Brain energy metabolism: Focus on Astrocyte-neuron metabolic cooperation

Cell Metabolism

Volumn 14, Issue 6, 2011, Pages 724-738

  Bélanger, Mireille ^a   Allaman, Igor ^a   Magistretti, Pierre J ^a,b  

^a EPFL   (Switzerland)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN; NEUROTRANSMITTER;

AEROBIC METABOLISM; ASTROCYTE; BRAIN BLOOD FLOW; BRAIN METABOLISM; BRAIN NERVE CELL; CELL INTERACTION; CELL STRUCTURE; CYTOARCHITECTURE; ENERGY METABOLISM; ENERGY TRANSFER; GLIA; GLYCOGEN METABOLISM; GLYCOLYSIS; HUMAN; NERVE CELL PLASTICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW;

ASTROCYTES; BRAIN; ENERGY METABOLISM; GLYCOGEN; LACTIC ACID; MODELS, BIOLOGICAL; NEURONS; OXIDATIVE STRESS; REGIONAL BLOOD FLOW;

EID: 82955168362     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2011.08.016     Document Type: Review

References (130)

1. E.K. Ainscow, S. Mirshamsi, T. Tang, M.L. Ashford, and G.A. Rutter Dynamic imaging of free cytosolic ATP concentration during fuel sensing by rat hypothalamic neurones: evidence for ATP-independent control of ATP-sensitive K(+) channels J. Physiol. 544 2002 429 445 (Pubitemid 35244260)
2. I. Allaman, M. Gavillet, M. Belanger, T. Laroche, D. Viertl, H.A. Lashuel, and P.J. Magistretti Amyloid-beta aggregates cause alterations of astrocytic metabolic phenotype: impact on neuronal viability J. Neurosci. 30 2010 3326 3338
3. I. Allaman, M. Belanger, and P.J. Magistretti Astrocyte-neuron metabolic relationships: for better and for worse Trends Neurosci. 34 2011 76 87
4. H. Alle, A. Roth, and J.R. Geiger Energy-efficient action potentials in hippocampal mossy fibers Science 325 2009 1405 1408
5. A. Almeida, J. Almeida, J.P. Bolanos, and S. Moncada Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically generated ATP in astrocyte protection Proc. Natl. Acad. Sci. USA 98 2001 15294 15299 (Pubitemid 34014008)
6. A. Almeida, S. Moncada, and J.P. Bolanos Nitric oxide switches on glycolysis through the AMP protein kinase and 6-phosphofructo-2-kinase pathway Nat. Cell Biol. 6 2004 45 51 (Pubitemid 38425729)
7. B.M. Ances, D.G. Buerk, J.H. Greenberg, and J.A. Detre Temporal dynamics of the partial pressure of brain tissue oxygen during functional forepaw stimulation in rats Neurosci. Lett. 306 2001 106 110 (Pubitemid 32524309)
8. D. Attwell, and S.B. Laughlin An energy budget for signaling in the grey matter of the brain J. Cereb. Blood Flow Metab. 21 2001 1133 1145 (Pubitemid 32947479)
9. D. Attwell, A.M. Buchan, S. Charpak, M. Lauritzen, B.A. MacVicar, and E.A. Newman Glial and neuronal control of brain blood flow Nature 468 2010 232 243
10. L.K. Bak, A. Schousboe, and H.S. Waagepetersen The glutamate/GABA- glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer J. Neurochem. 98 2006 641 653 (Pubitemid 44051266)
11. L.F. Barros, and J.W. Deitmer Glucose and lactate supply to the synapse Brain Res. Brain Res. Rev. 63 2010 149 159
12. L.F. Barros, R. Courjaret, P. Jakoby, A. Loaiza, C. Lohr, and J.W. Deitmer Preferential transport and metabolism of glucose in Bergmann glia over Purkinje cells: a multiphoton study of cerebellar slices Glia 57 2009 962 970
13. M. Belanger, and P.J. Magistretti The role of astroglia in neuroprotection Dialogues Clin. Neurosci. 11 2009 281 295
14. O. Ben Yoseph, P.A. Boxer, and B.D. Ross Assessment of the role of the glutathione and pentose phosphate pathways in the protection of primary cerebrocortical cultures from oxidative stress J. Neurochem. 66 1996 2329 2337 (Pubitemid 26159067)
