The ketogenic diet for the treatment of glioma: Insights from genetic profiling

Epilepsy Research

Volumn 100, Issue 3, 2012, Pages 327-337

  Scheck, Adrienne C ^a   Abdelwahab, Mohammed G ^a   Fenton, Kathryn E ^a   Stafford, Phillip ^b  

^a ST JOSEPH'S HOSPITAL AND MEDICAL CENTER   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Expression profiling; Gliomas; Growth factors; Ketogenic diet; Reactive oxygen species

Indexed keywords

CYCLIN DEPENDENT KINASE 5; CYCLOOXYGENASE 2; CYTOGLOBIN; GLUTATHIONE PEROXIDASE; GLUTATHIONE PEROXIDASE 7; GROWTH FACTOR; PEROXIREDOXIN 4; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL GENETICS; ANTINEOPLASTIC ACTIVITY; ARTICLE; BRAIN TUMOR; CANCER GROWTH; CANCER INHIBITION; COMPARATIVE STUDY; DISEASE MODEL; EPILEPSY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE MUTATION; GLIOMA; KETOGENIC DIET; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR CELL;

ANIMALS; BRAIN NEOPLASMS; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GLIOMA; HUMANS; KETOGENIC DIET; REACTIVE OXYGEN SPECIES;

EID: 84864108226     PISSN: 09201211     EISSN: 18726844     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2011.09.022     Document Type: Article

References (81)

