Cytosolic phospholipase A2α sustains pAKT, pERK and AR levels in PTEN-null/mutated prostate cancer cells

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1831, Issue 6, 2013, Pages 1146-1157

  Hua, Sheng ^a   Yao, Mu ^a   Vignarajan, Soma ^a   Witting, Paul ^b   Hejazi, Leila ^c   Gong, Zhen ^a   Teng, Ying ^a   Niknami, Marzieh ^b   Assinder, Stephen ^b   Richardson, Des ^b   Dong, Qihan ^a,b,c  

^a ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF WESTERN SYDNEY   (Australia)

Author keywords

AKT; AR; cPLA2 ; ERK; Prostate cancer; PTEN

Indexed keywords

5 HYDROXYICOSATETRAENOIC ACID; ANDROGEN RECEPTOR; ARACHIDONIC ACID; CYCLIN D1; CYTOSOLIC PHOSPHOLIPASE A2; CYTOSOLIC PHOSPHOLIPASE A2 ALPHA; DOXORUBICIN; EFIPLADIB; GLYCOGEN SYNTHASE KINASE 3BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; AR PROTEIN, HUMAN; DOXYCYCLINE; FATTY ACID; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE A2 GROUP IV; PROSTATE SPECIFIC ANTIGEN; PTEN PROTEIN, HUMAN;

ARTICLE; CANCER CELL CULTURE; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FRAMESHIFT MUTATION; GENE DELETION; GENE SILENCING; HUMAN; HUMAN CELL; MALE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; APOPTOSIS; DRUG ANTAGONISM; DRUG EFFECT; ENZYME IMMUNOASSAY; GENETICS; IMMUNOPRECIPITATION; METABOLISM; MUTATION; PATHOLOGY; PHOSPHORYLATION; PROSTATE TUMOR; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANTI-BACTERIAL AGENTS; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; DOXYCYCLINE; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FATTY ACIDS; GROUP IV PHOSPHOLIPASES A2; HUMANS; IMMUNOENZYME TECHNIQUES; IMMUNOPRECIPITATION; MALE; MUTATION; PHOSPHORYLATION; PROSTATE-SPECIFIC ANTIGEN; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ANDROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

MLCS; MLOWN;

EID: 84876945882     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2013.02.011     Document Type: Article

References (61)

