Feeding active neurons: (Re)emergence of a nursing role for astrocytes

Journal of Physiology Paris

Volumn 96, Issue 3-4, 2002, Pages 273-282

  Bouzier Sore, Anne Karine ^a,b   Merle, Michel ^b   Magistretti, Pierre J ^a   Pellerin, Luc ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b CNRS University Bordeaux Segalen   (France)

Author keywords

Astrocyte; Energy metabolism; Glucose; Lactate; Neuron

Indexed keywords

GLUCOSE; GLUTAMIC ACID; LACTIC ACID;

AMINO ACID TRANSPORT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CELL ACTIVITY; CELL FUNCTION; CELL SURVIVAL; CELL TYPE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENERGY METABOLISM; EVIDENCE BASED MEDICINE; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL; NONHUMAN; OXIDATION; SYNAPSE;

EID: 0036556478     PISSN: 09284257     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0928-4257(02)00016-5     Document Type: Article

References (130)

1. A. Ames III, CNS energy metabolism as related to function, Brain Res. Rev. 34 (2000) 42-68.
2. W.L. Andriezen, On a system of fibre-like cells surrounding the blood vessels of the brain of man and mammals, and its physiological significance, Int. Monatsschr. Anat. Physiol. 10 (1893) 532-540.
3. H.M. Assaf, A.J. Ricci, T.S. Whittingham, J.C. LaManna, R.A. Ratcheson, W.D. Lust, Lactate compartmentation in hippocampal slices: evidence for a transporter, Metab. Brain Dis. 5 (1990) 143-154.
4. A. Avogaro, R. Nosadini, A. Doria, C. Tremolada, U. Baccaglini, F. Ambrosio, C. Merkel, A. Nosadini, R. Trevisan, P. Fioretto, Substrate availability other than glucose in the brain during euglycemia and insulin-induced hypoglycemia in dogs, Metabolism 39 (1990) 46-50.
5. P.G. Bittar, Y. Charnay, L. Pellerin, C. Bouras, P.J. Magistretti, Selective distribution of lactate dehydrogenase isoenzymes in neurons and astrocytes of human brain, J. Cereb. Blood Flow Metab. 16 (1996) 1079-1089.
6. A.K. Bouzier, E. Thiaudiere, M. Biran, R. Rouland, P. Canioni, M. Merle, The metabolism of [3-(13)C]lactate in the rat brain is specific of a pyruvate carboxylase-deprived compartment, J. Neurochem. 75 (2000) 480-486.
7. K.P. Briski, Intraventricular lactate infusion attenuates the transactivational effects of the glucose antimetabolite, 2-deoxy-D-glucose, on hypothalamic vasopressinergic neurons, Brain Res. 839 (1999) 341-345.
8. S. Bröer, B. Rahman, G. Pellegri, L. Pellerin, J.-L. Martin, S. Verleysdonk, B. Hamprecht, P.J. Magistretti, Comparison of lactate transport in astroglial cells and monocarboxylate transporter I (MCT1) expressing Xenopus laevis oocytes: expression of two different monocarboxylate transporters in astroglial cells and neurons, J. Biol. Chem. 272 (1997) 30096-30102.
9. G. Brooks, Intra- and extra-cellular lactate shuttles, Med. Sci. Sports Exerc. 32 (2000) 790-799.
10. A.M. Brown, R. Wender, B.R. Ransom, Metabolic substrates other than glucose support axon function in central white matter, J. Neurosci. Res. 66 (2001) 839-843.
11. F.G. Carpenter, Substrates supporting activity in immature nerve fibers, Am. J. Physiol. 197 (1959) 813-816.
12. C.J. Cassady, J.W. Phillis, M.H. O'Regan, Further studies on the effects of topical lactate on amino acid efflux from the ischemic rat cortex, Brain Res. 901 (2001) 30-37.
13. H.L. Cater, C.D. Benham, L.E. Sundstrom, Neuroprotective role of monocarboxylate transport during glucose deprivation in slice cultures of rat hippocampus, J. Physiol. 531 (2001) 459-466.
14. + dynamics in mouse cortical astrocytes: implications for cellular bioenergetics, Eur. J. Neurosci. 12 (2000) 3843-3853.
