Energetic demands of the Na+/K+ ATPase in mammalian astrocytes

GLIA

Volumn 21, Issue 1, 1997, Pages 35-45

  Silver, Ian A ^a   Erecińska, Maria ^a,b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Astrocyte; ATP; C6 cells; Ions; Na+ K+ pump

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATE; CALCIUM; POTASSIUM; SODIUM;

ANIMAL; ARTICLE; ASTROCYTE; BRAIN; CELL CULTURE; ENERGY METABOLISM; FETUS; GLIA; GLIOMA; MAMMAL; METABOLISM; MOUSE; PH;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; ASTROCYTES; BRAIN; CALCIUM; CELLS, CULTURED; ENERGY METABOLISM; FETUS; GLIOMA; HYDROGEN-ION CONCENTRATION; MAMMALS; MICE; NA(+)-K(+)-EXCHANGING ATPASE; NEUROGLIA; POTASSIUM; SODIUM; TUMOR CELLS, CULTURED;

EID: 0031239472     PISSN: 08941491     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-1136(199709)21:1<35::AID-GLIA4>3.0.CO;2-0     Document Type: Article

References (101)

1. +-adenosine triphosphatase and associated ion fluxes in cultures from rat brain. Neuroscience, 14:361-373.
2. +-ATPase activity of glial, neuronal and synaptosomal enriched fractions from normal and freezing-injured rabbit cerebral cortex. Neurochem. Res., 12:607-612.
3. Ballanyi, K., Grafe, P., and Ten Bruggencate, G. (1987) Ion activities and potassium uptake mechanisms of glial cells in guinea-pig olfactory cortex slices. J. Physiol., 382:159-174.
4. Bowman, C.L. and Kimelberg, H.K. (1984) Excitatory amino acids directly depolarize rat brain astrocytes in primary cultures. Nature, 311:656-659.
5. Boyarsky, G., Ransom, B., Schlue, W.-R., Davis, M.B.E., and Boron, W.F. (1993) Intracellular pH regulation in single cultured astrocytes from rat forebrain. Glia, 8:241-248.
6. +-ATPase catalytic subunits in cultured neurons and glia: evidence for polarized distribution in neurons. Brain Res., 631:1-11.
7. Brookes, N. and Yarowsky, P.J. (1985) Determinants of deoxyglucose uptake in cultured astrocytes: the role of the sodium pump. J. Neurochem., 44:473-479.
8. Cambray-Deakin, M., Pearce, B., Morrow, C., and Murphy, S. (1988) Effects of extracellular potassium on glycogen stores of astrocytes in vitro. J. Neurochem., 51:1846-1851.
9. Cameron, R., Klein, L., Shyjan, A.W., Rakic, P., and Levenson, R. (1994) Neurons and astroglia express distinct subsets of Na,K-ATPase α and β subunits. Mol. Brain Res., 21:333-343.
10. Chesler, M. and Kraig, R.P. (1989) Intracellular pH transients of mammalian astrocytes. J. Neurosci., 9:2011-2019.
11. Chow, S.-Y., Li, J., and Woodbury, D.M. (1992) Water and electrolyte contents, cell pH, and membrane potential of primary cultures of astrocytes from DBA, C57 and SW mice. Epilepsia, 33:393-401.
12. Chow, S.Y., Yen-Chow, Y.C., White, H.S., and Woodbury, D.M. (1991) pH regulation after acid load in primary cultured of mouse astrocytes. Dev. Brain Res., 60:69-78.
13. Cummins, C.J., Lust, W.D., and Passonneau, J.V. (1983) Regulation of cerebral glycogen metabolism in primary and transformed astrocytes in vitro. J. Neurochem., 40:128-136.
14. 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. Neurosci. Res., 18:551-561.
15. Erecińska, M., Dagani, F., Nelson, D., Deas, J., and Silver, I.A. (1991) Relations between intracellular ions and energy metabolism: a study with monensin in synaptosomes, neurons, and C6 glioma cells. J. Neurosci., 11:2410-2421.
