Metabolism, compartmentation, transport and production of acetate in the cortical brain tissue slice

Neurochemical Research

Volumn 37, Issue 11, 2012, Pages 2541-2553

  Rae, Caroline ^a   Fekete, Aurélie D ^a   Kashem, Mohammed A ^a   Nasrallah, Fatima A ^a   Bröer, Stefan ^b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

13C NMR spectroscopy; Acetate; Neuron glia interactions

Indexed keywords

ACETIC ACID; ACETYL COENZYME A; ACETYL COENZYME A HYDROLASE; ACETYL COENZYME A SYNTHETASE; CARBON 13; CARRIER PROTEIN; CITRIC ACID; GLUCOSE; LACTIC ACID; MONOCARBOXYLATE TRANSPORTER 1; MONOCARBOXYLATE TRANSPORTER 2; MONOCARBOXYLATE TRANSPORTER 4; NICOTINAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE; PYRUVIC ACID; SMCT PROTEIN; UNCLASSIFIED DRUG;

ACETIC ACID METABOLISM; ACETYLATION; ACTIVE TRANSPORT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN LEVEL; BRAIN METABOLISM; BRAIN NERVE CELL; BRAIN SLICE; CARBON NUCLEAR MAGNETIC RESONANCE; CELL COMPARTMENTALIZATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FATTY ACID METABOLISM; FATTY ACID SYNTHESIS; FATTY ACID TRANSPORT; GLIA CELL; GUINEA PIG; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ASTROCYTES; BRAIN; GLUTAMIC ACID; HOMEOSTASIS; HUMANS; NEURONS;

EID: 84871415082     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-012-0847-5     Document Type: Article

References (77)

