Glial K+ clearance and cell swelling: Key roles for cotransporters and pumps

Neurochemical Research

Volumn 37, Issue 11, 2012, Pages 2299-2309

  MacAulay, Nanna ^a   Zeuthen, Thomas ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Cell swelling; Extracellular space; Glia; K+ clearance; Transport proteins

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); AQUAPORIN 4; INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR4.1; POTASSIUM ION; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; UNCLASSIFIED DRUG; WATER;

BRAIN SLICE; CELL CULTURE; CELL SWELLING; CONCENTRATION (PARAMETERS); CONCENTRATION RESPONSE; EVOKED RESPONSE; EXTRACELLULAR SPACE; GLIA CELL; HUMAN; NONHUMAN; OPTIC NERVE; POTASSIUM CELL LEVEL; POTASSIUM CLEARANCE; POTASSIUM TRANSPORT; PRIORITY JOURNAL; REVIEW; WATER TRANSPORT;

ANIMALS; HOMEOSTASIS; HUMANS; MEMBRANE TRANSPORT PROTEINS; NEUROGLIA; POTASSIUM;

EID: 84871414640     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-012-0731-3     Document Type: Review

References (112)

1. Frankenhaeuser B, Hodgkin AL (1956) The after-effects of impulses in the giant nerve fibres of Loligo. J Physiol 131: 341-376
2. Ballanyi K, Branchereau P, Champagnat J, Fortin G, Velluti J (1993) Extracellular potassium, glial and neuronal potentials in the solitary complex of rat brainstem slices. Brain Res 607: 99-107
3. Hackman JC, Ryan GP, Davidoff RA (1982) Excitatory amino acids and potassium release in the frog spinal cord. Neurosci Lett 33:289-293
4. 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
5. Kettenmann H, Sonnhof U, Schachner M (1983) Exclusive potassium dependence of the membrane potential in cultured mouse oligodendrocytes. J Neurosci 3:500-505
6. Kimelberg HK, Bowman C, Biddlecome S, Bourke RS (1979) Cation transport and membrane potential properties of primary astroglial cultures from neonatal rat brains. Brain Res 177: 533-550
7. Kuffler SW, Nicholls JG, Orkand RK (1966) Physiological properties of glial cells in the central nervous system of amphibia. J Neurophysiol 29:768-787
8. Ransom BR, Goldring S (1973) Ionic determinants of membrane potential of cells presumed to be glia in cerebral cortex of cat. J Neurophysiol 36:855-868
9. Amzica F, Massimini M, Manfridi A (2002) Spatial buffering during slow and paroxysmal sleep oscillations in cortical networks of glial cells in vivo. J Neurosci 22:1042-1053
10. Ballanyi K, Grafe P, Ten BG (1987) Ion activities and potassium uptake mechanisms of glial cells in guinea-pig olfactory cortex slices. J Physiol 382:159-174
11. Coles JA, Schneider-Picard G (1989) Increase in glial intracellular K+ in drone retina caused by photostimulation but not mediated by an increase in extracellular K+. Glia 2:213-222
12. 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
13. Grafe P, Ballanyi K (1987) Cellular mechanisms of potassium homeostasis in the mammalian nervous system. Can J Physiol Pharmacol 65:1038-1042
14. Chever O, Djukic B, McCarthy KD, Amzica F (2010) Implication of Kir4.1 channel in excess potassium clearance: An in vivo study on anesthetized glial-conditional Kir4.1 knock-out mice. J Neurosci 30:15769-15777
15. Haj-Yasein NN, Jensen V, Vindedal GF, Gundersen GA, Klungland A, Ottersen OP, Hvalby O, Nagelhus EA (2011) Evidence that compromised K(+) spatial buffering contributes to the epileptogenic effect of mutations in the human kir4.1 gene (KCNJ10). Glia 59:1635-1642
16. Meeks JP, Mennerick S (2007) Astrocyte membrane responses and potassium accumulation during neuronal activity. Hippocampus 17:1100-1108
17. Ransom CB, Ransom BR, Sontheimer H (2000) Activitydependent extracellular K+ accumulation in rat optic nerve: The role of glial and axonal Na+ pumps. J Physiol 522(Pt 3): 427-442
