D-amino acid oxidase gene therapy sensitizes glioma cells to the antiglycolytic effect of 3-bromopyruvate

Cancer Gene Therapy

Volumn 19, Issue 1, 2012, Pages 1-18

  El Sayed, S M ^a   Abou El Magd, R M ^a   Shishido, Y ^a   Chung, S P ^a   Sakai, T ^a   Watanabe, H ^a   Kagami, S ^a   Fukui, K ^a,b  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

3 bromopyruvate; D amino acid oxidase; glioblastoma; glycolysis double inhibition; hydrogen peroxide; oxidative stress energy depletion therapy

Indexed keywords

ATELOCOLLAGEN; DEXTRO AMINO ACID OXIDASE; DEXTRO SERINE; HYDROGEN PEROXIDE; PYRUVIC ACID DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ASTROCYTE; CELL PROLIFERATION; CELL VIABILITY; CLONOGENIC ASSAY; CONTROLLED STUDY; DISEASE MODEL; DRUG EFFECT; DRUG SENSITIZATION; FEMALE; GENE THERAPY; GENETIC TRANSFECTION; GLIOBLASTOMA; GLIOMA CELL; GLYCOLYSIS; HUMAN; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SPRAGUE DAWLEY RAT; TUMOR CELL;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELL LINE, TUMOR; D-AMINO-ACID OXIDASE; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; FEMALE; GENE THERAPY; GLIOBLASTOMA; GLIOMA; GLYCOLYSIS; HUMANS; HYDROGEN PEROXIDE; MICE; NEOPLASTIC STEM CELLS; OXIDATIVE STRESS; PYRUVATES; RATS; RATS, SPRAGUE-DAWLEY; TRANSFECTION;

RATTUS;

EID: 83555168279     PISSN: 09291903     EISSN: 14765500     Source Type: Journal    
DOI: 10.1038/cgt.2011.59     Document Type: Article

References (56)

