Ionic transporter activity in astrocytes, microglia, and oligodendrocytes during brain ischemia

Journal of Cerebral Blood Flow and Metabolism

Volumn 33, Issue 7, 2013, Pages 969-982

  Annunziato, Lucio ^a,b   Boscia, Francesca ^a   Pignataro, Giuseppe ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b IRCCS SDN   (Italy)

Author keywords

astrocytes; ionic transporters; microglia; oligodendrocytes; stroke

Indexed keywords

2 [2 [4 (4 NITROBENZYLOXY)PHENYL]ETHYL]ISOTHIOUREA METHANESULFONATE; 2 [4 (2,5 DIFLUOROBENZYLOXY)PHENOXY] 5 ETHOXYANILINE; ADENOSINE TRIPHOSPHATE; AMILORIDE; BRADYKININ; BRADYKININ B1 RECEPTOR AGONIST; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM ION; FATTY ACID; GAMMA INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 3; INTERLEUKIN 6; IONIC TRANSPORTER; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MYELIN PROTEIN; NERVE GROWTH FACTOR; NEUROPEPTIDE; NEUROTROPHIN; NITRIC OXIDE; POTASSIUM CHLORIDE COTRANSPORTER; REACTIVE OXYGEN METABOLITE; SODIUM CALCIUM EXCHANGE PROTEIN; SODIUM ION; SODIUM PROTON EXCHANGE PROTEIN; SOMATOMEDIN; SUPEROXIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG;

APOPTOSIS; ASTROCYTE; BRAIN ISCHEMIA; CELL DAMAGE; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL POPULATION; CELL RENEWAL; CENTRAL NERVOUS SYSTEM; CEREBROVASCULAR ACCIDENT; CHEMOTAXIS; CYTOKINE PRODUCTION; FATTY ACID METABOLISM; GLIA; GLIA CELL; HUMAN; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; ION TRANSPORT; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MYELIN FORMING OLIGODENDROCYTE; MYELINATION; NERVE CELL; NONHUMAN; NONMYELINATING OLIGODENDROCYTE; OLIGODENDROCYTE PRECURSOR CELL; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW;

ANIMALS; ASTROCYTES; BRAIN ISCHEMIA; CELL SURVIVAL; HUMANS; ION CHANNELS; ION TRANSPORT; MICROGLIA; NEUROPROTECTIVE AGENTS; OLIGODENDROGLIA;

EID: 84880326492     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2013.44     Document Type: Review

References (150)

1. Kettenmann H, Blankenfeld GV, Trotter J. Physiological properties of oligodendrocytes during development. Ann N Y Acad Sci 1991; 633: 64-77
2. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. Physiology of microglia. Physiol Rev 2011; 91: 461-553
3. Yamashita K, Vogel P, Fritze K, Back T, Hossmann KA, Wiessner C. Monitoring the temporal and spatial activation pattern of astrocytes in focal cerebral ischemia using in situ hybridization to GFAP mRNA: Comparison with sgp-2 and hsp70 mRNA and the effect of glutamate receptor antagonists. Brain Res 1996; 735: 285-297
4. Oberheim NA, Wang X, Goldman S, Nedergaard M. Astrocytic complexity distinguishes the human brain. Trends Neurosci 2006; 29: 547-553
5. Marin-Padilla M. Prenatal development of fibrous (white matter), protoplasmic (gray matter), and layer I astrocytes in the human cerebral cortex: A Golgi study. J Comp Neurol 1995; 357: 554-572
6. Sofroniew MV. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 2009; 32: 638-647
7. Sofroniew MV, Vinters HV. Astrocytes: Biology and pathology. Acta Neuropathol 2010; 119: 7-35
8. Liu PC, Lu SD, Huang YL, Sun FY. [The expression of nestin in ischemia-injured brain of adult rat]. Sheng Li Xue Bao 2002; 54: 294-299
9. Wilhelmsson U, Bushong EA, Price DL, Smarr BL, Phung V, Terada M et al. Redefining the concept of reactive astrocytes as cells that remain within their unique domains upon reaction to injury. Proc Natl Acad Sci USA 2006; 103: 17513-17518
