Modulation of redox signaling promotes apoptosis in epithelial ovarian cancer cells

Gynecologic Oncology

Volumn 122, Issue 2, 2011, Pages 418-423

  Jiang, Zhongliang ^a   Fletcher, Nicole M ^a   Ali Fehmi, Rouba ^a   Diamond, Michael P ^a   Abu Soud, Husam M ^a   Munkarah, Adnan R ^b   Saed, Ghassan M ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HENRY FORD HEALTH SYSTEM   (United States)

Author keywords

Diphenyleneiodonium; Epithelial ovarian cancer; Hypoxia inducible factor 1 alpha; NADPH oxidase; Oxidative stress; Superoxide dismutase

Indexed keywords

CASPASE 3; DIPHENYLIODONIUM SALT; EXTRACELLULAR SUPEROXIDE DISMUTASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER TISSUE; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; NICK END LABELING; OVARY; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REDOX STRESS; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

APOPTOSIS; CASPASE 3; CELL LINE, TUMOR; FEMALE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; NADPH OXIDASE; NEOPLASMS, GLANDULAR AND EPITHELIAL; ONIUM COMPOUNDS; OVARIAN NEOPLASMS; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE;

EID: 79960446246     PISSN: 00908258     EISSN: 10956859     Source Type: Journal    
DOI: 10.1016/j.ygyno.2011.04.051     Document Type: Article

References (47)

