Ketones prevent oxidative impairment of hippocampal synaptic integrity through KATP channels

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Kim, Do Young ^a   Abdelwahab, Mohammed G ^a   Lee, Soo Han ^a   O'Neill, Derek ^a   Thompson, Roger J ^b   Duff, Henry J ^c   Sullivan, Patrick G ^d   Rho, Jong M ^e  

^a BARROW NEUROLOGICAL INSTITUTE   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

^d UNIVERSITY OF KENTUCKY   (United States)

^e ALBERTA CHILDREN'S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYBUTYRIC ACID; ACETOACETIC ACID; ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; DIAZOXIDE; HYDROGEN PEROXIDE; INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; KETONE; NEUROPROTECTIVE AGENT; OXIDIZING AGENT; SULFONYLUREA RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOENERGY; BRAIN ELECTROPHYSIOLOGY; CELL VIABILITY; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; INTRACTABLE EPILEPSY; KETOGENIC DIET; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; RAT; STRATUM RADIATUM; SYNAPTIC INHIBITION; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; ANIMAL; CHANNEL GATING; DRUG EFFECTS; KNOCKOUT MOUSE; METABOLISM; MITOCHONDRION; MOUSE; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; HIPPOCAMPUS; HYDROGEN PEROXIDE; ION CHANNEL GATING; KATP CHANNELS; KETONES; LONG-TERM POTENTIATION; MICE; MICE, KNOCKOUT; MITOCHONDRIA; NEURONAL PLASTICITY; NEUROPROTECTIVE AGENTS; OXIDANTS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RATS; RATS, SPRAGUE-DAWLEY; SULFONYLUREA RECEPTORS;

EID: 84929991757     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0119316     Document Type: Article

References (57)