15. C.P. Chih, J. He, T.S. Sly, E.L. Roberts Jr., Comparison of glucose and lactate as substrates during NMDA-induced activation of hippocampal slices, Brain Res. 893 (2001) 143-154.
16. N. Cholet, L. Pellerin, E. Welker, P. Lacombe, J. Seylaz, P.J. Magistretti, G. Bonvento, Local injection of antisense oligonucleotides targeted to the glial glutamate transporter GLAST decreases the metabolic response to somatosensory activation, J. Cereb. Blood Flow Metab. 21 (2001) 404-412.
17. 2 subunit and the glial glutamate transporters GLAST and GLT-1 in the rat somatosensory cortex, Cerebral Cortex (in press) (2002).
18. D.W. Cox, H.S. Bachelard, Partial attenuation of dentate granule cell evoked activity by the alternative substrates, lactate and pyruvate: evidence for a postsynaptic action, Exp. Brain Res. 69 (1988) 368-372.
19. J.W. Deitmer, Strategies for metabolic exchange between glial cells and neurons, Resp. Physiol. 129 (2001) 71-81.
20. J.W. Deitmer, C.R. Rose, pH regulation and proton signalling in glial cells, Prog. Neurobiol. 48 (1996) 73-103.
21. M. Demestre, M. Boutelle, M. Fillenz, Stimulated release of lactate in freely moving rats is dependent on the uptake of glutamate. J. Physiol. (Lond.) 499 (1997) 825-832.
22. M. Dolivo, Les conditions métaboliques nécessaires à la survie fonctionnelle du tissu nerveux in vitro, Bull. Acad. Suisse Sci. Med. 18 (1962) 247-252.
23. R. Dringen, R. Gebhardt, B. Hamprecht, Glycogen in astrocytes: possible function as lactate supply for neighboring cells, Brain Res. 623 (1993) 208-214.
24. R. Dringen, H. Wiesinger, B. Hamprecht, Uptake of L-lactate by cultured rat brain neurons, Neurosci. Lett. 163 (1993) 5-7.
25. R. Dringen, H. Peters, H. Wiesinger, B. Hamprecht, Lactate transport in cultured glial cells, Dev. Neurosci. 17 (1995) 63-69.
26. H.W. Elliot, V.C. Sutherland, J. Cell Comp. Physiol. 40 (1952) 221.
27. L.K. Fellows, M.G. Boutelle, M. Fillenz, Physiological stimulation increases nonoxidative glucose metabolism in the brain of the freely moving rat, J. Neurochem. 60 (1993) 1258-1263.
28. E. Fernandez, J.M. Medina, Lactate utilization by the neonatal rat brain in vitro. Competition with glucose and 3-hydroxybutyrate, Biochem. J. 234 (1986) 489-492.
29. J.C. Fowler, Glucose deprivation results in a lactate preventable increase in adenosine and depression of synaptic transmission in rat hippocampal slices, J. Neurochem. 60 (1993) 572-576.
30. A.E. Fray, R.J. Forsyth, M.G. Boutelle, M. Fillenz, The mechanisms controlling physiologically stimulated changes in rat brain glucose and lactate: a microdialysis study, J. Physiol. 496 (1996) 49-57.
31. D.Z. Gerhart, B.E. Enerson, O.Y. Zhdankina, R.L. Leino, L.R. Drewes, Expression of monocarboxylate transporter MCT1 by brain endothelium and glia in adult and suckling rats, Am. J. Physiol. 273 (1997) E207-E213.
32. D.Z. Gerhart, B.E. Enerson, O.Y. Zhdankina, R.L. Leino, L.R. Drewes, Expression of the monocarboxylate transporter MCT2 by rat brain glia, Glia 22 (1998) 272-281.
33. E. Giacobini, A cytochemical study of the localization of carbonic anhydrase in the nervous system, J. Neurochem. 9 (1962) 169-177.
34. C. Golgi, Sulla fine anatomia degli organi centrali del sisterna nervoso, Hoepli, Milano, 1886.
35. M. Hamai, Y. Minokoshi, T. Shimazu, L-Glutamate and insulin enhance glycogen synthesis in cultured astrocytes from the rat brain through different intracellular mechanisms, J. Neurochem. 73 (1999) 400-407.
36. B. Hassel, A. Brathe, Cerebral metabolism of lactate in vivo: evidence for neuronal pyruvate carboxylation, J. Cereb. Blood Flow Metab. 20 (2000) 327-336.