1. Angoa-Perez M., Kreipke C.W., Thomas D.M., Van Shura K.E., Lyman M., McDonough J.H., Kuhn D.M. Soman increases neuronal COX-2 levels: possible link between seizures and protracted neuronal damage. Neurotoxicology 2010, 31:738-746.
2. Ashrafi M.R., Shams S., Nouri M., Mohseni M., Shabanian R., Yekaninejad M.S., Chegini N., Khodadad A., Safaralizadeh R. A probable causative factor for an old problem: selenium and glutathione peroxidase appear to play important roles in epilepsy pathogenesis. Epilepsia 2007, 48:1750-1755.
3. Baik E.J., Kim E.J., Lee S.H., Moon C. Cyclooxygenase-2 selective inhibitors aggravate kainic acid induced seizure and neuronal cell death in the hippocampus. Brain Res. 1999, 843:118-129.
4. Bellissimo M.I., Amado D., Abdalla D.S., Ferreira E.C., Cavalheiro E.A., Naffah-Mazzacoratti M.G. Superoxide dismutase, glutathione peroxidase activities and the hydroperoxide concentration are modified in the hippocampus of epileptic rats. Epilepsy Res. 2001, 46:121-128.
5. Bough K.J., Rho J.M. Anticonvulsant mechanisms of the ketogenic diet. Epilepsia 2007, 48:43-58.
6. Bough K.J., Wetherington J., Hassel B., Pare J.F., Gawryluk J.W., Greene J.G., Shaw R., Smith Y., Geiger J.D., Dingledine R.J. Mitochondrial biogenesis in the anticonvulsant mechanism of the ketogenic diet. Ann. Neurol. 2006, 60:223-235.
7. Cao Y., Prescott S.M. Many actions of cyclooxygenase-2 in cellular dynamics and in cancer. J. Cell. Physiol. 2002, 190:279-286.
8. Chen J., Berry M.J. Selenium and selenoproteins in the brain and brain diseases. J. Neurochem. 2003, 86:1-12.
9. Cheng G., Lambeth J.D. NOXO1 Regulation of lipid binding, localization, and activation of NOX1 by the Phox homology (PX) domain. J. Biol. Chem. 2004, 279:4737-4742.
10. Demaria S., Pikarsky E., Karin M., Coussens L.M., Chen Y.C., El-Omar E.M., Trinchieri G., Dubinett S.M., Mao J.T., Szabo E., Krieg A., Weiner G.J., Fox B.A., Coukos G., Wang E., Abraham R.T., Carbone M., Lotze M.T. Cancer and inflammation: promise for biologic therapy. J. Immunother. 2010, 33:335-351.
11. Eisinger M., Marko O., Ogata S.-I., Old L.J. Growth regulation of human melanocytes: mitogenic factors in extracts of melanoma, astrocytoma, and fibroblast cell lines. Science 1985, 229:984-986.
12. Ferreira S.H., Moncada S., Vane J.R. Further experiments to establish that the analgesic action of aspirin-like drugs depends on the inhibition of prostaglandin biosynthesis. Br. J. Pharmacol. 1973, 47:629P-630P.
13. Fretland D.J. Potential role of prostaglandins and leukotrienes in multiple sclerosis and experimental allergic encephalomyelitis. Prostaglandins Leukot. Essent. Fatty Acids 1992, 45:249-257.
14. Fruehauf J.P., Meyskens F.L. Reactive oxygen species: a breath of life or death?. Clin. Cancer Res. 2007, 13:789-794.
15. Gasior M., Rogawski M.A., Hartman A.L. Neuroprotective and disease-modifying effects of the ketogenic diet. Behav. Pharmacol. 2006, 17:431-439.
16. Giglio P., Levin V. Cyclooxygenase-2 inhibitors in glioma therapy. Am. J. Ther. 2004, 11:141-143.
17. Giglio P., Villano J.L. Newly diagnosed high-grade gliomas. Curr. Treat. Options Neurol. 2010, 12:309-320.
18. Greco A., Minghetti L., Sette G., Fieschi C., Levi G. Cerebrospinal fluid isoprostane shows oxidative stress in patients with multiple sclerosis. Neurology 1999, 53:1876-1879.
19. Harris R.E. Cyclooxygenase-2 (cox-2) and the inflammogenesis of cancer. Subcell. Biochem. 2007, 42:93-126.
20. Hertting G., Seregi A. Formation and function of eicosanoids in the central nervous system. Ann. N. Y. Acad. Sci. 1989, 559:84-99.
21. Holtman L., van Vliet E.A., van S.R., Queiroz C.M., Aronica E., Gorter J.A. Effects of SC58236, a selective COX-2 inhibitor, on epileptogenesis and spontaneous seizures in a rat model for temporal lobe epilepsy. Epilepsy Res. 2009, 84:56-66.
