Calcium- and metabolic state-dependent modulation of the voltage-dependent Kv2.1 channel regulates neuronal excitability in response to ischemia

Journal of Neuroscience

Volumn 25, Issue 48, 2005, Pages 11184-11193

  Misonou, Hiroaki ^a   Mohapatra, Durga P ^a   Menegola, Milena ^a   Trimmer, James S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Channel; Epilepsy; Hippocampus; Hypoxia; Ion channels; Neurons; Neuroprotection

Indexed keywords

CALCINEURIN; CALCIUM ACTIVATED POTASSIUM CHANNEL; ION CHANNEL; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL KV2.1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN HYPOXIA; BRAIN ISCHEMIA; BRAIN NERVE CELL; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL METABOLISM; CONTROLLED STUDY; HIPPOCAMPUS; HYPERPOLARIZATION; HYPOXEMIA; NERVE CELL EXCITABILITY; NERVE CELL LESION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT;

ANESTHESIA; ANIMALS; BIOLOGICAL TRANSPORT; BRAIN; BRAIN ISCHEMIA; CALCINEURIN; CALCIUM; CARBON DIOXIDE; CELLS, CULTURED; DELAYED RECTIFIER POTASSIUM CHANNELS; ELECTROPHYSIOLOGY; HIPPOCAMPUS; INTRACELLULAR MEMBRANES; NEURONS; NEUROPROTECTIVE AGENTS; OSMOLAR CONCENTRATION; PEPTIDES; PHOSPHORYLATION; POTASSIUM CHANNEL BLOCKERS; RATS; SEIZURES; SHAB POTASSIUM CHANNELS; SUBCELLULAR FRACTIONS; TETRAETHYLAMMONIUM; TISSUE DISTRIBUTION;

EID: 30644461158     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3370-05.2005     Document Type: Article

References (62)