10. Alilain WJ, Horn KP, Hu H, Dick TE, Silver J. Functional regeneration of respiratory pathways after spinal cord injury. Nature 2011; 475: 196-200
11. Voskuhl RR, Peterson RS, Song B, Ao Y, Morales LB, Tiwari-Woodruff S et al. Reactive astrocytes form scar-like perivascular barriers to leukocytes during adaptive immune inflammation of the CNS. J Neurosci 2009; 29: 11511-11522
12. Cotrina ML, Kang J, Lin JH, Bueno E, Hansen TW, He L et al. Astrocytic gap junctions remain open during ischemic conditions. J Neurosci 1998; 18: 2520-2537
13. Sullivan SM, Bjorkman ST, Miller SM, Colditz PB, Pow DV. Morphological changes in white matter astrocytes in response to hypoxia/ischemia in the neonatal pig. Brain Res 2010; 1319: 164-174
14. Sontheimer H. Astrocytes, as well as neurons, express a diversity of ion channels. Can J Physiol Pharmacol 1992; 70(Suppl): S223-S238
15. Hertz L, Chen Y, Spatz M. Involvement of non-neuronal brain cells in AVPmediated regulation of water space at the cellular, organ, and whole-body level. J Neurosci Res 2000; 62: 480-490
16. + exchange in hypoxia-related acute astrocyte death. Glia 2005; 49: 143-152
17. Obara M, Szeliga M, Albrecht J. Regulation of pH in the mammalian central nervous system under normal and pathological conditions: Facts and hypotheses. Neurochem Int 2008; 52: 905-919
18. + as a signalling route. ASN Neuro 2012; 4: 103-119
19. + and BK channels determine both arteriolar dilation and constriction. Proc Natl Acad Sci USA 2010; 107: 3811-3816
20. Kirischuk S, Parpura V, Verkhratsky A. Sodium dynamics: Another key to astroglial excitability? Trends Neurosci 2012; 35: 497-506
21. Lai AY, Todd KG. Hypoxia-Activated microglial mediators of neuronal survival are differentially regulated by tetracyclines. Glia 2006; 53: 809-816
22. Boscia F, Esposito CL, Di Crisci A, de Franciscis V, Annunziato L, Cerchia L. GDNF selectively induces microglial activation and neuronal survival in CA1/CA3 hippocampal regions exposed to NMDA insult through Ret/ERK signalling. PLoS One 2009; 4: E6486
23. Boscia F, Gala R, Pannaccione A, Secondo A, Scorziello A, Di Renzo G et al. NCX1 expression and functional activity increase in microglia invading the infarct core. Stroke 2009; 40: 3608-3617
24. Schilling M, Besselmann M, Muller M, Strecker JK, Ringelstein EB, Kiefer R. Predominant phagocytic activity of resident microglia over hematogenous macrophages following transient focal cerebral ischemia: An investigation using green fluorescent protein transgenic bone marrow chimeric mice. Exp Neurol 2005; 196: 290-297
25. Madinier A, Bertrand N, Mossiat C, Prigent-Tessier A, Beley A, Marie C et al. Microglial involvement in neuroplastic changes following focal brain ischemia in rats. PLoS One 2009; 4: E8101
26. Neumann J, Sauerzweig S, Ronicke R, Gunzer F, Dinkel K, Ullrich O et al. Microglia cells protect neurons by direct engulfment of invading neutrophil granulocytes: A new mechanism of CNS immune privilege. J Neurosci 2008; 28: 5965-5975
27. Thored P, Heldmann U, Gomes-Leal W, Gisler R, Darsalia V, Taneera J et al. Longterm accumulation of microglia with proneurogenic phenotype concomitant with persistent neurogenesis in adult subventricular zone after stroke. Glia 2009; 57: 835-849
28. Lalancette-Hebert M, Gowing G, Simard A, Weng YC, Kriz J. Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci 2007; 27: 2596-2605
