Targeting metabolism with arsenic trioxide and dichloroacetate in breast cancer cells

Molecular Cancer

Volumn 10, Issue , 2011, Pages

  Sun, Ramon C ^a,b   Board, Philip G ^a   Blackburn, Anneke C ^a  

^a Biology and Environment   (Australia)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Arsenic trioxide; Breast cancer; Dichloroacetate; Electron transport chain; Mitochondria

Indexed keywords

ADENOSINE TRIPHOSPHATE; ARSENIC TRIOXIDE; CYTOCHROME C OXIDASE; DICHLOROACETIC ACID; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MYC PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; REACTIVE OXYGEN METABOLITE; ANTINEOPLASTIC AGENT; ORGANOARSENIC DERIVATIVE; OXIDE;

ARTICLE; BREAST CANCER; CANCER CELL; CELL METABOLISM; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; DRUG POTENTIATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; PROTEIN EXPRESSION; RESPIRATORY CHAIN; UPREGULATION; APOPTOSIS; BREAST TUMOR; FEMALE; METABOLISM; MITOCHONDRION; TUMOR CELL LINE;

ADENOSINE TRIPHOSPHATE; ANTINEOPLASTIC AGENTS; APOPTOSIS; ARSENICALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DICHLOROACETATE; FEMALE; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; OXIDES; REACTIVE OXYGEN SPECIES;

EID: 81255178599     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-10-142     Document Type: Article

References (55)