18. Nicholls JG, Kuffler SW (1965) Na and K content of glial cells and neurons determined by flame photometry in the central nervous system of the leech. J Neurophysiol 28:519-525
19. Schlue WR, Wuttke W (1983) Potassium activity in leech neuropile glial cells changes with external potassium concentration. Brain Res 270:368-372
20. Wuttke WA (1990) Mechanism of potassium uptake in neuropile glial cells in the central nervous system of the leech. J Neurophysiol 63:1089-1097
21. Coles JA, Orkand RK (1983) Modification of potassium movement through the retina of the drone (Apis mellifera male) by glial uptake. J Physiol 340:157-174
22. Blaustein MP, Kao JPY, Matteson DR (2004) Cellular Physiology. Elsevier, USA
23. Djukic B, Casper KB, Philpot BD, Chin LS, McCarthy KD (2007) Conditional knock-out of Kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation. J Neurosci 27:11354-11365
24. 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
25. 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
26. Philippi M, Vyklicky L, Orkand RK (1996) Potassium currents in cultured glia of the frog optic nerve. Glia 17:72-82
27. Skatchkov SN, Krusek J, Reichenbach A, Orkand RK (1999) Potassium buffering by Muller cells isolated from the center and periphery of the frog retina. Glia 27:171-180
28. Kofuji P, Newman EA (2004) Potassium buffering in the central nervous system. Neuroscience 129:1045-1056
29. Orkand RK (1986) Glial-interstitial fluid exchange. Ann N Y Acad Sci 481:269-272
30. Olsen ML, Sontheimer H (2008) Functional implications for Kir4.1 channels in glial biology: From K+ buffering to cell differentiation. J Neurochem 107:589-601
31. Nagelhus EA, Horio Y, Inanobe A, Fujita A, Haug FM, Nielsen S, Kurachi Y, Ottersen OP (1999) Immunogold evidence suggests that coupling of K+ siphoning and water transport in rat retinal Muller cells is mediated by a coenrichment of Kir4.1 and AQP4 in specific membrane domains. Glia 26:47-54
32. Newman EA (1984) Regional specialization of retinal glial cell membrane. Nature 309:155-157
33. Newman EA (1986) High potassium conductance in astrocyte endfeet. Science 233:453-454
34. Karwoski CJ, Lu HK, Newman EA (1989) Spatial buffering of light-evoked potassium increases by retinal Muller (glial) cells. Science 244:578-580
35. Oakley B, Katz BJ, Xu Z, Zheng J (1992) Spatial buffering of extracellular potassium by Muller (glial) cells in the toad retina. Exp Eye Res 55:539-550
36. Newman EA, Frambach DA, Odette LL (1984) Control of extracellular potassium levels by retinal glial cell K+ siphoning. Science 225:1174-1175
37. 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
38. Scholl UI, Choi M, Liu T, Ramaekers VT, Hausler MG, Grimmer J, Tobe SW, Farhi A, Nelson-Williams C, Lifton RP (2009) Seizures, sensorineural deafness, ataxia, mental retardation, and electrolyte imbalance (SeSAME syndrome) caused by mutations in KCNJ10. Proc Natl Acad Sci USA 106:5842-5847
39. Ransom CB, Sontheimer H (1995) Biophysical and pharmacological characterization of inwardly rectifying K+ currents in rat spinal cord astrocytes. J Neurophysiol 73:333-346
40. 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
41. Xiong ZQ, Stringer JL (2000) Sodium pump activity, not glial spatial buffering, clears potassium after epileptiform activity induced in the dentate gyrus. J Neurophysiol 83:1443-1451
42. Kivi A, Lehmann TN, Kovacs R, Eilers A, Jauch R, Meencke HJ, von DA, Heinemann U, Gabriel S (2000) Effects of barium on stimulus-induced rises of [K+]o in human epileptic nonsclerotic and sclerotic hippocampal area CA1. Eur J Neurosci 12:2039-2048
43. Walz W, Shargool M, Hertz L (1984) Barium-induced inhibition of K+ transport mechanisms in cortical astrocytes-its possible contribution to the large Ba2+-evoked extracellular K+ signal in brain. Neuroscience 13:945-949