15. D.A. Berkich, M.S. Ola, J. Cole, A.J. Sweatt, S.M. Hutson, and K.F. LaNoue Mitochondrial transport proteins of the brain J. Neurosci. Res. 85 2007 3367 3377 (Pubitemid 350058525)
16. Y. Bernardinelli, P.J. Magistretti, and J.Y. Chatton Astrocytes generate Na+-mediated metabolic waves Proc. Natl. Acad. Sci. USA 101 2004 14937 14942 (Pubitemid 39410778)
17. C.X. Bittner, A. Loaiza, I. Ruminot, V. Larenas, T. Sotelo-Hitschfeld, R. Gutierrez, A. Cordova, R. Valdebenito, W.B. Frommer, and L.F. Barros High resolution measurement of the glycolytic rate Front Neuroenergetics. 2 2010 26 10.3389/fnene.2010.00026
18. J.P. Bolanos, A. Almeida, and S. Moncada Glycolysis: a bioenergetic or a survival pathway? Trends Biochem. Sci. 35 2010 145 149
19. F. Boumezbeur, G.F. Mason, R.A. de Graaf, K.L. Behar, G.W. Cline, G.I. Shulman, D.L. Rothman, and K.F. Petersen Altered brain mitochondrial metabolism in healthy aging as assessed by in vivo magnetic resonance spectroscopy J. Cereb. Blood Flow Metab. 30 2010 211 221
20. F. Boumezbeur, K.F. Petersen, G.W. Cline, G.F. Mason, K.L. Behar, G.I. Shulman, and D.L. Rothman The contribution of blood lactate to brain energy metabolism in humans measured by dynamic 13C nuclear magnetic resonance spectroscopy J. Neurosci. 30 2010 13983 13991
21. A.K. Bouzier, E. Thiaudiere, M. Biran, R. Rouland, P. Canioni, and 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 (Pubitemid 30485428)
22. A.K. Bouzier-Sore, P. Voisin, V. Bouchaud, E. Bezancon, J.M. Franconi, and L. Pellerin Competition between glucose and lactate as oxidative energy substrates in both neurons and astrocytes: a comparative NMR study Eur. J. Neurosci. 24 2006 1687 1694 (Pubitemid 44427537)
23. G.A. Brooks Cell-cell and intracellular lactate shuttles J. Physiol. 587 2009 5591 5600
24. A.M. Brown Brain glycogen re-awakened J. Neurochem. 89 2004 537 552 (Pubitemid 38534140)
25. A.M. Brown, and B.R. Ransom Astrocyte glycogen and brain energy metabolism Glia 55 2007 1263 1271 (Pubitemid 47235367)
26. A.M. Brown, H.M. Sickmann, K. Fosgerau, T.M. Lund, A. Schousboe, H.S. Waagepetersen, and B.R. Ransom Astrocyte glycogen metabolism is required for neural activity during aglycemia or intense stimulation in mouse white matter J. Neurosci. Res. 79 2005 74 80 (Pubitemid 40116420)
27. J.D. Cahoy, B. Emery, A. Kaushal, L.C. Foo, J.L. Zamanian, K.S. Christopherson, Y. Xing, J.L. Lubischer, P.A. Krieg, and S.A. Krupenko A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function J. Neurosci. 28 2008 264 278
28. G. Carmignoto, and M. Gomez-Gonzalo The contribution of astrocyte signalling to neurovascular coupling Brain Res. Brain Res. Rev. 63 2010 138 148
29. M.A. Castro, F.A. Beltran, S. Brauchi, and I.I. Concha A metabolic switch in brain: glucose and lactate metabolism modulation by ascorbic acid J. Neurochem. 110 2009 423 440
30. S. Cerdan, T.B. Rodrigues, A. Sierra, M. Benito, L.L. Fonseca, C.P. Fonseca, and M.L. Garcia-Martin The redox switch/redox coupling hypothesis Neurochem. Int. 48 2006 523 530
31. Y. Chen, N.E. Vartiainen, W. Ying, P.H. Chan, J. Koistinaho, and R.A. Swanson Astrocytes protect neurons from nitric oxide toxicity by a glutathione-dependent mechanism J. Neurochem. 77 2001 1601 1610 (Pubitemid 32574495)
