Ketogenic diet sensitizes glucose control of hippocampal excitability

Journal of Lipid Research

Volumn 55, Issue 11, 2014, Pages 2254-2260

  Kawamura, Masahito ^a   Ruskin, David N ^b   Geiger, Jonathan D ^c   Boison, Detlev ^d   Masino, Susan A ^b  

^a JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b TRINITY COLLEGE   (United States)

^c UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^d LEGACY RESEARCH   (United States)

Author keywords

8 Cyclopentyl 1,3 dipropylxanthine; Adenosine A1 receptors; Bicuculline; Epilepsy; KATP channel; Ketones; Metabolism; Pannexin; Purine; Seizure

Indexed keywords

ADENOSINE A1 RECEPTOR; GLUCOSE; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; GAP JUNCTION PROTEIN; NERVE PROTEIN; PANX1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; ELECTRIC POTENTIAL; EXCITABILITY; FEMALE; HIPPOCAMPAL CA3 REGION; IN VITRO STUDY; IN VIVO STUDY; KETOGENIC DIET; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; SEIZURE; ANIMAL; DEFICIENCY; GENE INACTIVATION; GENETICS; HIPPOCAMPUS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SEIZURES;

ANIMALS; CA3 REGION, HIPPOCAMPAL; CONNEXINS; FEMALE; GENE KNOCKOUT TECHNIQUES; GLUCOSE; HIPPOCAMPUS; KATP CHANNELS; KETOGENIC DIET; MALE; MICE; NERVE TISSUE PROTEINS; RATS; RECEPTOR, ADENOSINE A1; SEIZURES;

EID: 84965187383     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M046755     Document Type: Article

References (54)

