The Neuroglial Potassium Cycle during Neurotransmission: Role of Kir4.1 Channels

PLoS Computational Biology

Volumn 11, Issue 3, 2015, Pages

  Sibille, Jérémie ^a,b   Dao Duc, Khanh ^c,d   Holcman, David ^c   Rouach, Nathalie ^a  

^a Centre de Recherche Interdisciplinaire en Biologie   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c CNRS   (France)

^d SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMICS; ELECTROPHYSIOLOGY; NEURONS;

ACTION-POTENTIALS; ACTIVITY-DEPENDENT; COMPARTMENT MODELING; EXTRACELLULAR; EXTRACELLULAR SPACE; MOLECULAR PATHWAYS; POTASSIUM DYNAMICS; POTASSIUM HOMEOSTASIS; POTASSIUM IONS; RHYTHMIC ACTIVITY;

POTASSIUM;

INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR4.1; UNCLASSIFIED DRUG; KCNJ10 (CHANNEL); POTASSIUM;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; EXTRACELLULAR SPACE; FEMALE; GLIA CELL; HIPPOCAMPUS; HOMEOSTASIS; LOW FREQUENCY NOISE; MALE; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL STIMULATION; NEUROTRANSMISSION; NONHUMAN; POTASSIUM HOMEOSTASIS; POTASSIUM METABOLISM; POTASSIUM TRANSPORT; PROTEIN FUNCTION; QUANTITATIVE STUDY; THETA RHYTHM; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; GLIA; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; ASTROCYTES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, NEUROLOGICAL; NEUROGLIA; NEURONS; POTASSIUM; POTASSIUM CHANNELS, INWARDLY RECTIFYING; SYNAPTIC TRANSMISSION;

EID: 84926311570     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1004137     Document Type: Article

References (73)

