Synergistic anti-cancer effect of phenformin and oxamate

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Miskimins, W Keith ^a,b   Ahn, Hyun Joo ^c   Kim, Ji Yeon ^c   Ryu, Sun ^c   Jung, Yuh Seog ^d   Choi, Joon Young ^c  

^a SANFORD RESEARCH   (United States)

^b UNIVERSITY OF SOUTH DAKOTA   (United States)

^c Sungkyunkwan University School of Medicine   (South Korea)

^d National Cancer Center   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; FLUORODEOXYGLUCOSE F 18; LACTATE DEHYDROGENASE; LACTIC ACID; METFORMIN; OXAMIC ACID; PHENFORMIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CELL DEATH; COMPUTER ASSISTED EMISSION TOMOGRAPHY; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENCY; DRUG POTENTIATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE SILENCING; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; TUMOR CELL LINE; TUMOR VOLUME;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; COLONIC NEOPLASMS; DRUG COMBINATIONS; DRUG SYNERGISM; ELECTRON TRANSPORT COMPLEX I; FLUORODEOXYGLUCOSE F18; GLYCOLYSIS; L-LACTATE DEHYDROGENASE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; NEOPLASM TRANSPLANTATION; OXAMIC ACID; PHENFORMIN; REACTIVE OXYGEN SPECIES; TUMOR BURDEN;

EID: 84899851570     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085576     Document Type: Article

References (54)