1. Gonzalez SV, Nguyen NHT, Rise F, Hassel B (2005) Brain metabolism of exogenous pyruvate. J Neurochem 95:284-293
2. Cox DWG, Bachelard HS (1988) Partial attenuation of dentate granule cell evoked activity by the alternative substrates, lactate and pyruvate: Evidence for a postsynaptic action. Exp Brain Res 69:368-372
3. Tarasenko AS, Linetska MV, Storchak LG, Himmelreich NH (2006) Effectiveness of extracellular lactate/pyruvate for sustaining synaptic vesicle proton gradient generation and vesicular accumulation of GABA. J Neurochem 99:787-796
4. Berl S, Frigyesi TL (1969) Turnover of glutamate glutamine aspartate and GABA labeled with 1-14C acetate in caudate nucleus thalamus and motor cortex (cat). Brain Res 12:444-455
5. Starai VJ, Escalante-Semerena JC (2004) Acetyl-coenzyme A synthetase (AMP forming). Cell Mol Life Sci 61:2020-2030
6. Dadamo AF, Yatsu FM (1966) Acetate metabolism in nervous system. N-acetyl-L-aspartic acid and biosynthesis of brain lipids. J Neurochem 13:961
7. Soliman ML, Rosenberger TA (2011) Acetate supplementation increases brain histone acetylation and inhibits histone deacetylase activity and expression. Mol Cell Biochem 352:173-180
8. Carroll PT (1997) Evidence to suggest that extracellular acetate is accumulated by rat hippocampal cholinergic nerve terminals for acetylcholine formation and release. Brain Res 753:47-55
9. Ariyannur PS, Moffett JR, Madhavarao CN, Arun P, Vishnu N, Jacobowitz DM, Hallows WC, Denu JM, Namboodiri AMA (2010) Nuclear-cytoplasmic localization of acetyl coenzyme A synthetase-1 in the rat brain. J Comp Neurol 518:2952-2977
10. Tucek S (1967) Subcellular distribution of acetyl-CoA synthetase, ATP citrate lyase, citrate synthase, choline acetyltransferase, fumarate hydratase and lactate dehydrogenase in mammalian brain tissue. J Neurochem 14:531-545
11. Hirschey MD, Shimazu T, Capra JA, Pollard KS, Verdin E (2011) SIRT1 and SIRT3 deacetylate homologous substrates: AceCS1,2 and HMGCS1,2. Aging-US 3:635-642
12. Ramadori G, Lee CE, Bookout AL, Lee S, Williams KW, Anderson J, Elmquist JK, Coppari R (2008) Brain SIRT1: Anatomical distribution and regulation by energy availability. J Neurosci 28:9989-9996
13. Brand A, Richter-Landsberg C, Leibfritz D (1997) Metabolism of acetate in rat brain neurons, astrocytes and cocultures: Metabolic interactions between neurons and glia cells, monitored by NMR spectroscopy. Cell Mol Biol 43:645-657
14. Chapa F, Cruz F, Garcia-Martin ML, Garcia-Espinosa MA, Cerdan S (1999) Metabolism of (1-13C) glucose and (2-13C, 2-2H3) acetate in the neuronal and glial compartments of the adult rat brain as detected by 13C, 2H NMR spectroscopy. Pergamon-Elsevier Science Ltd, Wierzba
15. Badar-Goffer R, Bachelard H, Morris P (1990) Cerebral metabolism of acetate and glucose studied by 13C NMR spectroscopy. Biochem J 266:133-139
16. Rae C, Hare N, Bubb WA, McEwan SR, Bröer A, McQuillan JA, Balcar VJ, Conigrave AD, Bröer S (2003) Inhibition of glutamine transport depletes glutamate and GABA neurotransmitter pools: Further evidence for metabolic compartmentation. J Neurochem 85:503-514
17. Bergersen LH, Magistretti PJ, Pellerin L (2005) Selective postsynaptic co-localisation of MCT2 with AMPA receptor GluR2/3 subunits at excitatory synapses exhibiting AMPA receptor trafficking. Cereb Cortex 15:361-370
18. Pierre K, Pellerin L (2005) Monocarboxylate transporters in the central nervous system: Distribution, regulation and function. J Neurochem 94:1-14
19. Rafiki A, Boulland JL, Halestrap AP, Ottersen OP, Bergersen LH (2003) Highly differential expression of the monocarboxylate transporters MCT2 and MCT4 in the developing rat brain. Neuroscience 122:677-688
20. Martin PM, Dun Y, Mysona B, Ananth S, Roon P, Smith SB, Ganapathy V (2007) Expression of the sodium-coupled monocarboxylate transporters SMCT1 (SLC5A8) and SMCT2 (SLC5A12) in retina. Invest Ophthalmol Vis Sci 48:3356-3363
21. Waniewski R, Martin D (1998) Preferential utilization of acetate by astrocytes is attributable to transport. J Neurosci 18:5225-5233
22. Berl S, Nunez R, Colon AD, Clarke DD (1983) Acetylaction of synaptosomal protein-inhibition by veratridine. J Neurochem 40:176-183
23. Rae C, Nasrallah F, Bröer S (2009) Metabolic effects of blocking lactate transport in brain cortical tissue slices using an inhibitor specific to MCT1 and MCT2. Neurochem Res 34:1783-1791
24. Nasrallah F, Griffin JL, Balcar VJ, Rae C (2007) Understanding your inhibitions. Modulation of brain cortical metabolism by GABA-B receptors. J Cereb Blood Flow Metab 27:1510-1520
25. Bröer S, Bröer A, Hansen JT, Bubb WA, Balcar VJ, Nasrallah FA, Garner B, Rae C (2007) Alanine metabolism, transport and cycling in the brain. J Neurochem 102:1758-1770
26. Bröer S (2010) Xenopus laevis oocytes. Methods Mol Biol 637: 295-310
