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Regulation of potassium by glial cells in the centralnervous system

  • Paulo Kofuji
  • Eric A. Newman
Chapter

Rapid changes in extracellular K+ concentration ([K+]o) in the mammalian central nervous system (CNS) are counteracted by simple passive diffusion as well as by cellular mechanisms of K+ clearance. Regulation of [K+]o can occur via glial or neuronal uptake of K+ ions through transporters or K+-selective ion channels. The best studied mechanism of [K+]o regulation in the brain is K+spatial buffering, wherein the glial syncytium disperses local extracellular K+ increases by transferring K+ from sites of elevated [K+]o to those with lower [K+]o. In recent years, K+ spatial buffering has been implicated or directly demonstrated by a variety of experimental approaches, including electrophysiological and optical methods. A specialized form of spatial buffering termed K+siphoning takes place in the vertebrate retina, where glial Müller cells express inwardly rectifying K+channels (Kir channels) positioned in membrane domains near to the vitreous humor and blood vessels. This highly...

Keywords

Glial Cell Vitreous Humor Neurovascular Coupling Central Nervous System Region Dystrophin Glycoprotein Complex 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

AQP4

Aquaporin 4

CNS

Central nervous system

Cx

Connexins

DGC

Dystrophin glycoprotein complex

IOS

Intrinsic optic signal

KO

Knockout

[K+]o

Extracellular K+ concentration

Kir channel

Inwardly rectifying K+ channel

Na+ pump

Na+, K+-ATPase

References

  1. Ahn AH, Kunkel LM (1995) Syntrophin binds to an alternatively spliced exon of dystrophin. J Cell Biol 128:363–371.PubMedGoogle Scholar
  2. Amedee T, Robert A, Coles JA (1997) Potassium homeostasis and glial energy metabolism. Glia 21:46–55.PubMedGoogle Scholar
  3. Amiry-Moghaddam M, Otsuka T, Hurn PD, Traystman RJ, Haug FM, Froehner SC, Adams ME, Neely JD, Agre P, Ottersen OP, Bhardwaj A (2003) An α-syntrophin-dependent pool of AQP4 in astroglial end-feet confers bidirectional water flow between blood and brain. Proc Natl Acad Sci U S A 100:2106–2111.PubMedGoogle Scholar
  4. Ballanyi K, Grafe P, ten Bruggencate G (1987) Ion activities and potassium uptake mechanisms of glial cells in guinea-pig olfactory cortex slices. J Physiol 382:159–174.PubMedGoogle Scholar
  5. Barres BA, Koroshetz WJ, Chun LL, Corey DP (1990) Ion channel expression by white matter glia: the type-1 astrocyte. Neuron 5:527–544.PubMedGoogle Scholar
  6. Bordey A, Sontheimer H (1998) Properties of human glial cells associated with epileptic seizure foci. Epilepsy Res 32:286–303.PubMedGoogle Scholar
  7. Brew H, Gray P, Mobbs P, Attwell D (1986) Endfeet of retinal glial cells have higher densities of ion channels that mediate K+ buffering Nature 324:466–468.PubMedGoogle Scholar
  8. Claudepierre T, Dalloz C, Mornet D, Matsumura K, Sahel J, Rendon A (2000a) Characterization of the intermolecular associations of the dystrophin-associated glycoprotein complex in retinal Müller glial cells. J Cell Sci 113 (Pt 19):3409–3417.Google Scholar
  9. Claudepierre T, Mornet D, Pannicke T, Forster V, Dalloz C, Bolanos F, Sahel J, Reichenbach A, Rendon A (2000b) Expression of Dp71 in Müller glial cells: a comparison with utrophin- and dystrophin-associated proteins. Invest Ophthalmol Vis Sci 41:294–304.Google Scholar
  10. Coles JA, Orkand RK, Yamate CL, Tsacopoulos M (1986) Free concentrations of Na, K, and Cl in the retina of the honeybee drone: stimulus-induced redistribution and homeostasis. Ann N Y Acad Sci 481:303–317.PubMedGoogle Scholar
