition of apoptosis, but its functional mechanisms have not been fully explored. Previously, we reported that TPA effectively inhibited PKB activity and caused PKB degradation, which was correlated with the repression of PKB phosphorylation at Ser473. In this study, we focus on how PKB is regulated by TPA in gastric cancer cells. One of the TPA targets, PKCα, was found to mediate the inhibition of PKB phosphorylation and degredation caused by TPA. Furthermore, TPA induced the import of PKCα into the nucleus, where PKCα exerted an inhibitory effect on PKB expression and phosphorylation. As a result, cancer cell proliferation was arrested. Our study characterizes a novel function of PKCα in mediating the negative regulation of PKB by TPA, and suggests a potential application in the clinical treatment of gastric cancer.

Słowa kluczowe

EN

12-0-tetradecanoylphorbol-1,3-acetate; protein kinase C; gastric cancer; cell apoptosis; protein kinase B; translocation; growth inhibition

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2010
• Tom: 15
• Numer: 3
• Opis fizyczny: p.377-394,fig.,ref.

Twórcy

autor

Zhang B

• Xiamen University, Xiamen 361005, Fujian Province, China

autor

Xia C.

Bibliografia

• 1. Brazil, D.P. and Hemmings, B.A. Ten years of protein kinase B signalling: a hard Akt to follow. Trends Biochem. Sci. 26 (2001) 657-664.
• 2. Kohn, A.D., Kovacina, K.S. and Roth, R.A. Insulin stimulates the kinase activity of RAC-PK, a pleckstrin homology domain containing ser/thr kinase. EMBO J. 14 (1995) 4288-4295.
• 3. Alessi, D.R., Andjelkovic, M., Caudwell, B., Cron, P., Morrice, N., Cohen, P. and Hemmings, B.A. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15 (1996) 6541-6551.
• 4. Andjelkovic, M., Jakubowicz, T., Corn, P., Ming, X.F., Han, J.W. and Hemmings, B.A. Activation and phosphorylation of a pleckstrin homology domain containing protein kinase (RAC-PK/PKB) promoted by serum and protein phosphatase inhibitors. Proc. Natl. Acad. Sci. USA 93 (1996) 5699- 5704.
• 5. Vanhaesebroeck, B. and Alessi, D.R. The PI3k-PDK1 connection: more than just a road to PKB. Biochem. J. 346 (2000) 561-576.
• 6. Alessi, D.R., James, S.R., Downes, C.P., Holmes, A.B., Gaffney, P.R., Reese, C.B. and Cohen, P. Characterization of a 3-phosphoinositidedependent protein kinase which phosphorylates and activates protein kinase B alpha. Curr. Biol. 7 (1997) 261-269.
• 7. Kroner, C., Eybrechts, K. and Akkerman, J.W. Dual regulation of platelet protein kinase B. J. Biol. Chem. 275 (2000) 27790-27798.
• 8. Hill, M.M., Andjelkovic, M., Brazil, D.P., Ferrari, S., Fabbro, D. and Hemmings, B.A. Insulin-stimulated protein kinase B phosphorylation on Ser-473 is independent of its activity and occurs through a staurosporineinsensitive kinase. J. Biol. Chem. 276 (2001) 25643-25646.
• 9. Andjelkovic, M., Maira, S.M., Cron, P., Parker, P.J. and Hemmings, B.A. Domain swapping used to investigate the mechanism of protein kinase B regulation by 3-phosphoinositide-dependent protein kinase 1 and Ser473 kinase. Mol. Cell Biol. 19 (1999) 5061-5072.
• 10. Chen, D., Fucini, R.V., Olson, A.L., Hemmings, B.A. and Pessin, J.E. Osmotic shock inhibits insulin signaling by maintaining Akt/protein kinase B in an inactive dephosphorylated state. Mol. Cell Biol. 19 (1999) 4684- 4694.
• 11. Schubert, K.M., Scheid, M.P. and Duronio, V. Ceramide inhibits protein kinase B/Akt by promoting dephosphorylation of serine 473. J. Biol. Chem. 275 (2000) 13330-13335.
• 12. Zhang, B. and Xia, C. The expression of protein kinase B in gastric cancer cell apoptosis induced by 12-O-tetradecanoylphorbol-1, 3-acetate. Cell. Mol. Biol. Lett. 14 (2009) 466-480.