1. Neal EG, Chaffe H, Schwartz RH, Lawson MS, Edwards N, Fitzsimmons G, et al. The ketogenic diet for the treatment of childhood epilepsy: a randomised controlled trial. Lancet Neurol. 2008; 7: 500-506. doi: 10.1016/S1474-4422(08)70092-9 PMID: 18456557
2. 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. PMID: 10805800
3. Kim do Y, Vallejo J, Rho JM. Ketones prevent synaptic dysfunction induced by mitochondrial respiratory complex inhibitors. J Neurochem. 2010; 114: 130-141. doi: 10.1111/j.1471-4159.2010.06728.x PMID: 20374433
4. Smith SL, Heal DJ, Martin KF. KTX 0101: a potential metabolic approach to cytoprotection in major surgery and neurological disorders. CNS Drug Rev. 2005; 11: 113-140. PMID: 16007235
5. Krikorian R, Shidler MD, Dangelo K, Couch SC, Benoit SC, Clegg DJ. Dietary ketosis enhances memory in mild cognitive impairment. Neurobiol Aging. 2012; 33: 425 e419-427. doi: 10.1016/j.neurobiolaging.2010.10.006 PMID: 21130529
6. Kashiwaya Y, Bergman C, Lee JH, Wan R, King MT, Mughal MR, et al. A ketone ester diet exhibits anxiolytic and cognition-sparing properties, and lessens amyloid and tau pathologies in a mouse model of Alzheimer's disease. Neurobiol Aging. 2013; 34: 1530-1539. doi: 10.1016/j.neurobiolaging.2012.11.023 PMID: 23276384
7. Maalouf M, Rho JM. Oxidative impairment of hippocampal long-term potentiation involves activation of protein phosphatase 2A and is prevented by ketone bodies. J Neurosci Res. 2008; 86: 3322-3330. doi: 10.1002/jnr.21782 PMID: 18646208
8. Kirsch GE, Codina J, Birnbaumer L, Brown AM. Coupling of ATP-sensitive K+ channels to A1 receptors by G proteins in rat ventricular myocytes. Am J Physiol. 1990; 259: H820-826. PMID: 2118729
9. Honore E, Lazdunski M. Single-channel properties and regulation of pinacidil/glibenclamide-sensitive K+ channels in follicular cells from Xenopus oocyte. Pflugers Arch. 1993; 424: 113-121. PMID: 7692382
10. Xie J, Duan L, Qian X, Huang X, Ding J, Hu G. K(ATP) channel openers protect mesencephalic neurons against MPP+-induced cytotoxicity via inhibition of ROS production. J Neurosci Res. 2010; 88: 428-437. doi: 10.1002/jnr.22213 PMID: 19746425
11. Busija DW, Lacza Z, Rajapakse N, Shimizu K, Kis B, Bari F, et al. Targeting mitochondrial ATP-sensitive potassium channels - a novel approach to neuroprotection. Brain Res Brain Res Rev. 2004; 46: 282-294. PMID: 15571770
12. Kane GC, Liu XK, Yamada S, Olson TM, Terzic A. Cardiac KATP channels in health and disease. J Mol Cell Cardiol. 2005; 38: 937-943. PMID: 15910878
13. Costa AD, Garlid KD. MitoKATP activity in healthy and ischemic hearts. J Bioenerg Biomembr. 2009; 41: 123-126. doi: 10.1007/s10863-009-9213-y PMID: 19353252
14. Sun XL, Hu G. ATP-sensitive potassium channels: a promising target for protecting neurovascular unit function in stroke. Clin Exp Pharmacol Physiol. 2010; 37: 243-252. doi: 10.1111/j.1440-1681.2009.05190.x PMID: 19413600
15. Domoki F, Kis B, Nagy K, Farkas E, Busija DW, Bari F. Diazoxide preserves hypercapnia-induced arteriolar vasodilation after global cerebral ischemia in piglets. Am J Physiol Heart Circ Physiol. 2005; 289: H368-373. PMID: 15734886
16. Nagy K, Kis B, Rajapakse NC, Bari F, Busija DW. Diazoxide preconditioning protects against neuronal cell death by attenuation of oxidative stress upon glutamate stimulation. J Neurosci Res. 2004; 76: 697-704. PMID: 15139028
17. Robin E, Simerabet M, Hassoun SM, Adamczyk S, Tavernier B, Vallet B, et al. Postconditioning in focal cerebral ischemia: role of the mitochondrial ATP-dependent potassium channel. Brain Res. 2011; 1375: 137-146. doi: 10.1016/j.brainres.2010.12.054 PMID: 21182830
18. Teshima Y, Akao M, Li RA, Chong TH, Baumgartner WA, Johnston MV, et al. Mitochondrial ATP-sensitive potassium channel activation protects cerebellar granule neurons from apoptosis induced by oxidative stress. Stroke. 2003; 34: 1796-1802. PMID: 12791941
19. Ma W, Berg J, Yellen G. Ketogenic diet metabolites reduce firing in central neurons by opening K(ATP) channels. J Neurosci. 2007; 27: 3618-3625. PMID: 17409226
