Involvement of Kv1 potassium channels in spreading acidification and depression in the cerebellar cortex

Journal of Neurophysiology

Volumn 94, Issue 2, 2005, Pages 1287-1298

  Chen, Gang ^a   Gao, Wangcai ^a   Reinert, Kenneth C ^a   Popa, Laurentiu S ^a   Hendrix, Claudia M ^a   Ross, M Elizabeth ^b   Ebner, Timothy J ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETAZOLAMIDE; CARBAMAZEPINE; CYCLIN D2; DENDROTOXIN; DENDROTOXIN K; FLAVOPROTEIN; GLUTAMIC ACID; NEUTRAL RED; POTASSIUM CHANNEL; POTASSIUM CHANNEL BLOCKING AGENT; POTASSIUM CHANNEL KV1.1; POTASSIUM CHANNEL KV1.2; TITYUS TOXIN; UNCLASSIFIED DRUG;

ACIDIFICATION; ANIMAL EXPERIMENT; ARTICLE; ATAXIA; AUTOFLUORESCENCE; CONTROLLED STUDY; EPISODIC ATAXIA TYPE 1; EVOKED RESPONSE; GABAERGIC TRANSMISSION; IN VIVO STUDY; KNOCKOUT MOUSE; MICROINJECTION; MOUSE; NERVE CELL EXCITABILITY; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; SPREADING CEREBRAL CORTEX ACIDIFICATION AND DEPRESSION; SPREADING CORTICAL DEPRESSION; STELLATE CELL; WILD TYPE;

ACETAZOLAMIDE; ACIDS; ANIMALS; ANTICONVULSANTS; BACLOFEN; BICUCULLINE; CARBAMAZEPINE; CEREBRAL CORTEX; CYCLINS; DIAGNOSTIC IMAGING; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; DRUG INTERACTIONS; ELECTRIC STIMULATION; FEMALE; GABA ANTAGONISTS; GLUTAMIC ACID; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUTRAL RED; PEPTIDES; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS; REACTION TIME; SCORPION VENOMS; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS; SPREADING CORTICAL DEPRESSION; TIME FACTORS;

EID: 23044453632     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00224.2005     Document Type: Article

References (75)