22. Hoozemans J.J., Rozemuller J.M., van Haastert E.S., Veerhuis R., Eikelenboom P. Cyclooxygenase-1 and -2 in the different stages of Alzheimer's disease pathology. Curr. Pharm. Des. 2008, 14:1419-1427.
23. Humphrey P.A., Wong A.J., Vogelstein B., Friedman H.S., Werner M.H., Bigner D.D., Bigner S.H. Amplication and expression of epidermal growth factor receptor gene in human glioma xenografts. Cancer Res. 1988, 48:2231-2238.
24. Jain S.K., Kannan K., Lim G. Ketosis (acetoacetate) can generate oxygen radicals and cause increased lipid peroxidation and growth inhibition in human endothelial cells. Free Radic. Biol. Med. 1998, 25:1083-1088.
25. Jain S.K., McVie R. Hyperketonemia can increase lipid peroxidation and lower glutathione levels in human erythrocytes in vitro and in type 1 diabetic patients. Diabetes 1999, 48:1850-1855.
26. Jarrett S.G., Milder J.B., Liang L.P., Patel M. The ketogenic diet increases mitochondrial glutathione levels. J. Neurochem. 2008, 106:1044-1051.
27. Jiang D., Akopian G., Ho Y.S., Walsh J.P., Andersen J.K. Chronic brain oxidation in a glutathione peroxidase knockout mouse model results in increased resistance to induced epileptic seizures. Exp. Neurol. 2000, 164:257-268.
28. Kelley K.A., Ho L., Winger D., Freire-Moar J., Borelli C.B., Aisen P.S., Pasinetti G.M. Potentiation of excitotoxicity in transgenic mice overexpressing neuronal cyclooxygenase-2. Am. J. Pathol. 1999, 155:995-1004.
29. Kim C.K., Joe Y.A., Lee S.K., Kim E.K.O.E., Kim H.K., Oh B.J., Hong S.H., Hong Y.K. Enhancement of anti-tumor activity by low-dose combination of the recombinant urokinase kringle domain and celecoxib in a glioma model. Cancer Lett. 2010, 288:251-260.
30. Kim D.Y., Rho J.M. The ketogenic diet and epilepsy. Curr. Opin. Clin. Nutr. Metab. Care 2008, 11:113-120.
31. Knott C., Stern G., Wilkin G.P. Inflammatory regulators in Parkinson's disease: iNOS, lipocortin-1, and cyclooxygenases-1 and -2. Mol. Cell. Neurosci. 2000, 16:724-739.
32. Le Belle J.E., Orozco N.M., Paucar A.A., Saxe J.P., Mottahedeh J., Pyle A.D., Wu H., Kornblum H.I. Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell 2011, 8:59-71.
33. Li D., Chen X.Q., Li W.J., Yang Y.H., Wang J.Z., Yu A.C. Cytoglobin up-regulated by hydrogen peroxide plays a protective role in oxidative stress. Neurochem. Res. 2007, 32:1375-1380.
34. Maalouf M., Sullivan P.G., Davis L., Kim D.Y., Rho J.M. Ketones inhibit mitochondrial production of reactive oxygen species production following glutamate excitotoxicity by increasing NADH oxidation. Neuroscience 2007, 145:256-264.
35. Marcheselli V.L., Bazan N.G. Sustained induction of prostaglandin endoperoxide synthase-2 by seizures in hippocampus. Inhibition by a platelet-activating factor antagonist. J. Biol. Chem. 1996, 271:24794-24799.
36. Marsh J., Mukherjee P., Seyfried T.N. Drug/diet synergy for managing malignant astrocytoma in mice: 2-deoxy-d-glucose and the restricted ketogenic diet. Nutr. Metab. 2008, 5:33.
37. Mattila S., Tuominen H., Koivukangas J., Stenback F. The terminal prostaglandin synthases mPGES-1, mPGES-2, and cPGES are all overexpressed in human gliomas. Neuropathology 2009, 29:156-165.
38. Minghetti L. Role of COX-2 in inflammatory and degenerative brain diseases. Subcell. Biochem. 2007, 42:127-141.
39. Moots P.L., Shapiro J.R. Partial characterization of platelet-derived growth factor isoforms from tissue samples of malignant gliomas. Proc. Am. Assoc. Cancer Res. 1989, 30/64. (Ref. type: abstract).
40. Morford L.A., Boghaert E.R., Brooks W.H., Roszman T.L. Insulin-like growth factors (IGF) enhance three-dimensional (3D) growth of human glioblastomas. Cancer Lett. 1997, 115:81-90.
41. Mueller S.G., Trabesinger A.H., Boesiger P., Wieser H.G. Brain glutathione levels in patients with epilepsy measured by in vivo (1)H-MRS. Neurology 2001, 57:1422-1427.
42. Mukherjee P., Abate L.E., Seyfried T.N. Antiangiogenic and proapoptotic effects of dietary restriction on experimental mouse and human brain tumors. Clin. Cancer Res. 2004, 10:5622-5629.