1. Antonucci DE, Lim ST, Vassanelli S, Trimmer JS (2001) Dynamic localization and clustering of dendritic Kv2.1 voltage-dependent potassium channels in developing hippocampal neurons. Neuroscience 108:69-81.
2. Ballanyi K (2004) Protective role of neuronal KATP channels in brain hypoxia. J Exp Biol 207:3201-3212.
3. Bekkers JM (2000) Distribution and activation of voltage-gated potassium channels in cell-attached and outside-out patches from large layer 5 cortical pyramidal neurons of the rat. J Physiol (Lond) 525:611-620.
4. Bernstein BW, Bamburg JR (2003) Actin-ATP hydrolysis is a major energy drain for neurons. J Neurosci 23:1-6.
5. Berridge MJ (1998) Neuronal calcium signaling. Neuron 21:13-26.
6. Calabresi P, Cupini LM, Centonze D, Pisani F, Bernardi G (2003) Antiepileptic drugs as a possible neuroprotective strategy in brain ischemia. Ann Neurol 53:693-702.
7. 2+ flux. Cell 83:463-472.
8. Chi XX, Xu ZC (2000) Differential changes of potassium currents in CA1 pyramidal neurons after transient forebrain ischemia. J Neurophysiol 84:2834-2843.
9. Chi XX, Xu ZC (2001) Alterations of single potassium channel activity in CA1 pyramidal neurons after transient forebrain ischemia. Neuroscience 108:535-540.
10. Chow E, Haddad GG (1998) Differential effects of anoxia and glutamate on cultured neocortical neurons. Exp Neurol 150:52-59.
11. + channels in hippocampal CA1 pyramidal neurons. J Neurosci 19:8163-8171.
12. Cowan AI, Martin RL (1992) Ionic basis of membrane potential changes induced by anoxia in rat dorsal vagal motoneurones. J Physiol (Lond) 455:89-109.
13. Deng P, Pang ZP, Zhang Y, Xu ZC (2005) Increase of delayed rectifier potassium currents in large aspiny neurons in the neostriatum following transient forebrain ischemia. Neuroscience 131:135-146.
14. + channel, Kv2.1, is apposed to astrocytic processes and is associated with inhibitory postsynaptic membranes in hippocampal and cortical principal neurons and inhibitory interneurons. Neuroscience 84:37-48.
15. + channel subunit Kv2.1. J Physiol (Lond) 522:19-31.
16. Erdemli G, Xu YZ, Krnjevic K (1998) Potassium conductance causing hyperpolarization of CA1 hippocampal neurons during hypoxia. J Neurophysiol 80:2378-2390.
17. Griesemer D, Zawar C, Neumcke B (2002) Cell-type specific depression of neuronal excitability in rat hippocampus by activation of ATP-sensitive potassium channels. Eur Biophys J 31:467-477.
18. + current: a marker for apoptosis in differentiating neuronal progenitor cells? Eur J Neurosci 20:635-648.
19. Huang H, Gao TM, Gong L, Zhuang Z, Li X (2001) Potassium channel blocker TEA prevents CA1 hippocampal injury following transient forebrain ischemia in adult rats. Neurosci Lett 305:83-86.
20. Immke D, Wood M, Kiss L, Korn SJ (1999) Potassium-dependent changes in the conformation of the Kv2.1 potassium channel pore. J Gen Physiol 113:819-836.
21. + current in central neurons. Brain Res 614:352-356.
22. Kang J, Huguenard JR, Prince DA (2000) Voltage-gated potassium channels activated during action potentials in layer V neocortical pyramidal neurons. J Neurophysiol 83:70-80.
23. Katsuki H, Shinohara A, Fujimoto S, Kume T, Akaike A (2005) Tetraethylammonium exacerbates ischemic neuronal injury in rat cerebrocortical slice cultures. Eur J Pharmacol 508:85-91.
24. Kawasaki K, Traynelis SF, Dingledine R (1990) Different responses of CA1 and CA3 regions to hypoxia in rat hippocampal slice. J Neurophysiol 63:385-394.
25. + channels in layer 5 neocortical pyramidal neurones from young rats: subtypes and gradients. J Physiol (Lond) 525:621-639.
26. Lanni F, Wilson T (2000) Grating image systems or optical sectioning fluorescence microscopy of cells, tissues, and small organisms. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
27. Lee JM, Zipfel GJ, Choi DW (1999) The changing landscape of ischaemic brain injury mechanisms. Nature 399:A7-A14.
28. Leker RR, Neufeld MY (2003) Anti-epileptic drugs as possible neuroprotectants in cerebral ischemia. Brain Res Brain Res Rev 42:187-203.
29. Li Z, Okamoto K, Hayashi Y, Sheng M (2004) The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119:873-887.
30. + channel in hippocampal neurons. Neuron 25:385-397.
31. + currents, IK, are encoded by Kv2 α-subunits and regulate tonic firing in mammalian sympathetic neurons. J Neurosci 22:10094-10105.