27. Broer S, Broer A, Schneider HP, Stegen C, Halestrap AP, Deitmer JW (1999) Characterization of the high-affinity monocarboxylate transporter MCT2 in Xenopus laevis oocytes. Biochem J 341:529-535
28. Broer S, Schneider HP, Broer A, Rahman B, Hamprecht B, Deitmer JW (1998) Characterization of the monocarboxylate transporter 1 expressed in Xenopus laevis oocytes by changes in cytosolic pH. Biochem J 333:167-174
29. Tosco M, Orsenigo MN, Gastaldi G, Faelli A (2000) An endogenous monocarboxylate transport in Xenopus laevis oocytes. Am J Physiol-Regul Integr Comp Physiol 278:R1190-R1195
30. McIlwain H, Bachelard H (1985) Biochemistry and the central nervous system. Churchill Livingstone, Edinburgh, pp 7-29
31. Le Belle JE, Harris NG, Williams SR, Bhakoo KK (2002) A comparison of cell and tissue extraction techniques using highresolution 1H NMR spectroscopy. NMR Biomed 15:37-44
32. Kupce E, Freeman R (1995) Adiabatic pulses for wideband inversion and broadband decoupling. J Mag Reson A 115: 273-276
33. Skinner TE, Bendall MR (1997) A phase-cycling algorithm for reducing sidebands in adiabatic decoupling. J Magn Reson 124: 474-478
34. Rae C, Lawrance ML, Dias LS, Provis T, Bubb WA, Balcar VJ (2000) Strategies for studies of potentially neurotoxic mechanisms involving deficient transport of L-glutamate: Antisense knockout in rat brain in vivo and changes in the neurotransmitter metabolism following inhibition of glutamate transport in guinea pigs brain slices. Brain Res Bull 53:373-381
35. Nasrallah FA, Balcar VJ, Rae CD (2011) Activity dependent GABA release controls brain cortical tissue slice metabolism. J Neurosci Res 89:1935-1945
36. Nasrallah F, Griffin JL, Balcar VJ, Rae CD (2009) Understanding your inhibitions. Effects of GABA and GABAA receptors on brain cortical metabolism. J Neurochem 108:57-71
37. Wold S, Antti H, Lindgren F, Ohman J (1998) Orthogonal signal correction of near-infrared spectra. Chemom Intell Lab Syst 44:175-185
38. Halestrap AP, Price NT (1999) The proton-linked monocarboxylate transporter (MCT) family: Structure, function and regulation. Biochem J 343:281-299
39. Halestrap AP, Denton RM (1974) Specific inhibition of pyruvate transport in rat liver mitochondria and human erythrocytes by a-cyano-4-hydroxycinnamate. Biochem J 138:313-316
40. Martin PM, Gopal E, Ananth S, Zhuang L, Itagaki S, Prasad BM, Smith SB, Prasad PD, Ganapathy V (2006) Identify of SMCT1(SLC5A8) as a neuron-specific Na+-coupled transporter for active uptake of L-lactate and ketone bodies in the brain. J Neurochem 98:279-288
41. Tucek S, Cheng SC (1974) Provenance of acetyl group of acetylcholine and compartmentation of acetyl-CoA and Krebs cycle intermediates in brain in vivo. J Neurochem 22:893-914
42. Berl S, Clarke DD, Colon A, Nunez R (1983) H-3-Labelled acetate incorporation into protein of synaptosomes-effect of Na+ channel toxins. Hoppe Seylers Z Physiol Chem 364:1098-1099
43. Nakamura R, Cheng SC, Naruse H (1970) A study on precursors of acetyl moiety of acetylcholine in brain slices-observations on compartmentalization of acetyl-coenzyme A pool Biochem J 118:443
44. Kirkby B, Roman N, Kobe B, Kellie S, Forwood JK (2010) Functional and structural properties of mammalian acyl-coenzyme A thioesterases. Prog Lipid Res 49:366-377
45. Robinson JB, Mahan DE, Koeppe RE (1976) Studies on rat brain acyl-coenzyme-A hydrolase (short chain). Biochem Biophys Res Commun 71:959-965
46. Matsuda T, Yonehara N, Yoshida H (1976) Metabolism of precursors of acetylcholine synthesis in central nervous system-some properties of acetyl-CoA hydrolase in cytoplasmic soluble fraction from rat brain. Folia Pharmacol Jap 72:P63
47. Beigneux AP, Kosinski C, Gavino B, Horton JD, Skarnes WC, Young SG (2004) ATP-citrate lyase deficiency in the mouse. J Biol Chem 279:9557-9564
48. Alf MF, Lei H, Berthet C, Hirt L, Gruetter R, Mlynarik V (2012) High-resolution spatial mapping of changes in the neurochemical profile after focal ischemia in mice. NMR Biomed 25:247-254
49. Madhavarao CN, Arun P, Moffett JR, Szucs S, Surendran S, Matalon R, Garbern J, Hristova D, Johnson A, Jiang W, Namboodiri MAA (2005) Defective N-acetylaspartate catabolism reduces brain acetate levels and myelin lipid synthesis in Canavan's disease. Proc Natl Acad Sci USA 102:5221-5226
50. Urenjak J, Williams SR, Gadian DG, Noble M (1993) Proton nuclear magnetic resonance spectroscopy unambiguously identifies different neural types. J Neurosci 13:981-989
51. 2+ on labelling of glutamate, glutamine, aspartate and GABA by 1-C-14acetate, U-C-14glutamate and U-C-14 aspartate. J Neurochem 17:999-1007
52. Berl S, Lajtha A, Waelsch H (1961) Amino acid and protein metabolism-VI Cerebral compartments of glutamic acid metabolism. J Neurochem 7:186-197
53. Sonnewald U, Westergaard N, Hassel B, Müller TB, Unsgard G, Fonnum F, Hertz L, Schousboe A, Petersen SB (1993) NMR spectroscopy studies of 13C acetate and 13C glucose metabolism in neocortical astrocytes: Evidence for mitochondrial heterogeneity. Dev Neurosci 15:351-358
