Histamine promotes excitability in bovine adrenal chromaffin cells by inhibiting an M-current

Wallace, Damian J, Chen, Chen and Marley, Philip D (2002) Histamine promotes excitability in bovine adrenal chromaffin cells by inhibiting an M-current. The journal of physiology, 540 3: 921-939. doi:10.1113/jphysiol.2001.013370


Author Wallace, Damian J
Chen, Chen
Marley, Philip D
Title Histamine promotes excitability in bovine adrenal chromaffin cells by inhibiting an M-current
Journal name The journal of physiology   Check publisher's open access policy
ISSN 0022-3751
1469-7793
Publication date 2002
Year available 2002
Sub-type Article (original research)
DOI 10.1113/jphysiol.2001.013370
Volume 540
Issue 3
Start page 921
End page 939
Total pages 19
Place of publication Oxford
Publisher Blackwell for the Physiological Society
Collection year 2002
Language eng
Subject 110306 Endocrinology
110201 Cardiology (incl. Cardiovascular Diseases)
111201 Cancer Cell Biology
Abstract The current study has investigated the electrophysiological responses evoked by histamine in bovine adrenal chromaffin cells using perforated-patch techniques. Histamine caused a transient hyperpolarization followed by a sustained depolarization of 7.2 ±1.4 mV associated with an increase in spontaneous action potential frequency. The hyperpolarization was abolished after depleting intracellular Ca2+ stores with thapsigargin (100 nM), and was reduced by 40 % with apamin (100 nM). Membrane resistance increased by about 60 % during the histamine-induced depolarization suggesting inhibition of a K+ channel. An inward current relaxation, typical of an Mcurrent, was observed in response to negative voltage steps from a holding potential of _30 mV. This current reversed at _81.6 ±1.8 mV and was abolished by the M-channel inhibitor linopirdine (100 mM). During application of histamine, the amplitude of M-currents recorded at a time corresponding with the sustained depolarization was reduced by 40 %. No inward current rectification was observed in the range _150 to _70 mV, and glibenclamide (10 mM) had no effect on either resting membrane potential or the response to histamine. The results show that an M-current is present in bovine chromaffin cells and that this current is inhibited during sustained application of histamine, resulting in membrane depolarization and increased discharge of action potentials. These results demonstrate for the first time a possible mechanism coupling histamine receptors to activation of voltage-operated Ca2+ channels in these cells.
References AKOPIAN, A. N., SIVILOTTI, L. & WOOD, J. N. (1996). A tetrodotoxinresistant voltage-gated sodium channel expressed by sensory neurons. Nature 379, 257–262. ALBILLOS, A., CARBONE, E., GANDIA, L., GARCIA, A. G. & POLLO, A. (1996). Opioid inhibition of Ca2+ channel subtypes in bovine chromaffin cells: selectivity of action and voltage-dependence. European Journal of Neuroscience 8, 1561–1570. ARTALEJO, A. R., GARCIA, A. G. & NEHER, E. (1993). Smallconductance Ca2+-activated K+ channels in bovine chromaffin cells. Pflügers Archiv 423, 97–103. ASHCROFT, F. M. & RORSMAN, P. (1989). Electrophysiology of the pancreatic beta-cell. Progress in Biophysics and Molecular Biology 54, 87–143. 936 D. J. Wallace, C. Chen and P. D. Marley J. Physiol. 540.3 BARBARA, J. G., LEMOS, V. S. & TAKEDA, K. (1998). Pre- and postsynaptic muscarinic receptors in thin slices of rat adrenal gland. European Journal of Neuroscience 10, 3535–3545. BAUKROWITZ, T., SCHULTE, U., OLIVER, D., HERLITZE, S., KRAUTER, T., TUCKER, S. J., RUPPERSBERG, J. P. & FAKLER, B. (1998). PIP2 and PIP as determinants for ATP inhibition of KATP channels. Science 282, 1141–1144. BIALES, B., DICHTER, M. & TISCHLER, A. (1976) Electrical excitability of cultured adrenal chromaffin cells. Journal of Physiology 262, 743–753. BOLTON, T. B., CLARK, J. P., KITAMURA, K. & LANG, R. J. (1981). Evidence that histamine and carbachol may open the same ion channels in longitudinal smooth muscle of guinea-pig ileum. Journal of Physiology 320, 363–379. BÖDDING, M. (2000). Histamine evoked sustained elevations of cytosolic Ca2+ in bovine adrenal chromaffin cells independently of Ca2+ entry. Cell Calcium 27, 139–151. BROWN, D. A. & ADAMS, P. R. (1980). Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature 283, 673–676. BROWN, R. E., STEVENS, D. R. & HAAS, H. L. (2001). The physiology of brain histamine. Progress in Neurobiology 63, 637–672. BUNN, S. J. & BOYD, T. L. (1992). Characterization of histamineinduced catecholamine secretion from bovine adrenal medullary chromaffin cells. Journal of Neurochemistry 58, 1602–1610. BUNN, S. J. & DUNKLEY, P. R. (1997). Histamine-stimulated phospholipase C signalling in the adrenal chromaffin cell: effects on inositol phospholipid metabolism and tyrosine hydroxylase phosphorylation. Clinical and Experimental Pharmacology and Physiology 24, 624–631. CAFFREY, J. M., ENG, D. L., BLACK, J. A., WAXMAN, S. G. & KOCSIS, J. D. (1992). Three types of sodium channels in adult rat dorsal root ganglion neurons. Brain Research 592, 283–297. CHANG, R. S. L., TRAN, V. T. & SNYDER, S. H. (1979). Characteristics of histamine H1-receptors in peripheral tissues labelled with [3H]mepyramine. Journal of Pharmacology and Experimental Therapeutics 209, 437–442. CHEEK, T. R., MORGAN, A., O’SULLIVAN, A. J., MORETON, R. B., BERRIDGE, M. J. & BURGOYNE, R. D. (1993). Spatial localisation of agonist-induced Ca2+ entry in bovine adrenal chromaffin cells: different patterns induced by histamine and angiotensin II, and relationship to catecholamine release. Journal of Cell Science 105, 913–921. CONSTANTI, A. & BROWN, D. A. (1981). M-Currents in voltageclamped mammalian sympathetic neurones. Neuroscience Letters 24, 289–294. CONSTANTI, A. & GALVAN, M. (1983). M-current in voltage-clamped olfactory cortex neurones. Neuroscience Letters 39, 65–70. CRUZBLANCA, H., KOH, D. S. & HILLE, B. (1998). Bradykinin inhibits M current via phospholipase C and Ca2+ release from IP3-sensitive Ca2+ stores in rat sympathetic neurons. Proceedings of the National Academy of Sciences of the USA 95, 7151–7156. CURRIE, K. P. & FOX, A. P. (2000). Voltage-dependent, pertussis toxin insensitive inhibition of calcium currents by histamine in bovine adrenal chromaffin cells. Journal of Neurophysiology 83, 1435–1442. DOUGLAS, W. W., KANNO, T. & SAMPSON, S. R. (1967). Influence of the ionic environment on the membrane potential of adrenal chromaffin cells and on the depolarizing effect of acetylcholine. Journal of Physiology 191, 107–121. DOUPNIK, C. A. & PUN, R. Y. (1994). G-protein activation mediates prepulse facilitation of Ca2+ channel currents in bovine chromaffin cells. Journal of Membrane Biology 140, 47–56. FENWICK, E. M., MARTY, A. & NEHER, E. (1982a). A patch-clamp study of bovine chromaffin cells and of their sensitivity to acetylcholine. Journal of Physiology 331, 577–597. FENWICK, E. M., MARTY, A. & NEHER, E. (1982b). Sodium and calcium channels in bovine chromaffin cells. Journal of Physiology 331, 599–635. GANDIA, L., GARCIA, A. G. & MORAD, M. (1993). ATP modulation of calcium channels in chromaffin cells. Journal of Physiology 470, 55–72. GELLENS, M. E., GEORGE, A. L., JR, CHEN, L. Q., CHAHINE, M., HORN, R., BARCHI, R. L. & KALLEN, R. G. (1992). Primary structure and functional expression of the human cardiac tetrodotoxininsensitive voltage-dependent sodium channel. Proceedings of the National Academy of Sciences of the USA 89, 554–558. GOH, Y. & KUROSAWA, A. (1991). Characterization and Ca2+ requirement of histamine-induced catecholamine secretion in cultured bovine chromaffin cells. Journal of Neurochemistry 57, 1249–1257. GRIFFITH, W. H., HILLS, J. M. & BROWN, D. A. (1988). Substance Pmediated membrane currents in voltage-clamped guinea pig inferior mesenteric ganglion cells. Synapse 2, 432–441. HAAS, H. L. & KONNERTH, A. (1983). Histamine and noradrenaline decrease calcium-activated potassium conductance in hippocampal