44. Juhaszova M, Blaustein MP (1997) Na+ pump low and high ouabain affinity alpha subunit isoforms are differently distributed in cells. Proc Natl Acad Sci USA 94:1800-1805
45. McGrail KM, Phillips JM, Sweadner KJ (1991) 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 11:381-391
46. Blanco G, Mercer RW (1998) Isozymes of the Na-K-ATPase: Heterogeneity in structure, diversity in function. Am J Physiol 275:F633-F650
47. Crambert G, Hasler U, Beggah AT, Yu C, Modyanov NN, Horisberger JD, Lelievre L, Geering K (2000) Transport and pharmacological properties of nine different human Na, K-ATPase isozymes. J Biol Chem 275:1976-1986
48. Jewell EA, Lingrel JB (1991) Comparison of the substrate dependence properties of the rat Na, K-ATPase alpha 1, alpha 2, and alpha 3 isoforms expressed in HeLa cells. J Biol Chem 266:16925-16930
49. O'Brien WJ, Lingrel JB, Wallick ET (1994) Ouabain binding kinetics of the rat alpha two and alpha three isoforms of the sodium-potassium adenosine triphosphate. Arch Biochem Biophys 310:32-39
50. Atterwill CK, Cunningham VJ, Balazs R (1984) Characterization of Na+, K+-ATPase in cultured and separated neuronal and glial cells from rat cerebellum. J Neurochem 43:8-18
51. Sweadner KJ (1979) Two molecular forms of (Na+ ? K+)-stimulated ATPase in brain. Separation, and difference in affinity for strophanthidin. J Biol Chem 254:6060-6067
52. Blaesse P, Airaksinen MS, Rivera C, Kaila K (2009) Cation-chloride cotransporters and neuronal function. Neuron 61:820-838
53. 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
54. O'Donnell ME, Tran L, Lam TI, Liu XB, Anderson SE (2004) Bumetanide inhibition of the blood-brain barrier Na-K-Cl cotransporter reduces edema formation in the rat middle cerebral artery occlusion model of stroke. J Cereb Blood Flow Metab 24:1046-1056
55. Malek SA, Coderre E, Stys PK (2003) Aberrant chloride transport contributes to anoxic/ischemic white matter injury. J Neurosci 23:3826-3836
56. Ringel F, Plesnila N (2008) Expression and functional role of potassium-chloride cotransporters (KCC) in astrocytes and C6 glioma cells. Neurosci Lett 442:219-223
57. Johnson JH, Dunn DP, Rosenberg RN (1982) Furosemide-sensitive K+ channel in glioma cells but not neuroblastoma cells in culture. Biochem Biophys Res Commun 109:100-105
58. Tas PW, Massa PT, Koschel K (1986) Preliminary characterization of an Na+, K+, Cl-co-transport activity in cultured human astrocytes. Neurosci Lett 70:369-373
59. Tas PW, Massa PT, Kress HG, Koschel K (1987) Characterization of an Na+/K+/Cl-co-transport in primary cultures of rat astrocytes. Biochim Biophys Acta 903:411-416
60. Walz W, Hertz L (1982) Ouabain-sensitive and ouabain-resistant net uptake of potassium into astrocytes and neurons in primary cultures. J Neurochem 39:70-77
61. Walz W, Hinks EC (1985) Carrier-mediated KCl accumulation accompanied by water movements is involved in the control of physiological K+ levels by astrocytes. Brain Res 343:44-51
62. Wolpaw EW, Martin DL (1984) Cl-transport in a glioma cell line: Evidence for two transport mechanisms. Brain Res 297:317-327
63. Walz W, Hertz L (1984) Intense furosemide-sensitive potassium accumulation in astrocytes in the presence of pathologically high extracellular potassium levels. J Cereb Blood Flow Metab 4:301-304
64. Ballanyi K, Kettenmann H (1990) Intracellular Na+ activity in cultured mouse oligodendrocytes. J Neurosci Res 26:455-460
65. Kelly T, Kafitz KW, Roderigo C, Rose CR (2009) Ammoniumevoked alterations in intracellular sodium and pH reduce glial glutamate transport activity. Glia 57:921-934
66. Lund-Andersen H, Hertz L (1970) Effects of potassium content in brain-cortex slices from adult rats. Exp Brain Res 11:199-212