  11. Connors B, Dray A, Fox P, Hilmy M, Somjen G (1979) LSD‧s effect on neuron populations in visual cortex gauged by transient responses of extracellular potassium evoked by optical stimuli. Neurosci Lett 13:147–150.PubMedGoogle Scholar
  12. Connors BW, Ransom BR, Kunis DM, Gutnick MJ (1982) Activity-dependent K+ accumulation in the developing rat optic nerve Science 216:1341–1343.PubMedGoogle Scholar
  13. Connors NC, Kofuji P (2002) Dystrophin Dp71 is critical for the clustered localization of potassium channels in retinal glial cells. J Neurosci 22:4321–4327.PubMedGoogle Scholar
  14. D’Ambrosio R, Gordon DS, Winn HR (2002) Differential role of KIR channel and Na+/K+-pump in the regulation of extracellular K+ in rat hippocampus J Neurophysiol 87:87–102.PubMedGoogle Scholar
  15. Dalloz C, Sarig R, Fort P, Yaffe D, Bordais A, Pannicke T, Grosche J, Mornet D, Reichenbach A, Sahel J, Nudel U, Rendon A (2003) Targeted inactivation of dystrophin gene product Dp71: phenotypic impact in mouse retina. Hum Mol Genet. 12:1543–1554.PubMedGoogle Scholar
  16. Dennis MJ, Gerschenfeld HM (1969) Some physiological properties of identified mammalian neuroglial cells. J Physiol 203:211–222.PubMedGoogle Scholar
  17. Dermietzel R (1998) Diversification of gap junction proteins (connexins) in the central nervous system and the concept of functional compartments. Cell Biol Int 22:719–730.PubMedGoogle Scholar
  18. Dermietzel R, Gao Y, Scemes E, Vieira D, Urban M, Kremer M, Bennett MV, Spray DC (2000) Connexin43 null mice reveal that astrocytes express multiple connexins. Brain Res Brain Res Rev 32:45–56.PubMedGoogle Scholar
  19. Dietzel I, Heinemann U, Hofmeier G, Lux HD (1980) Transient changes in the size of the extracellular space in the sensorimotor cortex of cats in relation to stimulus-induced changes in potassium concentration. Exp Brain Res 40:432–439.PubMedGoogle Scholar
  20. Dietzel I, Heinemann U, Lux HD (1989) Relations between slow extracellular potential changes, glial potassium buffering, and electrolyte and cellular volume changes during neuronal hyperactivity in cat brain. Glia 2:25–44.PubMedGoogle Scholar
  21. Doupnik CA, Davidson N, Lester HA (1995) The inward rectifier potassium channel family. Curr Opin Neurobiol 5:268–277.PubMedGoogle Scholar
  22. Filosa JA, Bonev AD, Straub SV, Meredith AL, Wilkerson MK, Aldrich RW, Nelson MT (2006) Local potassium signaling couples neuronal activity to vasodilation in the brain. Nat Neurosci 9:1397–1403.PubMedGoogle Scholar
  23. Franck G, Grisar T, Moonen G (1983) Glial and neuronal Na+. In: ,K+ pumpFedoroff S, Hertz L, eds), pp Advances in Neurobiology (Academic. New York: 139–159.Google Scholar
  24. Frishman LJ, Yamamoto F, Bogucka J, Steinberg RH (1992) Light-evoked changes in [K+]o in proximal portion of light-adapted cat retina J Neurophysiol 67:1201–1212.PubMedGoogle Scholar
  25. Gardner-Medwin AR, Nicholson C (1983) Changes of extracellular potassium activity induced by electric current through brain tissue in the rat. J Physiol 335:375–392.PubMedGoogle Scholar
  26. Gardner-Medwin AR, Coles JA, Tsacopoulos M (1981) Clearance of extracellular potassium: evidence for spatial buffering by glial cells in the retina of the drone. Brain Res 209:452–457.PubMedGoogle Scholar
  27. Gnatenco C, Han J, Snyder AK, Kim D (2002) Functional expression of TREK-2 K+ channel in cultured rat brain astrocytes Brain Res 931:56–67.PubMedGoogle Scholar