1. Antman KH. Introduction: the history of arsenic trioxide in cancer therapy. Oncologist 2001, 6(Suppl 2):1-2.
2. Emadi A, Gore SD. Arsenic trioxide - An old drug rediscovered. Blood Rev 2010, 24:191-199. 10.1016/j.blre.2010.04.001, 2918685, 20471733.
3. Powell BL, Moser B, Stock W, Gallagher RE, Willman CL, Stone RM, Rowe JM, Coutre S, Feusner JH, Gregory J, et al. Arsenic trioxide improves event-free and overall survival for adults with acute promyelocytic leukemia: North American Leukemia Intergroup Study C9710. Blood 2010, 116:3751-3757. 10.1182/blood-2010-02-269621, 2981533, 20705755.
4. Wang ZY, Chen Z. Acute promyelocytic leukemia: from highly fatal to highly curable. Blood 2008, 111:2505-2515. 10.1182/blood-2007-07-102798, 18299451.
5. Dilda PJ, Hogg PJ. Arsenical-based cancer drugs. Cancer Treat Rev 2007, 33:542-564. 10.1016/j.ctrv.2007.05.001, 17624680.
6. Chen GQ, Zhu J, Shi XG, Ni JH, Zhong HJ, Si GY, Jin XL, Tang W, Li XS, Xong SM, et al. In vitro studies on cellular and molecular mechanisms of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia: As2O3 induces NB4 cell apoptosis with downregulation of Bcl-2 expression and modulation of PML-RAR alpha/PML proteins. 1996, 88:1052-1061.
7. Kanzawa T, Kondo Y, Ito H, Kondo S, Germano I. Induction of autophagic cell death in malignant glioma cells by arsenic trioxide. Cancer Res 2003, 63:2103-2108.
8. Nakagawa Y, Akao Y, Morikawa H, Hirata I, Katsu K, Naoe T, Ohishi N, Yagi K. Arsenic trioxide-induced apoptosis through oxidative stress in cells of colon cancer cell lines. Life Sciences 2002, 70:2253-2269. 10.1016/S0024-3205(01)01545-4, 12005185.
9. Ralph SJ. Arsenic-based antineoplastic drugs and their mechanisms of action. Met Based Drugs 2008, 2008:260146. 2292810, 18431449.
10. Cai X, Shen YL, Zhu Q, Jia PM, Yu Y, Zhou L, Huang Y, Zhang JW, Xiong SM, Chen SJ, et al. Arsenic trioxide-induced apoptosis and differentiation are associated respectively with mitochondrial transmembrane potential collapse and retinoic acid signaling pathways in acute promyelocytic leukemia. Leukemia 2000, 14:262-270. 10.1038/sj.leu.2401650, 10673743.
11. Zheng Y, Shi Y, Tian C, Jiang C, Jin H, Chen J, Almasan A, Tang H, Chen Q. Essential role of the voltage-dependent anion channel (VDAC) in mitochondrial permeability transition pore opening and cytochrome c release induced by arsenic trioxide. Oncogene 2004, 23:1239-1247. 10.1038/sj.onc.1207205, 2913247, 14647451.
12. Tian X, Ma X, Qiao D, Ma A, Yan F, Huang X. mCICR is required for As2O3-induced permeability transition pore opening and cytochrome c release from mitochondria. Mol Cell Biochem 2005, 277:33-42. 10.1007/s11010-005-4818-x, 16132712.
13. Lu J, Chew EH, Holmgren A. Targeting thioredoxin reductase is a basis for cancer therapy by arsenic trioxide. Proc Natl Acad Sci USA 2007, 104:12288-12293. 10.1073/pnas.0701549104, 1940330, 17640917.
14. Kim JW, Dang CV. Cancer's molecular sweet tooth and the Warburg effect. Cancer Res 2006, 66:8927-8930. 10.1158/0008-5472.CAN-06-1501, 16982728.
15. Warburg O, Wind F, Negelein E. Ueber den Stoffwechsel von Tumoren im körper. Klinische Wochenschrift 1926, 5:829-832.
16. DeBerardinis RJ, Mancuso A, Daikhin E, Nissim I, Yudkoff M, Wehrli S, Thompson CB. Beyond aerobic glycolysis: Transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc Natl Acad Sci 2007, 104:19345-19350. 10.1073/pnas.0709747104, 2148292, 18032601.
17. Wong JY, Huggins GS, Debidda M, Munshi NC, De Vivo I. Dichloroacetate induces apoptosis in endometrial cancer cells. Gynecol Oncol 2008, 109:394-402. 10.1016/j.ygyno.2008.01.038, 2735772, 18423823.
18. Cao W, Yacoub S, Shiverick KT, Namiki K, Sakai Y, Porvasnik S, Urbanek C, Rosser CJ. Dichloroacetate (DCA) sensitizes both wild-type and over expressing Bcl-2 prostate cancer cells in vitro to radiation. Prostate 2008, 68:1223-1231. 10.1002/pros.20788, 18465755.