1. Adelman JP, Bond CT, Pessia M, and Maylie J. Episodic ataxia results from voltage-dependent potassium channels with altered functions. Neuron 15: 1449-1454, 1995.
2. + channelopathies. J Biol Chem 277: 16376-16382, 2002.
3. Anderson TR and Andrew RD. Spreading depression: imaging and blockade in the rat neocortical brain slice. J Neurophysiol 88: 2713-2725, 2002.
4. Barbour B and Hausser M. Intersynaptic diffusion of neurotransmitter. Trends Neurosci 20: 377-384, 1997.
5. Boland LM, Price DL, and Jackson KA. Episodic ataxia/myokymia mutations functionally expressed in the Shaker potassium channel. Neuroscience 91: 1557-1564, 1999.
6. Bower JM. Is the cerebellum sensory for motor's sake, or motor for sensory's sake: the view from the whiskers of a rat? Prog Brain Res 114: 483-516, 1997.
7. Brandt T and Strupp M. Episodic ataxia type 1 and 2 (familial periodic ataxia/vertigo). Audiol Neurootol 2: 373-383, 1997.
8. Bretschneider F, Wrisch A, Lehmann-Horn F, and Grissmer S. Expression in mammalian cells and electrophysiological characterization of two mutant Kv1.1 channels causing episodic ataxia type 1 (EA-1). Eur J Neurosci 11: 2403-2412, 1999.
9. Browne DL, Brunt ER, Griggs RC, Nutt JG, Gancher ST, Smith EA, and Litt M. Identification of two new KCNA1 mutations in episodic ataxia/ myokymia families. Hum Mol Genet 4: 1671-1672, 1995.
10. Browne DL, Gancher ST, Nutt JG, Brunt ER, Smith EA, Kramer P, and Litt M. Episodic ataxia/myokymia syndrome is associated with point mutations in the human potassium channel gene, KCNA1. Nat Genet 8: 136-140, 1994.
11. Brunt ER and van Weerden TW. Familial paroxysmal kinesigenic ataxia and continuous myokymia. Brain 113:1361-1382, 1990.
12. Chen G, Dunbar RL, Gao W, and Ebner TJ. Role of calcium, glutamate neurotransmission, and nitric oxide in spreading acidification and depression in the cerebellar cortex. J Neurosci 21: 9877-9887, 2001.
13. Chen G, Hanson CL, Dunbar RL, and Ebner TJ. Novel form of spreading acidification and depression in the cerebellar cortex demonstrated by neutral red optical imaging. J Neurophysiol 81: 1992-1998, 1999.
14. Chen G, Hanson CL, and Ebner TJ. Functional parasagittal compartments in the rat cerebellar cortex: An in vivo optical imaging study using neutral red. J Neurophysiol 76: 4169-4174, 1996.
15. Chen G, Hanson CL, and Ebner TJ. Optical responses evoked by cerebellar surface stimulation in vivo using neutral red. Neuroscience 84: 645-668, 1998.
16. Chen JCT and Chesler M. Extracellular alkaline shifts in rat hippocampal slice are mediated by NMDA and non-NMDA receptors. J Neurophysiol 68: 342-344, 1992.
17. Chesler M. Regulation and modulation of pH in the brain. Physiol Rev 83: 1183-1221, 2003.
18. Chesler M and Kaila K. Modulation of pH by neuronal activity. Trends Neurosci 15: 396-402, 1992.
19. Chung YH, Shin C, Kim MJ, Lee BK, and Cha CI. Immunohistochemical study on the distribution of six members of the Kv1 channel subunits in the rat cerebellum. Brain Res 895: 173-177, 2001.
20. Cohen LB, Salzberg BM, Davila HV, Ross WN, Landowne D, Waggoner AS, and Wang CH. Changes in axon fluorescence during activity: molecular probes of membrane potential. J Membr Biol 19: 1-36, 1974.
21. Dodson PD, Barker MC, and Forsythe ID. Two heteromeric Kv1 potassium channels differentially regulate action potential firing. J Neurosci 22: 6953-6961, 2002.
22. 2+-dependent changes in the mitochondrial energetics in single dissociated mouse sensory neurons. Biochem J 283: 41-50, 1992.
23. Dunbar RL, Chen G, Gao W, Reinert KC, Feddersen R, and Ebner TJ. Imaging parallel fiber and climbing fiber responses and their short-term interactions in the mouse cerebellar cortex in vivo. Neuroscience 126: 213-227, 2004.
24. Ebner TJ and Chen G. Spreading acidification and depression in the cerebellar cortex. Neuroscientist 9: 37-45, 2003.
25. Ebner TJ, Chen G, Gao W, and Reinert K. Optical imaging of cerebellar functional architectures: parallel fiber beams, parasagittal bands and spreading acidification. Prog Brain Res 148: 125-138, 2004.