1. B. Vanhaesebroeck, S.J. Leevers, K. Ahmadi, J. Timms, R. Katso, P.C. Driscoll, R. Woscholski, P.J. Parker, and M.D. Waterfield Synthesis and function of 3-phosphorylated inositol lipids Annu. Rev. Biochem. 70 2001 535 602
2. N. Chalhoub, and S.J. Baker PTEN and the PI3-kinase pathway in cancer Annu. Rev. Pathol. 4 2009 127 150
3. A. Bellacosa, C.C. Kumar, A. Di Cristofano, and J.R. Testa Activation of AKT kinases in cancer: implications for therapeutic targeting Adv. Cancer Res. 94 2005 29 86
4. S.N. Malik, M. Brattain, P.M. Ghosh, D.A. Troyer, T. Prihoda, R. Bedolla, and J.I. Kreisberg Immunohistochemical demonstration of phospho-Akt in high Gleason grade prostate cancer Clin. Cancer Res. 8 2002 1168 1171
5. M. Sun, G. Wang, J.E. Paciga, R.I. Feldman, Z.Q. Yuan, X.L. Ma, S.A. Shelley, R. Jove, P.N. Tsichlis, S.V. Nicosia, and J.Q. Cheng AKT1/PKBalpha kinase is frequently elevated in human cancers and its constitutive activation is required for oncogenic transformation in NIH3T3 cells Am. J. Pathol. 159 2001 431 437
6. J.I. Kreisberg, S.N. Malik, T.J. Prihoda, R.G. Bedolla, D.A. Troyer, S. Kreisberg, and P.M. Ghosh Phosphorylation of Akt (Ser473) is an excellent predictor of poor clinical outcome in prostate cancer Cancer Res. 64 2004 5232 5236
7. P. McCall, C.J. Witton, S. Grimsley, K.V. Nielsen, and J. Edwards Is PTEN loss associated with clinical outcome measures in human prostate cancer? Br. J. Cancer 99 2008 1296 1301
8. N.Y. Kalaany, and D.M. Sabatini Tumours with PI3K activation are resistant to dietary restriction Nature 458 2009 725 731 (Epub 2009 Mar 2011)
9. K.E. O'Reilly, F. Rojo, Q.B. She, D. Solit, G.B. Mills, D. Smith, H. Lane, F. Hofmann, D.J. Hicklin, D.L. Ludwig, J. Baselga, and N. Rosen mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt Cancer Res. 66 2006 1500 1508
10. S. Grant Cotargeting survival signaling pathways in cancer J. Clin. Invest. 118 2008 3003 3006
11. J.D. Debes, and D.J. Tindall Mechanisms of androgen-refractory prostate cancer N. Engl. J. Med. 351 2004 1488 1490
12. M.E. Grossmann, H. Huang, and D.J. Tindall Androgen receptor signaling in androgen-refractory prostate cancer J. Natl Cancer Inst. 93 2001 1687 1697
13. H.I. Scher, and C.L. Sawyers Biology of progressive, castration-resistant prostate cancer: directed therapies targeting the androgen-receptor signaling axis J. Clin. Oncol. 23 2005 8253 8261
14. M.E. Taplin, and S.P. Balk Androgen receptor: a key molecule in the progression of prostate cancer to hormone independence J. Cell. Biochem. 91 2004 483 490
15. C.D. Chen, D.S. Welsbie, C. Tran, S.H. Baek, R. Chen, R. Vessella, M.G. Rosenfeld, and C.L. Sawyers Molecular determinants of resistance to antiandrogen therapy Nat. Med. 10 2004 33 39
16. X. Yuan, and S.P. Balk Mechanisms mediating androgen receptor reactivation after castration Urol. Oncol. 27 2009 36 41
17. M. Hambek, M. Baghi, J. Wagenblast, J. Schmitt, H. Baumann, and R. Knecht Inverse correlation between serum PGE2 and T classification in head and neck cancer Head Neck 29 2007 244 248
18. D. Wang, H. Wang, Q. Shi, S. Katkuri, W. Walhi, B. Desvergne, S.K. Das, S.K. Dey, and R.N. DuBois Prostaglandin E(2) promotes colorectal adenoma growth via transactivation of the nuclear peroxisome proliferator-activated receptor delta Cancer Cell 6 2004 285 295
19. D. Wang, and R.N. Dubois Eicosanoids and cancer Nat. Rev. Cancer 10 2010 181 193
20. S. Hassan, and R.E. Carraway Involvement of arachidonic acid metabolism and EGF receptor in neurotensin-induced prostate cancer PC3 cell growth Regul. Pept. 133 2006 105 114
21. M. Hughes-Fulford, C.F. Li, J. Boonyaratanakornkit, and S. Sayyah Arachidonic acid activates phosphatidylinositol 3-kinase signaling and induces gene expression in prostate cancer Cancer Res. 66 2006 1427 1433
22. R.S. Pruthi, J.E. Derksen, D. Moore, C.C. Carson, G. Grigson, C. Watkins, and E. Wallen Phase II trial of celecoxib in prostate-specific antigen recurrent prostate cancer after definitive radiation therapy or radical prostatectomy Clin. Cancer Res. 12 2006 2172 2177
23. M.R. Smith, J. Manola, D.S. Kaufman, W.K. Oh, G.J. Bubley, and P.W. Kantoff Celecoxib versus placebo for men with prostate cancer and a rising serum prostate-specific antigen after radical prostatectomy and/or radiation therapy J. Clin. Oncol. 24 2006 2723 2728
