Predominant enhancement of glucose uptake in astrocytes versus neurons during activation of the somatosensory cortex

Journal of Neuroscience

Volumn 30, Issue 45, 2010, Pages 15298-15303

  Chuquet, Julien ^a   Quilichini, Pascale ^a   Nimchinsky, Esther A ^a   Buzsáki, György ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 DEOXY N (7 NITROBENZ 2 OXA 1,3 DIAZOL 4 YL) AMINOGLUCOSE; GLUCOSE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN FUNCTION; CELL ACTIVATION; CELL ACTIVITY; FEMALE; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; IN VIVO STUDY; MALE; MULTIPHOTON MICROSCOPY; NERVE CELL; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SOMATOSENSORY CORTEX;

ANALYSIS OF VARIANCE; ANIMALS; ASTROCYTES; BIOLOGICAL TRANSPORT; GLUCOSE; MALE; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SOMATOSENSORY CORTEX; VIBRISSAE;

EID: 78149491490     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0762-10.2010     Document Type: Article

References (41)

1. Aller CB, Ehmann S, Gilman-Sachs A, Snyder AK (1997) Flow cytometric analysis of glucose transport by rat brain cells. Cytometry 27:262-268.
2. Almeida A, Almeida J, Balaños JP, 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 U S A 26:15294-15299.
3. Attwell D, Laughlin SB (2001) An energy budget for signalling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133-1145.
4. Barros LF, Courjaret R, Jakoby P, Loaiza A, Lohr C, Deitmer JW (2009) Preferential transport and metabolism of glucose in Bergmann glia over Purkinje cells: a multiphoton study of cerebellar slices. Glia 57:962-970.
5. Brookes N, Yarowsky PJ (1985) Determinants of deoxyglucose uptake in cultured astrocytes: the role of the sodium pump. J Neurochem 44:473-479.
6. Cerdán S, Rodrigues TB, Sierra A, Benito M, Fonseca LL, Fonseca CP, García-Martín ML (2006) The redox switch/redox coupling hypothesis. Neurochem Int 48:523-530.
7. Chung S, Li X, Nelson SB (2002) Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo. Neuron 34:437-446.
8. Chuquet J, Bhaukaurally K, Santello M, Liaudet N, Bouvier D, Di Castro A, Volterra A (2010) Fast and local calcium transients in astrocyte processes encode synaptic activity in the adult hippocampus. FENS Abstr 5:044.4.
9. Contreras D, Steriade M (1996) Spindle oscillation in cats: the role of corticothalamic feedback in a thalamically generated rhythm. J Physiol 490:159-179.
10. Cruz NF, Lasater A, Zielke HR, Dienel GA (2005) Activation of astrocytes in brain of conscious rats during acoustic stimulation: acetate utilization in working brain. J Neurochem 92:934-947.
11. Herrero-Mendez A, Almeida A, Fernández E, Maestre C, Moncada S, Bolaños JP (2009) The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key enzyme by APC/C-Cdh1. Nat Cell Biol 11:747-752.
12. Hertz L (2008) Bioenergetics of cerebral ischemia: a cellular perspective. Neuropharmacology 55:289-309.
13. Hertz L, Peng L, Dienel GA (2007) Energy metabolism in astrocytes: high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. J Cereb Blood Flow Metab 27:219-249.
14. Hyder F, Patel AB, Gjedde A, Rothman DL, Behar KL, Shulman RG (2006) Neuronal-glial glucose oxidation and glutamatergic-GABAergic function. J Cereb Blood Flow Metab 26:865-877.
15. Itoh Y, Abe T, Takaoka R, Tanahashi N (2004) Fluorimetric determination of glucose utilization in neurons in vitro and in vivo. J Cereb Blood Flow Metab 24:993-1003.
16. Jolivet R, Magistretti PJ, Weber B (2009) Deciphering neuron-glia compartmentalization in cortical energy metabolism. Front Neuroenergetics 1:1-10.
17. Loaiza A, Porras OH, Barros LF (2003) Glutamate triggers rapid glucose transport stimulation in astrocytes as evidenced by real-time confocal microscopy. J Neurosci 23:7337-7342.
18. Lopes-Cardozo M, Larsson OM, Schousboe A (1986) Acetoacetate and glucose as lipid precursors and energy substrates in primary cultures of astrocytes and neurons from mouse cerebral cortex. J Neurochem 46:773-778.
