D-β-hydroxybutyrate is neuroprotective against hypoxia in serum-free hippocampal primary cultures

Journal of Neuroscience Research

Volumn 80, Issue 4, 2005, Pages 501-509

  Masuda, R ^a,b   Monahan, J W ^a,c   Kashiwaya, Yoshihiro ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c DESALES UNIVERSITY   (United States)

Author keywords

Apoptosis; D hydroxybutyrate; Hippocampal neurons; Hypoxia; Ketone body; Necrosis

Indexed keywords

3 HYDROXYBUTYRIC ACID; CASPASE 3; CYTOCHROME C; KETONE BODY; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROPIDIUM IODIDE; TRYPAN BLUE;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; FIBRINOLYTIC THERAPY; HIPPOCAMPUS; HYPOXIA; KETOACIDOSIS; MEMBRANE POTENTIAL; NERVE CELL; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT;

3-HYDROXYBUTYRIC ACID; ANIMALS; CASPASE 3; CASPASES; CELL HYPOXIA; CELL SURVIVAL; CELLS, CULTURED; CULTURE MEDIA, SERUM-FREE; CYTOCHROMES C; EMBRYO; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MEMBRANE POTENTIALS; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; NEURONS; NEUROPROTECTIVE AGENTS; POLY(ADP-RIBOSE) POLYMERASES; PROPIDIUM; RATS; RATS, WISTAR; STATISTICS, NONPARAMETRIC; TIME FACTORS; TRYPAN BLUE;

EID: 20344408563     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20464     Document Type: Article

References (64)