24. M.I. Patel, C. Kurek, and Q. Dong The arachidonic acid pathway and its role in prostate cancer development and progression J. Urol. 179 2008 1668 1675
25. J. Cuzick, F. Otto, J.A. Baron, P.H. Brown, J. Burn, P. Greenwald, J. Jankowski, C. La Vecchia, F. Meyskens, H.J. Senn, and M. Thun Aspirin and non-steroidal anti-inflammatory drugs for cancer prevention: an international consensus statement Lancet Oncol. 10 2009 501 507
26. B.S. Cummings Phospholipase A2 as targets for anti-cancer drugs Biochem. Pharmacol. 74 2007 949 959
27. Q. Dong, M. Patel, K.F. Scott, G.G. Graham, P.J. Russell, and P. Sved Oncogenic action of phospholipase A2 in prostate cancer Cancer Lett. 240 2006 9 16
28. C.C. Leslie Regulation of the specific release of arachidonic acid by cytosolic phospholipase A2 Prostaglandins Leukot. Essent. Fatty Acids 70 2004 373 376
29. D.E. Tucker, M. Ghosh, F. Ghomashchi, R. Loper, S. Suram, B.S. John, M. Girotti, J.G. Bollinger, M.H. Gelb, and C.C. Leslie Role of phosphorylation and basic residues in the catalytic domain of cytosolic phospholipase A2alpha in regulating interfacial kinetics and binding and cellular function J. Biol. Chem. 284 2009 9596 9611
30. M.I. Patel, J. Singh, M. Niknami, C. Kurek, M. Yao, S. Lu, F. Maclean, N.J. King, M.H. Gelb, K.F. Scott, P.J. Russell, J. Boulas, and Q. Dong Cytosolic phospholipase A2-alpha: a potential therapeutic target for prostate cancer Clin. Cancer Res. 14 2008 8070 8079
31. M.F. McEntee, C. Ziegler, D. Reel, K. Tomer, A. Shoieb, M. Ray, X. Li, N. Neilen, F.B. Lih, D. O'Rourke, and J. Whelan Dietary n-3 polyunsaturated fatty acids enhance hormone ablation therapy in androgen-dependent prostate cancer Am. J. Pathol. 173 2008 229 241 (Epub 2008 Jun 2013)
32. U.P. Kelavkar, J. Hutzley, R. Dhir, P. Kim, K.G. Allen, and K. McHugh Prostate tumor growth and recurrence can be modulated by the omega-6:omega-3 ratio in diet: athymic mouse xenograft model simulating radical prostatectomy Neoplasia 8 2006 112 124
33. I.M. Berquin, Y. Min, R. Wu, J. Wu, D. Perry, J.M. Cline, M.J. Thomas, T. Thornburg, G. Kulik, A. Smith, I.J. Edwards, R. D'Agostino, H. Zhang, H. Wu, J.X. Kang, and Y.Q. Chen Modulation of prostate cancer genetic risk by omega-3 and omega-6 fatty acids J. Clin. Invest. 117 2007 1866 1875
34. J.A. Locke, E.S. Guns, M.L. Lehman, S. Ettinger, A. Zoubeidi, A. Lubik, K. Margiotti, L. Fazli, H. Adomat, K.M. Wasan, M.E. Gleave, and C.C. Nelson Arachidonic acid activation of intratumoral steroid synthesis during prostate cancer progression to castration resistance Prostate 70 2010 239 251
35. A.A. Chaudry, K.W. Wahle, S. McClinton, and L.E. Moffat Arachidonic acid metabolism in benign and malignant prostatic tissue in vitro: effects of fatty acids and cyclooxygenase inhibitors Int. J. Cancer 57 1994 176 180
36. M. Niknami, Q. Dong, and P.K. Witting Pitfalls in the use of arachidonic acid oxidation products to assign lipoxygenase activity in cancer cells Free Radic. Res. 43 2009 951 956
37. P.C. Norris, and E.A. Dennis Omega-3 fatty acids cause dramatic changes in TLR4 and purinergic eicosanoid signaling Proc. Natl. Acad. Sci. U. S. A. 109 2012 8517 8522
38. M. Yao, C. Xie, M. Constantine, S. Hua, B.D. Hambly, G. Jardine, P. Sved, and Q. Dong How can food extracts consumed in the Mediterranean and East Asia suppress prostate cancer proliferation? Br. J. Nutr. 108 2012 424 430
39. J. Li, C. Yen, D. Liaw, K. Podsypanina, S. Bose, S.I. Wang, J. Puc, C. Miliaresis, L. Rodgers, R. McCombie, S.H. Bigner, B.C. Giovanella, M. Ittmann, B. Tycko, H. Hibshoosh, M.H. Wigler, and R. Parsons PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer Science 275 1997 1943 1947
40. W.D. Tilley, J.M. Bentel, J.O. Aspinall, R.E. Hall, and D.J. Horsfall Evidence for a novel mechanism of androgen resistance in the human prostate cancer cell line, PC-3 Steroids 60 1995 180 186
41. M. Niknami, S. Vignarajan, M. Yao, S. Hua, P.K. Witting, Y. Kita, T. Shimizu, P. Sved, M.I. Patel, and Q. Dong Decrease in expression or activity of cytosolic phospholipase A2alpha increases cyclooxygenase-1 action: a cross-talk between key enzymes in arachidonic acid pathway in prostate cancer cells Biochim. Biophys. Acta 1801 2010 731 737
42. M. Abramovitz, E. Wong, M.E. Cox, C.D. Richardson, C. Li, and P.J. Vickers 5-Lipoxygenase-activating protein stimulates the utilization of arachidonic acid by 5-lipoxygenase Eur. J. Biochem. 215 1993 105 111
