Quantitative 13C NMR studies of metabolic compartmentation in the adult mammalian brain

NMR in Biomedicine

Volumn 12, Issue 7, 1999, Pages 451-462

  Cruz, Fátima ^a   Cerdán, Sebastián ^a  

^a INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

Author keywords

13C MRS; Glutamate glutamine GABA cycle; Neuronal glial interactions; Pyruvate recycling; Tricarboxylic acid cycle

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID; GLUTAMINE; PYRUVIC ACID; CARBON;

ARTICLE; BRAIN METABOLISM; CARBON NUCLEAR MAGNETIC RESONANCE; CITRIC ACID CYCLE; COMPARTMENT MODEL; PATHOPHYSIOLOGY; PRIORITY JOURNAL; BRAIN; CYTOLOGY; GLIA; METABOLISM; NERVE CELL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; REVIEW;

BRAIN; CARBON ISOTOPES; CITRIC ACID CYCLE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; GLUTAMINE; MAGNETIC RESONANCE SPECTROSCOPY; NEUROGLIA; NEURONS;

EID: 0033233212     PISSN: 09523480     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1099-1492(199911)12:7<451::AID-NBM571>3.0.CO;2-E     Document Type: Article

References (97)

1. Siegel, G., Agranoff, B., Albers, R. W., Molinoff, P. In Basic Neurochemistry, Raven Press, New York. (1989).
2. Nicholls, D. G. In Proteins, Transmitters and Synapses, pp. 15-25. Blackwell Science, Oxford (1995).
3. Benjamins, J. A., McKhan, G. M. Neurochemistry of development. In Basic Neurochemistry, pp 269-298 Albers, R. W., Siegel, G. J., Katzman, R., Agranoff, B. W. eds. Little Brown, Boston, MA (1972).
4. Girard, J. R., Cuendet, G. S., Marliss, E. B., Kebran, A., Rieutort, M. and Assan, R. Fuels, hormones, and liver metabolism at term and during the early postnatal period in the rat. J. Clin. Invest. 52, 3190-3200 (1973).
5. Fernández, E., Medina, J. M. Lactate utilization by the neonatal rat brain in vitro. Competition with glucose and 3-hydroxybutyrate. Biochem. J. 234, 489-492 (1986).
6. Williamsom, D. H. The production and utilization of ketone bodies in the neonate. In The Biochemical Development of the Fetus and the Neonate, pp 621-650. Jones, C. T. ed. Elsevier Biomedical Press, Amsterdam (1986).
7. Patel, A. J., Balázs, R. Manifestation of metabolic compartmentation during the maturation of the rat brain. J. Neurochem. 17, 955-971 (1970).
8. Van den Berg, C. J. Compartmentation of glutamate metabolism in the developing brain: experiments with labelled glucose, acetate, phenylalanine, tyrosine and proline. J. Neurochem. 17, 973-983 (1970).
9. Riggs, T. R., Pote, K. G., Hae-Sook, I., Huff, D. W. Developmental changes in the neutral amino acid transport systems of rat brain over the first three weeks after birth. J. Neurochem. 42, 1251-1259 (1984).
10. Vannucci, S. J., Maher, F., Simpson, I. A. Glucose transporter proteins in brain: delivery of glucose to neurons and glial cells. Glia 21, 2-21 (1997).
11. Cruz, F., Scott, R., Barroso, I., Santisteban, P., Cerdán, S. Ontogeny and cellular localization of the pyruvate recycling enzymes of rat brain. J. Neurochem. 70, 2613-2619 (1998).
12. Pardridge, W. M. Brain metabolism: a perspective from the blood brain barrier. Physiol. Rev. 63, 1481-1535 (1983).
13. Smolier, R., Smolier, A., Sorkin, L., Bolkin, V. Microcirculatory bed of the human trigeminal nerve. Anat. Rec. 250, 245-249 (1998).
14. 14C) deoxyglucose method for measurement of local cerebral glucose utilization. In Neuromethods 11. Carbohydrates and Energy Metabolism, pp 195-232. Boulton, A. A., Baker, G. B., Butterworth, R. F. eds. The Humana Press, Clifton, NJ (1983).
15. Herskovitch, P. Measurement of regional cerebral hemodynamics and metabolism by positron emission tomography. In Neuro-methods 8. Imaging and Correlative Physicochemical Techniques, pp 179-232. Boulton, A. A., Baker, G. B., Boisvert, D. P. J. eds. The Humana Press, Clifton, NJ (1988)