1. Landman GW, Kleefstra N, van Hateren KJ, Groenier KH, Gans RO, et al. (2010) Metformin associated with lower cancer mortality in type 2 diabetes: ZODIAC-16. Diabetes Care 33: 322-326.
2. Libby G, Donnelly LA, Donnan PT, Alessi DR, Morris AD, et al. (2009) New users of metformin are at low risk of incident cancer: a cohort study among people with type 2 diabetes. Diabetes Care 32: 1620-1625.
3. Hadad S, Iwamoto T, Jordan L, Purdie C, Bray S, et al. (2011) Evidence for biological effects of metformin in operable breast cancer: a pre-operative, window-of-opportunity, randomized trial. Breast Cancer Res Treat 128: 783-794.
4. Goodwin PJ, Ligibel JA, Stambolic V (2009) Metformin in breast cancer: time for action. J Clin Oncol 27: 3271-3273.
5. Rosand J, Friedberg JW, Yang JM (1997) Fatal phenformin-associated lactic acidosis. Ann Intern Med 127: 170.
6. Appleyard MVC, Murray KE, Coates PJ, Wullschleger S, Bray SE, et al. (2012) Phenformin as prophylaxis and therapy in breast cancer xenografts. Br J Cancer 106: 1117-1122.
7. Kisfalvi K, Eibl G, Sinnett-Smith J, Rozengurt E (2009) Metformin disrupts crosstalk between G protein-coupled receptor and insulin receptor signaling systems and inhibits pancreatic cancer growth. Cancer Res 69: 6539-6545.
8. Dowling RJ, Zakikhani M, Fantus IG, Pollak M, Sonenberg N (2007) Metformin inhibits mammalian target of rapamycin-dependent translation initiation in breast cancer cells. Cancer Res 67: 10804-10812. (Pubitemid 350145909)
9. King TD, Song L, Jope RS (2006) AMP-activated protein kinase (AMPK) activating agents cause dephosphorylation of Akt and glycogen synthase kinase-3. Biochem Pharmacol 71: 1637-1647.
10. Saito S, Furuno A, Sakurai J, Sakamoto A, Park HR, et al. (2009) Chemical genomics identifies the unfolded protein response as a target for selective cancer cell killing during glucose deprivation. Cancer Res 69: 4225-4234.
11. Alimova IN, Liu B, Fan Z, Edgerton SM, Dillon T, et al. (2009) Metformin inhibits breast cancer cell growth, colony formation and induces cell cycle arrest in vitro. Cell Cycle 8: 909-915.
12. Owen MR, Doran E, Halestrap AP (2000) Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochem J 348: 607-614. (Pubitemid 30410251)
13. Ota S, Horigome K, Ishii T, Nakai M, Hayashi K, et al. (2009) Metformin suppresses glucose-6-phosphatase expression by a complex I inhibition and AMPK activation-independent mechanism. Biochem Biophys Res Commun 388: 311-316.
14. Walenta S, Mueller-Klieser WF (2004) Lactate: mirror and motor of tumor malignancy. Semin Radiat Oncol 14: 267-274. (Pubitemid 38903231)
15. Quennet V, Yaromina A, Zips D, Rosner A, Walenta S, et al. (2006) Tumor lactate content predicts for response to fractionated irradiation of human squamous cell carcinomas in nude mice. Radiother Oncol 81: 130-135. (Pubitemid 44780779)
16. Fantin VR, St-Pierre J, Leder P (2006) Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell 9: 425-434. (Pubitemid 43832190)
17. Xie H, Valera VA, Merino MJ, Amato AM, Signoretti S, et al. (2009) LDH-A inhibition, a therapeutic strategy for treatment of hereditary leiomyomatosis and renal cell cancer. Mol Cancer Ther 8: 626-635.
18. Wieking BG, Vermeer DW, Spanos WC, Lee KM, Vermeer P, et al. (2012) Non-oncogenic HPV 16 E6/E7 vaccine enhances treatment of HPV expressing tumors. Cancer Gene Ther 19: 667-674.
19. Spanos WC, Nowicki P, Lee DW, Hoover A, Hostager B, et al. (2009) Immune response during therapy with cisplatin or radiation for human papillomavirus-related head and neck cancer. Arch Otolaryngol Head Neck Surg 135: 1137-1146.
20. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG (2010) Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
21. Zhuang Y, Miskimins WK (2008) Cell cycle arrest in Metformin treated breast cancer cells involves activation of AMPK, downregulation of cyclin D1, and requires p27Kip1 or p21Cip1. J Mol Signal 3: 18.
22. Zhuang Y, Miskimins WK (2011) Metformin induces both caspase-dependent and poly(ADP-ribose) polymerase-dependent cell death in breast cancer cells. Mol Cancer Res 9: 603-15.
23. Chan DK, Miskimins WK (2012) Metformin and phenethyl isothiocyanate combined treatment in vitro is cytotoxic to ovarian cancer cultures. J Ovarian Res 5: 19.
24. Dykens JA, Jamieson J, Marroquin L, Nadanaciva S, Billis PA, et al. (2008) Biguanide-induced mitochondrial dysfunction yields increased lactate production and cytotoxicity of aerobically-poised HepG2 cells and human hepatocytes in vitro. Toxicol Appl Pharmacol 233: 203-210. (Pubitemid 50293339)
25. Papaconstantinou J, Colowick SP (1961) The role of glycolysis in the growth of tumor cells. II. The effect of oxamic acid on the growth of HeLa cells in tissue culture. J Biol Chem 236: 285-8.
26. Chou TC (2006) Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 58: 621-81.
27. Wang Y, Dawson VL, Dawson TM (2009) Poly(ADP-ribose) signals to mitochondrial AIF: a key event in parthanatos. Exp Neurol 218: 193-202.
28. Schafer G (1983) Biguanides. A review of history, pharmacodynamics and therapy. Diabete Metab 9: 148-163.
