Lactate spares glucose as a metabolic fuel in neurons and astrocytes from primary culture

Neuroscience Research

Volumn 26, Issue 4, 1996, Pages 369-376

  Tabernero, A ^a   Vicario, C ^a   Medina, J M ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

Brain; Hyperlactiacidemia; Hypoglycaemia; Metabolism

Indexed keywords

FATTY ACID ESTER; GLUCOSE; LACTIC ACID; LIPID; PYRUVATE DEHYDROGENASE; STEROL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN METABOLISM; CITRIC ACID CYCLE; CONTROLLED STUDY; GLUCOSE METABOLISM; GLUCOSE OXIDATION; GLUCOSE UTILIZATION; LIPOGENESIS; NERVE CELL; NERVE CELL CULTURE; NEWBORN; NONHUMAN; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL; RAT;

ANIMALS; ASTROCYTES; CELLS, CULTURED; GLUCOSE; IMMUNOHISTOCHEMISTRY; LACTIC ACID; NEURONS; RATS; RATS, WISTAR;

EID: 0030465844     PISSN: 01680102     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-0102(96)01121-2     Document Type: Article

References (60)

1. Baquer, N.Z., Hothersall, J.S. and McLean, P. (1988) Function and regulation of the pentose phosphate pathway in brain. In: B.L. Horecker and E.R. Stadtman (Eds.), Current Topics in Cellular Regulation. Vol. 29, Academic Press, New York, pp. 265-289.
2. Bergmeyer, H.U., Bernt, E., Schmidt, F. and Stork, H. (1974) D-glucose determination with bexokinase and glucose-6-phosphate dehydrogenase. In: H.U. Bergmeyer (Ed.), Methods of Enzymatic Analysis. Vol. 3, Verlag Chemie International, Deerfield Beach, FL, pp. 1196-1201.
3. Bignami, A., Eng, L.F., Dahl, D. and Uyeda, C.T. (1972) Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res., 43: 429-435.
4. Bock, A., Tegtmeier, F., Hansen, A. and Holler, M. (1993) Lactate and postischemic recovery of energy metabolism and electrical activity in the isolated perfused rat brain. J. Neurosurg. Anesthesiol., 5: 94-103.
5. Cataldo, A.M. and Broadwell, R.D. (1986) Cytochemical identification of cerebral glycogen and glucose-6-phosphatase activity under normal and experimental conditions. I. Neurons and glia. J. Electron Microsc. Tech., 3: 413-437.
6. Cheeseman, A.J. and Clarck, J.B. (1988) Influence of the malate-aspartate shuttle on oxidative metabolism in synaptosomes. J. Neurochem., 50: 1559-1565.
7. Clark, J.B. and Lai, J.C.K. (1989) Glycolytic and TCA cycle enzymes. In: A.A. Boulton, G.B. Baker, and R.F. Butterworth (Eds.), Neuromethods. Carbohydrates and Energy Metabolism. Vol. 11, Humana Press, Clifton, New Jersey, pp. 283-306.
8. Cremer, J.E. (1981) Nutrients for the brain: problems in supply. Early Human Development, 5: 117-132.
9. Cuezva, J.M., Moreno, F.J., Medina, J.M. and Mayor, F. (1980) Prematurity in the rat. I. Fuels and gluconeogenic enzymes. Biol. Neonate, 37: 88-95.
10. Dahl, D. and Bignami, A. (1977) Preparation of antisera to neurofilament protein from chicken brain and human sciatic nerve. J. Comp. Neurol., 176: 645-658.
11. Dombrowski, G.J., Swiatek, K.R. and Chao, K.L. (1989) Lactate, 3-hydroxybutyrate and glucose as substrates for the early postnatal rat brain. Neurochem Res, 14: 667-675.
12. Dringen, R., Gebhardt, R. and Hamprecht, B. (1993a) Glycogen in astrocytes, possible function as lactate supply for neighboring cells. Brain Res., 62: 208-214.
13. Dringen, R., Wiesinger, H. and Hamprecht, B. (1993b) Uptake of L-lactate by cultured rat brain neurons. Neurosci. Lett., 163: 5-7.
14. Edmond, J. (1992) Energy metabolism in developing brain cells. Can. J. Physiol. Pharmacol., 70: S118-S129.
15. Edmond, J., Robbins, R.A., Bergstrom, J.D., Cole, R.A. and De Vellis, J. (1987) Capacity for substrate utilization in oxidative metabolism by neurons, astrocytes and oligodendrocytes from developing brain in primary culture. J. Neurosc. Res., 18: 551-561.
16. Fernandez, E., Valcarce, C., Cuezva, J.M. and Medina, J.M. (1983) Postnatal hypoglycæmia and gluconeogenesis in the newborn rat. Delayed onset of gluconeogenesis in prematurely delivered newborns. Biochem. J., 214: 525-532.
17. Girard, J.R., Cuendet, G.S., Marliss, E.B., Kevran, A., Rieutort, M. and Assan, R. (1973) Fuels, hormones and liver metabolism at term during the early postnatal period in the rat. J. Clin. Invest., 53: 3190-3200.