19. Magistretti PJ, Pellerin L (1996a) Cellular mechanisms of brain energy metabolism. Relevance to functional brain imaging and to neurodegenerative disorders. Ann N Y Acad Sci 777:380-387.
20. Magistretti PJ, Pellerin L (1996b) The contribution of astrocytes to the 18F-2-deoxyglucose signal in PET activation studies. Mol Psychiatry 1:445-452.
21. Magistretti PJ, Pellerin L (1999) Cellular mechanism of brain energy metabolism and their relevance to functional brain imaging. Philos Trans R Soc Lond B Biol Sci 354:1155-1163.
22. Mangia S, Simpson IA, Vannucci SJ, Carruthers A (2009) The in vivo neuron-to-astrocyte lactate shuttle in human brain: evidence from modeling of measured lactate levels during visual stimulation. J Neurochem 109:55-62.
23. McCasland JS (1996) Metabolic activity in antigenically identified neurons: a double labeling method for high-resolution 2-deoxyglucose and immunohistochemistry. J Neurosci Methods 68:113-123.
24. Nehlig A, Coles JA (2007) Cellular pathways of energy metabolism in the brain: is glucose used by neurons or astrocytes? Glia 55:1238-1250.
25. 14C-trajectography combined with immunohistochemistry. J Cereb Blood Flow Metab 24:1004-1014.
26. Nimmerjahn A, Kirchhoff F, Kerr JN, Helmchen F (2004) Sulforhodamine-101 as a specific marker of astroglia in the neocortex in vivo. Nat Methods 1:31-37.
27. Norenberg MD (1994) Astrocyte response to CNS injury. J Neuropathol Exp Neurol 53:213-220.
28. Oz G, Berkich DA, Henry PG, Xu Y, LaNoue K, Hutson SM, Gruetter R (2004) Neuroglial metabolism in the awake rat brain: CO2 fixation increases with brain activity. J Neurosci 24:11273-11279.
29. Patel AB, de Graaf RA, Mason GF, Rothman DL, Shulman RG, Behar KL (2005) The contribution of GABA to glutamate/glutamine cycling and energy metabolism in the rat cortex in vivo. Proc Natl Acad Sci U S A 102:5588-5593.
30. Pellerin L, Bouzier-Sore AK, Aubert A, Serres S, Merle M, Costalat R, Magistretti PJ (2007) Activity-dependent regulation of energy metabolism by astrocytes: an update. Glia 55:1251-1262.
31. Porras OH, Loaiza A, Barros LF (2004) Glutamate mediates acute glucose transport inhibition in hippocampal neurons. J Neurosci 24:9669-9673.
32. Raichle ME, Mintun MA (2006) Brain work and brain imaging. Annu Rev Neurosci 29:449-476.
33. Rouach N, Koulakoff A, Abudara V, Willecke K, Giaume C (2008) Astroglial metabolic network sustain hippocampal synaptic transmission. Science 322:1551-1555.
34. Shimada M, Kawamoto S, Hirose Y, Nakanishi M, Watanabe H, Watanabe M (1994) Regional differences in glucose transport in the mouse hippocampus. Histochem J 26:207-212.
35. Sibson NR, Mason GF, Shen J, Cline GW, Herskovits AZ, Wall JE, Behar KL, Rothman DL, Shulman RG (2001) In vivo (13)C NMR measurement of neurotransmitter glutamate cycling, anaplerosis and TCA cycle flux in rat brain during [2-13C]glucose infusion. J Neurochem 76:975-989.
36. Sokoloff L (1977) Relation between physiological function and energy metabolism in the central nervous system. J Neurochem 29:13-26.
37. Somjen GG, Kager H, Wadman WJ (2008) Computer simulations of neuron-glia interactions mediated by ion flux. J Comput Neurosci 25:349-365.
38. Speizer L, Haugland R, Kutchai H (1985) Asymmetric transport of a fluorescent glucose analogue by human erythrocytes. Biochim Biophys Acta 815:75-84. (Pubitemid 15071517)
39. Voutsinos-Porche B, Bonvento G, Tanaka K, Steiner P, Welker E, Chatton JY, Magistretti PJ, Pellerin L (2003) Glial glutamate transporters mediate a functional metabolic crosstalk between neurons and astrocytes in the mouse developing cortex. Neuron 37:275-286.
40. Wyss MT, Weber B, Treyer V, Heer S, Pellerin L, Magistretti PJ, Buck A (2009) Stimulation-induced increases of astrocytic oxidative metabolism in rats and in humans investigated with 1-11C-acetate. J Cereb Blood Flow Metab 29:44-56.
41. Yamada K, Nakata M, Horimoto N, Saito M, Matsuoka H, Inagaki N (2000) Measurement of glucose uptake and intracellular calcium concentration in single, living pancreatic beta-cells. J Biol Chem 275:22278-22283.