Targeting energy metabolism in brain cancer: review and hypothesis

Kaiser J: No meeting of minds on childhood cancer. Science. 1999, 286: 1832-1834. 10.1126/science.286.5446.1832. Lowry JK, Snyder JJ, Lowry PW: Brain tumors in the elderly: recent trends in a Minnesota cohort study. Arch Neurol. 1998, 55: 922-928. 10.1001/archneur.55.7.922. Kaatsch P, Rickert CH, Kuhl J, Schuz J, Michaelis J: Population-based epidemiologic data on brain tumors in German children. Cancer. 2001, 92: 3155-3164. 10.1002/1097-0142(20011215)92:12<3155::AID-CNCR10158>3.0.CO;2-C. Jukich PJ, McCarthy BJ, Surawicz TS, Freels S, Davis FG: Trends in incidence of primary brain tumors in the United States, 1985–1994. Neuro-oncol. 2001, 3: 141-151. 10.1215/S1522851700000557. Zimmerman HM: The nature of gliomas as revealed by animal experimentation. Amer J Pathol. 1955, 31: 1-29. Chang SM, Parney IF, Huang W, Anderson FA, Asher AL, Bernstein M, Lillehei KO, Brem H, Berger MS, Laws ER: Patterns of care for adults with newly diagnosed malignant glioma. Jama. 2005, 293: 557-564. 10.1001/jama.293.5.557. Fisher PG, Buffler PA: Malignant gliomas in 2005: where to GO from here?. Jama. 2005, 293: 615-617. 10.1001/jama.293.5.615. Seyfried TN: Perspectives on brain tumor formation involving macrophages, glia, and neural stem cells. Perspect Biol Med. 2001, 44: 263-282. Sonnenschein C, Soto AM: The Society of Cells: Cancer and the Control of Cell Proliferation. 1999, New York: Springer-Verlag Shapiro WR: Current therapy for brain tumors: back to the future. Arch Neurol. 1999, 56: 429-432. 10.1001/archneur.56.4.429. Sonnenschein C, Soto AM: Somatic mutation theory of carcinogenesis: why it should be dropped and replaced. Mol Carcinog. 2000, 29: 205-211. 10.1002/1098-2744(200012)29:4<205::AID-MC1002>3.0.CO;2-W. Kiebish MA, Seyfried TN: Absence of pathogenic mitochondrial DNA mutations in mouse brain tumors. BMC Cancer. 2005, 5: 102-10.1186/1471-2407-5-102. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U: Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005, 352: 987-996. 10.1056/NEJMoa043330. Veech RL: The therapeutic implications of ketone bodies: the effects of ketone bodies in pathological conditions: ketosis, ketogenic diet, redox states, insulin resistance, and mitochondrial metabolism. Prostaglandins Leukot Essent Fatty Acids. 2004, 70: 309-319. 10.1016/j.plefa.2003.09.007. Greene AE, Todorova MT, Seyfried TN: Perspectives on the metabolic management of epilepsy through dietary reduction of glucose and elevation of ketone bodies. J Neurochem. 2003, 86: 529-537. 10.1046/j.1471-4159.2003.01862.x. Veech RL: Metabolic control analysis of ketone and insulin action: Implications for phenotyping of disease and design of therapy. 2002, http://www.biodynamichealthaging.org/ Strohman R: Maneuvering in the complex path from genotype to phenotype. Science. 2002, 296: 701-703. 10.1126/science.1070534. Kacser H, Burns JA: The molecular basis of dominance. Genetics. 1981, 97: 639-666. Greenspan RJ: The flexible genome. Nat Rev Genet. 2001, 2: 383-387. 