pyramidal cells. Nature 302, 432–434. HALLIWELL, J. V. (1986). M-current in human neocortical neurones. Neuroscience Letters 67, 1–6. HÄPPÖALÄ, O., SOINILA, S., PÄIVÄRINTA, H., JOH, T. H. & PANULA, P. (1985). Histamine-immunoreactive endocrine cells in the adrenal medulla of the rat. Brain Research 339, 393–396. Hille, B. (1992). Ionic Channels of Excitable Membranes, 2nd edn. Sinauer Associates Inc., Sunderland MA, USA. HILLSLEY, K., KENYON, J. L. & SMITH, T. K. (2000). Ryanodinesensitive stores regulate the excitability of AH neurons in the myenteric plexus of guinea-pig ileum. Journal of Neurophysiology 84, 2777–2785. HOGG, R. C. & ADAMS, D. J. (2001). An ATP-sensitive K+ conductance in dissociated neurones from adult rat intracardiac ganglia. Journal of Physiology 534, 713–720. HOLMAN, M. E., COLEMAN, H. A., TONTA, M. A. & PARKINGTON, H. C. (1994). Synaptic transmission from splanchnic nerves to the adrenal medulla of guinea-pigs. Journal of Physiology 478, 115–124. HOLMAN, M. E., TONTA, M. A., COLEMAN, H. A. & PARKINGTON, H. C. (1998). Muscarinic receptor activation in guinea-pig chromaffin cells causes decreased membrane conductance and depolarization. Journal of the Autonomic Nervous System 68, 140–144. HONG, K. H., ARMSTRONG, C. M. & MILLER, C. (2001). Revisiting the role of Ca2+ in Shaker K+ channel gating. Biophysical Journal 80, 2216–2220. HUANG, C. L., FENG, S. & HILGEMANN, D. W. (1998). Direct activation of inward rectifier potassium channels by PIP2 and its stabilization by Gbg. Nature 391, 803–806. INOUE, M., FUJISHIRO, N. & IMANAGA, I. (1998). Hypoxia and cyanide induce depolarization and catecholamine release in dispersed guinea-pig chromaffin cells. Journal of Physiology 507, 807–818. JOBLING, P., MCLACHLAN, E. M. & SAH, P. (1993). Calcium induced calcium release is involved in the afterhyperpolarization in one class of guinea pig sympathetic neurone. Journal of the Autonomic Nervous System 42, 251–257. J. Physiol. 540.3 M-current modulation in chromaffin cells 937 KLEPPISCH, T., AHNERT-HILGER, G., GOLLASCH, M., SPICHER, K., HESCHELER, J., SCHULTZ, G. & ROSENTHAL, W. (1992). Inhibition of voltage-dependent Ca2+ channels via alpha 2-adrenergic and opioid receptors in cultured bovine adrenal chromaffin cells. Pflügers Archiv 421, 131–137. LAMAS, J. A., SELYANKO, A. A. & BROWN, D. A. (1997). Effects of a cognition-enhancer, linopirdine (DuP 996), on M-type potassium currents (IKM) and some other voltage- and ligand-gated membrane currents in rat sympathetic neurons. European Journal of Neuroscience 9, 605–616. LI, Z. & HATTON, G. I. (1996). Histamine-induced prolonged depolarization in rat supraoptic neurons: G-protein-mediated, Ca2+-independent suppression of K+ leakage conductance. Neuroscience 70, 145–158. LIVETT, B. G. (1984). Adrenal medullary chromaffin cells in vitro. Physiological Reviews 64, 1103–1161. LIVETT, B. G. & MARLEY, P. D. (1986). Effects of opioid peptides and morphine on histamine-induced catecholamine secretion from cultured, bovine adrenal chromaffin cells. British Journal of Pharmacology 89, 327–334. MARLEY, P. D., BUNN, S. J., WAN, D. C. C., ALLEN, A. M. & MENDELSOHN, F. A. O. (1989). Localization of angiotensin II binding sites in the bovine adrenal medulla using a labelled specific antagonist. Neuroscience 28, 777–787. MARRION, N. V. (1997). Control of M-current. Annual Review of Physiology 59, 483–504. MARTY, A. (1981). Ca2+-dependent K+ channels with large unitary conductance in chromaffin cell membranes. Nature 291, 497–500. MARTY, A. & NEHER, E. (1985). Potassium channels in cultured bovine adrenal chromaffin cells. Journal of Physiology 367, 117–141. MEVES, H., SCHWARZ, J. R. & WULFSEN, I. (1999). Separation of M-like current and ERG current in NG108–15 cells. British Journal of Pharmacology 127, 1213–1223. MOORE, S. D., MADAMBA, S. G., JOELS, M. & SIGGINS, G. R. (1988). Somatostatin augments the M-current in hippocampal neurons. Science 239, 278–280. NASSAR-GENTINA, V., POLLARD, H. B. & ROJAS, E. (1988). Electrical