Acetate supplementation increases brain phosphocreatine and reduces AMP levels with no effect on mitochondrial biogenesis

Neurochemistry International

Volumn 62, Issue 3, 2013, Pages 296-305

  Bhatt, Dhaval P ^a   Houdek, Heidi M ^a   Watt, John A ^b   Rosenberger, Thad A ^a  

^a UNIVERSITY OF NORTH DAKOTA   (United States)

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

Author keywords

Acetate supplementation; Brain; Energy; Glycogen; Mitochondria; Nucleotides; Phosphocreatine

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; CARDIOLIPIN; CREATINE PHOSPHATE; GLYCOGEN; GUANOSINE TRIPHOSPHATE; NICOTINAMIDE ADENINE DINUCLEOTIDE; TRIACETIN;

ANIMAL EXPERIMENT; ARTICLE; BIOGENESIS; BRAIN; BRAIN NERVE CELL; CHEMICAL ANALYSIS; CONTROLLED STUDY; CYTOPLASM; ENERGY METABOLISM; GLUCOSE UTILIZATION; GLYCOGEN SYNTHESIS; GLYCOGENOLYSIS; HIPPOCAMPAL CA3 REGION; LIPID COMPOSITION; LONG TERM CARE; MALE; MICROWAVE IRRADIATION; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; SINGLE DRUG DOSE; TREATMENT DURATION;

ACETATES; ADENOSINE MONOPHOSPHATE; ANIMALS; BRAIN; GLYCOGEN; MICE; MITOCHONDRIA; PHOSPHOCREATINE; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 84873373580     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2013.01.004     Document Type: Article

References (72)