10.1038/35072018. Seyfried TN, Mukherjee P, Adams E, Mulroony T, Abate LE: Metabolic Control of Brain Cancer: Role of Glucose and Ketone Bodies. Proc Amer Assoc Cancer Res. 2005, 46: 1147- Seyfried TN, Sanderson TM, El-Abbadi MM, McGowan R, Mukherjee P: Role of glucose and ketone bodies in the metabolic control of experimental brain cancer. Br J Cancer. 2003, 89: 1375-1382. 10.1038/sj.bjc.6601269. Kirsch WM, Schulz Q, Van Buskirk J, Nakane P: Anaerobic energy metabolism in brain tumors. Prog Exp Tumor Res. 1972, 17: 163-191. Mangiardi JR, Yodice P: Metabolism of the malignant astrocytoma. Neurosurgery. 1990, 26: 1-19. 10.1097/00006123-199001000-00001. Lichtor T, Dohrmann GJ: Respiratory patterns in human brain tumors. Neurosurgery. 1986, 19: 896-899. Lowry OH, Passonneau JV, Hasselberger FX, Shulz DW: Effect of ischemia on known substrates and cofactors of the glycolytic pathway in brain. J Biol Chem. 1964, 239: 18-30. Clarke DD, Sokoloff L: Circulation and energy metabolism in the brain. Basic Neurochemistry. Edited by: Siegel GJ, Agranoff BW, Albers RW, Fisher SK, Uhler MD. 1999, New York: Lippincott-Raven, 637-669. sixth Cahill GF: Starvation in man. N Engl J Med. 1970, 282: 668-675. Ebert D, Haller RG, Walton ME: Energy contribution of octanoate to intact rat brain metabolism measured by 13C nuclear magnetic resonance spectroscopy. J Neurosci. 2003, 23: 5928-5935. Allen NJ, Karadottir R, Attwell D: A preferential role for glycolysis in preventing the anoxic depolarization of rat hippocampal area CA1 pyramidal cells. J Neurosci. 2005, 25: 848-859. 10.1523/JNEUROSCI.4157-04.2005. Pellerin L, Pellegri G, Martin JL, Magistretti PJ: Expression of monocarboxylate transporter mRNAs in mouse brain: support for a distinct role of lactate as an energy substrate for the neonatal vs. adult brain. Proc Natl Acad Sci U S A. 1998, 95: 3990-3995. 10.1073/pnas.95.7.3990. Pellerin L, Bergersen LH, Halestrap AP, Pierre K: Cellular and subcellular distribution of monocarboxylate transporters in cultured brain cells and in the adult brain. J Neurosci Res. 2005, 79: 55-64. 10.1002/jnr.20307. Owen OE, Morgan AP, Kemp HG, Sullivan JM, Herrera MG, Cahill GF: Brain metabolism during fasting. J Clin Invest. 1967, 46: 1589-1595. VanItallie TB, Nufert TH: Ketones: metabolism's ugly duckling. Nutr Rev. 2003, 61: 327-341. 10.1301/nr.2003.oct.327-341. Morris AA: Cerebral ketone body metabolism. J Inherit Metab Dis. 2005, 28: 109-121. 10.1007/s10545-005-5518-0. Cahill GF, Veech RL: Ketoacids? Good medicine?. Trans Am Clin Climatol Assoc. 2003, 114: 149-161. discussion 162–143 Mantis JG, Centeno NA, Todorova MT, McGowan R, Seyfried TN: Management of multifactorial idiopathic epilepsy in EL mice with caloric restriction and the ketogenic diet: role of glucose and ketone bodies. Nutr Metab (Lond). 2004, 1: 11-10.1186/1743-7075-1-11. Seyfried TN, Mukherjee P: Anti-Angiogenic and Pro-Apoptotic Effects of Dietary Restriction in Experimental Brain Cancer: Role of Glucose and Ketone Bodies. Integration/Interaction of Oncologic Growth. Edited by: Meadows GG. 2005, New York: Kluwer Academic, 15: 2 Leino RL, Gerhart DZ, Duelli R, Enerson BE, Drewes LR: Diet-induced ketosis increases monocarboxylate transporter (MCT1) levels in rat brain. Neurochem Int. 2001, 38: 519-527. 