Bioenergetics and redox adaptations of astrocytes to neuronal activity

Journal of Neurochemistry

Volumn 139, Issue , 2016, Pages 115-125

  Bolaños, Juan P ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

AMPK; Cdh1; Glycolysis; GSH; Nrf2; PFKFB3

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); GLUCOSE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUTATHIONE; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TRANSCRIPTOME; TRICARBOXYLIC ACID;

ARTICLE; ASTROCYTE; BIOENERGY; CALCIUM TRANSPORT; CELL FATE; CELL METABOLISM; CELL SURVIVAL; ENERGY METABOLISM; EXCITOTOXICITY; GLYCOLYSIS; HUMAN; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE FUNCTION; NEUROTRANSMISSION; OXIDATION REDUCTION REACTION; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION; ANIMAL; BRAIN; METABOLISM; NERVE CELL; PHYSIOLOGY; SYNAPSE;

ANIMALS; ASTROCYTES; BRAIN; ENERGY METABOLISM; HUMANS; NEURONS; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; SYNAPSES;

EID: 84960539010     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13486     Document Type: Article

References (121)

1. Allaman I., Belanger M. and Magistretti P. J. (2011) Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci. 34, 76–87.
2. Allen N. J. and Barres B. A. (2009) Neuroscience: Glia - more than just brain glue. Nature 457, 675–677.
3. Almeida A. and Bolaños J. P. (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., Almeida J., Bolaños J. P. and Moncada S. (2001) Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically-generated ATP in astrocyte protection. Proc. Natl Acad. Sci. USA 98, 15294–15299.
5. Almeida A., Moncada S. and Bolaños J. P. (2004) Nitric oxide switches on glycolysis through the AMP protein kinase and 6-phosphofructo-2-kinase pathway. Nat. Cell Biol. 6, 45–51.
6. Almeida A., Bolaños J. P. and Moreno S. (2005) Cdh1/Hct1-APC is essential for the survival of postmitotic neurons. J. Neurosci. 25, 8115–8121.
7. Bak L. K., Schousboe A., Sonnewald U. and Waagepetersen H. S. (2006) Glucose is necessary to maintain neurotransmitter homeostasis during synaptic activity in cultured glutamatergic neurons. J. Cereb. Blood Flow Metab. 26, 1285–1297.
8. 2+ levels. J. Neurochem. 109(Suppl 1), 87–93.
9. 2+ signalling in cultured mouse glutamatergic neurons. ASN Neuro. 4, e00083.
10. 2+ exchanger in excitotoxicity. Cell 120, 275–285.
11. Barros L. F. (2013) Metabolic signaling by lactate in the brain. Trends Neurosci. 36, 396–404.
12. Baxter P. S., Bell K. F., Hasel P., Kaindl A. M., Fricker M., Thomson D., Cregan S. P., Gillingwater T. H. and Hardingham G. E. (2015) Synaptic NMDA receptor activity is coupled to the transcriptional control of the glutathione system. Nat. Commun. 6, 6761.
13. Bell K. F., Al-Mubarak B., Fowler J. H. et al. (2011) Mild oxidative stress activates Nrf2 in astrocytes, which contributes to neuroprotective ischemic preconditioning. Proc. Natl Acad. Sci. USA 108, E1–E2.
14. Bell K. F., Al-Mubarak B., Martel M. A. et al. (2015) Neuronal development is promoted by weakened intrinsic antioxidant defences due to epigenetic repression of Nrf2. Nat. Commun. 6, 7066.
15. Beltran B., Mathur A., Duchen M. R., Erusalimsky J. D. and Moncada S. (2000) The effect of nitric oxide on cell respiration: a key to understanding its role in cell survival or death. Proc. Natl Acad. Sci. USA 97, 14602–14607.
16. Ben-Yoseph O., Boxer P. A. and Ross B. D. (1996) Assessment of the role of the glutathione and pentose phosphate pathways in the protection of primary cerebrocortical cultures from oxidative stress. J. Neurochem. 66, 2329–2337.
17. + and a delayed and persistent effect of glutamate. J. Neurosci. 31, 4709–4713.
18. Bockaert J. and Marin P. (2015) mTOR in Brain Physiology and Pathologies. Physiol. Rev. 95, 1157–1187.
19. Bolaños J. P., Peuchen S., Heales S. J. R., Land J. M. and Clark J. B. (1994) Nitric oxide-mediated inhibition of the mitochondrial respiratory chain in cultured astrocytes. J. Neurochem. 63, 910–916.