43. Mukherjee P., El-Abbadi M.M., Kasperzyk J.L., Ranes M.K., Seyfried T.N. Dietary restriction reduces angiogenesis and growth in an orthotopic mouse brain tumour model. Br. J. Cancer 2002, 86:1615-1621.
44. Murad A., Lewis S.J., Smith G.D., Collin S.M., Chen L., Hamdy F.C., Neal D.E., Donovan J., Martin R.M. PTGS2-899G>C and prostate cancer risk: a population-based nested case-control study (ProtecT) and a systematic review with meta-analysis. Prostate Cancer Prostatic Dis. 2009, 12:296-300.
45. Nectoux J., Fichou Y., Cagnard N., Bahi-Buisson N., Nusbaum P., Letourneur F., Chelly J., Bienvenu T. Cell cloning-based transcriptome analysis in cyclin-dependent kinase-like 5 mutation patients with severe epileptic encephalopathy. J. Mol. Med. 2010.
46. Noble M., Mayer-Pröschel M. Growth factors, glia and gliomas. J. Neuro-Oncol. 1997, 35:193-209.
47. Noh H.S., Lee H.P., Kim D.W., Kang S.S., Cho G.J., Rho J.M., Choi W.S. A cDNA microarray analysis of gene expression profiles in rat hippocampus following a ketogenic diet. Brain Res. Mol. Brain Res. 2004, 129:80-87.
48. Okado-Matsumoto A., Matsumoto A., Fujii J., Taniguchi N. Peroxiredoxin IV is a secretable protein with heparin-binding properties under reduced conditions. J. Biochem. 2000, 127:493-501.
49. Pedersen P.-H., Ness G.O., Engebraaten O., Bjerkvig R., Lillehaug J.R., Laerum O.D. Heterogeneous response to the growth factors [EGF, PDGF (bb), TGF-α, bFGF, IL-2] on glioma spheroid growth, migration and invasion. Int. J. Cancer 1994, 56:255-261.
50. Pereira C., Medeiros R.M., nis-Ribeiro M.J. Cyclooxygenase polymorphisms in gastric and colorectal carcinogenesis: are conclusive results available?. Eur. J. Gastroenterol. Hepatol. 2009, 21:76-91.
51. Pigeolet E., Remacle J. Susceptibility of glutathione peroxidase to proteolysis after oxidative alteration by peroxides and hydroxyl radicals. Free Radic. Biol. Med. 1991, 11:191-195.
52. Polascheck N., Bankstahl M., Loscher W. The COX-2 inhibitor parecoxib is neuroprotective but not antiepileptogenic in the pilocarpine model of temporal lobe epilepsy. Exp. Neurol. 2010, 224:219-233.
53. Rose J.W., Hill K.E., Watt H.E., Carlson N.G. Inflammatory cell expression of cyclooxygenase-2 in the multiple sclerosis lesion. J. Neuroimmunol. 2004, 149:40-49.
54. Ruge M.I., Ilmberger J., Tonn J.C., Kreth F.W. Health-related quality of life and cognitive functioning in adult patients with supratentorial WHO grade II glioma: status prior to therapy. J. Neurooncol. 2011, 103:129-136.
55. Ruggiero A., Cefalo G., Garre M.L., Massimino M., Colosimo C., Attina G., Lazzareschi I., Maurizi P., Ridola V., Mazzarella G., Caldarelli M., Rocco C.D., Madon E., Abate M.E., Clerico A., Sandri A., Riccardi R. Phase II trial of temozolomide in children with recurrent high-grade glioma. J. Neurooncol. 2005, 1-6.
56. Schonthal A.H. Antitumor properties of dimethyl-celecoxib, a derivative of celecoxib that does not inhibit cyclooxygenase-2: implications for glioma therapy. Neurosurg. Focus 2006, 20:E21.
57. Schwartzkroin P.A. Mechanisms underlying the anti-epileptic efficacy of the ketogenic diet. Epilepsy Res. 1999, 37:171-180.
58. Seyfried T.N., Mukherjee P. Targeting energy metabolism in brain cancer: review and hypothesis. Nutr. Metab. 2005, 2:30-38.
59. Seyfried T.N, Sanderson T.M., El-Abbadi M.M., 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.
60. Seyfried T.N., Shelton L.M. Cancer as a metabolic disease. Nutr. Metab. (Lond.) 2010, 7:7.
61. Sharma A.K., Searfoss G.H., Reams R.Y., Jordan W.H., Snyder P.W., Chiang A.Y., Jolly R.A., Ryan T.P. Kainic acid-induced F-344 rat model of mesial temporal lobe epilepsy: gene expression and canonical pathways. Toxicol. Pathol. 2009, 37:776-789.
62. Sobolewski C., Cerella C., Dicato M., Ghibelli L., Diederich M. The role of cyclooxygenase-2 in cell proliferation and cell death in human malignancies. Int. J. Cell Biol. 2010, 215158. (Epub on March 17, 2010).