18. Gutmann, I. and Wahlefeld, A.W. (1974) L-(+)-Lactate determination with lactate dehydrogenase and NAD. In: H.U. Bergmeyer (Ed.), Methods of Enzymatic Analysis. Vol. 3, Verlag Chemie GmbH, Weinheim, pp. 1464-1468.
19. Hajra, A.K. and Burke, C. (1978) Biosynthesis of phosphatidic acid in rat brain via acyldihydroxyacetone phosphate. J. Neurochem., 31: 125-134.
20. Hertz, L., Drjer, J. and Schousboe, A. (1988) Energy metabolism in glutamatergic neurons, GABAergic neurons and astrocytes in primary cultures. Neurochem. Res., 13: 605-610.
21. Hertz, L. and Peng, L. (1992) Energy metabolism at the cellular level of the CNS. Can. J. Physiol. Pharmacol., 70: S145-S157.
22. Hothersall, J.S., Baquer, N.Z., Greenbaum, A.L. and McLean, P. (1979) Alternative pathways of glucose utilization in brain. Changes in the pattern of glucose utilization in brain during development and the effect of phenazine methosulphate on the integration of metabolic routes. Arch. Biochem. Biophys., 198: 478-492.
23. Hothersall, J.S., Zubariu, S., McLean, P. and Greenbaum, A.L. (1981) Alternative pathways of glucose utilization in brain; changes in the pattern of glucose utilization in brain resulting from treatment of rats with 6-aminonicotinamide. J. Neurochem., 37: 1484-1496.
24. Izumi, Y., Benz, A., Zorumski, C. and Olney, J. (1994) Effects of lactate and pyruvate on glucose deprivation in rat hippocampal slices. Neuroreport, 5: 617-20.
25. Juanes, M.C., Arizmendi, C. and Medina, J.M. (1986) Attenuation of postnatal hypoxia in the premature newborn rat by maternal treatment with dexamethasone: its relationship with lung phospholipid content. Biol. Neonate, 50: 337-344.
26. Katoh-Semba, R., Keino, H. and Kashiwamata, S. (1988) A possible contribution by glial cells to neuronal energy production: enzymehistochemical studies in the developing rat cerebellum. Cell Tissue Res., 252: 133-139.
27. Kaufman, E.E. and Driscoll, B.F. (1992) Carbon dioxide fixation in neuronal and astroglial cells in culture. J. Neurochem., 58: 258-262.
28. Ksiezak, H. and Gibson, G.E. (1981) Acetylcholine synthesis and CO2 production from various labeled glucose in rat brain slices and synaptosomes. J. Neurochem., 37: 88-94.
29. Larrabee, M.G. (1983) Lactate uptake and release in the presence of glucose by sympathetic ganglia of chicken embryos and by neuronal and nonneuronal cultures prepared from these ganglia. J. Neurochem., 40: 1237-1250.
30. 2 data. Fallibility of a classic equation when applied to non-homogeneous tissues. Biochem. J., 272: 127-132.
31. Larrabee, M.G. (1992) Extracellular intermediates of glucose metabolism: fluxes of endogenous lactate and alanine through extracellular pools in embryonic sympathetic ganglia. J. Neurochem., 59: 1041-1052.
32. Larrabee, M.G. (1995) lactate metabolism and its effect on glucose metabolism in an excised neural tissue. J. Neurochem., 64: 1734-1741.
33. Lopes-Cardozo, M., Larsson, O.M. and 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.
34. Lowry, O.H. and Passonneau, J.V. (1964) The relationships between substrates and enzymes of glycolysis in brain. J. Biol. Chem., 239: 31-42.
35. Lund-Andersen, H. (1979) Transport of glucose from blood to brain. Physiol. Rev., 59: 305-352.
36. Magistretti, P., Sorg, O., Yu, N., Martin, J. and Pellerin, L. (1993) Neurotransmitters regulate energy metabolism in astrocytes: implications for the metabolic trafficking between neural cells. Dev. Neurosci., 15: 306-12.
37. Maran, A., Cranston, I., Lomas, J., Macdonald, I. and Amiel, S. (1994) Protection by lactate of cerebral function during hypoglycaemia. Lancet, 343: 16-20.
38. McKenna, M.C., Tildon, J.T., Stevenson, J., Boatright, R. and Huang, S. (1993) Regulation of energy-metabolism in synaptic terminals and cultured rat-brain astrocytes. Diferences revealed using aminooxyacetate. Dev. Neurosci., 15: 320-329.
39. Medina, J.M., Cuezva, J.M. and Mayor, F. (1980) Non-gluconeogenic fate of lactate during the early neonatal period in the rat. FEBS Lett., 114: 132-134.
