Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Subscribe

Logo for

Science 292 (5521): 1543-1546

Copyright © 2001 by the American Association for the Advancement of Science

Protective Role of ATP-Sensitive Potassium Channels in Hypoxia-Induced Generalized Seizure

Katsuya Yamada,1* Juan Juan Ji,1* Hongjie Yuan,1 Takashi Miki,4 Shinichi Sato,1 Naoki Horimoto,1 Tetsuo Shimizu,2 Susumu Seino,4 Nobuya Inagaki13dagger

Adenosine triphosphate (ATP)-sensitive potassium (KATP) channels are activated by various metabolic stresses, including hypoxia. The substantia nigra pars reticulata (SNr), the area with the highest expression of KATP channels in the brain, plays a pivotal role in the control of seizures. Mutant mice lacking the Kir6.2 subunit of KATP channels [knockout (KO) mice] were susceptible to generalized seizures after brief hypoxia. In normal mice, SNr neuron activity was inactivated during hypoxia by the opening of the postsynaptic KATP channels, whereas in KO mice, the activity of these neurons was enhanced. KATP channels exert a depressant effect on SNr neuronal activity during hypoxia and may be involved in the nigral protection mechanism against generalized seizures.

1 Department of Physiology and
2 Department of Psychiatry, Akita University School of Medicine, and
3 CREST of Japan Science and Technology Cooperation (JST), 1-1-1, Hondo, Akita 010-8543, Japan.
4 Department of Cellular and Molecular Medicine, Graduate School of Medicine, Chiba University, 1-8-1 Inohana Chuo-Ku, Chiba 260-8670, Japan.
*   These authors contributed equally to this work.

dagger    To whom correspondence should be addressed: E-mail: inagaki{at}med.akita-u.ac.jp