32. C.P. Chih, and E.L. Roberts Jr. Energy substrates for neurons during neural activity: a critical review of the astrocyte-neuron lactate shuttle hypothesis J. Cereb. Blood Flow Metab. 23 2003 1263 1281 (Pubitemid 37409789)
33. N. Cholet, L. Pellerin, E. Welker, P. Lacombe, J. Seylaz, P. Magistretti, and 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 (Pubitemid 32298887)
34. J. Chuquet, P. Quilichini, E.A. Nimchinsky, and G. Buzsaki Predominant enhancement of glucose uptake in astrocytes versus neurons during activation of the somatosensory cortex J. Neurosci. 30 2010 15298 15303
35. D.D. Clarke, and L. Sokoloff Circulation and energy metabolism of the brain G.J. Siegel, B.W. Agranoff, R.W. Albers, S.K. Fisher, M.D. Uhler, Basic Neurochemistry: Molecular, Cellular and Medical Aspects 1999 Lippincott-Raven New York 637 669
36. G.A. Dienel, K.K. Ball, and N.F. Cruz A glycogen phosphorylase inhibitor selectively enhances local rates of glucose utilization in brain during sensory stimulation of conscious rats: implications for glycogen turnover J. Neurochem. 102 2007 466 478 (Pubitemid 47000604)
37. M. DiNuzzo, S. Mangia, B. Maraviglia, and F. Giove Changes in glucose uptake rather than lactate shuttle take center stage in subserving neuroenergetics: evidence from mathematical modeling J. Cereb. Blood Flow Metab. 30 2010 586 602
38. R. Dringen Metabolism and functions of glutathione in brain Prog. Neurobiol. 62 2000 649 671 (Pubitemid 30407139)
39. R. Dringen, R. Gebhardt, and B. Hamprecht Glycogen in astrocytes: possible function as lactate supply for neighboring cells Brain Res. 623 1993 208 214 (Pubitemid 23275402)
40. J.S. Erlichman, A. Hewitt, T.L. Damon, M. Hart, J. Kurascz, A. Li, and J.C. Leiter Inhibition of Monocarboxylate Transporter 2 in the retrotrapezoid nucleus in rats: a test of the astrocyte-neuron lactate-shuttle hypothesis J. Neurosci. 28 2008 4888 4896
41. C.R. Figley, and P.W. Stroman The role(s) of astrocytes and astrocyte activity in neurometabolism, neurovascular coupling, and the production of functional neuroimaging signals Eur. J. Neurosci. 33 2011 577 588
42. P.T. Fox, and M.E. Raichle Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects Proc. Natl. Acad. Sci. USA 83 1986 1140 1144 (Pubitemid 16086428)
43. P.T. Fox, M.E. Raichle, M.A. Mintun, and C. Dence Nonoxidative glucose consumption during focal physiologic neural activity Science 241 1988 462 464
44. C.N. Gallagher, K.L. Carpenter, P. Grice, D.J. Howe, A. Mason, I. Timofeev, D.K. Menon, P.J. Kirkpatrick, J.D. Pickard, and G.R. Sutherland The human brain utilizes lactate via the tricarboxylic acid cycle: a 13C-labelled microdialysis and high-resolution nuclear magnetic resonance study Brain 132 2009 2839 2849
45. P. Garcia-Nogales, A. Almeida, and J.P. Bolanos Peroxynitrite protects neurons against nitric oxide-mediated apoptosis. A key role for glucose-6-phosphate dehydrogenase activity in neuroprotection J. Biol. Chem. 278 2003 864 874 (Pubitemid 36790760)
46. C. Genoud, C. Quairiaux, P. Steiner, H. Hirling, E. Welker, and G.W. Knott Plasticity of astrocytic coverage and glutamate transporter expression in adult mouse cortex PLoS Biol. 4 2006 e343 10.1371/journal.pbio.0040343 (Pubitemid 44760019)
47. C. Giaume, A. Koulakoff, L. Roux, D. Holcman, and N. Rouach Astroglial networks: a step further in neuroglial and gliovascular interactions Nat. Rev. Neurosci. 11 2010 87 99
