QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

HOME  |   SEARCH  |   ARCHIVE  |   SUBSCRIBE  |   CONTACT  |   HELP

This Article Full Text Full Text (PDF) Submit an eLetter Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (99) Citing Articles via Google Scholar Google Scholar Articles by Hu, H. Articles by Storm, J. F. Search for Related Content PubMed PubMed Citation Articles by Hu, H. Articles by Storm, J. F.

 Previous Article  |  Next Article 

The Journal of Neuroscience, December 15, 2001, 21(24):9585-9597

Presynaptic Ca²⁺-Activated K⁺ Channels in Glutamatergic Hippocampal Terminals and Their Role in Spike Repolarization and Regulation of Transmitter Release

Hua Hu¹, Li-Rong Shao¹, Sorush Chavoshy², Ning Gu¹, Maria Trieb⁴, Ralf Behrens⁵, Petter Laake³, Olaf Pongs⁵, Hans Günther Knaus⁴, Ole Petter Ottersen², and Johan F. Storm¹

Institutes of ¹ Physiology, ² Anatomy and ³ Medical Statistics, University of Oslo, Blindern, N-0317 Oslo, Norway, ⁴ Institute of Biochemical Pharmacology, A-6020 Innsbruck, Austria, and ⁵ Institut für Neurale Signalverarbeitung, Zentrum für Moleculare Neurobiologie, Universität Hamburg, D-20246 Hamburg, Germany

Large-conductance Ca²⁺-activated K⁺ channels (BK, also called Maxi-K or Slo channels) are widespread in the vertebrate nervous system, but their functional roles in synaptic transmission in the mammalian brain are largely unknown. By combining electrophysiology and immunogold cytochemistry, we demonstrate the existence of functional BK channels in presynaptic terminals in the hippocampus and compare their functional roles in somata and terminals of CA3 pyramidal cells. Double-labeling immunogold analysis with BK channel and glutamate receptor antibodies indicated that BK channels are targeted to the presynaptic membrane facing the synaptic cleft in terminals of Schaffer collaterals in stratum radiatum. Whole-cell, intracellular, and field-potential recordings from CA1 pyramidal cells showed that the presynaptic BK channels are activated by calcium influx and can contribute to repolarization of the presynaptic action potential (AP) and negative feedback control of Ca²⁺ influx and transmitter release. This was observed in the presence of 4-aminopyridine (4-AP, 40-100 µM), which broadened the presynaptic compound action potential. In contrast, the presynaptic BK channels did not contribute significantly to regulation of action potentials or transmitter release under basal experimental conditions, i.e., without 4-AP, even at high stimulation frequencies. This is unlike the situation in the parent cell bodies (CA3 pyramidal cells), where BK channels contribute strongly to action potential repolarization. These results indicate that the functional role of BK channels depends on their subcellular localization.

Key words: calcium-activated potassium channels; BK channels; Slo; Maxi-K; presynaptic mechanisms; hippocampus; CA1; CA3; action potential repolarization; glutamatergic synapses; immunogold cytochemistry; BK-4; KCNMB4

---

Copyright © 2001 Society for Neuroscience  0270-6474/01/21249585-13$05.00/0

This article has been cited by other articles:

				U. S. Lee and J. Cui {beta} subunit-specific modulations of BK channel function by a mutation associated with epilepsy and dyskinesia J. Physiol., April 1, 2009; 587(7): 1481 - 1498. [Abstract] [Full Text] [PDF]

				T.-B. Sweet and D. H. Cox Measurements of the BKCa Channel's High-Affinity Ca2+ Binding Constants: Effects of Membrane Voltage J. Gen. Physiol., November 1, 2008; 132(5): 491 - 505. [Abstract] [Full Text] [PDF]

				J. Yan, J. V. Olsen, K.-S. Park, W. Li, W. Bildl, U. Schulte, R. W. Aldrich, B. Fakler, and J. S. Trimmer Profiling the Phospho-status of the BKCa Channel {alpha} Subunit in Rat Brain Reveals Unexpected Patterns and Complexity Mol. Cell. Proteomics, November 1, 2008; 7(11): 2188 - 2198. [Abstract] [Full Text] [PDF]

				L. Liao, S. K. Park, T. Xu, P. Vanderklish, and J. R. Yates III Quantitative proteomic analysis of primary neurons reveals diverse changes in synaptic protein content in fmr1 knockout mice PNAS, October 7, 2008; 105(40): 15281 - 15286. [Abstract] [Full Text] [PDF]

