Conditional transgenic suppression of M channels in mouse brain reveals functions in neuronal excitability, resonance and behavior

Nature Neuroscience

Volumn 8, Issue 1, 2005, Pages 51-60

  Peters, H Christian ^a   Hu, Hua ^b   Pongs, Olaf ^a   Storm, Johan F ^b   Isbrandt, Dirk ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM CHANNEL KCNQ1; PROTEIN SUBUNIT; KCNQ2 PROTEIN, MOUSE; NERVE PROTEIN; POTASSIUM CHANNEL KCNQ2; VOLTAGE GATED POTASSIUM CHANNEL;

AFTERHYPERPOLARIZATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; COGNITIVE DEFECT; CONTROLLED STUDY; EPILEPSY; GENE DELETION; GENE EXPRESSION; HIPPOCAMPUS; HYPERACTIVITY; MALE; MAZE TEST; MEMBRANE CHANNEL; MEMBRANE CURRENT; MEMORY DISORDER; MOUSE; NERVE CELL EXCITABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SPATIAL MEMORY; THETA RHYTHM; TRANSGENIC MOUSE; ANIMAL; ANIMAL BEHAVIOR; BIOPHYSICS; BRAIN; DOMINANT GENE; DRUG ANTAGONISM; ELECTROPHYSIOLOGY; FEMALE; GENETICS; HYPERKINESIA; METABOLISM; MOLECULAR GENETICS; NERVE CELL; OOCYTE; PATHOLOGY; PATHOPHYSIOLOGY; PSYCHOLOGICAL ASPECT; SWIMMING; XENOPUS LAEVIS;

ANIMALS; BEHAVIOR, ANIMAL; BIOPHYSICS; BRAIN; ELECTROPHYSIOLOGY; EPILEPSY; FEMALE; GENES, DOMINANT; HYPERKINESIS; KCNQ2 POTASSIUM CHANNEL; MALE; MAZE LEARNING; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEURONS; OOCYTES; PHENOTYPE; POTASSIUM CHANNELS, VOLTAGE-GATED; PYRAMIDAL CELLS; SWIMMING; XENOPUS LAEVIS;

EID: 16644379267     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1375     Document Type: Article

References (50)