  28. Gutnick MJ, Heinemann U, Lux HD (1979) Stimulus induced and seizure related changes in extracellular potassium concentration in cat thalamus (VPL). Electroencephalogr Clin Neurophysiol 47:329–344.PubMedGoogle Scholar
  29. Haas M, Forbush B, III (1998) The Na-K-Cl cotransporters. J Bioenerg Biomembr 30:161–172.PubMedGoogle Scholar
  30. Heinemann U, Lux HD (1977) Ceiling of stimulus induced rises in extracellular potassium concentration in the cerebral cortex of cat. Brain Res 120:231–249.PubMedGoogle Scholar
  31. Heinemann U, Schaible HG, Schmidt RF (1990) Changes in extracellular potassium concentration in cat spinal cord in response to innocuous and noxious stimulation of legs with healthy and inflamed knee joints. Exp Brain Res 79:283–292.PubMedGoogle Scholar
  32. Heinemann U, Gabriel S, Jauch R, Schulze K, Kivi A, Eilers A, Kovacs R, Lehmann TN (2000) Alterations of glial cell function in temporal lobe epilepsy. Epilepsia 41:S185–S189.PubMedGoogle Scholar
  33. Higashi K, Fujita A, Inanobe A, Tanemoto M, Doi K, Kubo T, Kurachi Y (2001) An inwardly rectifying K+ channel, Kir4.1, expressed in astrocytes surrounds synapses and blood vessels in brain Am J Physiol Cell Physiol 281:C922–C931.PubMedGoogle Scholar
  34. Hinterkeuser S, Schroder W, Hager G, Seifert G, Blumcke I, Elger CE, Schramm J, Steinhauser C (2000) Astrocytes in the hippocampus of patients with temporal lobe epilepsy display changes in potassium conductances. Eur J Neurosci 12:2087–2096.PubMedGoogle Scholar
  35. Holthoff K, Witte OW (2000) Directed spatial potassium redistribution in rat neocortex. Glia 29:288–292.PubMedGoogle Scholar
  36. Horio Y, Hibino H, Inanobe A, Yamada M, Ishii M, Tada Y, Satoh E, Hata Y, Takai Y, Kurachi Y (1997) Clustering and enhanced activity of an inwardly rectifying potassium channel, Kir4.1, by an anchoring protein, PSD-95/SAP90. J Bio Chem 272:12885–12888.Google Scholar
  37. Hung AY, Sheng M (2002) PDZ domains: structural modules for protein complex assembly. J Biol Chem 277:5699–5702.PubMedGoogle Scholar
  38. Iandiev I, Tenckhoff S, Pannicke T, Biedermann B, Hollborn M, Wiedemann P, Reichenbach A, Bringmann A (2006) Differential regulation of Kir4.1 and Kir2.1 expression in the ischemic rat retina. Neurosci Lett 396:97–101.PubMedGoogle Scholar
  39. Ishii M, Horio Y, Tada Y, Hibino H, Inanobe A, Ito M, Yamada M, Gotow T, Uchiyama Y, Kurachi Y (1997) Expression and clustered distribution of an inwardly rectifying potassium channel, KAB-2/Kir4.1, on mammalian retinal Müller cell membrane: their regulation by insulin and laminin signals. J Neurosci 17:7725–7735.PubMedGoogle Scholar
  40. Ishii M, Fujita A, Iwai K, Kusaka S, Higashi K, Inanobe A, Hibino H, Kurachi Y (2003) Differential expression and distribution of Kir5.1 and Kir4.1 inwardly rectifying K+ channels in retina Am J Physiol Cell Physiol 285:C260–267.PubMedGoogle Scholar
  41. Jorgensen PL, Hakansson KO, Karlish SJ (2003) Structure and mechanism of Na,K-ATPase: functional sites and their interactions. Annu Rev Physiol 65:817–849.PubMedGoogle Scholar
  42. Kaiser M, Maletzki I, Hulsmann S, Holtmann B, Schulz-Schaeffer W, Kirchhoff F, Bahr M, Neusch C (2006) Progressive loss of a glial potassium channel (KCNJ10) in the spinal cord of the SOD1 (G93A) transgenic mouse model of amyotrophic lateral sclerosis. J Neurochem 99:900–912.PubMedGoogle Scholar
  43. Kalsi AS, Greenwood K, Wilkin G, Butt AM (2004) Kir4.1 expression by astrocytes and oligodendrocytes in CNS white matter: a developmental study in the rat optic nerve. J Anat 204:475–485.PubMedGoogle Scholar
  44. Kaplan JH (2002) Biochemistry of Na,K-ATPase. Annu Rev Biochem 71:511–535.PubMedGoogle Scholar