activity in chromaffin cells of intact mouse adrenal gland. American Journal of Physiology 254, C675–683. NILIUS, B., SCHWARZ, G. & DROOGMANS, G. (1993). Modulation by histamine of an inwardly rectifying potassium channel in human endothelial cells. Journal of Physiology 472, 359–371. NOBLE, E. P., BOMMER, M., LIEBISCH, D. & HERZ, A. (1988). H1- histaminergic activation of catecholamine release by chromaffin cells. Biochemical Pharmacology 37, 221–228. NOBLE, E. P., BOMMER, M., SINCINI, E., COSTA, T. & HERZ, A. (1986). H1-Histaminergic activation stimulates inositol-1-phosphate accumulation in chromaffin cells. Biochemical and Biophysical Research Communications 135, 566–573. O’FARRELL, M. & MARLEY, P. D. (1997). Multiple calcium channels are required for pituitary adenylate cyclase-activating polypeptideinduced catecholamine secretion from bovine cultured adrenal chromaffin cells. Naunyn-Schmiedeberg’s Archives of Pharmacology 356, 536–542. O’FARRELL, M. & MARLEY, P. D. (1999). Different contributions of voltage-sensitive Ca2+ channels to histamine-induced catecholamine release and tyrosine hydroxylase activation in bovine adrenal chromaffin cells. Cell Calcium 25, 209–217. O’SULLIVAN, A. J., CHEEK, T. R., MORETON, R. B., BERRIDGE, M. J. & BURGOYNE, R. D. (1989). Localization and heterogeneity of agonist-induced changes in cytosolic calcium concentration in single bovine adrenal chromaffin cells from video imaging of fura- 2. The EMBO Journal 8, 401–411. OHNO-SHOSAKU, T. & YAMAMOTO, C. (1992). Identification of an ATP-sensitive K+ channel in rat cultured cortical neurons. Pflügers Archiv 422, 260–266. PENDER, N. & BURGOYNE, R. D. (1992). Histamine stimulates exocytosis in a sub-population of bovine adrenal chromaffin cells. Neuroscience Letters 144, 207–210. PLEVIN, R. & BOARDER, M. R. (1988). Stimulation of formation of inositol phosphates in primary cultures of bovine adrenal chromaffin cells by angiotensin II, histamine, bradykinin, and carbachol. Journal of Neurochemistry 51, 634–641. POWELL, A. D., TESCHEMACHER, A. G. & SEWARD, E. P (2000). P2Y purinoceptors inhibit exocytosis in adrenal chromaffin cells via modulation of voltage-operated calcium channels. Journal of Neuroscience 20, 606–616. REINER, P. B. & KAMONDI, A. (1994). Mechanisms of antihistamineinduced sedation in the human brain: H1 receptor activation reduces a background leakage potassium current. Neuroscience 59, 579–588. ROBBINS, J. (2001) KCNQ potassium channels: physiology, pathophysiology, and pharmacology. Pharmacology and Therapeutics 90, 1–19. ROBERTS-THOMSON, E. L., SAUNDERS, H. I., PALMER, S. M., POWIS, D. A., DUNKLEY, P. R. & BUNN, S. J. (2000). Ca2+ influx stimulated phospholipase C activity in bovine adrenal chromaffin cells: responses to K+ depolarization and histamine. European Journal of Pharmacology 398, 199–207. SAH, P. & MCLACHLAN, E. M. (1991). Ca2+-activated K+ currents underlying the afterhyperpolarization in guinea pig vagal neurons: a role for Ca2+-activated Ca2+ release. Neuron 7, 257–264. SANKARANARAYANAN, S. & SIMASKO, S. M. (1996). Characterization of an M-like current modulated by thyrotropin-releasing hormone in normal rat lactotrophs. Journal of Neuroscience 16, 1668–1678. SHAH, M. & HAYLETT, D. G. (2000). Ca2+ channels involved in the generation of the slow afterhyperpolarization in cultured rat hippocampal pyramidal neurons. Journal of Neurophysiology 83, 2554–2561. SHYNG, S. L. & NICHOLS, C. G. (1998). Membrane phospholipid control of nucleotide sensitivity of KATP channels. Science 282, 1138–1141. SIMMONS, M. A. & SCHNEIDER, C. R. (1998). Regulation of M-type potassium current by intracellular nucleotide phosphates. Journal of Neuroscience 18, 6254–6260. SIMS, S. M., SINGER, J. J. & WALSH, J. V. JR (1985). Cholinergic agonists suppress a potassium current in freshly dissociated smooth muscle cells of the toad. Journal of Physiology 367, 503–529. STAUDERMAN, K. A., MCKINNEY, R. A. & MURAWSKY, M. M. (1991). The