43. J.C. McKew, K.L. Lee, M.W. Shen, P. Thakker, M.A. Foley, M.L. Behnke, B. Hu, F.W. Sum, S. Tam, Y. Hu, L. Chen, S.J. Kirincich, R. Michalak, J. Thomason, M. Ipek, K. Wu, L. Wooder, M.K. Ramarao, E.A. Murphy, D.G. Goodwin, L. Albert, X. Xu, F. Donahue, M.S. Ku, J. Keith, C.L. Nickerson-Nutter, W.M. Abraham, C. Williams, M. Hegen, and J.D. Clark Indole cytosolic phospholipase A2 alpha inhibitors: discovery and in vitro and in vivo characterization of 4-{3-[5-chloro-2-(2-{[(3,4-dichlorobenzyl)sulfonyl]amino}ethyl) -1-(diphenylmethyl)-1H-indol-3-yl]propylbenzoic acid, efipladib J. Med. Chem. 51 2008 3388 3413
44. N.G. Nickols, and P.B. Dervan Suppression of androgen receptor-mediated gene expression by a sequence-specific DNA-binding polyamide Proc. Natl. Acad. Sci. U. S. A. 104 2007 10418 10423
45. D.A. Cross, D.R. Alessi, P. Cohen, M. Andjelkovich, and B.A. Hemmings Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B Nature 378 1995 785 789
46. R.J. Vlietstra, D.C. van Alewijk, K.G. Hermans, G.J. van Steenbrugge, and J. Trapman Frequent inactivation of PTEN in prostate cancer cell lines and xenografts Cancer Res. 58 1998 2720 2723
47. G. Rodriguez-Berriguete, B. Fraile, P. Martinez-Onsurbe, G. Olmedilla, R. Paniagua, and M. Royuela MAP kinases and prostate cancer J. Signal Transduct. 2012 2012 169170
48. E.G. Bluemn, and P.S. Nelson The androgen/androgen receptor axis in prostate cancer Curr. Opin. Oncol. 24 2012 251 257
49. C. Rommel, G. Radziwill, J. Lovric, J. Noeldeke, T. Heinicke, D. Jones, A. Aitken, and K. Moelling Activated Ras displaces 14-3-3 protein from the amino terminus of c-Raf-1 Oncogene 12 1996 609 619
50. S. Zimmermann, and K. Moelling Phosphorylation and regulation of Raf by Akt (protein kinase B) Science 286 1999 1741 1744
51. L.O. Murphy, and J. Blenis MAPK signal specificity: the right place at the right time Trends Biochem. Sci. 31 2006 268 275
52. X. Wu, S.J. Noh, G. Zhou, J.E. Dixon, and K.L. Guan Selective activation of MEK1 but not MEK2 by A-Raf from epidermal growth factor-stimulated Hela cells J. Biol. Chem. 271 1996 3265 3271
53. Y. Xu, S.Y. Chen, K.N. Ross, and S.P. Balk Androgens induce prostate cancer cell proliferation through mammalian target of rapamycin activation and post-transcriptional increases in cyclin D proteins Cancer Res. 66 2006 7783 7792
54. Z.X. Zhou, M.V. Lane, J.A. Kemppainen, F.S. French, and E.M. Wilson Specificity of ligand-dependent androgen receptor stabilization: receptor domain interactions influence ligand dissociation and receptor stability Mol. Endocrinol. 9 1995 208 218
55. C. Gupta, and A.S. Goldman The arachidonic acid cascade is involved in the masculinizing action of testosterone on embryonic external genitalia in mice Proc. Natl. Acad. Sci. U. S. A. 83 1986 4346 4349
56. S. Ha, R. Ruoff, N. Kahoud, T.F. Franke, and S.K. Logan Androgen receptor levels are pregulated by Akt in prostate cancer Endocr.-Relat. Cancer 18 2011 245 255
57. M. Manin, S. Baron, K. Goossens, C. Beaudoin, C. Jean, G. Veyssiere, G. Verhoeven, and L. Morel Androgen receptor expression is regulated by the phosphoinositide 3-kinase/Akt pathway in normal and tumoral epithelial cells Biochem. J. 366 2002 729 736
58. Z.H. Wen, Y.C. Su, P.L. Lai, Y. Zhang, Y.F. Xu, A. Zhao, G.Y. Yao, C.H. Jia, J. Lin, S. Xu, L. Wang, X.K. Wang, A.L. Liu, Y. Jiang, Y.F. Dai, and X.C. Bai Critical role of arachidonic acid-activated mTOR signaling in breast carcinogenesis and angiogenesis Oncogene 32 2012 160 170
59. M.K. Ramarao, M.W. Shen, E.A. Murphy, W. Duan, Y. Zhao, J. McKew, K.L. Lee, P. Thakker, M.L. Behnke, and J.D. Clark Thermodynamic characterization of cytosolic phospholipase A2 alpha inhibitors Anal. Biochem. 383 2008 217 225
60. S.P. Herbert, A.F. Odell, S. Ponnambalam, and J.H. Walker Activation of cytosolic hospholipase A2-{alpha} as a novel mechanism regulating endothelial cell cycle progression and angiogenesis J. Biol. Chem. 284 2009 5784 5796
61. Z. Ni, N.M. Okeley, B.P. Smart, and M.H. Gelb Intracellular actions of group IIA secreted phospholipase A2 and group IVA cytosolic phospholipase A2 contribute to arachidonic acid release and prostaglandin production in rat gastric mucosal cells and transfected human embryonic kidney cells J. Biol. Chem. 281 2006 16245 16255