20. Bolaños J. P., Heales S. J. R., Land J. M. and Clark J. B. (1995) Effect of peroxynitrite on the mitochondrial respiratory chain: differential susceptibility of neurones and astrocytes in primary cultures. J. Neurochem. 64, 1965–1972.
21. Bolaños J. P., Heales S. J. R., Peuchen S., Barker J. E., Land J. M. and Clark J. B. (1996) Nitric oxide-mediated mitochondrial damage: a potential neuroprotective role for glutathione. Free Radic. Biol. Med. 21, 995–1001.
22. Bolaños J. P., Almeida A. and Moncada S. (2010) Glycolysis: a bioenergetic or a survival pathway?. Trends Biochem. Sci. 35, 145–149.
23. Bouzier-Sore A. K. and Bolanos J. P. (2015) Uncertainties in pentose-phosphate pathway flux assessment underestimate its contribution to neuronal glucose consumption: relevance for neurodegeneration and aging. Front. Aging Neurosci. 7, 89.
24. Bouzier-Sore A. K., Voisin P., Canioni P., Magistretti P. J. and Pellerin L. (2003) Lactate is a preferential oxidative energy substrate over glucose for neurons in culture. J. Cereb. Blood Flow Metab. 23, 1298–1306.
25. Bouzier-Sore A. K., Voisin P., Bouchaud V., Bezancon E., Franconi J. M. and Pellerin L. (2006) Competition between glucose and lactate as oxidative energy substrates in both neurons and astrocytes: a comparative NMR study. Eur. J. Neurosci. 24, 1687–1694.
26. Bringmann A., Pannicke T., Biedermann B., Francke M., Iandiev I., Grosche J., Wiedemann P., Albrecht J. and Reichenbach A. (2009) Role of retinal glial cells in neurotransmitter uptake and metabolism. Neurochem. Int. 54, 143–160.
27. Brix B., Mesters J. R., Pellerin L. and Johren O. (2012) Endothelial cell-derived nitric oxide enhances aerobic glycolysis in astrocytes via HIF-1alpha-mediated target gene activation. J. Neurosci. 32, 9727–9735.
28. Brown G. C. and Cooper C. E. (1994) Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett. 356, 295–298.
29. Brown A. M. and Ransom B. R. (2007) Astrocyte glycogen and brain energy metabolism. Glia 55, 1263–1271.
30. 2+ exchanger degradation occur downstream of calcium deregulation in hippocampal neurons exposed to excitotoxic glutamate. J. Neurosci. Res. 88, 1317–1328.
31. 2+ homeostasis. J. Neurochem. 66, 403–411.
32. Cai Q. and Sheng Z. H. (2009) Molecular motors and synaptic assembly. Neuroscientist 15, 78–89.
33. Choi D. W. (1987) Ionic dependence of glutamate neurotoxicity in cortical cell culture. J. Neurosci. 7, 369–379.
34. Choi S. W., Gerencser A. A. and Nicholls D. G. (2009) Bioenergetic analysis of isolated cerebrocortical nerve terminals on a microgram scale: spare respiratory capacity and stochastic mitochondrial failure. J. Neurochem. 109, 1179–1191.
35. Cleeter M. W. J., Cooper J. M., Darley-Usmar V. M., Moncada S. and Schapira A. H. (1994) Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett. 345, 50–54.
36. Conti F., DeBiasi S., Minelli A. and Melone M. (1996) Expression of NR1 and NR2A/B subunits of the NMDA receptor in cortical astrocytes. Glia 17, 254–258.
37. Deighton R. F., Markus N. M., Al-Mubarak B., Bell K. F., Papadia S., Meakin P. J., Chowdhry S., Hayes J. D. and Hardingham G. E. (2014) Nrf2 target genes can be controlled by neuronal activity in the absence of Nrf2 and astrocytes. Proc. Natl Acad. Sci. USA 111, E1818–E1820.
38. Delgado-Esteban M., Almeida A. and Bolaños J. P. (2000) D-Glucose prevents glutathione oxidation and mitochondrial damage after glutamate receptor stimulation in rat cortical primary neurons. J. Neurochem. 75, 1618–1624.
39. Delgado-Esteban M., Garcia-Higuera I., Maestre C., Moreno S. and Almeida A. (2013) APC/C-Cdh1 coordinates neurogenesis and cortical size during development. Nat. Commun. 4, 2879.