1. Bushong EA, Martone ME, Ellisman MH, Maturation of astrocyte morphology and the establishment of astrocyte domains during postnatal hippocampal development. Int J Dev Neurosci. 2004;22: 73–86. 15036382
2. Perea G, Navarrete M, Araque A, Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci. 2009;32: 421–431. doi: 10.1016/j.tins.2009.05.001 19615761
3. Verkhratsky A, Rodriguez JJ, Parpura V, Calcium signalling in astroglia. Mol Cell Endocrinol. 2012;353: 45–56. doi: 10.1016/j.mce.2011.08.039 21945602
4. Bergles DE, Jahr CE, Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron. 1997;19: 1297–1308. 9427252
5. Diamond JS, Bergles DE, Jahr CE, Glutamate release monitored with astrocyte transporter currents during LTP. Neuron. 1998;21: 425–433. 9728923
6. Goubard V, Fino E, Venance L, Contribution of astrocytic glutamate and GABA uptake to corticostriatal information processing. J Physiol. 2011;589: 2301–2319. doi: 10.1113/jphysiol.2010.203125 21486792
7. Luscher C, Malenka RC, Nicoll RA, Monitoring glutamate release during LTP with glial transporter currents. Neuron. 1998;21: 435–441. 9728924
8. Karwoski CJ, Coles JA, Lu HK, Huang B, Current-evoked transcellular K+ flux in frog retina. J Neurophysiol. 1989;61: 939–952. 2786057
9. Meeks JP, Mennerick S, Astrocyte membrane responses and potassium accumulation during neuronal activity. Hippocampus. 2007;17: 1100–1108. 17853441
10. Orkand RK, Nicholls JG, Kuffler SW, Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J Neurophysiol. 1966;29: 788–806. 5966435
11. Nedergaard M, Verkhratsky A, Artifact versus reality—how astrocytes contribute to synaptic events. Glia. 2012;60: 1013–1023. doi: 10.1002/glia.22288 22228580
12. Kuffler SW, Nicholls JG, Orkand RK, Physiological properties of glial cells in the central nervous system of amphibia. J Neurophysiol. 1966;29: 768–787. 5966434
13. Cressman JR, Jr.Ullah G, Ziburkus J, Schiff SJ, Barreto E, The influence of sodium and potassium dynamics on excitability, seizures, and the stability of persistent states: I. Single neuron dynamics. J Comput Neurosci. 2009;26: 159–170. doi: 10.1007/s10827-008-0132-4 19169801
14. David Y, Cacheaux LP, Ivens S, Lapilover E, Heinemann U, et al. Astrocytic dysfunction in epileptogenesis: consequence of altered potassium and glutamate homeostasis? J Neurosci. 2009;29: 10588–10599. doi: 10.1523/JNEUROSCI.2323-09.2009 19710312
15. Ullah G, Cressman JR, Jr.Barreto E, Schiff SJ., The influence of sodium and potassium dynamics on excitability, seizures, and the stability of persistent states. II. Network and glial dynamics. J Comput Neurosci. 2009;26: 171–183. doi: 10.1007/s10827-008-0130-6 19083088
16. Dronne MA, Boissel JP, Grenier E, A mathematical model of ion movements in grey matter during a stroke. J Theor Biol. 2006;240: 599–615. 16368113
17. Dronne MA, Grenier E, Dumont T, Hommel M, Boissel JP, Role of astrocytes in grey matter during stroke: a modelling approach. Brain Res. 2007;1138: 231–242. 17274959
18. Butt AM, Kalsi A, Inwardly rectifying potassium channels (Kir) in central nervous system glia: a special role for Kir4.1 in glial functions. J Cell Mol Med. 2006;10: 33–44. 16563220
19. Walz W, Role of astrocytes in the clearance of excess extracellular potassium. Neurochem Int. 2000;36: 291–300. 10732996
20. Bay V, Butt AM, Relationship between glial potassium regulation and axon excitability: a role for glial Kir4.1 channels. Glia. 2012;60: 651–660. doi: 10.1002/glia.22299 22290828
21. Chever O, Djukic B, McCarthy KD, Amzica F, Implication of Kir4.1 channel in excess potassium clearance: an in vivo study on anesthetized glial-conditional Kir4.1 knock-out mice. J Neurosci. 2010;30: 15769–15777. doi: 10.1523/JNEUROSCI.2078-10.2010 21106816
22. Djukic B, Casper KB, Philpot BD, Chin LS, McCarthy KD, 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. 2007;27: 11354–11365. 17942730
23. Haj-Yasein NN, Jensen V, Vindedal GF, Gundersen GA, Klungland A, et al. Evidence that compromised K+ spatial buffering contributes to the epileptogenic effect of mutations in the human Kir4.1 gene (KCNJ10). Glia. 2011;59: 1635–1642. doi: 10.1002/glia.21205 21748805
24. Kager H, Wadman WJ, Somjen GG, Simulated seizures and spreading depression in a neuron model incorporating interstitial space and ion concentrations. J Neurophysiol. 2000;84: 495–512. 10899222
25. Dallerac G, Chever O, Rouach N, How do astrocytes shape synaptic transmission? Insights from electrophysiology. Front Cell Neurosci. 2013;7: 159. doi: 10.3389/fncel.2013.00159 24101894
