Astrocytic energy metabolism and glutamate formation - relevance for 13C-NMR spectroscopy and importance of cytosolic/mitochondrial trafficking

Magnetic Resonance Imaging

Volumn 29, Issue 10, 2011, Pages 1319-1329

  Hertz, Leif ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Aralar; Astrocyte; Glucose metabolism; Glutamate formation and oxidation; K + clearance; Malate aspartate shuttle; Pyruvate carboxylation

Indexed keywords

4 AMINOBUTYRIC ACID; ACETIC ACID; ADENOSINE TRIPHOSPHATE; CALCIUM ION; GLUTAMATE DEHYDROGENASE; GLUTAMIC ACID; GLYCEROPHOSPHATE; NICOTINAMIDE ADENINE DINUCLEOTIDE; OXALOACETIC ACID; POTASSIUM ION; PYRUVATE DEHYDROGENASE; PYRUVIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

AEROBIC METABOLISM; ARTICLE; ASTROCYTE; BRAIN METABOLISM; BRAIN SIZE; CALCIUM CURRENT; CALCIUM HOMEOSTASIS; CARBON NUCLEAR MAGNETIC RESONANCE; CARBOXYLATION; CITRIC ACID CYCLE; CYTOSOL; DEHYDROGENATION; ENERGY METABOLISM; EPILEPTIC FOCUS; GLUCOSE METABOLISM; HUMAN; MITOCHONDRION; NONHUMAN; OXYGEN CONSUMPTION; POTASSIUM TRANSPORT; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; ANIMALS; ASTROCYTES; CARBON ISOTOPES; CONTRAST MEDIA; CYTOSOL; ENERGY METABOLISM; GLUTAMIC ACID; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MITOCHONDRIA; OXIDATION-REDUCTION; PYRUVIC ACID;

EID: 82455199255     PISSN: 0730725X     EISSN: 18735894     Source Type: Journal    
DOI: 10.1016/j.mri.2011.04.013     Document Type: Article

References (105)

