Functional identification of an outwardly rectifying pH- and anesthetic-sensitive leak K+ conductance in hippocampal astrocytes

European Journal of Neuroscience

Volumn 32, Issue 5, 2010, Pages 725-735

  Chu, Kuo Chang ^a   Chiu, Cheng Di ^b   Hsu, Tsan Ting ^a   Hsieh, Yu Ming ^a   Huang, Yu Yin ^c   Lien, Cheng Chang ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b TAICHUNG HOSPITAL   (Taiwan)

^c CHENG HSIN GENERAL HOSPITAL   (Taiwan)

Author keywords

glia; hippocampus; potassium channel; TASK channel

Indexed keywords

BICARBONATE SODIUM COTRANSPORTER; BUPIVACAINE; ISOFLURANE; POTASSIUM CHANNEL; POTASSIUM CHANNEL TREK 1; POTASSIUM CHANNEL TWIK 1; QUININE; TETRODOTOXIN; UNCLASSIFIED DRUG;

ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN SLICE; CONTROLLED STUDY; HIPPOCAMPUS; MALE; NONHUMAN; PH; POTASSIUM CONDUCTANCE; POTASSIUM CURRENT; PRIORITY JOURNAL; RAT; VOLTAGE CLAMP;

4,4'-DIISOTHIOCYANOSTILBENE-2,2'-DISULFONIC ACID; ANIMALS; ASTROCYTES; BARIUM; BUPIVACAINE; HIPPOCAMPUS; HYDROGEN-ION CONCENTRATION; ISOFLURANE; MALE; MEMBRANE POTENTIALS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; QUININE; RATS; RATS, SPRAGUE-DAWLEY; TETRODOTOXIN;

EID: 77956403381     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07323.x     Document Type: Article

References (52)