16. Noremberg, D. The distribution of glutamine synthethase in the rat central nervous system. J. Histochem. Cytochem. 27, 756-762 (1979).
17. Laake, J. H., Torp, R., Ottersen, O. P. Ultrastructural immunocytochemical studies as a means or distinguishing between transmitter and non-transmitter glutamate. Biochem. Soc. Trans. 21, 47-49 (1993).
18. Berl, S., Clarke, D. D. The metabolic compartmentation concept. In Glutamine, Glutamate and GABA in the Central Nervous System, pp 205-217. Hertz, L., Kvame, E., McGeer, G., Schousboe, A. eds. Liss, New York (1983).
19. Erecinska, M., Silver, I. Metabolism and role of glutamate in mammalian brain. Prog. Neurobiol. 35, 245-296 (1990).
20. Bachelard, H., Baddar-Goffer, R. NMR spectroscopy in neurochemistry. J. Neurochem. 61, 412-429 (1993).
21. 13C nuclear magnetic resonance spectroscopy. Essays Biochem. 26, 105-119 (1991).
22. 13C NMR spectroscopy to metabolic studies in animals. In Carbon-13 NMR Spectroscopy of Biological Systems, pp 155-267. Beckmann, N. ed. New York, Academic Press (1995).
23. Schousboe A., Westergaard N., Waagepetersen H. S., Larsson O. M., Bakken I. J., Sonnewald U. Trafficking between glia and neurons of TCA cycle intermediates and related metabolites. Glia 21, 99-105 (1997).
24. Cooper, A. J. L., Plum, F. Biochemistry and physiology of brain ammonia. review. Physiol. Rev. 67, 440-519 (1987).
25. Yudkoff, M., Nissim, I., Hertz, L., Pleasure, D., Erecinska, M. Nitrogen metabolism: neuronal-astroglial relationships. In Neuronal-Astrocytic Interactions. Vol 94. Yu, A. C. H., Hertz, L., Norenberg, M. D., Syková, E., Waxman, S. G. eds. Elsevier, Amsterdam pp. 213-224 (1992).
26. Lajhta, A., Berl, S., Waelch H. Amino acid and protein metabolism of the brain IV. The metabolism of glutamic acid. J. Neurochem. 3, 322-332 (1959).
27. Berl, S., Lajhta, A., Waelch, H. Amino acid and protein metabolism VI. Cerebral compartments of glutamic acid metabolism. J. Neurochem. 7, 186-192 (1961).
28. Berl, S., Takagi, T., Clarke, D. D., Waelch, H. Metabolic compartments in vivo. Ammonia and glutamic acid metabolism in brain and liver. J. Biol. Chem. 237, 2562-2569 (1962).
29. Berl, S., Takagi, T., Clarke, D. D., Waelch, H. Carbon dioxide fixation in the brain. J. Biol. Chem 237, 2570-2573 (1962).
30. Berl, S., Clarke, D. D. Compartmentation of amino acid metabolism. In Handbook of Neurochemistry, Lajhta, A. ed. Plenum Press, New York 2, pp 447-472 (1969).
31. Garfinkel, D. A simulation study of the metabolism and compartmentation in brain of glutamate, aspartate, the Krebs cycle and related metabolites. J. Biol. Chem. 241, 3918-3929 (1966).
32. Balazs, R., Patel, A. J., Richter, D. Metabolic compartments in the brain: their properties and relation to morphological structures. In Metabolic Compartmentation in the Brain, pp 167-184. Balazs, R. and Cremer, J. E. eds. Macmillan, New York (1972).
33. Van den Berg, C. J., Garfinkel, D. A simulation study of brain compartments. Metabolism of glutamate and related substances in mouse brain. Biochem. J. 123, 211-218 (1971).
34. Benjamin, A. M., Quastel, J. H. Fate of L-glutamate in the brain. J. Neurochem. 23, 457-464 (1974).
35. Benjamin, A. M., Quastel, J. H. Locations of amino acids in brain slices from the rat. Tetrodoxin-sensitive release of amino acids. Biochem. J. 128, 631-646 (1972).
36. Muir, D., Berl, S., Clarke, D. D. Acetate and fluoroacetate as possible markers for glia metabolism in vivo. Brain Res. 380, 336-340 (1986).
37. Yu, A. C. H., Drejer, J., Hertz, L., Schousboe, A. Pyruvate carboxylase activity in primary cultures of astrocytes and neurons. J. Neurochem. 41, 1484-1487 (1983).
38. Kuriyama, K., Ohkuma, S. Development of cerebral GABAergic neurons in vitro. In Model Systems of Development and Aging of the Nervous System, pp 45-56. Vernadakis, A. Privat, J. M. Lauder, P. S. Timiras, E. Giacobini eds. Nihoff, Boston, MA (1987).