20. Tanner GR, Lutas A, Martinez-Francois JR, Yellen G. Single K ATP channel opening in response to action potential firing in mouse dentate granule neurons. J Neurosci. 2011; 31: 8689-8696. doi: 10.1523/JNEUROSCI.5951-10.2011 PMID: 21653873
21. Chen Y, Chad JE, Wheal HV. Synaptic release rather than failure in the conditioning pulse results in paired-pulse facilitation during minimal synaptic stimulation in the rat hippocampal CA1 neurones. Neurosci Lett. 1996; 218: 204-208. PMID: 8945764
22. Dargusch R, Schubert D. Specificity of resistance to oxidative stress. J Neurochem. 2002; 81: 1394-1400. PMID: 12068086
23. Izumi Y, Ishii K, Katsuki H, Benz AM, Zorumski CF. beta-Hydroxybutyrate fuels synaptic function during development. Histological and physiological evidence in rat hippocampal slices. J Clin Invest. 1998; 101: 1121-1132. PMID: 9486983
24. Thio LL, Wong M, Yamada KA. Ketone bodies do not directly alter excitatory or inhibitory hippocampal synaptic transmission. Neurology. 2000; 54: 325-331. PMID: 10668691
25. Nordli DR, Jr., De Vivo DC. The ketogenic diet revisited: back to the future. Epilepsia. 1997; 38: 743-749. PMID: 9579900
26. Kim do Y, Rho JM. The ketogenic diet and epilepsy. Curr Opin Clin Nutr Metab Care. 2008; 11: 113-120. doi: 10.1097/MCO.0b013e3282f44c06 PMID: 18301085
27. Robin E, Simerabet M, Hassoun SM, Adamczyk S, Tavernier B, Vallet B, et al. Postconditioning in focal cerebral ischemia: role of the mitochondrial ATP-dependent potassium channel. Brain Res. 2011; 1375: 137-146. doi: 10.1016/j.brainres.2010.12.054 PMID: 21182830
28. Hartman AL, Gasior M, Vining EP, Rogawski MA. The neuropharmacology of the ketogenic diet. Pediatr Neurol. 2007; 36: 281-292. PMID: 17509459
29. Liang HW, Xia Q, Bruce IC. Reactive oxygen species mediate the neuroprotection conferred by a mitochondrial ATP-sensitive potassium channel opener during ischemia in the rat hippocampal slice. Brain Res. 2005; 1042: 169-175. PMID: 15854588
30. Suzuki M, Sasaki N, Miki T, Sakamoto N, Ohmoto-Sekine Y, Tamagawa M, et al. Role of sarcolemmal K(ATP) channels in cardioprotection against ischemia/reperfusion injury in mice. J Clin Invest. 2002; 109: 509-516. PMID: 11854323
31. Choeiri C, Staines WA, Miki T, Seino S, Renaud JM, Teutenberg K, et al. Cerebral glucose transporters expression and spatial learning in the K-ATP Kir6.2(-/-) knockout mice. Behav Brain Res. 2006; 172: 233-239. PMID: 16797737
32. Schroder UH, Hock FJ, Wirth K, Englert HC, Reymann KG. The ATP-regulated K+-channel inhibitor HMR-1372 affects synaptic plasticity in hippocampal slices. Eur J Pharmacol. 2004; 502: 99-104. PMID: 15464094
33. Liu D, Pitta M, Lee JH, Ray B, Lahiri DK, Furukawa K, et al. The KATP channel activator diazoxide ameliorates amyloid-beta and tau pathologies and improves memory in the 3xTgAD mouse model of Alzheimer's disease. J Alzheimers Dis. 2010; 22: 443-457. doi: 10.3233/JAD-2010-101017 PMID: 20847430
34. Ienco EC, LoGerfo A, Carlesi C, Orsucci D, Ricci G, Mancuso M, et al. Oxidative stress treatment for clinical trials in neurodegenerative diseases. J Alzheimers Dis. 2011; 24 Suppl 2: 111-126. doi: 10.3233/JAD-2011-110164 PMID: 21422516
35. Lin MT, Beal MF. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature. 2006; 443: 787-795. PMID: 17051205
36. Kim do Y, Davis LM, Sullivan PG, Maalouf M, Simeone TA, van Brederode J, et al. Ketone bodies are protective against oxidative stress in neocortical neurons. J Neurochem. 2007; 101: 1316-1326. PMID: 17403035
37. Kamsler A, Segal M. Hydrogen peroxide modulation of synaptic plasticity. J Neurosci. 2003; 23: 269-276. PMID: 12514224
38. Avshalumov MV, Rice ME. NMDA receptor activation mediates hydrogen peroxide-induced pathophysiology in rat hippocampal slices. J Neurophysiol. 2002; 87: 2896-2903. PMID: 12037193
39. Sakurai T, Yang B, Takata T, Yokono K. [Exogenous lactate sustains synaptic activity and neuronal viability, but fails to induce long-term potentiation (LTP)]. Nihon Ronen Igakkai Zasshi. 2000; 37: 962-965. PMID: 11201184
