Expression of Kir4.1 and Kir5.1 inwardly rectifying potassium channels in oligodendrocytes, the myelinating cells of the CNS

Brain Structure and Function

Volumn 222, Issue 1, 2017, Pages 41-59

  Brasko, C ^a   Hawkins, V ^a   De La Rocha, I Chacon ^a   Butt, A M ^a  

^a UNIVERSITY OF PORTSMOUTH   (United Kingdom)

Author keywords

Astrocyte; Glia; Inward rectifying potassium channel; Oligodendrocyte; Potassium regulation; White matter

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR4.1; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR5.1; POSTSYNAPTIC DENSITY PROTEIN 95; POTASSIUM; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; KCNJ10 (CHANNEL); KIR5.1 CHANNEL;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AXON; CELL MEMBRANE; CONTROLLED STUDY; GENE INACTIVATION; GLIA; IMMUNOLOCALIZATION; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; OLIGODENDROGLIA; OPTIC NERVE; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; WESTERN BLOTTING; WHITE MATTER; ANIMAL; BRAIN; C57BL MOUSE; CEREBELLUM; GENETICS; KNOCKOUT MOUSE; METABOLISM; MYELIN SHEATH;

ANIMALS; ASTROCYTES; BRAIN; CEREBELLUM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELIN SHEATH; OLIGODENDROGLIA; OPTIC NERVE; POTASSIUM CHANNELS, INWARDLY RECTIFYING; WHITE MATTER;

EID: 84958236151     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-016-1199-8     Document Type: Article

References (71)