10.1016/S0197-0186(00)00102-9. Koehler-Stec EM, Simpson IA, Vannucci SJ, Landschulz KT, Landschulz WH: Monocarboxylate transporter expression in mouse brain. Am J Physiol. 1998, 275: E516-524. Zhang F, Vannucci SJ, Philp NJ, Simpson IA: Monocarboxylate transporter expression in the spontaneous hypertensive rat: effect of stroke. J Neurosci Res. 2005, 79: 139-145. 10.1002/jnr.20312. Pan JW, de Graaf RA, Rothman DL, Hetherington HP: 13C-[2,4]-b-hydroxybutyrate metabolism in human brain. J Neurochem. 2002, 81 (suppl 1): 45- Fredericks M, Ramsey RB: 3-Oxo acid coenzyme A transferase activity in brain and tumors of the nervous system. J Neurochem. 1978, 31: 1529-1531. Bhagavan NV: Medical Biochemistry. 2002, New York: Harcourt, Fourth Veech RL, Chance B, Kashiwaya Y, Lardy HA, Cahill GF: Ketone bodies, potential therapeutic uses. IUBMB Life. 2001, 51: 241-247. Laterra J, Keep R, Betz AL, Goldstein GW: Blood-brain-cerebrospinal fluid barriers. Basic Neurochemistry: Molecular, Cellular and Medical Aspects. Edited by: Siegel GJ, Agranoff BW, Albers RW, Fisher SK, Uhler MD. 1999, New York: Lippincott-Raven, 671-689. sixth Fanelli C, Di Vincenzo A, Modarelli F, Lepore M, Ciofetta M, Epifano L, Pampanelli S, Brunetti P, Bolli GB: Post-hypoglycaemic hyperketonaemia does not contribute to brain metabolism during insulin-induced hypoglycaemia in humans. Diabetologia. 1993, 36: 1191-1197. 10.1007/BF00401065. Kashiwaya Y, Takeshima T, Mori N, Nakashima K, Clarke K, Veech RL: D-beta-hydroxybutyrate protects neurons in models of Alzheimer's and Parkinson's disease. Proc Natl Acad Sci U S A. 2000, 97: 5440-5444. 10.1073/pnas.97.10.5440. Masuda R, Monahan JW, Kashiwaya Y: D-beta-hydroxybutyrate is neuroprotective against hypoxia in serum-free hippocampal primary cultures. J Neurosci Res. 2005, 80: 501-509. 10.1002/jnr.20464. Nehlig A, Pereira de Vasconcelos A: Glucose and ketone body utilization by the brain of neonatal rats. Prog Neurobiol. 1993, 40: 163-221. 10.1016/0301-0082(93)90022-K. Sato K, Kashiwaya Y, Keon CA, Tsuchiya N, King MT, Radda GK, Chance B, Clarke K, Veech RL: Insulin, ketone bodies, and mitochondrial energy transduction. Faseb J. 1995, 9: 651-658. Chance B, Sies H, Boveris A: Hydroperoxide metabolism in mammalian organs. Physiol Rev. 1979, 59: 527-605. Rhodes CG, Wise RJ, Gibbs JM, Frackowiak RS, Hatazawa J, Palmer AJ, Thomas DG, Jones T: In vivo disturbance of the oxidative metabolism of glucose in human cerebral gliomas. Ann Neurol. 1983, 14: 614-626. 10.1002/ana.410140604. 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 (Pt 2): 477-482. Roslin M, Henriksson R, Bergstrom P, Ungerstedt U, Bergenheim AT: Baseline levels of glucose metabolites, glutamate and glycerol in malignant glioma assessed by stereotactic microdialysis. J Neurooncol. 2003, 61: 151-160. 10.1023/A:1022106910017. Floridi A, Paggi MG, Fanciulli M: Modulation of glycolysis in neuroepithelial tumors. J Neurosurg Sci. 1989, 33: 55-64. Galarraga J, Loreck DJ, Graham JF, DeLaPaz RL, Smith BH, Hallgren D, Cummins CJ: Glucose metabolism in human gliomas: correspondence of in situ and in vitro metabolic rates and altered energy metabolism. Metab Brain Dis. 1986, 1: 279-291. 