Activation of nuclear factor κB (NF-κB) in prostate cancer is mediated by protein kinase C ∈ (PKC∈)

Journal of Biological Chemistry

Volumn 287, Issue 44, 2012, Pages 37570-37582

  Garg, Rachana ^a   Blando, Jorge ^b   Perez, Carlos J ^c   Wang, Hong Bin ^c   Benavides, Fernando J ^a   Kazanietz, Marcelo G ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C1 DOMAIN; NUCLEAR FACTORS; PROSTATE CANCERS; PROTEIN KINASE C;

BIOCHEMISTRY; BIOLOGY;

DISEASES;

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHOSPHATIDYLCHOLINE; PHOSPHOLIPASE C; PROTEIN KINASE C EPSILON; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED DEATH DOMAIN PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVATION; ENZYME ACTIVITY; EXPRESSION VECTOR; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, REPORTER; HUMANS; I-KAPPA B PROTEINS; LUCIFERASES, RENILLA; MALE; MICE; MICE, TRANSGENIC; NF-KAPPA B; PROSTATIC NEOPLASMS; PROTEIN BINDING; PROTEIN KINASE C-EPSILON; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA; TYPE C PHOSPHOLIPASES;

EID: 84868241317     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.398925     Document Type: Article

References (61)

1. Karin, M., and Lin, A. (2002) NF-κB at the crossroads of life and death. Nat. Immunol. 3, 221-227
2. May, M. J., and Ghosh, S. (1997) Rel/NF-κB and IκB proteins. An overview. Semin. Cancer Biol. 8, 63-73
3. Hayden, M. S., and Ghosh, S. (2004) Signaling to NF-κB. Genes Dev. 18, 2195-2224
4. Stock, D., Groome, P. A., and Siemens, D. R. (2008) Inflammation and prostate cancer. A future target for prevention and therapy? Urol. Clin. North Am. 35, 117-130
5. Suh, J., Payvandi, F., Edelstein, L. C., Amenta, P. S., Zong, W. X., Gélinas, C., and Rabson, A. B. (2002) Mechanisms of constitutive NF-κB activation in human prostate cancer cells. Prostate 52, 183-200
6. Madrid, L. V., and Baldwin, A. S., Jr. (2003) Regulation of NF-κB by oncoproteins and tumor suppressor proteins. Methods Mol. Biol. 223, 523-532
7. Romashkova, J. A., and Makarov, S. S. (1999) NF-κB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401, 86-90
8. Jin, R. J., Lho, Y., Connelly, L., Wang, Y., Yu, X., Saint Jean, L., Case, T. C., Ellwood-Yen, K., Sawyers, C. L., Bhowmick, N. A., Blackwell, T. S., Yull, F. E., and Matusik, R. J. (2008) The nuclear factor κB pathway controls the progression of prostate cancer to androgen-independent growth. Cancer Res. 68, 6762-6769
9. Shukla, S., MacLennan, G. T., Fu, P., Patel, J., Marengo, S. R., Resnick, M. I., and Gupta, S. (2004) Nuclear factor κB/p65 (Rel A) is constitutively activated in human prostate adenocarcinoma and correlates with disease progression. Neoplasia 6, 390-400
10. Zerbini, L. F., Wang, Y., Cho, J. Y., and Libermann, T. A. (2003) Constitutive activation of nuclear factor κB p50/p65 and Fra-1 and JunD is essential for deregulated interleukin 6 expression in prostate cancer. Cancer Res. 63, 2206-2215
11. Pahl, H. L. (1999) Activators and target genes of Rel/NF-κB transcription factors. Oncogene 18, 6853-6866
12. Chen, G., and Goeddel, D. V. (2002) TNF-R1 signaling. A beautiful pathway. Science 296, 1634-1635
13. MacEwan, D. J. (2002) TNF ligands and receptors. A matter of life and death. Br. J. Pharmacol. 135, 855-875
14. Diaz-Meco, M. T., and Moscat, J. (2012) The atypical PKCs in inflammation. NF-κB and beyond. Immunol. Rev. 246, 154-167
15. Ishiguro, H., Akimoto, K., Nagashima, Y., Kojima, Y., Sasaki, T., Ishiguro-Imagawa, Y., Nakaigawa, N., Ohno, S., Kubota, Y., and Uemura, H. (2009) aPKCλ/ ι promotes growth of prostate cancer cells in an autocrine manner through transcriptional activation of interleukin-6. Proc. Natl. Acad. Sci. U.S.A. 106, 16369-16374
