Dichloroacetate induces apoptosis of epithelial ovarian cancer cells through a mechanism involving modulation of oxidative stress

Reproductive Sciences

Volumn 18, Issue 12, 2011, Pages 1253-1261

  Saed, Ghassan M ^a   Fletcher, Nicole M ^a   Jiang, Zhong L ^a   Abu Soud, Husam M ^a   Diamond, Michael P ^a  

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

Author keywords

apoptosis; dichloroacetate; epithelial ovarian cancer; oxidative stress; real time RT PCR

Indexed keywords

CASPASE 3; DICHLOROACETIC ACID; DNA NUCLEOTIDYLEXOTRANSFERASE; EXTRACELLULAR SUPEROXIDE DISMUTASE; HYPOXIA INDUCIBLE FACTOR; MESSENGER RNA; MYELOPEROXIDASE; NITRIC OXIDE SYNTHASE;

AEROBIC METABOLISM; ANAEROBIC METABOLISM; APOPTOSIS; ARTICLE; CANCER CELL; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MODULATION; NICK END LABELING; OVARY CANCER; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN RNA BINDING; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; CASPASE 3; CELL LINE, TUMOR; DICHLOROACETATE; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; FEMALE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOPRECIPITATION; IN SITU NICK-END LABELING; NITRIC OXIDE SYNTHASE TYPE II; OVARIAN NEOPLASMS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PEROXIDASE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SUPEROXIDE DISMUTASE;

EID: 81555215094     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719111411731     Document Type: Article

References (56)