67. Rose CR, Ransom BR (1996) Intracellular sodium homeostasis in rat hippocampal astrocytes. J Physiol 491(Pt 2):291-305
68. Walz W, Hinks EC (1986) A transmembrane sodium cycle in astrocytes. Brain Res 368:226-232
69. Walz W, Hertz L (1983) Intracellular ion changes of astrocytes in response to extracellular potassium. J Neurosci Res 10: 411-423
70. Boyle PJ, Conway EJ (1941) Potassium accumulation in muscle and associated changes. J Physiol 100:1-63
71. Ballanyi K, Grafe P, Serve G, Schlue WR (1990) Electrophysiological measurements of volume changes in leech neuropile glial cells. Glia 3:151-158
72. Bourke RS, Nelson KM (1972) Further studies on the K ?-dependent swelling of primate cerebral cortex in vivo: The enzymatic basis of the K ?-dependent transport of chloride. J Neurochem 19:663-685
73. 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
74. MacVicar BA, Hochman D (1991) Imaging of synaptically evoked intrinsic optical signals in hippocampal slices. J Neurosci 11:1458-1469
75. Orkand RK, Dietzel I, Coles JA (1984) Light-induced changes in extracellular volume in the retina of the drone, Apis mellifera. Neurosci Lett 45:273-278
76. Ransom BR, Yamate CL, Connors BW (1985) Activity-dependent shrinkage of extracellular space in rat optic nerve: A developmental study. J Neurosci 5:532-535
77. Bourke RS, Nelson KM, Naumann RA, Young OM (1970) Studies of the production and subsequent reduction swelling in primate. Cerebral cortex under isosmotic conditions in vivo. Exp Brain Res 10:427-446
78. Risher WC, Andrew RD, Kirov SA (2009) Real-time passive volume responses of astrocytes to acute osmotic and ischemic stress in cortical slices and in vivo revealed by two-photon microscopy. Glia 57:207-221
79. Sykova E, Vargova L, Prokopova S, Simonova Z (1999) Glial swelling and astrogliosis produce diffusion barriers in the rat spinal cord. Glia 25:56-70
80. Bourke RS (1969) Studies of the development and subsequent reduction of swelling of mammalian cerebral cortex under isosmotic conditions in vitro. Exp Brain Res 8:232-248
81. Su G, Kintner DB, Sun D (2002) Contribution of Na(+)-K(+)-Cl(-) cotransporter to high-[K(+)](o)-induced swelling and EAA release in astrocytes. Am J Physiol Cell Physiol 282: C1136-C1146
82. Su G, Kintner DB, Flagella M, Shull GE, Sun D (2002) Astrocytes from Na(+)-K(+)-Cl(-) cotransporter-null mice exhibit absence of swelling and decrease in EAA release. Am J Physiol Cell Physiol 282:C1147-C1160
83. Hamann S, Herrera-Perez JJ, Zeuthen T, Alvarez-Leefmans FJ (2010) Cotransport of water by the Na+-K+-2Cl-cotransporter NKCC1 in mammalian epithelial cells. J Physiol 588: 4089-4101
84. Zeuthen T, MacAulay N (2012) Cotransport of water by Na+-K+-2Cl- cotransporters expressed in Xenopus oocytes: NKCC1 versus NKCC2. J. Physiol (in press)
85. MacAulay N, Zeuthen T (2010) Water transport between CNS compartments: Contributions of aquaporins and cotransporters. Neuroscience 168:941-956
86. Zeuthen T (2010) Water-transporting proteins. J Membr Biol 234:57-73
87. MacAulay N, Hamann S, Zeuthen T (2004) Water transport in the brain: Role of cotransporters. Neuroscience 129:1031-1044
88. Zeuthen T (1994) Cotransport of K+, Cl-and H2O by membrane proteins from choroid plexus epithelium of Necturus maculosus. J Physiol 478(Pt 2):203-219
89. Bergles DE, Jahr CE (1997) Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron 19:1297-1308
90. Izumi Y, Kirby CO, Benz AM, Olney JW, Zorumski CF (1999) Muller cell swelling, glutamate uptake, and excitotoxic neurodegeneration in the isolated rat retina. Glia 25:379-389
91. Koyama Y, Ishibashi T, Okamoto T, Matsuda T, Hashimoto H, Baba A (2000) Transient treatments with L-glutamate and threobeta-hydroxyaspartate induce swelling of rat cultured astrocytes. Neurochem Int 36:167-173