29. Imai F, Suzuki H, Oda J, Ninomiya T, Ono K, Sano H et al. Neuroprotective effect of exogenous microglia in global brain ischemia. J Cereb Blood Flow Metab 2007; 27: 488-500
30. Iglesias-Rozas JR, Garrosa M. The discovery of oligodendroglia cells by Rio-Hortega: His original articles. Clin Neuropathol 2012; 31: 437-439
31. Chong SY, Chan Jr. Tapping into the glial reservoir: Cells committed to remaining uncommitted. J Cell Biol 2010; 188: 305-312
32. Rivers LE, Young KM, Rizzi M, Jamen F, Psachoulia K, Wade A et al. PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci 2008; 11: 1392-1401
33. Nishiyama A, Komitova M, Suzuki R, Zhu X. Polydendrocytes (NG2 cells): Multifunctional cells with lineage plasticity. Nat Rev Neurosci 2009; 10: 9-22
34. Franklin RJ, Kotter MR. The biology of CNS remyelination: The key to therapeutic advances. J Neurol 2008; 255(Suppl 1): 19-25
35. Dai X, Lercher LD, Clinton PM, Du Y, Livingston DL, Vieira C et al. The trophic role of oligodendrocytes in the basal forebrain. J Neurosci 2003; 23: 5846-5853
36. Lee S, Leach MK, Redmond SA, Chong SY, Mellon SH, Tuck SJ et al. A culture system to study oligodendrocyte myelination processes using engineered nanofibers. Nat Methods 2012; 9: 917-922
37. Ludwin SK, Maitland M. Long-term remyelination fails to reconstitute normal thickness of central myelin sheaths. J Neurol Sci 1984; 64: 193-198
38. Szuchet S, Nielsen JA, Lovas G, Domowicz MS, de Velasco JM, Maric D et al. The genetic signature of perineuronal oligodendrocytes reveals their unique phenotype. Eur J Neurosci 2011; 34: 1906-1922
39. Stys PK. White matter injury mechanisms. Curr Mol Med 2004; 4: 113-130
40. Arai K, Lo EH. Experimental models for analysis of oligodendrocyte pathophysiology in stroke. Exp Transl Stroke Med 2009; 1: 6.
41. Li S, Stys PK. Mechanisms of ionotropic glutamate receptor-mediated excitotoxicity in isolated spinal cord white matter. J Neurosci 2000; 20: 1190-1198
42. Matute C, Alberdi E, Domercq M, Sanchez-Gomez MV, Perez-Samartin A, Rodriguez-Antiguedad A et al. Excitotoxic damage to white matter. J Anat 2007; 210: 693-702
43. Claus HL, Walberer M, Simard ML, Emig B, Muesken SM, Rueger MA et al. NG2 and NG2-positive cells delineate focal cerebral infarct demarcation in rats. Neuropathology 2012
44. Honsa P, Pivonkova H, Dzamba D, Filipova M, Anderova M. Polydendrocytes display large lineage plasticity following focal cerebral ischemia. PLoS One 2012; 7: E36816
45. Gregersen R, Christensen T, Lehrmann E, Diemer NH, Finsen B. Focal cerebral ischemia induces increased myelin basic protein and growth-Associated protein-43 gene transcription in peri-infarct areas in the rat brain. Exp Brain Res 2001; 138: 384-392
46. + influx. J Neurosci 2009; 29: 6663-6676
47. Soliven B. Calcium signalling in cells of oligodendroglial lineage. Microsc Res Tech 2001; 52: 672-679
48. Kettenmann H. Electrophysiological behavior of microglia. Neuropathol Appl Neurobiol 1994; 20: 177-178
49. + exchanger: From molecular biology to therapeutic perspectives. Pharmacol Rev 2004; 56: 633-654
50. Philipson KD, Nicoll DA. Sodium-calcium exchange: A molecular perspective. Annu Rev Physiol 2000; 62: 111-133
51. + exchanger. J Biol Chem 1999; 274: 910-917
52. + exchanger. Science 1990; 250: 562-565
53. + exchanger. J Biol Chem 1994; 269: 17434-17439