1. Barakat RR, Markman M, Randall M Principles and Practice of Gynecologic Oncology. 5 th ed. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2009. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins ; 2009 :
2. Flora SJ. Role of free radicals and antioxidants in health and disease. Cell Mol Biol (Noisy-le-grand). 2007 ; 53 (1). 1-2 (Pubitemid 46799686)
3. Wiseman H, Halliwell B. Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem J. 1996 ; 313 ((Pt 1)). 17-29 (Pubitemid 26013419)
4. Li H, Fan X, Houghton J. Tumor microenvironment: the role of the tumor stroma in cancer. J Cell Biochem. 2007 ; 101 (4). 805-815 (Pubitemid 47040863)
5. Saed GM, Ali-Fehmi R, Jiang ZL, et al. Myeloperoxidase serves as a redox switch that regulates apoptosis in epithelial ovarian cancer. Gynecol Oncol. 2010 ; 116 (2). 276-281
6. Motoo Y, Shimasaki T, Ishigaki Y, Nakajima H, Kawakami K, Minomoto T. Metabolic disorder, inflammation, and deregulated molecular pathways converging in pancreatic cancer development: implications for new therapeutic strategies. Cancers. 2011 ; 3 (1). 446-460
7. Ozben T. Oxidative stress and apoptosis: impact on cancer therapy. J Pharm Sci. 2007 ; 96 (9). 2181-2196 (Pubitemid 47477879)
8. Gibellini L, Pinti M, Nasi M, et al. Interfering with ROS metabolism in cancer cells: the potential role of quercetin. Cancers. 2010 ; (2). 1288-1311
9. Pelicano H, Carney D, Huang P. ROS stress in cancer cells and therapeutic implications. Drug Resist Updat. 2004 ; 7 (2). 97-110 (Pubitemid 38736063)
10. Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB. Oxidative stress, inflammation, and cancer: how are they linked?. Free Radic Biol Med. 2010 ; 49 (11). 1603-1616
11. Zelko IN, Mariani TJ, Folz RJ. Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Rad Biol Med. 2002 ; 33 (3). 337-349 (Pubitemid 34790245)
12. Michelakis ED, Webster L, Mackey Jr. Dichloroacetate (DCA) as a potential metabolic-targeting therapy for cancer. Br J Cancer. 2008 ; 99 (7). 989-994
13. Kroemer G, Pouyssegur J. Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell. 2008 ; 13 (6). 472-482 (Pubitemid 351766797)
14. Fang J, Seki T, Maeda H. Therapeutic strategies by modulating oxygen stress in cancer and inflammation. Adv Drug Deliv Rev. 2009 ; 61 (4). 290-302
15. Virgili F, Marino M. Regulation of cellular signals from nutritional molecules: a specific role for phytochemicals, beyond antioxidant activity. Free Radic Biol Med. 2008 ; 45 (9). 1205-1216
16. Surh YJ, Kundu JK, Na HK, Lee JS. Redox-sensitive transcription factors as prime targets for chemoprevention with anti-inflammatory and antioxidative phytochemicals. J Nutr. 2005 ; 135 ((12 suppl)). 2993S - 3001S (Pubitemid 43156578)
17. Kato M, Li J, Chuang JL, Chuang DT. Distinct structural mechanisms for inhibition of pyruvate dehydrogenase kinase isoforms by AZD7545, dichloroacetate, and radicicol. Structure. 2007 ; 15 (8). 992-1004 (Pubitemid 47212754)
18. Diamond MP, El-Hammady E, Wang R, Saed G. Regulation of matrix metalloproteinase-1 and tissue inhibitor of matrix metalloproteinase-1 by dichloroacetic acid in human fibroblasts from normal peritoneum and adhesions. Fertil Steril. 2004 ; 81 (1). 185-190 (Pubitemid 38058346)
19. Saed GM, Diamond MP. Modulation of the expression of tissue plasminogen activator and its inhibitor by hypoxia in human peritoneal and adhesion fibroblasts. Fertil Steril. 2003 ; 79 (1). 164-168 (Pubitemid 36071256)
20. Suh YA, Arnold RS, Lassegue B, et al. Cell transformation by the superoxide-generating oxidase Mox1. Nature. 1999 ; 401 (6748). 79-82
21. Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis?. Nat Rev Cancer. 2004 ; 4 (11). 891-899 (Pubitemid 39472955)
22. Geiszt M, Kopp JB, Varnai P, Leto TL. Identification of renox, an NAD(P)H oxidase in kidney. Proc Natl Acad Sci USA. 2000 ; 97 (14). 8010-8014 (Pubitemid 30460764)
23. Nemoto S, Takeda K, Yu ZX, Ferrans VJ, Finkel T. Role for mitochondrial oxidants as regulators of cellular metabolism. Mol Cell Biol. 2000 ; 20 (19). 7311-7318
24. Banerjee S, Randeva H, Chambers AE. Mouse models for preeclampsia: disruption of redox-regulated signaling. Reprod Biol Endocrinol. 2009 ; 4: 7
25. Tapia PC. Sublethal mitochondrial stress with an attendant stoichiometric augmentation of reactive oxygen species may precipitate many of the beneficial alterations in cellular physiology produced by caloric restriction, intermittent fasting, exercise and dietary phytonutrients: "Mitohormesis" for health and vitality. Med Hypotheses. 2006 ; 66 (4). 832-843 (Pubitemid 43181634)
26. Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nat Rev Cancer. 2011 ; 11 (2). 85-95
27. Kinnula VL, Crapo JD. Superoxide dismutases in malignant cells and human tumors. Free Radic Biol Med. 2004 ; 36 (6). 718-744 (Pubitemid 38264416)
28. Tandon V, Sharma S, Mahajan A, Bardi G. Oxidative stress: a novel strategy in cancer treatment. JK Sci. 2005 ; 7 (1). 56