1. Schwartz, M. W., and D. Porte, Jr. 2005. Diabetes, obesity, and the brain. Science. 307: 375-379.
2. Cherbuin, N., P. Sachdev, and K. J. Anstey. 2012. Higher normal fasting plasma glucose is associated with hippocampal atrophy: the PATH Study. Neurology. 79: 1019-1026.
3. Aviles-Olmos, I., P. Limousin, A. Lees, and T. Foltynie. 2013. Parkinson's disease, insulin resistance and novel agents of neuroprotection. Brain. 136: 374-384.
4. Kim, B., C. Backus, S. Oh, J. M. Hayes, and E. L. Feldman. 2009. Increased tau phosphorylation and cleavage in mouse models of type 1 and type 2 diabetes. Endocrinology. 150: 5294-5301.
5. Yau, P. L., M. G. Castro, A. Tagani, W. H. Tsui, and A. Convit. 2012. Obesity and metabolic syndrome and functional and structural brain impairments in adolescence. Pediatrics. 130: e856-e864.
6. Wilder, R. M. 1921. The effects of ketonemia on the course of epilepsy. Mayo Clin. Bull. 2: 307-308.
7. Wilder, R. M. 1921. High fat diets in epilepsy. Mayo Clin. Bull. 2: 308.
8. Freeman, J. M., E. P. Vining, D. J. Pillas, P. L. Pyzik, J. C. Casey, and L. M. Kelly. 1998. The efficacy of the ketogenic diet-1998: a prospective evaluation of intervention in 150 children. Pediatrics. 102: 1358-1363.
9. Hassan, A. M., D. L. Keene, S. E. Whiting, P. J. Jacob, J. R. Champagne, and P. Humphreys. 1999. Ketogenic diet in the treatment of refractory epilepsy in childhood. Pediatr. Neurol. 21: 548-552.
10. Groesbeck, D. K., R. M. Bluml, and E. H. Kossoff. 2006. Long-term use of the ketogenic diet in the treatment of epilepsy. Dev. Med. Child Neurol. 48: 978-981.
11. Neal, E. G., H. Chaffe, R. H. Schwartz, M. S. Lawson, N. Edwards, G. Fitzsimmons, A. Whitney, and J. H. Cross. 2008. The ketogenic diet for the treatment of childhood epilepsy: a randomised controlled trial. Lancet Neurol. 7: 500-506.
12. Masino, S. A., M. Kawamura, Jr., C. D. Wasser, L. T. Pomeroy, and D. N. Ruskin. 2009. Adenosine, ketogenic diet and epilepsy: the emerging therapeutic relationship between metabolism and brain activity. Curr. Neuropharmacol. 7: 257-268.
13. Erratum Masino, S. A., M. Kawamura, Jr., C. D. Wasser, L. T. Pomeroy, and D. N. Ruskin. 2010. Adenosine, ketogenic diet and epilepsy: the emerging therapeutic relationship between metabolism and brain activity. Curr. Neuropharmacol. 8: 81.
14. Stafstrom, C. E., and J. M. Rho. 2012. The ketogenic diet as a treatment paradigm for diverse neurological disorders. Front. Pharmacol. 3: 59.
15. Dell, C. A., S. S. Likhodii, K. Musa, M. A. Ryan, W. C. Burnham, and S. C. Cunnane. 2001. Lipid and fatty acid profiles in rats consuming different high-fat ketogenic diets. Lipids. 36: 373-378.
16. Dahlin, M., L. Hjelte, S. Nilsson, and P. Åmark. 2007. Plasma phospholipid fatty acids are influenced by a ketogenic diet enriched with n-3 fatty acids in children with epilepsy. Epilepsy Res. 73: 199-207.
17. 1H-MRS in patients with epilepsy controlled by ketogenic diet. MAGMA. 8: 33-42.
18. Bough, K. J., R. S. Chen, and D. A. Eagles. 1999. Path analysis shows that increasing ketogenic ratio, but not β-hydroxybutyrate, elevates seizure threshold in the rat. Dev. Neurosci. 21: 400-406.
19. Musa-Veloso, K., S. S. Likhodii, and S. C. Cunnane. 2002. Breath acetone is a reliable indicator of ketosis in adults consuming ketogenic meals. Am. J. Clin. Nutr. 76: 65-70.
20. Clarke, K., K. Tchabanenko, R. Pawlosky, E. Carter, M. T. King, K. Musa-Veloso, M. Ho, A. Roberts, J. Robertson, T. B. VanItallie, et al. 2012. Kinetics, safety and tolerability of (R)-3-hydroxybutyl (R)-3-hydroxybutyrate in healthy adult subjects. Regul. Toxicol. Pharmacol. 63: 401-408.
21. D'Agostino, D. P., R. Pilla, H. E. Held, C. S. Landon, M. Puchowicz, H. Brunengraber, C. Ari, P. Arnold, and J. B. Dean. 2013. Therapeutic ketosis with ketone ester delays central nervous system oxygen toxicity seizures in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 304: R829-R836.
22. Huttenlocher, P. R. 1976. Ketonemia and seizures: metabolic and anticonvulsant effects of two ketogenic diets in childhood epilepsy. Pediatr. Res. 10: 536-540.
23. DeVivo, D. C., M. P. Leckie, J. S. Ferrendelli, and D. B. McDougal, Jr. 1978. Chronic ketosis and cerebral metabolism. Ann. Neurol. 3: 331-337.
24. Nakazawa, M., S. Kodama, and T. Matsuo. 1983. Effects of ketogenic diet on electroconvulsive threshold and brain contents of adenosine nucleotides. Brain Dev. 5: 375-380.
25. Thibert, R. L., H. H. Pfeiffer, A. M. Larson, A. R. Raby, A. A. Reynolds, A. K. Morgan, and E. A. Thiele. 2012. Low glycemic index treatment for seizures in Angelman syndrome. Epilepsia. 53: 1498-1502.