  45. Karwoski CJ, Xu X (1999) Current source-density analysis of light-evoked field potentials in rabbit retina. Vis Neurosci 16:369–377.PubMedGoogle Scholar
  46. Karwoski CJ, Newman EA, Shimazaki H, Proenza LM (1985) Light-evoked increases in extracellular K+ in the plexiform layers of amphibian retinas J Gen Physiol 86:189–213.PubMedGoogle Scholar
  47. Karwoski CJ, Lu HK, Newman EA (1989) Spatial buffering of light-evoked potassium increases by retinal Müller (glial) cells. Science 244:578–580.PubMedGoogle Scholar
  48. Katzman R (1976) Maintenance of a constant brain extracellular potassium. Fed Proc 35:1244–1247. PubMedGoogle Scholar
  49. Kimelberg HK, Frangakis MV (1985) Furosemide- and bumetanide-sensitive ion transport and volume control in primary astrocyte cultures from rat brain. Brain Res 361:125–134.PubMedGoogle Scholar
  50. Kindler CH, Pietruck C, Yost CS, Sampson ER, Gray AT (2000) Localization of the tandem pore domain K+ channel TASK-1 in the rat central nervous system Brain Res Mol Brain Res 80:99–108.PubMedGoogle Scholar
  51. Kofuji P, Connors NC (2003) Molecular substrates of potassium spatial buffering in glial cells. Mol Neurobiol 28:195–208.PubMedGoogle Scholar
  52. Kofuji P, Newman EA (2004) Potassium buffering in the central nervous system. Neuroscience 129:1045–1056.PubMedGoogle Scholar
  53. Kofuji P, Ceelen P, Zahs KR, Surbeck LW, Lester HA, Newman EA (2000) Genetic inactivation of an inwardly rectifying potassium channel (Kir4.1 subunit) in mice: phenotypic impact in retina. J Neurosci 20:5733–5740.PubMedGoogle Scholar
  54. Kofuji P, Biedermann B, Siddharthan V, Raap M, Iandiev I, Milenkovic I, Thomzig A, Veh RW, Bringmann A, Reichenbach A (2002) Kir potassium channel subunit expression in retinal glial cells: implications for spatial potassium buffering. Glia 39:292–303.PubMedGoogle Scholar
  55. Kubo Y, Baldwin TJ, Jan YN, Jan LY (1993) Primary structure and functional expression of a mouse inward rectifier potassium channel. Nature 362:127–133.PubMedGoogle Scholar
  56. Kucheryavykh YV, Kucheryavykh LY, Nichols CG, Maldonado HM, Baksi K, Reichenbach A, Skatchkov SN, Eaton MJ (2007) Downregulation of Kir4.1 inward rectifying potassium channel subunits by RNAi impairs potassium transfer and glutamate uptake by cultured cortical astrocytes. Glia 55:274–281.PubMedGoogle Scholar
  57. Kuffler SW, Nicholls JG, Orkand RK (1966) Physiological properties of glial cells in the central nervous system of amphibia. J Neurophysiol 29:768–787.PubMedGoogle Scholar
  58. Kume-Kick J, Mazel T, Vorisek I, Hrabetova S, Tao L, Nicholson C (2002) Independence of extracellular tortuosity and volume fraction during osmotic challenge in rat neocortex. J Physiol 542:515–527.PubMedGoogle Scholar
  59. Leonoudakis D, Mailliard W, Wingerd K, Clegg D, Vandenberg C (2001) Inward rectifier potassium channel Kir2.2 is associated with synapse-associated protein SAP97. J Cell Sci 114:987–998.PubMedGoogle Scholar
  60. Li L, Head V, Timpe LC (2001) Identification of an inward rectifier potassium channel gene expressed in mouse cortical astrocytes. Glia 33:57–71.PubMedGoogle Scholar
  61. MacVicar BA, Feighan D, Brown A, Ransom B (2002) Intrinsic optical signals in the rat optic nerve: role for K(+) uptake via NKCC1 and swelling of astrocytes. Glia 37:114–123.PubMedGoogle Scholar
  62. Matthias K, Kirchhoff F, Seifert G, Huttmann K, Matyash M, Kettenmann H, Steinhauser C (2003) Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J Neurosci 23:1750–1758.PubMedGoogle Scholar
