Omega-3 PUFA ethanolamides DHEA and EPEA induce autophagy through PPARγ activation in MCF-7 breast cancer cells

Journal of Cellular Physiology

Volumn 228, Issue 6, 2013, Pages 1314-1322

  Rovito, Daniela ^a   Giordano, Cinzia ^a   Vizza, Donatella ^a   Plastina, Pierluigi ^a   Barone, Ines ^a   Casaburi, Ivan ^a   Lanzino, Marilena ^a   De Amicis, Francesca ^a   Sisci, Diego ^a   Mauro, Loredana ^a   Aquila, Saveria ^a   Catalano, Stefania ^a   Bonofiglio, Daniela ^a   Andò, Sebastiano ^a  

^a UNIVERSITY OF CALABRIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BECLIN 1; DOCOSAHEXAENOIC ACID; DOCOSAHEXAENOYL ETHANOLAMINE; EICOSAPENTAENOYL ETHANOLAMINE; ETHANOLAMINE DERIVATIVE; ICOSAPENTAENOIC ACID; MAMMALIAN TARGET OF RAPAMYCIN; MICROTUBULE ASSOCIATED PROTEIN 1; OMEGA 3 FATTY ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN BCL 2; PROTEIN KINASE B; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BREAST CANCER; CANCER CELL CULTURE; CANCER INHIBITION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIETARY INTAKE; DNA FRAGMENTATION; ENZYME ACTIVATION; FEMALE; HUMAN; HUMAN CELL; IC 50; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; LIGHT CHAIN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSCRIPTION INITIATION;

ANTINEOPLASTIC AGENTS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BREAST NEOPLASMS; CELL PROLIFERATION; CELL SURVIVAL; DOCOSAHEXAENOIC ACIDS; DOSE-RESPONSE RELATIONSHIP, DRUG; EICOSAPENTAENOIC ACID; ETHANOLAMINE; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MCF-7 CELLS; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; PPAR GAMMA; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; PTEN PHOSPHOHYDROLASE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TOR SERINE-THREONINE KINASES; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; UP-REGULATION;

EID: 84874218519     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24288     Document Type: Article

References (49)