1. A. Jemal, R. Siegel, E. Ward, T. Murray, J. Xu, and C. Smigal Cancer statistics, 2006 CA Cancer J Clin 56 2 2006 106 130
2. D. Trachootham, J. Alexandre, and P. Huang Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 8 7 2009 579 591
3. H. Pelicano, D. Carney, and P. Huang ROS stress in cancer cells and therapeutic implications Drug Resist Updat 7 2 2004 97 110 (Pubitemid 38736063)
4. A.A. Starkov, G. Fiskum, C. Chinopoulos, B.J. Lorenzo, S.E. Browne, and M.S. Patel Mitochondrial alpha-ketoglutarate dehydrogenase complex generates reactive oxygen species J Neurosci 24 36 2004 7779 7788 (Pubitemid 39215681)
5. E.O. Hileman, J. Liu, M. Albitar, M.J. Keating, and P. Huang Intrinsic oxidative stress in cancer cells: a biochemical basis for therapeutic selectivity Cancer Chemother Pharmacol 53 3 2004 209 219 (Pubitemid 38293718)
6. G. Cheng, Z. Cao, X. Xu, E.G. van Meir, and J.D. Lambeth Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5 Gene 269 1-2 2001 131 140 (Pubitemid 32488913)
7. M. Ushio-Fukai, and R.W. Alexander Reactive oxygen species as mediators of angiogenesis signaling: role of NAD(P)H oxidase Mol Cell Biochem 264 1-2 2004 85 97 (Pubitemid 39366107)
8. K. Bedard, and K.H. Krause The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology Physiol Rev 87 1 2007 245 313 (Pubitemid 46209993)
9. J. Dong, K.K. Sulik, and S.Y. Chen The role of NOX enzymes in ethanol-induced oxidative stress and apoptosis in mouse embryos Toxicol Lett 193 1 2010 94 100 (PMCID: 2822117)
10. B. Meier, A.R. Cross, J.T. Hancock, F.J. Kaup, and O.T. Jones Identification of a superoxide-generating NADPH oxidase system in human fibroblasts Biochem J 275 Pt 1 1991 241 245 (PMCID: 1150038)
11. T.P. Szatrowski, and C.F. Nathan Production of large amounts of hydrogen peroxide by human tumor cells Cancer Res 51 3 1991 794 798
12. K.K. Griendling, C.A. Minieri, J.D. Ollerenshaw, and R.W. Alexander Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells Circ Res 74 6 1994 1141 1148 (Pubitemid 24176909)
13. J.D. Lambeth NOX enzymes and the biology of reactive oxygen Nat Rev Immunol 4 3 2004 181 189 (Pubitemid 38339084)
14. N.M. Fletcher, Z.L. Jiang, M.P. Diamond, H.M. Abu-Soud, and G.M. Saed Hypoxia-generated superoxide induces the development of the adhesion phenotype Free Radic Biol Med 45 4 2008 530 536 (PMCID: 2574925)
15. I. Fridovich The biology of oxygen radicals Science 201 4359 1978 875 880
16. L.M. Carlsson, J. Jonsson, T. Edlund, and S.L. Marklund Mice lacking extracellular superoxide dismutase are more sensitive to hyperoxia Proc Natl Acad Sci U S A 92 14 1995 6264 6268
17. L. Chaiswing, W. Zhong, J.J. Cullen, L.W. Oberley, and T.D. Oberley Extracellular redox state regulates features associated with prostate cancer cell invasion Cancer Res 68 14 2008 5820 5826
18. G.L. Semenza Hypoxia-inducible factor 1: control of oxygen homeostasis in health and disease Pediatr Res 49 5 2001 614 617 (Pubitemid 32390848)
19. R. Takeya, and H. Sumimoto Molecular mechanism for activation of superoxide-producing NADPH oxidases Mol Cells 16 3 2003 271 277 (Pubitemid 41582851)
20. N.S. Chandel, E. Maltepe, E. Goldwasser, C.E. Mathieu, M.C. Simon, and P.T. Schumacker Mitochondrial reactive oxygen species trigger hypoxia-induced transcription Proc Natl Acad Sci U S A 95 20 1998 11715 11720 (Pubitemid 28460480)
21. H.B. Suliman, M. Ali, and C.A. Piantadosi Superoxide dismutase-3 promotes full expression of the EPO response to hypoxia Blood 104 1 2004 43 50 (Pubitemid 38879836)
22. A.R. Cross, and O.T. Jones The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils. Specific labelling of a component polypeptide of the oxidase Biochem J 237 1 1986 111 116 (Pubitemid 16063096)
23. G.M. Saed, M. Zhao, M.P. Diamond, and H.M. Abu-Soud Regulation of inducible nitric oxide synthase in post-operative adhesions Hum Reprod 21 6 2006 1605 1611 (Pubitemid 44445043)
24. A. Boveris, and B. Chance The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen Biochem J 134 3 1973 707 716
25. M. Volm, and R. Koomagi Hypoxia-inducible factor (HIF-1) and its relationship to apoptosis and proliferation in lung cancer Anticancer Res 20 3A 2000 1527 1533 (Pubitemid 30628160)
26. S. Brault, F. Gobeil Jr., A. Fortier, J.C. Honore, J.S. Joyal, and P.S. Sapieha Lysophosphatidic acid induces endothelial cell death by modulating the redox environment Am J Physiol Regul Integr Comp Physiol 292 3 2007 R1174 R1183