  63. Metea MR, Kofuji P, Newman EA (2007) Neurovascular coupling is not mediated by potassium siphoning from glial cells. J Neurosci 27:2468–2471.PubMedGoogle Scholar
  64. Nagelhus E, Horio Y, Inanobe A, Fujita A, Haug F, Nielsen S, Kurachi Y, Ottersen O (1999) Immnunogold evidence suggests that coupling of K+ siphoning and water transport in rat retinal Müller cells is mediated by coenrichment of Kir4.1 and AQP4 in specific membrane domains Glia 26:47–54.PubMedGoogle Scholar
  65. Nagy JI, Rash JE (2000) Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS. Brain Res Brain Res Rev 32:29–44.PubMedGoogle Scholar
  66. Neely JD, Amiry-Moghaddam M, Ottersen OP, Froehner SC, Agre P, Adams ME (2001) Syntrophin-dependent expression and localization of Aquaporin-4 water channel protein. Proc Natl Acad Sci U S A 98:14108–14113.PubMedGoogle Scholar
  67. Neusch C, Papadopoulos N, Muller M, Maletzki I, Winter SM, Hirrlinger J, Handschuh M, Bahr M, Richter DW, Kirchhoff F, Hulsmann S (2006) Lack of the Kir4.1 channel subunit abolishes K+ buffering properties of astrocytes in the ventral respiratory group: impact on extracellular K+ regulation J Neurophysiol 95:1843–1852.PubMedGoogle Scholar
  68. Newman EA (1984) Regional specialization of retinal glial cell membrane. Nature 309:155–157.PubMedGoogle Scholar
  69. Newman EA (1985) Membrane physiology of retinal glial (Müller) cells. J Neurosci 5:2225–2239.PubMedGoogle Scholar
  70. Newman EA (1986) High potassium conductance in astrocyte endfeet. Science 233:453–454.PubMedGoogle Scholar
  71. Newman EA (1987a) Regulation of potassium levels by Müller cells in the vertebrate retina. Can J Phys & Pharm 65:1028–1034.Google Scholar
  72. Newman EA (1987b) Distribution of potassium conductance in mammalian Müller (glial) cells: a comparative study. J Neurosci 7:2423–2432.Google Scholar
  73. Newman EA (1993) Inward-rectifying potassium channels in retinal glial (Müller) cells. J Neurosci 13:3333–3345.PubMedGoogle Scholar
  74. Newman EA (1995) Glial cell regulation of extracellular potassium. In: Kettenmann H, Ransom B, eds), pp Neuroglia (Oxford University Press. New York: 717–731.Google Scholar
  75. Newman EA (1996a) Acid efflux from retinal glial cells generated by sodium bicarbonate cotransport. J Neurosci 16:159–168.Google Scholar
  76. Newman EA (1996b) Regulation of extracellular K+ and pH by polarized ion fluxes in glial cells: the retinal Muller cell. The Neuroscientist 2:109–117.Google Scholar
  77. Newman EA, Reichenbach A (1996) The Müller cell: a functional element of the retina. Trends Neurosci 19:307–312.PubMedGoogle Scholar
  78. Newman EA, Frambach DA, Odette LL (1984) Control of extracellular potassium levels by retinal glial cell K+ siphoning Science 225:1174–1175.PubMedGoogle Scholar
  79. Nichols CG, Lopatin AN (1997) Inward rectifier potassium channels. Annu Rev Physiol 59:171–191.PubMedGoogle Scholar
  80. Nicholson C, Sykova E (1998) Extracellular space structure revealed by diffusion analysis. Trends Neurosci 21:207–215.PubMedGoogle Scholar
  81. Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP (1997) Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci 17:171–180.PubMedGoogle Scholar
  82. Noel G, Belda M, Guadagno E, Micoud J, Klocker N, Moukhles H (2005) Dystroglycan and Kir4.1 coclustering in retinal Müller glia is regulated by laminin-1 and requires the PDZ-ligand domain of Kir4.1. J Neurochem 94:691–702.PubMedGoogle Scholar
  83. Oakley BI, Katz B, Xu Z, Zheng J (1992) Spatial buffering of extracellular potassium by Müller (glial) cells in the toad retina. Exp Eye Res 55:539–550.PubMedGoogle Scholar