48. M.E. Gibbs, D.G. Anderson, and L. Hertz Inhibition of glycogenolysis in astrocytes interrupts memory consolidation in young chickens Glia 54 2006 214 222 (Pubitemid 44230858)
49. G.R. Gordon, H.B. Choi, R.L. Rungta, G.C. Ellis-Davies, and B.A. MacVicar Brain metabolism dictates the polarity of astrocyte control over arterioles Nature 456 2008 745 749
50. D.A. Gusnard, and M.E. Raichle Searching for a baseline: functional imaging and the resting human brain Nat. Rev. Neurosci. 2 2001 685 694 (Pubitemid 33674814)
51. M.M. Halassa, T. Fellin, H. Takano, J.H. Dong, and P.G. Haydon Synaptic islands defined by the territory of a single astrocyte J. Neurosci. 27 2007 6473 6477 (Pubitemid 46920364)
52. N.D. Halim, T. Mcfate, A. Mohyeldin, P. Okagaki, L.G. Korotchkina, M.S. Patel, N.H. Jeoung, R.A. Harris, M.J. Schell, and A. Verma Phosphorylation status of pyruvate dehydrogenase distinguishes metabolic phenotypes of cultured rat brain astrocytes and neurons Glia 58 2010 1168 1176
53. T. Hashimoto, R. Hussien, H.S. Cho, D. Kaufer, and G.A. Brooks Evidence for the mitochondrial lactate oxidation complex in rat neurons: demonstration of an essential component of brain lactate shuttles PLoS ONE 3 2008 e2915 10.1371/journal.pone.0002915
54. A.S. Herard, A. Dubois, C. Escartin, K. Tanaka, T. Delzescaux, P. Hantraye, and G. Bonvento Decreased metabolic response to visual stimulation in the superior colliculus of mice lacking the glial glutamate transporter GLT-1 Eur. J. Neurosci. 22 2005 1807 1811 (Pubitemid 41482970)
55. A. Herrero-Mendez, A. Almeida, E. Fernandez, C. Maestre, S. Moncada, and J.P. Bolanos The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C-Cdh1 Nat. Cell Biol. 11 2009 747 752
56. Y. Hu, and G.S. Wilson A temporary local energy pool coupled to neuronal activity: fluctuations of extracellular lactate levels in rat brain monitored with rapid-response enzyme-based sensor J. Neurochem. 69 1997 1484 1490 (Pubitemid 27406949)
57. F. Hyder, A.B. Patel, A. Gjedde, D.L. Rothman, K.L. Behar, and R.G. Shulman Neuronal-glial glucose oxidation and glutamatergic-GABAergic function J. Cereb. Blood Flow Metab. 26 2006 865 877 (Pubitemid 43980402)
58. C. Iadecola, and M. Nedergaard Glial regulation of the cerebral microvasculature Nat. Neurosci. 10 2007 1369 1376 (Pubitemid 350014688)
59. Y. Itoh, T. Esaki, K. Shimoji, M. Cook, M.J. Law, E. Kaufman, and L. Sokoloff Dichloroacetate effects on glucose and lactate oxidation by neurons and astroglia in vitro and on glucose utilization by brain in vivo Proc. Natl. Acad. Sci. USA 100 2003 4879 4884 (Pubitemid 36457822)
60. R. Jolivet, I. Allaman, L. Pellerin, P.J. Magistretti, and B. Weber Comment on recent modeling studies of astrocyte-neuron metabolic interactions J. Cereb. Blood Flow Metab. 30 2010 1982 1986
61. K. Kacem, P. Lacombe, J. Seylaz, and G. Bonvento Structural organization of the perivascular astrocyte endfeet and their relationship with the endothelial glucose transporter: a confocal microscopy study Glia 23 1998 1 10 (Pubitemid 28174041)
62. K.A. Kasischke, H.D. Vishwasrao, P.J. Fisher, W.R. Zipfel, and W.W. Webb Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis Science 305 2004 99 103 (Pubitemid 38869381)
63. K.A. Kasischke, E.M. Lambert, B. Panepento, A. Sun, H.A. Gelbard, R.W. Burgess, T.H. Foster, and M. Nedergaard Two-photon NADH imaging exposes boundaries of oxygen diffusion in cortical vascular supply regions J. Cereb. Blood Flow Metab. 31 2011 68 81