26. Eccles JC, Ito M, and Szentagothai J. The Cerebellum as a Neuronal Machine. Berlin: Springer-Verlag, 1967.
27. + channel from squid (sqKv1A). Biochemistry 40: 5942-5953, 2001.
28. Eunson LH, Rea R, Zuberi SM, Youroukos S, Panayiotopoulos CP, Liguori R, Avoni P, McWilliam RC, Stephenson JB, Hanna MG, Kullmann DM, and Spauschus A. Clinical, genetic, and expression studies of mutations in the potassium channel gene KCNA1 reveal new phenotypic variability. Ann Neurol 48: 647-656, 2000.
29. Gao W, Dunbar RL, Chen G, Reinert KC, Oberdick J, and Ebner TJ. Optical imaging of long-term depression in the mouse cerebellar cortex in vivo. J Neurosci 23: 1859-1866, 2003.
30. Glazebrook PA, Ramirez AN, Schild JH, Shieh CC, Doan T, Wible BA, and Kunze DL. Potassium channels Kv1.1, Kv1.2 and Kv1.6 influence excitability of rat visceral sensory neurons. Journal of Physiology-London 541: 467-482, 2002.
31. Herson PS, Virk M, Rustay NR, Bond CT, Crabbe JC, Adelman JP, and Maylie J. A mouse model of episodic ataxia type-1. Nat Neurosci 6: 378-383, 2003.
32. Hille B. Ionic Channels of Excitable Membranes. Sunderland, MA: Sinauer, 1992.
33. Hopkins WF. Toxin and subunit specificity of blocking affinity of three peptide toxins for heteromultimeric, voltage-gated potassium channels expressed in Xenopus oocytes. J Pharmacol Exp Ther 285: 1051-1060, 1998.
34. Huard JM, Forster CC, Carter ML, Sicinski P, and Ross ME. Cerebellar histogenesis is disturbed in mice lacking cyclin D2. Development 126: 1927-1935, 1999.
35. Kado RT. Neutral red: a specific fluorescent dye in the cerebellum. Jpn J Physiol 43: s161-s169, 1993.
36. + channels. Basis for high-affinity toxin interactions and pharmacology. J Biol Chem 272: 27577-27581, 1997.
37. Kraig RP, Ferreira-Filho CR, and Nicholson C. Alkaline and acid transients in cerebellar microenvironment. J Neurophysiol 49: 831-850, 1983.
38. Kullmann DM, Rea R, Spauschus A, and Jouvenceau A. The inherited episodic ataxias: how well do we understand the disease mechanisms? Neuroscientist 7: 80-88, 2001.
39. + currents: quantitative distinction from phenytoin and possible therapeutic implications. Mol Pharmacol 51: 1077-1083, 1997.
40. LaManna JC and McCracken KA. The use of neutral red as intracellular pH indicator in rat brain cortex in vivo. Anal Biochem 142: 117-125, 1984.
41. Leao AAP. Spreading depression of activity in the cerebral cortex. J Neurophysiol 7: 359-390, 1944.
42. Levenes C, Daniel H, and Crepel F. Retrograde modulation of transmitter release by postsynaptic subtype 1 metabotropic glutamate receptors in the rat cerebellum. J Physiol 537: 125-140, 2001.
43. Llinas R and Nicholson C. Reversal properties of climbing fiber potential in cat Purkinje cells: an example of a distributed synapse. J Neurophysiol 39: 1976.
44. Llinas R and Sugimori M. Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol 305: 197-213, 1980.
45. Loewenstein Y, Mahon S, Chadderton P, Kitamura K, Sompolinsky H, Yarom Y, and Hausser M. Bistability of cerebellar Purkinje cells modulated by sensory stimulation. Nat Neurosci 8: 202-211, 2005.
46. Lubbers WJ, Brunt ER, Scheffer H, Litt M, Stulp R, Browne DL, and van Weerden TW. Hereditary myokymia and paroxysmal ataxia linked to chromosome 12 is responsive to acetazolamide. J Neurol Neurosurg Psychir 59: 400-405, 1995.
47. Mayevsky A and Chance B. Repetitive patterns of metabolic changes during cortical spreading depression of the awake rat. Brain Res 65: 529-533, 1974.
48. + channels control Purkinje cell output to facilitate postsynaptic rebound discharge in deep cerebellar neurons. J Neurosci 25: 1481-1492, 2005.
49. Momose-Sato Y, Sato K, Mochida H, Yazawa I, Sasaki S, and Kamino K. Spreading depolarization waves triggered by vagal stimulation in the embryonic chick brain: optical evidence for intercellular communication in the developing central nervous system. Neuroscience 102: 245-262, 2001.
50. Newman EA and Zahs KR. Calcium waves in retinal glial cells. Science 275: 844-847, 1997.
51. Nicholson C and Kraig RP. Chloride and potassium changes measured during spreading depression in catfish cerebellum. Brain Res 96: 384-389, 1975.
