Inwardly rectifying potassium channel Kir4.1 is responsible for the native inward potassium conductance of satellite glial cells in sensory ganglia

Neuroscience

Volumn 166, Issue 2, 2010, Pages 397-407

  Tang, X ^a   Schmidt, T M ^a   Perez Leighton, C E ^a   Kofuji, P ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Dorsal root ganglia; KCNJ10; Pain; Potassium buffering; Potassium channel; Trigeminal ganglia

Indexed keywords

BARIUM; CESIUM; DESIPRAMINE; ENHANCED GREEN FLUORESCENT PROTEIN; INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR3.1; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR3.2; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR4.1; UNCLASSIFIED DRUG; POTASSIUM; POTASSIUM INWARDLY RECTIFYING CHANNEL, SUBFAMILY J, MEMBER 10; POTASSIUM INWARDLY-RECTIFYING CHANNEL, SUBFAMILY J, MEMBER 10;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; GLIA CELL; IMMUNOCYTOCHEMISTRY; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NEWBORN; NONHUMAN; PATCH CLAMP; POTASSIUM CONDUCTANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SATELLITE CELL; SENSORY GANGLION; SIGNAL TRANSDUCTION; SPINAL GANGLION; TRIGEMINUS GANGLION; WHOLE CELL; ANALYSIS OF VARIANCE; ANIMAL; CHANNEL GATING; GENETICS; IMAGE PROCESSING; IMMUNOHISTOCHEMISTRY; ION TRANSPORT; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

ANALYSIS OF VARIANCE; ANIMALS; GANGLIA, SENSORY; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; ION CHANNEL GATING; ION TRANSPORT; MICE; MICE, TRANSGENIC; PATCH-CLAMP TECHNIQUES; POTASSIUM; POTASSIUM CHANNELS, INWARDLY RECTIFYING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SATELLITE CELLS, PERINEURONAL;

EID: 77951911563     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.01.005     Document Type: Article

References (36)