19. Papandreou I, Goliasova T, Denko NC. Anticancer drugs that target metabolism: Is dichloroacetate the new paradigm?. Int J Cancer 2011, 128:1001-1008. 10.1002/ijc.25728, 20957634.
20. Bonnet S, Archer SL, Allalunis-Turner J, Haromy A, Beaulieu C, Thompson R, Lee CT, Lopaschuk GD, Puttagunta L, Bonnet S, et al. A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell 2007, 11:37-51. 10.1016/j.ccr.2006.10.020, 17222789.
21. Chen Y, Cairns R, Papandreou I, Koong A, Denko NC. Oxygen consumption can regulate the growth of tumors, a new perspective on the Warburg effect. PLoS One 2009, 4:e7033. 10.1371/journal.pone.0007033, 2737639, 19753307.
22. 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, 120:253-260. 10.1007/s10549-009-0435-9, 19543830.
23. Michelakis ED, Sutendra G, Dromparis P, Webster L, Haromy A, Niven E, Maguire C, Gammer TL, Mackey JR, Fulton D, et al. Metabolic modulation of glioblastoma with dichloroacetate. Sci Transl Med 2010, 2:31ra34. 10.1126/scitranslmed.3000677, 20463368.
24. Chrzanowska-Lightowlers ZMA, Turnbull DM, Lightowlers RN. A microtiter plate assay for cytochrome c oxidase in permeabilized whole cells. Analytical Biochemistry 1993, 214:45-49. 10.1006/abio.1993.1454, 8250253.
25. Theodoratos A, Tu WJ, Cappello J, Blackburn AC, Matthaei K, Board PG. Phenylalanine-induced leucopenia in genetic and dichloroacetic acid generated deficiency of glutathione transferase Zeta. Biochem Pharmacol 2009, 77:1358-1363. 10.1016/j.bcp.2009.01.017, 19426674.
26. Shen ZX, Chen GQ, Ni JH, Li XS, Xiong SM, Qiu QY, Zhu J, Tang W, Sun GL, Yang KQ, et al. Use of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia (APL): II. Clinical efficacy and pharmacokinetics in relapsed patients. Blood 1997, 89:3354-3360.
27. Maeda H, Hori S, Nishitoh H, Ichijo H, Ogawa O, Kakehi Y, Kakizuka A. Tumor Growth Inhibition by Arsenic Trioxide (As2O3) in the Orthotopic Metastasis Model of Androgen-independent Prostate Cancer. Cancer Res 2001, (61):5432-5440.
28. Samikkannu T, Chen CH, Yih LH, Wang AS, Lin SY, Chen TC, Jan KY. Reactive oxygen species are involved in arsenic trioxide inhibition of pyruvate dehydrogenase activity. Chem Res Toxicol 2003, 16:409-414. 10.1021/tx025615j, 12641442.
29. Campbell MK, Farrell SO. Biochemistry 2003, Thomson learning, Inc., 4.
30. Liu Y, Fiskum G, Schubert D. Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem 2002, 80:780-787. 10.1046/j.0022-3042.2002.00744.x, 11948241.
31. Larochette N, Decaudin D, Jacotot E, Brenner C, Marzo I, Susin SA, Zamzami N, Xie Z, Reed J, Kroemer G. Arsenite induces apoptosis via a direct effect on the mitochondrial permeability transition pore. Exp Cell Res 1999, 249:413-421. 10.1006/excr.1999.4519, 10366441.
32. Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, Vieira HL, Prevost MC, Xie Z, Matsuyama S, Reed JC, Kroemer G. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 1998, 281:2027-2031.
33. Semenza GL. Regulation of cancer cell metabolism by hypoxia-inducible factor 1. Semin Cancer Biol 2009, 19:12-16. 10.1016/j.semcancer.2008.11.009, 19114105.
34. Dang CV, O'Donnell KA, Zeller KI, Nguyen T, Osthus RC, Li F. The c-Myc target gene network. Seminars in Cancer Biology 2006, 16:253-264. 10.1016/j.semcancer.2006.07.014, 16904903.
35. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP, Wang X. Prevention of apoptosis by Bcl-2: Release of cytochrome c from mitochondria blocked. Science 1997, 275:1129-1132. 10.1126/science.275.5303.1129, 9027314.
36. Carney DA. Arsenic trioxide mechanisms of action--looking beyond acute promyelocytic leukemia. Leuk Lymphoma 2008, 49:1846-1851. 10.1080/10428190802464745, 18949607.