1. Fitzpatrick S.M., Hetherington H.P., Behar K.L., Shulman R.G. The flux from glucose to glutamate in the rat brain in vivo as determined by 1H-observed, 13C-edited NMR spectroscopy. J Cereb Blood Flow Metab 1990, 10:170-179.
2. Gruetter R., Adriany G., Choi I.Y., Henry P.G., Lei H., Öz G. Localized in vivo 13C NMR spectroscopy of the brain. NMR Biomed 2003, 16:313-338.
3. 13C]glucose into biochemical pathways reveals a complex compartmentation and metabolite trafficking between glia and neurons: a study by 13C-NMR spectroscopy. Brain Res 1997, 765:218-227.
4. 13C NMR studies of metabolic compartmentation in the adult mammalian brain. NMR Biomed 1999, 12:451-462.
5. 13C NMR. Proc Natl Acad Sci U S A 1999, 96:8235-8240.
6. Gruetter R., Seaquist E.R., Uǧurbil K. A mathematical model of compartmentalized neurotransmitter metabolism in the human brain. Am J Physiol Endocrinol Metab 2001, 281:E100-E112.
7. Blüml S., Moreno-Torres A., Shic F., Nguy C.H., Ross B.D. Tricarboxylic acid cycle of glia in the in vivo human brain. NMR Biomed 2002, 15:1-5.
8. 13C nuclear magnetic resonance spectroscopy, elucidation of the dominant pathway for neurotransmitter glutamate repletion and measurement of astrocytic oxidative metabolism. J Neurosci 2002, 22:1523-1531.
9. Choi I.Y., Lei H., Gruetter R. Effect of deep pentobarbital anesthesia on neurotransmitter metabolism in vivo: on the correlation of total glucose consumption with glutamatergic action. J Cereb Blood Flow Metab 2002, 22:1343-1351.
10. 2 fixation increases with brain activity. J Neurosci 2004, 24:11273-11279.
11. Xu Y., Öz G., LaNoue K.F., Keiger C.J., Berkich D.A., Gruetter R., et al. Whole-brain glutamate metabolism evaluated by steady-state kinetics using a double-isotope procedure: effects of gabapentin. J Neurochem 2004, 90:1104-1116.
12. Patel A.B., Chowdhury G.M., de Graaf R.A., Rothman D.L., Shulman R.G., Behar K.L. Cerebral pyruvate carboxylase flux is unaltered during bicuculline-seizures. J Neurosci Res 2005, 79:128-138.
13. 13C] glucose. J Neurochem 2007, 100:73-86.
14. Deelchand D.K., Shestov A.A., Koski D.M., Uǧurbil K., Henry P.G. Acetate transport and utilization in the rat brain. J Neurochem 2009, 109(Suppl 1):46-54.
15. 13C]-NMR. J Cereb Blood Flow Metab 2010, 30:1200-1213.
16. 1H[13C] NMR spectroscopy. Abstracts, 9th International Conference on Brain Energy Metabolism, Budapest 2010, 25.
17. Muir D., Berl S., Clarke D.D. Acetate and fluoroacetate as possible markers for glial metabolism in vivo. Brain Res 1986, 380:336-340.
18. Yu A.C.H., Drejer J., Hertz L., Schousboe A. Pyruvate carboxylase activity in primary cultures of astrocytes and neurons. J Neurochem 1983, 41:1484-1487.
19. Shank R.P., Bennett G.S., Freytag S.O., Campbell G.L. Pyruvate carboxylase, an astrocyte-specific enzyme implicated in the replenishment of amino acid neurotransmitter pools. Brain Res 1985, 329:364-367.
20. Hertz L. Brain glutamine synthesis requires neuronal aspartate: a commentary. J Cereb Blood Flow Metab 2011, 31:384-387.
21. Norenberg M.D., Martinez-Hernandez A. Fine structural localization of glutamine synthetase in astrocytes of rat brain. Brain Res 1979, 161:303-310.
22. Chaudhry F.A., Reimer R.J., Edwards R.H. The glutamine commute: take the N line and transfer to the A. J Cell Biol 2002, 157:349-355.
23. Hertz L. Glutamate, a neurotransmitter - and so much more. A synopsis of Wierzba III. Neurochem Int 2006, 48:416-425.
24. Hogstad S., Svenneby G., Torgner I.A., Kvamme E., Hertz L., Schousboe A. Glutaminase in neurons and astrocytes cultured from mouse brain: kinetic properties and effects of phosphate, glutamate, and ammonia. Neurochem Res 1988, 13:383-388.
25. Maciejewski P.K., Rothman D.L. Proposed cycles for possible glutamate trafficking in synaptic neurotransmission. Neurochem Int 2008, 52:809-825.
26. 2+-dependent glutamate release from astrocytes: vesicular glutamate transporters and cytosolic glutamate levels. Glia 2009, 57:1296-1305.
27. 13C]glucose metabolites. J Biol Chem 1994, 269:27198-27208.
28. Hyder F., Patel A.B., Gjedde A., Rothman D.L., Behar K.L., Shulman R.G. Neuronal-glial glucose oxidation and glutamatergic-GABAergic function. J Cereb Blood Flow Metab 2006, 26:865-877.
29. Kurz G.M., Wiesinger H., Hamprecht B. Purification of cytosolic malic enzyme from bovine brain, generation of monoclonal antibodies, and immunocytochemical localization of the enzyme in glial cells of neural primary cultures. J Neurochem 1993, 60:1467-1474.
