Distribution of M-channel subunits KCNQ2 and KCNQ3 in rat hippocampus

NeuroImage

Volumn 58, Issue 3, 2011, Pages 761-769

  Klinger, Felicia ^a,b   Gould, Georgianna ^a   Boehm, Stefan ^b   Shapiro, Mark S ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Confocal microscopy; Hippocampus; Immunostaining; M channel; Neurophysiology

Indexed keywords

POTASSIUM CHANNEL KCNQ2; POTASSIUM CHANNEL KCNQ3; SYNAPTOPHYSIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN REGION; BRAIN SLICE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EXPERIMENTAL DESIGN; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LATERAL BRAIN VENTRICLE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT;

ANIMALS; BRAIN CHEMISTRY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; KCNQ2 POTASSIUM CHANNEL; KCNQ3 POTASSIUM CHANNEL; MICROSCOPY, CONFOCAL; PROTEIN SUBUNITS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 80052150384     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.07.003     Document Type: Article

References (56)

1. Amaral D.G., Witter M.P. Hippocampal Formation. The Rat Nervous System 1995, 443-493.
2. Biervert C., Schroeder B.C., Kubisch C., Berkovic S.F., Propping P., Jentsch T.J., Steinlein O.K. A potassium channel mutation in neonatal human epilepsy. Science 1998, 279:403-406.
3. Boscia F., Annunziato L., Taglialatela M. Retigabine and flupirtine exert neuroprotective actions in organotypic hippocampal cultures. Neuropharmacology 2006, 51:283-294.
4. Brown B.S., Yu S.P. Modulation and genetic identification of the M channel. Prog. Biophys. Mol. Biol. 2000, 73:135-166.
5. Brown D.A., Adams P.R. Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature 1980, 283:673-676.
6. Constanti A., Brown D.A. M-Currents in voltage-clamped mammalian sympathetic neurones. Neurosci. Lett. 1981, 24:289-294.
7. Cooper E.C., Aldape K.D., Abosch A., Barbaro N.M., Berger M.S., Peacock W.S., Jan Y.N., Jan L.Y. Colocalization and coassembly of two human brain M-type potassium channel subunits that are mutated in epilepsy. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:4914-4919.
8. Cooper E.C., Harrington E., Jan Y.N., Jan L.Y. M channel KCNQ2 subunits are localized to key sites for control of neuronal network oscillations and synchronization in mouse brain. J. Neurosci. 2001, 21:9529-9540.
9. Coucke P.J., Hauwe P.V., Kelley P.M., Kunst H., Schatteman I., Velzen D.V., Meyers J., Ensink R.J., Verstreken M., Declau F., Marres H., Kastury K., Bhasin S., McGuirt W.T., Smith R.J., Cremers C.W., Heyning P.V., Willems P.J., Smith S.D., Camp G.V. Mutations in the KCNQ4 gene are responsible for autosomal dominant deafness in four DFNA2 families. Hum. Mol. Genet. 1999, 8:1321-1328.
10. Delmas P., Brown D.A. Pathways modulating neural KCNQ/M (Kv7) potassium channels. Nat. Rev. Neurosci. 2005, 6:850-862.
11. Devaux J.J., Kleopa K.A., Cooper E.C., Scherer S.S. KCNQ2 is a nodal K+ channel. J. Neurosci. 2004, 24:1236-1244.
12. Gage F.H. Mammalian neural stem cells. Science 2000, 287:1433-1438.
13. Gamper N., Zaika O., Li Y., Martin P., Hernandez C.C., Perez M.R., Wang A.Y., Jaffe D.B., Shapiro M.S. Oxidative modification of M-type K+ channels as a mechanism of cytoprotective neuronal silencing. EMBO J. 2006, 25:4996-5004.
14. Graumann W., Sasse D. Zentrales Nervensystem. Compact Lehrbuch Anatomie 2005, 202-384. Schattauer, stuttgart.
15. Greenwood I.A., Ohya S. New tricks for old dogs: KCNQ expression and role in smooth muscle. Br. J. Pharmacol. 2009, 156:1196-1203.
16. Gu N., Vervaeke K., Hu H., Storm J.F. Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells. J. Physiol. 2005, 566:689-715.
17. Hernandez C.C., Zaika O., Tolstykh G.P., Shapiro M.S. Regulation of neural KCNQ channels: signalling pathways, structural motifs and functional implications. J. Physiol. 2008, 586:1811-1821.
18. Huang H., Trussell L.O. KCNQ5 channels control resting properties and release probability of a synapse. Nat. Neurosci. 2011, 14:840-847.