92. Schneider GH, Baethmann A, Kempski O (1992) Mechanisms of glial swelling induced by glutamate. Can J Physiol Pharmacol 70(Suppl):S334-S343
93. MacAulay N, Gether U, Klaerke DA, Zeuthen T (2001) Water transport by the human Na+-coupled glutamate cotransporter expressed in Xenopus oocytes. J Physiol 530:367-378
94. MacAulay N, Gether U, Klaeke DA, Zeuthen T (2002) Passive water and urea permeability of a human Na(+)-glutamate cotransporter expressed in Xenopus oocytes. J Physiol 542: 817-828
95. Vandenberg RJ, Handford CA, Campbell EM, Ryan RM, Yool AJ (2011) Water and urea permeation pathways of the human excitatory amino acid transporter EAAT1. Biochem J 439: 333-340
96. Chaudhry FA, Lehre KP, van Lookeren CM, Ottersen OP, Danbolt NC, Storm-Mathisen J (1995) Glutamate transporters in glial plasma membranes: Highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15:711-720
97. Nielsen S, Nagelhus EA, miry-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
98. Kitaura H, Tsujita M, Huber VJ, Kakita A, Shibuki K, Sakimura K, Kwee IL, Nakada T (2009) Activity-dependent glial swelling is impaired in aquaporin-4 knockout mice. Neurosci Res 64:208-212
99. Amiry-Moghaddam M, Williamson A, Palomba M, Eid T, de Lanerolle NC, Nagelhus EA, Adams ME, Froehner SC, Agre P, Ottersen OP (2003) Delayed K+ clearance associated with aquaporin-4 mislocalization: Phenotypic defects in brains of alpha-syntrophin-null mice. Proc Natl Acad Sci USA 100: 13615-13620
100. Nagelhus EA, Mathiisen TM, Ottersen OP (2004) Aquaporin-4 in the central nervous system: Cellular and subcellular distribution and coexpression with KIR4.1. Neuroscience 129:905-913
101. Strohschein S, Huttmann K, Gabriel S, Binder DK, Heinemann U, Steinhauser C (2011) Impact of aquaporin-4 channels on K+ buffering and gap junction coupling in the hippocampus. Glia 59:973-980
102. Soe R, MacAulay N, Klaerke DA (2009) Modulation of Kir4.1 and Kir4.1-Kir5.1 channels by small changes in cell volume. Neurosci Lett 457:80-84
103. Ruiz-Ederra J, Zhang H, Verkman AS (2007) Evidence against functional interaction between aquaporin-4 water channels and Kir4.1 potassium channels in retinal Muller cells. J Biol Chem 282:21866-21872
104. Zhang H, Verkman AS (2008) Aquaporin-4 independent Kir4.1 K+ channel function in brain glial cells. Mol Cell Neurosci 37:1-10
105. Walz W (2000) Role of astrocytes in the clearance of excess extracellular potassium. Neurochem Int 36:291-300
106. Kimelberg HK (1995) Current concepts of brain edema. Review of laboratory investigations. J Neurosurg 83:1051-1059
107. 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. Nat Methods 2:825-827
108. Binder DK, Yao X, Zador Z, Sick TJ, Verkman AS, Manley GT (2006) Increased seizure duration and slowed potassium kinetics in mice lacking aquaporin-4 water channels. Glia 53:631-636
109. Yao X, Hrabetova S, Nicholson C, Manley GT (2008) Aquaporin-4-deficient mice have increased extracellular space without tortuosity change. J Neurosci 28:5460-5464
110. Zeng XN, Sun XL, Gao L, Fan Y, Ding JH, Hu G (2007) Aquaporin-4 deficiency down-regulates glutamate uptake and GLT-1 expression in astrocytes. Mol Cell Neurosci 34:34-39
111. Haj-Yasein NN, Vindedal GF, Eilert-Olsen M, Gundersen GA, Skare O, Laake P, Klungland A, Thoren AE, Burkhardt JM, Ottersen OP, Nagelhus EA (2011) Glial-conditional deletion of aquaporin-4 (Aqp4) reduces blood-brain water uptake and confers barrier function on perivascular astrocyte endfeet. Proc Natl Acad Sci USA 108:17815-17820
112. Zeuthen T, Belhage B, Zeuthen E (2006) Water transport by Na+-coupled cotransporters of glucose (SGLT1) and of iodide (NIS). The dependence of substrate size studied at high resolution. J Physiol 570:485-499