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Single KATP channel opening in response to stimulation of AMPA/kainate receptors is mediated by Na+ accumulation and submembrane ATP and ADP changes.
R. Mollajew, J. Toloe, and S. L. Mironov (2013)
J. Physiol. 591, 2593-2609
   Abstract »    Full Text »    PDF »
KATP channel openers in the trigeminovascular system.
K. Ploug, D. Amrutkar, M. Baun, R. Ramachandran, A. Iversen, T. Lund, S. Gupta, A. Hay-Schmidt, J. Olesen, and I. Jansen-Olesen (2012)
Cephalalgia 32, 55-65
   Abstract »    Full Text »    PDF »
Single KATP Channel Opening in Response to Action Potential Firing in Mouse Dentate Granule Neurons.
G. R. Tanner, A. Lutas, J. R. Martinez-Francois, and G. Yellen (2011)
J. Neurosci. 31, 8689-8696
   Abstract »    Full Text »    PDF »
ATP-Sensitive Potassium Channel-Mediated Lactate Effect on Orexin Neurons: Implications for Brain Energetics during Arousal.
M. P. Parsons and M. Hirasawa (2010)
J. Neurosci. 30, 8061-8070
   Abstract »    Full Text »    PDF »
Homeostatic Regulation of Neuronal Excitability by K+ Channels in Normal and Diseased Brains.
H. Misonou (2010)
Neuroscientist 16, 51-64
   Abstract »    PDF »
Inwardly Rectifying Potassium Channels: Their Structure, Function, and Physiological Roles.
H. Hibino, A. Inanobe, K. Furutani, S. Murakami, I. Findlay, and Y. Kurachi (2010)
Physiol Rev 90, 291-366
   Abstract »    Full Text »    PDF »
Fasting-induced suppression of LH secretion does not require activation of ATP-sensitive potassium channels.
W. Huang, M. Acosta-Martinez, T. H. Horton, and J. E. Levine (2008)
Am J Physiol Endocrinol Metab 295, E1439-E1446
   Abstract »    Full Text »    PDF »
Metabolic Environment in Substantia Nigra Reticulata Is Critical for the Expression and Control of Hypoglycemia-Induced Seizures.
L. Velisek, J. Veliskova, O. Chudomel, K.-L. Poon, K. Robeson, B. Marshall, A. Sharma, and S. L. Moshe (2008)
J. Neurosci. 28, 9349-9362
   Abstract »    Full Text »    PDF »
Dynamic Regulation of the Kv2.1 Voltage-Gated Potassium Channel during Brain Ischemia through Neuroglial Interaction.
H. Misonou, S. M. Thompson, and X. Cai (2008)
J. Neurosci. 28, 8529-8538
   Abstract »    Full Text »    PDF »
How ATP Inhibits the Open KATP Channel.
T. J. Craig, F. M. Ashcroft, and P. Proks (2008)
J. Gen. Physiol. 132, 131-144
   Abstract »    Full Text »    PDF »
Quantitative evaluation of ontogenetic change in heart rate and its autonomic regulation in newborn mice with the use of a noninvasive piezoelectric sensor.
S. Sato (2008)
Am J Physiol Heart Circ Physiol 294, H1708-H1715
   Abstract »    Full Text »    PDF »
Infantile Spasms as an Epileptic Feature of DEND Syndrome Associated With an Activating Mutation in the Potassium Adenosine Triphosphate (ATP) Channel, Kir6.2.
N. Bahi-Buisson, M. Eisermann, S. Nivot, C. Bellanne-Chantelot, O. Dulac, N. Bach, P. Plouin, C. Chiron, and P. de Lonlay (2007)
J Child Neurol 22, 1147-1150
   Abstract »    PDF »
ABCA2 Deficiency Results in Abnormal Sphingolipid Metabolism in Mouse Brain.
H. Sakai, Y. Tanaka, M. Tanaka, N. Ban, K. Yamada, Y. Matsumura, D. Watanabe, M. Sasaki, T. Kita, and N. Inagaki (2007)
J. Biol. Chem. 282, 19692-19699
   Abstract »    Full Text »    PDF »
Ketogenic Diet Metabolites Reduce Firing in Central Neurons by Opening KATP Channels.
W. Ma, J. Berg, and G. Yellen (2007)
J. Neurosci. 27, 3618-3625
   Abstract »    Full Text »    PDF »
Ionic currents underlying the response of rat dorsal vagal neurones to hypoglycaemia and chemical anoxia.
R. H. Balfour and S. Trapp (2007)