37. T. Himmi, J. Perrin, M. Dallaporta, J.C. Orsini, Effects of lactate on glucose-sensing neurons in the solitary tract nucleus, Physiol. Behav. 74 (2001) 391-397.
38. H.E. Himwich, K.M. Bowman, C. Daly, J.F. Fazekas, J. Wortis, W. Goldfarb, Cerebral blood flow and brain metabolism during insulin hypoglycemia, Am. J. Physiol. 132 (1941) 640-647.
39. Y. Hu, G.S. Wilson, Rapid changes in local extracellular rat brain glucose observed with an in vivo glucose sensor, J. Neurochem. 68 (1997) 1745-1752.
40. K. Ide, A. Horn, N.H. Secher, Cerebral metabolic response to submaximal exercise, J. Appl. Physiol. 87 (1999) 1604-1608.
41. 2, uptake in human brain during recovery from maximal exercise, J. Physiol. 522 (2000) 159-164.
42. T. Ide, J. Steinke, G.F. Cahill Jr., Metabolic interactions of glucose, lactate, and β-hydroxybutyrate in rat brain slices, Am. J. Physiol. 217 (1969) 784-792.
43. Y. Izumi, A.M. Benz, C.F. Zorumski, J.W. Olney, Effects of lactate and pyruvate on glucose utilization in rat hippocampal slices, Neuroreport 5 (1994) 617-620.
44. Y. lzumi, A.M. Benz, H. Katsuki, C.F. Zorumski, Endogenous monocarboxylates sustain hippocampal synaptic function and morphological integrity during energy deprivation, J. Neurosci. 17 (1997) 9448-9457.
45. Y. Izumi, H. Katsuki, C.F. Zorumski, Monocarboxylates (pyruvate and lactate) as alternative energy substrates for the induction of long-term potentiation in rat hippocampal slices, Neurosci. Lett. 232 (1997) 17-20.
46. V.N. Jackson, N.T. Price, L. Carpenter, A.P. Halestrap, Cloning of the monocarboxylate transporter isoform isoforni MCT2 from rat testis provides evidence that expression in tissues is species-specific and may involve post-transcriptional regulation, Biochem. J. 324 (1997) 447-453.
47. D.A. Jones, J. Ros, H. Landolt, M. Fillenz, M. Boutelle, Dynamic changes in glucose and lactate in the cortex of the freely moving rat monitored using microdialysis, J. Neurochem. 75 (2000) 1703-1708.
48. T. Kanatani, K. Mizuno, Y., Okada, Effects of glycolytic metabolites on preservation of high energy phosphate level and synaptic transmission in the granule cells of guinea pig hippocampal slices, Experientia 51 (1995) 213-216.
49. J.N. Keller, M.R., Steiner, M.P. Mattson, S.M. Steiner, Lysophosphatidic acid decreases glutamate and glucose uptake by astrocytes, J. Neurochem. 67 (1996) 2300-2305.
50. J.R. Klein, N.S. Olsen, J. Biol. Chem. 167 (1947) 1.
51. P. King, M.F. Kong, H. Parkin, I.A. MacDonald, C. Barber, R.B. Tattersall, Intravenous lactate prevents cerebral dysfunction during hypoglycemia in insulin-dependent diabetes mellitus, Clin. Sci. 94 (1998) 157-163.
52. E.M. Koehler-Stec, I.A. Simpson, S.J. Vannucci, K.T. Landschulz, W.H. Landschulz, Monocarboxylate transporter expression in mouse brain, Am. J. Physiol. 275 (1998) E516-E524.
53. C.C. Kratzing, Biochem. J. 54 (1953) 312.
54. M.G. Larrabee, Lactate uptake and release in the presence of glucose by sympathetic ganglia of chicken embryos and by neuronal and nonneuronal cultures prepared from these ganglia, J. Neurochem. 40 (1983) 1237-1250.
55. M.G. Larrabee, Extracellular intermediates of glucose metabolism: fluxes of endogenous lactate and alanine through extra-cellular pools in embryonic sympathetic ganglia, J. Neurochem. 59 (1992) 1041-1052.
56. M.G. Larrabee, Lactate metabolism and its effect on glucose metabolism in an excised neural tissue, J. Neurochem. 64 (1995) 1734-1741.