1. Alam HB, Austin B, Koustova E, Rhee P. 2001. Resuscitation-induced pulmonary apoptosis and intracellular adhesion molecule-1 expression in rats are attenuated by the use of Ketone Ringer's solution. J Am Coll Surg 193:255-263.
2. Almeida A, Allen KL, Bates TE, Clark JB. 1995. Effect of reperfusion following cerebral ischaemia on the activity of the mitochondrial respiratory chain in the gerbil brain. J Neurochem 65:1698-1703.
3. Almeida A, Bolanos JP. 2001. A transient inhibition of mitochondrial ATP synthesis by nitric oxide synthase activation triggered apoptosis in primary cortical neurons. J Neurochem 77:676-690.
4. Almeida A, Delgado-Esteban M, Bolanos JP, Medina JM. 2002. Oxygen and glucose deprivation induces mitochondrial dysfunction and oxidative stress in neurones but not in astrocytes in primary culture. J Neurochem 81:207-217.
5. Althaus FR, Lawrence SD, Sattler GL, Pitot HC. 1982. ADP- ribosyltransferase activity in cultured hepatocytes. Interactions with DNA repair. J Biol Chem 257:5528-5535.
6. American Heart Association. 2004. Heart Disease and Stroke Statistics-2004 Update. American Heart Association.
7. Astrup J, Siesjo BK, Symon L. 1981. Thresholds in cerebral ischemia-the ischemic penumbra. Stroke 12:723-725.
8. Benchoua A, Guegan C, Couriaud C, Hosseini H, Sampaio N, Morin D, Onteniente B. 2001. Specific caspase pathways are activated in the two stages of cerebral infarction. J Neurosci 21:7127-7134.
9. Brewer GJ, Torricelli JR, Evege EK, Price PJ. 1993. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35:567-576.
10. Brott TG, Haley EC Jr, Levy DE, Barsan W, Broderick J, Sheppard GL, Spilker J, Kongable GL, Massey S, Reed R. 1992. Urgent therapy for stroke. Part I. Pilot study of tissue plasminogen activator administered within 90 minutes. Stroke 23:632-640.
11. Cahill GF Jr, Owen OE. 1968. Starvation and survival. Trans Am Clin Climatol Assoc 79:13-20.
12. Chance B, Sies H, Boveris A. 1979. Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527-605.
13. Chen J, Nagayama T, Jin K, Stetler RA, Zhu RL, Graham SH, Simon RP. 1998. Induction of caspase-3-like protease may mediate delayed neuronal death in the hippocampus after transient cerebral ischemia. J Neurosci 18:4914-4928.
14. Choi DW. 1992. Excitotoxic cell death. J Neurobiol 23:1261-1276.
15. Choi DW. 1996. Ischemia-induced neuronal apoptosis. Curr Opin Neurobiol 6:667-672.
16. Dirnagl U, Iadecola C, Moskowitz MA. 1999. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22:391-397.
17. Fujimura M, Morita-Fujimura Y, Murakami K, Kawase M, Chan PH. 1998. Cytosolic redistribution of cytochrome c after transient focal cerebral ischemia in rats. J Cereb Blood Flow Metab 18:1239-1247.
18. Garcia JH, Liu KF, Ho KL. 1995. Neuronal necrosis after middle cerebral artery occlusion in Wistar rats progresses at different time intervals in the caudoputamen and the cortex. Stroke 26:636-642.
19. Go KG, Prenen GH, Korf J. 1988. Protective effect of fasting upon cerebral hypoxic-ischemic injury. Metab Brain Dis 3:257-263.
20. Greene AE, Todorova MT, McGowan R, Seyfried TN. 2001. Caloric restriction inhibits seizure susceptibility in epileptic EL mice by reducing blood glucose. Epilepsia 42:1371-1378.
21. Haley EC Jr, Levy DE, Brott TG, Sheppard GL, Wong MC, Kongable GL, Torner JC, Marier JR. 1992. Urgent therapy for stroke. Part II. Pilot study of tissue plasminogen activator administered 91-180 minutes from onset. Stroke 23:641-645.
22. Heiss WD, Graf R. 1994. The ischemic penumbra. Curr Opin Neurol 7:11-19.
23. Huber G, Matus A. 1984. Differences in the cellular distributions of two microtubule-associated proteins, MAP1 and MAP2, in rat brain. J Neurosci 4:151-160.
24. Iijima T, Mishima T, Akagawa K, Iwao Y. 2003. Mitochondrial hyperpolarization after transient oxygen-glucose deprivation and subsequent apoptosis in cultured rat hippocampal neurons. Brain Res 993:140-145.
25. Izumi Y, Ishii K, Katsuki H, Benz AM, Zorumski CF. 1998. beta-Hydroxybutyrate fuels synaptic function during development. Histological and physiological evidence in rat hippocampal slices. J Clin Invest 101:1121-1132.
26. Kashiwaya Y, Takeshima T, Mori N, Nakashima K, Clarke K, Veech RL. 2000. D-beta-Hydroxybutyrate protects neurons in models of Alzheimer's and Parkinson's disease. Proc Natl Acad Sci USA 97:5440-5444.
27. Katsura K, Kristian T, Siesjo BK. 1994. Energy metabolism, ion homeostasis, and cell damage in the brain. Biochem Soc Trans 22:991-996.
28. Kirsch JR, D'Alecy LG, Mongroo PB. 1980. Butanediol induced ketosis increases tolerance to hypoxia in the mouse. Stroke 11:506-513.
29. Koustova E, Rhee P, Hancock T, Chen H, Inocencio R, Jaskille A, Hanes W, Valen CR, Alam HB. 2003. Ketone and pyruvate Ringer's solutions decrease pulmonary apoptosis in a rat model of severe hemorrhagic shock and resuscitation. Surgery 134:267-274.
30. Kroemer G, Dallaporta B, Resche-Rigon M. 1998. The mitochondrial death/life regulator in apoptosis and necrosis. Annu Rev Physiol 60:619-642.
31. Li P, Nijhawan D, Budihardjo I, Srimvasula SM, Ahmad M, Alnemri ES, Wang X. 1997. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479-489.
32. Linnik MD, Miller JA, Sprinkle-Cavallo J, Mason PJ, Thompson FY, Montgomery LR, Schroeder KK. 1995. Apoptotic DNA fragmentation in the rat cerebral cortex induced by permanent middle cerebral artery occlusion. Brain Res Mol Brain Res 32:116-124.
33. Linnik MD, Zobrist RH, Hatfield MD. 1993. Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke 24:2002-2008.