10.1007/BF00999357. Mies G, Paschen W, Ebhardt G, Hossmann KA: Relationship between of blood flow, glucose metabolism, protein synthesis, glucose and ATP content in experimentally-induced glioma (RG1 2.2) of rat brain. J Neurooncol. 1990, 9: 17-28. 10.1007/BF00167064. Oudard S, Boitier E, Miccoli L, Rousset S, Dutrillaux B, Poupon MF: Gliomas are driven by glycolysis: putative roles of hexokinase, oxidative phosphorylation and mitochondrial ultrastructure. Anticancer Res. 1997, 17: 1903-1911. Tisdale MJ: Biology of cachexia. J Natl Cancer Inst. 1997, 89: 1763-1773. 10.1093/jnci/89.23.1763. Patel MS, Russell JJ, Gershman H: Ketone-body metabolism in glioma and neuroblastoma cells. Proc Natl Acad Sci U S A. 1981, 78: 7214-7218. Roeder LM, Poduslo SE, Tildon JT: Utilization of ketone bodies and glucose by established neural cell lines. J Neurosci Res. 1982, 8: 671-682. 10.1002/jnr.490080412. Sawai M, Yashiro M, Nishiguchi Y, Ohira M, Hirakawa K: Growth-inhibitory effects of the ketone body, monoacetoacetin, on human gastric cancer cells with succinyl-CoA: 3-oxoacid CoA-transferase (SCOT) deficiency. Anticancer Res. 2004, 24: 2213-2217. Tisdale MJ: Role of acetoacetyl-CoA synthetase in acetoacetate utilization by tumor cells. Cancer Biochem Biophys. 1984, 7: 101-107. Portais JC, Voisin P, Merle M, Canioni P: Glucose and glutamine metabolism in C6 glioma cells studied by carbon 13 NMR. Biochimie. 1996, 78: 155-164. 10.1016/0300-9084(96)89500-9. Meixensberger J, Herting B, Roggendorf W, Reichmann H: Metabolic patterns in malignant gliomas. J Neurooncol. 1995, 24: 153-161. 10.1007/BF01078485. Pedersen PL: Tumor mitochondria and the bioenergetics of cancer cells. Prog Exp Tumor Res. 1978, 22: 190-274. Warburg O: The Metabolism of Tumours. 1931, New York: Richard R. Smith Warburg O: On the origin of cancer cells. Science. 1956, 123: 309-314. Cuezva JM, Chen G, Alonso AM, Isidore A, Misek DE, Hanash SM, Beer DG: The bioenergetic signature of lung adenocarcinomas is a molecular marker of cancer diagnosis and prognosis. Carcinogenesis. 2004, 25: 1157-1163. 10.1093/carcin/bgh113. Aisenberg AC: The Glycolysis and Respiration of Tumors. 1961, New York: Academic Press Ikezaki K, Black KL, Conklin SG, Becker DP: Histochemical evaluation of energy metabolism in rat glioma. Neurol Res. 1992, 14: 289-293. Schlame M, Rua D, Greenberg ML: The biosynthesis and functional role of cardiolipin. Prog Lipid Res. 2000, 39: 257-288. 10.1016/S0163-7827(00)00005-9. Canuto RA, Biocca ME, Muzio G, Dianzani MU: Fatty acid composition of phospholipids in mitochondria and microsomes during diethylnitrosamine carcinogenesis in rat liver. Cell Biochem Funct. 1989, 7: 11-19. 10.1002/cbf.290070104. Elstrom RL, Bauer DE, Buzzai M, Karnauskas R, Harris MH, Plas DR, Zhuang H, Cinalli RM, Alavi A, Rudin CM: Akt stimulates aerobic glycolysis in cancer cells. Cancer Res. 2004, 64: 3892-3899. 10.1158/0008-5472.CAN-03-2904. Nebeling LC, Miraldi F, Shurin SB, Lerner E: Effects of a ketogenic diet on tumor metabolism and nutritional status in pediatric oncology patients: two case reports. J Am Coll Nutr. 1995, 14: 202-208. Stafstrom CE, Bough KJ: The ketogenic diet for the treatment of epilepsy: a challenge for nutritional neuroscientists. Nutr Neurosci. 2003, 6: 67-79. 