• 13. Moore, E.D., Ring, M., Scriven, D.R., Smith, V.C., Meloche, R.M. and Buchan, A.M. The role of protein kinase C isozymes in bombesin-stimulated gastrin release from human antral gastrin cells. J. Biol. Chem. 274 (1999) 22493-22501.
• 14. Kelly, M.L., Tang, Y., Rosensweig, N., Clejan, S. and Beckman, B.S. Granulocyte-macrophage colony-stimulating factor rescues TF-1 leukemia cells from ionizing radiation-induced apoptosis through a pathway mediated by protein kinase Calpha. Blood 92 (1998) 416-424.
• 15. Shao, R.G., Cao, C.X. and Prommier, Y. Activation of PKCalpha downstream from caspases apoptosis induced by 7-hydroxystaurosporine or the topoisomerase inhibitors, camptothecin and etoposide, in human myeloid leukemia HL60 cells. J. Biol. Chem. 272 (1997)31321-31325.
• 16. Iioka, Y., Mishima, K., Azuma, N., Tsuchida, A., Takagi, Y., Aoki, T. and Saito, I. Overexpression of protein kinase Cdelta enhances cisplatin-induced cytotoxicity correlated with p53 in gastric cancer cell line. Pathobiology 72 (2005) 152-159.
• 17. Endo, K., Kohnoe, S., Tsujita, E., Watanabe, A., Nakashima, H., Baba, H. and Maehara, Y. Modulation of anti-apoptosis by endogenous IAP expression in MKN45 human gastric cancer cells. Anticancer Res. 25 (2005) 2713-2717.
• 18. Zhu, G.H., Wong, B.C., Slosberg, E.D., Eggo, M.C., Ching, C.K., Yuen, S.T., Lai, K.C., Soh, J.W., Weinstein, I.B. and Lam, S.K. Overexpression of protein kinase C-beta1 isoenzyme suppresses indomethacin-induced apoptosis in gastric epithelial cells. Gastroenterology 118 (2000) 507-514.
• 19. Jiang, X.H., Lam, S.K. Lin, M.C., Jiang, S.H., Kung, H.F. Slosberg E.D., Soh, J.W., Weinstein, I.B. and Wong, B.C. Novel target for induction of apoptosis by cyclo-oxygenase-2 inhibitor SC-236 through a protein kinase C-beta(1)-dependent pathway. Oncogene 21 (2002) 6113-6122.
• 20. Li, W., Zhang, J., Flechner, L., Hyun, T., Yam, A., Franke, T.F. and Pierce, J.H. Protein kinase C-alpha overexpression stimulates Akt activity and suppresses apoptosis induced by interleukin 3 withdrawal. Oncogene 18 (1999) 6564-6572.
• 21. Doornbos, R.P., Theelen, M., Van Der Hoeven, P.C., Van Blitterswijk, W.J., Verkleij, A.J. and Van Bergen En Henegouwen, P.M. Protein kinase Czeta is a negative regulator of protein kinase B activity. J. Biol. Chem. 274 (1999) 8589-8596.
• 22. Kawakami, Y., Nishimoto, H., Kitaura, J., Maeda-Yamamoto, M., Kato, R.M., Littman, D.R., Leitges, M., Rawlings, D.J. and Kawakami, T. Protein kinase C betaII regulates Akt phosphorylation on Ser-473 in a cell type- and stimulus-specific fashion. J. Biol. Chem. 279 (2004) 47720-47725.
• 23. Aicher, B., Lerch, M.M., Muller, T., Schilling, J. and Ullrich, A. Cellular redistribution of protein tyrosine phosphatases LAR and PTPsigma by inducible proteolytic processing. J. Biol. Chem. 138 (1997) 681-696.
• 24. Wu, Q., Lin, X.F., Zhang, B., Xie, Z. and Su, W.J. Ubiquitinated or sumoylated retinoic acid receptor alpha determines its characteristic and interacting model with retinoid X receptor alpha in gastric and breast cancer cells. J. Mol. Endocrinol. 32 (2004) 595-613.
• 25. Zhao, B.X., Chen, H.Z., Lei, N.Z., Li, G.D., Zhao, W.X., Zhan, Y.Y., Liu, B., Lin, S.C. and Wu, Q. p53 mediates the negative regulation of MDM2 by orphan receptor TR3. EMBO J. 25 (2006) 5703-5715.
• 26. Partovian, C., Zhuang, Z., Moodie, K., Lin, M., Ouchi, N., Sessa, W.C., Walsh, K. and Simons, M. PKCalpha activates eNOS and increases arterial blood flow in vivo. Circ. Res. 97 (2005) 482-487.
• 27. Chipuk, J.E., Kuwana, T., Bouchier-Hayes, L., Droin, N.M., Newmeyer, D.D., Schuler, M. and Green, D.R. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303 (2004) 1010-1014.