1. Reardon DA, Wen PY. Therapeutic advances in the treatment of glioblastoma: rationale and potential role of targeted agents. Oncologist 2006; 11: 152-164. (Pubitemid 43261762)
2. Kawazoe T, Park HK, Iwana S, Tsuge H, Fukui K. Human D-amino acid oxidase: an update and review. Chem Rec 2007; 7: 305-315.
3. Dale DC, Boxer L, Liles WC. The phagocytes: neutrophils and monocytes. Blood 2008; 112: 935-945.
4. Stegman LD, Zheng H, Neal ER, Ben-Yoseph O, Pollegioni L, Pilone MS et al. Induction of cytotoxic oxidative stress by D-alanine in brain tumor cells expressing Rhodotorula gracilis D-amino acid oxidase: a cancer gene therapy strategy. Hum Gene Ther 1998; 9: 185-193. (Pubitemid 28066163)
5. Wilson JE. Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. J Exp Biol 2003; 206: 2049-2057. (Pubitemid 36761808)
6. Paggi MG, Fanciulli M, Del Carlo C, Citro G, Carapella CM, Floridi A. The membrane-bound hexokinase as a potential marker for malignancy in human gliomas. J Neurosurg Sci 1990; 34: 209-213.
7. Nakashima RA, Paggi MG, Pedersen PL. Contributions of glycolysis and oxidative phosphorylation to adenosine 50-triphosphate production in AS-30D hepatoma cells. Cancer Res 1984; 44: 5702-5706. (Pubitemid 15183582)
8. Pedersen PL. The cancer cell's 'power plants' as promising therapeutic targets: an overview. J Bioenerg Biomembr 2007; 39: 1-12. (Pubitemid 46877182)
9. Warburg O. On the origin of cancer cells. Science 1956; 123: 309-314.
10. Michelakis ED, Sutendra G, Dromparis P, Webster L, Haromy A, Niven E et al. Metabolic modulation of glioblastoma with dichloroacetate. Sci Transl Med 2010; 2: 31-34.
11. Shaw RJ. Glucose metabolism and cancer. Curr Opin Cell Biol 2006; 18: 598-608. (Pubitemid 44692479)
12. Mazurek S, Boschek CB, Eigenbrodt E. The role of phosphometabolites in cell proliferation, energy metabolism, and tumor therapy. J Bioenerg Biomembr 1997; 29: 315-330. (Pubitemid 27498411)
13. Gambhir SS. Molecular imaging of cancer with positron emission tomography. Nat Rev Cancer 2002; 2: 683-693. (Pubitemid 37328919)
14. Mineura K, Yasuda T, Kowada M, Sakamoto T, Ogawa T, Shishido F et al. Positron emission tomographic evaluations in the diagnosis and therapy of multifocal glioblastoma. Report of a pediatric case. Pediatr Neurosci 1986; 12: 208-212.
15. Spence AM, Muzi M, Graham MM, O'Sullivan F, Krohn KA, Link JM et al. Glucose metabolism in human malignant gliomas measured quantitatively with PET, 1-[C-11] glucose and FDG: analysis of the FDG lumped constant. J Nucl Med 1998; 39: 440-448. (Pubitemid 28136841)
16. Geschwind JH, Ko YH, Torbenson MS, Magee C, Pedersen PL. Novel therapy for liver cancer: direct intraarterial injection of a potent inhibitor of ATP production. Cancer Res 2002; 62: 3909-3913. (Pubitemid 34791050)
17. Park HK, Shishido Y, Ichise-Shishido S, Kawazoe T, Ono K, Iwana S et al. Potential role for astroglial D-amino acid oxidase in extracellular D-serine metabolism and cytotoxicity. J Biochem 2006; 139: 295-304.
18. Urai Y, Jinnouchi O, Kwak KT, Suzue A, Nagahiro S, Fukui K. Gene expression of D-amino acid oxidase in cultured rat astrocytes: regional and cell type specific expression. Neurosci Lett 2002; 324: 101-104. (Pubitemid 34457815)
19. Ihrlund LS, Hernlund E, Khan O, Shoshan MC. 3-Bromopyruvate as inhibitor of tumour cell energy metabolism and chemopotentiator of platinum drugs. Mol Oncol 2008; 2: 94-101.
20. Altinoz MA, Bilir A, Ozar E, Onar FD, Sav A. Medroxyprogesterone acetate alone or synergistic with chemotherapy suppresses colony formation and DNA synthesis in C6 glioma in vitro. Int J Dev Neurosci 2001; 19: 541-547. (Pubitemid 32904482)
21. Friedrich J, Seidel C, Ebner R, Kunz-Schughart LA. Spheroid-based drug screen: considerations and practical approach. Nat Protoc 2009; 4: 309-324.
22. Abou El-Magd RM, Park HK, Kawazoe T, Iwana S, Ono K, Chung SP et al. The effect of resperidone on D-amino acid oxidase activity as a hypothesis for a novel mechanism of action in the treatment of schizophrenia. J Psychopharmacol 2010; 24: 1055-1067.
23. Ko YH, Pedersen PL, Geschwind JF. Glucose catabolism in the rabbit VX2 tumor model for liver cancer: characterization and targeting hexokinase. Cancer Lett 2001; 173: 83-91. (Pubitemid 32907513)
24. Pytel P. Spectrum of pediatric gliomas: implications for the development of future therapies. Expert Rev Anticancer Ther 2007; 7: 51-60.
25. Fang J, Seki T, Maeda H. Therapeutic strategies by modulating oxygen stress in cancer and inflammation. Adv Drug Deliv Rev 2009; 61: 290-302.
26. Grobben B, De Deyn PP, Slegers H. Rat C6 glioma as experimental model system for the study of glioblastoma growth and invasion. Cell Tissue Res 2002; 310: 257-270. (Pubitemid 35435769)
27. Nagamatsu S, Nakamichi Y, Inoue N, Inoue M, Nishino H, Sawa H. Rat C6 glioma cell growth is related to glucose transport and metabolism. Biochem J 1996; 319: 477-482. (Pubitemid 26372206)
28. Ikezaki K, Black KL, Conklin SG, Becker DP. Histochemical evaluation of energy metabolism in rat glioma. Neurol Res 1992; 14: 289-293.
29. Machida K, Ohta Y, Osada H. Suppression of apoptosis by cyclophilin D via stabilization of hexokinase II mitochondrial binding in cancer cells. J Biol Chem 2006; 281: 14314-14320. (Pubitemid 43848360)