10.1080/1028415031000084427. Freeman JM, Freeman JB, Kelly MT: The Ketogenic Diet: A Treatment for Epilepsy. 2000, New York: Demos, third Stewart JW, Koehler K, Jackson W, Hawley J, Wang W, Au A, Myers R, Birt DF: Prevention of mouse skin tumor promotion by dietary energy restriction requires an intact adrenal gland and glucocorticoid supplementation restores inhibition. Carcinogenesis. 2005, 26: 1077-1084. 10.1093/carcin/bgi051. Zhu Z, Jiang W, Thompson HJ: Mechanisms by which energy restriction inhibits rat mammary carcinogenesis: in vivo effects of corticosterone on cell cycle machinery in mammary carcinomas. Carcinogenesis. 2003, 24: 1225-1231. 10.1093/carcin/bgg077. Patel NV, Finch CE: The glucocorticoid paradox of caloric restriction in slowing brain aging. Neurobiol Aging. 2002, 23: 707-717. 10.1016/S0197-4580(02)00017-9. Mukherjee P, Abate LE, Seyfried TN: Antiangiogenic and proapoptotic effects of dietary restriction on experimental mouse and human brain tumors. Clin Cancer Res. 2004, 10: 5622-5629. 10.1158/1078-0432.CCR-04-0308. Mukherjee P, El-Abbadi MM, Kasperzyk JL, Ranes MK, Seyfried TN: Dietary restriction reduces angiogenesis and growth in an orthotopic mouse brain tumour model. Br J Cancer. 2002, 86: 1615-1621. 10.1038/sj.bjc.6600298. Duan W, Lee J, Guo Z, Mattson MP: Dietary restriction stimulates BDNF production in the brain and thereby protects neurons against excitotoxic injury. J Mol Neurosci. 2001, 16: 1-12. 10.1385/JMN:16:1:1. Birt DF, Yaktine A, Duysen E: Glucocorticoid mediation of dietary energy restriction inhibition of mouse skin carcinogenesis. J Nutr. 1999, 129: 571S-574S. Spindler SR: Rapid and reversible induction of the longevity, anticancer and genomic effects of caloric restriction. Mech Ageing Dev. 2005 Chung HY, Kim HJ, Kim KW, Choi JS, Yu BP: Molecular inflammation hypothesis of aging based on the anti-aging mechanism of calorie restriction. Microsc Res Tech. 2002, 59: 264-272. 10.1002/jemt.10203. Weindruch R, Walford RL: The retardation of aging and disease by dietary restriction. 1988, Springfield, IL: Thomas Tannenbaum A: Nutrition and cancer. Physiopathology of Cancer. Edited by: Homburger F. 1959, NY: Paul B. Hober, 517-562. Rebrin I, Kamzalov S, Sohal RS: Effects of age and caloric restriction on glutathione redox state in mice. Free Radic Biol Med. 2003, 35: 626-635. 10.1016/S0891-5849(03)00388-5. Aronen HJ, Pardo FS, Kennedy DN, Belliveau JW, Packard SD, Hsu DW, Hochberg FH, Fischman AJ, Rosen BR: High microvascular blood volume is associated with high glucose uptake and tumor angiogenesis in human gliomas. Clin Cancer Res. 2000, 6: 2189-2200. Tannenbaum A: The genesis and growth of tumors: II. Effects of caloric restriction per se. Cancer Res. 1942, 2: 460-467. Mukherjee P, Sotnikov AV, Mangian HJ, Zhou JR, Visek WJ, Clinton SK: Energy intake and prostate tumor growth, angiogenesis, and vascular endothelial growth factor expression. J Natl Cancer Inst. 1999, 91: 512-523. 10.1093/jnci/91.6.512. Pennathur S, Ido Y, Heller JI, Byun J, Danda R, Pergola P, Williamson JR, Heinecke JW: Reactive carbonyls and polyunsaturated fatty acids produce a hydroxyl radical-like species: A potential pathway for oxidative damage of retinal proteins in diabetes. J Biol Chem. 2005 Andersson AK, Ronnback L, Hansson E: Lactate induces tumour necrosis factor-alpha, interleukin-6 and interleukin-1beta release in microglial- and astroglial-enriched primary cultures. J Neurochem. 