30. Rao V.L., Murthy C.R. Uptake, release and metabolism of glutamate and aspartate by rat cerebellar subcellular preparations. Biochem Mol Biol Int 1993, 29:711-717.
31. Berkich D.A., Ola M.S., Cole J., Sweatt A.J., Hutson S.M., LaNoue K.F. Mitochondrial transport proteins of the brain. J Neurosci Res 2007, 85:3367-3377.
32. Hertz L., Peng L., Dienel G.A. Energy metabolism in astrocytes, high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. J Cereb Blood Flow Metab 2007, 27:219-249.
33. Rajkowska G., Miguel-Hidalgo J.J., Wei J., Dilley G., Pittman S.D., Meltzer H.Y., et al. Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biol Psychiatry 1999, 45:1085-1098.
34. Pakkenberg B., Pelvig D., Marner L., Bundgaard M.J., Gundersen H.J., Nyengaard J.R., et al. Aging and the human neocortex. Exp Gerontol 2003, 38:95-99.
35. Pelvig D.P., Pakkenberg H., Stark A.K., Pakkenberg B. Neocortical glial cell numbers in human brains. Neurobiol Aging 2008, 29:1754-1762.
36. Chklovskii D.B., Schikorski T., Stevens C.F. Wiring optimization in cortical circuits. Neuron 2002, 34:341-347.
37. Van Harreveld A., Crowell J., Malhotra S.K. A study of extracellular space in central nervous tissue by freeze-substitution. J Cell Biol 1965, 25:117-137.
38. +, and pH in the developing rat cortex and corpus callosum. J Cereb Blood Flow Metab 1997, 17:191-203.
39. Derouiche A., Frotscher M. Peripheral astrocyte processes, monitoring by selective immunostaining for the actin-binding ERM proteins. Glia 2001, 36:330-341.
40. Nedergaard M., Ransom B., Goldman S.A. New roles for astrocytes, redefining the functional architecture of the brain. Trends Neurosci 2003, 26:523-530.
41. Wolff J., Chao T.I. Cytoarchitectonics of non-neuronal cells in the central nervous system. Non-neuronal cells of the nervous system, function and dysfunction 2004, 1-52. Elsevier, Amsterdam. L. Hertz (Ed.).
42. Bass N.H., Hess H.H., Pope A., Thalheimer C. Quantitative cytoarchitectonic distribution of neurons, glia, and DNA in rat cerebral cortex. J Comp Neurol 1971, 43:481-490.
43. Pope A. Neuroglia, quantitative aspects. In: E. Schoffeniels, G. Franck, L. Hertz, D. Tower, editors. Dynamic properties of glia cells. Oxford: Pergamon Press; 1978. p. 13-20.
44. Williams V., Grossman R.G., Edmunds S.M. Volume and surface area estimates of astrocytes in the sensorimotor cortex of the cat. Neuroscience 1980, 5:1151-1159.
45. Hertz L. Bioenergetics of cerebral ischemia: a cellular perspective. Neuropharmacology 2008, 55:289-309.
46. von Economo C. Ein Koeffizient für die Organisationshöhe der Grosshirnrinde. Klin Wschr 1926, 5:593-595.
47. Peters V.B., Flexner L.B. Biochemical and physiological differentiation during morphogenesis; quantitative morphologic studies on the developing cerebral cortex of the fetal guinea pig. Am J Anat 1950, 86:133-161.
48. Salganicoff L., Koeppe R.E. Subcellular distribution of pyruvate carboxylase, diphosphopyridine nucleotide and triphosphopyridine nucleotide isocitrate dehydrogenases, and malate enzyme in rat brain. J Biol Chem 1968, 243:3416-3420.
49. Schadé J.P., Baxter C.F. Changes during growth in the volume and surface area of cortical neurons in the rabbit. Exp Neurol 1960, 2:158-178.
50. Schadé J.P., van Backer H., Colon E. Quantitative analysis of neuronal parameters in the maturing cerebral cortex. Prog Brain Res 1964, 4:150-175.
51. Perge J.A., Koch K., Miller R., Sterling P., Balasubramanian V. How the optic nerve allocates space, energy capacity, and information. J Neurosci 2009, 29:7917-7928.
52. Lovatt D., Sonnewald U., Waagepetersen H.S., Schousboe A., He W., Lin J.H., et al. The transcriptome and metabolic gene signature of protoplasmic astrocytes in the adult murine cortex. J Neurosci 2007, 27:12255-12266.
53. Hertz L., Dienel G.A. Energy metabolism in the brain. Int Rev Neurobiol 2002, 51:1-102.
54. 2+-regulated mitochondrial aspartate-glutamate carrier aralar1 in brain and prominent expression in the spinal cord. Dev Brain Res 2003, 143:33-46.
55. Pardo B., Rodrigues T.B., Contreras L., Garzón M., Llorente-Folch I., Kobayashi K., et al. Brain glutamine synthesis requires neuronal-born aspartate as amino donor for glial glutamate formation. J Cereb Blood Flow Metab 2011, 31:90-101.