16. Holden, N. S., Squires, P. E., Kaur, M., Bland, R., Jones, C. E., and Newton, R. (2008) Phorbol ester-stimulated NF-κB-dependent transcription. Roles for isoforms of novel protein kinase C. Cell. Signal. 20, 1338-1348
17. Lu, Z. G., Liu, H., Yamaguchi, T., Miki, Y., and Yoshida, K. (2009) Protein kinase CΔ activates RelA/p65 and nuclear factor κB signaling in response to tumor necrosis factor α. Cancer Res. 69, 5927-5935
18. Satoh, A., Gukovskaya, A. S., Nieto, J. M., Cheng, J. H., Gukovsky, I., Reeve, J. R., Jr., Shimosegawa, T., and Pandol, S. J. (2004) PKC-Δ and -∈ regulate NF-κB activation induced by cholecystokinin and TNF-α in pancreatic acinar cells. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G582-591
19. Aziz, M. H., Manoharan, H. T., Church, D. R., Dreckschmidt, N. E., Zhong, W., Oberley, T. D., Wilding, G., and Verma, A. K. (2007) Protein kinase C∈interacts with signal transducers and activators of transcription 3 (Stat3), phosphorylates Stat3Ser727, and regulates its constitutive activation in prostate cancer. Cancer Res. 67, 8828-8838
20. Basu, A., and Sivaprasad, U. (2007) Protein kinase C∈ makes the life and death decision. Cell. Signal. 19, 1633-1642
21. Griner, E. M., Caino, M. C., Sosa, M. S., Colón-González, F., Chalmers, M. J., Mischak, H., and Kazanietz, M. G. (2010) A novel cross-talk in diacylglycerol signaling. The Rac-GAP β2-chimaerin is negatively regulated by protein kinase CΔ-mediated phosphorylation. J. Biol. Chem. 285, 16931-16941
22. Gonzalez-Guerrico, A. M., and Kazanietz, M. G. (2005) Phorbol esterinduced apoptosis in prostate cancer cells via autocrine activation of the extrinsic apoptotic cascade. A key role for protein kinase C Δ. J. Biol. Chem. 280, 38982-38991
23. Gavrielides, M. V., Frijhoff, A. F., Conti, C. J., and Kazanietz, M. G. (2004) Protein kinase C and prostate carcinogenesis. Targeting the cell cycle and apoptotic mechanisms. Curr. Drug Targets 5, 431-443
24. Meshki, J., Caino, M. C., von Burstin, V. A., Griner, E., and Kazanietz, M. G. (2010) Regulation of prostate cancer cell survival by protein kinase C∈ involves bad phosphorylation and modulation of the TNFα/JNK pathway. J. Biol. Chem. 285, 26033-26040
25. Wu, D., Foreman, T. L., Gregory, C. W., McJilton, M. A., Wescott, G. G., Ford, O. H., Alvey, R. F., Mohler, J. L., and Terrian, D. M. (2002) Protein kinase C∈ has the potential to advance the recurrence of human prostate cancer. Cancer Res. 62, 2423-2429
26. Bae, K. M., Wang, H., Jiang, G., Chen, M. G., Lu, L., and Xiao, L. (2007) Protein kinase C∈ is overexpressed in primary human non-small cell lung cancers and functionally required for proliferation of non-small cell lung cancer cells in a p21/Cip1-dependent manner. Cancer Res. 67, 6053-6063
27. Gorin, M. A., and Pan, Q. (2009) Protein kinase C ∈. An oncogene and emerging tumor biomarker. Mol. Cancer 8, 9
28. Cornford, P., Evans, J., Dodson, A., Parsons, K., Woolfenden, A., Neoptolemos, J., and Foster, C. S. (1999) Protein kinase C isoenzyme patterns characteristically modulated in early prostate cancer. Am. J. Pathol. 154, 137-144
29. Koren, R., Ben Meir, D., Langzam, L., Dekel, Y., Konichezky, M., Baniel, J., Livne, P. M., Gal, R., and Sampson, S. R. (2004) Expression of protein kinase C isoenzymes in benign hyperplasia and carcinoma of prostate. Oncol. Rep. 11, 321-326
30. Benavides, F., Blando, J., Perez, C. J., Garg, R., Conti, C. J., DiGiovanni, J., and Kazanietz, M. G. (2011) Transgenic overexpression of PKC∈reneoplastic lesions. Cell Cycle 10, 268-277
