Involvement of hydroperoxide in mitochondria in the induction of apoptosis by the eicosapentaenoic acid

Free Radical Research

Volumn 39, Issue 3, 2005, Pages 225-235

  Koumura, Tomoko ^a   Nakamura, Chika ^a   Nakagawa, Yasuhito ^a  

^a KITASATO UNIVERSITY   (Japan)

Author keywords

Apoptosis; Apoptosis inducing factor; Eicosapentaenoic acid; Hydroperoxide; Mitochondria; Phospholipid hydroperoxide glutathione peroxidase

Indexed keywords

APOPTOSIS INDUCING FACTOR; CASPASE 3; CASPASE INHIBITOR; CYTOCHROME C; DOCOSAHEXAENOIC ACID; HYDROPEROXIDE; ICOSAPENTAENOIC ACID; LINOLEIC ACID; MITOCHONDRIAL PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL NUCLEUS; CELL STRAIN L 929; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME MECHANISM; ENZYME RELEASE; ENZYME REPRESSION; ENZYME SYNTHESIS; HELA CELL; HUMAN; HUMAN CELL; LEUKEMIA CELL; MAST CELL LEUKEMIA; MITOCHONDRION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TRANSPORT; RAT; SENSITIVITY ANALYSIS;

ANIMALS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; CASPASE 3; CASPASES; CELL NUCLEUS; CYTOCHROMES C; EICOSAPENTAENOIC ACID; ENZYME ACTIVATION; FLAVOPROTEINS; GLUTATHIONE PEROXIDASE; HELA CELLS; HUMANS; HYDROGEN PEROXIDE; MEMBRANE PROTEINS; MICE; MITOCHONDRIA; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN TRANSPORT; RATS;

EID: 15944428554     PISSN: 10715762     EISSN: None     Source Type: Journal    
DOI: 10.1080/10715760500043587     Document Type: Article

References (56)