• 28. Lu, D., Huang, J. and Basu, A. Deregulation of PKB influences antiapoptotic signaling by PKC in breast cancer cells. Int. J. Oncol. 25 (2004) 671-676.
• 29. Wu, Q., Liu, S., Ding, L., Ye, X. and Su, W. PKC alpha translocation from mitochondria to nucleus is closely related to induction of apoptosis in gastric cancer cells. Science in China 45 (2002) 237-244.
• 30. Bunn, C.F., Neidig, J.A., Freidinger, K.E., Stankiewicz, T.A., Weaver, B.S., Mcgrew, J. and Allison, L.A. Nucleocytoplasmic shuttling of the thyroid hormone receptor alpha. Mol. Endocrinol. 15 (2001) 512-533.
• 31. Hermann, A., Maisel, M., Wegner, F., Liebau, S., Kim, D.W., Gerlach, M., Schwarz, J., Kim, K.S. and Storch, A. Multipotent neural stem cells from the adult tegmentum with dopaminergic potential develop essential properties of functional neurons. Stem Cells 24 (2006) 949-964.
• 32. Kolluri, S.K., Bruey-Sedano, N., Cao, X., Lin, B., Lin, F., Han, Y.H., Dawson, M.I. and Zhang, X.K. Mitogenic effect of orphan receptor TR3 and its regulation by MEKK1 in lung cancer cells. Mol. Cell Biol. 23 (2003) 8651-8667.
• 33. Balendran, A., Casamayor, A., Deak, M., Paterson, A., Gaffney, P., Currie, R., Downes, P.S., and Alessi, D.R. PDK1 acquires PDK2 activity in the presence of a synthetic peptide derived from the carboxyl terminus of PRK2. Curr. Biol. 9 (1999) 393-404.
• 34. Delcommenne, M., Tan, C., Gray, V., Rue, L., Woodgett, J. and Dedhar, S. Phosphoinositide-3-OH kinase-dependent regulation of glycogen synthase kinase 3 and protein kinase B/AKT by the integrin-linked kinase. Proc. Natl. Acad. Sci. USA 95 (1998) 11211-11216.
• 35. Peterson, R.T. and Schreiber, S.L. Kinase phosphorylation: Keeping it all in the family. Curr. Biol. 9 (1999) R521-R524.
• 36. Li, L., Sampat, K., Hu, N., Zakari, J. and Yuspa, S.H. Protein kinase C negatively regulates Akt activity and modifies UVC-induced apoptosis in mouse keratinocytes. J. Biol. Chem. 281 (2006) 3237-3243.
• 37. Munteanu, A., Taddei, M., Tamburini, I., Bergamini, E., Azzi, A. and Zingg, J.M. Antagonistic effects of oxidized low density lipoprotein and alphatocopherol on CD36 scavenger receptor expression in monocytes: involvement of protein kinase B and peroxisome proliferator-activated receptor-gamma. J. Biol. Chem. 281 (2006) 6489-6497.
• 38. Partovian, C. and Simons, M. Regulation of protein kinase B/Akt activity and Ser473 phosphorylation by protein kinase Calpha in endothelial cells. Cell Signal. 16 (2004) 951-957.
• 39. Galetic, I., Andjelkovic, M., Meier, R., Brodbeck, D., Park, J. and Hemmings, B.A. Mechanism of protein kinase B activation by insulin/insulin-like growth factor-1 revealed by specific inhibitors of phosphoinositide 3-kinase--significance for diabetes and cancer. Pharmacol. Ther. 82 (1999) 409-425.
• 40. Wen, H.C., Huang, W.C., Ali, A., Woodgett, J.R. and Lin, W.W. Negative regulation of phosphatidylinositol 3-kinase and Akt signalling pathway by PKC. Cell. Signal. 15 (2003) 37-45.
• 41. Wang, R. and Brattain, M.G. AKT can be activated in the nucleus. Cell. Signal. 18 (2006) 1722-1731.
• 42. Newton, A.C. Protein kinase C: structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions. Chem. Rev. 101 (2001) 2353-2364.
• 43. Martelli, A.M., Evangelisti, C., Nyakern, M. and Manzoli, F.A. Nuclear protein kinase C. Biochim. Biophys. Acta 1761 (2006) 542-551.
• 44. Eliyahu, E. and Shalgi, R. A role for protein kinase C during rat egg activation. Biol. Reprod. 67 (2002) 189-195.
• 45. Carter, C.A., Parham, G.P. and Chambers, T. Cytoskeletal reorganization induced by retinoic acid treatment of human endometrial adenocarcinoma (RL95-2) cells is correlated with alterations in protein kinase C-alpha. Pathobiology 66 (1998) 284-292.