63. Soroceanu L., Kharbanda S., Chen R., Soriano R.H., Aldape K., Misra A., Zha J., Forrest W.F., Nigro J.M., Modrusan Z., Feuerstein B.G., Phillips H.S. Identification of IGF2 signaling through phosphoinositide-3-kinase regulatory subunit 3 as a growth-promoting axis in glioblastoma. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:3466-3471.
64. Spulber G., Spulber S., Hagenas L., Amark P., Dahlin M. Growth dependence on insulin-like growth factor-1 during the ketogenic diet. Epilepsia 2009, 50:297-303.
65. Stafford P., Abdelwahab M.G., Kim d.Y., Preul M.C., Rho J.M., Scheck A.C. The ketogenic diet reverses gene expression patterns and reduces reactive oxygen species levels when used as an adjuvant therapy for glioma. Nutr. Metab. (Lond.) 2010, 7:74.
66. Sudha K., Rao A.V., Rao A. Oxidative stress and antioxidants in epilepsy. Clin. Chim. Acta 2001, 303:19-24.
67. Sullivan P.G., Rippy N.A., Dorenbos K., Concepcion R.C., Agarwal A.K., Rho J.M. The ketogenic diet increases mitochondrial uncoupling protein levels and activity. Ann. Neurol. 2004, 55:576-580.
68. Takemiya T., Maehara M., Matsumura K., Yasuda S., Sugiura H., Yamagata K. Prostaglandin E2 produced by late induced COX-2 stimulates hippocampal neuron loss after seizure in the CA3 region. Neurosci. Res. 2006, 56:103-110.
69. Teismann P., Tieu K., Choi D.K., Wu D.C., Naini A., Hunot S., Vila M., Jackson-Lewis V., Przedborski S. Cyclooxygenase-2 is instrumental in Parkinson's disease neurodegeneration. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:5473-5478.
70. Thorn C.F., Grosser T., Klein T.E., Altman R.B. PharmGKB summary: very important pharmacogene information for PTGS2. Pharmacogenet. Genomics 2010, (Epub ahead of print).
71. Toscano C.D., Ueda Y., Tomita Y.A., Vicini S., Bosetti F. Altered GABAergic neurotransmission is associated with increased kainate-induced seizure in prostaglandin-endoperoxide synthase-2 deficient mice. Brain Res. Bull. 2008, 75:598-609.
72. Trojan J., Cloix J.F., Ardourel M.Y., Chatel M., Anthony D.D. Insulin-like growth factor type I biology and targeting in malignant gliomas. Neuroscience 2007, 145:795-811.
73. Utomo A., Jiang X., Furuta S., Yun J., Levin D.S., Wang Y.C., Desai K.V., Green J.E., Chen P.L., Lee W.H. Identification of a novel putative non-selenocysteine containing phospholipid hydroperoxide glutathione peroxidase (NPGPx) essential for alleviating oxidative stress generated from polyunsaturated fatty acids in breast cancer cells. J. Biol. Chem. 2004, 279:43522-43529.
74. Waldbaum S., Patel M. Mitochondrial dysfunction and oxidative stress: a contributing link to acquired epilepsy?. J. Bioenergy Biomembr. 2010, 42:449-455.
75. Warburg O. On the origin of cancer cells. Science 1956, 123:309-314.
76. Ward K.P., Arthur J.R., Russell G., Aggett P.J. Blood selenium content and glutathione peroxidase activity in children with cystic fibrosis, coeliac disease, asthma, and epilepsy. Eur. J. Pediatr. 1984, 142:21-24.
77. Weber G.F., Maertens P., Meng X.Z., Pippenger C.E. Glutathione peroxidase deficiency and childhood seizures. Lancet 1991, 337:1443-1444.
78. Westermark B., Nistér M., Heldin C.-H. Growth factors and oncogenes in human malignant glioma. Neurol. Clin. 1985, 3:785-799.
79. Westphal M., Herrmann H.-D. Growth factor biology and oncogene activation in human gliomas and their implications for specific therapeutic concepts. Neurosurgery 1989, 25:681-694.
80. Zhou W., Mukherjee P., Kiebish M.A., Markis W.T., Mantis J.G., Seyfried T.N. The calorically restricted ketogenic diet, an effective alternative therapy for malignant brain cancer. Nutr. Metab. (Lond.) 2007, 4:5.
81. Ziegler D.R., Ribeiro L.C., Hagenn M., Siqueira I.R., Araujo E., Torres I.L., Gottfried C., Netto C.A., Goncalves C.A. Ketogenic diet increases glutathione peroxidase activity in rat hippocampus. Neurochem. Res. 2003, 28:1793-1797.