1. Allred CD, Talbert DR, Southard RC, Wang X, Kilgore MW. 2008. PPARgamma1 as a molecular target of eicosapentaenoic acid in human colon cancer (HT-29) cells. J Nutr 138:250-256.
2. Biederbick A, Kern HF, Elsässer HP. 1995. Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. Eur J Cell Biol 66:3-14.
3. Bonofiglio D, Gabriele S, Aquila S, Catalano S, Gentile M, Middea E, Giordano F, Andò S. 2005. Estrogen receptor alpha binds to peroxisome proliferator-activated receptor (PPAR) response element and negatively interferes with PPARgamma signalling in breast cancer cells. Clin Cancer Res 11:6139-6147.
4. Bonofiglio D, Aquila S, Catalano S, Gabriele S, Belmonte M, Middea E, Qi H, Morelli C, Gentile M, Maggiolini M, Andò S. 2006. Peroxisome proliferator-activated receptoractivates p53 gene promoter binding to the nuclear factor-kappa B sequence in human MCF7 breast cancer cells. Mol Endocrinol 20:3083-3092.
5. Bonofiglio D, Gabriele S, Aquila S, Qi H, Belmonte M, Catalano S, Andò S. 2009a. Peroxisome proliferator-activated receptoractivates fas ligand gene promoter inducing apoptosis in human breast cancer cells. Breast Cancer Res Treat 113:423-434.
6. Bonofiglio D, Cione E, Qi H, Pingitore A, Perri M, Catalano S, Vizza D, Panno ML, Genchi G, Fuqua SA, Andò S. 2009b. Combined low doses of PPARgamma and RXR ligands trigger an intrinsic apoptotic pathway in human breast cancer cells. Am J Pathol 175:1270-1280.
7. Bougnoux P, Hajjaji N, Maheo K, Couet C, Chevalier S. 2010. Fatty acids and breast cancer: Sensitization to treatments and prevention of metastatic re-growth. Prog Lipid Res 49:76-86.
8. Brown I, Wahle KW, Cascio MG, Smoum-Jaouni R, Mechoulam R, Pertwee RG, Heys SD. 2011. Omega-3 N-acylethanolamines are endogenously synthesised from omega-3 fatty acids in different human prostate and breast cancer cell lines. Prostaglandins Leukot Essent Fatty Acids 85:305-310.
9. Chapkin RS, McMurray DN, Lupton JR. 2007. Colon cancer, fatty acids and anti-inflammatory compounds. Curr Opin Gastroenterol 23:48-54.
10. Chapkin RS, McMurray DN, Davidson LA, Patil BS, Fan YY, Lupton JR. 2008. Bioactive dietary long-chain fatty acids: Emerging mechanisms of action. Br J Nutr 100:1152-1157.
11. Chiacchiera F, Simone C. 2008. Signal-dependent regulation of gene expression as a target for cancer treatment: Inhibiting p38alpha in colorectal tumors. Cancer Lett 265:16-26.
12. Cohen LA. 1997. Breast cancer risk in rats fed a diet high in n-6 polyunsaturated fatty acids during pregnancy. J Natl Cancer Inst 89:662-663.
13. Comes F, Matrone A, Lastella P, Nico B, Susca FC, Bagnulo R, Ingravallo G, Modica S, Lo Sasso G, Moschetta A, Guanti G, Simone C. 2007. A novel cell type-specific role of p38alpha in the control of autophagy and cell death in colorectal cancer cells. Cell Death Differ 14:693-702.
14. Courtney ED, Matthews S, Finlayson C, Di Pierro D, Belluzzi A, Roda E, Kang JY, Leicester RJ. 2007. Eicosapentaenoic acid (EPA) reduces crypt cell proliferation and increases apoptosis in normal colonic mucosa in subjects with a history of colorectal adenomas. Int J Colorectal Dis 22:765-776.
15. DeGraffenried LA, Friedrichs WE, Fulcher L, Fernandes G, Silva JM, Peralba JM, Hidalgo M. 2003. Eicosapentaenoic acid restores tamoxifen sensitivity in breast cancer cells with high Akt activity. Ann Oncol 14:1051-1056.
16. Desvergne B, Wahli W. 1999. Peroxisome proliferator-activated receptors: Nuclear control of metabolism. Endocr Rev 20:649-688.
17. Evans LM, Hardy RW. 2010. Optimizing dietary fat to reduce breast cancer risk: Are we there yet? Open Breast Cancer J 2:108-122.
18. Fradet V, Cheng I, Casey G, Witte JS. 2009. Dietary omega-3 fatty acids, cyclooxygenase-2 genetic variation, and aggressive prostate cancer risk. Clin Cancer Res 15:2559-2566.
19. Gani OA. 2008. Are fish oil omega-3 long-chain fatty acids and their derivatives peroxisome proliferator-activated receptor agonists? Cardiovasc Diabetol 20:1-6.
20. Glade MJ. 1999. Food, nutrition, and the prevention of cancer: A global perspective. American Institute for Cancer Research/World Cancer Research Fund, American Institute for Cancer Research, 1997. Nutrition 15:523-526.
21. Gleissman H, Johnsen JI, Kogner P. 2010. Omega-3 fatty acids in cancer, the protectors of good and the killers of evil? Exp Cell Res 316:1365-1373.
22. Gu G, Barone I, Gelsomino L, Giordano C, Bonofiglio D, Statti G, Menichini F, Catalano S, Andò S. 2012. Oldenlandia diffusa extracts exert antiproliferative and apoptotic effects on human breast cancer cells through ERα/Sp1-mediated p53 activation. J Cell Physiol 227:3363-3372.
23. Hammamieh R, Chakraborty N, Miller SA, Waddy E, Barmada M, Das R, Peel SA, Day AA, Jett M. 2007. Differential effects of omega-3 and omega-6 fatty acids on gene expression in breast cancer cells. Breast Cancer Res Treat 101:7-16.