57. M.G. Larrabee, Partitioning of CO2 production between glucose and lactate in excised sympathetic ganglia, with implications for brain, J. Neurochem. 67 (1996) 1726-1734.
58. J.D. Laughton, Y. Charnay, B. Belloir, L. Pellerin, P.J. Magistretti, C. Bouras, Differential messenger RNA distribution of lactate dehydrogenase LDH-1 and LDH-5 isoforms in the rat brain, Neuroscience 96 (2000) 619-625.
59. P.J. Magistretti, O. Sorg, N. Yu, J.-L. Martin, L., Pellerin, Neurotransmitters regulate energy metabolism in astrocytes: implications for the metabolic trafficking between neural cells, Dev. Neurosci. 15 (1993) 306-312.
60. P.J Magistretti, L. Pellerin, Cellular bases of brain energy metabolism and their relevance to functional brain imaging: evidence for a prominent role of astrocytes, Cerebral Cortex 6 (1996) 50-61.
61. P.J. Magistretti, L. Pellerin, Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging, Phil. Trans. R. Soc. Lond. B 354 (1999) 1155-1163.
62. P.J. Magistretti, L. Pellerin, D.L. Rothman, R.G. Shulman, Energy on demand, Science 283 (1999) 496-497.
63. F. Maher, S.J. Vannucci, I.A. Simpson, Glucose transporter proteins in brain, FASEB J. 8 (1994) 1003-1011.
64. A. Maran, I. Cranston, J. Lomas, I. Macdonald, S.A. Amiel, Protection by lactate of cerebral function during hypoglycemia. Lancet 343 (1994) 16-20.
65. A. Maran, C. Crepaldi, S. Trupiani, T. Lucca, E. Jori, I.A. Macdonald, A. Tiengo, A. Avogaro, S. Del Prato, Brain function rescue effect of lactate following hypoglycaemia is not an adaptation process in both normal and type I diabetic subjects, Diabetologia 43 (2000) 733-741.
66. M. Maus, P. Marin, M. Israël, J. Glowinski, J. Prémont, Pyruvate and lactate protect striatal neurons against N-methyl-D-aspartate-induced neurotoxicity, Eur. J. Neurosci. 11 (1999) 3215-3224.
67. H. McIlwain, Substances which support respiration and metabolic response to electrical impulses in human cerebral tissues, J. Neurol. Neurosurg. Psychiat. 16 (1953) 257-266.
68. H. McIlwain, Electrical influences and speed of chemical change in the brain, Physiol. Rev. 36 (1956) 355-375.
69. M.C. McKenna, J.T. Tildon, J.H. Stevenson, R. Boatright, S. Huang, Regulation of energy metabolism in synaptic terminals and cultured rat brain astrocytes: differences revealed using aminooxyacetate, Dev. Neurosci. 15 (1993) 320-329.
70. M.C. McKenna, J.T. Tildon, J.H. Stevenson, I.B. Hopkins, Energy metabolism in cortical synaptic terminals from weanling weanliiig and mature rat brain: evidence for multiple compartments of tricarboxylic acid cycle activity, Dev. Neurosci. 16 (1994) 291-300.
71. M.C. McKenna, J.T. Tildon, J.H. Stevenson, I.B. Hopkins, X. Huang, R. Couto, Lactate transport by cortical synaptosomes from adult brain: characterization of kinetics and inhibitor specificity, Dev. Neurosci. 20 (1998) 300-309.
72. M.C. McKenna, I.B. Hopkins, A. Carey, α-cyano-4-hydroxycinnamate decreases both glucose and lactate metabolism in neurons and astrocytes: implications for lactate as an energy substrate for neurons, J. Neurosci. Res. 66 (2001) 747-754.
73. A. Mendelowitsch, M.F. Ritz, J. Ros, H. Langemann, O. Gratzl, 17β-Estradiol reduces cortical lesion size in the glutamate excitotoxicity model by enhancing extracellular lactate: a new neuroprotective pathway, Brain Res. 901 (2001) 230-236.
74. M. Mita, P.F. Hall, Metabolism of round spermatids from rats: lactate as the preferred substrate, Biol. Reprod. 26 (1982) 1535-1541.
75. C.V. Mobbs, L.M. Kow, X.J. Yang, Brain glucose-sensing mechanisms: ubiquitous silencing by aglycemia vs. hypothalamic neuroendocrine responses, Am. J. Physiol. 281 (2001) E649-E654.