19. Jentsch T.J. Neuronal KCNQ potassium channels: physiology and role in disease. Nat. Rev. Neurosci. 2000, 1:21-30.
20. Jin Z., Liang G.H., Cooper E.C., Jarlebark L. Expression and localization of K+ channels KCNQ2 and KCNQ3 in the mammalian cochlea. Audiol. Neurootol. 2009, 14:98-105.
21. Kharkovets T., Hardelin J.P., Safieddine S., Schweizer M., El-Amraoui A., Petit C., Jentsch T.J. KCNQ4, a K+ channel mutated in a form of dominant deafness, is expressed in the inner ear and the central auditory pathway. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:4333-4338.
22. Kristufek D., Koth G., Motejlek A., Schwarz K., Huck S., Boehm S. Modulation of spontaneous and stimulation-evoked transmitter release from rat sympathetic neurons by the cognition enhancer linopirdine: insights into its mechanisms of action. J. Neurochem. 1999, 72:2083-2091.
23. Kubisch C., Schroeder B.C., Friedrich T., Lutjohann B., El-Amraoui A., Marlin S., Petit C., Jentsch T.J. KCNQ4, a novel potassium channel expressed in sensory outer hair cells, is mutated in dominant deafness. Cell 1999, 96:437-446.
24. Lawrence J.J., Saraga F., Churchill J.F., Statland J.M., Travis K.E., Skinner F.K., McBain C.J. Somatodendritic Kv7/KCNQ/M channels control interspike interval in hippocampal interneurons. J. Neurosci. 2006, 26:12325-12338.
25. Lechner S.G., Mayer M., Boehm S. Activation of M1 muscarinic receptors triggers transmitter release from rat sympathetic neurons through an inhibition of M-type K+ channels. J. Physiol. 2003, 553:789-802.
26. Lerche C., Scherer C.R., Seebohm G., Derst C., Wei A.D., Busch A.E., Steinmeyer K. Molecular cloning and functional expression of KCNQ5, a potassium channel subunit that may contribute to neuronal M-current diversity. J. Biol. Chem. 2000, 275:22395-22400.
27. Lv P., Wei D., Yamoah E.N. Kv7-type channel currents in spiral ganglion neurons: involvement in sensorineural hearing loss. J. Biol. Chem. 2010, 285:34699-34707.
28. Mackie A.R., Brueggemann L.I., Henderson K.K., Shiels A.J., Cribbs L.L., Scrogin K.E., Byron K.L. Vascular KCNQ potassium channels as novel targets for the control of mesenteric artery constriction by vasopressin, based on studies in single cells, pressurized arteries, and in vivo measurements of mesenteric vascular resistance. J. Pharmacol. Exp. Ther. 2008, 325:475-483.
29. Martire M., Castaldo P., D'Amico M., Preziosi P., Annunziato L., Taglialatela M. M channels containing KCNQ2 subunits modulate norepinephrine, aspartate, and GABA release from hippocampal nerve terminals. J. Neurosci. 2004, 24:592-597.
30. Martire M., D'Amico M., Panza E., Miceli F., Viggiano D., Lavergata F., Iannotti F.A., Barrese V., Preziosi P., Annunziato L., Taglialatela M. Involvement of KCNQ2 subunits in [3H]dopamine release triggered by depolarization and pre-synaptic muscarinic receptor activation from rat striatal synaptosomes. J. Neurochem. 2007, 102:179-193.
31. Otto J.F., Kimball M.M., Wilcox K.S. Effects of the anticonvulsant retigabine on cultured cortical neurons: changes in electroresponsive properties and synaptic transmission. Mol. Pharmacol. 2002, 61:921-927.
32. Pan Z., Kao T., Horvath Z., Lemos J., Sul J.Y., Cranstoun S.D., Bennett V., Scherer S.S., Cooper E.C. A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J. Neurosci. 2006, 26:2599-2613.
33. Peretz A., Sheinin A., Yue C., Degani-Katzav N., Gibor G., Nachman R., Gopin A., Tam E., Shabat D., Yaari Y., Attali B. Pre- and postsynaptic activation of M-channels by a novel opener dampens neuronal firing and transmitter release. J. Neurophysiol. 2007, 97:283-295.
34. Rahimi S.Y., Brown J.H., Macomson S.D., Jensen M.A., Alleyne C.H. Evolution of the treatment of cerebral vasospasm. Neurosurg. Focus. 2006, 20:E4.
35. Rasband M.N. The axon initial segment and the maintenance of neuronal polarity. Nat. Rev. Neurosci. 2010, 11:552-562.
36. Rasmussen H.B., Frokjaer-Jensen C., Jensen C.S., Jensen H.S., Jorgensen N.K., Misonou H., Trimmer J.S., Olesen S.P., Schmitt N. Requirement of subunit co-assembly and ankyrin-G for M-channel localization at the axon initial segment. J. Cell Sci. 2007, 120:953-963.