16. Erecińska, M., Deas, J., and Silver, I.A. (1995) The effect of pH on glycolysis and phosphofructokinase activity in cultured cells and synaptosomes. J. Neurochem., 65:2765-2772.
17. Erecińska, M., Nelson, D., Dagani, F., Deas, J., and Silver, I.A. (1993) Relations between intracellular ions and energy metabolism under acidotic conditions: A study with nigericin in synaptosomes, neurons and C6 glioma cells. J. Neurochem., 61:1356-1368.
18. Erecińska, M. and Silver, I.A. (1986) The role of glial cells in regulation of neurotransmitter amino acids in the external environment. I. Transmembrane electrical and ion gradients and energy parameters in cultured glial-derived cell lines. Brain Res., 369:193-202.
19. Ereciriska, M. and Silver, I.A. (1989) ATP and brain function. J. Cereb. Blood Flow Metab., 9:2-19.
20. Erecińska, M. and Silver, I.A. (1994) Ions and energy in mammalian brain. Prog. Neurobiol., 43:37-71.
21. Eriksson, G., Peterson, A., Iverfeldt, K., and Walum, E. (1995) Sodium-dependent glutamate uptake as an activator of oxidative metabolism in primary astrocyte cultures from newborn rat. Glia, 15:152-156.
22. Finkbeiner, S.M. (1993) Glial calcium. Glia, 9:83-104.
23. Futamachi, K.J. and Pedley, T.A. (1976) Glial cells and extracellular potassium: their relationship in mammalian cortex. Brain Res., 109:311-322.
24. Gemba, T., Oshima, T., and Ninomiya, M. (1994) Glutamate efflux via the reversal of the sodium-dependent glutamate transporter caused by glycolytic inhibition in rat cultured astrocytes. Neuroscience, 63:789-795.
25. Glynn, I.A. and Karlish, S.J.D. (1975) The sodium pump. Annu. Rev. Physiol., 37:13-55.
26. Goldman, W.F., Yarowsky, P.J., Juhaszova, M., Krueger, B.K., and Blaustein, M.P. (1994) Sodium/calcium exchange in rat cortical astrocytes. J. Neurosci., 14:5834-5843.
27. Gregory, G.A., Welsh, F.A., Yu, A.C.H., and Chan, P.H. (1990) Fructose-1,6-bisphosphate reduces ATP loss from hypoxic astrocytes. Brain Res., 516:310-312.
28. +)-ATPase in bulk isolated glial and synaptosomes of epileptogenic cortex. Brain Res., 261:75-84.
29. Harold, D.E. and Walz, W. (1992) Metabolic inhibition and electrical properties of type-1-like cortical astrocytes. Neuroscience, 47:203-211.
30. Hertz, E., Shargool, M., and Hertz, L. (1986) Effects of barbiturates on energy metabolism by cultured astrocytes and neurons in the presence of normal and elevated concentrations of potassium. Neuropharmacology, 25:533-539.
31. Hertz, L. (1966) Neuroglial localization of potassium and sodium effects on respiration in brain. J. Neurochem., 13:1373-1387.
32. + induced stimulation of oxygen uptake in cultured cerebral glial cells. Brain Res., 60:517-520.
33. Hertz, L., Drejer, J., and Schousboe, A. (1988) Energy metabolism in glutamatergic neurons, GABAergic neurons and astrocytes in primary cultures. Neurochem. Res., 13:605-610.
34. Hori, O., Matsumoto, M., Maeda, Y., Ueda, H., Ohtsuki, T., Stern, D.M., Kinoshita, T., Ogawa, S., and Kamada, T. (1994) Metabolic and biosynthetic alterations in cultured astrocytes exposed to hypoxia/oxygenation. J. Neurochem., 62:1489-1495.
35. Ikehara, T., Yamaguchi, H., Hosokawa, K., Sakai, T., and Miyamoto, H. (1984) Rb influx in response to changes in energy generation: Effect of regulation of the ATP content of HeLa cells. J. Cell. Physiol., 119:273-282.
36. +-ATPase) activity in the central nervous system. Acta Histochem. Cytochem., 16:277-285.