29. Hileman EO, Liu J, Albitar M, Keating MJ, Huang P. Intrinsic oxidative stress in cancer cells: a biochemical basis for therapeutic selectivity. Cancer Chemother Pharmacol. 2004 ; 53 (3). 209-219 (Pubitemid 38293718)
30. Bhosle SM, Pandey BN, Huilgol NG, Mishra KP. Membrane oxidative damage and apoptosis in cervical carcinoma cells of patients after radiation therapy. Methods Cell Sci. 2002 ; 24 ((1-3)). 65-68 (Pubitemid 36826788)
31. Huang P, Feng L, Oldham EA, Keating MJ, Plunkett W. Superoxide dismutase as a target for the selective killing of cancer cells. Nature. 2000 ; 407 (6802). 390-395
32. Storz P. Reactive oxygen species in tumor progression. Front Biosci. 2005 ; 10: 1881-1896 (Pubitemid 40529044)
33. Fleischauer AT, Olson SH, Mignone L, Simonsen N, Caputo TA, Harlap S. Dietary antioxidants, supplements, and risk of epithelial ovarian cancer. Nutr Cancer. 2001 ; 40 (2). 92-98 (Pubitemid 34274913)
34. Schuurman AG, Goldbohm RA, Brants HA, van den Brandt PA. A prospective cohort study on intake of retinol, vitamins C and E, and carotenoids and prostate cancer risk (Netherlands). Cancer Causes Control. 2002 ; 13 (6). 573-582 (Pubitemid 34833109)
35. Moriya K, Nakagawa K, Santa T, et al. Oxidative stress in the absence of inflammation in a mouse model for hepatitis C virus-associated hepatocarcinogenesis. Cancer Res. 2001 ; 61 (11). 4365-4370 (Pubitemid 32685760)
36. Semenza GL, Roth PH, Fang HM, Wang GL. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem. 1994 ; 269 (38). 23757-23763 (Pubitemid 24293585)
37. Kim JW, Tchernyshyov I, Semenza GL, Dang CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 2006 ; 3 (3). 177-185
38. Stacpoole PW, Kerr DS, Barnes C, et al. Controlled clinical trial of dichloroacetate for treatment of congenital lactic acidosis in children. Pediatrics. 2006 ; 117 (5). 1519-1531 (Pubitemid 46071378)
39. Stacpoole PW, Gilbert LR, Neiberger RE, et al. Evaluation of long-term treatment of children with congenital lactic acidosis with dichloroacetate. Pediatrics. 2008 ; 121 (5). e1223 - e1228
40. Berendzen K, Theriaque DW, Shuster J, Stacpoole PW. Therapeutic potential of dichloroacetate for pyruvate dehydrogenase complex deficiency. Mitochondrion. 2006 ; 6 (3). 126-135 (Pubitemid 43872023)
41. Sun RC, Fadia M, Dahlstrom JE, Parish CR, Board PG, Blackburn AC. Reversal of the glycolytic phenotype by dichloroacetate inhibits metastatic breast cancer cell growth in vitro and in vivo. Breast Cancer Res Treat. 2010 ; 120 (1). 253-260
42. Bonnet S, Archer SL, Allalunis-Turner J, et al. A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell. 2007 ; 11 (1). 37-51 (Pubitemid 46054520)
43. Dhar S, Lippard SJ. Mitaplatin, a potent fusion of cisplatin and the orphan drug dichloroacetate. Proc Natl Acad Sci U S A. 2009 ; 106 (52). 22199-22204
44. Plas DR, Thompson CB. Cell metabolism in the regulation of programmed cell death. Trends Endocrinol Metab. 2002 ; 13 (2). 75-78
45. Kim JW, Dang CV. Multifaceted roles of glycolytic enzymes. Trends Biochem Sci. 2005 ; 30 (3). 142-150 (Pubitemid 40332530)
46. Kim JW, Dang CV. Cancer's molecular sweet tooth and the Warburg effect. Cancer Res. 2006 ; 66 (18). 8927-8930 (Pubitemid 44521105)
47. Xu RH, Pelicano H, Zhou Y, et al. Inhibition of glycolysis in cancer cells: a novel strategy to overcome drug resistance associated with mitochondrial respiratory defect and hypoxia. Cancer Res. 2005 ; 65 (2). 613-621
48. Stacpoole PW. The pharmacology of dichloroacetate. Metabolism. 1989 ; 38 (11). 1124-1144 (Pubitemid 19273807)
49. Sugden MC, Holness MJ. Recent advances in mechanisms regulating glucose oxidation at the level of the pyruvate dehydrogenase complex by PDKs. Am J Physiol Endocrinol Metab. 2003 ; 284 (5). E855 - E862
50. Howlett RA, Heigenhauser GJ, Hultman E, Hollidge-Horvat MG, Spriet LL. Effects of dichloroacetate infusion on human skeletal muscle metabolism at the onset of exercise. Am J Physiol. 1999 ; 277 ((1 Pt 1)). E18 - E25
51. Parolin ML, Spriet LL, Hultman E, et al. Effects of PDH activation by dichloroacetate in human skeletal muscle during exercise in hypoxia. Am J Physiol Endocrinol Metab. 2000 ; 279 (4). E752 - E761
52. Beckman KB, Ames BN. The free radical theory of aging matures. Physiol Rev. 1998 ; 78 (2). 547-581 (Pubitemid 28182903)
53. Choi JY, Neuhouser ML, Barnett MJ, et al. Iron intake, oxidative stress-related genes (MnSOD and MPO) and prostate cancer risk in CARET cohort. Carcinogenesis. 2008 ; 29 (5). 964-970 (Pubitemid 351982241)
54. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002 ; 420 (6917). 860-867 (Pubitemid 36019639)
55. Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature. 2000 ; 408 (6809). 239-247
56. Galijasevic S, Saed GM, Diamond MP, Abu-Soud HM. Myeloperoxidase up-regulates the catalytic activity of inducible nitric oxide synthase by preventing nitric oxide feedback inhibition. Proc Natl Acad Sci USA. 2003 ; 100 (25). 14766-14771 (Pubitemid 37517965)