54. + exchanger, NCX3. J Biol Chem 1996; 271: 24914-24921
55. + exchanger isoforms. J Biol Chem 1994; 269: 14849-14852
56. + exchanger 3 (NCX3) gene leads to a worsening of ischemic brain damage. J Neurosci 2008; 28: 1179-1184
57. Pignataro G, Gala R, Cuomo O, Tortiglione A, Giaccio L, Castaldo P et al. Two sodium/calcium exchanger gene products, NCX1 and NCX3, play a major role in the development of permanent focal cerebral ischemia. Stroke 2004; 35: 2566-2570
58. + exchanger in cerebral ischemia induced by middle cerebral artery occlusion in male rats. Neuropharmacology 2004; 46: 439-448
59. + exchanger activity, effectively protects against stroke damage. Mol Pharmacol 2012; 83: 142-156
60. + exchanger (NCX-SQ1). J Gen Physiol 1998; 111: 857-873
61. +i signal induced by hypo-osmotic stress in rat cerebellar astrocytes. The effect of osmolarity on exchange activity. J Physiol Sci 2008; 58: 277-279
62. + exchanger-operated exocytotic glutamate release triggered by mild depolarization. J Neurochem 2007; 103: 1196-1207
63. + sources for the exocytotic glutamate release from astrocytes. Neurochem Int 2009; 55: 2-8.
64. Kintner DB, Wang Y, Sun D. Role of membrane ion transport proteins in cerebral ischemic damage. Front Biosci 2007; 12: 762-770
65. + exchange activity by interferon-gamma in cultured rat microglia. J Neurochem 2004; 90: 784-791
66. + exchanger, attenuates reperfusion injury in the in vitro and in vivo cerebral ischemic models. J Pharmacol Exp Ther 2001; 298: 249-256
67. + exchanger, attenuates sodium nitroprusside-induced apoptosis in cultured rat microglia. Br J Pharmacol 2005; 144: 669-679
68. + exchanger. J Neurosci 2007; 27: 13065-13073
69. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 2010; 330: 841-845
70. + influx and respiratory burst in microglia. Channels (Austin) 2007; 1: 366-376
71. +) exchanger-3 (NCX3) impairs oligodendrocyte differentiation. Cell Death Differ 2012; 19: 562-572
72. + exchanger in mammalian myelinated axons. Brain Res 1997; 776: 1-9.
73. +) exchangers is required for GABA-induced NG2 cell migration. J Cell Biol 2009; 186: 113-128
74. +) exchange in spinal cord white matter injury at physiological temperature. J Neurophysiol 2000; 84: 1116-1119
75. Wolf JA, Stys PK, Lusardi T, Meaney D, Smith DH. Traumatic axonal injury induces calcium influx modulated by tetrodotoxin-sensitive sodium channels. J Neurosci 2001; 21: 1923-1930
76. Craner MJ, Hains BC, Lo AC, Black JA, Waxman SG. Co-localization of sodium channel Nav1.6 and the sodium-calcium exchanger at sites of axonal injury in the spinal cord in EAE. Brain 2004; 127: 294-303
77. +) exchanger. J Neurochem 2007; 102: 1783-1795
78. Douglas RM, Xue J, Chen JY, Haddad CG, Alper SL, Haddad GG. Chronic intermittent hypoxia decreases the expression of Na/H exchangers and HCO3-dependent transporters in mouse CNS. J Appl Physiol 2003; 95: 292-299
79. + exchanger isoform 1-null mice after in vitro and in vivo ischemia. J Neurosci 2005; 25: 11256-11268
80. + exchanger reduces infarct volume of focal cerebral ischemia in rats. Brain Res 2001; 922: 223-228
81. +) exchanger isoform 1 null mice. Am J Physiol Cell Physiol 2004; 287: C12-C21
82. + exchange activity in cultured rat hippocampal astrocytes. J Neurosci Res 1996; 44: 191-198
83. + homeostasis. J Neurosci 2010; 30: 15210-15220
84. + exchanger are involved in intracellular pH regulation of cultured mature rat cerebellar oligodendrocytes. Glia 1997; 19: 74-84