1. Azim K, Rivera A, Raineteau O, Butt AM (2014) GSK3beta regulates oligodendrogenesis in the dorsal microdomain of the subventricular zone via Wnt-beta-catenin signaling. Glia 62:778–779
2. Barlow AL, Macleod A, Noppen S, Sanderson J, Guerin CJ (2010) Colocalization analysis in fluorescence micrographs: verification of a more accurate calculation of Pearson’s correlation coefficient. Microsc Microanal 16:710–724
3. Bay V, Butt AM (2013) Relationship between glial potassium regulation and axon excitability: a role for glial Kir4.1 channels. Glia 60:651–660
4. Bhat RV, Axt KJ, Fosnaugh JS, Smith KJ, Johnson KA, Hill DE, Kinzler KW, Baraban JM (1996) Expression of the APC tumor suppressor protein in oligodendroglia. Glia 17:169–174
5. Bolton S, Butt AM (2006) Cyclic AMP-mediated regulation of the resting membrane potential in myelin-forming oligodendrocytes in the isolated intact rat optic nerve. Exp Neurol 202:36–43
6. Bolton S, Greenwood K, Hamilton N, Butt AM (2006) Regulation of the astrocyte resting membrane potential by cyclic AMP and protein kinase A. Glia 54:316–328
7. Boussouf A, Gaillard S (2000) Intracellular pH changes during oligodendrocyte differentiation in primary culture. J Neurosci Res 59:731–739
8. Brakeman JS, Gu SH, Wang XB, Dolin G, Baraban JM (1999) Neuronal localization of the adenomatous polyposis coli tumor suppressor protein. Neuroscience 91:661–672
9. Butt AM (2011) ATP: a ubiquitous gliotransmitter integrating neuron-glial networks. Semin Cell Dev Biol 22:205–213
10. 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
11. Butt AM, Pugh M, Hubbard P, James G (2004) Functions of optic nerve glia: axoglial signalling in physiology and pathology. Eye (London, England) 18:1110–1121
12. Butt AM, Fern RF, Matute C (2014) Neurotransmitter signaling in white matter. Glia 62:1762–1779
13. Cui N, Giwa LR, Xu H, Rojas A, Abdulkadir L, Jiang C (2001) Modulation of the heteromeric Kir4.1–Kir5.1 channels by P(CO(2)) at physiological levels. J Cell Physiol 189:229–236
14. Derst C, Karschin C, Wischmeyer E, Hirsch JR, Preisig-Müller R, Rajan S, Engel H, Grzeschik K, Daut J, Karschin A (2001) Genetic and functional linkage of Kir5.1 and Kir2.1 channel subunits. FEBS Lett 491:305–311
15. Djukic B, Casper KB, Philpot BD, Chin L-S, 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
16. Fancy SP, Harrington EP, Baranzini SE, Silbereis JC, Shiow LR, Yuen TJ, Huang EJ, Lomvardas S, Rowitch DH (2014) Parallel states of pathological Wnt signaling in neonatal brain injury and colon cancer. Nat Neurosci 17:506–512
17. Fomina S, Howard TD, Sleator OK, Golovanova M, O’Ryan L, Leyland ML, Grossmann JGN, Collins RF, Prince SM (2011) Self-directed assembly and clustering of the cytoplasmic domains of inwardly rectifying Kir2.1 potassium channels on association with PSD-95. Biochim Biophys Acta 1808:2374–2389
18. Fujita A, Horio Y, Higashi K, Mouri T, Hata F, Takeguchi N, Kurachi Y (2002) Specific localization of an inwardly rectifying K(+) channel, Kir4.1, at the apical membrane of rat gastric parietal cells; its possible involvement in K(+) recycling for the H(+)–K(+)-pump. J Physiol 540:85–92
19. Hamilton N, Vayro S, Kirchhoff F, Verkhratsky A, Robbins J, Gorecki DC, Butt AM (2008) Mechanisms of ATP- and glutamate-mediated calcium signaling in white matter astrocytes. Glia 56:734–749
20. Hamilton N, Vayro S, Wigley R, Butt AM (2010) Axons and astrocytes release ATP and glutamate to evoke calcium signals in NG2-glia. Glia 58:66–79
21. Hawkins V, Butt A (2013) TASK-1 channels in oligodendrocytes: a role in ischemia mediated disruption. Neurobiol Dis 55:87–94
22. 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
23. Hibino H, Inanobe A, Furutani K, Murakami S, Findlay I, Kurachi Y (2010) Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol Rev 90:291–366
24. Hirrlinger PG, Scheller A, Braun C, Quintela-Schneider M, Fuss B, Hirrlinger J, Kirchhoff F (2005) Expression of reef coral fluorescent proteins in the central nervous system of transgenic mice. Mol Cell Neurosci 30:291–303
25. Horio Y (2001) Potassium channels of glial cells: distribution and function. Jpn J Pharmacol 87:1–6
26. 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 Biol Chem 272:12885–12888
27. Howe MW, Feig SL, Osting SMK, Haberly LB (2008) Cellular and subcellular localization of Kir2.1 subunits in neurons and glia in piriform cortex with implications for K+ spatial buffering. J Comp Neurol 506:877–893
28. 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–C267
29. 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
30. Kang SJ, Cho S-H, Park K, Yi J, Yoo SJ, Shin KS (2008) Expression of Kir2.1 channels in astrocytes under pathophysiological conditions. Mol Cells 25:124–130
31. Kaufhold M-A, Krabbenhöft A, Song P, Engelhardt R, Riederer B, Fährmann M, Klöcker N, Beil W, Manns M, Hagen SJ, Seidler U (2008) Localization, trafficking, and significance for acid secretion of parietal cell Kir4.1 and KCNQ1 K+ channels. Gastroenterology 134:1058–1069
32. 3− solution. Glia 3:110–117
33. Kofuji P, Newman EA (2004) Potassium buffering in the central nervous system. Neuroscience 129:1045–1056
34. 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
35. Kofuji P, Biedermann B, Siddharthan V, Raap M, Iandiev I, Milenkovic I, Thomzig A, Veh RdW, Bringmann A, Reichenbach A (2002) Kir potassium channel subunit expression in retinal glial cells: implications for spatial potassium buffering. Glia 39:292–303
36. Konstas A-A, Korbmacher C, Tucker SJ (2003) Identification of domains that control the heteromeric assembly of Kir5.1/Kir4.0 potassium channels. Am J Physiol Cell Physiol 284:C910–C917