39. Schousboe, A., Westegard, N., Hertz, L. Neuronal-astrocytic interactions in glutamate metabolism. Biochem. Soc. Trans. 21, 49-53 (1992).
40. 13C NMR spectroscopy. J. Biol. Chem. 263, 6964-6971 (1988).
41. 13C isotope isomers. Am. J. Physiol. 28, H987-H995 (1990).
42. Passoneau, J., Lowry, O. H. Phosphofructokinase and the Pasteur effect. Biochem. Biophys. Res. Commun. 7, 10-15 (1962).
43. 14C) glucose. J. Neurochem. 59, 1430-1436 (1992).
44. Mason, G. F., Rothman, D. L., Behar, K. L., Shulman, R. G. NMR determination of the TCA cycle rate and α-ketoglutatarate/glutamate exchange in rat brain. J. Cereb. Blood Flow Metab. 12, 434-447 (1992).
45. Krebs, H. A. Rate control of the tricarboxylic acid cycle. In Advances in Enzyme Regulation, pp 335-353. Weber, G. Ed. Pergamon Press, Oxford, (1970).
46. 13C) glucose. Magn. Reson. Med. 3, 911-920 (1986).
47. 13C nuclear magnetic resonance studies of glucose metabolism in guinea pig brain slices. Biochem. Soc. Trans. 14, 1720-1721 (1986).
48. 13C decouple spectroscopic measurements of lactate and glutamate in rat brain in vivo. Proc. Natl Acad. Sci. USA. 81, 6330-6334 (1985).
49. 13C-edited NMR spectroscopy. J. Cereb. Blood Flow Metab. 10, 170-179 (1990).
50. Mason, G. F., Gruetter, R., Rothman, D. L., Behar, K. L., Shulman, R. G., Novotny, E. G. Simultaneous determination of the TCA cycle, glucose utilization. α-ketoglutarate/glutamate exchange and glutamine synthesis in human brain by NMR. J. Cereb. Blood Flow Metab. 15, 12-25 (1995).
51. 13C]NMR. Proc. Natl Acad. Sci. USA 93, 7612-7617 (1996).
52. 13C NMR measurements of cerebral glutamine synthesis as evidence for glutamate-glutamine cycling. Proc. Natl Acad. Sci. USA 94, 2699-2704 (1997).
53. Sibson, N. R., Dhankar, A., Mason, G. F., Rothman, D. L., Behar, K. L., Shulman, R. G. Stoichiometric coupling of brain metabolism and glutamatergic neuronal activity. Proc. Natl Acad. Sci. USA 95, 316-321 (1998).
54. 13C NMR spectroscopy: a technique for investigating metabolic compartmentation in the brain. Biochem. J. 266, 133-139 (1990).
55. 13C n.m.r. study. Biochem. J. 282, 225-230 (1992).
56. 13C NMR. J. Biol. Chem. 265, 12916-12926 (1990).
57. 13C nuclear magnetic resonance evidence for γ-aminobutyrate formation via pyruvate carboxylase in rat brain: a metabolic basis for compartmentation. J. Neurochem. 53, 1285-1292 (1989).
58. 13C]glucose metabolism J. Neurochem. 61, 315-323 (1993).
59. 13C] glucose metabolites. J. Biol. Chem. 269, 27198-27208 (1994).
60. 13C NMR spectroscopy. NMR Biomed. 6, 264-277 (1994).
61. Preece, N., Cerdán, S. Metabolic precursors and compartmentation of cerebral GABA in vigabatrin treated rats. J. Neurochem. 67, 1718-1725 (1996).
62. 2) acetate. Endocrinology 136, 296-305 (1995).
63. 13C) glutamine in cultured astrocytes studied by NMR spectroscopy: first evidence of astrocytic pyruvate recycling. J. Neurochem. 67, 2566-2572 (1996).
64. 13C) NMR spectroscopy that glutamine from astrocytes is a precursor for GABA synthesis in neurons. Neurochem. Int. 22, 19-29 (1993).
65. Martin, M., Canioni, P. and Merle, M. Analysis of carbon metabolism in cultured cerebellar and cortical astrocytes. Cell Mol. Biol. 43, 631-643 (1997).
66. 13C) glucose inoculation. Eur. J. Biochem. 217, 457-468 (1993).
67. 13C) glucose metabolism in rat cerebellar granule cells and astrocytes in primary culture. Eur. J. Biochem. 217, 617-625 (1993).
68. 13C glucose. Eur. J. Biochem. 239, 742-751 (1996).
69. Aghajanian, G. K., Bloom, F. E. The formation of synaptic junctions in developing rat brain: a quantitative electron microscopic study. Brain Res. 6, 716-727 (1967).
70. Fazekas, J. F., Burton, G. F., Alman, R. W. The influence of the thyroid state on cerebral metabolism. Endocrinology 48, 169-174 (1950).
71. 15N NMR. J. Biol. Chem. 270, 24805-24809 (1995).