37. Jameson, N., Olson, J., Nguyen, H., and Holtzman, D. (1984) Respiration of primary cultured cerebellar granule neurons and cerebral cortical neurons. J. Neurochem., 42:470-474.
38. + exchange system in glial cell lines. Properties and activation by an hyperosmotic shock. Eur. J. Biochem., 160:211-219.
39. Kauppinen, R.A., Enkvist, K.I.H., and Akerman, K.E.O. (1988) Glucose deprivation depolarizes plasma membrane of cultured astro-cytes and collapses transtnembrane potential and glutamate gradients. Neuroscience, 26:283-289.
40. + concentrations and acidosis in vitro. Neurochem. Pathol., 9:109-125.
41. Kimelberg, H.K., Biddlecome, S., Narumi, S., and Bourke, R.S. (1978a) ATPase and carbonic anhydrase activities of bulk isolated neurons, glia and synaptosome fractions from rat brain. Brain Res., 141:305-323.
42. Kimelberg, H.K., Bowman, C., Biddlecome, S., and Bourke, R.I. (1979) Cation transport and membrane potential properties of primary astroglial cultures from neonatal rat brain. Brain Res., 177:533-550.
43. Kimelberg, H.K. and Goderie, S.K. (1988) Volume regulation after swelling in primary astrocyte cultures. Neurol. Neurobiol., 39:299-311.
44. Kimelberg, H.K., Narumi, S., and Bourke, R.S. (1978b) Enzymatic properties and morphological development of primary rat brain astrocyte cultures and enzyme development in vivo. Brain Res., 153:55-77.
45. +) ATPase activity in cultured glioma and neuroblastoma cells. J. Neurochem., 22:971-976.
46. + in a glial cell line. Brain Res., 104:93-105.
47. Kukes, G., Elul, R., and De Vellis, J. (1976a) The ionic basis of the membrane potential in a rat glial cell line. Brain Res., 104:71-92.
48. Latzkovits, L., Torday, C., Labourdette, G., Pettmann, B., and Sensenbrenner, M. (1988) Sodium and potassium uptake in primary cultures of proliferating rat astroglial cells induced by short-term exposure to an astroglial growth factor. Neurochem. Res., 13:837-848.
49. Longuemare, M.C., Hill, M.P., and Swanson, R.A. (1994) Glycolysis can prevent non-synaptic excitatory amino acid release during hypoxia. NeuroReport, 5:1789-1792.
50. Lopez-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.
51. Lothman, E., LaManna, J., Cordingley, G., Rosenthal, M., and Somjen, G. (1975) Responses of electrical potential, potassium levels and oxidative metabolic activity of the cerebral neocortex of cats. Brain Res., 88:15-36.
52. Lothman, E.W. and Somjen, G.G. (1975) Extracellular potassium activity, intracellular and extracellular potential responses in the spinal cord. J. Physioi. (London), 252:115-136.
53. Lust, W.D., Schwartz, J.P., and Passonneau, J.V. (1975) Glycolytic metabolism in cultured cells of the nervous system. I. Glucose transport and metabolism in the C6 glioma cell like. Mol. Cell. Biochem., 8:169-181.
54. Medzihradsky, F., Nandhasri, P.S., Idoyaga-Vargas, V., and Sellinger, O.Z. (1971) A comparison of the ATPase activity of the glial cell fraction and the neuronal perikaryal fraction isolated in bulk from rat cerebral cortex. J. Neurochem., 18:1599-1603.
55. Molloy, G.R., Wilson, C.D., Benfield, P., deVellis, J., and Kumar, S. (1992) Rat brain creatine kinase messenger RNA levels are high in primary cultures of brain astrocytes and oligodendrocytes and low in neurons. J. Neurochem., 59:1925-1932.
56. + influx in cultured primary astrocytes. Brain Res., 655:110-114.
57. +-ATPase activity of cultured newborn rat astroblasts during differentiation. Neurosci. Lett., 4:263-267.
58. Moonen, G., Franck, G., and Schoffeniels, E. (1980) Glial control of neuronal excitability in mammals. 1. Electrophysiological and isotopic evidence in culture. Neurochem. Int., 2:299-310.