J. Physiol. 579, 691-702
   Abstract »    Full Text »    PDF »
The N-terminal transmembrane domain (TMD0) and a cytosolic linker (L0) of sulphonylurea receptor define the unique intrinsic gating of KATP channels.
K. Fang, L. Csanady, and K. W. Chan (2006)
J. Physiol. 576, 379-389
   Abstract »    Full Text »    PDF »
Dopaminergic Neurons Reduced to Silence by Oxidative Stress: An Early Step in the Death Cascade in Parkinson's Disease?.
P. P. Michel, M. Ruberg, and E. Hirsch (2006)
Sci. STKE 2006, pe19
   Abstract »    Full Text »    PDF »
Enhanced Neuronal Damage After Ischemic Insults in Mice Lacking Kir6.2-Containing ATP-Sensitive K+ Channels.
H.-S. Sun, Z.-P. Feng, T. Miki, S. Seino, and R. J. French (2006)
J Neurophysiol 95, 2590-2601
   Abstract »    Full Text »    PDF »
Identification and characterization of a novel member of the ATP-sensitive K+ channel subunit family, Kir6.3, in zebrafish.
C. Zhang, T. Miki, T. Shibasaki, M. Yokokura, A. Saraya, and S. Seino (2006)
Physiol Genomics 24, 290-297
   Abstract »    Full Text »    PDF »
Calcium- and Metabolic State-Dependent Modulation of the Voltage-Dependent Kv2.1 Channel Regulates Neuronal Excitability in Response to Ischemia.
H. Misonou, D. P. Mohapatra, M. Menegola, and J. S. Trimmer (2005)
J. Neurosci. 25, 11184-11193
   Abstract »    Full Text »    PDF »
Diabetes and Insulin Secretion: The ATP-Sensitive K+ Channel (KATP) Connection.
J. C. Koster, M. A. Permutt, and C. G. Nichols (2005)
Diabetes 54, 3065-3072
   Abstract »    Full Text »    PDF »
Activating Mutations in Kir6.2 and Neonatal Diabetes: New Clinical Syndromes, New Scientific Insights, and New Therapy.
A. T. Hattersley and F. M. Ashcroft (2005)
Diabetes 54, 2503-2513
   Abstract »    Full Text »    PDF »
Kir6.2-deficient mice are susceptible to stimulated ANP secretion: KATP channel acts as a negative feedback mechanism?.
N. Saegusa, T. Sato, T. Saito, M. Tamagawa, I. Komuro, and H. Nakaya (2005)
Cardiovasc Res 67, 60-68
   Abstract »    Full Text »    PDF »
Two SUR1-specific Histidine Residues Mandatory for Zinc-induced Activation of the Rat KATP Channel.
V. Bancila, T. Cens, D. Monnier, F. Chanson, C. Faure, Y. Dunant, and A. Bloc (2005)
J. Biol. Chem. 280, 8793-8799
   Abstract »    Full Text »    PDF »
ATP-Sensitive K+ Channel Knockout Compromises the Metabolic Benefit of Exercise Training, Resulting in Cardiac Deficits.
G. C. Kane, A. Behfar, S. Yamada, C. Perez-Terzic, F. O'Cochlain, S. Reyes, P. P. Dzeja, T. Miki, S. Seino, and A. Terzic (2004)
Diabetes 53, S169-S175
   Abstract »    Full Text »    PDF »
Roles of ATP-Sensitive K+ Channels as Metabolic Sensors: Studies of Kir6.x Null Mice.
K. Minami, T. Miki, T. Kadowaki, and S. Seino (2004)
Diabetes 53, S176-S180
   Abstract »    Full Text »    PDF »
Gene targeting approach to clarification of ion channel function: studies of Kir6.x null mice.
S. Seino and T. Miki (2004)
J. Physiol. 554, 295-300
   Abstract »    Full Text »    PDF »
ATP-dependent interaction of the cytosolic domains of the inwardly rectifying K+ channel Kir6.2 revealed by fluorescence resonance energy transfer.
T. Tsuboi, J. D. Lippiat, F. M. Ashcroft, and G. A. Rutter (2004)
PNAS 101, 76-81
   Abstract »    Full Text »    PDF »
A role for nitric oxide in hypoxia-induced activation of cardiac KATP channels in goldfish (Carassius auratus).
J. S. Cameron, K. E. Hoffmann, C. Zia, H. M. Hemmett, A. Kronsteiner, and C. M. Lee (2003)
J. Exp. Biol. 206, 4057-4065
   Abstract »    Full Text »    PDF »
N-terminal transmembrane domain of the SUR controls trafficking and gating of Kir6 channel subunits.