64. T.K. Lam, R. Gutierrez-Juarez, A. Pocai, and L. Rossetti Regulation of blood glucose by hypothalamic pyruvate metabolism Science 309 2005 943 947 (Pubitemid 41099933)
65. C.K. Lam, M. Chari, and T.K. Lam CNS regulation of glucose homeostasis Physiology (Bethesda) 24 2009 159 170
66. J.D. Laughton, P. Bittar, Y. Charnay, L. Pellerin, E. Kovari, P.J. Magistretti, and C. Bouras Metabolic compartmentalization in the human cortex and hippocampus: evidence for a cell- and region-specific localization of lactate dehydrogenase 5 and pyruvate dehydrogenase BMC Neurosci. 8 2007 35 10.1186/1471-2202-8-35 (Pubitemid 46995053)
67. V. Lebon, K.F. Petersen, G.W. Cline, J. Shen, G.F. Mason, S. Dufour, K.L. Behar, G.I. Shulman, and D.L. Rothman Astroglial contribution to brain energy metabolism in humans revealed by 13C nuclear magnetic resonance spectroscopy: elucidation of the dominant pathway for neurotransmitter glutamate repletion and measurement of astrocytic oxidative metabolism J. Neurosci. 22 2002 1523 1531 (Pubitemid 35386271)
68. A.L. Lin, P.T. Fox, J. Hardies, T.Q. Duong, and J.H. Gao Nonlinear coupling between cerebral blood flow, oxygen consumption, and ATP production in human visual cortex Proc. Natl. Acad. Sci. USA 107 2010 8446 8451
69. D. Lovatt, U. Sonnewald, H.S. Waagepetersen, A. Schousboe, W. He, J.H. Lin, X. Han, T. Takano, S. Wang, and F.J. Sim The transcriptome and metabolic gene signature of protoplasmic astrocytes in the adult murine cortex J. Neurosci. 27 2007 12255 12266 (Pubitemid 350085462)
70. P.J. Magistretti Brain energy metabolism L.R. Squire, D. Berg, F.E. Bloom, S. du Lac, A. Ghosh, N.C. Spitzer, Fundamental Neuroscience 2008 Academic Press San Diego 271 293
71. P.J. Magistretti Role of glutamate in neuron-glia metabolic coupling Am. J. Clin. Nutr. 90 2009 875S 880S
72. P.J. Magistretti, and J.Y. Chatton Relationship between L-glutamate-regulated intracellular Na+ dynamics and ATP hydrolysis in astrocytes J. Neural Transm. 112 2005 77 85 (Pubitemid 40104718)
73. P.J. Magistretti, and L. Pellerin Cellular bases of brain energy metabolism and their relevance to functional brain imaging: evidence for a prominent role of astrocytes Cereb. Cortex 6 1996 50 61
74. P.J. Magistretti, J.H. Morrison, W.J. Shoemaker, V. Sapin, and F.E. Bloom Vasoactive intestinal polypeptide induces glycogenolysis in mouse cortical slices: a possible regulatory mechanism for the local control of energy metabolism Proc. Natl. Acad. Sci. USA 78 1981 6535 6539 (Pubitemid 12208177)
75. P.J. Magistretti, M. Manthorpe, F.E. Bloom, and S. Varon Functional receptors for vasoactive intestinal polypeptide in cultured astroglia from neonatal rat brain Regul. Pept. 6 1983 71 80 (Pubitemid 13042596)
76. P.J. Magistretti, O. Sorg, and J.L. Martin Regulation of glycogen metabolism in astrocytes: physiological, pharmacological, and pathological aspects S. Murphy, Astrocytes: Pharmacology and Function 1993 Academic Press San Diego 243 265
77. S. Mangia, G. Garreffa, M. Bianciardi, F. Giove, F. Di Salle, and B. Maraviglia The aerobic brain: lactate decrease at the onset of neural activity Neuroscience 118 2003 7 10 (Pubitemid 36369524)
78. S. Mangia, I.A. Simpson, S.J. Vannucci, and A. Carruthers The in vivo neuron-to-astrocyte lactate shuttle in human brain: evidence from modeling of measured lactate levels during visual stimulation J. Neurochem. 109 Suppl 1 2009 55 62