1. Bockenhauer D, Feather S, Stanescu HC, Bandulik S, Zdebik AA, Reichold M, Tobin J, Lieberer E, Sterner C, Landoure G, Arora R, Sirimanna T, Thompson D, Cross JH, van't Hoff W, Al Masri O, Tullus K, Yeung S, Anikster Y, Klootwijk E, Hubank M, Dillon MJ, Heitzmann D, Arcos-Burgos M, Knepper MA, Dobbie A, Gahl WA, Warth R, Sheridan E, Kleta R (2009) Epilepsy, ataxia, sensorineural deafness, tubulopathy, and KCNJ10 mutations. N Engl J Med 360:1960-1970.
2. Butt AM, 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.
3. Cherkas PS, Huang TY, Pannicke T, Tal M, Reichenbach A, Hanani M (2004) The effects of axotomy on neurons and satellite glial cells in mouse trigeminal ganglion. Pain 110:290-298.
4. Doupnik CA, Davidson N, Lester HA (1995) The inward rectifier potassium channel family. Curr Opin Neurobiol 5:268-277.
5. Dublin P, Hanani M (2007) Satellite glial cells in sensory ganglia: their possible contribution to inflammatory pain. Brain Behav Immun 21:592-598.
6. Gola M, Niel JP, Delmas P, Jacquet G (1993) Satellite glial cells in situ within mammalian prevertebral ganglia express K+ channels active at rest potential. J Membr Biol 136:75-84.
7. Hanani M (2005) Satellite glial cells in sensory ganglia: from form to function. Brain Res Brain Res Rev 48:457-476.
8. Hibino H, Fujita A, Iwai K, Yamada M, Kurachi Y (2004) Differential assembly of inwardly rectifying K+ channel subunits, Kir4.1 and Kir5.1, in brain astrocytes. J Biol Chem 279:44065-44073.
9. Hibino H, Horio Y, Fujita A, Inanobe A, Doi K, Gotow T, Uchiyama Y, Kubo T, Kurachi Y (1999) Expression of an inwardly rectifying K(+) channel, Kir4.1, in satellite cells of rat cochlear ganglia. Am J Physiol 277:C638-C644.
10. Huang TY, Cherkas PS, Rosenthal DW, Hanani M (2005) Dye coupling among satellite glial cells in mammalian dorsal root ganglia. Brain Res 1036:42-49.
11. 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 285:C260-C267.
12. Isomoto S, Kondo C, Kurachi Y (1997) Inwardly rectifying potassium channels: their molecular heterogeneity and function. Jpn J Physiol 47:11-39.
13. 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.
14. Kofuji P, Connors NC (2003) Molecular substrates of potassium spatial buffering in glial cells. Mol Neurobiol 28:195-208.
15. Kofuji P, Newman EA (2004) Potassium buffering in the central nervous system. Neuroscience 129:1045-1056.
16. Konishi T (1996) Developmental and activity-dependent changes in K+ currents in satellite glial cells in mouse superior cervical ganglion. Brain Res 708:7-15.
17. Kubo Y, Adelman JP, Clapham DE, Jan LY, Karschin A, Kurachi Y, Lazdunski M, Nichols CG, Seino S, Vandenberg CA (2005) International Union of Pharmacology. LIV. Nomenclature and molecular relationships of inwardly rectifying potassium channels. Pharmacol Rev 57:509-526.
18. Lachheb S, Cluzeaud F, Bens M, Genete M, Hibino H, Lourdel S, Kurachi Y, Vandewalle A, Teulon J, Paulais M (2008) Kir4.1/Kir5.1 channel forms the major K+ channel in the basolateral membrane of mouse renal collecting duct principal cells. Am J Physiol Renal Physiol 294:F1398-F1407.
19. Maingret F, Honore E, Lazdunski M, Patel AJ (2002) Molecular basis of the voltage-dependent gating of TREK-1, a mechano-sensitive K(+) channel. Biochem Biophys Res Commun 292:339-346.
20. Neusch C, Rozengurt N, Jacobs RE, Lester HA, Kofuji P (2001) Kir4.1 potassium channel subunit is crucial for oligodendrocyte development and in vivo myelination. J Neurosci 21:5429-5438.
21. Nichols CG, Lopatin AN (1997) Inward rectifier potassium channels. Annu Rev Physiol 59:171-191.
22. Ohara PT, Vit JP, Bhargava A, Jasmin L (2008) Evidence for a role of connexin 43 in trigeminal pain using RNA interference in vivo. J Neurophysiol 100:3064-3073.
23. Ohara PT, Vit JP, Bhargava A, Romero M, Sundberg C, Charles AC, Jasmin L (2009) Gliopathic pain: when satellite glial cells go bad. Neuroscientist 15:450-463.
24. 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.
25. Pessia M, Tucker SJ, Lee K, Bond CT, Adelman JP (1996) Subunit positional effects revealed by novel heteromeric inwardly rectifying K+ channels. EMBO J 15:2980-2987.
26. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.
27. Rojas A, Cui N, Su J, Yang L, Muhumuza JP, Jiang C (2007) Protein kinase C dependent inhibition of the heteromeric Kir4.1-Kir5.1 channel. Biochim Biophys Acta 1768:2030-2042.
28. 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 U S A 106:5842-5847.
29. Seifert G, Huttmann K, Binder DK, Hartmann C, Wyczynski A, Neusch C, Steinhauser C (2009) Analysis of astroglial K+ channel expression in the developing hippocampus reveals a predominant role of the Kir4.1 subunit. J Neurosci 29:7474-7488.
30. Su S, Ohno Y, Lossin C, Hibino H, Inanobe A, Kurachi Y (2007) Inhibition of astroglial inwardly rectifying Kir4.1 channels by a tricyclic antidepressant, nortriptyline. J Pharmacol Exp Ther 320: 573-580.
31. Tanemoto M, Kittaka N, Inanobe A, Kurachi Y (2000) In vivo formation of a proton-sensitive K+ channel by heteromeric subunit assembly of Kir5.1 with Kir4.1. J Physiol 525:587-592.
32. Tang X, Taniguchi K, Kofuji P (2009) Heterogeneity of Kir4.1 channel expression in glia revealed by mouse transgenesis. Glia 57:1706- 1715.
33. Vit JP, Ohara PT, Bhargava A, Kelley K, Jasmin L (2008) Silencing the Kir4.1 potassium channel subunit in satellite glial cells of the rat trigeminal ganglion results in pain-like behavior in the absence of nerve injury. J Neurosci 28:4161-4171.
34. Zhang H, Mei X, Zhang P, Ma C, White FA, Donnelly DF, Lamotte RH (2009) Altered functional properties of satellite glial cells in compressed spinal ganglia. Glia 57:1588-1599.
35. 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.
36. Zhou M, Xu G, Xie M, Zhang X, Schools GP, Ma L, Kimelberg HK, 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.