34. MacManus JP, Buchan AM, Hill IE, Rasquinha I, Preston E. 1993. Global ischemia can cause DNA fragmentation indicative of apoptosis in rat brain. Neurosci Lett 164:89-92.
35. Malagelada C, Xifro X, Badiola N, Sabria J, Rodriguez-Alvarez J. 2004. Histamine H2-receptor antagonist ranitidine protects against neural death induced by oxygen-glucose deprivation. Stroke 35:2396-2401.
36. Mao Y, Yang GY, Zhou LF, Stern JD, Betz AL. 1999. Focal cerebral ischemia in the mouse: description of a model and effects of permanent and temporary occlusion. Brain Res Mol Brain Res 63:366-370.
37. Marler JR, Tilley BC, Lu M, Brott TG, Lyden PC, Grotta JC, Broderick JP, Levine SR, Frankel MP, Horowitz SH, Haley EC Jr, Lewandowski CA, Kwiatkowski TP. 2000. Early stroke treatment associated with better outcome: the NINDS rt-PA stroke study. Neurology 55:1649-1655.
38. Massieu L, Races ML, Montiel T, Hernandez-Fonseca K. 2003. Acetoacetate protects hippocampal neurons against glutamate-mediated neuronal damage during glycolysis inhibition. Neuroscience 120:365-378.
39. Mattson MP. 2000. Apoptosis in neurodegenerative disorders. Nat Rev Mol Cell Biol 1:120-129.
40. Matyja E, Kida E. 1992. Hippocampal damage in vitro after different periods of oxygen deprivation. Neuropatol Pol 30:231-243.
41. Moore TJ, Lione AP, Sugden MC, Regen DM. 1976. Beta-hydroxybutyrate transport in rat brain: developmental and dietary modulations. Am J Physiol 230:619-630.
42. Namura S, Zhu J, Fink K, Endres M, Srinivasan A, Tomaselli KJ, Yuan J, Moskowitz MA. 1998. Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia. J Neurosci 18:3659-3668.
43. Otomo E. 2003. Effect of a novel free radical scavenger, edaravone (MCI-186), on acute brain infarction. Randomized, placebo-controlled, double-blind study at multicenters. Cerebrovasc Dis 15:222-229.
44. Owen OE, Morgan AP, Kemp HG, Sullivan JM, Herrera MG, Cahill GF Jr. 1967. Brain metabolism during fasting. J Clin Invest 46:1589-1595.
45. Pan JW, Bebin EM, Chu WJ, Hetherington HP. 1999. Ketosis and epilepsy: 31P spectroscopic imaging at 4.1 T. Epilepsia 40:703-707.
46. Poot M, Zhang YZ, Kramer JA, Wells KS, Jones LJ, Hanzel DK, Lugade AG, Singer VL, Haugland RP. 1996. Analysis of mitochondrial morphology and function with novel fixable fluorescent stains. J Histochem Cytochem 44:1363-1372.
47. Rehncrona S, Mela L, Siesjo BK. 1979. Recovery of brain mitochondrial function in the rat after complete and incomplete cerebral ischemia. Stroke 10:437-446.
48. Sato K, Kashiwaya Y, Keon CA, Tsuchiya N, King MT, Radda GK, Chance B, Clarke K, Veech RL. 1995. Insulin, ketone bodies, and mitochondrial energy transduction. FASEB J 9:651-658.
49. Shiino A, Matsuda M, Handa J, Chance B. 1998. Poor recovery of mitochondrial redox state in CA1 after transient forebrain ischemia in gerbils. Stroke 29:2421-2424.
50. Sims NR, Anderson MF. 2002. Mitochondrial contributions to tissue damage in stroke. Neurochem Int 40:511-526.
51. Sims NR, Pulsinelli WA. 1987. Altered mitochondrial respiration in selectively vulnerable brain subregions following transient forebrain ischemia in the rat. J Neurochem 49:1367-1374.
52. Sugano T, Oshino N, Chance B. 1974. Mitochondrial functions under hypoxic conditions. The steady states of cytochrome c reduction and of energy metabolism. Biochim Biophys Acta 347:340-358.
53. Suzuki M, Suzuki M, Sato K, Dohi S, Sato T, Matsuura A, Hiraide A. 2001. Effect of beta-hydroxybutyrate, a cerebral function improving agent, on cerebral hypoxia, anoxia and ischemia in mice and rats. Jpn J Pharmacol 87:143-150.
54. Swmk TD, Vining EP, Freeman JM. 1997. The ketogenic diet: 1997. Adv Pediatr 44:297-329.
55. Tewari M, Quan LT, O'Rourke K, Desnoyers S, Zeng Z, Beidler DR, Poirier GG, Salvesen GS, Dixit VM. 1995. Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81:801-809.
56. Tieu K, Perier C, Caspersen C, Teismann P, Wu DC, Yan SD, Naini A, Vila M, Jackson-Lewis V, Ramasamy R, Przedborski S. 2003. D-beta-Hydroxybutyrate rescues mitochondrial respiration and mitigates features of Parkinson disease. J Clin Invest 112:892-901.
57. Tomatsuri N, Yoshida N, Takagi T, Katada K, Isozaki Y, Imamoto E, Uchiyama K, Kokura S, Ichikawa H, Naito Y, Okanoue T, Yoshikawa T. 2004. Edaravone, a newly developed radical scavenger, protects against ischemia-reperfusion injury of the small intestine in rats. Int J Mol Med 13:105-109.
58. Tombaugh GC, Sapolsky RM. 1990. Mechanistic distinctions between excitotoxic and acidotic hippocampal damage in an in vitro model of ischemia. J Cereb Blood Flow Metab 10:527-535.
59. Veech RL. 2004. 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 70:309-319.
60. Veech RL, Chance B, Kashiwaya Y, Lardy HA, Cahill GF Jr. 2001. Ketone bodies, potential therapeutic uses. IUBMB Life 51:241-247.
61. Veech RL, Kashiwaya Y, King MT. 1995. The resting membrane potential of cells are measures of electrical work, not of ionic currents. Integr Physiol Behav Sci 30:283-307.
62. Xiao AY, Wei L, Xia S, Rothman S, Yu SP. 2002. Ionic mechanism of ouabain-induced concurrent apoptosis and necrosis in individual cultured cortical neurons. J Neurosci 22:1350-1362.
63. Zivin JA, Fisher M, DeGirolami U, Hemenway CC, Stashak JA. 1985. Tissue plasminogen activator reduces neurological damage after cerebral embolism. Science 230:1289-1292.
64. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. 1997. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90:405-413.