26. Kossoff, E. H., G. L. Krauss, J. R. McGrogan, and J. M. Freeman. 2003. Efficacy of the Atkins diet as therapy for intractable epilepsy. Neurology. 61: 1789-1791.
27. Masino, S. A., and J. D. Geiger. 2008. Are purines mediators of the anticonvulsant/neuroprotective effects of ketogenic diets? Trends Neurosci. 31: 273-278.
28. Masino, S. A., M. Kawamura, Jr., D. N. Ruskin, J. Gawryluk, X. Chen, and J. D. Geiger. 2010. Purines and the anti-epileptic actions of ketogenic diets. Open Neurosci. J. 4: 58-63.
29. Dunwiddie, T. V., L. Diao, and W. R. Proctor. 1997. Adenine nucleotides undergo rapid, quantitative conversion to adenosine in the extracellular space in rat hippocampus. J. Neurosci. 17: 7673-7682.
30. 1 receptors. J. Clin. Invest. 121: 2679-2683.
31. 1 receptor. Proc. Natl. Acad. Sci. USA. 98: 9407-9412.
32. Ruskin, D. N., T. A. C. S. Suter, J. L. Ross, and S. A. Masino. 2013. Ketogenic diets and thermal pain: dissociation of hypoalgesia, elevated ketones, and lowered glucose in rats. J. Pain. 14: 467-474.
33. 1 receptors. J. Pharmacol. Exp. Ther. 303: 356-363.
34. 1 receptors in the hippocampal slice. J. Neurosci. 24: 10835-10845.
35. Shram, N. F., L. I. Netchiporouk, C. Martelet, N. Jaffrezic-Renault, and R. Cespuglio. 1997. Brain glucose: voltammetric determination in normal and hyperglycaemic rats using a glucose microsensor. Neuroreport. 8: 1109-1112.
36. Hu, Y., and G. S. Wilson. 1997. Rapid changes in local extracellular rat brain glucose observed with an in vivo glucose sensor. J. Neurochem. 68: 1745-1752.
37. Tian, G-F., and A. J. Baker. 2000. Glycolysis prevents anoxia-induced synaptic transmission damage in rat hippocampal slices. J. Neurophysiol. 83: 1830-1839.
38. Kawamura, M., Jr., and D. N. Ruskin. 2013. Adenosine and autocrine metabolic regulation of neuronal activity. In Adenosine: A Key Link between Metabolism and Brain Activity. S. A. Masino and D. Boison, editors. Springer, New York. 71-85.
39. Thompson, S. M., H. L. Haas, and B. H. Gähwiler. 1992. Comparison of the actions of adenosine at pre- and postsynaptic receptors in the rat hippocampus in vitro. J. Physiol. 451: 347-363.
40. ATP channels. J. Neurosci. 30: 3886-3895.
41. ATP channels. J. Neurosci. 27: 3618-3625.
42. ATP channel opening in response to action potential firing in mouse dentate granule neurons. J. Neurosci. 31: 8689-8696.
43. Romanov, R. A., O. A. Rogachevskaja, M. F. Bystrova, P. Jiang, R. F. Margolskee, and S. S. Kolesnikov. 2007. Afferent neurotransmission mediated by hemichannels in mammalian taste cells. EMBO J. 26: 657-667.
44. Fowler, J. C. 1993. Purine release and inhibition of synaptic transmission during hypoxia and hypoglycemia in rat hippocampal slices. Neurosci. Lett. 157: 83-86.
45. Greene, A. E., M. T. Todorova, R. McGowan, and T. N. Seyfried. 2001. Caloric restriction inhibits seizure susceptibility in epileptic EL mice by reducing blood glucose. Epilepsia. 42: 1371-1378.
46. Mantis, J. G., N. A. Centeno, M. T. Todorova, R. McGowan, and T. N. Seyfried. 2004. Management of multifactorial idiopathic epilepsy in EL mice with caloric restriction and the ketogenic diet: role of glucose and ketone bodies. Nutr. Metab. (Lond). 1: 11.
47. Uhlemann, E. R., and A. H. Neims. 1972. Anticonvulsant properties of the ketogenic diet in mice. J. Pharmacol. Exp. Ther. 180: 231-238.
48. Appleton, D. B., and D. C. DeVivo. 1974. An animal model for the ketogenic diet. Epilepsia. 15: 211-227.
49. Juge, N., J. A. Gray, H. Omote, T. Miyaji, T. Inoue, C. Hara, H. Uneyama, R. H. Edwards, R. A. Nicoll, and Y. Moriyama. 2010. Metabolic control of vesicular glutamate transport and release. Neuron. 68: 99-112.
50. Kim do, Y., J. Vallejo, and J. M. Rho. 2010. Ketones prevent synaptic dysfunction induced by mitochondrial respiratory complex inhibitors. J. Neurochem. 114: 130-141.
51. Samoilova, M., M. Weisspapir, P. Abdelmalik, A. A. Velumian, and P. L. Carlen. 2010. Chronic in vitro ketosis is neuroprotective but not anticonvulsant. J. Neurochem. 113: 826-835.
52. Dunwiddie, T. V., and S. A. Masino. 2001. The role and regulation of adenosine in the central nervous system. Annu. Rev. Neurosci. 24: 31-55.
53. Boison, D., S. A. Masino, and J. D. Geiger. 2011. Homeostatic bioenergetic network regulation: a novel concept to avoid pharmacoresistance in epilepsy. Expert Opin. Drug Discov. 6: 713-724.
54. Samala, R., J. Klein, and K. Borges. 2011. The ketogenic diet changes metabolite levels in hippocampal extracellular fluid. Neurochem. Int. 58: 5-8.