The role of astrocytes and noradrenaline in neuronal glucose metabolism

Acta Physiologica Scandinavica

Volumn 167, Issue 4, 1999, Pages 275-284

  Fillenz, M ^a   Lowry, J P ^a,b   Boutelle, M G ^a,c   Fray, A E ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^c KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Astrocytes; Glucose; Neurones; Noradrenaline

Indexed keywords

ARGININE; BETA ADRENERGIC RECEPTOR; GLUCOSE; GLUTAMATE RECEPTOR; GLYCOGEN; NITRIC OXIDE; NORADRENALIN;

ASTROCYTE; BRAIN BLOOD FLOW; CELL METABOLISM; GLUCOSE METABOLISM; NERVE CELL; PRIORITY JOURNAL; REVIEW;

ANIMALS; ASTROCYTES; BLOOD GLUCOSE; BRAIN; CEREBROVASCULAR CIRCULATION; HUMANS; NEURONS; NITRIC OXIDE; NOREPINEPHRINE;

EID: 0033378037     PISSN: 00016772     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-201X.1999.00578.x     Document Type: Review

References (87)

1. Akgoren, N., Mathiesen, C., Rubin, I. & Lauritzen, M. 1997. Laminar analysis of activity-dependent increases of CBF in rat cerebellar cortex: Dependence on synaptic strength. Am J Physiol 273, H1166-H1176.
2. Amedee, T., Robert, A. & Coles, J.A. 1997. Potassium homeostasis and glial energy metabolism. Glia 21, 46-55.
3. Aoki, C. & Pickel, V.M. 1992. Ultrastructural relations between β-adrenergic receptors and catecholaminergic neurones. Brain Res Bull 29, 257-263.
4. Ballanyi, K., Grafe, P. & Ten Bruggencate, G. 1987. Ion activities and potassium uptake mechanisms of glial cells in guinea-pig olfactory cortex slices. J Physiol Lond 382, 159-174.
5. Cambray Deakin, M., Pearce, B., Morrow, C. & Murphy, S. 1988. Effects of neurotransmitters on astrocyte glycogen stores in vitro. J Neurochem 51, 1852-1857.
6. Choi, D.W. 1990. Cerebral hypoxia: Some new approaches and unanswered questions. J Neurosci 10, 2493-2501.
7. Cholet, N., Seylaz, J., Lacombe, P. & Bonvento, G. 1997. Local uncoupling of the cerebrovascular and metabolic responses to somatosensory stimulation after neuronal nitric oxide synthase inhibition. J Cereb Blood Flow Metab 17, 1191-1201.
8. Demestre, M., Boutelle, M.G. & Fillenz, M. 1997. Stimulated release of lactate in freely moving rats is dependent on the uptake of glutamate. J Physiol Lond 499, 825-832.
9. Dirnagl, U., Lindauer, U. & Villringer, A. 1993. Role of nitric oxide in the coupling of cerebral blood flow to neuronal activation in rats. Neurosci Lett 149, 43-46.
10. Dirnagl, U., Niwa, K., Lindauer, U. & Villringer, A. 1994. Coupling of cerebral blood flow to neuronal activation: Role of adenosine and nitric oxide. Am J Physiol 267, H296-H301.
11. Dreier, J.P., Korner, K., Gorner, A. et al. 1995. Nitric oxide modulates the CBF response to increased extracellular potassium. J Cereb Blood Flow Metab 15, 914-919.
12. Dringen, R., Gebhardt, R. & Hamprecht, B. 1993. Glycogen in astrocytes: Possible function as lactate supply for neighboring cells. Brain Res 623, 208-214.
13. Estrada, C. & DeFelipe, J. 1998. Nitric oxide-producing neurons in the neocortex: Morphological and functional relationship with intraparenchymal microvasculature. Cereb Cortex 8, 193-203.
14. Faraci, F.M. 1990. Role of nitric oxide in regulation of basilar artery tone in vivo. Am J Physiol 259, H1216-H1221.
15. Faraci, F.M. & Breese, K.R. 1993. Nitric oxide mediates vasodilatation in response to activation of N-methyl-D-aspartate receptors in brain. Circ Res 72, 476-480.
16. Faraci, F.M. & Sobey, C.G. 1998. Role of potassium channels in regulation of cerebral vascular tone. J Cereb Blood Flow Metab 18, 1047-1063.
17. Fillenz, M. & Lowry, J. 1998a. The relation between local cerebral blood flow and extracellular glucose concentration in rat striatum. J Exp Physiol 83, 233-238.
18. Fillenz, M. & Lowry, J. 1998b. Studies of the Source of Glucose in the Extracellular Compartment of the Rat Brain. Dev Neurosci 20, 365-368.
19. Fox, P.T. & 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.