79. M.C. McKenna The glutamate-glutamine cycle is not stoichiometric: fates of glutamate in brain J. Neurosci. Res. 85 2007 3347 3358 (Pubitemid 350058523)
80. M.R. Metea, and E.A. Newman Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling J. Neurosci. 26 2006 2862 2870
81. L. Mosconi, A. Pupi, and M.J. de Leon Brain glucose hypometabolism and oxidative stress in preclinical Alzheimer's disease Ann. N Y Acad. Sci. 1147 2008 180 195
82. J. Mozrzymas, T. Szczesny, and D. Rakus The effect of glycogen phosphorolysis on basal glutaminergic transmission Biochem. Biophys. Res. Commun. 404 2011 652 655
83. S.J. Mulligan, and B.A. MacVicar Calcium transients in astrocyte endfeet cause cerebrovascular constrictions Nature 431 2004 195 199 (Pubitemid 39243473)
84. M. Nedergaard, B. Ransom, and S.A. Goldman New roles for astrocytes: redefining the functional architecture of the brain Trends Neurosci. 26 2003 523 530 (Pubitemid 37176906)
85. A. Nehlig Brain uptake and metabolism of ketone bodies in animal models Prostaglandins Leukot. Essent. Fatty Acids 70 2004 265 275 (Pubitemid 38200953)
86. A. Nehlig, E. Wittendorp-Rechenmann, and C.D. Lam Selective uptake of [14C]2-deoxyglucose by neurons and astrocytes: high-resolution microautoradiographic imaging by cellular 14C-trajectography combined with immunohistochemistry J. Cereb. Blood Flow Metab. 24 2004 1004 1014 (Pubitemid 39223624)
87. N.A. Oberheim, X. Wang, S. Goldman, and M. Nedergaard Astrocytic complexity distinguishes the human brain Trends Neurosci. 29 2006 547 553 (Pubitemid 44416461)
88. N.A. Oberheim, T. Takano, X. Han, W. He, J.H. Lin, F. Wang, Q. Xu, J.D. Wyatt, W. Pilcher, and J.G. Ojemann Uniquely hominid features of adult human astrocytes J. Neurosci. 29 2009 3276 3287
89. N. Offenhauser, K. Thomsen, K. Caesar, and M. Lauritzen Activity-induced tissue oxygenation changes in rat cerebellar cortex: interplay of postsynaptic activation and blood flow J. Physiol. 565 2005 279 294 (Pubitemid 40723709)
90. S. Ogawa, D.W. Tank, R. Menon, J.M. Ellermann, S.G. Kim, H. Merkle, and K. Ugurbil Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging Proc. Natl. Acad. Sci. USA 89 1992 5951 5955
91. M.P. Parsons, and M. Hirasawa ATP-sensitive potassium channel-mediated lactate effect on orexin neurons: implications for brain energetics during arousal J. Neurosci. 30 2010 8061 8070
92. L. Pellerin, and 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 (Pubitemid 24329051)
93. L. Pellerin, A.K. Bouzier-Sore, A. Aubert, S. Serres, M. Merle, R. Costalat, and P.J. Magistretti Activity-dependent regulation of energy metabolism by astrocytes: an update Glia 55 2007 1251 1262 (Pubitemid 47235366)
94. O.H. Porras, A. Loaiza, and L.F. Barros Glutamate mediates acute glucose transport inhibition in hippocampal neurons J. Neurosci. 24 2004 9669 9673 (Pubitemid 39441521)
95. J. Prichard, D. Rothman, E. Novotny, O. Petroff, T. Kuwabara, M. Avison, A. Howseman, C. Hanstock, and R. Shulman Lactate rise detected by 1H NMR in human visual cortex during physiologic stimulation Proc. Natl. Acad. Sci. USA 88 1991 5829 5831 (Pubitemid 21914839)
96. H. Qu, A. Haberg, O. Haraldseth, G. Unsgard, and U. Sonnewald (13)C MR spectroscopy study of lactate as substrate for rat brain Dev. Neurosci. 22 2000 429 436