30. Pedersen PL. Voltage dependent anion channels (VDACs): a brief introduction with a focus on the outer mitochondrial compartment's roles together with hexokinase-2 in the 'Warburg effect' in cancer. J Bioenerg Biomembr 2008; 40: 123-126.
31. da-Silva WS, Gomez-Puyou A, de Gomez-Puyou MT, Moreno-Sanchez R, De Felice FG, de Meis L et al. Mitochondrial bound hexokinase activity as a preventive antioxidant defense: steady-state ADP formation as a regulatory mechanism of membrane potential and reactive oxygen species generation in mitochondria. J Biol Chem 2004; 279: 39846-39855. (Pubitemid 39258256)
32. Yang MS, Yu LC, Gupta RC. Analysis of changes in energy and redox states in HepG2 hepatoma and C6 glioma cells upon exposure to cadmium. Toxicology 2004; 201: 105-113. (Pubitemid 39023938)
33. Makino N, Mise T, Sagara J. Kinetics of hydrogen peroxide elimination by astrocytes and C6 glioma cells: analysis based on a mathematical model. Biochim Biophys Acta 2008; 1780: 927-936.
34. Smith TA. Mammalian hexokinases and their abnormal expression in cancer. Br J Biomed Sci 2000; 57: 170-178. (Pubitemid 30417071)
35. Pelicano H, Martin DS, Xu RH, Huang P. Glycolysis inhibition for anticancer treatment. Oncogene 2006; 25: 254633-254646.
36. Lee KH, Park JH, Won R, Lee H, Nam TS, Lee BH. Inhibition of hexokinase leads to neuroprotection against excitotoxicity in organotypic hippocampal slice culture. J Neurosci Res 2011; 89: 96-107.
37. Kantrowitz JT, Malhotra AK, Cornblatt B, Silipo G, Balla A, Suckow RF et al. High dose D-serine in the treatment of schizophrenia. Schizophr Res 2010; 121: 125-130.
38. Starkov AA, Fiskum G. Regulation of brain mitochondrial H2O2 production by membrane potential and NAD(P)H redox state. J Neurochem 2003; 86: 1101-1107. (Pubitemid 37022186)
39. McEligot AJ, Yang S, Meyskens FLJR. Redox regulation by intrinsic species and extrinsic nutrients in normal and cancer cells. Annu Rev Nutr 2005; 25: 261-295. (Pubitemid 41209003)
40. Korshunov SS, Skulachev VP, Starkov AA. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 1997; 416: 15-18. (Pubitemid 27470791)
41. Kim JS, Ahn KJ, Kim JA, Kim HM, Lee JD, Lee JM et al. Role of reactive oxygen species-mediated mitochondrial dysregulation in 3-bromopyruvate induced cell death in hepatoma cells: ROS-mediated cell death by 3-bromopyruvate. J Bioenerg Biomembr 2008; 40: 607-618.
42. Simons AL, Mattson DM, Dornfeld K, Spitz DR. Glucose deprivation-induced metabolic oxidative stress and cancer therapy. J Cancer Res Ther 2009; 5: 2-6.
43. Qin JZ, Xin H, Nickoloff BJ. 3-Bromopyruvate induces necrotic cell death in sensitive melanoma cell lines. Biochem Biophys Res Commun 2010; 396: 495-500.
44. Tsai KL, Wang SM, Chen CC, Fong TH, Wu ML. Mechanism of oxidative stress-induced intracellular acidosis in rat cerebellar astrocytes and C6 glioma cells. J Physiol 1997; 502: 161-174.
45. Hyslop PA, Hinshaw DB, Halsey Jr WA, Schraufstä tter IU, Sauerheber RD, Spragg RG et al. Mechanisms of oxidantmediated cell injury: the glycolytic and mitochondrial pathways of phosphorylation are major intracellular targets inactivated by hydrogen peroxide. J Biol Chem 1988; 263: 1665-1675. (Pubitemid 18052113)
46. Appelskog IB, Ammerpohl O, Svechnikova IG, Lui WO, Almqvist PM, Ekström TJ. Histone deacetylase inhibitor 4-phenylbutyrate suppresses GAPDH mRNA expression in glioma cells. Int J Oncol 2004; 24: 1419-1425.
47. Mazurek S, Boschek CB, Eigenbrodt E. The role of phosphometabolites in cell proliferation, energy metabolism and tumor therapy. J Bioenerg Biomembr 1997; 29: 315-330. (Pubitemid 27498411)
48. Zong WX, Ditsworth D, Bauer DE, Wang ZQ, Thompson CB. Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev 2004; 18: 1272-1282. (Pubitemid 38720595)
49. Proskuryakov SY, Konoplyannikov AG, Gabai VL. Necrosis: a specific form of programmed cell death? Exp Cell Res 2003; 283: 1-16. (Pubitemid 36259891)
50. Segel IH. Enzyme activation. In: Segel IH (ed). Enzyme kinetics: Behaviour and analysis of rapid equilibrium and steady-state enzyme systems, 1st edn. John Wiley & Sons: Inc. New York, 1993, pp 227-272.
51. Chung SP, Sogabe K, Park HK, Song Y, Ono K, Abou El-Magd RM et al. Potential cytotoxic effect of hydroxypyruvate produced from D-serine by astroglial D-amino acid oxidase. J Biochem 2010; 148: 743-753.
52. Robey RB, Hay N. Mitochondrial hexokinases, novel mediators of the antiapoptotic effects of growth factors and Akt. Oncogene 2006; 25: 4683-4696. (Pubitemid 44187618)
53. Kim W, Yoon JH, Jeong JM, Cheon GJ, Lee TS, Yang JI et al. Apoptosis-inducing antitumor efficacy of hexokinase II inhibitor in hepatocellular carcinoma. Mol Cancer Ther 2007; 6: 2554-2262.
54. Kowaltowski AJ, Castilho RF, Vercesi AE. Opening of the mitochondrial permeability transition pore by uncoupling or inorganic phosphate in the presence of Ca2+ is dependent on mitochondrial-generated reactive oxygen species. FEBS Lett 1996; 378: 150-152.
55. Watanabe K, Sakamoto M, Somiya M, Amin MR, Kamitani H, Watanabe T. Feasibility and limitations of the rat model by C6 gliomas implanted at the subcutaneous region. Neurol Res 2002; 24: 485-490. (Pubitemid 34742684)
56. Ko YH, Smith BL, Wang Y, Pomper MG, Rini DA, Torbenson MS et al. Advanced cancers: eradication in all cases using 3-bromopyruvate therapy to deplete ATP. Biochem Biophys Res Commun 2004; 324: 269-275. (Pubitemid 39311489)