26. Sibille J, Pannasch U, Rouach N, Astroglial potassium clearance contributes to short-term plasticity of synaptically evoked currents at the tripartite synapse. J Physiol. 2014;592: 87–102. doi: 10.1113/jphysiol.2013.261735 24081156
27. Balestrino M, Aitken PG, Somjen GG, The effects of moderate changes of extracellular K+ and Ca2+ on synaptic and neural function in the CA1 region of the hippocampal slice. Brain Res. 1986;377: 229–239. 3015348
28. Hablitz JJ, Lundervold A, Hippocampal excitability and changes in extracellular potassium. Exp Neurol. 1981;71: 410–420. 7449908
29. Izquierdo I, Nasello AG, Marichich ES, The dependence of hippocampal function on extracellular potassium levels. Curr Mod Biol. 1971;4: 35–46. 4930771
30. Poolos NP, Kocsis JD, Elevated extracellular potassium concentration enhances synaptic activation of N-methyl-D-aspartate receptors in hippocampus. Brain Res. 1990;508: 7–12. 2159824
31. Poolos NP, Mauk MD, Kocsis JD, Activity-evoked increases in extracellular potassium modulate presynaptic excitability in the CA1 region of the hippocampus. J Neurophysiol. 1987;58: 404–416. 3655875
32. Raffaelli G, Saviane C, Mohajerani MH, Pedarzani P, Cherubini E, BK potassium channels control transmitter release at CA3-CA3 synapses in the rat hippocampus. J Physiol. 2004;557: 147–157. 15034127
33. Florence G, Dahlem MA, Almeida AC, Bassani JW, Kurths J, The role of extracellular potassium dynamics in the different stages of ictal bursting and spreading depression: a computational study. J Theor Biol. 2009;258: 219–228. doi: 10.1016/j.jtbi.2009.01.032 19490858
34. Oyehaug L, Ostby I, Lloyd CM, Omholt SW, Einevoll GT, Dependence of spontaneous neuronal firing and depolarisation block on astroglial membrane transport mechanisms. J Comput Neurosci. 2012;32: 147–165. doi: 10.1007/s10827-011-0345-9 21667153
35. Ziburkus J, Cressman JR, Barreto E, Schiff SJ, Interneuron and pyramidal cell interplay during in vitro seizure-like events. J Neurophysiol. 2006;95: 3948–3954. 16554499
36. McBain CJ, Hippocampal inhibitory neuron activity in the elevated potassium model of epilepsy. J Neurophysiol. 1994;72: 2853–2863. 7897494
37. Parpura V, Grubisic V, Verkhratsky A, Ca(2+) sources for the exocytotic release of glutamate from astrocytes. Biochim Biophys Acta. 2011;1813: 984–991. doi: 10.1016/j.bbamcr.2010.11.006 21118669
38. Kindler CH, Pietruck C, Yost CS, Sampson ER, Gray AT, Localization of the tandem pore domain K+ channel TASK-1 in the rat central nervous system. Brain Res Mol Brain Res. 2000;80: 99–108. 11039733
39. Verkhrastky A, Butt A, Glial physiology and pathophysiology. Chichester: Wiley Blackwell; 2013.
40. Pasler D, Gabriel S, Heinemann U, Two-pore-domain potassium channels contribute to neuronal potassium release and glial potassium buffering in the rat hippocampus. Brain Res. 2007;1173: 14–26. 17850772
41. Larsen BR, Assentoft M, Cotrina ML, Hua SZ, Nedergaard M, et al. Contributions of the Na(+)/K(+)-ATPase, NKCC1, and Kir4.1 to hippocampal K(+) clearance and volume responses. Glia. 2014;62: 608–622. doi: 10.1002/glia.22629 24482245
42. Freche D, Pannasch U, Rouach N, Holcman D, Synapse geometry and receptor dynamics modulate synaptic strength. PLoS One. 2011;6: e25122. doi: 10.1371/journal.pone.0025122 21984900
43. Bordey A, Sontheimer H, Properties of human glial cells associated with epileptic seizure foci. Epilepsy Res. 1998;32: 286–303. 9761328
44. Das A, Wallace GCt, Holmes C, McDowell ML, Smith JA, et al. Hippocampal tissue of patients with refractory temporal lobe epilepsy is associated with astrocyte activation, inflammation, and altered expression of channels and receptors. Neuroscience. 2012;220: 237–246. doi: 10.1016/j.neuroscience.2012.06.002 22698689
45. Hinterkeuser S, Schroder W, Hager G, Seifert G, Blumcke I, et al. Astrocytes in the hippocampus of patients with temporal lobe epilepsy display changes in potassium conductances. Eur J Neurosci. 2000;12: 2087–2096. 10886348
46. Kivi A, Lehmann TN, Kovacs R, Eilers A, Jauch R, et al. Effects of barium on stimulus-induced rises of [K+]o in human epileptic non-sclerotic and sclerotic hippocampal area CA1. Eur J Neurosci. 2000;12: 2039–2048. 10886343
47. Kofuji P, Biedermann B, Siddharthan V, Raap M, Iandiev I, et al. Kir potassium channel subunit expression in retinal glial cells: implications for spatial potassium buffering. Glia. 2002;39: 292–303. 12203395