59. Ogata, T., Nakamura, Y, Tsuji, K., Shibata, T., and Kataoka, K. (1995) A possible mechanism for the hypoxia-hypoglycemia-induced release of excitatory amino acids from cultured hippocampal astrocytes. Neurochem. Res., 20:737-743.
60. Olson, J.E. and Holtzman, D. (1981) Factors influencing the growth and respiration of rat cerebral astrocytes in primary culture. Neurochem. Res., 6:1337-1343.
61. Olson, J.E., Sankar, R., Holtzman, D., James, A., and Fleischhacker, D. (1986) Energy-dependent volume regulation in primary cultured cerebral astrocytes. J. Cell. Physiol., 128:209-215.
62. Pappas, C.A. and Ransom, B.R. (1994) Depolarization-induced alkalinization (DIA) in rat hippocampal astrocytes. J. Neurophysiol., 72:2816-2826.
63. Pasqualatto, B.A. and Shaw, C.A. (1996) Regulation of ionotropic receptors by protein phosphorylation. Biochem. Pharmacol., 51: 1417-1425.
64. Pauwels, P.J., Opperdoes, F.R., and Trouet, A. (1985) Effects of antimycin, glucose deprivation, and serum on cultures of neurons, astrocytes, and neuroblastoma cells. J. Neurochem., 44:143-148.
65. Pellerin, L. and Magistretti, P.J. (1994) Glutamate uptake in astrocytes stimulates aerobic glycolysis: A mechanism coupling neuronal activity to glucose utilization. Proc. Natl. Acad. Sci. U.S.A., 91:10625-10629.
66. Peng, L., Zhang, X., and Hertz, L. (1994) High extracellular potassium concentrations stimulate oxidative metabolism in a glutamatergic neuronal culture and glycolysis in cultured astrocytes but have no stimulatory effect in a GABAergic neuronal culture. Brain Res., 663:168-172.
67. Peuchen, S., Duchen, M.R., and Clark, J.B. (1996) Energy metabolism in adult cultured astrocytes in vitro. Neuroscience, 71:855-870.
68. Pianet, I., Merle, M., Labousse, J., and Canioni, P. (1991) Phosphorus-31 nuclear magnetic resonance of C6 glioma cells in rat astrocytes. Eur. J. Biochem., 195:87-95.
69. Ransom, B.R. and Goldring, S. (1973) Ionic determinants of membrane potential of cells presumed to be glia in cerebral cortex of cat. J. Neurophysiol., 36:855-868.
70. + dependence similar to that of brain astrocytes. Neurosci. Lett., 59:281-284.
71. +)-activated ATPase. Enzymatic and transport properties. Biochim. Biophys. Acta, 549:145-176.
72. Rose, C.R. and Ranson, B.R. (1996) Intracellular sodium homeostasis in rat hippocampal astrocytes. J. Physiol. (London), 491:291-305.
73. + ATPase activity in astrocytes cultured from dissociated brain hemispheres. J. Neurochem., 26:1053-1055.
74. Shrode, L.D. and Putnam, R.W. (1994) Intracellular pH regulation in primary rat astrocytes and C6 glioma cells. Glia, 12:196-210.
75. Siesjö, B.K. (1978) Brain Energy Metabolism. John Wiley and Sons, New York, pp. 1-607.
76. Silver, I.A., Deas, J., and Erecińska, M. (1997) Ion homeostasis in brain cells. Differences in intracellular ion responses to energy limitation between cultured neurons and glial cells. Neuroscience, 78:589-601.
77. 2+] in hypoxia and ischemia in rat brain in vivo. J. Gen. Physiol., 95:837-866.
78. +] in the hippocampus during recovery from short-term, transient ischemia. J. Cereb. Blood Flow. Metab., 12:759-772.
79. Soltoff, S.P. and Mandel, L.P. (1984) Active ion transport in the renal proximal tubule. J. Gen. Physiol., 84:643-662.
80. Sonnewald, U., Müller, T.B., Westergaard, N., Unsgård, G., Petersen, S.B., and Schousboe, A. (1994) NMR spectroscopic study of cell cultures of astrocytes and neurons exposed to hypoxia: compartmentation of astrocyte metabolism. Neurochem. Int., 24:473-483.