  84. Olsen ML, Higashimori H, Campbell SL, Hablitz JJ, Sontheimer H (2006) Functional expression of Kir4.1 channels in spinal cord astrocytes. Glia 53:516–528.PubMedGoogle Scholar
  85. Orkand RK (1986) Glial–interstitial fluid exchange. Ann N Y Acad Sci 481:269–272.PubMedGoogle Scholar
  86. Orkand RK, Nicholls JG, Kuffler SW (1966) Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J Neurophysiol 29:788–806.PubMedGoogle Scholar
  87. Padmawar P, Yao X, Bloch O, Manley GT, Verkman AS (2005) K+ waves in brain cortex visualized using a long-wavelength K+-sensing fluorescent indicator Nature Methods 2:825–827.PubMedGoogle Scholar
  88. Pannicke T, Iandiev I, Wurm A, Uckermann O, vom Hagen F, Reichenbach A, Wiedemann P, Hammes HP, Bringmann A (2006) Diabetes alters osmotic swelling characteristics and membrane conductance of glial cells in rat retina. Diabetes 55:633–639.PubMedGoogle Scholar
  89. Patel AJ, Honore E (2001) Properties and modulation of mammalian 2P domain K+ channels Trends Neurosci 24:339–346.PubMedGoogle Scholar
  90. Paulson OB, Newman EA (1987) Does the release of potassium from astrocyte endfeet regulate cerebral blood flow? Science 237:896–898.PubMedGoogle Scholar
  91. Poopalasundaram S, Knott C, Shamotienko OG, Foran PG, Dolly JO, Ghiani CA, Gallo V, Wilkin GP (2000) Glial heterogeneity in expression of the inwardly rectifying K+ channel, Kir4.1, in adult rat CNS Glia 30:362–372.PubMedGoogle Scholar
  92. Ransom BR, Sontheimer H (1992) The neurophysiology of glial cells. J Clin Neurophysiol 9:224–251.PubMedGoogle Scholar
  93. Ransom BR, Carlini WG, Connors BW (1986) Brain extracellular space: developmental studies in rat optic nerve. Ann N Y Acad Sci 481:87–105.PubMedGoogle Scholar
  94. Ransom C, Sontheimer H, Janigro D (1996) Astrocytic inwardly rectifying potassium currents are dependent on external sodium ions. J Neurophys 76:626–630. Google Scholar
  95. Ransom CB, Sontheimer H (1995) Biophysical and pharmacological characterization of inwardly rectifying K+ currents in rat spinal cord astrocytes. J Neurophysiol 73:333–346.PubMedGoogle Scholar
  96. Ransom CB, Ransom BR, Sontheimer H (2000) Activity-dependent extracellular K+ accumulation in rat optic nerve: the role of glial and axonal Na+ pumps J Physiol 522:427–442.PubMedGoogle Scholar
  97. Reichenbach A, Henke A, Eberhardt W, Reichelt W, Dettmer D (1992) K+ ion regulation in retina Can J Physiol Pharmacol 70:(Suppl)S239–247.PubMedGoogle Scholar
  98. Rose CR, Ransom BR (1996) Mechanisms of H+ and Na+ changes induced by glutamate, kainate, and d-aspartate in rat hippocampal astrocytes J Neurosci 16:5393–5404.PubMedGoogle Scholar
  99. Rouach N, Avignone E, Meme W, Koulakoff A, Venance L, Blomstrand F, Giaume C (2002) Gap junctions and connexin expression in the normal and pathological central nervous system. Biol Cell 94:457–475.PubMedGoogle Scholar
  100. Rusznak Z, Pocsai K, Kovacs I, Por A, Pal B, Biro T, Szucs G (2004) Differential distribution of TASK-1, TASK-2 and TASK-3 immunoreactivities in the rat and human cerebellum. Cell Mol Life Sci 61:1532–1542.PubMedGoogle Scholar
  101. Schroder W, Seifert G, Huttmann K, Hinterkeuser S, Steinhauser C (2002) AMPA receptor-mediated modulation of inward rectifier K+ channels in astrocytes of mouse hippocampus Mol Cell Neurosci 19:447–458.PubMedGoogle Scholar
  102. Sheng M, Sala C (2001) PDZ domains and the organization of supramolecular complexes. Annu Rev Neurosci 24:1–29.PubMedGoogle Scholar
  103. Singer W, Lux HD (1975) Extracellular potassium gradients and visual receptive fields in the cat striate cortex. Brain Res 96:378–383.PubMedGoogle Scholar