48. Buono RJ, Lohoff FW, Sander T, Sperling MR, O’Connor MJ, et al. Association between variation in the human KCNJ10 potassium ion channel gene and seizure susceptibility. Epilepsy Res. 2004;58: 175–183. 15120748
49. Heuser K, Nagelhus EA, Tauboll E, Indahl U, Berg PR, et al. Variants of the genes encoding AQP4 and Kir4.1 are associated with subgroups of patients with temporal lobe epilepsy. Epilepsy Res. 2010;88: 55–64. doi: 10.1016/j.eplepsyres.2009.09.023 19864112
50. Tong X, Ao Y, Faas GC, Nwaobi SE, Xu J, et al. Astrocyte Kir4.1 ion channel deficits contribute to neuronal dysfunction in Huntington’s disease model mice. Nat Neurosci. 2014;17: 694–703. doi: 10.1038/nn.3691 24686787
51. Srivastava R, Aslam M, Kalluri SR, Schirmer L, Buck D, et al. Potassium channel KIR4.1 as an immune target in multiple sclerosis. N Engl J Med. 2012;367: 115–123. doi: 10.1056/NEJMoa1110740 22784115
52. Pannasch U, Derangeon M, Chever O, Rouach N, Astroglial gap junctions shape neuronal network activity. Commun Integr Biol. 2012;5: 248–254. doi: 10.4161/cib.19410 22896785
53. Pannasch U, Freche D, Dallerac G, Ghezali G, Escartin C, et al. Connexin 30 sets synaptic strength by controlling astroglial synapse invasion. Nat Neurosci. 2014;17: 549–558. doi: 10.1038/nn.3662 24584052
54. Pannasch U, Sibille J, Rouach N, Dual electrophysiological recordings of synaptically-evoked astroglial and neuronal responses in acute hippocampal slices. J Vis Exp. 2012: e4418. doi: 10.3791/4418 23222635
55. Tsodyks MV, Markram H, The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci U S A. 1997;94: 719–723. 9012851
56. Markram H, Wang Y, Tsodyks M, Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci U S A. 1998;95: 5323–5328. 9560274
57. Tsodyks M, Pawelzik K, Markram H, Neural networks with dynamic synapses. Neural Comput. 1998;10: 821–835. 9573407
58. Hodgkin AL, Huxley AF, A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952;117: 500–544. 12991237
59. Siegenbeek van, Heukelom J, The role of the potassium inward rectifier in defining cell membrane potentials in low potassium media, analyzed by computer simulation. Biophys Chem. 1994;50: 345–360.
60. Ransom CB, Sontheimer H, Biophysical and pharmacological characterization of inwardly rectifying K+ currents in rat spinal cord astrocytes. J Neurophysiol. 1995;73: 333–346. 7714576
61. Carmeliet E, Biermans G, Callewaert G, Vereecke J, Potassium currents in cardiac cells. Experientia. 1987;43: 1175–1184. 2446912
62. Hagiwara S, Takahashi K, The anomalous rectification and cation selectivity of the membrane of a starfish egg cell. J Membr Biol. 1974;18: 61–80. 4854650
63. Mazzanti M, DeFelice LJ, K channel kinetics during the spontaneous heart beat in embryonic chick ventricle cells. Biophys J. 1988;54: 1139–1148. 3233269
64. Sakmann B, Trube G, Conductance properties of single inwardly rectifying potassium channels in ventricular cells from guinea-pig heart. J Physiol. 1984;347: 641–657. 6323703
65. Ransom CB, Sontheimer H, Janigro D, Astrocytic inwardly rectifying potassium currents are dependent on external sodium ions. J Neurophysiol. 1996;76: 626–630. 8836250
66. Reichenbach A, Henke A, Eberhardt W, Reichelt W, Dettmer D, K+ ion regulation in retina. Can J Physiol Pharmacol. 1992;70 Suppl: S239–247. 1295673
67. Cox TC, Helman SI, Na+ and K+ transport at basolateral membranes of epithelial cells. II. K+ efflux and stoichiometry of the Na,K-ATPase. J Gen Physiol. 1986;87: 485–502. 2420920
68. Lesage F, Lazdunski M, Molecular and functional properties of two-pore-domain potassium channels. Am J Physiol Renal Physiol. 2000;279: F793–801. 11053038
69. Chever O, Lee CY, Rouach N, Astroglial connexin43 hemichannels tune basal excitatory synaptic transmission. J Neurosci. 2014;34: 11228–11232. doi: 10.1523/JNEUROSCI.0015-14.2014 25143604
70. Bolshakov VY, Siegelbaum SA, Regulation of hippocampal transmitter release during development and long-term potentiation. Science. 1995;269: 1730–1734. 7569903
71. Hodgkin AL, Huxley AF, Katz B, Measurement of current-voltage relations in the membrane of the giant axon of Loligo. J Physiol. 1952;116: 424–448. 14946712
72. Chever O, Pannasch U, Ezan P, Rouach N, Astroglial connexin 43 sustains glutamatergic synaptic efficacy. Philos Trans R Soc Lond B Biol Sci. 2014;369.
73. Chen KC, Nicholson C, Spatial buffering of potassium ions in brain extracellular space. Biophys J. 2000;78: 2776–2797. 10827962