37. Lachheb S, Fo Cluzeaud, Bens M, Genete M, Hibino H, Sp Lourdel, 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
38. Lang J, Maeda Y, Bannerman P, Xu J, Horiuchi M, Pleasure D, Guo F (2013) Adenomatous polyposis coli regulates oligodendroglial development. J Neurosci 33:3113–3130
39. 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
40. Matute C, Torre I, Perez-Cerda F, Perez-Samartin A, Alberdi E, Etxebarria E, Arranz AM, Ravid R, Rodriguez-Antiguedad A, Sanchez-Gomez M, Domercq M (2007) P2X(7) receptor blockade prevents ATP excitotoxicity in oligodendrocytes and ameliorates experimental autoimmune encephalomyelitis. J Neurosci 27:9525–9533
41. Menichella DM, Majdan M, Awatramani R, Goodenough DA, Sirkowski E, Scherer SS, Paul DL (2006) Genetic and physiological evidence that oligodendrocyte gap junctions contribute to spatial buffering of potassium released during neuronal activity. J Neurosci 26:10984–10991
42. Mulkey DK, Wenker IC (2011) Astrocyte chemoreceptors: mechanisms of H+ sensing by astrocytes in the retrotrapezoid nucleus and their possible contribution to respiratory drive. Exp Physiol 96:400–406
43. Nehring RB, Wischmeyer E, Döring F, Veh RW, Sheng M, Karschin A (2000) Neuronal inwardly rectifying K(+) channels differentially couple to PDZ proteins of the PSD-95/SAP90 family. J Neurosci 20:156–162
44. 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
45. Neusch C, Papadopoulos N, Müller M, Maletzki I, Winter SM, Hirrlinger J, Handschuh M, Bähr M, Richter DW, Kirchhoff F, Hüsmann 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
46. Nolte C, Matyash M, Pivneva T, Schipke CG, Ohlemeyer C, Hanisch UK, Kirchhoff F, Kettenmann H (2001) GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 33:72–86
47. 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
48. Paulais M, Bloch-Faure M, Picard N, Jacques T, Ramakrishnan SK, Keck M, Sohet F, Eladari D, Houillier P, Sp Lourdel, Teulon J, Tucker SJ (2011) Renal phenotype in mice lacking the Kir5.1 (Kcnj16) K+ channel subunit contrasts with that observed in SeSAME/EAST syndrome. Proc Natl Acad Sci USA 108:10361–10366
49. Pegan S, Tan J, Huang A, Slesinger PA, Riek R, Choe S (2007) NMR studies of interactions between C-terminal tail of Kir2.1 channel and PDZ1, 2 domains of PSD95. Biochemistry 46:5315–5322
50. Pessia M, Imbrici P, D’Adamo MC, Salvatore L, Tucker SJ (2001) Differential pH sensitivity of Kir4.1 and Kir4.2 potassium channels and their modulation by heteropolymerisation with Kir5.1. J Physiol 532:359–367
51. 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
52. Ransom BR (1992) Glial modulation of neural excitability mediated by extracellular pH: a hypothesis. Prog Brain Res 94:37–46
53. Rapedius M, Paynter JJ, Fowler PW, Shang L, Sansom MSP, Tucker SJ, Baukrowitz T (2007) Control of pH and PIP2 gating in heteromeric Kir4.1/Kir5.1 channels by H-bonding at the helix-bundle crossing. Channels (Austin, Tex) 1:327–330
54. Ro HA, Carson JH (2004) pH microdomains in oligodendrocytes. J Biol Chem 279:37115–37123
55. Rojas A, Cui N, Su J, Yang L, Muhumuza J-P, Jiang C (2007) Protein kinase C dependent inhibition of the heteromeric Kir4.1–Kir5.1 channel. Biochim Biophys Acta 1768:2030–2042
56. Rojas A, Su J, Yang L, Lee M, Cui N, Zhang X, Fountain D, Jiang C (2008) Modulation of the heteromeric Kir4.1–Kir5.1 channel by multiple neurotransmitters via Galphaq-coupled receptors. J Cell Physiol 214:84–95
57. Seifert G, Hüttmann K, Binder DK, Hartmann C, Wyczynski A, Neusch C, Steinhäuser 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
58. Stolt CC, Schlierf A, Lommes P, Hillgartner S, Werner T, Kosian T, Sock E, Kessaris N, Richardson WD, Lefebvre V, Wegner M (2006) SoxD proteins influence multiple stages of oligodendrocyte development and modulate SoxE protein function. Dev Cell 11:697–709
59. 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(Pt 3):587–592
60. Tanemoto M, Fujita A, Higashi K, Kurachi Y (2002) PSD-95 mediates formation of a functional homomeric Kir5.1 channel in the brain. Neuron 34:387–397
61. Tanemoto M, Abe T, Onogawa T, Ito S (2004) PDZ binding motif-dependent localization of K+ channel on the basolateral side in distal tubules. Am J Physiol Renal Physiol 287:F1148–F1153
62. Tanemoto M, Toyohara T, Abe T, Ito S (2008) MAGI-1a functions as a scaffolding protein for the distal renal tubular basolateral K+ channels. J Biol Chem 283:12241–12247
63. Tang X, Taniguchi K, Kofuji P (2009) Heterogeneity of Kir4.1 channel expression in glia revealed by mouse transgenesis. Glia 57:1706–1715
64. 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
65. Ulbricht E, Pannicke T, Hollborn M, Raap M, Goczalik I, Iandiev I, Härtig W, Uhlmann S, Wiedemann P, Reichenbach A, Bringmann A, Francke M (2008) Proliferative gliosis causes mislocation and inactivation of inwardly rectifying K(+) (Kir) channels in rabbit retinal glial cells. Exp Eye Res 86:305–313
66. Verkhratsky A, Steinhäuser C (2000) Ion channels in glial cells. Brain Res Brain Res Rev 32:380–412
67. Wenker IC, Kréneisz O, Nishiyama A, Mulkey DK (2012) Astrocytes in the retrotrapezoid nucleus sense H+ by inhibition of a Kir4.1–Kir5.1-like current and may contribute to chemoreception by a purinergic mechanism. J Neurophysiol 104:3042–3052
68. 2-sensitive Kir channels in brainstem neurons of rats. J Membr Biol 197:179–191
69. Xu H, Cui N, Yang Z, Qu Z, Jiang C (2000) Modulation of kir4.1 and kir5.1 by hypercapnia and intracellular acidosis. J Physiol 524(Pt 3):725–735
70. Yamamoto Y, Ishikawa R, Omoe K, Yoshikawa N, Yamaguchi-Yamada M, Taniguchi K (2008) Immunohistochemical distribution of inwardly rectifying K+ channels in the medulla oblongata of the rat. J Vet Med Sci 70:265–271
71. 2 and pH. J Gen Physiol 116:33–45