  104. Skatchkov SN, Eaton MJ, Shuba YM, Kucheryavykh YV, Derst C, Veh RW, Wurm A, Iandiev I, Pannicke T, Bringmann A, Reichenbach A (2006) Tandem-pore domain potassium channels are functionally expressed in retinal (Muller) glial cells. Glia 53:266–276.PubMedGoogle Scholar
  105. Somjen GG (1979) Extracellular potassium in the mammalian central nervous system. Annu Rev Physiol 41:159–177. PubMedGoogle Scholar
  106. Somjen GG (2001) Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 81:1065–1096.PubMedGoogle Scholar
  107. Somjen GG (2002) Ion regulation in the brain: implications for pathophysiology. Neuroscientist 8:254–267.PubMedGoogle Scholar
  108. Sontheimer (1994) Voltage-dependent ion channels in glial cells. Glia 11:156–172.PubMedGoogle Scholar
  109. Stanfield PR, Nakajima S, Nakajima Y (2002) Constitutively active and G-protein coupled inward rectifier K+ channels: Kir2.0 and Kir3.0 Rev Physiol Biochem Pharmacol 145:47–179.PubMedGoogle Scholar
  110. Stonehouse AH, Pringle JH, Norman RI, Stanfield PR, Conley EC, Brammar WJ (1999) Characterisation of Kir2.0 proteins in the rat cerebellum and hippocampus by polyclonal antibodies. Histochem Cell Biol 112:457–465.PubMedGoogle Scholar
  111. Sweadner KJ (1995) Na,K-ATPase and its isoforms. In: Kettenmann H, Ransom BR, eds), pp Neuroglia (Oxford University Press. New York: 259–272.Google Scholar
  112. Tada Y, Horio Y, Kurachi Y (1998) Inwardly rectifying K+ channel in retinal Müller cells: comparison with the KAB-2/Kir4.1 channel expressed in HEK293T cells Jpn J Physiol 48:71–80.PubMedGoogle Scholar
  113. Takumi T, Ishii T, Horio Y, Morishige K, Takahashi N, Yamada M, Yamashita T, Kiyami H, Sohmiya K, Nakanishi S, Kurachi Y (1995) A novel ATP-dependent inward rectifier potassium channel expressed predominantly in glial cells. J Biol Chem 270:16339–16346.PubMedGoogle Scholar
  114. Tucker SJ, Imbrici P, Salvatore L, D’Adamo MC, Pessia M (2000) pH dependence of the inwardly rectifying potassium channel, Kir5.1, and localization in renal tubular epithelia. J Biol Chem 275:16404–16407.PubMedGoogle Scholar
  115. Vyskocil F, Kritz N, Bures J (1972) Potassium-selective microelectrodes used for measuring the extracellular brain potassium during spreading depression and anoxic depolarization in rats. Brain Res 39:255–259.PubMedGoogle Scholar
  116. Wallraff A, Kohling R, Heinemann U, Theis M, Willecke K, Steinhauser C (2006) The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. J Neurosci 26:5438–5447.PubMedGoogle Scholar
  117. Walz W (1992) Role of Na/K/Cl cotransport in astrocytes. Can J Physiol Pharmacol 70 (Suppl):S260–S262.Google Scholar
  118. Walz W (2002) Chloride/anion channels in glial cell membranes. Glia 40:1–10.PubMedGoogle Scholar
  119. Xu X, Karwoski C (1997) The origin of slow PIII in frog retina: current source density analysis in the eyecup and isolated retina. Vis Neurosci 14:827–833.PubMedGoogle Scholar
  120. Zahs KR, Kofuji P, Meier C, Dermietzel R (2003) Connexin immunoreactivity in glial cells of the rat retina. J Comp Neurol 455:531–546.PubMedGoogle Scholar
  121. Zhou M, Schools GP, Kimelberg HK (2006) Development of GLAST(+) astrocytes and NG2(+) glia in rat hippocampus CA1: mature astrocytes are electrophysiologically passive. J Neurophysiol 95:134–143.PubMedGoogle Scholar

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© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Paulo Kofuji
    • 1
  • Eric A. Newman
    • 1
  1. 1.Department of NeuroscienceUniversity of MinnesotaMinneapolisUSA

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