76. M. Nedergaard, S.A. Goldman, Carrier-mediated transport of lactic acid in cultured neurons and astrocytes, Am. J. Physiol. 265 (1993) R282-R289.
77. A. Nehlig, A. Pereira de Vasconcelos, Glucose and ketone body utilization by the brain of neonatal rats, Prog. Neurobiol. 40 (1993) 163-221.
78. E.M. Nemoto, J.T. Hoff, J.W. Severinghaus, Lactate uptake and metabolism by brain during hyperlactatemia and hypoglycemia, Stroke 5 (1974) 48-53.
79. L. Pellerin, P.J. Magistretti, Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization, Proc. Natl. Acad. Sci. USA 91 (1994) 10625-10629.
80. +-ATPase activity in astrocytes via activation of a distinct subunit highly sensitive to ouabain, J. Neurochem. 69 (1997) 2132-2137.
81. L. Pellerin, G. Pellegri, P.G. Bittar, Y. Charnay, C. Bouras, J.-L. Martin, N. Stella, P.J. Magistretti, Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle, Dev. Neurosci. 20 (1998) 291-299.
82. L. Pellerin, G. Pellegri, J.-L. Martin, P.J. Magistretti, Expression of monocarboxylate transporter mRNAs in mouse brain: support for a distinct role of lactate as an energy substrate for the neonatal vs. adult brain, Proc. Natl. Acad. Sci. USA 95 (1998) 3990-3995.
83. K. Pierre, L. Pellerin, R. Debernardi, B.M. Riederer, P.J. Magistretti, Cell-specific localization of monocarboxylate transporters, MCT1 and MCT2, in the adult mouse brain revealed by double immunohistochemical labeling and confocal microscopy, Neuroscience 100 (2000) 617-627.
84. K. Pierre, P.J. Magistretti, L. Pellerin, MCT2 is a major neuronal monocarboxylate transporter in the adult mouse brain, J. Cereb. Blood Flow Metab. (2002).
85. S. Poitry, C. Poitry-Yamate, J. Ueberfeld, P.R. MacLeish, M. Tsacopoulos, Mechanisms of glutamate metabolic signaling in retinal glial (Müller) cells, J. Neurosci. 20 (2000) 1809-1821.
86. C.L. Poitry-Yamate, S. Poitry, M. Tsacopoulos, Lactate released by Müller glial cells is metabolized by photoreceptors from mammalian retina, J. Neurosci. 15 (1995) 5179-5191.
87. H. Qu, A. Haberg, O. Haraldseth, G. Unsgard, U. Sonnewald, (13)C MR spectroscopy study of lactate as substrate for rat brain, Dev. Neurosci. 22 (2000) 429-436.
88. E.P. Rivers, N.A. Paradis, G.B. Martin, M.E. Goetting, J.A. Rosenberg, H.A. Smithline, T.J. Appleton, R.M. Nowak, Cerebral lactate uptake during cardiopulmonary resuscitation in humans, J. Cereb. Blood Flow Metab. 11 (1991) 479-484.
89. J. Ros, N. Pecinska, B. Alessandri, H. Landolt, M. Fillenz, Lactate reduces glutamate-induced neurotoxicity in rat cortex, J. Neurosci. Res. 66 (2001) 790-794.
90. M. Saitoh, Y. Okada, M. Nabetani, Effect of mannose, fructose and lactate on the preservation of synaptic potentials in hippocampal slices, Neurosci. Lett. 171 (1994) 125-128.
91. T. Sakurai, B. Yang, T. Takata, K. Yokono, Exogenous lactate sustains synaptic activity and neuronal viability, but fails to induce long-term potentiation (LTP), Nippon Ronen Igakkai Zasshi 37 (2000) 962-965.
92. L. Sala, Zur feineren Anatomie des grossen Seepferdefusses, Zeitschr. Wissenschaftl. Zool 52 (1891) 18-45.
93. A. Schousboe, N. Westergaard, H.S. Waagepetersen, O.M. Larsson, I.J. Bakken, U. Sonnewald, Trafficking between glia and neurons of TCA cycle intermediates and related metabolites, Glia 21 (1997) 99-105.