K. W. Chan, H. Zhang, and D. E. Logothetis (2003)
EMBO J. 22, 3833-3843
   Abstract »    Full Text »    PDF »
Identification of residues contributing to the ATP binding site of Kir6.2.
S. Trapp, S. Haider, P. Jones, M. S. P. Sansom, and F. M. Ashcroft (2003)
EMBO J. 22, 2903-2912
   Abstract »    Full Text »    PDF »
ATP-Sensitive Potassium Channels Mediate Dilatation of Basilar Artery in Response to Intracellular Acidification In Vivo.
N. Santa, T. Kitazono, T. Ago, H. Ooboshi, M. Kamouchi, M. Wakisaka, S. Ibayashi, and M. Iida (2003)
Stroke 34, 1276-1280
   Abstract »    Full Text »    PDF »
Cellular remodeling in heart failure disrupts KATP channel-dependent stress tolerance.
D. M. Hodgson, L. V. Zingman, G. C. Kane, C. Perez-Terzic, M. Bienengraeber, C. Ozcan, R. J. Gumina, D. Pucar, F. O'Coclain, D. L. Mann, et al. (2003)
EMBO J. 22, 1732-1742
   Abstract »    Full Text »    PDF »
Nateglinide, a D-Phenylalanine Derivative Lacking Either a Sulfonylurea or Benzamido Moiety, Specifically Inhibits Pancreatic beta -Cell-Type KATP Channels.
M. Chachin, M. Yamada, A. Fujita, T. Matsuoka, K. Matsushita, and Y. Kurachi (2003)
J. Pharmacol. Exp. Ther. 304, 1025-1032
   Abstract »    Full Text »    PDF »
Ischemic Preconditioning in the Hippocampus of a Knockout Mouse Lacking SUR1-Based KATP Channels.
A. Munoz, M. Nakazaki, J. C. Goodman, R. Barrios, C. G. Onetti, J. Bryan, and L. Aguilar-Bryan (2003)
Stroke 34, 164-170
   Abstract »    Full Text »    PDF »
ATP-sensitive potassium channels participate in glucose uptake in skeletal muscle and adipose tissue.
T. Miki, K. Minami, L. Zhang, M. Morita, T. Gonoi, T. Shiuchi, Y. Minokoshi, J.-M. Renaud, and S. Seino (2002)
Am J Physiol Endocrinol Metab 283, E1178-E1184
   Abstract »    Full Text »    PDF »
Sulfonylurea Stimulation of Insulin Secretion.
P. Proks, F. Reimann, N. Green, F. Gribble, and F. Ashcroft (2002)
Diabetes 51, S368-376
   Abstract »    Full Text »    PDF »
Progesterone reverses the neuronal responses to hypoxia in rat nucleus tractus solitarius in vitro.
O. Pascual, M.-P. Morin-Surun, B. Barna, M. Denavit-Saubie, J.-M. Pequignot, and J. Champagnat (2002)
J. Physiol. 544, 511-520
   Abstract »    Full Text »    PDF »
Kir6.2 is required for adaptation to stress.
L. V. Zingman, D. M. Hodgson, P. H. Bast, G. C. Kane, C. Perez-Terzic, R. J. Gumina, D. Pucar, M. Bienengraeber, P. P. Dzeja, T. Miki, et al. (2002)
PNAS 99, 13278-13283
   Abstract »    Full Text »    PDF »
Coupling of Cell Energetics with Membrane Metabolic Sensing. INTEGRATIVE SIGNALING THROUGH CREATINE KINASE PHOSPHOTRANSFER DISRUPTED BY M-CK GENE KNOCK-OUT.
M. R. Abraham, V. A. Selivanov, D. M. Hodgson, D. Pucar, L. V. Zingman, B. Wieringa, P. P. Dzeja, A. E. Alekseev, and A. Terzic (2002)
J. Biol. Chem. 277, 24427-24434
   Abstract »    Full Text »    PDF »
ATP-Sensitive K+ Channels in the Brain: Sensors of Hypoxic Conditions.
K. Yamada and N. Inagaki (2002)
Physiology 17, 127-130
   Abstract »    Full Text »    PDF »
Pre- and postsynaptic ATP-sensitive potassium channels during metabolic inhibition of rat hippocampal CA1 neurons.
N. Matsumoto, S. Komiyama, and N. Akaike (2002)
J. Physiol. 541, 511-520
   Abstract »    Full Text »    PDF »
Mitochondria: Gateway for Cytoprotection.
P. P. Dzeja, E. L. Holmuhamedov, C. Ozcan, D. Pucar, A. Jahangir, and A. Terzic (2001)
Circ. Res. 89, 744-746
   Full Text »    PDF »
The Neuroscientist Comments.
(2001)
Neuroscientist 7, 353-355
   PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882