85. Ro HA, Carson JH. pH microdomains in oligodendrocytes. J Biol Chem 2004; 279: 37115-37123
86. Lauf PK, Adragna NC. K-Cl cotransport: Properties and molecular mechanism. Cell Physiol Biochem 2000; 10: 341-354
87. Le Rouzic P, Ivanov TR, Stanley PJ, Baudoin FM, Chan F, Pinteaux E et al. KCC3 and KCC4 expression in rat adult forebrain. Brain Res 2006; 1110: 39-45
88. Adragna NC, Di Fulvio M, Lauf PK. Regulation of K-Cl cotransport: From function to genes. J Membr Biol 2004; 201: 109-137
89. Ernest NJ, Weaver AK, Van Duyn LB, Sontheimer HW. Relative contribution of chloride channels and transporters to regulatory volume decrease in human glioma cells. Am J Physiol Cell Physiol 2005; 288: C1451-C1460
90. Ringel F, Plesnila N. Expression and functional role of potassium-chloride cotransporters (KCC) in astrocytes and C6 glioma cells. Neurosci Lett 2008; 442: 219-223
91. Zierler S, Frei E, Grissmer S, Kerschbaum HH. Chloride influx provokes lamellipodium formation in microglial cells. Cell Physiol Biochem 2008; 21: 55-62
92. + channels for lysophosphatidic acid-induced microglial migration. Eur J Neurosci 2004; 19: 1469-1474
93. Pearson KG. Plasticity of neuronal networks in the spinal cord: Modifications in response to altered sensory input. Prog Brain Res 2000; 128: 61-70
94. +)-Cl(-) cotransporter, KCC3, in the central and peripheral nervous systems: Expression in the choroid plexus, large neurons and white matter tracts. Neuroscience 2001; 103: 481-491
95. Howard HC, Mount DB, Rochefort D, Byun N, Dupre N, Lu J et al. The K-Cl cotransporter KCC3 is mutant in a severe peripheral neuropathy associated with agenesis of the corpus callosum. Nat Genet 2002; 32: 384-392
96. Boettger T, Rust MB, Maier H, Seidenbecher T, Schweizer M, Keating DJ et al. Loss of K-Cl co-transporter KCC3 causes deafness, neurodegeneration and reduced seizure threshold. Embo J 2003; 22: 5422-5434
97. +)-mediated injury in myelinated CNS axons. Brain Res 1994; 644: 197-204
98. Malek SA, Coderre E, Stys PK. Aberrant chloride transport contributes to anoxic/ischemic white matter injury. J Neurosci 2003; 23: 3826-3836
99. +)-dependent chloride transporter (NKCC1)-null mice exhibit less gray and white matter damage after focal cerebral ischemia. J Cereb Blood Flow Metab 2005; 25: 54-66
100. Jayakumar AR, Norenberg MD. The Na-K-Cl Co-transporter in astrocyte swelling. Metab Brain Dis 2010; 25: 31-38
101. Yang H, Wang Z, Miyamoto Y, Reinach PS. Cell signaling pathways mediating epidermal growth factor stimulation of Na:K:2Cl cotransport activity in rabbit corneal epithelial cells. J Membr Biol 2001; 183: 93-101
102. Rutledge EM, Kimelberg HK. Release of [3H]-D-Aspartate from primary astrocyte cultures in response to raised external potassium. J Neurosci 1996; 16: 7803-7811
103. Walz W. Role of astrocytes in the clearance of excess extracellular potassium. Neurochem Int 2000; 36: 291-300
104. +)-Cl(-) cotransporter-null mice exhibit absence of swelling and decrease in EAA release. Am J Physiol Cell Physiol 2002; 282: C1147-C1160
105. +)](o)-induced swelling and EAA release in astrocytes. Am J Physiol Cell Physiol 2002; 282: C1136-C1146
106. Siesjo BK. Pathophysiology and treatment of focal cerebral ischemia. Part I: Pathophysiology. (1992). J Neurosurg 2008; 108: 616-631
107. + signaling in astrocytes in an in vitro ischemic model. J Neurosci 2004; 24: 9585-9597