37. Kito M, Matsumoto K, Wada N, Sera K, Futatsugawa S, Naoe T, Nozawa Y, Akao Y. Antitumor effect of arsenic trioxide in murine xenograft model. Cancer Sci 2003, 94:1010-1014. 10.1111/j.1349-7006.2003.tb01393.x, 14611680.
38. Xu HY, Yang YL, Liu SM, Bi L, Chen SX. Effect of arsenic trioxide on human hepatocarcinoma in nude mice. World J Gastroenterol 2004, 10:3677-3679.
39. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science 1996, 272:1136-1144. 10.1126/science.272.5265.1136, 8638158.
40. Pelicano H, Carney D, Huang P. ROS stress in cancer cells and therapeutic implications. Drug Resist Updat 2004, 7:97-110. 10.1016/j.drup.2004.01.004, 15158766.
41. Kamata H, Hirata H. Redox regulation of cellular signalling. Cellular Signalling 1999, 11:1-14. 10.1016/S0898-6568(98)00037-0, 10206339.
42. Hayes JD, McLellan LI. Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radic Res 1999, 31:273-300. 10.1080/10715769900300851, 10517533.
43. Nordberg J, Arner ESJ. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radical Biology and Medicine 2001, 31:1287-1312. 10.1016/S0891-5849(01)00724-9, 11728801.
44. Yao LL, Wang YG, Cai WJ, Yao T, Zhu YC. Survivin mediates the anti-apoptotic effect of δ-opioid receptor stimulation in cardiomyocytes. Journal of Cell Science 2007, 120:895-907. 10.1242/jcs.03393, 17298978.
45. Martindale JL, Holbrook NJ. Cellular response to oxidative stress: Signaling for suicide and survival. J Cell Physiol 2002, 192:1-15. 10.1002/jcp.10119, 12115731.
46. Perkins C, Kim CN, Fang G, Bhalla KN. Arsenic induces apoptosis of multidrug-resistant human myeloid leukemia cells that express Bcr-Abl or overexpress MDR, MRP, Bcl-2, or Bcl-x(L). Blood 2000, 95:1014-1022.
47. Ma XD, Qiao DF, Tian XM, Yan F, Ma AD. Mechanism of opening of mitochondrial permeability transition pore induced by arsenic trioxide. Ai Zheng 2006, 25:17-21.
48. Stockwin LH, Yu SX, Borgel S, Hancock C, Wolfe TL, Phillips LR, Hollingshead MG, Newton DL. Sodium Dichloroacetate (DCA) selectively targets cells with defects in the mitochondrial ETC. Int J Cancer 2010,
49. Sanchez-Arago M, Chamorro M, Cuezva JM. Selection of cancer cells with repressed mitochondria triggers colon cancer progression. Carcinogenesis 2010, 31:567-576. 10.1093/carcin/bgq012, 20080835.
50. Isidoro A, Martinez M, Fernandez PL, Ortega AD, Santamaria G, Chamorro M, Reed JC, Cuezva JM. Alteration of the bioenergetic phenotype of mitochondria is a hallmark of breast, gastric, lung and oesophageal cancer. Biochemical Journal 2004, 378:17-20. 10.1042/BJ20031541, 1223948, 14683524.
51. Susin SA, Zamzami N, Kroemer G. Mitochondria as regulators of apoptosis: Doubt no more. Biochimica et Biophysica Acta - Bioenergetics 1998, 1366:151-165.
52. Shim H, Dolde C, Lewis BC, Wu CS, Dang G, Jungmann RA, Dalla-Favera R, Dang CV. c-Myc transactivation of LDH-A: Implications for tumor metabolism and growth. Proc Natl Acad Sci USA 1997, 94:6658-6663. 10.1073/pnas.94.13.6658, 21214, 9192621.
53. Kim KB, Bedikian AY, Camacho LH, Papadopoulos NE, McCullough C. A phase II trial of arsenic trioxide in patients with metastatic melanoma. Cancer 2005, 104:1687-1692. 10.1002/cncr.21386, 16130126.
54. Subbarayan PR, Lima M, Ardalan B. Arsenic trioxide/ascorbic acid therapy in patients with refractory metastatic colorectal carcinoma: a clinical experience. Acta Oncol 2007, 46:557-561. 10.1080/02841860601042456, 17497326.
55. Ardalan B, Subbarayan PR, Ramos Y, Gonzalez M, Fernandez A, Mezentsev D, Reis I, Duncan R, Podolsky L, Lee K, et al. A phase I study of 5-fluorouracil/leucovorin and arsenic trioxide for patients with refractory/relapsed colorectal carcinoma. Clin Cancer Res 2010, 16:3019-3027. 10.1158/1078-0432.CCR-09-2590, 20501625.