role of caffeine-sensitive Ca2+ stores in agonist- and inositol 1,4,5-trisphosphate-induced Ca2+ release from bovine adrenal chromaffin cells. Biochemical Journal 278, 643–650. STAUDERMAN, K. A. & MURAWSKY, M. M. (1991). The inositol 1,4,5- trisphosphate-forming agonist histamine activates a ryanodinesensitive Ca2+ release mechanism in bovine adrenal chromaffin cells. Journal of Biological Chemistry 266, 19 150–19 153. STAUDERMAN, K. A., MURAWSKY, M. M. & PRUSS, R. M. (1990). Agonist-dependent patterns of cytosolic Ca2+ changes in single bovine adrenal chromaffin cells: relationship to catecholamine release. Cell Regulation 1, 683–691. 938 D. J. Wallace, C. Chen and P. D. Marley J. Physiol. 540.3 STAUDERMAN, K. A. & PRUSS, R. M. (1990). Different patterns of agonist-stimulated increases of 3H-inositol phosphate isomers and cytosolic Ca2+ in bovine adrenal chromaffin cells: comparison of the effects of histamine and angiotensin II. Journal of Neurochemistry 54, 946–953. TAKAHIRA, M. & HUGHES, B. A. (1997). Isolated bovine retinal pigment epithelial cells express delayed rectifier type and M-type K+ currents. American Journal of Physiology 273, C790–803. TUOMINEN, R. K., KARHUNEN, T., PANULA, P. & YAMATODANI, A. (1993). Endogenous histamine in cultured bovine adrenal chromaffin cells. European Journal of Neuroscience 5, 1436–1441. VILLARROEL, A. (1996). M-current suppression in PC12 cells by bradykinin is mediated by a pertussis toxin-insensitive G-protein and modulated by intracellular calcium. Brain Research 740, 227–233. VILLARROEL, A., MARRION, N. V., LOPEZ, H. & ADAMS, P. R. (1989). Bradykinin inhibits a potassium M-like current in rat pheochromocytoma PC12 cells. FEBS Letters 255, 42–46. VOGALIS, F., FURNESS, J. B. & KUNZE, W. A. (2001). Afterhyperpolarization current in myenteric neurons of the guinea pig duodenum. Journal of Neurophysiology 85, 1941–1951. WALLACE, D. J. & MARLEY, P. D. (2001). Activation of voltageoperated Ca2+ channels by histamine in chromaffin cells does not require Ca2+ release from intracellular stores. Proceedings of the Australian Neuroscience Society 12, 35. WANG, H. S., PAN, Z., SHI, W., BROWN, B. S., WYMORE, R. S., COHEN, I. S., DIXON, J. E. & MCKINNON, D. (1998). KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science 282, 1890–1893. WARASHINA, A. (1997). Involvement of protein kinase C in homologous desensitization of histamine-evoked secretory responses in rat chromaffin cells. Brain Research 762, 40–46. WOLLMUTH, L. P. (1994). Mechanism of Ba2+ block of M-like K channels of rod photoreceptors of tiger salamanders. Journal of General Physiology 103, 45–66. WOMBLE, M. D. & MOISES, H. C. (1992). Muscarinic inhibition of Mcurrent and a potassium leak conductance in neurones of the rat basolateral amygdala. Journal of Physiology 457, 93–114. XU, Z. J. & ADAMS, D. J. (1992). Resting membrane potential and potassium currents in cultured parasympathetic neurones from rat intracardiac ganglia. Journal of Physiology 456, 405–424. ZERBES, M., BUNN, S. J. & POWIS, D. A. (1998). Histamine causes Ca2+ entry via both a store-operated and a store-independent pathway in bovine adrenal chromaffin cells. Cell Calcium 23, 379–386. ZHOU, Z. & MISLER, S. (1995). Action potential-induced quantal secretion of catecholamines from rat adrenal chromaffin cells. Journal of Biological Chemistry 270, 3498–3505.
Q-Index Code C1
Q-Index Status Provisional Code
Institutional Status Unknown

Document type: Journal Article
Sub-type: Article (original research)
Collections: Excellence in Research Australia (ERA) - Collection
School of Biomedical Sciences Publications
 
Versions
Version Filter Type
Citation counts: TR Web of Science Citation Count  Cited 40 times in Thomson Reuters Web of Science Article | Citations
Scopus Citation Count Cited 43 times in Scopus Article | Citations
Google Scholar Search Google Scholar
Created: Mon, 12 Jan 2009, 16:38:18 EST by Marianne Steentsma on behalf of Library Corporate Services