29. Soini Y, Vakkala M, Kahlos K, Paakko P, Kinnula V (2001) MnSOD expression is less frequent in tumour cells of invasive breast carcinomas than in in situ carcinomas or non-neoplastic breast epithelial cells. J Pathol 195: 156-162. (Pubitemid 32899023)
30. Hitchler MJ, Oberley LW, Domann FE (2008) Epigenetic silencing of SOD2 by histone modifications in human breast cancer cells. Free Radic Biol Med 45: 1573-1580.
31. Reynolds VH, Fleming JH, Jr., Richie RE, Foster JH, Colowick SP (1963) Inhibition of Lactic Dehydrogenase: A New Approach to Cancer Chemotherapy. Surg Forum 14: 128-130.
32. Koukourakis MI, Giatromanolaki A, Sivridis E, Bougioukas G, Didilis V, et al. (2003) Lactate dehydrogenase-5 (LDH-5) overexpression in non-small-cell lung cancer tissues is linked to tumour hypoxia, angiogenic factor production and poor prognosis. Br J Cancer 89: 877-885. (Pubitemid 37175811)
33. Greiner EF, Guppy M, Brand K (1994) Glucose is essential for proliferation and the glycolytic enzyme induction that provokes a transition to glycolytic energy production. J Biol Chem 269: 31484-90. (Pubitemid 24379505)
34. Jin S, DiPaola RS, Mathew R, White E (2007) Metabolic catastrophe as a means to cancer cell death. J Cell Sci 120: 379-383. (Pubitemid 46332501)
35. Cheong JH, Park ES, Liang J, Dennison JB, Tsavachidou D, et al. (2011) Dual inhibition of tumor energy pathway by 2-deoxyglucose and metformin is effective against a broad spectrum of preclinical cancer models. Mol Cancer Ther 10: 2350-2362.
36. Lea MA, Chacko J, Bolikal S, Hong JY, Chung R, et al. (2011) Addition of 2-deoxyglucose enhances growth inhibition but reverses acidification in colon cancer cells treated with phenformin. Anticancer Res 31: 421-426.
37. Koukourakis MI, Giatromanolaki A, Sivridis E, Gatter KC, Trarbach T, et al. (2011) Prognostic and predictive role of lactate dehydrogenase 5 (LDH5) expression in colorectal cancer patients treated with PTK787/ZK 222584 (Vatalanib) anti-angiogenic therapy. Clin Cancer Res 17: 4892-4900.
38. Thornburg JM, Nelson KK, Clem BF, Lane AN, Arumugam S, et al. (2008) Targeting aspartate aminotransferase in breast cancer. Breast Cancer Res 10: R84.
39. Goldberg EB, Colowick SP (1965) The Role of Glycolysis in the Growth of Tumor Cells: III. Lactic dehydrogenase as the site of action of oxamate on the growth of cultured cells. J Biol Chem 240: 2786-2790.
40. Elwood JC (1968) Effect of Oxamate on Glycolysis and Respiration in Sarcoma 37 Ascites Cells. Cancer Res 28: 2056-2060.
41. Martin-Requero A, Ayuso MS, Parrilla R (1986) Rate-limiting Steps for Hepatic Gluconeogenesis J Biol Chem 261: 13973-13978.
42. Thoren FB, Romero AI, Hellstrand K (2006) Oxygen radicals induce poly(ADP-ribose) polymerase-dependent cell death in cytotoxic lymphocytes. J Immunol 176: 7301-7307. (Pubitemid 43849030)
43. Blenn C, Althaus FR, Malanga M (2006) Poly(ADP-ribose) glycohydrolase silencing protects against H2O2-induced cell death. Biochem J 396: 419-429. (Pubitemid 44228157)
44. Tesniere A, Apetoh L, Ghiringhelli F, Joza N, Panaretakis T, et al. (2008) Immunogenic cancer cell death: a key-lock paradigm. Curr Opin Immunol 20: 504-511.
45. Wang Y, Dawson VL, Dawson TM (2009) Poly(ADP-ribose) signals to mitochondrial AIF: a key event in parthanatos. Exp Neurol 218: 193-202.
46. Shackelford DB, Abt E, Gerken L, Vasquez DS, Seki A, et al. (2013) LKB1 Mutation Sensitizes NSCLC Cells to Phenformin. Cancer Discovery 3: OF14.
47. Yaromina A, Meyer S, Fabian C, Zaleska K, Sattler UG (2012) Effects of three modifiers of glycolysis on ATP, lactate, hypoxia, and growth in human tumor cell lines in vivo. Strahlenther Onkol 188: 431-7.
48. Gottfried E, Kunz-Schughart LA, Ebner S, Mueller-Klieser W, Hoves S, et al (2006) Tumor-derived lactic acid modulates dendritic cell activation and antigen expression. Blood 107: 2013-21. (Pubitemid 43289385)
49. Goetze K, Walenta S, Ksiazkiewicz M, Kunz-Schughart LA, Mueller-Klieser W (2011) Lactate enhances motility of tumor cells and inhibits monocyte migration and cytokine release. Int J Oncol 39: 453-463.
50. Fischer K, Hoffmann P, Voelkl S, Meidenbauer N, Ammer J, et al (2007). Inhibitory effect of tumor cell-derived lactic acid on human T cells. Blood 109: 3812-9. (Pubitemid 46641732)
51. Coppock JD, Wieking BG, Molinolo AA, Gutkind JS, Miskimins WK, at al (2013). Improved clearance during treatment of HPV-positive head and neck cancer through mTOR inhibition. Neoplasia 15: 620-630.
52. McLarty K, Fasih A, Scollard DA, Done SJ, Vines DC, et al. (2009) 18F-FDG small-animal PET/CT differentiates trastuzumab-responsive from unresponsive human breast cancer xenografts in athymic mice. J Nucl Med 50: 1848-1856.
53. Salpeter S, Greyber E, Pasternak G, Salpeter E (2006) Risk of fatal and nonfatal lactic acidosis with metformin use in type 2 diabetes mellitus. Cochrane Database Syst Rev CD002967.
54. Kanno H, Takano T, Fujii H, Tani K, Morisaki T, et al. (1988) A new glucose-6-phosphate dehydrogenase variant (G6PD Iwate) associated with congenital non-spherocytic hemolytic anemia. Nippon Ketsueki Gakkai Zasshi 51: 715-719.