94. A. Schurr, C.A. West, B.M. Rigor, Lactate-supported synaptic function in the rat hippocampal slice preparation, Science 240 (1988) 1326-1328.
95. A. Schurr, R.S. Payne, J.J. Miller, B.M. Rigor, Brain lactate, not glucose, fuels the recovery of synaptic function from hypoxia upon reoxygenation: an in vitro study, Brain Res. 744 (1997) 105-111.
96. A. Schurr, R.S. Payne, J.J. Miller, B.M. Rigor, Glia are the main source of lactate utilized by neurons for recovery of function posthypoxia, Brain Res. 774 (1997) 221-224.
97. A. Schurr, R.S. Payne, J.J. Miller, B.M. Rigor, Brain lactate is an obligatory aerobic energy substrate for functional recovery after hypoxia: further in vitro validation, J. Neurochem. 69 (1997) 423-426.
98. A. Schurr, J.J. Miller, R.S. Payne, B.M. Rigor, An increase in lactate output by brain tissue serves to meet the energy needs of glutamate-activated neurons, J. Neurosci. 19 (1999) 34-39.
99. A. Schurr, R.S. Payne, J.J. Miller, M.T. Tseng, B.M. Rigor, Blockade of lactate transport exacerbates delayed neuronal damage in a rat model of cerebral ischemia, Brain Res. 895 (2001) 268-272.
100. A. Schurr, R.S. Payne, M.T. Tseng, E. Gozal, D. Gozal, Excitotoxic preconditioning elicited by both glutamate and hypoxia and abolished by lactate transport inhibition in rat hippocampal slices, Neurosci. Lett. 307 (2001) 151-154.
101. R.P. Shank, G.S. Bennett, S.O. Freytag, G.L. Campbell, Pyruvate carboxylase: an astrocyte-specific enzyme implicated in the replenishment of amino acid neurotransmitter pools, Brain Res. 329 (1985) 364-367.
102. W.E. Stone, Biochem. J. 32 (1938) 1908.
103. A. Tabernero, C. Vicario, J.M. Medina, Lactate spares glucose as a metabolic fuel in neurons and astrocytes from primary cultures, Neurosci. Res. 26 (1996) 369-376.
104. S. Takahashi, B.F. Driscoll, M.J. Law, L. Sokoloff, Role of sodium and potassium ions in regulation of glucose metabolism in cultured astroglia, Proc. Natl. Acad. Sci. USA 92 (1995) 4616-4620.
105. T. Takata, Y. Okada, Effects of deprivation of oxygen or glucose on the neural activity in the guinea pig hippocampal slice-intracellular recording study of pyramidal neurons, Brain Res. 683 (1995) 109-116.
106. T. Takata, T. Sakurai, B. Yang, K. Yokono, Y. Okada, Effect of lactate on the synaptic potential energy metabolism, calcium homeostasis and extracellular glutamate concentration in the dentate gyrus of the hippocampus from guinea-pig, Neuroscience 104 (2001) 371-378.
107. G. Tholey, B.F. Roth-Schechter, P. Mandel, Activity and isoenzyme pattern of lactate dehydrogenase in neurons and astroblasts cultured from brains of chick embryos, J. Neurochem. 36 (1981) 77-81.
108. J.H. Thurston, R.E. Hauhart, J.A. Schiro, Lactate reverses insulin-induced hypoglycemic stupor in suckling-weanling mice: biochemical correlates in blood, liver, and brain, J. Cereb. Blood Flow Metab. 3 (1983) 498-506.
109. J.H. Thurston, R.E. Hauhart, Effect of momentary stress on brain energy metabolism in weanling mice: apparent use of lactate as cerebral metabolic fuel concomitant with a decrease in brain glucose utilization, Metab. Brain Dis. 4 (1989) 177-186.
110. J.T. Tildon, M.C. McKenna, J. Stevenson, R. Couto, Transport of L-lactate by cultured rat brain astrocytes, Neurochem. Res. 18 (1993) 177-184.
111. M. Tsacopoulos, P.J. Magistretti, Metabolic coupling between glia and neurons, J. Neurosci. 16 (1996) 877-885.
112. M. Tsacopoulos, C.L. Poitry-Yamate, S. Poitry, P. Perrottet, A.L. Veuthey, The nutritive function of glia is regulated by signals released by neurons, Glia 21 (1997) 84-91.