32. + channels of fastspiking interneurons and pyramidal neurons of rat hippocampus. J Neurosci 18:8111-8125.
33. Misonou H, Mohapatra DP, Park EW, Leung V, Zhen D, Misonou K, Anderson AE, Trimmer JS (2004) Regulation of ion channel localization and phosphorylation by neuronal activity. Nat Neurosci 7:711-718.
34. + channel critical to dynamic control of neuronal excitability. Neurotoxicology 26:743-752.
35. Muennich EA, Fyffe RE (2003) Focal aggregation of a voltage-gated potassium channel, Kv2.1, at synaptic sites in rat spinal motoneurons. J Physiol (Lond) 554:673-685.
36. + current in rat hippocampal neurons. J Neurosci 19:1728-1735.
37. + channel alters voltage-dependent activation. Mol Pharmacol 52:821-828.
38. 2+ concentration by dexamethasone in acidotic mouse brain. Brain Res 957:271-277.
39. 2+ channel activation of ryanodine receptors. Neuron 40:53-63.
40. Pal S, Hartnett KA, Nerbonne JM, Levitan ES, Aizenman E (2003) Mediation of neuronal apoptosis by Kv2.1-encoded potassium channels. J Neurosci 23:4798-4802.
41. Paspalas CD, Goldman-Rakic PS (2004) Microdomains for dopamine volume neurotransmission in primate prefrontal cortex. J Neurosci 24:5292-5300.
42. Rhodes KJ, Carroll KI, Sung MA, Doliveira LC, Monaghan MM, Burke SL, Strassle BW, Buchwalder L, Menegola M, Cao J, An WF, Trimmer JS (2004) KChIPs and Kv4 α subunits as integral components of A-type potassium channels in mammalian brain. J Neurosci 24:7903-7915.
43. Runden-Pran E, Haug FM, Storm JF, Ottersen OP (2002) BK channel activity determines the extent of cell degeneration after oxygen and glucose deprivation: a study in organotypical hippocampal slice cultures. Neuroscience 112:277-288.
44. + channels expressed in transfected mammalian cells. J Biol Chem 269:23204-23211.
45. Surmeier DJ, Foehring R (2004) A mechanism for homeostatic plasticity. Nat Neurosci 7:691-692.
46. Swanson RA, Benington JH (1996) Astrocyte glucose metabolism under normal and pathological conditions in vitro. Dev Neurosci 18:515-521.
47. + current response during chemical ischemia in CA3 pyramidal cells. J Neurophysiol 82:2876-2882.
48. + channel polypeptide in rat brain. Proc Natl Acad Sci USA 88:10764-10768.
49. Trimmer JS, Rhodes KJ (2004) Localization of voltage-gated ion channels in mammalian brain. Annu Rev Physiol 66:477-519.
50. Varelas PN, Mirski MA (2001) Seizures in the adult intensive care unit. J Neurosurg Anesthesiol 13:163-175.
51. Wang X, Xiao AY, Ichinose T, Yu SP (2000) Effects of tetraethylammonium analogs on apoptosis and membrane currents in cultured cortical neurons. J Pharmacol Exp Ther 295:524-530.
52. Wei L, Yu SP, Gottron F, Snider BJ, Zipfel GJ, Choi DW (2003) Potassium channel blockers attenuate hypoxia- and ischemia-induced neuronal death in vitro and in vivo. Stroke 34:1281-1286.
53. Yamada K, Ji JJ, Yuan H, Miki T, Sato S, Horimoto N, Shimizu T, Seino S, InagakiN (2001) Protective role of ATP-sensitive potassium channels in hypoxia-induced generalized seizure. Science 292:1543-1546.
54. Yamamoto S, Tanaka E, Higashi H (1997) Mediation by intracellular calcium-dependent signals of hypoxic hyperpolarization in rat hippocampal CA1 neurons in vitro. J Neurophysiol 77:386-392.
55. 2+ exchanger and protein kinase C. J Cell Biol 163:511-523.
56. Yu SP, Yeh CH, Sensi SL, Gwag BJ, Canzoniero LM, Farhangrazi ZS, Ying HS, Tian M, Dugan LL, Choi DW (1997) Mediation of neuronal apoptosis by enhancement of outward potassium current. Science 278:114-117.
57. + efflux and neuronal apoptosis. Science 284:336-339.
58. + current in ceramide-induced caspase activation and apoptosis in cultured cortical neurons. J Neurochem 73:933-941.
59. Zawar C, Neumcke B (2000) Differential activation of ATP-sensitive potassium channels during energy depletion in CA1 pyramidal cells and interneurones of rat hippocampus. Pflügers Arch 439:256-262.
60. Zhang F, Yin W, Chen J (2004) Apoptosis in cerebral ischemia: executional and regulatory signaling mechanisms. Neurol Res 26:835-845.
61. 2+ release from mitochondria. J Neurosci 19:3307-3315.
62. Zou B, Li Y, Deng P, Xu ZC (2005) Alterations of potassium currents in ischemia-vulnerable and ischemia-resistant neurons in the hippocampus after ischemia. Brain Res 1033:78-89.