1. Burns CP, Spector AA. Effects of lipids on cancer therapy. Nutr Rev 1990;48:233-239.
2. Reddy BS. Dietary fat and colon cancer. Lipids 1992;27:807-813.
3. Blot WJ, Lanier A, Fraumeni JF, Bender TR. Cancer mortality among Alaska natives. J Natl Cancer Inst 1975;55:547-554.
4. Bang HO, Dyerberg J, Hjiorne N. The composition of food consumed by Greenland Eskimos. Acta Med Scand 1976;200:69-73.
5. Nielsen NH, Hansen JP. Breast cancer in Greenland. J Cancer Res Clin Oncol 1980;98:287-299.
6. Minoura T, Takata T, Sakaguchi M, Takada H, Yamamura M, Hioki K, Yamamoto M. Effect of dietary eicosapentaenoic acid on Azoxymethane-induced colon carcinogenesis. Cancer Res 1988;48:4790-4794.
7. Deschner EE, Lytle JS, Wong G, Ruperto JF, Newmark HL. The effect of dietary omega-3 fatty acids and colon tumor incidence. Cancer 1990;66:2350-2356.
8. Latham P, Lund EK, Johnson IT. Dietary n-3 PUFA increases the apoptotic response to 1,2-dimethylhydrazine, reduces mitosis and suppresses the induction of carcinogenesis in the rat colon. Carcinogenesis 1999;20:645-650.
9. Sagar PS, Das UN. Cytotoxic action of cis-unsaturated fatty acids on human cervical carnoma (HeLa) cells in vitro. Prostaglandins Leukot Essent Fatty Acids 1995;53:287-299.
10. Grammatikos SI, Subbaiah PV, Victor TA, Miller WM. n-3 and n-6 fatty acid processing and growth effects in neoplastic and non-cancerous human epithelial cell lines. Br J Cancer 1994;70:219-227.
11. Falconer JS, Ross JA, Fearon KCH, Hawkins RA, O'Riordain MG, Carter DC. Effect of eicosapentaenoic acid and other fatty acid on the growth in vitro of human pancreatic cancer cell lines. Br J Cancer 1994;69:826-832.
12. Hawkins RA, Sangster K, Arends MJ. Apoptotic death of pancreatic cancer cella induced by polyunsaturated fatty acids varies with double bond number and involves an oxidative mechanism. J Pathol 1998;185:61-70.
13. Sessler AM, Ntambi JM. Polyunsaturated fatty acid regulation of gene expression. J Nutr 1998;128:923-926.
14. Calviello G, Palozza P, Maggiano N, Piccioni E, Franceschelli P, Frattucci A, Di Nicuolo F, Bartoli GM. Cell proliferation, differentiation and apoptosis are modified by n-3 polyunsaturated fatty acids in normal colonic mucosa. Lipids 1999;34:599-604.
15. Finstad HS, Kolset SO, Holme JA, Wiger R, Farrants AK, Blomhoff R, Drevon CA. Effect of n-3 and n-6 fatty acids on proliferation and differentiation of promyelocytic leukemic HL-60 cells. Bood 1994;84:3799-3809.
16. Vento R, D'Alessandro N, Giuliano M, Lauricella M, Carabillo M, Tesoriere G. Induction of apoptosis by arachidonic acid in human retinoblastoma Y79 cells: involvement of oxidative stress. Exp Eye Res 2000;70:503-517.
17. Lowe SW, Lin AW. Apoptosis in cancer. Carcinogenesis 2000;21:485-495.
18. Arita K, Kobuchi H, Utsumi T, Takehara Y, Akiyama J, Horton AA, Ustumi K. Mechanism of apoptosis in HL-60 cells induced by n-3 and n-6 polyunsaturated fatty acids. Biochem Pharm. 2001;62:821-828.
19. Chiu LCM, Wan JMF. Induction of apoptosis in HL-60 cells by eicosapentaenoic acid (EPA) is associated with downregulation of bcl-2 expression. Cancer Lett 1999;145:17-27.
20. Colquhoun A, Schumacher RI. γ-Linolenic acid and eicosapentaenoic acid induce modifications in mitochondrial metabolism, reactive oxygen species generation, lipid peroxidation and apoptosis in Walker 256 rat carcinosarcoma cells. Biochim Biophys Acta 2001;1533:207-219.
21. Heimli H, Giske C, Naderi S, Drevon CA, Hollung K. Eicosapentaenoic acid promotes apoptosis in Ramos cells via activation of caspase-3 and -9. Lipids 37:797-802.
22. Clarke RG, Lund EK, Latham P, Pinder AC, Johnson I. Effect of eicoapentaenoic acid on the proliferation and incidence of apoptosis in colorectal cell line HT29. Lipids 1999;34:1287-1295.
23. Kroemer G, Dallaporta B, Resche-Rigon M. The mitochondrial death/life regulation in apoptosis and necrosis. Annu Rev Physiol 1998;60:619-642.
24. Jabs T. Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem Pharmacol 1999;57:231-245.
25. Skukachev VP. Cytochrome c in the apoptotic and antioxidant cascade. FEBS Lett 1998;423:275-280.
26. Arita K, Yamamoto Y, Takehara Y, Utsumi T, Kanno T, Miyaguchi C, Akiyama J, Yoshioka T, Utsumi K. Mechanism of enhanced apoptosis in HL-60 cells by UV-irradiated N-3 and N-6 polyunsaturated fatty acids. Free Radic Biol Med 2003;35:189-199.
27. Igarashi M, Miyazawa. T. Do conjugated eicosapentaenoic acid and conjugated docosahexacnoic acid induce apoptosis via lipid peroxidation in culture human tumor cell? Biochem Biophys Res Commun 2000;270:649-656.
28. Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Hirsch T, Susin SA, Petit PX, Mignotte B, Kroemer G. Sequential reduction of mitochondrial transmenbrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 1995;182:367-377.
29. Arai M, Imai H, Koumura T, Yoshida M, Emoto K, Umeda M, Chiba N, Nakagawa Y. Mitochondrial phospholipid hydroperoxide glutathione peroxidase plays a major role in preventing oxidative injury to cells. J Biol Chem 1999;274:4924-4933.
30. Yu S-W, Wang H, Poitras MF, Coombs C, Bowers W, Federoff HJ, Poirier GC, Dawson TM, Dawson VL. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 2002;297:259-263.