97. M.E. Raichle, and M.A. Mintun Brain work and brain imaging Annu. Rev. Neurosci. 29 2006 449 476 (Pubitemid 44476853)
98. M. Ramos, A. del Arco, B. Pardo, A. Martinez-Serrano, J.R. Martinez-Morales, K. Kobayashi, T. Yasuda, E. Bogonez, P. Bovolenta, and T. Saheki Developmental changes in the Ca2+-regulated mitochondrial aspartate-glutamate carrier aralar1 in brain and prominent expression in the spinal cord Brain Res. Dev. Brain Res. 143 2003 33 46 (Pubitemid 36603318)
99. N. Rouach, A. Koulakoff, V. Abudara, K. Willecke, and C. Giaume Astroglial metabolic networks sustain hippocampal synaptic transmission Science 322 2008 1551 1555
100. S. Schmidt, M. Richter, D. Montag, T. Sartorius, V. Gawlik, A.M. Hennige, S. Scherneck, H. Himmelbauer, S.Z. Lutz, and R. Augustin Neuronal functions, feeding behavior, and energy balance in Slc2a3+/- mice Am. J. Physiol. Endocrinol. Metab. 295 2008 E1084 E1094
101. A. Schurr, and R.S. Payne Lactate, not pyruvate, is neuronal aerobic glycolysis end product: an in vitro electrophysiological study Neuroscience 147 2007 613 619 (Pubitemid 46992819)
102. A. Schurr, R.S. Payne, J.J. Miller, and 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 (Pubitemid 27274200)
103. A. Schurr, J.J. Miller, R.S. Payne, and 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 (Pubitemid 29028946)
104. S. Serres, E. Bezancon, J.M. Franconi, and M. Merle Ex vivo NMR study of lactate metabolism in rat brain under various depressed states J. Neurosci. Res. 79 2005 19 25 (Pubitemid 40116413)
105. A.Y. Shih, D.A. Johnson, G. Wong, A.D. Kraft, L. Jiang, H. Erb, J.A. Johnson, and T.H. Murphy Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress J. Neurosci. 23 2003 3394 3406 (Pubitemid 36531981)
106. H. Shimizu, E. Watanabe, T.Y. Hiyama, A. Nagakura, A. Fujikawa, H. Okado, Y. Yanagawa, K. Obata, and M. Noda Glial Na(x) channels control lactate signaling to neurons for brain [Na+] sensing Neuron 54 2007 59 72 (Pubitemid 46498695)
107. R.G. Shulman, D.L. Rothman, K.L. Behar, and F. Hyder Energetic basis of brain activity: implications for neuroimaging Trends Neurosci. 27 2004 489 495 (Pubitemid 38951042)
108. N.R. Sibson, J. Shen, G.F. Mason, D.L. Rothman, K.L. Behar, and R.G. Shulman Functional energy metabolism: in vivo 13C-NMR spectroscopy evidence for coupling of cerebral glucose consumption and glutamatergic neuronal activity Dev. Neurosci. 20 1998 321 330 (Pubitemid 28495526)
109. H.M. Sickmann, A.B. Walls, A. Schousboe, S.D. Bouman, and H.S. Waagepetersen Functional significance of brain glycogen in sustaining glutamatergic neurotransmission J. Neurochem. 109 Suppl 1 2009 80 86
110. I.A. Simpson, A. Carruthers, and S.J. Vannucci Supply and demand in cerebral energy metabolism: the role of nutrient transporters J. Cereb. Blood Flow Metab. 27 2007 1766 1791 (Pubitemid 47624552)
111. D. Smith, A. Pernet, W.A. Hallett, E. Bingham, P.K. Marsden, and S.A. Amiel Lactate: a preferred fuel for human brain metabolism in vivo J. Cereb. Blood Flow Metab. 23 2003 658 664 (Pubitemid 36713670)
112. 14C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat J. Neurochem. 28 1977 897 916 (Pubitemid 8098854)
113. C.A. Stuart, I.R. Ross, M.E. Howell, M.P. McCurry, T.G. Wood, J.D. Ceci, S.J. Kennel, and J. Wall Brain glucose transporter (Glut3) haploinsufficiency does not impair mouse brain glucose uptake Brain Res. 1384 2011 15 22