52. Popa LS, Chen G, Gao W, and Ebner TJ. Activation of parallel fibers by extra-synaptic glutamate spillover mediates propagation of spreading acidification and depression. Soc Neurosci Abstr 30: 535.6, 2004.
53. Reinert KC, Dunbar RL, Gao W, Chen G, and Ebner TJ. Flavoprotein autofluorescence imaging of neuronal activation in the cerebellar cortex in vivo. J Neurophysiol 92: 199-211, 2004.
54. Robertson B, Owen D, Stow J, Butler C, and Newland C. Novel effects of dendrotoxin homologues on subtypes of mammalian Kv1 potassium channels expressed in Xenopus oocytes. FEBS Lett 383: 26-30, 1996.
55. Scheffer H, Brunt ER, Mol GJ, van d V, Stulp RP, Verlind E, Mantel G, Averyanov YN, Hofstra RM, and Buys CH. Three novel KCNA1 mutations in episodic ataxia type I families. Hum Genet 102: 464-466, 1998.
56. Schmolesky MT, Weber JT, De Zeeuw CI, and Hansel C. The making of a complex spike: ionic composition and plasticity. Ann NY Acad Sci 978: 359-390, 2002.
57. Sharon D and Grinvald A. Dynamics and constancy in cortical spatiotemporal patterns of orientation processing. Science 295: 512-515, 2002.
58. Shimizu K, Bari F, and Busija DW. Glibenclamide enhances cortical spreading depression-associated hyperemia in the rat. Neuroreport 11: 2103-2106, 2000.
59. Shoham D, Glaser DE, Arieli A, Kenet T, Wijnbergen C, Toledo Y, Hildesheim R, and Grinvald A. Imaging cortical dynamics at high spatial and temporal resolution with novel blue voltage-sensitive dyes. Neuron 24: 791-802, 1999.
60. Smart SL, Lopantsev V, Zhang CL, Robbins CA, Wang H, Chiu SY, Schwartzkroin PA, Messing A, and Tempel BL. Deletion of the Kv1.1 potassium channel causes epilepsy in mice. Neuron 20: 809-819, 1998.
61. Soderpalm B. Anticonvulsants: aspects of their mechanisms of action. Eur J Pain 6: 3-9, 2002.
62. Somjen GG. Mechanisms of spreading depression and hypoxic spreading depression- like depolarization. Physiol Rev 81: 1065-1096, 2001.
63. Southan AP and Owen DG. The contrasting effects of dendrotoxins and other potassium channel blockers in the CA1 and dentate gyrus regions of rat hippocampal slices. Br J Pharmacol 122: 335-343, 1997.
64. + channel blockers. Br J Pharmacol 125: 1375-1381, 1998.
65. + currents in cerebellar basket and purkinje cells: Kv1 and Kv3 channel subfamilies are present in basket cell nerve terminals. J Neurosci 20: 114-122, 2000.
66. 2+ concentration rises in rat cerebellar basket cell axons. J Physiol 520: 65-78, 1999.
67. 2+ currents in isolated rat CA1 neurons. J Physiol 493: 719-732, 1996.
68. + sensitivity of excitatory amino acid receptor channels in rat cerebellar granule neurons. J Physiol 433: 727-763, 1991.
69. Veh RW, Lichtinghagen R, Sewing S, Wunder F, Grumbach IM, and Pongs O. Immunohistochemical localization of five members of the Kv1 channel subunits: contrasting subcellular locations and neuron-specific co- localizations in rat brain. Eur J Neurosci 7: 2189-2205, 1995.
70. Vyskocil F, Kritz N, and Bures J. Potassium-selective microelectrodes used for measuring the extracellular brain potassium during spreading depression and anoxic depolarization in rats. Brain Res 39: 255-259, 1972.
71. + channels containing Kv1.1 and 1.2 alpha subunits. Eur J Biochem 263: 222-229, 1999.
72. Wang H, Kunkel DD, Schwartzkroin PA, and Tempel BL. Localization of Kv1.1 and Kv1.2, two K channel proteins, to synaptic terminals, somata, and dendrites in the mouse brain. J Neurosci 14: 4588-4599, 1994.
73. Zhang CL, Messing A, and Chiu SY. Specific alteration of spontaneous GABAergic inhibition in cerebellar purkinje cells in mice lacking the potassium channel Kv1.1. J Neurosci 19: 2852-2864, 1999.
74. Zhao HM, Wenthold RJ, Wang YX, and Petralia RS. Delta-glutamate receptors are differentially distributed at parallel and climbing fiber synapses on Purkinje cells. J Neurochem 68: 1041-1052, 1997.
75. Zhou L, Zhang CL, Messing A, and Chiu SY. Temperature-sensitive neuromuscular transmission in Kv1.1 null mice: role of potassium channels under the myelin sheath in young nerves. J Neurosci 18: 7200-7215, 1998.