				H. Berkefeld and B. Fakler Repolarizing Responses of BKCa-Cav Complexes Are Distinctly Shaped by Their Cav Subunits J. Neurosci., August 13, 2008; 28(33): 8238 - 8245. [Abstract] [Full Text] [PDF]

				W. Cerpa, J. A. Godoy, I. Alfaro, G. G. Farias, M. J. Metcalfe, R. Fuentealba, C. Bonansco, and N. C. Inestrosa Wnt-7a Modulates the Synaptic Vesicle Cycle and Synaptic Transmission in Hippocampal Neurons J. Biol. Chem., February 29, 2008; 283(9): 5918 - 5927. [Abstract] [Full Text] [PDF]

				A. Li, Q. Xi, E. S. Umstot, L. Bellner, M. L. Schwartzman, J. H. Jaggar, and C. W. Leffler Astrocyte-Derived CO Is a Diffusible Messenger That Mediates Glutamate-Induced Cerebral Arteriolar Dilation by Activating Smooth Muscle Cell KCa Channels Circ. Res., February 1, 2008; 102(2): 234 - 241. [Abstract] [Full Text] [PDF]

				P. J. Brunton, M. Sausbier, G. Wietzorrek, U. Sausbier, H.-G. Knaus, J. A. Russell, P. Ruth, and M. J. Shipston Hypothalamic-Pituitary-Adrenal Axis Hyporesponsiveness to Restraint Stress in Mice Deficient for Large-Conductance Calcium- and Voltage-Activated Potassium (BK) Channels Endocrinology, November 1, 2007; 148(11): 5496 - 5506. [Abstract] [Full Text] [PDF]

				A. Kanu and C. W. Leffler Carbon monoxide and Ca2+-activated K+ channels in cerebral arteriolar responses to glutamate and hypoxia in newborn pigs Am J Physiol Heart Circ Physiol, November 1, 2007; 293(5): H3193 - H3200. [Abstract] [Full Text] [PDF]

				N. Gu, K. Vervaeke, and J. F. Storm BK potassium channels facilitate high-frequency firing and cause early spike frequency adaptation in rat CA1 hippocampal pyramidal cells J. Physiol., May 1, 2007; 580(3): 859 - 882. [Abstract] [Full Text] [PDF]

				B. E. McKay, J. D. T. Engbers, W. H. Mehaffey, G. R. J. Gordon, M. L. Molineux, J. S. Bains, and R. W. Turner Climbing Fiber Discharge Regulates Cerebellar Functions by Controlling the Intrinsic Characteristics of Purkinje Cell Output J Neurophysiol, April 1, 2007; 97(4): 2590 - 2604. [Abstract] [Full Text] [PDF]

				J. Ster, F. De Bock, N. C. Guerineau, A. Janossy, S. Barrere-Lemaire, J. L. Bos, J. Bockaert, and L. Fagni Exchange protein activated by cAMP (Epac) mediates cAMP activation of p38 MAPK and modulation of Ca2+-dependent K+ channels in cerebellar neurons PNAS, February 13, 2007; 104(7): 2519 - 2524. [Abstract] [Full Text] [PDF]

				S. J. Pyott, A. L. Meredith, A. A. Fodor, A. E. Vazquez, E. N. Yamoah, and R. W. Aldrich Cochlear Function in Mice Lacking the BK Channel {alpha}, beta1, or beta4 Subunits J. Biol. Chem., February 2, 2007; 282(5): 3312 - 3324. [Abstract] [Full Text] [PDF]

				X. Sun, D. Zhou, P. Zhang, E. G. Moczydlowski, and G. G. Haddad beta-Subunit-Dependent Modulation of hSlo BK Current by Arachidonic Acid J Neurophysiol, January 1, 2007; 97(1): 62 - 69. [Abstract] [Full Text] [PDF]

				L. Tian, L. Chen, H. McClafferty, C. A. Sailer, P. Ruth, H.-G. Knaus, and M. J. Shipston A noncanonical SH3 domain binding motif links BK channels to the actin cytoskeleton via the SH3 adapter cortactin FASEB J, December 1, 2006; 20(14): 2588 - 2590. [Abstract] [Full Text] [PDF]

				H. Berkefeld, C. A. Sailer, W. Bildl, V. Rohde, J.-O. Thumfart, S. Eble, N. Klugbauer, E. Reisinger, J. Bischofberger, D. Oliver, et al. BKCa-Cav channel complexes mediate rapid and localized Ca2+-activated K+ signaling. Science, October 27, 2006; 314(5799): 615 - 620. [Abstract] [Full Text] [PDF]