24. Hihi AK, Michalik L, Wahli W. 2002. PPARs: Transcriptional effectors of fatty acids and their derivatives. Cell Mol Life Sci 59:790-798.
25. Hyde CA, Missailidis S. 2009. Inhibition of arachidonic acid metabolism and its implication on cell proliferation and tumour-angiogenesis. Int Immunopharmacol 9:701-715.
26. Ito T, Deng X, Carr B, May WS. 1997. Bcl-2 phosphorylation required for anti-apoptosis function. J Biol Chem 272:11671-11673.
27. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. 2011. Global cancer statistics. CA Cancer J Clin 61:69-90.
28. Kang KS, Wang P, Yamabe N, Fukui M, Jay T, Zhu BT. 2010. Docosahexaenoic acid induces apoptosis in MCF-7 cells in vitro and in vivo via reactive oxygen species formation and caspase 8 activation. PLoS ONE 5:e10296.
29. Lanson M, Bougnoux P, Besson P, Lansac J, Hubert B, Couet C, Le Floch O. 1990. N-6 polyunsaturated fatty acids in human breast carcinoma phosphatidylethanolamine and early relapse. Br J Cancer 61:776-778.
30. Levine B, Deretic V. 2007. Unveiling the roles of autophagy in innate and adaptive immunity. Nat Rev Immunol 7:767-777.
31. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B. 1999. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402:672-676.
32. Martin H. 2009. Role of PPAR-gamma in inflammation. Prospects for therapeutic intervention by food components. Mutat Res 669:1-7.
33. Patel L, Pass I, Coxon P, Downes CP, Smith SA, Macphee CH. 2001. Tumor suppressor and anti-inflammatory actions of PPARgamma agonist are mediated via up-regulation of PTEN. Curr Biol 11:764-768.
34. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. 2005. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122:927-939.
35. Plastina P, Meijerink J, Vincken JP, Gruppen H, Witkamp R, Gabriele B. 2009. Selective synthesis of unsaturated N-acylethanolamines by lipase-catalyzed N-acylation of ethanolamine with unsaturated fatty acids. Lett Org Chem 6:444-447.
36. Rocchi S, Auwerx J. 1999. Peroxisome proliferator-activated receptor-gamma: A versatile metabolic regulator. Ann Med 31:342-351.
37. Rock CL, Demark-Wahnefried W. 2002. Nutrition and survival after the diagnosis of breast cancer: A review of the evidence. J Clin Oncol 20:3302-3316.
38. Serini S, Fasano E, Piccioni E, Cittadini AR, Calviello G. 2011. Dietary n-3 polyunsaturated fatty acids and the paradox of their health benefits and potential harmful effects. Chem Res Toxicol 24:2093-2105.
39. Smith-Warner SA, Spiegelman D, Ritz J, Albanes D, Beeson WL, Bernstein L, Berrino F, van den Brandt PA, Buring JE, Cho E, Colditz GA, Folsom AR, Freudenheim JL, Giovannucci E, Goldbohm RA, Graham S, Harnack L, Horn-Ross PL, Krogh V, Leitzmann MF, McCullough ML, Miller AB, Rodriguez C, Rohan TE, Schatzkin A, Shore R, Virtanen M, Willett WC, Wolk A, Zeleniuch-Jacquotte A, Zhang SM, Hunter DJ. 2006. Methods for pooling results of epidemiologic studies: The pooling project of prospective studies of diet and cancer. Am J Epidemiol 63:1053-1064.
40. Tan NS, Shaw NS, Vinckenbosch N, Liu P, Yasmin R, Desvergne B, Wahli W, Noy N. 2002. Selective cooperation between fatty acid binding proteins and peroxisome proliferator-activated receptors in regulating transcription. Mol Cell Biol 22:5114-5127.
41. Thiebaut AC, Chajes V, Gerber M, Boutron-Ruault MC, Joulin V, Lenoir G, Berrino F, Riboli E, Benichou J, Clavel-Chapelon F. 2009. Dietary intakes of omega-6 and omega-3 polyunsaturated fatty acids and the risk of breast cancer. Int J Cancer 124:924-931.
42. Waite KA, Eng C. 2002. Protean PTEN: Form and function. Am J Hum Genet 70:829-844.
43. Wei Y, Pattingre S, Sinha S, Bassik M, Levine B. 2008. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol Cell 30:678-688.
44. West NJ, Clark SK, Phillips RK, Hutchinson JM, Leicester RJ, Belluzzi A, Hull MA. 2010. Eicosapentaenoic acid reduces rectal polyp number and size in familial adenomatous polyposis. Gut 59:918-925.
45. Williams CM, Burdge G. 2006. Long-chain n-3 PUFA: Plant v. marine sources. Proc Nutr Soc 65:42-50.
46. Wolfrum C, Borrmann CM, Borchers T, Spener F. 2001. Fatty acids and hypolipidemic drugs regulate peroxisome proliferator-activated receptors alpha- and gamma-mediated gene expression via liver fatty acid binding protein: A signaling path to the nucleus. Proc Natl Acad Sci USA 98:2323-2328.
47. Wolk A, Larsson SC, Johansson JE, Ekman P. 2006. Long-term fatty fish consumption and renal cell carcinoma incidence in women. JAMA 296:1371-1376.
48. Yamamoto K, Ichijo H, Korsmeyer SJ. 1999. BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G2/M. Mol Cell Biol 19:8469-8478.
49. Yu L, McPhee CK, Zheng L, Mardones GA, Rong Y, Peng J, Mi N, Zhao Y, Liu Z, Wan F, Hailey DW, Oorschot V, Klumperman J, Baehrecke EH, Lenardo MJ. 2010. Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 465:942-946.