40. Dringen R., Pfeiffer B. and Hamprecht B. (1999) Synthesis of the antioxidant glutathione in neurons: supply by astrocytes of CysGly as precursor for neuronal glutathione. J. Neurosci. 19, 562–569.
41. Duran J. and Guinovart J. J. (2015) Brain glycogen in health and disease. Mol. Aspects Med. 46, 70–77. doi: 10.1016/j.mam.2015.08.007.
42. Eggleston L. V. and Krebs H. A. (1974) Regulation of the pentose phosphate cycle. Biochem. J. 138, 425–435.
43. +)-ATPase pump. Biochem. J. 460, 353–361.
44. Ferreira I. L., Cunha-Oliveira T., Nascimento M. V., Ribeiro M., Proenca M. T., Januario C., Oliveira C. R. and Rego A. C. (2011) Bioenergetic dysfunction in Huntington's disease human cybrids. Exp. Neurol. 231, 127–134.
45. Fox P. T. and Raichle M. E. (1986) Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc. Natl Acad. Sci. USA 83, 1140–1144.
46. Fu W., Shi D., Westaway D. and Jhamandas J. H. (2015) Bioenergetic mechanisms in astrocytes may contribute to amyloid plaque deposition and toxicity. J. Biol. Chem. 290, 12504–12513.
47. Garcia O., Almeida A., Massieu L. and Bolaños J. P. (2005) Increased mitochondrial respiration maintains the mitochondrial membrane potential and promotes survival of cerebellar neurons in an endogenous model of glutamate receptor activation. J. Neurochem. 92, 183–190.
48. Garcia-Higuera I., Manchado E., Dubus P., Canamero M., Mendez J., Moreno S. and Malumbres M. (2008) Genomic stability and tumour suppression by the APC/C cofactor Cdh1. Nat. Cell Biol. 10, 802–811.
49. Garcia-Nogales P., Almeida A. and Bolaños J. P. (2003) Peroxynitrite protects neurons against nitric oxide-mediated apoptosis. A key role for glucose-6-phosphate dehydrogenase activity in neuroprotection. J. Biol. Chem. 278, 864–874.
50. Garthwaite J., Charles S. L. and Chess-Williams R. (1988) Endothelium-derived relaxing factor release on activation of NMDA receptors suggests a role as intercellular messenger in the brain. Nature 336, 385–387.
51. i and mitochondrial membrane potential in glutamate toxicity. J. Neurochem. 109, 644–655.
52. Habas A., Hahn J., Wang X. and Margeta M. (2013) Neuronal activity regulates astrocytic Nrf2 signaling. Proc. Natl Acad. Sci. USA 110, 18291–18296.
53. Harmey D., Smith A., Simanski S., Moussa C. Z. and Ayad N. G. (2009) The anaphase promoting complex induces substrate degradation during neuronal differentiation. J. Biol. Chem. 284, 4317–4323.
54. Haskew-Layton R. E., Payappilly J. B., Smirnova N. A. et al. (2010) Controlled enzymatic production of astrocytic hydrogen peroxide protects neurons from oxidative stress via an Nrf2-independent pathway. Proc. Natl Acad. Sci. USA 107, 17385–17390.
55. Herrero-Mendez A., Almeida A., Fernandez E., Maestre C., Moncada S. and Bolaños J. P. (2009) 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, 747–752.
56. Hertz L., Peng L. and Dienel G. A. (2007) Energy metabolism in astrocytes: high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. J. Cereb. Blood Flow Metab. 27, 219–249.
57. Huynh M. A., Stegmuller J., Litterman N. and Bonni A. (2009) Regulation of Cdh1-APC function in axon growth by Cdh1 phosphorylation. J. Neurosci. 29, 4322–4327.
58. Ivanov A. I., Malkov A. E., Waseem T., Mukhtarov M., Buldakova S., Gubkina O., Zilberter M. and Zilberter Y. (2014) Glycolysis and oxidative phosphorylation in neurons and astrocytes during network activity in hippocampal slices. J. Cereb. Blood Flow Metab. 34, 397–407.
59. Jekabsons M. B. and Nicholls D. G. (2004) In situ respiration and bioenergetic status of mitochondria in primary cerebellar granule neuronal cultures exposed continuously to glutamate. J. Biol. Chem. 279, 32989–33000.
60. Jimenez-Blasco D., Santofimia-Castano P., Gonzalez A., Almeida A. and Bolaños J. P. (2015) Astrocyte NMDA receptors’ activity sustains neuronal survival through a Cdk5-Nrf2 pathway. Cell Death Differ. 22, 1877–1889.