1. P. Arun, P.S. Ariyannur, J.R. Moffett, G. Xing, K. Hamilton, N.E. Grunberg, J.A. Ives, and A.M. Namboodiri Metabolic acetate therapy for the treatment of traumatic brain injury J. Neurotrauma 27 2010 293 298
2. M. Balestrino, M. Lensman, M. Parodi, L. Perasso, R. Rebaudo, R. Melani, S. Polenov, and A. Cupello Role of creatine and phosphocreatine in neuronal protection from anoxic and ischemic damage Amino Acids 23 2002 221 229
3. M. Balestrino, R. Rebaudo, and G. Lunardi Exogenous creatine delays anoxic depolarization and protects from hypoxic damage: dose-effect relationship Brain Res. 816 1999 124 130 (Pubitemid 29225430)
4. K.J. Bough, J. Wetherington, B. Hassel, J.F. Pare, J.W. Gawryluk, J.G. Greene, R. Shaw, Y. Smith, J.D. Geiger, and R.J. Dingledine Mitochondrial biogenesis in the anticonvulsant mechanism of the ketogenic diet Ann. Neurol. 60 2006 223 235 (Pubitemid 44182397)
5. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
6. A. Brand, C. Richter-Landsberg, and D. Leibfritz Metabolism of acetate in rat brain neurons, astrocytes and cocultures: metabolic interactions between neurons and glia cells, monitored by NMR spectroscopy Cell Mol. Biol. 43 1997 645 657
7. G.J. Brewer, and T.W. Wallimann Protective effect of the energy precursor creatine against toxicity of glutamate and beta-amyloid in rat hippocampal neurons J. Neurochem. 74 2000 1968 1978 (Pubitemid 30217652)
8. C.A. Brissette, H.M. Houdek, A.M. Floden, and T.A. Rosenberger Acetate supplementation reduces microglia activation and brain interleukin-1beta levels in a rat model of Lyme neuroborreliosis J. Neuroinflamm. 9 2012 249
9. A.M. Brown Brain glycogen re-awakened J. Neurochem. 89 2004 537 552 (Pubitemid 38534140)
10. I.Y. Choi, and R. Gruetter In vivo 13C NMR assessment of brain glycogen concentration and turnover in the awake rat Neurochem. Int. 43 2003 317 322 (Pubitemid 36561284)
11. J.E. Cremer Incorporation of label from D- -hydroxy(14 C)butyrate and (3-14 C)acetoacetate into amino acids in rat brain in vivo Biochem. J. 122 1971 135 138
12. N.F. Cruz, and G.A. Dienel High glycogen levels in brains of rats with minimal environmental stimuli: implications for metabolic contributions of working astrocytes J. Cereb. Blood Flow Metab. 22 2002 1476 1489 (Pubitemid 35424932)
13. R.A. Cunha Neuroprotection by adenosine in the brain: from A(1) receptor activation to A (2A) receptor blockade Purinergic Signal. 1 2005 111 134 (Pubitemid 40466898)
14. G. Daum Lipids of mitochondria Biochim. Biophys. Acta 822 1985 1 42 (Pubitemid 15042024)
15. D.K. Deelchand, A.A. Shestov, D.M. Koski, K. Ugurbil, and P.G. Henry Acetate transport and utilization in the rat brain J. Neurochem. 109 Suppl 1 2009 46 54
16. S.M. Delaney, and J.D. Geiger Brain regional levels of adenosine and adenosine nucleotides in rats killed by high-energy focused microwave irradiation J. Neurosci. Methods 64 1996 151 156 (Pubitemid 26083301)
17. F. Di Virgilio, S. Ceruti, P. Bramanti, and M.P. Abbracchio Purinergic signalling in inflammation of the central nervous system Trends Neurosci. 32 2009 79 87
18. M. Dinuzzo, S. Mangia, B. Maraviglia, and F. Giove The role of astrocytic glycogen in supporting the energetics of neuronal activity Neurochem. Res. 37 2012 2432 2438
19. M. Dunnett, R.C. Harris, and C.E. Orme Reverse-phase ion-pairing high-performance liquid chromatography of phosphocreatine, creatine and creatinine in equine muscle Scand. J. Clin. Lab. Invest. 51 1991 137 141
20. M. Erecinska, and I.A. Silver ATP and brain function J. Cereb. Blood Flow Metab. 9 1989 2 19 (Pubitemid 19053430)
21. R.C. Gupta, and W.D. Dettbarn Prevention of kainic acid seizures-induced changes in levels of nitric oxide and high-energy phosphates by 7-nitroindazole in rat brain regions Brain Res. 981 2003 184 192 (Pubitemid 37281234)
22. W.C. Hallows, S. Lee, and J.M. Denu Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases Proc. Natl. Acad. Sci. USA 103 2006 10230 10235 (Pubitemid 44051149)
23. D.F. Hammer, D.V. Unverferth, R.E. Kelley, P.A. Harvan, and R.A. Altschuld Extraction and measurement of myocardial nucleotides, nucleosides, and purine bases by high-performance liquid chromatography Anal. Biochem. 169 1988 300 305 (Pubitemid 18081403)
24. R.I. Herzog, O. Chan, S. Yu, J. Dziura, E.C. McNay, and R.S. Sherwin Effect of acute and recurrent hypoglycemia on changes in brain glycogen concentration Endocrinology 149 2008 1499 1504 (Pubitemid 351468331)