108. +) uptake via NKCC1 and swelling of astrocytes. Glia 2002; 37: 114-123
109. Rothman SM. The neurotoxicity of excitatory amino acids is produced by passive chloride influx. J Neurosci 1985; 5: 1483-1489
110. + homeostasis in rat spinal cord astrocytes. J Neurosci 1998; 18: 3554-3562
111. Bondarenko A, Chesler M. Rapid astrocyte death induced by transient hypoxia, acidosis, and extracellular ion shifts. Glia 2001; 34: 134-142
112. Waxman SG, Ritchie JM. Molecular dissection of the myelinated axon. Ann Neurol 1993; 33: 121-136
113. + exchange in mitochondrial dysfunction in astrocytes following in vitro ischemia. Am J Physiol Cell Physiol 2007; 292: C1113-C1122
114. Plotkin MD, Snyder EY, Hebert SC, Delpire E. Expression of the Na-K-2Cl cotransporter is developmentally regulated in postnatal rat brains: A possible mechanism underlying gabás excitatory role in immature brain. J Neurobiol 1997; 33: 781-795
115. Wang C, Rougon G, Kiss JZ. Requirement of polysialic acid for the migration of the O-2A glial progenitor cell from neurohypophyseal explants. J Neurosci 1994; 14: 4446-4457
116. Tekkok SB, Goldberg MP. Ampa/kainate receptor activation mediates hypoxic oligodendrocyte death and axonal injury in cerebral white matter. J Neurosci 2001; 21: 4237-4248
117. +:HCO(3-) cotransporters (NBC): Cloning and characterization. J Membr Biol 2001; 183: 71-84
118. Majumdar D, Bevensee MO. Na-coupled bicarbonate transporters of the solute carrier 4 family in the nervous system: Function, localization, and relevance to neurologic function. Neuroscience 2010; 171: 951-972
119. Schmitt BM, Berger UV, Douglas RM, Bevensee MO, Hediger MA, Haddad GG et al. Na/HCO3 cotransporters in rat brain: Expression in glia, neurons, and choroid plexus. J Neurosci 2000; 20: 6839-6848
120. Giffard RG, Papadopoulos MC, van Hooft JA, Xu L, Giuffrida R, Monyer H. The electrogenic sodium bicarbonate cotransporter: Developmental expression in rat brain and possible role in acid vulnerability. J Neurosci 2000; 20: 1001-1008
121. Jung YW, Choi IJ, Kwon TH. Altered expression of sodium transporters in ischemic penumbra after focal cerebral ischemia in rats. Neurosci Res 2007; 59: 152-159
122. +/HCO3-cotransporter immunoreactivity changes in neurons and expresses in astrocytes in the gerbil hippocampal CA1 region after ischemia/reperfusion. Neurochem Res 2011; 36: 2459-2469
123. Faff L, Ohlemeyer C, Kettenmann H. Intracellular pH regulation in cultured microglial cells from mouse brain. J Neurosci Res 1996; 46: 294-304
124. Deitmer JW, Rose CR. pH regulation and proton signalling by glial cells. Prog Neurobiol 1996; 48: 73-103
125. Kettenmann H, Schlue WR. Intracellular pH regulation in cultured mouse oligodendrocytes. J Physiol 1988; 406: 147-162
126. Boussouf A, Gaillard S. Intracellular pH changes during oligodendrocyte differentiation in primary culture. J Neurosci Res 2000; 59: 731-739
127. Lascola C, Kraig RP. Astroglial acid-base dynamics in hyperglycemic and normoglycemic global ischemia. Neurosci Biobehav Rev 1997; 21: 143-150
128. Clausen T, Van Hardeveld C, Everts ME. Significance of cation transport in control of energy metabolism and thermogenesis. Physiol Rev 1991; 71: 733-774
129. Friberg H, Wieloch T. Mitochondrial permeability transition in acute neurodegeneration. Biochimie 2002; 84: 241-250