61. Kasparov S. (2016) Are Astrocytes the Pressure-Reservoirs of Lactate in the Brain? (2016) Cell Metabolism, http://dx.doi.org/10.1016/j.cmet.2015.11.001
62. Kauppinen R. A. and Nicholls D. G. (1986) Failure to maintain glycolysis in anoxic nerve terminals. J. Neurochem. 47, 1864–1869.
63. Knott A. B., Perkins G., Schwarzenbacher R. and Bossy-Wetzel E. (2008) Mitochondrial fragmentation in neurodegeneration. Nat. Rev. Neurosci. 9, 505–518.
64. Konishi Y., Stegmuller J., Matsuda T., Bonni S. and Bonni A. (2004) Cdh1-APC controls axonal growth and patterning in the mammalian brain. Science 303, 1026–1030.
65. Lage R., Dieguez C., Vidal-Puig A. and Lopez M. (2008) AMPK: a metabolic gauge regulating whole-body energy homeostasis. Trends Mol. Med. 14, 539–549.
66. Lee M., Ting K., Adams S., Brew B., Chung R. and Guillemin G. (2010) Characterisation of the expression of NMDA receptors in human astrocytes. PLoS ONE 30, e14123.
67. + triggers the release of astrocytic lactate via mitochondrial pyruvate shunting. Proc. Natl Acad. Sci. USA 112, 11090–11095.
68. Loaiza A., Porras O. H. and Barros L. F. (2003) Glutamate triggers rapid glucose transport stimulation in astrocytes as evidenced by real-time confocal microscopy. J. Neurosci. 23, 7337–7342.
69. Luetjens C. M., Bui N. T., Sengpiel B., Munstermann G., Poppe M., Krohn A. J., Bauerbach E., Krieglstein J. and Prehn J. H. (2000) Delayed mitochondrial dysfunction in excitotoxic neuron death: cytochrome c release and a secondary increase in superoxide production. J. Neurosci. 20, 5715–5723.
70. Lundgaard I., Li B., Xie L. et al. (2015) Direct neuronal glucose uptake Heralds activitydependent increases incerebral metabolism. Nat. Commun. 6, 6807.
71. Maechler P., Wyss M. T., Elsayed M., Stobart J., Gutierrez R., von Faber-Castell A., Kaelin V., Zuend M., San Martin A., Romero-Gomez I., Baeza-Lehnert F., Lengacher S., Schneider B. L., Aebischer P., Magistretti P. J., Barros L. F. and Weber B. (2016) In Vivo Evidence for a Lactate Gradient from Astrocytes to Neurons. Cell Metabolism, http://dx.doi.org/10.1016/j.cmet.2015.10.010
72. Maestre C., Delgado-Esteban M., Gomez-Sanchez J. C., Bolaños J. P. and Almeida A. (2008) Cdk5 phosphorylates Cdh1 and modulates cyclin B1 stability in excitotoxicity. EMBO J. 27, 2736–2745.
73. Magistretti P. J. (2006) Neuron-glia metabolic coupling and plasticity. J. Exp. Biol. 209, 2304–2311.
74. Magistretti P. J. and Allaman I. (2015) A cellular perspective on brain energy metabolism and functional imaging. Neuron 86, 883–901.
75. Makar T. K., Nedergaard M., Preuss A., Gelbard A. S., Perumal A. S. and Cooper A. J. L. (1994) Vitamin E, ascorbate, glutathione, glutathione disulfide, and enzymes of glutathione metabolism in cultures of chick astrocytes and neurones: evidence that astrocytes play an important role in antioxidative processes in the brain. J. Neurochem. 62, 45–53.
76. Mattson M. P. and Liu D. (2002) Energetics and oxidative stress in synaptic plasticity and neurodegenerative disorders. Neuromolecular Med. 2, 215–231.
77. Nguyen D., Alavi M. V., Kim K. Y. et al. (2011) A new vicious cycle involving glutamate excitotoxicity, oxidative stress and mitochondrial dynamics. Cell Death Dis. 2, e240.
78. Nicholls D. G. (2008) Oxidative stress and energy crises in neuronal dysfunction. Ann. N. Y. Acad. Sci. 1147, 53–60.
79. Nicholls D. G., Johnson-Cadwell L., Vesce S., Jekabsons M. and Yadava N. (2007) Bioenergetics of mitochondria in cultured neurons and their role in glutamate excitotoxicity. J. Neurosci. Res. 85, 3206–3212.