31. von Burstin, V. A., Xiao, L., and Kazanietz, M. G. (2010) Bryostatin 1 inhibits phorbol ester-induced apoptosis in prostate cancer cells by differentially modulating protein kinase C (PKC) Δ translocation and preventing PKCΔ-mediated release of tumor necrosis factor α. Mol. Pharmacol. 78, 325-332
32. Shinohara, H., Kayagaki, N., Yagita, H., Oyaizu, N., Ohba, M., Kuroki, T., and Ikawa, Y. (2001) A protective role of PKC∈ against TNF-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in glioma cells. Biochem. Biophys. Res. Commun. 284, 1162-1167
33. Caloca, M. J., Fernandez, N., Lewin, N. E., Ching, D., Modali, R., Blumberg, P. M., and Kazanietz, M. G. (1997) β2-Chimaerin is a high-affinity receptor for the phorbol ester tumor promoters. J. Biol. Chem. 272, 26488-26496
34. Garg, R., Ramchandani, A. G., and Maru, G. B. (2008) Curcumin decreases 12-O-tetradecanoylphorbol-13-acetate-induced protein kinaseCtranslocation to modulate downstream targets in mouse skin. Carcinogenesis 29, 1249-1257
35. Garg, R., Ingle, A., and Maru, G. (2008) Dietary turmeric modulates DMBA-induced p21ras, MAP kinases and AP-1/NF-κB pathway to alter cellular responses during hamster buccal pouch carcinogenesis. Toxicol. Appl. Pharmacol. 232, 428-439
36. Yang, D., Kedei, N., Li, L., Tao, J., Velasquez, J. F., Michalowski, A. M., Tóth, B. I., Marincsák, R., Varga, A., Bíró, T., Yuspa, S. H., and Blumberg, P. M. (2010) RasGRP3 contributes to formation and maintenance of the prostate cancer phenotype. Cancer Res. 70, 7905-7917
37. Gandellini, P., Folini, M., Longoni, N., Pennati, M., Binda, M., Colecchia, M., Salvioni, R., Supino, R., Moretti, R., Limonta, P., Valdagni, R., Daidone, M. G., and Zaffaroni, N. (2009) miR-205 Exerts tumor-suppressive functions in human prostate through down-regulation of protein kinase C∈.Cancer Res. 69, 2287-2295
38. Lavalle, C. R., Bravo-Altamirano, K., Giridhar, K. V., Chen, J., Sharlow, E., Lazo, J. S., Wipf, P., and Wang, Q. J. (2010) Novel protein kinase D inhibitors cause potent arrest in prostate cancer cell growth and motility. BMC Chem. Biol. 10, 5
39. Caino, M. C., von Burstin, V. A., Lopez-Haber, C., and Kazanietz, M. G. (2011) Differential regulation of gene expression by protein kinase C isozymes as determined by genome-wide expression analysis. J. Biol. Chem. 286, 11254-11264
40. Begley, R., Liron, T., Baryza, J., and Mochly-Rosen, D. (2004) Biodistribution of intracellularly acting peptides conjugated reversibly to Tat. Biochem. Biophys. Res. Commun. 318, 949-954
41. Griner, E. M., and Kazanietz, M. G. (2007) Protein kinase C and other diacylglycerol effectors in cancer. Nat. Rev. Cancer 7, 281-294
42. Fujii, T., García-Bermejo, M. L., Bernabó, J. L., Caamaño, J., Ohba, M., Kuroki, T., Li, L., Yuspa, S. H., and Kazanietz, M. G. (2000) Involvement of protein kinase C Δ (PKCΔ) in phorbol ester-induced apoptosis in LNCaP prostate cancer cells. Lack of proteolytic cleavage of PKCΔ. J. Biol. Chem. 275, 7574-7582
43. Wang, S., Kazanietz, M. G., Blumberg, P. M., Marquez, V. E., and Milne, G. W. (1996) Molecular modeling and site-directed mutagenesis studies of a phorbol ester-binding site in protein kinase C. J. Med. Chem. 39, 2541-2553
44. Hammond, G., Thomas, C., and Schiavo, G. (2004) in Phosphoinositides in Subcellular Targeting and Enzyme Activation (Stenmark, H. ed) Vol. 282, pp. 177-206, Springer Publishing, Berlin
45. Schütze, S., Berkovic, D., Tomsing, O., Unger, C., and Krönke, M. (1991) Tumor necrosis factor induces rapid production of 1′2′ diacylglycerol by a phosphatidylcholine-specific phospholipase C. J. Exp. Med. 174, 975-988
46. Micheau, O., and Tschopp, J. (2003) Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114, 181-190
