Sensitization of metformin-cytotoxicity by dichloroacetate via reprogramming glucose metabolism in cancer cells

Cancer Letters

Volumn 346, Issue 2, 2014, Pages 300-308

  Choi, Yong Won ^a   Lim, In Kyoung ^a  

^a Ajou University School of Medicine   (South Korea)

Author keywords

Dichloroacetate (DCA); Glucose deprivation; Glutathione contents; Metformin; Oxidative stress

Indexed keywords

DICHLOROACETIC ACID; GLUCOSE; GLUTATHIONE; LACTIC ACID; METFORMIN; PYRUVATE DEHYDROGENASE KINASE; ANTINEOPLASTIC AGENT; PYRUVATE DEHYDROGENASE COMPLEX;

ACIDIFICATION; ARTICLE; CANCER CELL; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG POTENTIATION; DRUG SENSITIVITY; GLUCOSE METABOLISM; GLYCOLYSIS; MITOCHONDRIAL RESPIRATION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL; BREAST NEOPLASMS; CELL RESPIRATION; DRUG EFFECTS; FEMALE; HELA CELL LINE; HUMAN; MCF 7 CELL LINE; METABOLISM; MITOCHONDRION;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BREAST NEOPLASMS; CELL RESPIRATION; DICHLOROACETIC ACID; DRUG SYNERGISM; FEMALE; GLUCOSE; HELA CELLS; HUMANS; MCF-7 CELLS; METFORMIN; MITOCHONDRIA; OXIDATIVE STRESS; PYRUVATE DEHYDROGENASE COMPLEX;

EID: 84896140171     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.01.015     Document Type: Article

References (36)