20. Fox, P.T., Raichle, M.E., Mintun, M.A. & Dence, C. 1988. Nonoxidative glucose consumption during focal physiologic neural activity. Science 241, 462-464.
21. Fray, A.E., Boutelle, M. & Fillenz, M. 1997. Extracellular glucose turnover in the striatum of unanaesthetized rats measured by quantitative microdialysis. J Physiol Lond 504, 721-726.
22. Fray, A.E., Forsyth, R.J., Boutelle, M.G. & Fillenz, M. 1996. The mechanisms controlling physiologically stimulated changes in rat brain glucose and lactate: A microdialysis study. J Physiol Lond 496, 49-57.
23. Gardner-Medwin, A.R. 1983. Analysis of potassium dynamics in mammalian brain tissue. J Physiol Lond 335, 393-426.
24. Giaume, C., Tabernero, A. & Medina, J.M. 1997. Metabolic trafficking through astrocytic gap junctions. Glia 21,114-123.
25. Grima, G., Benz, B. & Do, K.Q. 1997. Glutamate-induced release of the nitric oxide precursor, arginine, from glial cells. Eur J Neurosci 9, 2248-2258.
26. Grima, G., Cuenod, M., Pfeiffer, S., Mayer, B. & Do, K.Q. 1998. Arginine availability controls the N-Methyl-D-Aspartate-induced nitric oxide synthesis: Involvement of a glial-nauronal arginine transfer. J Neurochem 71, 2139-2144.
27. Gutnick, M.J., Connors, B.W. & Ransom, B.R. 1981. Dye-coupling between glial cells in the guinea pig neocortical slice. Brain Res 213, 486-492.
28. Harder, D.R., Alkayed, N.J., Lange, A.R., Gebremedhin, D. & Roman, RJ. 1998. Functional hyperemia in the brain: Hypothesis for astrocyte-derived vasodilator metabolites. Stroke 29, 229-234.
29. Harik, S.I., Busto, R. & Martinez, E. 1982. Norepinephrine regulation of cerebral glycogen utilization during seizures and ischemia. J Neurosci 2, 409-414.
30. Harik, S.I., LaManna, J.C., Light, A.I. & Rosenthal, M. 1979. Cerebral norepinephrine: Influence on cortical oxidative metabolism. Science 206, 205-206.
31. Harik, S.I., Sharma, V.K., Wetherbee, J.R., Warren, R.H. & Banerjee, S.P. 1981. Adrenergic and cholinergic receptors of cerebral microvessels. J Cereb Blood Flow Metab 1, 329-338.
32. 14C]glucose labeled in the, 1, 2 or 6 position. Am J Physiol 248.
33. Hertz, L. & Peng, L. 1992. Effects of monoamine transmitters on neurons and astrocytes: correlation between energy metabolism and intracellular messengers. Prog Brain Res 94, 283-301.
34. ladecola, C. 1992. Nitric oxide participates in the cerebrovasodilation elicited from cerebellar fastigial nucleus. Am J Physiol 263, R1156-R1161.
35. Iadecola, C. & Kraig, R.P. 1991. Focal elevations in neocortical interstitial K (+) produced by stimulation of the fastigial nucleus in rat. Brain Res 563, 273-277.
36. Iadecola, C., Li, J., Ebner, T.J. & Xu, X. 1995. Nitric oxide contributes to functional hyperemia in cerebellar cortex. Am J Physiol 268, R1153-R1162.
37. Iadecola, C., Yang, G., Ebner, T.J. & Chen, G. 1997. Local and propagated vascular responses evoked by focal synaptic activity in cerebellar cortex. J Neurophysiol 78, 651-659.
38. Kacem, K., Lacombe, P., Seylaz, J. & Bonvento, G. 1998. Structural organization of the perivascular astrocytic endfeet and their relationship with the endothelial glucose transporter: a confocal microscopy study. Glia 23, 1-10.
39. Kraig, R.P. & Iadecola, C. 1989. Reduction of astroglial K+ accumulation enhances elevation in cerebral blood flow from neural activation. J Cereb Blood Flow Metab 9, S207.
40. LaManna, J.C., Harik, S.I., Light, A.I. & Rosenthal, M. 1981. Norepinephrine depletion alters cerebral oxidative metabolism in the 'active' state. Brain Res 204, 87-101.
41. Li, J. & Iadecola, C. 1994. Nitric oxide and adenosine mediate vasodilation during functional activation in cerebellar cortex. Neuropharm 33, 1453-1414 61.
42. Lindauer, U., Villringer, A. & Dirnagl, U. 1993. Characterization of CBF response to somatosensory stimulation: model and influence of anesthetics. Am J Physiol 264, H1223-H1228.
43. Lowry, J.P., Boutelle, M.G. & Fillenz, M. 1997. Measurement of brain tissue oxygen at a carbon paste electrode can serve as an index of increases in regional cerebral blood flow. J Neurosci Meth 71, 177-182.