40. Maalouf M, Sullivan PG, Davis L, Kim DY, Rho JM. Ketones inhibit mitochondrial production of reactive oxygen species production following glutamate excitotoxicity by increasing NADH oxidation. Neuroscience. 2007; 145: 256-264. PMID: 17240074
41. Simao F, Matte A, Matte C, Soares FM, Wyse AT, Netto CA, et al. Resveratrol prevents oxidative stress and inhibition of Na(+)K(+)-ATPase activity induced by transient global cerebral ischemia in rats. J Nutr Biochem. 2011; 22: 921-928. doi: 10.1016/j.jnutbio.2010.07.013 PMID: 21208792
42. Jarrett SG, Milder JB, Liang LP, Patel M. The ketogenic diet increases mitochondrial glutathione levels. J Neurochem. 2008; 106: 1044-1051. doi: 10.1111/j.1471-4159.2008.05460.x PMID: 18466343
43. Milder J, Patel M. Modulation of oxidative stress and mitochondrial function by the ketogenic diet. Epilepsy Res. 2012; 100: 295-303. doi: 10.1016/j.eplepsyres.2011.09.021 PMID: 22078747
44. Ashcroft FM, Gribble FM. Correlating structure and function in ATP-sensitive K+ channels. Trends Neurosci. 1998; 21: 288-294. PMID: 9683320
45. Ben-Ari Y, Krnjevic K, Crepel V. Activators of ATP-sensitive K+ channels reduce anoxic depolarization in CA3 hippocampal neurons. Neuroscience. 1990; 37: 55-60. PMID: 1978742
46. Aguilar-Bryan L, Nichols CG, Wechsler SW, Clement JPt, Boyd AE 3rd, Gonzalez G, et al. Cloning of the beta cell high-affinity sulfonylurea receptor: a regulator of insulin secretion. Science. 1995; 268: 423-426. PMID: 7716547
47. Drose S, Hanley PJ, Brandt U. Ambivalent effects of diazoxide on mitochondrial ROS production at respiratory chain complexes I and III. Biochim Biophys Acta. 2009; 1790: 558-565. doi: 10.1016/j.bbagen.2009.01.011 PMID: 19364480
48. Liu B, Zhu X, Chen CL, Hu K, Swartz HM, Chen YR, et al. Opening of the mitoKATP channel and decoupling of mitochondrial complex II and III contribute to the suppression of myocardial reperfusion hyperoxygenation. Mol Cell Biochem. 2010; 337: 25-38. doi: 10.1007/s11010-009-0283-2 PMID: 19851835
49. Kleman AM, Yuan JY, Aja S, Ronnett GV, Landree LE. Physiological glucose is critical for optimized neuronal viability and AMPK responsiveness in vitro. J Neurosci Methods. 2008; 167: 292-301. PMID: 17936912
50. Huang CW, Huang CC, Cheng JT, Tsai JJ, Wu SN. Glucose and hippocampal neuronal excitability: role of ATP-sensitive potassium channels. J Neurosci Res. 2007; 85: 1468-1477. PMID: 17410601
51. Lund TM, Ploug KB, Iversen A, Jensen AA, Jansen-Olesen I. The metabolic impact of beta-hydroxybutyrate on neurotransmission: Reduced glycolysis mediates changes in calcium responses and K receptor sensitivity. J Neurochem. 2014; doi: 10.1111/jnc.12975
52. Lund TM, Risa O, Sonnewald U, Schousboe A, Waagepetersen HS. Availability of neurotransmitter glutamate is diminished when beta-hydroxybutyrate replaces glucose in cultured neurons. J Neurochem. 2009; 110: 80-91. doi: 10.1111/j.1471-4159.2009.06115.x PMID: 19457063
53. de Weille JR, Schmid-Antomarchi H, Fosset M, Lazdunski M. Regulation of ATP-sensitive K+ channels in insulinoma cells: activation by somatostatin and protein kinase C and the role of cAMP. Proc Natl Acad Sci U S A. 1989; 86: 2971-2975. PMID: 2565041
54. Won YJ, Lu VB, Puhl HL 3rd, Ikeda SR. beta-Hydroxybutyrate modulates N-type calcium channels in rat sympathetic neurons by acting as an agonist for the G-protein-coupled receptor FFA3. J Neurosci. 2013; 33: 19314-19325. doi: 10.1523/JNEUROSCI.3102-13.2013 PMID: 24305827
55. Heurteaux C, Lauritzen I, Widmann C, Lazdunski M. Essential role of adenosine, adenosine A1 receptors, and ATP-sensitive K+ channels in cerebral ischemic preconditioning. Proc Natl Acad Sci U S A. 1995; 92: 4666-4670. PMID: 7753861
56. Wang L, Zhu QL, Wang GZ, Deng TZ, Chen R, Liu MH, et al. The protective roles of mitochondrial ATP-sensitive potassium channels during hypoxia-ischemia-reperfusion in brain. Neurosci Lett. 2011; 491: 63-67. doi: 10.1016/j.neulet.2010.12.065 PMID: 21215294
57. Betourne A, Bertholet AM, Labroue E, Halley H, Sun HS, Lorsignol A, et al. Involvement of hippocampal CA3 K(ATP) channels in contextual memory. Neuropharmacology. 2009; 56: 615-625. doi: 10.1016/j.neuropharm.2008.11.001 PMID: 19059420