81. +-ATPase activity. J. Neurosci., 14:2464-2475.
82. Sorg, O. and 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.
83. +-ATPase in brain. Fed. Proc., 35:1260-1265.
84. Swanson, R.A., Yu, A.C.H., Sharp, F.R., and Chan, P.H. (1989) Regulation of glycogen content in primary astrocyte culture: effects of glucose analogues, phenobarbital and methionine sulfoximine. J. Neurochem., 52:1359-1365.
85. +)-stimulated ATPase in brain. J. Biol. Chem., 254:6060-6067.
86. Tessitore, N., Sakhrani, L.M., and Massry, S.G. (1986) Quantitative requirement for ATP for active transport in isolated renal cells. Am. J. Physiol., 251:C120-C127.
87. Tombaugh, G.C. and Sapolsky, R.M. (1992) Corticosterone accelerates hypoxia- and cyanide-induced ATP loss in cultured hippocampal astrocytes. Brain Res., 588:154-158.
88. Tymiak, A.A., Norman, J.A., Bolgar, M., DiDonato, G.C., Lee, H., Parker, W.L., Lo, L.-G, Berova, N., Nakanishi, K., Haber, E., and Haupert, J.G.T. (1993) Physicochemical characterization of a ouabain isomer isolated from bovine hypothalamus. Proc. Natl. Acad. Sci. U.S.A., 90:8189-8193.
89. Vanderkooi, J.M., Erecińska, M., and Silver, I.A. (1991) Oxygen in mammalian tissue: methods of measurement and affinities of various reactions. Am. J. Physiol., 260:C1131-1150.
90. Walz, W. (1989) Role of glial cells in the regulation of the brain microenvironment. Prog. Neurobiol., 33:309-333.
91. Walz, W. and Hertz, L. (1982) Ouabain-sensitive and ouabainresistant net uptake of potassium into astrocytes and neurons in primary cultures. J. Neurochem., 39:70-77.
92. Walz, W. and Hertz, L. (1983) Intracellular ion changes of astrocytes in response to extracellular potassium. J. Neurosci. Res., 10:411-423.
93. Walz, W. and Hinks, E.C. (1986) A transmembrane sodium cycle in astrocytes. Brain Res., 368:226-232.
94. Walz, W. and Kimelberg, H.K. (1985) Differences in cation transport properties of primary astrocyte cultures from mouse and rat brain. Brain Res., 340:333-340.
95. Walz, W. and Mukerji, S. (1988) Lactate release from cultured astrocytes and neurons. A comparison. Glia, 1:366-370.
96. Walz, W., Wuttke, W., and Hertz, L. (1984) Astrocytes in primary cultures: membrane potential characteristics reveal exclusive potassium conductance and potassium accumulator properties. Brain Res., 292:367-374.
97. Wuttke, W. and Walz, W. (1990) Sodium- and bicarbonate-independent regulation of intacellular pH in cultured mouse astrocytes. Neurosci. Lett, 117:105-110.
98. Yager, J.Y., Kala, G., Hertz, L., and Juurlink, B.H.J. (1994) Correlation between content of high-energy phosphates and hypoxic-ischemic damage in immature and mature astrocytes. Dev. Brain Res., 82:62-68.
99. Yamada, H., Naruse, M., Naruse, K., Demura, H., Takahashi, H., Yoshimura, M., and Ochi, J. (1992) Histological study on ouabain immunoreactivities in the mammalian hypothalamus. Neurosci. Lett., 141:143-146.
100. Yarowsky, P., Boyne, A.F., Wierwille, R., and Brookes, N. (1986) Effect of monensin on deoxyglucose uptake in cultured astrocytes: energy metabolism is coupled to sodium entry. J. Neurosci., 6:859-866.
101. Yoshimine, T., Morimoto, K., Homburger, H.A., and Yanagihara, T. (1983) Immunochemical localization of creatine kinase BB-isoenzyme in human brain: Comparison with tubulin and astroprotein. Brain Res., 265:101-108.