44. Lowry, J.P., Demestre, M. & Fillenz, M. 1998a. Relation between cerebral blood flow and extracellular glucose in rat striatum during mild hypoxia and hyperoxia. Dev Neurosci 20, 52-58.
45. Lowry, J.P. & Fillenz, M. 1997. Evidence for the uncoupling of oxygen and glucose utilization during neuronal activation in rat striatum. J Physiol Lond 498, 497-501.
46. Lowry, J.P., O'Neill, R.D., Boutelle, M.G. & Fillenz, M. 1998b. Continuous monitoring of extracellular glucose concentrations in the striatum of freely moving rats with an implanted glucose biosensor. J Neurochem 70, 391-396.
47. Madsen, P.L., Linde, R., Hasselbalch, S.G., Paulson, O.B. & Lassen, N.A. 1998. Activation-induced resetting of cerebral oxygen and glucose uptake in the rat. J Cereb Blood Flow Metab 18, 742-748.
48. Magistretti, P.J., Sorg, O. & Martin, J.-L. 1993. Regulation of glycogen metabolism in astrocytes: physiological, pharmacological, and pathological aspects. In: S. Murphy (ed.) Astrocytes, pp. 243-265. Academic Press, San Diego.
49. Marshall, J.J., Wei, E.P. & Kontos, H.A. 1988. Independent blockade of cerebral vasodilation from acetylcholine and nitric oxide. Am J Physiol 255, H847-H854.
50. McCarthy, K.D. 1988. An autoradiographic analysis of beta-adrenergic receptors on immunocytochemically defined astroglia. J Pharmacol Exp Ther 226, 282-290.
51. Miele, M., Boutelle, M.G. & Fillenz, M. 1996. The source of physiologically stimulated glutamate efflux from the striatum of conscious rats. J Physiol Lond 497, 745-751.
52. Murphy, T.H., Blatter, L.A., Wier, W.G. & Baraban, J.M. 1993. Rapid communication between neurons and astrocytes in primary cortical cultures. J Neurosci 13, 2672-2679.
53. Nakai, M., Iadecola, C, Ruggiero, D.A., Tucker, L.W. & Reis, DJ. 1983. Electrical stimulation of cerebellar fastigial nucleus increases cerebral cortical blood flow without change in local metabolism: evidence for an intrinsic system in brain for primary vasodilatation. Brain Res 260, 35-49.
54. Nedergaard, M. 1994. Direct signalling from astrocytes to neurons in cultures of mammalian brain cells. Science 263, 1768-1771.
55. Newman, E.A. 1986. High potassium conductance in astrocytic endfeet. Science 233, 453-454.
56. Northington, F.J., Matherne, G.P., Coleman, S.D. & Berne, R.M. 1992. Sciatic nerve stimulation does not increase endogenous adenosine production in sensory-motor cortex. J Cereb Blood Flow Metab 12, 835-843.
57. Papsapalas, C.D. & Papadopoulos, G.C. 1996. Ultrastructural relationship between noradrenergic nerve fibres and non-neural elements in the rat cerebral cortex. Glia 17, 133-146.
58. Paulson, O.B. & Newman, E.A. 1987. Does the release of potassium from astrocyte endfeet regulate cerebral blood flow? Science 237, 896-898.
59. Pellerin, L. & Magistretti, P.J. 1994. Glutamate uptake into astrocytes stimulates aerobic glycolysis: A mechanism coupling neuronal activity to glucose utilisation. Proc Natl Acad Sci USA 91, 10625-10629.
60. Pellerin, L., Stolz, M., Sorg, O., Martin, J.L., Deschepper, C.F. & Magistretti, P.J. 1997. Regulation of energy metabolism by neurotransmitters in astrocytes in primary culture and in an immortalized cell line. Glia 21, 74-83.
61. Peters, A., Palay, S.L. & de Webster, H. 1991. The Fine Structure of the Nervous System: Neurons and their Supporting Cells. Oxford University Press, New York.
62. Poitry Yamate, C.L., Poitry, S. & Tsacopoulos, M. 1995. Lactate released by Muller glial cells is metabolized by photoreceptors from mammalian retina. J Neurosci 15, 5179-5191.
63. 3H]2-deoxy-d-glucose in mammalian retina. Neurosci Lett 122, 241-244.
64. Quayle, J.M., McCarron, J.G., Brayden, J.E. & Nelson, M.T. 1993. Inward rectifier K+ currents in smooth muscle cells from rat resistance-sized cerebral arteries. Am J Physiol 265, C1363-C1370.