				K. Vervaeke, N. Gu, C. Agdestein, H. Hu, and J. F. Storm Kv7/KCNQ/M-channels in rat glutamatergic hippocampal axons and their role in regulation of excitability and transmitter release J. Physiol., October 1, 2006; 576(1): 235 - 256. [Abstract] [Full Text] [PDF]

				F. Laumonnier, S. Roger, P. Guerin, F. Molinari, R. M'Rad, D. Cahard, A. Belhadj, M. Halayem, A. M. Persico, M. Elia, et al. Association of a Functional Deficit of the BKCa Channel, a Synaptic Regulator of Neuronal Excitability, With Autism and Mental Retardation Am J Psychiatry, September 1, 2006; 163(9): 1622 - 1629. [Abstract] [Full Text] [PDF]

				B. Wang, B. S. Rothberg, and R. Brenner Mechanism of {beta}4 Subunit Modulation of BK Channels J. Gen. Physiol., March 27, 2006; 127(4): 449 - 465. [Abstract] [Full Text] [PDF]

				S. Lajus, P. Vacher, D. Huber, M. Dubois, M.-N. Benassy, Y. Ushkaryov, and J. Lang {alpha}-Latrotoxin Induces Exocytosis by Inhibition of Voltage-dependent K+ Channels and by Stimulation of L-type Ca2+ Channels via Latrophilin in beta-Cells J. Biol. Chem., March 3, 2006; 281(9): 5522 - 5531. [Abstract] [Full Text] [PDF]

				L. C. Santarelli, R. Wassef, S. H. Heinemann, and T. Hoshi Three methionine residues located within the regulator of conductance for K+ (RCK) domains confer oxidative sensitivity to large-conductance Ca2+-activated K+ channels J. Physiol., March 1, 2006; 571(2): 329 - 348. [Abstract] [Full Text] [PDF]

				B. Pelucchi, G. Aguiari, A. Pignatelli, E. Manzati, R. Witzgall, L. del Senno, and O. Belluzzi Nonspecific Cation Current Associated with Native Polycystin-2 in HEK-293 Cells J. Am. Soc. Nephrol., February 1, 2006; 17(2): 388 - 397. [Abstract] [Full Text] [PDF]

				A. Limon, C. Perez, R. Vega, and E. Soto Ca2+-Activated K+-Current Density Is Correlated With Soma Size in Rat Vestibular-Afferent Neurons in Culture J Neurophysiol, December 1, 2005; 94(6): 3751 - 3761. [Abstract] [Full Text] [PDF]

				T. Giraldez, T. E. Hughes, and F. J. Sigworth Generation of Functional Fluorescent BK Channels by Random Insertion of GFP Variants J. Gen. Physiol., October 31, 2005; 126(5): 429 - 438. [Abstract] [Full Text] [PDF]

				S. I. Zakharov, J. P. Morrow, G. Liu, L. Yang, and S. O. Marx Activation of the BK (SLO1) Potassium Channel by Mallotoxin J. Biol. Chem., September 2, 2005; 280(35): 30882 - 30887. [Abstract] [Full Text] [PDF]

				J. W. Xu and M. M. Slaughter Large-Conductance Calcium-Activated Potassium Channels Facilitate Transmitter Release in Salamander Rod Synapse J. Neurosci., August 17, 2005; 25(33): 7660 - 7668. [Abstract] [Full Text] [PDF]

				M. Sausbier, C. Arntz, I. Bucurenciu, H. Zhao, X.-B. Zhou, U. Sausbier, S. Feil, S. Kamm, K. Essin, C. A. Sailer, et al. Elevated Blood Pressure Linked to Primary Hyperaldosteronism and Impaired Vasodilation in BK Channel-Deficient Mice Circulation, July 5, 2005; 112(1): 60 - 68. [Abstract] [Full Text] [PDF]

				E. M. Goldberg, S. Watanabe, S. Y. Chang, R. H. Joho, Z. J. Huang, C. S. Leonard, and B. Rudy Specific Functions of Synaptically Localized Potassium Channels in Synaptic Transmission at the Neocortical GABAergic Fast-Spiking Cell Synapse J. Neurosci., May 25, 2005; 25(21): 5230 - 5235. [Abstract] [Full Text] [PDF]

				P. K. Bahia, R. Suzuki, D. C. H. Benton, A. J. Jowett, M. X. Chen, Derek. J. Trezise, A. H. Dickenson, and G. W. J. Moss A Functional Role for Small-Conductance Calcium-Activated Potassium Channels in Sensory Pathways Including Nociceptive Processes J. Neurosci., April 6, 2005; 25(14): 3489 - 3498. [Abstract] [Full Text] [PDF]