72. 15N heteronuclear multiple-quantum coherence transfer NMR. Biochem. J. 311, 681-688 (1995).
73. 15N nuclear magnetic resonance. Biochem. J. 305, 329-336 (1995).
74. Paulsen, R. E., Odden, E. and Fonnum, F. Importance of glutamine for gamma-aminobutyric acid synthesis in rat neostriatum in vivo. J. Neurochem. 51, 1294-1299 (1988).
75. Cooper, A. J. L., Mora, S. L., Cruz, N. F., Gelbard, A. S. Cerebral ammonia metabolism in hyperammoniemic rats. J. Neurochem. 44, 1716-1723 (1985).
76. 3]-glutamate transport in glial cultures. J. Neurochem. 64, 2572-2580 (1995).
77. Nilsson, M., Hansson, E., Rönnback, L. Interactions between valproate, glutamate, aspartate and GABA with respect to uptake in astroglial primary cultures. Neurochem. Res. 17, 327-332 (1992).
78. Yu, A. C. H., Hertz, L. Uptake of glutamate, GABA and glutamine into a predominantly GABAergic and a predominantly glutamatergic nerve cell population. J. Neurosci. Res. 7, 23-35 (1982).
79. Peng, L., Hertz, L., Sonnewald, U., Petersen, S. B., Westergaard, N., Larsson, O., Schousboe, A. Utilization of glutamine and of TCA cycle constituents as precursors for transmitter glutamate and GABA. Dev. Neurosci. 15, 367-377 (1993).
80. Hassel, B., Sonnewald, U., Unsgard, G., Fonnum, F. NMR spectroscopy of cultured astrocytes: effects of glutamine and the gliotoxin fluorocitrate. J. Neurochem. 62, 2187-2194 (1994).
81. 13C) NMR spectroscopy of cultured neurons and astrocytes. Neurosci. Lett. 128, 235-239 (1991).
82. Westergaard, N., Sonnewald, U., Unsgard, G., Peng, L., Hertz, L. and Schousboe, A. Uptake release and metabolism of citrate in neurons and astrocytes in primary cultures. J. Neurochem. 62, 1727-1733 (1994).
83. Hertz, L., Yu, A. C. H., Schousboe, A., Uptake and metabolism of malate in neurons and astrocytes in primary cultures. J. Neurosci. Res. 33, 289-296 (1992).
84. Erecinska, M., Nelson, D., Nissim, I., Daikhin and Yudkoff, M. Cerebral alanine transport and alanine aminotransferase reaction: alanine as source of neuronal glutamate. J. Neurochem. 62, 1953-1964 (1994).
85. Tsacopoulos, M., Magistretti, P. J. Metabolic coupling between glia and neurons. J. Neurosci. 16, 877-885 (1996).
86. 13C) NMR spectroscopy. Neuroreport 6, 2201-2204 (1995).
87. 13C nuclear magnetic resonance spectroscopy. J. Cereb. Blood Flow Metab. 18, 109-117 (1998).
88. Schurr, A., West, C. A. and Rigor, B. M. Lactate-supported synaptic function in the rat hippocampal slice preparation. Science 240, 1326-1328 (1988).
89. Schurr, A., Payne, R. S., Miller, J. J., Rigor, B. M. Brain lactate, not glucose, fuels the recovery of synaptic function from hypoxia upon reoxygenation: an in vitro study. Brain Res. 744, 105-111 (1997).
90. Pascual, J. M., Carceller, F., Roda, J. M., Cerdán, S. Glutamate, glutamine and GABA as substrates for the neuronal and glial compartments after focal cerebral ischemia in rats. Stroke 29, 1048-1057 (1998).
91. 31P-n.m.r. study. Biochem. J. 291, 915-919 (1993).
92. Gamberino, W. C., Berkich, D. A., Lynch, C. J., Xu, B., LaNoue, K. F. Role of pyruvate carboxylase in facilitation of synthesis of glutamate and glutamine in culured astrocytes. J. Neurochem. 69, 2312-2325 (1997).
93. Chan, P. H. Role of oxidants in ischemic brain damage. Stroke 27, 1124-1129 (1998).
94. Ruiz, F., Alvarez, G., Pereira, R., Hernández, M., Villalba, M., Cruz, F., Cerdán, S., Bogónez, E., Satrústegui, J. Protection by pyruvate and malate against glutamate mediated neurotoxicity. Neuroreport 9, 1277-1282 (1998).
95. 3]propionate. FEBS Lett. 412, 131-137 (1997).
96. Magistretti, P. G., Pellerin, L., Rothman, D. L., Shulman, R. G. Energy on demand. Science 283, 496-497 (1999).
97. Waniewski, R. A., Martin, D. L. Preferential utilization of acetate by astrocytes is attributable to transport. J. Neurosci 18, 5225-5233 (1998).