130. Astrup J. Energy-requiring cell functions in the ischemic brain. Their critical supply and possible inhibition in protective therapy. J Neurosurg 1982; 56: 482-497
131. Kaplan JH. Biochemistry of Na,K-ATPase. Annu Rev Biochem 2002; 71: 511-535
132. +-ATPase isozyme diversity; comparative biochemistry and physiological implications of novel functional interactions. Biosci Rep 2000; 20: 51-91
133. Scheiner-Bobis G. The sodium pump. Its molecular properties and mechanics of ion transport. Eur J Biochem 2002; 269: 2424-2433
134. +)-ATPase alpha-And beta-subunit isoforms within the rat central nervous system. Proc Natl Acad Sci USA 1991; 88: 7425-7429
135. +-ATPase alpha-subunit from rat brain. Biochemistry 1986; 25: 8125-8132
136. Moseley AE, Lieske SP, Wetzel RK, James PF, He S, Shelly DA et al. The Na,KATPase alpha 2 isoform is expressed in neurons, and its absence disrupts neuronal activity in newborn mice. J Biol Chem 2003; 278: 5317-5324
137. McGrail KM, Phillips JM, Sweadner KJ. Immunofluorescent localization of three Na,K-ATPase isozymes in the rat central nervous system: Both neurons and glia can express more than one Na,K-ATPase. J Neurosci 1991; 11: 381-391
138. Cameron R, Klein L, Shyjan AW, Rakic P, Levenson R. Neurons and astroglia express distinct subsets of Na,K-ATPase alpha and beta subunits. Brain Res Mol Brain Res 1994; 21: 333-343
139. Lecuona E, Luquin S, Avila J, Garcia-Segura LM, Martin-Vasallo P. Expression of the beta 1 and beta 2(AMOG) subunits of the Na,K-ATPase in neural tissues: Cellular and developmental distribution patterns. Brain Res Bull 1996; 40: 167-174
140. +-ATPase alpha 2 subunit and the glutamate transporters GLAST and GLT-1 in the rat somatosensory cortex. Cereb Cortex 2002; 12: 515-525
141. Blaustein MP, Juhaszova M, Golovina VA, Church PJ, Stanley EF. Na/Ca exchanger and PMCA localization in neurons and astrocytes: Functional implications. Ann N Y Acad Sci 2002; 976: 356-366
142. Leis JA, Bekar LK, Walz W. Potassium homeostasis in the ischemic brain. Glia 2005; 50: 407-416
143. Peng L, Martin-Vasallo P, Sweadner KJ. Isoforms of Na,K-ATPase alpha and beta subunits in the rat cerebellum and in granule cell cultures. J Neurosci 1997; 17: 3488-3502
144. Shirihai O, Smith P, Hammar K, Dagan D. Microglia generate external proton and potassium ion gradients utilizing a member of the H/K ATPase family. Glia 1998; 23: 339-348
145. Fink D, Knapp PE, Mata M. Differential expression of Na,K-ATPase isoforms in oligodendrocytes and astrocytes. Dev Neurosci 1996; 18: 319-326
146. Martin-Vasallo P, Wetzel RK, Garcia-Segura LM, Molina-Holgado E, Arystarkhova E, Sweadner KJ. Oligodendrocytes in brain and optic nerve express the beta3 subunit isoform of Na,K-ATPase. Glia 2000; 31: 206-218
147. Knapp PE, Itkis OS, Mata M. Neuronal interaction determines the expression of the alpha-2 isoform of Na, K-ATPase in oligodendrocytes. Brain Res Dev Brain Res 2000; 125: 89-97
148. Dobretsov M, Stimers Jr. Characterization of the Na/K pump current in N20.1 oligodendrocytes. Brain Res 1996; 724: 103-111
149. Qu WS, Wang YH, Wang JP, Tang YX, Zhang Q, Tian DS et al. Galectin-1 enhances astrocytic BDNF production and improves functional outcome in rats following ischemia. Neurochem Res 2010; 35: 1716-1724
150. Xu L, Emery JF, Ouyang YB, Voloboueva LA, Giffard RG. Astrocyte targeted overexpression of Hsp72 or SOD2 reduces neuronal vulnerability to forebrain ischemia. Glia 2010; 58: 1042-1049