80. Oliveira J. F., Sardinha V. M., Guerra-Gomes S., Araque A. and Sousa N. (2015) Do stars govern our actions? Astrocyte involvement in rodent behavior. Trends Neurosci. 38, 535–549.
81. Palmer A. M. (1999) The activity of the pentose phosphate pathway is increased in response to oxidative stress in Alzheimer's disease. J. Neural. Transm. 106, 317–328.
82. Palygin O., Lalo U. and Pankratov Y. (2011) Distinct pharmacological and functional properties of NMDA receptors in mouse cortical astrocytes. Br. J. Pharmacol. 163, 1755–1766.
83. Papadia S., Soriano F. X., Leveille F. et al. (2008) Synaptic NMDA receptor activity boosts intrinsic antioxidant defenses. Nat. Neurosci. 11, 476–487.
84. Parpura V., Basarsky T. A., Liu F., Jeftinija K., Jeftinija S. and Haydon P. G. (1994) Glutamate-mediated astrocyte-neuron signalling. Nature 369, 744–747.
85. Partanen J. I., Nieminen A. I. and Klefstrom J. (2009) 3D view to tumor suppression: Lkb1, polarity and the arrest of oncogenic c-Myc. Cell Cycle 8, 716–724.
86. Pellerin L. and Magistretti P. J. (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl Acad. Sci. USA 91, 10625–10629.
87. Pellerin L. and Magistretti P. J. (2012) Sweet sixteen for ANLS. J. Cereb. Blood Flow Metab. 32, 1152–1166.
88. Pellerin L., Pellegri G., Bittar P. G., Charnay Y., Bouras C., Martin J. L., Stella N. and Magistretti P. J. (1998) Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle. Dev. Neurosci. 20, 291–299.
89. Pellerin L., Bouzier-Sore A. K., Aubert A., Serres S., Merle M., Costalat R. and Magistretti P. J. (2007) Activity-dependent regulation of energy metabolism by astrocytes: an update. Glia 55, 1251–1262.
90. Perea G., Sur M. and Araque A. (2014) Neuron-glia networks: integral gear of brain function. Front. Cell. Neurosci. 8, 378.
91. Pesin J. A. and Orr-Weaver T. L. (2008) Regulation of APC/C activators in mitosis and meiosis. Annu. Rev. Cell Dev. Biol. 24, 475–499.
92. Pierre K. and Pellerin L. (2005) Monocarboxylate transporters in the central nervous system: distribution, regulation and function. J. Neurochem. 94, 1–14.
93. Pilkis S. J., Claus T. H., Kurland I. J. and Lange A. J. (1995) 6-Phosphofructo-2-kinase/fructose-2,6-bisphosphatase: a metabolic signaling enzyme. Annu. Rev. Biochem. 64, 799–835.
94. Porras O. H., Loaiza A. and Barros L. F. (2004) Glutamate mediates acute glucose transport inhibition in hippocampal neurons. J. Neurosci. 24, 9669–9673.
95. 2+ cosignaling in the stimulation of the glucose transporter GLUT1 in cultured astrocytes. Glia 56, 59–68.
96. Rodriguez-Rodriguez P., Fernandez E., Almeida A. and Bolaños J. P. (2012) Excitotoxic stimulus stabilizes PFKFB3 causing pentose-phosphate pathway to glycolysis switch and neurodegeneration. Cell Death Differ. 19, 1582–1589.
97. Ronnett G. V., Ramamurthy S., Kleman A. M., Landree L. E. and Aja S. (2009) AMPK in the brain: its roles in energy balance and neuroprotection. J. Neurochem. 109(Suppl 1), 17–23.
98. Russell R. L., Siedlak S. L., Raina A. K., Bautista J. M., Smith M. A. and Perry G. (1999) Increased neuronal glucose-6-phosphate dehydrogenase and sulfhydryl levels indicate reductive compensation to oxidative stress in Alzheimer disease. Arch. Biochem. Biophys. 370, 236–239.
99. Sada N., Lee S., Katsu T., Otsuki T. and Inoue T. (2015) Epilepsy treatment. Targeting LDH enzymes with a stiripentol analog to treat epilepsy. Science 347, 1362–1367.
100. Sanders M. J., Grondin P. O., Hegarty B. D., Snowden M. A. and Carling D. (2007) Investigating the mechanism for AMP activation of the AMP-activated protein kinase cascade. Biochem. J. 403, 139–148.
101. Schipke C., Ohlemeyer C., Matyash M., Nolte C., Kettenmann H. and Kirchhoff F. (2001) Astrocytes of the mouse neocortex express functional N-methyl-d-aspartate receptors. FASEB J. 15, 1270–1272.