40. Medina, J.M., Vicario, C., Juanes, M. and Fernández, E. (1992) Biochemical adaptations to early extrauterine life. In: Herrera, E. and Knopp, R. (Eds.), Perinatal Biochemistry. CRC Press, Boca Raton, FL, pp. 233-258.
41. Pauwels, P.J. and Trouet, A. (1984) Role of fructose 2,6-bisphosphate in the regulation of glycolisis in various types of cultivated brain cell. Neurosci. Lett., 46: 173-177.
42. Peng, L., Schousboe, A. and Hertz, L. (1991) Utilization of α-ketoglutarate as a precursor for transmitter glutamate in cultured cerebellar granule cells. Neurochem. Res., 16: 29-34.
43. Poitry Yamate, C.L., Poitry, S. and Tsacopoulos, M. (1995) Lactate released by Muller glial cells is metabolized by photoreceptors from mammalian retina. J. Neurosci., 15 (7 Part 2): 5179-91.
44. Schurr, A., West, C.A. and Rigor, B.M. (1988) Lactate-supported synaptic function in the rat hippocampal slice preparation. Science, 240: 1326-1328.
45. Shank, R.P. and Campbell, G.L. (1984) α-Ketoglutarate and malate uptake and metabolism by synaptosomes: further evidence for an astrocyte-to-neuron metabolic shuttle. J. Neurochem., 42: 1153-1161.
46. Snyder, C.D. and Wilson, J.E. (1983) Relative levels of hexokinase in isolated neuronal, astrocytic, and oligodendroglial fractions from rat brain. J. Neurochem., 40: 1178-1181.
47. Sonnewald, U., Wang, A., Petersen, S., Westergaard, N., Schousboe, A., Erikson, R. and Skottner, A. (1995) 13C NMR study of IGF-I-and insulin-effects on mitochondrial function in cultured brain cells. Neuroreport, 6: 878-80.
48. Sonnewald, U., Westergaard, N., Hassel, B., Mueller, T., Unsgaard, G., Fonnum, F., Hertz, L., Schousboe, A. and Petersen, S. (1993) NMR spectroscopic studies of super(13)C acetate and super(13)C glucose metabolism in neocortical astrocytes: Evidence for mitochondrial heterogeneity. Dev. Neurosci., 15: 351-358.
49. Sonnewald, U., Westergaard, N., Krane, J., Unsgard, G., Petersen, S.B. and Schousboe, A. (1991) First direct demonstration of preferential release of citrate from astrocytes using NMR spectroscopy of cultured neurons and astrocytes. Neurosci. Lett., 128: 235-239.
50. Swanson, R.A. and Choi, D.W. (1993) Glial glycogen stores affect neuronal survival during glucose deprivation in vitro. J. Cereb. Blood Flow Metab., 13: 162-169.
51. Tabernero, A., Bolaños, J.P. and Medina, J.M. (1993) Lipogenesis from lactate in rat neurons and astrocytes in primary culture. Biochem. J., 294: 635-638.
52. Tabernero, A., Giaume, C. and Medina, J.M. (1996) Endothelin-1 regulates glucose utilization in cultured rat astrocytes by controlling intercellular communication through gap junctions. Glia, 16: 187-195.
53. Tildon, J.T., Mckenna, M.C., Stevenson, J. and Couto, R. (1993) Transport of L-Lactate by cultured rat brain astrocytes. Neurochem Res, 18: 177-184.
54. Vannucci, R.C., Nardis, E.E., Vannucci, S.J. and Campbell, P.A. (1981) Cerebral carbohydrate and energy metabolism during hypoglycemia in newborn dogs. Am. J. Physiol., 240: R192-R199.
55. Ventura, F., JL, R., Ambrosio, S., Gil, J. and Bartrons, R. (1991) 6-Phosphofructo-2-kinase/fructose-2,6-bisphosphatase in rat brain. Biochem. J., 276: 455-460.
56. Vicario, C. and Medina, J.M. (1992) Metabolism of lactate in the rat brain during the early neonatal period. J. Neurochem., 58: 32-40.
57. Vicario, C., Tabernero, A. and Medina, J.M. (1993) Regulation of lactate metabolism by albumin in rat neurons and astrocytes from primary culture. Pediatr. Res., 34: 709-715.
58. Walz, W. and Mukerji, S. (1988) Lactate release from cultured astrocytes and neurons: a comparison. Glia, 1: 366-370.
59. Westergaard, N., Varming, T., Peng, L., Sonnewald, U., Hertz, L. and Schousboe, A. (1993) Uptake, release, and metabolism of alanine in neurons and astrocytes in primary cultures. J. Neurosci. Res., 35: 540-545.
60. Willoughby, J., Harvey, S.A.K. and Clark, J.B. (1986) Compartmentation and regulation of acetylcholine synthesis at the synapse. Biochem. J., 235: 215-223.