31. Maziere C, Dantin F, Conte MA, Degonville J, Ali D, Dubois F, Maziere JC. Polyunsaturated fatty acid enrichment enhances endothelial cell-induced low density lipoprotein peroxidation. Biochem J 1998;336:57-62.
32. Robinson BS, Hii CST, Ferrante A. Activation of phospholipase A2 in human neutrophils by polyunsaturated fatty acid and its role in the stimulation of superoxide production. Biochem J 1998;336:611-617.
33. Maziere C, Conte MA, Degonville J, Ali D, Dubois F, Maziere JC. Cellular enrichment with polyunsaturated fatty acids induces an oxidative stress and activates the transcription. Bichem Biophys Res Commun 1999;265:116-122.
34. Buttke TM, Sandstrom PA. Oxidative stress as a mediator of apoptosis. Immunol Today 1994;15:7-10.
35. Polyak K, Xia Y, Zweier JL, Kinzler KW, Vogelstein B. A model for p53-induced apoptosis. Nature 1997;389:300-305.
36. Kane DJ, Sarafian TA, Anton R, Hahn H, Gralla EB, Valentine JS, Ord T, Bredesen DE. Bcl-2 inhibitor of neural death: Decreased generation of reactive oxygen species. Science 1993;262:1274-1277.
37. Albina JE, Cui S, Mateo RB, Reichner JS. Nitric oxide-mediated apoptosis in murine peritoneal macrophages. J Immunol 1993;150:5080-5085.
38. Fang W, Rivard JJ, Ganser JA, LeBien TW, Nath KA, Mueller DL, Behrens TW. Bcl-xL rescues WEHI 231 B lymphocytes from oxidant-mediated death following diverse apoptotic stimuli. J Immunol 1995;155:66-75.
39. Mignotte B, Vayssiere JL. Mitochondria and apoptosis. Eur J Biochem 1998;252:1-15.
40. Quillet-Mary A, Jaffrezou JP, Mansat V, Bordier C, Naval J, Laurent G. Implication of mitochondrial hydrogen peroxide generation in ceramide-induced apoptosis. J Biol Chem 1997;272:21388-21395.
41. Keller JN, Kindy MS, Holtsberg FW, St Clair DK, Yen HC, Germeyer A, Steiner SM, Bruce-Kekker AJ, Hutchin JB, Mattson MP. Mitochondrial manganese superoxide dismutase prevent neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation, and mitochondrial dysfunction. J Neurosci 1998;18:687-697.
42. Majima HJ, Oberley TD, Furukawa K, Mattson MP, Yen HC, Szweda LI, Clair DK. Prevention of mitochondrial injury by manganese superoxide dismutase reveals a primary mechanism for alkaline-induced cell death. J Biol Chem 1998;273:8217-8224.
43. Nomura K, Imai H, Koumura T, Arai M, Nakagawa Y Mitochondrial phospholipid hydroperoxide glutathione peroxidase suppresses apoptosis mediated by a mitochondrial death pathway. J Biol Chem 1999;274:29294-29302.
44. Colquhoum A, Schumacher RI. γ-Linoenic acid an eicosapentaenoic acid induce modification in mitochondrial metabolism, reactive oxygen species generation, lipid peroxidation and apoptosis in Walker 256 rat carcinosarcoma cells. Biochim Biophys Acta 2001;1533:207-219.
45. Wang X. The expanding role of mitochondria in apoptosis. Genes Dev 2001;15:2922-2933.
46. Vielia HL, Haouzi D, EI Hamel C, Jacotot E, Belzacq AS, Brenner C, Kroemer G. Permeabilization of the mitochondrial inner membrane during apoptosis: impact of adenine nucleotide translocator. Cell Death Differ 2000;7:1146-1154.
47. Imai H, Koumura T, Najima R, Nomura K, Nakagawa Y. Protection from inactivation of adenine nucleotide translocator during hypoglycemia-induced apoptosis by mitochondrial phospholipid hydroperoxide glutathione peroxidase. Biochem J 2003;371:799-809.
48. Schonfeld P, Bohnensack R. Fatty acid-promoted mitochondrial permeability transition by membrane depolarization and binding to the ADP/ATP carrier. FEBS Lett 1997; 420:167-170.
49. Laurier D, Lagueux J, Thibodeau J, Menard G, Poirier G. Molecular and biochemical features of poly (ADP-ribose) metabolism. Mol Cell Biochem 1993;122:171-193.
50. Eliasson MJ, Sampel K, Mandir AS, Hum PD, Traystman RJ, Bao J, Pieper A, Wang ZQ, Dawson TM, Snyder SH, Dawson VL. Poly (ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nature Med 1997;3:1089-1095.
51. Pieper AA, Walles T, Wei G, Clements EE, Verma A, Snyder SH, Zweier JL. Myocardial postischemic injury is reduced by polyADPribose polymerase-1 gene disruption. Mol Med 2000;6:271-282.
52. Mandir AS, Poitras MF, Berliner AR, Herring WJ, Guastella DB, Feldman A, Poirier GG, Wang ZQ, Dawson TM, Dawson VL. NMDA but not non-NMDA excitotoxicity is mediated by poly (ADP-ribose) polymerase. J Neurosci 2000;20:8005-8011.
53. Szabo C, Dawson VL. Role of poly (ADP-ribose) synthetase in inflammation and ischemia-reperfusion. Trends Pharmacol Sci 1998;19:287-298.
54. Cande C, Cohen I, Daugas E, Ravagnan L, Larochette N, Zamzami N, Kroemer G. Apotosis-inducing factor (AIF): A novel caspase-independent death effector released from mitochondria. Biochimie 2002;84:215-222.
55. Rippo MR, Malisan F, Ravagnan L, Tomassini B, Condo I, Costantini P, Susin SA, Rufini A, Todaro M, Kroemer G. GD3 ganglioside directly targets mitochondria in a bcl-2-controlled fashion. FASEB J 2000;14:2047-2054.
56. Bidere N, Lorenzo HK, Carmona S, Laforge M, Harper F, Dumont C, Senik A. Cathepsin D triggers Bax activation, resulting in selective apoptosis-inducing factor (AIF) relocation in T lymphocytes entering the early commitment phase to apoptosis. J Biol Chem 2003;278:31401-31411.