47. Yemelyanov, A., Gasparian, A., Lindholm, P., Dang, L., Pierce, J. W., Kisseljov, F., Karseladze, A., and Budunova, I. (2006) Effects of IKK inhibitor PS1145 on NF-κB function, proliferation, apoptosis and invasion activity in prostate carcinoma cells. Oncogene 25, 387-398
48. Fernandez-Marcos, P. J., Abu-Baker, S., Joshi, J., Galvez, A., Castilla, E. A., Cañamero, M., Collado, M., Saez, C., Moreno-Bueno, G., Palacios, J., Leitges, M., Serrano, M., Moscat, J., and Diaz-Meco, M. T. (2009) Simultaneous inactivation of Par-4 and PTEN in vivo leads to synergistic NF-κB activation and invasive prostate carcinoma. Proc. Natl. Acad. Sci. U.S.A. 106, 12962-12967
49. Min, J., Zaslavsky, A., Fedele, G., McLaughlin, S. K., Reczek, E. E., De Raedt, T., Guney, I., Strochlic, D. E., Macconaill, L. E., Beroukhim, R., Bronson, R. T., Ryeom, S., Hahn, W. C., Loda, M., and Cichowski, K. (2010) An oncogene-tumor suppressor cascade drives metastatic prostate cancer by coordinately activating Ras and nuclear factor-κB. Nat. Med. 16, 286-294
50. Win, H. Y., and Acevedo-Duncan, M. (2008) Atypical protein kinase C phosphorylates IKKαβ in transformed non-malignant and malignant prostate cell survival. Cancer Lett. 270, 302-311
51. Hafeez, B. B., Zhong, W., Weichert, J., Dreckschmidt, N. E., Jamal, M. S., and Verma, A. K. (2011) Genetic ablation of PKC∈ inhibits prostate cancer development and metastasis in transgenic mouse model of prostate adenocarcinoma. Cancer Res. 71, 2318-2327
52. Mischak, H., Goodnight, J. A., Kolch, W., Martiny-Baron, G., Schaechtle, C., Kazanietz, M. G., Blumberg, P. M., Pierce, J. H., and Mushinski, J. F. (1993) Overexpression of protein kinase C-Δ and -∈ in NIH 3T3 cells induces opposite effects on growth, morphology, anchorage dependence, and tumorigenicity. J. Biol. Chem. 268, 6090-6096
53. Tojima, Y., Fujimoto, A., Delhase, M., Chen, Y., Hatakeyama, S., Nakayama, K., Kaneko, Y., Nimura, Y., Motoyama, N., Ikeda, K., Karin, M., and Nakanishi, M. (2000) NAK is an IκB kinase-activating kinase. Nature 404, 778-782
54. Chang, Q., and Tepperman, B. L. (2003) Effect of selective PKC isoform activation and inhibition on TNF-α-induced injury and apoptosis in human intestinal epithelial cells. Br. J. Pharmacol. 140, 41-52
55. Kilpatrick, L. E., Sun, S., and Korchak, H. M. (2004) Selective regulation by Δ-PKC and PI 3-kinase in the assembly of the antiapoptotic TNFR-1 signaling complex in neutrophils. Am. J. Physiol. Cell Physiol. 287, C633-642
56. Wang, H., and Kazanietz, M. G. (2010) p23/Tmp21 differentially targets the Rac-GAP β2-chimaerin and protein kinase C via their C1 domains. Mol. Biol. Cell 21, 1398-1408
57. Jaken, S., and Parker, P. J. (2000) Protein kinase C binding partners. Bio-Essays 22, 245-254
58. Bao, L., Gorin, M. A., Zhang, M., Ventura, A. C., Pomerantz, W. C., Merajver, S. D., Teknos, T. N., Mapp, A. K., and Pan, Q. (2009) Preclinical development of a bifunctional cancer cell homing, PKC∈ inhibitory peptide for the treatment of head and neck cancer. Cancer Res. 69, 5829-5834
59. Koyanagi, T., Noguchi, K., Ootani, A., Inagaki, K., Robbins, R. C., and Mochly-Rosen, D. (2007) Pharmacological inhibition of ∈ PKC suppresses chronic inflammation in murine cardiac transplantation model. J. Mol. Cell Cardiol. 43, 517-522
60. Caino, M. C., Lopez-Haber, C., Kim, J., Mochly-Rosen, D., and Kazanietz, M. G. (2012) Proteins kinase Cvar∈ is required for non-small cell lung carcinoma growth and regulates the expression of apoptotic genes. Oncogene 31, 2593-2600
61. Caino, M. C., Lopez-Haber, C., Kissil, J. L., and Kazanietz, M. G. (2012) Non-small cell lung carcinoma cell motility, rac activation and metastatic dissemination are mediated by protein kinase C ∈. PLoS ONE 7, e31714