37. Regev N., Degani-Katzav N., Korngreen A., Etzioni A., Siloni S., Alaimo A., Chikvashvili D., Villarroel A., Attali B., Lotan I. Selective interaction of syntaxin 1A with KCNQ2: possible implications for specific modulation of presynaptic activity. PLoS One 2009, 4:e6586.
38. Robbins J. KCNQ potassium channels: physiology, pathophysiology, and pharmacology. Pharmacol. Ther. 2001, 90:1-19.
39. Roche J.P., Westenbroek R., Sorom A.J., Hille B., Mackie K., Shapiro M.S. Antibodies and a cysteine-modifying reagent show correspondence of M current in neurons to KCNQ2 and KCNQ3 K+ channels. Br. J. Pharmacol. 2002, 137:1173-1186.
40. Safiulina V.F., Zacchi P., Taglialatela M., Yaari Y., Cherubini E. Low expression of Kv7/M channels facilitates intrinsic and network bursting in the developing rat hippocampus. J. Physiol. 2008, 586:5437-5453.
41. Schroeder B.C., Hechenberger M., Weinreich F., Kubisch C., Jentsch T.J. KCNQ5, a novel potassium channel broadly expressed in brain, mediates M-type currents. J. Biol. Chem. 2000, 275:24089-24095.
42. Schroeder B.C., Kubisch C., Stein V., Jentsch T.J. Moderate loss of function of cyclic-AMP-modulated KCNQ2/KCNQ3 K+ channels causes epilepsy. Nature 1998, 396:687-690.
43. Shah M.M., Migliore M., Valencia I., Cooper E.C., Brown D.A. Functional significance of axonal Kv7 channels in hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:7869-7874.
44. Shah M.M., Mistry M., Marsh S.J., Brown D.A., Delmas P. Molecular correlates of the M-current in cultured rat hippocampal neurons. J. Physiol. 2002, 544:29-37.
45. Singh N.A., Charlier C., Stauffer D., DuPont B.R., Leach R.J., Melis R., Ronen G.M., Bjerre I., Quattlebaum T., Murphy J.V., McHarg M.L., Gagnon D., Rosales T.O., Peiffer A., Anderson V.E., Leppert M. A novel potassium channel gene, KCNQ2, is mutated in an inherited epilepsy of newborns. Nat. Genet. 1998, 18:25-29.
46. Somogyi P., Klausberger T. Defined types of cortical interneurone structure space and spike timing in the hippocampus. J. Physiol. 2005, 562:9-26.
47. Stankovic K., Rio C., Xia A., Sugawara M., Adams J.C., Liberman M.C., Corfas G. Survival of adult spiral ganglion neurons requires erbB receptor signaling in the inner ear. J. Neurosci. 2004, 24:8651-8661.
48. Suarez J.I. Treatment of ruptured cerebral aneurysms and vasospasm after subarachnoid hemorrhage. Neurosurg. Clin. N. Am. 2006, 17(Suppl. 1):57-69.
49. Wang H.S., Pan Z., Shi W., Brown B.S., Wymore R.S., Cohen I.S., Dixon J.E., McKinnon D. KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science 1998, 282:1890-1893.
50. Wei D., Levic S., Nie L., Gao W.Q., Petit C., Jones E.G., Yamoah E.N. Cells of adult brain germinal zone have properties akin to hair cells and can be used to replace inner ear sensory cells after damage. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:21000-21005.
51. Wickenden A.D., Zou A., Wagoner P.K., Jegla T. Characterization of KCNQ5/Q3 potassium channels expressed in mammalian cells. Br. J. Pharmacol. 2001, 132:381-384.
52. Yeung S.Y., Pucovsky V., Moffatt J.D., Saldanha L., Schwake M., Ohya S., Greenwood I.A. Molecular expression and pharmacological identification of a role for Kv7 channels in murine vascular reactivity. Br. J. Pharmacol. 2007, 151:758-770.
53. Yue C., Yaari Y. KCNQ/M channels control spike afterdepolarization and burst generation in hippocampal neurons. J. Neurosci. 2004, 24:4614-4624.
54. Zaika O., Lara L.S., Gamper N., Hilgemann D.W., Jaffe D.B., Shapiro M.S. Angiotensin II regulates neuronal excitability via phosphatidylinositol 4,5-bisphosphate-dependent modulation of Kv7 (M-type) K+ channels. J. Physiol. 2006, 575:49-67.
55. Zaika O., Zhang J., Shapiro M.S. Functional role of M-type (KCNQ) K+ channels in adrenergic control of cardiomyocyte contraction rate by sympathetic neurons. J. Physiol. 2011, 589:2559-2568.
56. Zecevic N. Specific characteristic of radial glia in the human fetal telencephalon. Glia 2004, 48:27-35.