2005, 93: 1327-1333. 10.1111/j.1471-4159.2005.03132.x. Dong W, Selgrade MK, Gilmour IM, Lange RW, Park P, Luster MI, Kari FW: Altered alveolar macrophage function in calorie-restricted rats. Am J Respir Cell Mol Biol. 1998, 19: 462-469. Potts R: Humanity's Descent: The Consequences of Ecological Instability. 1996, New York: William Morrow & Co., Inc Harold FM: The Vital Force: A Study of Bioenergetics. 1986, New York: W. H. Freeman Albers RW, Siegel GJ: Membrane transport. Basic Neurochemistry. Edited by: Siegel GJ, Agranoff BW, Albers RW, Fisher SK, Uhler MD. 1999, New York: Lippincott-Raven, 95-118. sixth Lipton P, Robacker K: Glycolysis and brain function: [K+]o stimulation of protein synthesis and K+ uptake require glycolysis. Fed Proc. 1983, 42: 2875-2880. Nishioka T, Oda Y, Seino Y, Yamamoto T, Inagaki N, Yano H, Imura H, Shigemoto R, Kikuchi H: Distribution of the glucose transporters in human brain tumors. Cancer Res. 1992, 52: 3972-3979. Boado RJ, Black KL, Pardridge WM: Gene expression of GLUT3 and GLUT1 glucose transporters in human brain tumors. Brain Res Mol Brain Res. 1994, 27: 51-57. 10.1016/0169-328X(94)90183-X. Strohman R: Thermodynamics – old laws in medicine and complex disease. Nat Biotechnol. 2003, 21: 477-479. 10.1038/nbt0503-477. Nebeling LC, Lerner E: Implementing a ketogenic diet based on medium-chain triglyceride oil in pediatric patients with cancer. J Am Diet Assoc. 1995, 95: 693-697. 10.1016/S0002-8223(95)00189-1. Covarrubias DJ, Rosen BR, Lev MH: Dynamic magnetic resonance perfusion imaging of brain tumors. Oncologist. 2004, 9: 528-537. 10.1634/theoncologist.9-5-528. Ko YH, Smith BL, Wang Y, Pomper MG, Rini DA, Torbenson MS, Hullihen J, Pedersen PL: Advanced cancers: eradication in all cases using 3-bromopyruvate therapy to deplete ATP. Biochem Biophys Res Commun. 2004, 324: 269-275. 10.1016/j.bbrc.2004.09.047. Fearon KC: Nutritional pharmacology in the treatment of neoplastic disease. Baillieres Clin Gastroenterol. 1988, 2: 941-949. 10.1016/0950-3528(88)90043-7. Sokoloff B, Eddy WH, Saelof CC, Beach J: Glucose antagonists in experimental cancer. Arch Pathol. Magee BA, Potezny N, Rofe AM, Conyers RA: The inhibition of malignant cell growth by ketone bodies. Aust J Exp Biol Med Sci. 1979, 57: 529-539. Landau BR, Laszlo J, Stengle J, Burk D: Certain metabolic and pharmacologic effects in cancer patients given infusions of 2-deoxy-D-glucose. J Natl Cancer Inst. 1958, 21: 485-494. Cleary MP, Jacobson MK, Phillips FC, Getzin SC, Grande JP, Maihle NJ: Weight-cycling decreases incidence and increases latency of mammary tumors to a greater extent than does chronic caloric restriction in mouse mammary tumor virus-transforming growth factor-alpha female mice. Cancer Epidemiol Biomarkers Prev. 2002, 11: 836-843. Meadows GG, Fu Y-M: Dietary restriction of specific amino acids modulates tumor and host interactions. Integration/Interaction of Oncologic Growth. Edited by: Meadows GG. 2005, New York: Kluwer Academic, 15: 2