56. Cahoy J.D., Emery B., Kaushal A., Foo L.C., Zamanian J.L., Christopherson K.S., et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 2009, 28:264-278.
57. 14C-labeled glutamate in astrocytes in primary cultures. J Neurochem 1982, 39:954-960.
58. McKenna M.C., Sonnewald U., Huang X., Stevenson J., Zielke H.R. Exogenous glutamate concentration regulates the metabolic fate of glutamate in astrocytes. J Neurochem 1996, 66:386-393.
59. Fitzpatrick S.M., Cooper A.J., Hertz L. Effects of ammonia and beta-methylene-DL-aspartate on the oxidation of glucose and pyruvate by neurons and astrocytes in primary culture. J Neurochem 1988, 51:1197-1203.
60. Gandhi G.K., Cruz N.F., Ball K.K., Theus S.A., Dienel G.A. Selective astrocytic gap junctional trafficking of molecules involved in the glycolytic pathway: impact on cellular brain imaging. J Neurochem 2009, 110:857-869.
61. Gandhi G.K., Cruz N.F., Ball K.K., Dienel G.A. Astrocytes are poised for lactate trafficking and release from activated brain and for supply of glucose to neurons. J Neurochem 2009, 111:522-536.
62. Palaiologos G., Hertz L., Schousboe A. Role of aspartate aminotransferase and mitochondrial dicarboxylate transport for release of endogenously and exogenously supplied neurotransmitter in glutamatergic neurons. Neurochem Res 1989, 14:359-366.
63. Bak L.K., Ziemińska E., Waagepetersen H.S., Schousboe A., Albrecht J. Metabolism of [U-13C]glutamine and [U-13C]glutamate in isolated rat brain mitochondria suggests functional phosphate-activated glutaminase activity in matrix. Neurochem Res 2008, 33:273-278.
64. Jalil M.A., Begum L., Contreras L., Pardo B., Iijima M., Li M.X., et al. Reduced N-acetylaspartate levels in mice lacking aralar, a brain- and muscle-type mitochondrial aspartate-glutamate carrier. J Biol Chem 2005, 280:31333-31339.
65. Drickamer L.C. Seasonal variation in litter size, body weight and sexual maturation in juvenile female house mice (Mus musculus). Lab Anim 1977, 11:159-162.
66. Chowdhury G.M., Patel A.B., Mason G.F., Rothman D.L., Behar K.L. Glutamatergic and GABAergic neurotransmitter cycling and energy metabolism in rat cerebral cortex during postnatal development. J Cereb Blood Flow Metab 2007, 27:1895-1907.
67. Gaitonde M.K., Richter D. Changes with age in the utilization of glucose carbon in liver and brain. J Neurochem 1966, 13:1309-1316.
68. Kulak A., Duarte J.M., Do K.Q., Gruetter R. Neurochemical profile of the developing mouse cortex determined by in vivo 1H NMR spectroscopy at 14.1 T and the effect of recurrent anaesthesia. J Neurochem 2010, 115:1466-1477.
69. Cruz N.F., Lasater A., Zielke H.R., Dienel G.A. Activation of astrocytes in brain of conscious rats during acoustic stimulation: acetate utilization in working brain. J Neurochem 2005, 92:934-947.
70. Dienel G.A., Schmidt K.C., Cruz N.F. Astrocyte activation in vivo during graded photic stimulation. J Neurochem 2007, 103:1506-1522.
71. Dienel G.A., Cruz N.F., Ball K., Popp D., Gokden M., Baron S., et al. Behavioral training increases local astrocytic metabolic activity but does not alter outcome of mild transient ischemia. Brain Res 2003, 96:201-212.
72. 11C-acetate. J Cereb Blood Flow Metab 2009, 29:44-56.
73. Chuquet J., Quilichini P., Nimchinsky E.A., Buzsáki G. Predominant enhancement of glucose uptake in astrocytes versus neurons during activation of the somatosensory cortex. J Neurosci 2010, 30:15298-15303.
74. Jolivet R., Magistretti P.J., Weber B. Deciphering neuron-glia compartmentalization in cortical energy metabolism. Front Neuroenergetics 2009, 1:4.
75. Mangia S, Dinuzzo M, Giove F, Carruthers A, Simpson IA, Vannucci SJ. Response to 'comment on recent modeling studies of astrocyte-neuron metabolic interactions': much ado about nothing. J Cereb Blood Flow Metab 2011 Mar 23. [Epub ahead of print].
76. 14C-labeled acetate and butyrate in rat brain in vivo during spreading cortical depression. J Neurosci Res 2001, 66:812-820.
77. Vyskocil F., Kritz N., Bures J. Potassium-selective microelectrodes used for measuring the extracellular brain potassium during spreading depression and anoxic depolarization in rats. Brain Res 1972, 39:255-259.
78. Somjen GG, Kager H, Wadman WJ, Computer simulations of neuron-glia interactions mediated by ion flux. J Comput Neurosci 2008;25:349:365.
79. Xiong Z.Q., Stringer J.L. Sodium pump activity, not glial spatial buffering, clears potassium after epileptiform activity induced in the dentate gyrus. J Neurophysiol 2004, 83:1443-1451.