114. A. Suzuki, S.A. Stern, O. Bozdagi, G.W. Huntley, R.H. Walker, P.J. Magistretti, and C.M. Alberini Astrocyte-neuron lactate transport is required for long-term memory formation Cell 144 2011 810 823
115. R.A. Swanson, M.M. Morton, S.M. Sagar, and F.R. Sharp Sensory stimulation induces local cerebral glycogenolysis: demonstration by autoradiography Neuroscience 51 1992 451 461
116. T. Takano, G.F. Tian, W. Peng, N. Lou, W. Libionka, X. Han, and M. Nedergaard Astrocyte-mediated control of cerebral blood flow Nat. Neurosci. 9 2006 260 267 (Pubitemid 43164550)
117. A. Tarasov, J. Dusonchet, and F. Ashcroft Metabolic regulation of the pancreatic beta-cell ATP-sensitive K+ channel: a pas de deux Diabetes 53 Suppl 3 2004 S113 S122
118. S.B. Tekkok, A.M. Brown, R. Westenbroek, L. Pellerin, and B.R. Ransom Transfer of glycogen-derived lactate from astrocytes to axons via specific monocarboxylate transporters supports mouse optic nerve activity J. Neurosci. Res. 81 2005 644 652 (Pubitemid 41532160)
119. N. Tsujino, and T. Sakurai Orexin/hypocretin: a neuropeptide at the interface of sleep, energy homeostasis, and reward system Pharmacol. Rev. 61 2009 162 176
120. G. van Hall, M. Stromstad, P. Rasmussen, O. Jans, M. Zaar, C. Gam, B. Quistorff, N.H. Secher, and H.B. Nielsen Blood lactate is an important energy source for the human brain J. Cereb. Blood Flow Metab. 29 2009 1121 1129
121. M.R. Vargas, and J.A. Johnson The Nrf2-ARE cytoprotective pathway in astrocytes Expert Rev. Mol. Med. 11 2009 e17 10.1017/S1462399409001094
122. D. Vilchez, S. Ros, D. Cifuentes, L. Pujadas, J. Valles, B. Garcia-Fojeda, O. Criado-Garcia, E. Fernandez-Sanchez, I. Medrano-Fernandez, and J. Dominguez Mechanism suppressing glycogen synthesis in neurons and its demise in progressive myoclonus epilepsy Nat. Neurosci. 10 2007 1407 1413 (Pubitemid 350014686)
123. A. Volterra, and J. Meldolesi Astrocytes, from brain glue to communication elements: the revolution continues Nat. Rev. Neurosci. 6 2005 626 640 (Pubitemid 41059337)
124. B. Voutsinos-Porche, G. Bonvento, K. Tanaka, P. Steiner, E. Welker, J.Y. Chatton, P.J. Magistretti, and L. Pellerin Glial glutamate transporters mediate a functional metabolic crosstalk between neurons and astrocytes in the mouse developing cortex Neuron 37 2003 275 286 (Pubitemid 36143822)
125. A.B. Walls, C.M. Heimburger, S.D. Bouman, A. Schousboe, and H.S. Waagepetersen Robust glycogen shunt activity in astrocytes: effects of glutamatergic and adrenergic agents Neuroscience 158 2009 284 292
126. D. Wang, J.M. Pascual, H. Yang, K. Engelstad, X. Mao, J. Cheng, J. Yoo, J.L. Noebels, and D.C. De Vivo A mouse model for Glut-1 haploinsufficiency Hum. Mol. Genet. 15 2006 1169 1179
127. J.X. Wilson Antioxidant defense of the brain: a role for astrocytes Can. J. Physiol. Pharmacol. 75 1997 1149 1163 (Pubitemid 28033933)
128. M.R. Witcher, S.A. Kirov, and K.M. Harris Plasticity of perisynaptic astroglia during synaptogenesis in the mature rat hippocampus Glia 55 2007 13 23 (Pubitemid 44845505)
129. H.R. Zielke, C.L. Zielke, and P.J. Baab Direct measurement of oxidative metabolism in the living brain by microdialysis: a review J. Neurochem. 109 Suppl 1 2009 24 29
130. M. Zonta, M.C. Angulo, S. Gobbo, B. Rosengarten, K.A. Hossmann, T. Pozzan, and G. Carmignoto Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation Nat. Neurosci. 6 2003 43 50 (Pubitemid 36026331)