54. Wyss MT, Magistretti PJ, Buck A, Weber B (2011) Labeled acetate as a marker of astrocytic metabolism. J Cereb Blood Flow Metab 31:1668-1674
55. Badar-Goffer R, Bachelard H, Morris P (1992) Neuronal-glial metabolism under depolarising conditions. Biochem J 282:225-230
56. Westergaard N, Sonnewald U, Unsgard G, Peng L, Hertz L, Schousboe A (1994) Uptake, release and metabolism of citrate in neurons and astrocytes in primary cultures. J Neurochem 62: 1727-1733
57. Sonnewald U, Westergaard N, Krane J, Unsgard G, Petersen SB, Schousboe A (1991) First direct demonstration of preferential release of citrate from astrocytes using C-13 NMR spectroscopy of cultured neurons and astrocytes. Neurosci Lett 128:235-239
58. Waagepetersen HS, Sonnewald U, Larsson OM, Schousboe A (2001) Multiple compartments with different metabolic characteristics are involved in biosynthesis of intracellular and released glutamine and citrate in astrocytes. Glia 35:246-252
59. Cheng SC, Nakamura R (1972) Metabolism related to tricarboxylic acid cycle in rat brain slices-observations on CO2 fixation and metabolic compartmentation. Brain Res 38:355
60. Wellen KE, Hatzivassiliou G, Sachdeva UM, Bui TV, Cross JR, Thompson CB (2009) ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324:1076-1080
61. Shin JY, Zhang D, Chen D (2011) Reversible acetylation of metabolic enzymes celebration: SIRT2 and p300 join the party. Mol Cell 43:3-5
62. Hallows WC, Lee S, Denu JM (2006) Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc Natl Acad Sci USA 103:10230-10235
63. Bitterman KJ, Anderson RM, Cohen HY, Latorre-Esteves M, Sinclair DA (2002) Inhibition of silencing and accelerated aging by nicotinamide, a putative negative regulator of yeast Sir2 and human SIRT1. J Biol Chem 277:45099-45107
64. Canto C, Auwerx J (2012) Targeting Sirtuin 1 to improve metabolism: All you need is NAD(?)? Pharmacol Rev 64: 166-187
65. Billington RA, Travelli C, Ercolano E, Galli U, Roman CB, Grolla AA, Canonico PL, Condorelli F, Genazzani AA (2008) Characterization of NAD uptake in mammalian cells. J Biol Chem 283:6367-6374
66. Pittelli M, Felici R, Pitozzi V, Giovannelli L, Bigagli E, Cialdai F, Romano G, Moroni F, Chiarugi A (2011) Pharmacological effects of exogenous NAD on mitochondrial bioenergetics, DNA repair, and apoptosis. Mol Pharmacol 80:1136-1146
67. Clarke DD (1999) Acetate and fluoroacetate as possible markers for glial metabolism: An historical perspective. J Neurochem 72:S2
68. Galic S, Schneider HP, Bröer A, Deitmer JW, Bröer S (2003) The loop between helix 4 and helix 5 in the monocarboxylate transporter MCT1 is important for substrate selection and protein stability. Biochem J 376:413-422
69. Carpenter L, Halestrap AP (1994) The kinetics, substrate and inhibitor specificity of the lactate transporter of ehrlich-lettre tumor cells studied with the intracellular pH indicator BCECF. Biochem J 304:751-760
70. Bröer S, Rahman B, Pellegri G, Pellerin L, Martin JL, Verleysdonk S, Hamprecht B, Magistretti PJ (1997) Comparison of lactate transport in astroglial cells and transporter 1 (MCT 1) expressing Xenopus laevis oocytes. Expression of two different monocarboxylate transporters in astroglial cells and neurons. J Biol Chem 272:30096-30102
71. Fox JEM, Meredith D, Halestrap AP (2000) Characterisation of human monocarboxylate transporter 4 substantiates its role in lactic acid efflux from skeletal muscle. J Physiol Lond 529: 285-293
72. Ovens MJ, Manoharan C, Wilson MC, Murray CM, Halestrap AP (2010) The inhibition of monocarboxylate transporter 2 (MCT2) by AR-C155858 is modulated by the associated ancillary protein. Biochem J 431:217-225
73. Lin RY, Vera JC, Chaganti RSK, Golde DW (1998) Human monocarboxylate transporter 2 (MCT2) is a high affinity pyruvate transporter. J Biol Chem 273:28959-28965
74. Dimmer KS, Friedrich B, Lang F, Deitmer JW, Broer S (2000) The low-affinity monocarboxylate transporter MCT4 is adapted to the export of lactate in highly glycolytic cells. Biochem J 350:219-227
75. Babu E, Ramachandran S, CoothanKandaswamy V, Elangovan S, Prasad PD, Ganapathy V, Thangaraju M (2011) Role of SLC5A8, a plasma membrane transporter and a tumor suppressor, in the antitumor activity of dichloroacetate. Oncogene 30:4026-4037
76. Miyauchi S, Gopal E, Fei YJ, Ganapathy V (2004) Functional identification of SLC5A8, a tumor suppressor down-regulated in colon cancer, as a Na+-coupled transporter for short-chain fatty acids. J Biol Chem 279:13293-13296
77. Gopal E, Umapathy NS, Martin PM, Ananth S, Gnana-Prakasam JP, Becker H, Wagner CA, Ganapathy V, Prasad PD (2007) Cloning and functional characterization of human SMCT2 (SLC5A12) and expression pattern of the transporter in kidney. Biochim Biophys Acta 1768:2690-2697