113. C. Véga, C.L. Poitry-Yamate, P. Jirounek, M. Tsacopoulos, J.A. Coles, Lactate is released and taken up by isolated rabbit vagus nerve during aerobic metabolism, J. Neurochem. 71 (1998) 330-337.
114. L. Venkov, L. Rosental, M. Manolova, Subcellular distribution of LDH isoenzymes in neuronal- and glial-enriched fractions, Brain Res. 109 (1976) 323-333.
115. C. Vicario, C. Arizmendi, G. Malloch, J.B. Clark, J.M. Medina, Lactate utilization by isolated cells from early neonatal rat brain, J. Neurochem. 57 (1991) 1700-1707.
116. B. Voutsinos-Porche, C. Coste, K. Tanaka, J. Seylaz, G. Bonvento, Role of the glial glutamate transporter GLAST in coupling glucose use to neuronal activity: a study in young and adult GLAST KO mice, Soc. Neurosci. Abstr. 26 (2000) 647, 4.
117. H.S. Waagepetersen, I.J. Bakken, O.M. Larsson, U. Sonnewald, A. Schousboe, Comparison of lactate and glucose metabolism in cultured neocortical neurons and astrocytes using 13C-NMR spectroscopy, Dev. Neurosci, 20 (1998) 310-320.
118. H.S. Waagepetersen, I.J. Bakken, O.M. Larsson, U. Sonnewald, A. Schousboe, Metabolism of lactate in cultured GABAergic neurons studied by 13C nuclear magnetic resonance spectroscopy, J. Cereb. Blood Flow Metab. 18 (1998) 109-117.
119. H.S. Waagepetersen, U. Sonnewald, O.M. Larsson, A. Schousboe, A possible role of alanine for ammonia transfer between astrocytes and glutamatergic neurons, J. Neurochem. 75 (2000) 471-479.
120. H. Wada, Y. Okada, M. Nabetani, H. Nakamura, The effects of lactate and β-hydroxybutyrate on the energy metabolism and neural activity of hippocampal slices from adult and immature rat, Dev. Brain Res. 101 (1997) 1-7.
121. H. Wada, Y. Okada, T. Uzuo, H. Nakamura, The effects of glucose, mannose, fructose and lactate on the preservation of neural activity in the hippocampal slices from the guinea pig, Brain Res. 788 (1998) 144-150.
122. W. Walz, S. Mukerji, Lactate production and release in cultured astrocytes, Neurosci. Lett. 86 (1988) 296-300.
123. W. Walz, S. Mukerji, Lactate release from cultured astrocytes and neurons: a comparison, Glia 1 (1988) 366-370.
124. R. Wender, A.M. Brown, R. Fern, R.A. Swanson, K. Farrell, B.R. Ransom, Astrocytic glycogen influences axon function and survival during glucose deprivation in central white matter, J. Neurosci. 20 (2000) 6804-6810.
125. J. Wortis, K.M. Bowman, W. Goldfarb, J.F. Fazekas, H.E. Himwich, Availability of lactic acid for brain oxidations, J. Neurophysiol. (1941) 243-249.
126. K. Yamane, K. Yokono, Y. Okada, Anaerobic glycolysis is crucial for the maintenance of neural activity in guinea pig hippocampal slices, J. Neurosci. Methods 103 (2000) 163-171.
127. X.J. Yang, L.M. Kow, T. Funabashi, C.V. Mobbs, Hypothalamic glucose sensor: similarities to and differences from pancreatic β-cell mechanisms, Diabetes 48 (1999) 1763-1772.
128. A.C. Yu, J. Drejer, L. Hertz, A. Schousboe, Pyruvate carboxylase activity in primary cultures of astrocytes and neurons, J. Neurochem. 41 (1983) 1484-1487.
129. C. Zwingmann, C. Richter-Landsberg, A. Brand, D. Leibfritz, NMR spectroscopic study on the metabolic fate of [3-(13)C]alanine in astrocytes, neurons and cocultures; implications for glia-neuron interactions in neurotransmitter metabolism, Glia 32 (2000) 286-303.
130. C. Zwingmann, C. Richter-Landsberg, D. Leibfritz, 13C isotopomer analysis of glucose and alanine metabolism reveals cytosolic pyruvate compartmentation as part of enrgy metabolism in astrocytes, Glia 34 (2001) 200-212.