80. Xu L., Zeng L.H., Wong M. Impaired astrocytic gap junction coupling and potassium buffering in a mouse model of tuberous sclerosis complex. Neurobiol Dis 2009, 34:291-309.
81. Walz W. Role of astrocytes in the clearance of excess extracellular potassium. Neurochem Int 2000, 36:291-300.
82. Walz. W. Potassium homeostasis in the brain at the organ and cell level. In: L. Hertz, editor. Non-neuronal cells of the nervous system, function and dysfunction. Amsterdam: Elsevier; 2004. p. 595-609.
83. +-ATPase activity in cultured mouse neurons and astrocytes. Neurochem Int 1996, 28:335-342.
84. +-ATPase (EC 3.6.1.3) of bulk isolated glial cells, perikarya and synaptosomes from rabbit brain cortex. Brain Res 1979, 165:87-103.
85. Attwell D., Laughlin S.B. An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 2001, 21:1133-1145.
86. Danbolt N. Glutamate uptake. Prog Neurobiol 2001, 65:1-105.
87. 2+ signaling evoked by sensory stimulation in vivo. Nat Neurosci 2006, 9:816-823.
88. Wang X., Takano T., Nedergaard M. Astrocytic calcium signaling: mechanism and implications for functional brain imaging. Methods Mol Biol 2009, 489:93-109.
89. Nimmerjahn A., Mukamel E.A., Schnitzer M.J. Motor behavior activates Bergmann glial networks. Neuron 2009, 62:400-412.
90. Hoogland T.M., Kuhn B. Recent developments in the understanding of astrocyte function in the cerebellum in vivo. Cerebellum 2010, 9:264-271.
91. Subbarao K.V., Hertz L. Stimulation of energy metabolism by alpha-adrenergic agonists in primary cultures of astrocytes. J Neurosci Res 1991, 28:399-405.
92. i. Neurochem Int 2010, 57:411-420.
93. MacKenzie E.T., McCulloch J., Harper A.M. Influence of endogenous norepinephrine on cerebral blood flow and metabolism. Am J Physiol 1976, 231:489-494.
94. Xu Y., Ola M.S., Berkich D.A., Gardner T.W., Barber A.J., Palmieri F., et al. Energy sources for glutamate neurotransmission in the retina: absence of the aspartate/glutamate carrier produces reliance on glycolysis in glia. J Neurochem 2007, 101:120-131.
95. Serres S., Raffard G., Franconi J.M., Merle M. Close coupling between astrocytic and neuronal metabolisms to fulfill anaplerotic and energy needs in the rat brain. J Cereb Blood Flow Metab 2008, 28:712-724.
96. Dienel G.A., Wang R.Y., Cruz N.F. Generalized sensory stimulation of conscious rats increases labeling of oxidative pathways of glucose metabolism when the brain glucose-oxygen uptake ratio rises. J Cereb Blood Flow Metab 2002, 22:1490-1502.
97. Mangia S., Giove F., Tkác I., Logothetis N.K., Henry P.G., Olman C.A., et al. Metabolic and hemodynamic events after changes in neuronal activity: current hypotheses, theoretical predictions and in vivo NMR experimental findings. J Cereb Blood Flow Metab 2009, 29:441-463.
98. Gibbs M.E., Lloyd H.G., Santa T., Hertz L. Glycogen is a preferred glutamate precursor during learning in 1-day-old chick, biochemical and behavioral evidence. J Neurosci Res 2008, 85:3326-3333.
99. Giove F., Garreffa G., Peca S., Carní M., Macrì M.A., Di Bonaventura C., et al. Metabolic alteration transients during paroxysmal activity in an epileptic patient with fixation-off sensitivity: a case study. Magn Reson Imaging 2006, 24:373-379.
100. Plaitakis A., Latsoudis H., Spanaki C. The human GLUD2 glutamate dehydrogenase and its regulation in health and disease. Neurochem Int 2011, Mar 21. [Epub ahead of print].
101. García-Espinosa M.A., Rodrigues T.B., Sierra A., Benito M., Fonseca C., Gray H.L., et al. Cerebral glucose metabolism and the glutamine cycle as detected by in vivo and in vitro 13C NMR spectroscopy. Neurochem Int 2004, 45:297-303.
102. Paulsen R.E., Fonnum F. Role of glial cells for the basal and Ca2+-dependent K+-evoked release of transmitter amino acids investigated by microdialysis. J Neurochem 1989, 52:1823-1829.
103. Fonnum F., Paulsen R.E. Comparison of transmitter amino acid levels in rat globus pallidus and neostriatum during hypoglycemia or after treatment with methionine sulfoximine or gamma-vinyl gamma-aminobutyric acid. J Neurochem 1990, 54:1253-1257.
104. Somers D.L., Beckstead R.M. Chronic methionine sulfoximine administration reduces synaptosomal aspartate and glutamate in rat striatum. Neurosci Lett 1990, 115:335-340.
105. 13C MRS brain exam for clinical diagnostic use. J Magn Reson 2010, 207:352-355.