65. Raichle, M.E. 1998. Behind the scenes of functional brain imaging: a historical and physiological perspective. Proc Natl Acad Sci USA 95, 765-772.
66. Rosenblum, W.I., Nishimura, H. & Nelson, G.H. 1990. Endothelium-dependent L-Arg-and L-NMMA-sensitive mechanisms regulate tone of brain microvessels. Am J Physiol 259, H1396-H1401.
67. Roy, C.S. & Sherrington, C.S. 1890. On the regulation of the blood supply of the brain. J Physiol Lond 11, 85-108.
68. Sacks, W.S. & Fleischer, A. 1983. A comparison of the cerebral uptake and metabolism of labelled glucose and deoxyglucose in vivo in rats. Neurochem Res 8, 661-685.
69. Scheinberg, P. & Joyne, H.W. 1952. Factors influencing cerebral blood flow and metabolism. Circulation 5, 225-236.
70. Schurr, A., Payne, R.S., Miller, J.J. & Rigor, B.M. 1997a. Brain lactate is an obligatory aerobic energy substrate for functional recovery after hypoxia: further in vitro validation. J Neurochem 69, 423-426.
71. Schurr, A., Payne, R.S., Miller, J.J. & Rigor, B.M. 1997b. Brain lactate, not glucose, fuels the recovery of synaptic function from hypoxia upon reoxygenation: an in vitro study. Brain Res 744, 105-111.
72. Schurr, A., West, C.A. & Rigor, B.M. 1988. Lactate-supported synaptic function in the rat hippocampal slice preparation. Science 240, 1326-1328.
73. Sokoloff, L. 1960. Metabolism of the central nervous system in vivo. In: H.W. Magoun (ed.) Handbook of Physiology. Section 1 Neurophysiology, pp. 1843-1864. Williams and Wilkins, Washington DC.
74. Sokoloff, L. 1989. Circulation and energy metabolism of the brain. In: G.J. Siegel (ed.) Basic Neurochemistry, pp. 565-590. Raven Press, New York.
75. 14C]deoxyglucose method for the measurement of local cerebral utilization: theory, procedure and normal values in the conscious and anaesthetized albino rat. J Neurochem 28, 897-916.
76. Sorg, O. & Magistretti, P.J. 1991. Characterization of the glycogenolysis elicited by vasoactive intestinal peptide, noradrenaline and adenosine in primary cultures of mouse cerebral cortical astrocytes. Brain Res 563, 227-233.
77. Stone, E.A. & Ariano, M.A. 1989. Are glial cells targets of the central noradrenergic system? A review of the evidence. Brain Res Brain Res Rev 14, 297-309.
78. Subbarao, K.V. & Hertz, L. 1990. Effect of adrenergic agonists on glycogenolysis in primary cultures of astrocytes. Brain Res 536, 220-226.
79. Swanson, R.A. 1992. Physiologic coupling of glial glycogen metabolism to neuronal activity in brain. Can J Physiol Pharmacoll 70 (Suppl), S138-S144.
80. Swanson, R.A., Morton, M.M., Sagar, S.M. & Sharp, F.R. 1992. Sensory stimulation induces local cerebral glycogenolysis: demonstration by autoradiography. Neuroscience 51, 451-461.
81. Sykova, E., Jendelova, P., Svoboda, J. & Chvatal, A. 1992. Extracellular K+, pH, and volume changes in spinal cord of adult rats and during postnatal development. Can J Physiol Pharmacol 70 (Suppl), S301-S309.
82. Tanaka, K., Gotoh, F., Gomi, S. et al. 1991. Inhibition of nitric oxide synthesis induces a significant reduction in local cerebral blood flow in the rat. Neurosci Lett 127, 129-132.
83. Timmerman, W. & Westerink, B.H. 1997. Brain microdialysis of GABA and glutamate: what does it signify? Synapse 27, 242-261.
84. Welker, C. 1971. Microelectrode delineation of fine grain somatotopic organization of SMI cerebral neocortex in albino rat. Brain Res 26, 259-275.
85. Woolsey, T.A., Rovainen, C.M., Wei, L. et al. 1996. Dynamic measurements of local cerebral blood flow. Examples from rodent whisker barrel cortex. In: A.W. Toga & J.C. Mazziotta (eds) Brain Mapping: the methods, pp. 99-113. Academic Press, San Diego.
86. Yang, S.T. & Chang, H.H. 1998. Nitric oxide of neuronal origin mediates NMDA-induced cerebral hyperemia in rats. Neuroreport 9, 415-418.
87. Zhang, X., Peng, L., Chen, Y. & Hertz, L. 1993. Stimulation of glycogenolysis in astrocytes by fluoxetine, an antidepressant acting like 5-HT. Neuroreport 4, 1235-1238.