25. F.L. Hoch Cardiolipins and biomembrane function Biochim. Biophys. Acta 1113 1992 71 133
26. R.H. Houtkooper, and F.M. Vaz Cardiolipin, the heart of mitochondrial metabolism Cell. Mol. Life Sci. 65 2008 2493 2506
27. P. Klivenyi, R.J. Ferrante, R.T. Matthews, M.B. Bogdanov, A.M. Klein, O.A. Andreassen, G. Mueller, M. Wermer, R. Kaddurah-Daouk, and M.F. Beal Neuroprotective effects of creatine in a transgenic animal model of amyotrophic lateral sclerosis Nat. Med. 5 1999 347 350 (Pubitemid 29124375)
28. J. Kong, P.N. Shepel, C.P. Holden, M. Mackiewicz, A.I. Pack, and J.D. Geiger Brain glycogen decreases with increased periods of wakefulness: implications for homeostatic drive to sleep J. Neurosci. 22 2002 5581 5587 (Pubitemid 35386479)
29. J.W. Lawson, and R.L. Veech Effects of pH and free Mg2+ on the Keq of the creatine kinase reaction and other phosphate hydrolyses and phosphate transfer reactions J. Biol. Chem. 254 1979 6528 6537 (Pubitemid 10225613)
30. E.K. Long, T.A. Rosenberger, and M.J. Picklo Sr. Ethanol withdrawal increases glutathione adducts of 4-hydroxy-2-hexenal but not 4-hydroxyl-2-nonenal in the rat cerebral cortex Free Radic. Biol. Med. 48 2010 384 390
31. O.H. Lowry, J.V. Passonneau, F.X. Hasselberger, and D.W. Schulz Effect of ischemia on known substrates and cofactors of the glycolytic pathway in brain J. Biol. Chem. 239 1964 18 30
32. M. Maalouf, J.M. Rho, and M.P. Mattson The neuroprotective properties of calorie restriction, the ketogenic diet, and ketone bodies Brain Res. Rev. 59 2009 293 315
33. R. Mathew, P. Arun, C.N. Madhavarao, J.R. Moffett, and M.A. Namboodiri Progress toward acetate supplementation therapy for Canavan disease: glyceryl triacetate administration increases acetate, but not N-acetylaspartate, levels in brain J. Pharmacol. Exp. Ther. 315 2005 297 303 (Pubitemid 41380524)
34. R.T. Matthews, R.J. Ferrante, P. Klivenyi, L. Yang, A.M. Klein, G. Mueller, R. Kaddurah-Daouk, and M.F. Beal Creatine and cyclocreatine attenuate MPTP neurotoxicity Exp. Neurol. 157 1999 142 149 (Pubitemid 29226877)
35. R.T. Matthews, L. Yang, B.G. Jenkins, R.J. Ferrante, B.R. Rosen, R. Kaddurah-Daouk, and M.F. Beal Neuroprotective effects of creatine and cyclocreatine in animal models of Huntington's disease J. Neurosci. 18 1998 156 163 (Pubitemid 28046777)
36. T.M. Melo, A. Nehlig, and U. Sonnewald Neuronal-glial interactions in rats fed a ketogenic diet Neurochem. Int. 48 2006 498 507
37. R.A. Menzies, and P.H. Gold The turnover of mitochondria in a variety of tissues of young adult and aged rats J. Biol. Chem. 246 1971 2425 2429
38. R.A. Meyer, H.L. Sweeney, and M.J. Kushmerick A simple analysis of the "phosphocreatine shuttle" Am. J. Physiol. 246 1984 C365 377
39. M.C. Minchin, and P.M. Beart Compartmentation of amino acid metabolism in the rat dorsal root ganglion; a metabolic and autoradiographic study Brain Res. 83 1975 437 449
40. V.A. Morais, and B. De Strooper Mitochondria dysfunction and neurodegenerative disorders: cause or consequence J. Alzheimers Dis. 20 Suppl 2 2010 S255 263
41. F.D. Morgenthaler, B.R. Lanz, J.M. Petit, H. Frenkel, P.J. Magistretti, and R. Gruetter Alteration of brain glycogen turnover in the conscious rat after 5h of prolonged wakefulness Neurochem. Int. 55 2009 45 51
42. I. Moschen, A. Broer, S. Galic, F. Lang, and S. Broer Significance of short chain fatty acid transport by members of the monocarboxylate transporter family (MCT) Neurochem. Res. 37 2012 2562 2568
43. S.R. Nelson Effects of microwave irradiation on enzymes and metabolites in mouse brain Radiat. Res. 55 1973 153 159
44. E. Nisoli, and M.O. Carruba Nitric oxide and mitochondrial biogenesis J. Cell. Sci. 119 2006 2855 2862 (Pubitemid 44177863)
45. K. Norberg, B. Quistorff, and B.K. Siesjo Effects of hypoxia of 10-45 seconds duration on energy metabolism in the cerebral cortex of unanesthetized and anesthetized rats Acta Physiol. Scand. 95 1975 301 310
46. A. Novelli, J.A. Reilly, P.G. Lysko, and R.C. Henneberry Glutamate becomes neurotoxic via the N-methyl-D-aspartate receptor when intracellular energy levels are reduced Brain Res. 451 1988 205 212
47. K. Nylen, J.L. Velazquez, V. Sayed, K.M. Gibson, W.M. Burnham, and O.C. Snead 3rd The effects of a ketogenic diet on ATP concentrations and the number of hippocampal mitochondria in Aldh5a1(-/-) mice Biochim. Biophys. Acta 1790 2009 208 212