102. Schreiner B., Romanelli E., Liberski P. et al. (2015) Astrocyte depletion impairs redox homeostasis and triggers neuronal loss in the adult CNS. Cell Rep. 12, 1377–1384.
103. Schweizer M. and Richter C. (1994) Nitric oxide potently and reversibly deenergizes mitochondria at low oxygen tension. Biochem. Biophys. Res. Commun. 204, 169–175.
104. Seifert G. and Steinhäuser C. (2001) Ionotropic glutamate receptors in astrocytes. Prog. Brain Res. 132, 287–299.
105. Silverman D. H., Small G. W., Chang C. Y. et al. (2001) Positron emission tomography in evaluation of dementia: regional brain metabolism and long-term outcome. JAMA 286, 2120–2127.
106. Sotelo-Hitschfeld T., Fernandez-Moncada I. and Barros L. F. (2012) Acute feedback control of astrocytic glycolysis by lactate. Glia 60, 674–680.
107. Sotelo-Hitschfeld T., Niemeyer M. I., Machler P. et al. (2015) Channel-mediated lactate release by K(+)-stimulated astrocytes. J. Neurosci. 35, 4168–4178.
108. Soucek T., Cumming R., Dargusch R., Maher P. and Schubert D. (2003) The regulation of glucose metabolism by HIF-1 mediates a neuroprotective response to amyloid beta peptide. Neuron 39, 43–56.
109. Stegmuller J. and Bonni A. (2005) Moving past proliferation: new roles for Cdh1-APC in postmitotic neurons. Trends Neurosci. 28, 596–601.
110. Suh S. W., Bergher J. P., Anderson C. M., Treadway J. L., Fosgerau K. and Swanson R. A. (2007) Astrocyte glycogen sustains neuronal activity during hypoglycemia: studies with the glycogen phosphorylase inhibitor CP-316,819 ([R-R*, S*]-5-chloro-N-[2-hydroxy-3-(methoxymethylamino)-3-oxo-1-(phenylmethyl)propyl]-1H-indole-2 carboxamide). J. Pharmacol. Exp. Ther. 321, 45–50.
111. Tadi M., Allaman I., Lengacher S., Grenningloh G. and Magistretti P. J. (2015) Learning-induced gene expression in the hippocampus reveals a role of neuron -astrocyte metabolic coupling in long term memory. PLoS ONE 10, e0141568.
112. Thompson J. K., Peterson M. R. and Freeman R. D. (2003) Single-neuron activity and tissue oxygenation in the cerebral cortex. Science 299, 1070–1072.
113. Vaughn A. E. and Deshmukh M. (2008) Glucose metabolism inhibits apoptosis in neurons and cancer cells by redox inactivation of cytochrome c. Nat. Cell Biol. 10, 1477–1483.
114. Verkhratsky A. and Kirchhoff F. (2007) NMDA Receptors in glia. Neuroscientist 13, 28–37.
115. Vilchez D., Ros S., Cifuentes D. et al. (2007) Mechanism suppressing glycogen synthesis in neurons and its demise in progressive myoclonus epilepsy. Nat. Neurosci. 10, 1407–1413.
116. Volkenhoff A., Weiler A., Letzel M., Stehling M., Klambt C. and Schirmeier S. (2015) Glial glycolysis is essential for neuronal survival in drosophila. Cell Metab. 22, 437–447.
117. Wamelink M. M., Struys E. A. and Jakobs C. (2008) The biochemistry, metabolism and inherited defects of the pentose phosphate pathway: a review. J. Inherit. Metab. Dis. 31, 703–717.
118. Wullschleger S., Loewith R. and Hall M. N. (2006) TOR signaling in growth and metabolism. Cell 124, 471–484.
119. Xu Y., Ola M. S., Berkich D. A., Gardner T. W., Barber A. J., Palmieri F., Hutson S. M. and LaNoue K. F. (2007) Energy sources for glutamate neurotransmission in the retina: absence of the aspartate/glutamate carrier produces reliance on glycolysis in glia. J. Neurochem. 101, 120–131.
120. Zala D., Hinckelmann M. V., Yu H., Lyra da Cunha M. M., Liot G., Cordelieres F. P., Marco S. and Saudou F. (2013) Vesicular glycolysis provides on-board energy for fast axonal transport. Cell 152, 479–491.
121. Zhang Y., Chen K., Sloan S. A. et al. (2014) An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J. Neurosci. 34, 11929–11947.