1. Brown, D.A. & Adams, P.R. Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature 283, 673-676 (1980).
2. Brown, D.A. M-currents: an update. Trends Neurosci. 11, 294-299 (1988).
3. Halliwell, J.V. & Adams, P.R. Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res. 250, 71-92 (1982).
4. Storm, J.F. Potassium currents in hippocampal pyramidal cells. Prog. Brain Res. 83, 161-187 (1990).
5. Jentsch, T.J. Neuronal KCNQ potassium channels: physiology and role in disease. Nat. Rev. Neurosci. 1, 21-30 (2000).
6. Ryan, S.G. et al. Benign familial neonatal convulsions: evidence for clinical and genetic heterogeneity. Ann. Neurol. 29, 469-473 (1991).
7. Dedek, K., Fusco, L., Teloy, N. & Steinlein, O.K. Neonatal convulsions and epileptic encephalopathy in an Italian family with a missense mutation in the fifth transmembrane region of KCNQ2. Epilepsy Res. 54, 21-27 (2003).
8. Borgatti, R. et al. A novel mutation in KCNQ2 associated with BFNC, drug resistant epilepsy, and mental retardation. Neurology 63, 57-65 (2004).
9. Dedek, K. et al. Myokymia and neonatal epilepsy caused by a mutation in the voltage sensor of the KCNQ2 K+ channel. Proc. Natl. Acad. Sci. USA 98, 12272-12277 (2001).
10. Marrion, N.V. Control of M-current. Annu. Rev. Physiol. 59, 483-504 (1997).
11. Wang, H.S. et al. KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science 282, 1890-1893 (1998).
12. Selyanko, A.A. et al. Inhibition of KCNQ1-4 potassium channels expressed in mammalian cells via M1 muscarinic acetylcholine receptors. J. Physiol. (Lond.) 522, 349-355 (2000).
13. Hadley, J. K. et al. Stoichiometry of expressed KCNQ2/KCNQ3 potassium channels and subunit composition of native ganglionic M channels deduced from block by tetraethylammonium. J. Neurosci. 23, 5012-5019 (2003).
14. Cooper, E.C. et al. Colocalization and coassembly of two human brain M-type potassium channel subunits that are mutated in epilepsy. Proc. Natl. Acad. Sci. USA 97, 4914-4919 (2000).
15. 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. (Lond.) 544, 29-37 (2002).
16. 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. 21, 9529-9540 (2001).
17. Devaux, J.J., Kleopa, K.A., Cooper, E.C. & Scherer, S.S. KCNQ2 is a nodal K+ channel. J. Neurosci. 24, 1236-1244 (2004).
18. Storm, J.F. An after-hyperpolarization of medium duration in rat hippocampal pyramidal cells. J. Physiol. (Lond.) 409, 171-190 (1989).
19. Madison, D.V. & Nicoll, R.A. Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. J. Physiol. (Lond.) 354, 319-331 (1984).
20. Malenka, R.C., Madison, D.V., Andrade, R. & Nicoll, R.A. Phorbol esters mimic some cholinergic actions in hippocampal pyramidal neurons. J. Neurosci. 6, 475-480 (1986).
21. Watanabe, H. et al. Disruption of the epilepsy KCNQ2 gene results in neural hyperexcitability. J. Neurochem. 75, 28-33 (2000).
22. Yang, Y. et al. Spontaneous deletion of epilepsy gene orthologs in a mutant mouse with a low electroconvulsive threshold. Hum. Mol. Genet. 12, 975-984 (2003).
23. Gossen, M. & Bujard, H. Tight control of gene expression in mammalian cells by tetracycline- responsive promoters. Proc. Natl. Acad. Sci. USA 89, 5547-5551 (1992).
24. Tremblay, P. et al. Doxycycline control of prion protein transgene expression modulates prion disease in mice. Proc. Natl. Acad. Sci. USA 95, 12580-12585 (1998).
25. 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 396, 687-690 (1998).
26. Hu, H., Vervaeke, K. & Storm, J.F. Two forms of electrical resonance at theta frequencies, generated by M-current, h-current and persistent Na+ current in rat hippocampal pyramidal cells. J. Physiol. (Lond.) 545, 783-805 (2002).
27. Nitecka, L. et al. Maturation of kainic acid seizure-brain damage syndrome in the rat. II. Histopathological sequelae. Neuroscience 13, 1073-1094 (1984).
28. Mello, L.E. et al. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 34, 985-995 (1993).
29. Holmes, G.L. & Ben-Ari, Y. Seizures in the developing brain: perhaps not so benign after all. Neuron 21, 1231-1234 (1998).
30. Stocker, M., Krause, M. & Pedarzani, P. An apamin-sensitive Ca2+-activated K+ current in hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. USA 96, 4662-4667 (1999).
31. Hutcheon, B. & Yarom, Y. Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci. 23, 216-222 (2000).
32. Pike, F.G. et al. Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents. J. Physiol. (Lond.) 529, 205-213 (2000).
33. Leung, L.S. & Yu, H.W. Theta-frequency resonance in hippocampal CA1 neurons in vitro demonstrated by sinusoidal current injection. J. Neurophysiol. 79, 1592-1596 (1998).
34. Hutcheon, B., Miura, R.M. & Puil, E. Subthreshold membrane resonance in neocortical neurons. J. Neurophysiol. 76, 683-697 (1996).
35. Morris, R.G., Garrud, P., Rawlins, J.N. & O'Keefe, J. Place navigation impaired in rats with hippocampal lesions. Nature 297, 681-683 (1982).
36. Buzsaki, G. Theta oscillations in the hippocampus. Neuron 33, 325-340 (2002).
37. Sah, P. Ca(2+)-activated K+ currents in neurones: types, physiological roles and modulation. Trends Neurosci. 19, 150-154 (1996).
38. 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. 275, 24089-24095 (2000).
39. Vergara, C., Latorre, R., Marrion, N.V. & Adelman, J.P. Calcium-activated potassium channels. Curr. Opin. Neurobiol. 8, 321-329 (1998).
40. Bond, C.T. et al. Small conductance Ca2+-activated K+ channel knock-out mice reveal the identity of calcium-dependent afterhyperpolarization currents. J. Neurosci. 24, 5301-5306 (2004).
41. Williamson, A. & Alger, B.E. Characterization of an early afterhyperpolarization after a brief train of action potentials in rat hippocampal neurons in vitro. J. Neurophysiol. 63, 72-81 (1990).
42. Raghavachari, S. et al. Gating of human theta oscillations by a working memory task. J. Neurosci. 21, 3175-3183 (2001).
43. Kahana, M.J., Seelig, D. & Madsen, J.R. Theta returns. Curr. Opin. Neurobiol. 11, 739-744 (2001).
44. Sarnthein, J., Petsche, H., Rappelsberger, P., Shaw, G.L. & von Stein, A. Synchronization between prefrontal and posterior association cortex during human working memory. Proc. Natl. Acad. Sci. USA 95, 7092-7096 (1998).
45. Blümcke, I., Thom, M. & Wiestler, O.D. Ammon's horn sclerosis: a maldevelopmental disorder associated with temporal lobe epilepsy. Brain Pathol. 12, 199-211 (2002).
46. Khazipov, R. et al. Developmental changes in GABAergic actions and seizure susceptibility in the rat hippocampus. Eur. J. Neurosci. 19, 590-600 (2004).
47. Ben-Ari, Y. Excitatory actions of GABA during development: the nature of the nurture. Nat. Rev. Neurosci. 3, 728-739 (2002).
48. 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. (Lond.) 553, 789-802 (2003).
49. Martire, M. et al. M channels containing KCNQ2 subunits modulate norepinephrine, aspartate, and GABA release from hippocampal nerve terminals. J. Neurosci. 24, 592-597 (2004).
50. Noebels, J.L. The biology of epilepsy genes. Annu. Rev. Neurosci. 26, 599-625 (2003).