48. J.W. Pettegrew, K. Panchalingam, W.E. Klunk, R.J. McClure, and L.R. Muenz Alterations of cerebral metabolism in probable Alzheimer's disease: a preliminary study Neurobiol. Aging 15 1994 117 132 (Pubitemid 24075020)
49. K. Pierre, and L. Pellerin Monocarboxylate transporters in the central nervous system: distribution, regulation and function J. Neurochem. 94 2005 1 14 (Pubitemid 40911387)
50. U. Ponten, R.A. Ratcheson, L.G. Salford, and B.K. Siesjo Optimal freezing conditions for cerebral metabolites in rats J. Neurochem. 21 1973 1127 1138
51. N.S. Radin Extraction of tissue lipids with a solvent of low toxicity Methods Enzymol. 72 1981 5 7
52. C. Rae, A.D. Fekete, M.A. Kashem, F.A. Nasrallah, and S. Broer Metabolism, compartmentation, transport and production of acetate in the cortical brain tissue slice Neurochem. Res. 37 2012 2541 2553
53. C.J. Reisenauer, D.P. Bhatt, D.J. Mitteness, E.R. Slanczka, H.M. Gienger, J.A. Watt, and T.A. Rosenberger Acetate supplementation attenuates lipopolysaccharide-induced neuroinflammation J. Neurochem. 117 2011 264 274
54. J.A. Ribeiro What can adenosine neuromodulation do for neuroprotection? Curr. Drug Targets CNS Neurol. Disord. 4 2005 325 329 (Pubitemid 41086753)
55. J.T. Rodgers, C. Lerin, W. Haas, S.P. Gygi, B.M. Spiegelman, and P. Puigserver Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1 Nature 434 2005 113 118 (Pubitemid 40349395)
56. G. Rouser, A.N. Siakotos, and S. Fleischer Quantitative analysis of phospholipids by thin-layer chromatography and phosphorus analysis of spots Lipids 1 1966 85 86
57. M. Schlame Assays of cardiolipin levels Methods Cell Biol. 80 2007 223 240
58. M. Soliman, and T.A. Rosenberger Acetate supplementation increases brain histone acetylation and inhibits histone deacetylase activity and expression Mol. Cell. Biochem. 352 2011 173 180
59. M.L. Soliman, C.K. Combs, and T.A. Rosenberger Modulation of inflammatory cytokines and mitogen-activated protein kinases by acetate in primary astrocytes J. Neuroimmune Pharmacol. 2012 http://dx.doi.org/10.1007/s11481-012- 9426-4
60. M.L. Soliman, K.L. Puig, C.K. Combs, and T.A. Rosenberger Acetate reduces microglia inflammatory signaling in vitro J. Neurochem. 123 2012 555 567
61. M.L. Soliman, M.D. Smith, H.M. Houdek, and T.A. Rosenberger Acetate supplementation modulates brain histone acetylation and decreases interleukin-1beta expression in a rat model of neuroinflammation J. Neuroinflamm. 9 2012 51
62. S. Srivastava, Y. Kashiwaya, X. Chen, J.D. Geiger, R. Pawlosky, and R.L. Veech Microwave irradiation decreases ATP, increases free [Mg(2+) ], and alters in vivo intracellular reactions in rat brain J. Neurochem. 123 2012 668 675
63. M. Tachikawa, M. Fukaya, T. Terasaki, S. Ohtsuki, and M. Watanabe Distinct cellular expressions of creatine synthetic enzyme GAMT and creatine kinases uCK-Mi and CK-B suggest a novel neuron-glial relationship for brain energy homeostasis Eur. J. Neurosci. 20 2004 144 160 (Pubitemid 38932135)
64. R.L. Veech, R.L. Harris, D. Veloso, and E.H. Veech Freeze-blowing: a new technique for the study of brain in vivo J. Neurochem. 20 1973 183 188
65. D.C. Wallace, W. Fan, and V. Procaccio Mitochondrial energetics and therapeutics Annu. Rev. Pathol. 5 2010 297 348
66. T. Wallimann, M. Wyss, D. Brdiczka, K. Nicolay, and H.M. Eppenberger Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine circuit' for cellular energy homeostasis Biochem. J. 281 Pt 1 1992 21 40
67. R.A. Waniewski, and D.L. Martin Preferential utilization of acetate by astrocytes is attributable to transport J. Neurosci. 18 1998 5225 5233 (Pubitemid 28311939)
68. H. White, and B. Venkatesh Clinical review: ketones and brain injury Crit. Care 15 2011 219
69. F. Wilhelm, and J. Hirrlinger Multifunctional roles of NAD(+) and NADH in astrocytes Neurochem. Res. 37 2012 2317 2325
70. M.T. Wyss, P.J. Magistretti, A. Buck, and B. Weber Labeled acetate as a marker of astrocytic metabolism J. Cereb. Blood Flow Metab. 31 2011 1668 1674
71. M. Yudkoff, Y. Daikhin, I. Nissim, O. Horyn, A. Lazarow, B. Luhovyy, S. Wehrli, and I. Nissim Response of brain amino acid metabolism to ketosis Neurochem. Int. 47 2005 119 128 (Pubitemid 40848700)
72. C.R. Zamzow, R. Bose, and F.E. Parkinson The effect of acidosis on adenosine release from cultured rat forebrain neurons Brain Res. Mol. Brain Res. 1082 2006 23 31