1. 2 mediate glucose deprivation-induced stress in human cancer cells. J. Biol. Chem. 2005, 280:4254-4263.
2. Ben Sahra I., Laurent K., Giuliano S., Larbret F., Ponzio G., Gounon P., Le Marchand-Brustel Y., Giorgetti-Peraldi S., Cormont M., Bertolotto C., Deckert M., Auberger P., Tanti J.F., Bost F. Targeting cancer cell metabolism: the combination of metformin and 2-deoxyglucose induces p53-dependent apoptosis in prostate cancer cells. Cancer Res. 2010, 70:2465-2475.
3. Ben Sahra I., Le Marchand-Brustel Y., Tanti J.F., Bost F. Metformin in cancer therapy: a new perspective for an old antidiabetic drug?. Mol. Cancer Ther. 2010, 9:1092-1099.
4. Bonnet S., Archer S.L., Allalunis-Turner J., Haromy A., Beaulieu C., Thompson R., Lee C.T., Lopaschuk G.D., Puttagunta L., Bonnet S., Harry G., Hashimoto K., Porter C.J., Andrade M.A., Thebaud B., Michelakis E.D. A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell 2007, 11:37-51.
5. Cantor J.R., Sabatini D.M. Cancer cell metabolism: one hallmark, many faces. Cancer Discov. 2012, 2:881-898.
6. Cheong J.H., Park E.S., Liang J., Dennison J.B., Tsavachidou D., Nguyen-Charles C., Wa Cheng K., Hall H., Zhang D., Lu Y., Ravoori M., Kundra V., Ajani J., Lee J.S., Ki Hong W., Mills G.B. Dual inhibition of tumor energy pathway by 2-deoxyglucose and metformin is effective against a broad spectrum of preclinical cancer models. Mol. Cancer Ther. 2011, 10:2350-2362.
7. Clark E.P., Epp E.R., Biaglow J.E., Morse-Gaudio M., Zachgo E. Glutathione depletion, radiosensitization, and misonidazole potentiation in hypoxic Chinese hamster ovary cells by buthionine sulfoximine. Radiat. Res. 1984, 98:370-380.
8. El-Mir M.Y., Nogueira V., Fontaine E., Averet N., Rigoulet M., Leverve X. Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I. J. Biol. Chem. 2000, 275:223-228.
9. Hamanaka R.B., Chandel N.S. Cell biology. Warburg effect and redox balance. Science 2011, 334:1219-1220.
10. Ishimoto T., Nagano O., Yae T., Tamada M., Motohara T., Oshima H., Oshima M., Ikeda T., Asaba R., Yagi H., Masuko T., Shimizu T., Ishikawa T., Kai K., Takahashi E., Imamura Y., Baba Y., Ohmura M., Suematsu M., Baba H., Saya H. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell 2011, 19:387-400.
11. Javeshghani S., Zakikhani M., Austin S., Bazile M., Blouin M.J., Topisirovic I., St-Pierre J., Pollak M.N. Carbon source and myc expression influence the antiproliferative actions of metformin. Cancer Res. 2012, 72:6257-6267.
12. Jeon S.M., Chandel N.S., Hay N. AMPK regulates NADPH homeostasis to promote tumour cell survival during energy stress. Nature 2012, 485:661-665.
13. Kroemer G., Pouyssegur J. Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell 2008, 13:472-482.
14. Lea M.A., Chacko J., Bolikal S., Hong J.Y., Chung R., Ortega A., Desbordes C. Addition of 2-deoxyglucose enhances growth inhibition but reverses acidification in colon cancer cells treated with phenformin. Anticancer Res. 2011, 31:421-426.
15. Lin X., Zhang F., Bradbury C.M., Kaushal A., Li L., Spitz D.R., Aft R.L., Gius D. 2-Deoxy-d-glucose-induced cytotoxicity and radiosensitization in tumor cells is mediated via disruptions in thiol metabolism. Cancer Res. 2003, 63:3413-3417.
16. Luo L., Huang W., Tao R., Hu N., Xiao Z.X., Luo Z. ATM and LKB1 dependent activation of AMPK sensitizes cancer cells to etoposide-induced apoptosis. Cancer Lett. 2013, 328:114-119.
17. Menendez J.A., Oliveras-Ferraros C., Cufi S., Corominas-Faja B., Joven J., Martin-Castillo B., Vazquez-Martin A. Metformin is synthetically lethal with glucose withdrawal in cancer cells. Cell Cycle 2012, 11:2782-2792.
18. Michelakis E.D., Sutendra G., Dromparis P., Webster L., Haromy A., Niven E., Maguire C., Gammer T.L., Mackey J.R., Fulton D., Abdulkarim B., McMurtry M.S., Petruk K.C. Metabolic modulation of glioblastoma with dichloroacetate. Sci. Translat. Med. 2010, 2:31ra34.
19. Mullen A.R., Wheaton W.W., Jin E.S., Chen P.H., Sullivan L.B., Cheng T., Yang Y., Linehan W.M., Chandel N.S., DeBerardinis R.J. Reductive carboxylation supports growth in tumour cells with defective mitochondria. Nature 2012, 481:385-388.
20. Niewisch M.R., Kuci Z., Wolburg H., Sautter M., Krampen L., Deubzer B., Handgretinger R., Bruchelt G. Influence of dichloroacetate (DCA) on lactate production and oxygen consumption in neuroblastoma cells: is DCA a suitable drug for neuroblastoma therapy?. Cell. Physiol. Biochem.: Int. J. Exp. Cell. Physiol., Biochem., Pharmacol. 2012, 29:373-380.
21. Owen M.R., Doran E., Halestrap A.P. Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochem. J. 2000, 348(Pt 3):607-614.
22. Riganti C., Gazzano E., Polimeni M., Aldieri E., Ghigo D. The pentose phosphate pathway: an antioxidant defense and a crossroad in tumor cell fate. Free Radical Biol. Med. 2012, 53:421-436.
23. Rocha G.Z., Dias M.M., Ropelle E.R., Osorio-Costa F., Rossato F.A., Vercesi A.E., Saad M.J., Carvalheira J.B. Metformin amplifies chemotherapy-induced AMPK activation and antitumoral growth. Clin. Cancer Res.: Official J. Am. Assoc. Cancer Res. 2011, 17:3993-4005.
24. Shackelford D.B., Abt E., Gerken L., Vasquez D.S., Seki A., Leblanc M., Wei L., Fishbein M.C., Czernin J., Mischel P.S., Shaw R.J. LKB1 inactivation dictates therapeutic response of non-small cell lung cancer to the metabolism drug phenformin. Cancer Cell 2013, 23:143-158.
25. Sinnett-Smith J., Kisfalvi K., Kui R., Rozengurt E. Metformin inhibition of mTORC1 activation, DNA synthesis and proliferation in pancreatic cancer cells: dependence on glucose concentration and role of AMPK. Biochem. Biophys. Res. Commun. 2013, 430:352-357.
26. Stockwin L.H., Yu S.X., Borgel S., Hancock C., Wolfe T.L., Phillips L.R., Hollingshead M.G., Newton D.L. Sodium dichloroacetate selectively targets cells with defects in the mitochondrial ETC. Int. J. Cancer J. Int. Cancer 2010, 127:2510-2519.
27. Sun R.C., Fadia M., Dahlstrom J.E., Parish C.R., Board P.G., Blackburn A.C. 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.
28. Sutendra G., Dromparis P., Kinnaird A., Stenson T.H., Haromy A., Parker J.M., McMurtry M.S., Michelakis E.D. Mitochondrial activation by inhibition of PDKII suppresses HIF1a signaling and angiogenesis in cancer. Oncogene 2013, 32:1638-1650.
29. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 1969, 27:502-522.
30. Vander Heiden M.G. Targeting cancer metabolism: a therapeutic window opens. Nat. Rev. Drug Discovery 2011, 10:671-684.
31. Ward P.S., Thompson C.B. Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell 2012, 21:297-308.
32. Whitehouse S., Cooper R.H., Randle P.J. Mechanism of activation of pyruvate dehydrogenase by dichloroacetate and other halogenated carboxylic acids. Biochem. J. 1974, 141:761-774.
33. Wu M., Neilson A., Swift A.L., Moran R., Tamagnine J., Parslow D., Armistead S., Lemire K., Orrell J., Teich J., Chomicz S., Ferrick D.A. Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol. 2007, 292:C125-136.
34. Xiao X., He Q., Lu C., Werle K.D., Zhao R.X., Chen J., Davis B.C., Cui R., Liang J., Xu Z.X. Metformin impairs the growth of liver kinase B1-intact cervical cancer cells. Gynecol. Oncol. 2012, 127:249-255.
35. Zhuang Y., Miskimins W.K. Metformin induces both caspase-dependent and poly(ADP-ribose) polymerase-dependent cell death in breast cancer cells. Mol. Cancer Res.: MCR 2011, 9:603-615.
36. Zmijewski J.W., Lorne E., Zhao X., Tsuruta Y., Sha Y., Liu G., Siegal G.P., Abraham E. Mitochondrial respiratory complex I regulates neutrophil activation and severity of lung injury. Am. J. Respir. Crit. Care Med. 2008, 178:168-179.