27. B.V. O'Donnell, D.G. Tew, O.T. Jones, and P.J. England Studies on the inhibitory mechanism of iodonium compounds with special reference to neutrophil NADPH oxidase Biochem J 290 Pt 1 1993 41 49 (PMCID: 1132380) (Pubitemid 23081198)
28. S.E. Park, J.D. Song, K.M. Kim, Y.M. Park, N.D. Kim, and Y.H. Yoo Diphenyleneiodonium induces ROS-independent p53 expression and apoptosis in human RPE cells FEBS Lett 581 2 2007 180 186 (Pubitemid 46096460)
29. Y.A. Suh, R.S. Arnold, B. Lassegue, J. Shi, X. Xu, and D. Sorescu Cell transformation by the superoxide-generating oxidase Mox1 Nature 401 6748 1999 79 82
30. J.L. Arbiser, J. Petros, R. Klafter, B. Govindajaran, E.R. McLaughlin, and L.F. Brown Reactive oxygen generated by Nox1 triggers the angiogenic switch Proc Natl Acad Sci U S A 99 2 2002 715 720 (Pubitemid 34106576)
31. M. Tanaka, K. Kogawa, K. Nakamura, Y. Nishihori, K. Kuribayashi, and S. Hagiwara Anti-metastatic gene therapy utilizing subcutaneous inoculation of EC-SOD gene transduced autologous fibroblast suppressed lung metastasis of Meth-A cells and 3LL cells in mice Gene Ther 8 2 2001 149 156 (Pubitemid 32162428)
32. M.D. Wheeler, O.M. Smutney, and R.J. Samulski Secretion of extracellular superoxide dismutase from muscle transduced with recombinant adenovirus inhibits the growth of B16 melanomas in mice Mol Cancer Res 1 12 2003 871 881 (Pubitemid 37288706)
33. M.M. Desouki, M. Kulawiec, S. Bansal, G.M. Das, and K.K. Singh Cross talk between mitochondria and superoxide generating NADPH oxidase in breast and ovarian tumors Cancer Biol Ther 4 12 2005 1367 1373 (Pubitemid 43131182)
34. T. Mochizuki, S. Furuta, J. Mitsushita, W.H. Shang, M. Ito, and Y. Yokoo Inhibition of NADPH oxidase 4 activates apoptosis via the AKT/apoptosis signal-regulating kinase 1 pathway in pancreatic cancer PANC-1 cells Oncogene 25 26 2006 3699 3707 (Pubitemid 43980491)
35. S. Mabuchi, M. Ohmichi, A. Kimura, Y. Nishio, E. Arimoto-Ishida, and N. Yada-Hashimoto Estrogen inhibits paclitaxel-induced apoptosis via the phosphorylation of apoptosis signal-regulating kinase 1 in human ovarian cancer cell lines Endocrinology 145 1 2004 49 58 (Pubitemid 38094500)
36. X. Wang, K.D. McCullough, T.F. Franke, and N.J. Holbrook Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival J Biol Chem 275 19 2000 14624 14631 (Pubitemid 30339753)
37. J.P. Piret, D. Mottet, M. Raes, and C. Michiels CoCl2, a chemical inducer of hypoxia-inducible factor-1, and hypoxia reduce apoptotic cell death in hepatoma cell line HepG2 Ann N Y Acad Sci 973 2002 443 447 (Pubitemid 36125050)
38. Y. Li, and M.A. Trush Diphenyleneiodonium, an NAD(P)H oxidase inhibitor, also potently inhibits mitochondrial reactive oxygen species production Biochem Biophys Res Commun 253 2 1998 295 299 (Pubitemid 29026697)
39. Y. Shi, A. Frankel, L.G. Radvanyi, L.Z. Penn, R.G. Miller, and G.B. Mills Rapamycin enhances apoptosis and increases sensitivity to cisplatin in vitro Cancer Res 55 9 1995 1982 1988
40. R.M. Scaife Selective and irreversible cell cycle inhibition by diphenyleneiodonium Mol Cancer Ther 4 6 2005 876 884 (Pubitemid 40909070)
41. A.P. Goud, P.T. Goud, M.P. Diamond, B. Gonik, and H.M. Abu-Soud Reactive oxygen species and oocyte aging: role of superoxide, hydrogen peroxide, and hypochlorous acid Free Radic Biol Med 44 7 2008 1295 1304
42. J.M. McCord, and I. Fridovich Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein) J Biol Chem 244 22 1969 6049 6055
43. K.U. Schallreuter, J. Moore, J.M. Wood, W.D. Beazley, D.C. Gaze, and D.J. Tobin In vivo and in vitro evidence for hydrogen peroxide (H2O2) accumulation in the epidermis of patients with vitiligo and its successful removal by a UVB-activated pseudocatalase J Investig Dermatol Symp Proc 4 1 1999 91 96 (Pubitemid 29491263)
44. Y. Hu, D.G. Rosen, Y. Zhou, L. Feng, G. Yang, and J. Liu Mitochondrial manganese-superoxide dismutase expression in ovarian cancer: role in cell proliferation and response to oxidative stress J Biol Chem 280 47 2005 39485 39492 (Pubitemid 41713906)
45. A. Calastretti, A. Bevilacqua, C. Ceriani, S. Vigano, P. Zancai, and S. Capaccioli Damaged microtubules can inactivate BCL-2 by means of the mTOR kinase Oncogene 20 43 2001 6172 6180 (Pubitemid 32964429)
46. H. Jiang, and Y. Feng Hypoxia-inducible factor 1alpha (HIF-1alpha) correlated with tumor growth and apoptosis in ovarian cancer Int J Gynecol Cancer 16 Suppl 1 2006 405 412
47. S. Kaewpila, S. Venkataraman, G.R. Buettner, and L.W. Oberley Manganese superoxide dismutase modulates hypoxia-inducible factor-1 alpha induction via superoxide Cancer Res 68 8 2008 2781 2788 (Pubitemid 351556276)