				D. D. Kline, M. C. F. Buniel, P. Glazebrook, Y.-J. Peng, A. Ramirez-Navarro, N. R. Prabhakar, and D. L. Kunze Kv1.1 Deletion Augments the Afferent Hypoxic Chemosensory Pathway and Respiration J. Neurosci., March 30, 2005; 25(13): 3389 - 3399. [Abstract] [Full Text] [PDF]

				H.-H. Lim and C.-S. Park Identification and Functional Characterization of Ankyrin-Repeat Family Protein ANKRA as a Protein Interacting with BKCa Channel Mol. Biol. Cell, March 1, 2005; 16(3): 1013 - 1025. [Abstract] [Full Text] [PDF]

				A. F Soleng, A Baginskas, P Andersen, and M Raastad Activity-dependent excitability changes in hippocampal CA3 cell Schaffer axons J. Physiol., October 15, 2004; 560(2): 491 - 503. [Abstract] [Full Text] [PDF]

				M. Grunnet and W. A. Kaufmann Coassembly of Big Conductance Ca2+-activated K+ Channels and L-type Voltage-gated Ca2+ Channels in Rat Brain J. Biol. Chem., August 27, 2004; 279(35): 36445 - 36453. [Abstract] [Full Text] [PDF]

				D. Trauner and R. H. Kramer Metabolic Modulation of Potassium Channels Sci. Signal., May 18, 2004; 2004(233): pe22 - pe22. [Abstract] [Full Text] [PDF]

				G. Raffaelli, C. Saviane, M. H. Mohajerani, P. Pedarzani, and E. Cherubini BK potassium channels control transmitter release at CA3-CA3 synapses in the rat hippocampus J. Physiol., May 15, 2004; 557(1): 147 - 157. [Abstract] [Full Text] [PDF]

				F. Lesage, H. Hibino, and A. J. Hudspeth Association of {beta}-catenin with the {alpha}-subunit of neuronal large-conductance Ca2+-activated K+ channels PNAS, January 13, 2004; 101(2): 671 - 675. [Abstract] [Full Text] [PDF]

				C. G. Reich, S. E. Mason, and B. E. Alger Novel Form of LTD Induced by Transient, Partial Inhibition of the Na,K-Pump in Rat Hippocampal CA1 Cells J Neurophysiol, January 1, 2004; 91(1): 239 - 247. [Abstract] [Full Text] [PDF]

				T. Ishikawa, Y. Nakamura, N. Saitoh, W.-B. Li, S. Iwasaki, and T. Takahashi Distinct Roles of Kv1 and Kv3 Potassium Channels at the Calyx of Held Presynaptic Terminal J. Neurosci., November 12, 2003; 23(32): 10445 - 10453. [Abstract] [Full Text] [PDF]

				H. A Widmer, I. C M Rowe, and M. J Shipston Conditional protein phosphorylation regulates BK channel activity in rat cerebellar Purkinje neurons J. Physiol., October 15, 2003; 552(2): 379 - 391. [Abstract] [Full Text] [PDF]

				E S L. Faber and P. Sah Ca2+-activated K+ (BK) channel inactivation contributes to spike broadening during repetitive firing in the rat lateral amygdala J. Physiol., October 15, 2003; 552(2): 483 - 497. [Abstract] [Full Text] [PDF]

				E. S. L. Faber and P. Sah Calcium-Activated Potassium Channels: Multiple Contributions to Neuronal Function Neuroscientist, June 1, 2003; 9(3): 181 - 194. [Abstract] [PDF]

				L J Shanley, D O'Malley, A J Irving, M L Ashford, and J Harvey Leptin inhibits epileptiform-like activity in rat hippocampal neurones via PI 3-kinase-driven activation of BK channels J. Physiol., December 15, 2002; 545(3): 933 - 944. [Abstract] [Full Text] [PDF]

				C. A. Sailer, H. Hu, W. A. Kaufmann, M. Trieb, C. Schwarzer, J. F. Storm, and H.-G. Knaus Regional Differences in Distribution and Functional Expression of Small-Conductance Ca2+-Activated K+ Channels in Rat Brain J. Neurosci., November 15, 2002; 22(22): 9698 - 9707. [Abstract] [Full Text] [PDF]

				M. Druzin, D. Haage, E. Malinina, and S. Johansson Dual and opposing roles of presynaptic Ca2+ influx for spontaneous GABA release from rat medial preoptic nerve terminals J. Physiol., July 1, 2002; 542(1): 131 - 146. [Abstract] [Full Text] [PDF]

Home  |   Search  |   Archive  |   Subscribe  |   Contact  |   Help