1. +-activated currents in hippocampal neurons. J. Biol. Chem., 279, 18296 18305.
2. Balestrino, M. Somjen, G.G. (1988) Concentration of carbon dioxide, interstitial pH and synaptic transmission in hippocampal formation of the rat. J. Physiol., 396, 247 266.
3. Baron, A., Waldmann, R. Lazdunski, M. (2002) ASIC-like, proton-activated currents in rat hippocampal neurons. J. Physiol., 539, 485 494.
4. Bayliss, D.A. Barrett, P.Q. (2008) Emerging roles for two-pore-domain potassium channels and their potential therapeutic impact. Trends Pharmacol. Sci., 29, 566 575.
5. + channels. Mol. Interv., 3, 205 219.
6. +-gated channels in mouse sensory neurons. Proc. Natl Acad. Sci. USA, 99, 2338 2343.
7. Brockway, L.M., Zhou, Z.H., Bubien, J.K., Jovov, B., Benos, D.J. Keyser, K.T. (2002) Rabbit retinal neurons and glia express a variety of ENaC/DEG subunits. Am. J. Physiol. Cell Physiol., 283, C126 C134.
8. Buckler, K.J., Williams, B.A. Honore, E. (2000) An oxygen-, acid- and anaesthetic-sensitive TASK-like background potassium channel in rat arterial chemoreceptor cells. J. Physiol., 525, 135 142.
9. + channels mediate inhibition of orexin neurons by glucose. Neuron, 50, 711 722.
10. Butt, A.M. Kalsi, A. (2006) Inwardly rectifying potassium channels (Kir) in central nervous system glia: a special role for Kir4.1 in glial functions, J. Cell Mol. Med. 10, 33 44.
11. Chesler, M. (2003) Regulation and modulation of pH in the brain. Physiol. Rev., 83, 1183 1221.
12. Chesler, M. Kaila, K. (1992) Modulation of pH by neuronal activity. Trends Neurosci., 15, 396 402.
13. Deitmer, J.W. Rose, C.R. (1996) pH regulation and proton signalling by glial cells. Prog. Neurobiol., 48, 73 103.
14. Dhaka, A., Viswanath, V. Patapoutian, A. (2006) TRP ion channels and temperature sensation. Annu. Rev. Neurosci., 29, 135 161.
15. 2+ signals contribute to neuronal excitotoxicity after status epilepticus. J. Neurosci., 27, 10674 10684.
16. + channel to sense external pH variations near physiological pH. EMBO J., 16, 5464 5471.
17. Duprat, F., Lauritzen, I., Patel, A. Honoré, E. (2007) The TASK background K2P channels: chemo- and nutrient sensors. Trends Neurosci., 30, 573 580.
18. Feldman, D.H., Horiuchi, M., Keachie, K., Mccauley, E., Bannerman, P., Itoh, A., Itoh, T. Pleasure, D. (2008) Characterization of acid-sensing ion channel expression in oligodendrocyte-lineage cells. Glia, 56, 1238 1249.
19. Gao, J., Duan, B., Wang, D.G., Deng, X.H., Zhang, G.Y., Xu, L. Xu, T.L. (2005) Coupling between NMDA receptor and acid-sensing ion channel contributes to ischemic neuronal death. Neuron, 48, 635 646.
20. Goldstein, S.A., Bockenhauer, D., O'Kelly, I. Zilberberg, N. (2001) Potassium leak channels and the KCNK family of two-P-domain subunits. Nat. Rev. Neurosci., 2, 175 184.
21. Hille, B. (2001) Ion channels of excitable membranes. Sinauer, Sunderland, MA.
22. Kafitz, K.W., Meier, S.D., Stephan, J. Rose, C.R. (2008) Developmental profile and properties of sulforhodamine 101-labeled glial cells in acute brain slices of rat hippocampus. J. Neurosci. Methods, 169, 84 92.
23. Kang, D., Han, J., Talley, E.M., Bayliss, D.A. Kim, D. (2004) Functional expression of TASK-1/TASK-3 heteromers in cerebellar granule cells. J. Physiol., 554, 64 77.
24. + channel family. J. Biol. Chem., 275, 9340 9347.
25. +-1 channel immunoreactivity in the rat hippocampal complex following pilocarpine-induced status epilepticus. J. Comp. Neurol., 510, 463 474.
26. + channel TASK-1 in the rat central nervous system. Brain Res. Mol. Brain Res., 80, 99 108.
27. Lauritzen, I., Blondeau, N., Heurteaux, C., Widmann, C., Romey, G. Lazdunski, M. (2000) Polyunsaturated fatty acids are potent neuroprotectors. EMBO J., 19, 1784 1793.
28. Lien, C.C. Jonas, P. (2003) Kv3 potassium conductance is necessary and kinetically optimized for high-frequency action potential generation in hippocampal interneurons. J. Neurosci., 23, 2058 2068.
29. + channels in dendritic inhibitory interneurones of rat hippocampus. J. Physiol., 538, 405 419.
30. Nimmerjahn, A., Kirchhoff, F., Kerr, J.N. Helmchen, F. (2004) Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat. Methods, 1, 31 37.
31. O'Connor, E.R., Sontheimer, H. Ransom, B.R. (1994) Rat hippocampal astrocytes exhibit electrogenic sodium-bicarbonate co-transport. J. Neurophysiol., 72, 2580 2589.
32. + channels. Nat. Neurosci., 2, 422 426.
33. - cotransporters: cloning and physiology. Annu. Rev. Physiol., 61, 699 723.
34. Rossi, D.J., Brady, J.D. Mohr, C. (2007) Astrocyte metabolism and signaling during brain ischemia. Nat. Neurosci., 10, 1377 1386.
35. Rusznák, Z., Pocsai, K., Kovács, I., Pór, Á., Pál, B., Bíró, T. Szücs, 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.
36. Seifert, G., Schilling, K. Steinhäuser, C. (2006) Astrocyte dysfunction in neurological disorders: a molecular perspective. Nat. Rev. Neurosci., 7, 194 206.
37. + channel expression in the developing hippocampus reveals a predominant role of the Kir4.1 subunit. J. Neurosci., 29, 7474 7488.
38. Siesjö, B.K., von Hanwehr, R., Nergelius, G., Nevander, G. Ingvar, M. (1985) Extra- and intracellular pH in the brain during seizures and in the recovery period following the arrest of seizure activity. J. Cereb. Blood Flow Metab., 5, 47 57.
39. + channel is a molecular substrate for neuronal effects of inhalation anesthetics. J. Neurosci., 20, 6347 6354.
40. Stuart, G.J., Dodt, H.U. Sakmann, B. (1993) Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pflügers Arch., 423, 511 518.
41. + channel, is modulated by multiple neurotransmitters in motoneurons. Neuron, 25, 399 410.
42. Talley, E.M., Solórzano, G., Lei, Q., Kim, D. Bayliss, D.A. (2001) CNS distribution of members of the two-pore-domain (KCNK) potassium channel family. J. Neurosci., 21, 7491 7505.
43. Taverna, S., Tkatch, T., Metz, A.E. Martina, M. (2005) Differential expression of TASK channels between horizontal interneurons and pyramidal cells of rat hippocampus. J. Neurosci., 25, 9162 9170.
44. Torborg, C.L., Berg, A.P., Jeffries, B.W., Bayliss, D.A. McBain, C.J. (2006) TASK-like conductances are present within hippocampal CA1 stratum oriens interneuron subpopulations. J. Neurosci., 26, 7362 7367.
45. Waldmann, R., Champigny, G., Bassilana, F., Heurteaux, C. Lazdunski, M. (1997) A proton-gated cation channel involved in acid-sensing. Nature, 386, 173 177.
46. Wemmie, J.A., Price, M.P. Welsh, M.J. (2006) Acid-sensing ion channels: advances, questions and therapeutic opportunities. Trends Neurosci., 29, 578 586.
47. Weng, X.C., Zheng, J.Q., Gai, X.D., Li, J. Xiao, W.B. (2004) Two types of acid-sensing ion channel currents in rat hippocampal neurons. Neurosci. Res., 50, 493 499.
48. Weng, J.Y., Lin, Y.C. Lien, C.C. (2010) Cell Type-Specific Expression of Acid-Sensing Ion Channels in Hippocampal Interneurons. J. Neurosci., 30, 6548 6558.
49. 2. Proc. Natl Acad. Sci. USA, 104, 10685 10690.
50. Xiong, Z.G., Zhu, X.M., Chu, X.P., Minami, M., Hey, J., Wei, W.L., MacDonald, J.F., Wemmie, J.A., Price, M.P., Welsh, M.J. Simon, R.P. (2004) Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell, 118, 687 698.
51. Zhou, M., Xu, G., Xie, M., Zhang, X., Schools, G.P., Ma, L., Kimelberg, H.K. Chen, H. (2009) TWIK-1 and TREK-1 are potassium channels contributing significantly to astrocyte passive conductance in rat hippocampal slices. J. Neurosci., 29, 8551 8564.
52. Ziemann, A.E., Schnizler, M.K., Albert, G.W., Severson, M.A., Howard, M.A. III., Welsh, M.J. Wemmie, J.A. (2008) Seizure termination by acidosis depends on ASIC1a. Nat. Neurosci., 11, 816 822.