Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1995 Jun 1;485(Pt 2):297–318. doi: 10.1113/jphysiol.1995.sp020731

The suppression of Ca(2+)- and voltage-dependent outward K+ current during mAChR activation in rat adrenal chromaffin cells.

J Herrington 1, C R Solaro 1, A Neely 1, C J Lingle 1
PMCID: PMC1157994  PMID: 7666360

Abstract

1. The mechanism by which muscarine, ionomycin or caffeine results in suppression of Ca(2+)- and voltage-dependent outward current in rat adrenal chromaffin cells was evaluated using both whole-cell voltage clamp and single channel recording. 2. The whole-cell current activated following the elevation of the cytosolic calcium concentration ([Ca2+]i) by muscarine inactivates with a time course comparable to that of single Ca(2+)- and voltage-dependent potassium (BK) channels. 3. The whole-cell inactivating current is pharmacologically similar to BK current. 4. The voltage dependence of inactivation and rate of recovery from inactivation are qualitatively similar for both whole-cell current and ensemble averages of single BK channels. Furthermore, changes in the rate of whole-cell current inactivation track expected changes in submembrane [Ca2+]. 5. The suppression of outward current can be accounted for solely by inactivation of BK channels and does not depend on the means by which [Ca2+]i is elevated. 6. Muscarinic acetylcholine receptor (mAChR) activation, changes in holding potential (-50 to -20 mV), and step depolarizations of different amplitude and duration were tested for their ability to elevate [Ca2+]i and thereby regulate the availability of BK current for activation. 7. Following muscarine-induced elevation of [Ca2+]i at holding potentials positive to -40 mV, the availability of BK current for activation was typically reduced by more than 50%. 8. Holding potentials in the range of -50 to -20 mV produced only slight alterations in the availability of BK current for activation. 9. Step depolarizations that cause maximal rates of Ca2+ influx (0 to +10 mV) must exceed 200 ms to reduce the availability of BK current by approximately 50%. 10. The results show that the muscarine-induced elevation of [Ca2+]i produces a profound reduction in the availability of BK channels for activation at membrane potentials likely to be physiologically meaningful. Although depolarization- induced Ca2+ influx can inactivate BK current, we propose that short duration depolarizations that occur during normal electrical activity will not significantly alter BK channel availability.

Full text

PDF
297

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams P. R., Constanti A., Brown D. A., Clark R. B. Intracellular Ca2+ activates a fast voltage-sensitive K+ current in vertebrate sympathetic neurones. Nature. 1982 Apr 22;296(5859):746–749. doi: 10.1038/296746a0. [DOI] [PubMed] [Google Scholar]
  2. Artalejo C. R., Rossie S., Perlman R. L., Fox A. P. Voltage-dependent phosphorylation may recruit Ca2+ current facilitation in chromaffin cells. Nature. 1992 Jul 2;358(6381):63–66. doi: 10.1038/358063a0. [DOI] [PubMed] [Google Scholar]
  3. Blatz A. L., Magleby K. L. Single apamin-blocked Ca-activated K+ channels of small conductance in cultured rat skeletal muscle. Nature. 1986 Oct 23;323(6090):718–720. doi: 10.1038/323718a0. [DOI] [PubMed] [Google Scholar]
  4. Capiod T., Ogden D. C. The properties of calcium-activated potassium ion channels in guinea-pig isolated hepatocytes. J Physiol. 1989 Feb;409:285–295. doi: 10.1113/jphysiol.1989.sp017497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cheek T. R., Burgoyne R. D. Effect of activation of muscarinic receptors on intracellular free calcium and secretion in bovine adrenal chromaffin cells. Biochim Biophys Acta. 1985 Jul 30;846(1):167–173. doi: 10.1016/0167-4889(85)90122-3. [DOI] [PubMed] [Google Scholar]
  6. Cheek T. R., O'Sullivan A. J., Moreton R. B., Berridge M. J., Burgoyne R. D. Spatial localization of the stimulus-induced rise in cytosolic Ca2+ in bovine adrenal chromaffin cells. Distinct nicotinic and muscarinic patterns. FEBS Lett. 1989 Apr 24;247(2):429–434. doi: 10.1016/0014-5793(89)81385-7. [DOI] [PubMed] [Google Scholar]
  7. Cole W. C., Carl A., Sanders K. M. Muscarinic suppression of Ca2+-dependent K current in colonic smooth muscle. Am J Physiol. 1989 Sep;257(3 Pt 1):C481–C487. doi: 10.1152/ajpcell.1989.257.3.C481. [DOI] [PubMed] [Google Scholar]
  8. Fenwick E. M., Fajdiga P. B., Howe N. B., Livett B. G. Functional and morphological characterization of isolated bovine adrenal medullary cells. J Cell Biol. 1978 Jan;76(1):12–30. doi: 10.1083/jcb.76.1.12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Goh J. W., Pennefather P. S. Pharmacological and physiological properties of the after-hyperpolarization current of bullfrog ganglion neurones. J Physiol. 1987 Dec;394:315–330. doi: 10.1113/jphysiol.1987.sp016872. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  12. Horn R., Marty A. Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol. 1988 Aug;92(2):145–159. doi: 10.1085/jgp.92.2.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Inoue M., Kuriyama H. Muscarinic receptor is coupled with a cation channel through a GTP-binding protein in guinea-pig chromaffin cells. J Physiol. 1991 May;436:511–529. doi: 10.1113/jphysiol.1991.sp018564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kidokoro Y., Ritchie A. K. Chromaffin cell action potentials and their possible role in adrenaline secretion from rat adrenal medulla. J Physiol. 1980 Oct;307:199–216. doi: 10.1113/jphysiol.1980.sp013431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kilpatrick D. L., Ledbetter F. H., Carson K. A., Kirshner A. G., Slepetis R., Kirshner N. Stability of bovine adrenal medulla cells in culture. J Neurochem. 1980 Sep;35(3):679–692. doi: 10.1111/j.1471-4159.1980.tb03707.x. [DOI] [PubMed] [Google Scholar]
  16. Konnerth A., Lux H. D., Morad M. Proton-induced transformation of calcium channel in chick dorsal root ganglion cells. J Physiol. 1987 May;386:603–633. doi: 10.1113/jphysiol.1987.sp016553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kume H., Takai A., Tokuno H., Tomita T. Regulation of Ca2+-dependent K+-channel activity in tracheal myocytes by phosphorylation. Nature. 1989 Sep 14;341(6238):152–154. doi: 10.1038/341152a0. [DOI] [PubMed] [Google Scholar]
  18. Lancaster B., Nicoll R. A., Perkel D. J. Calcium activates two types of potassium channels in rat hippocampal neurons in culture. J Neurosci. 1991 Jan;11(1):23–30. doi: 10.1523/JNEUROSCI.11-01-00023.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lancaster B., Nicoll R. A. Properties of two calcium-activated hyperpolarizations in rat hippocampal neurones. J Physiol. 1987 Aug;389:187–203. doi: 10.1113/jphysiol.1987.sp016653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lancaster B., Pennefather P. Potassium currents evoked by brief depolarizations in bull-frog sympathetic ganglion cells. J Physiol. 1987 Jun;387:519–548. doi: 10.1113/jphysiol.1987.sp016587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lang D. G., Ritchie A. K. Large and small conductance calcium-activated potassium channels in the GH3 anterior pituitary cell line. Pflugers Arch. 1987 Dec;410(6):614–622. doi: 10.1007/BF00581321. [DOI] [PubMed] [Google Scholar]
  22. Lang D. G., Ritchie A. K. Tetraethylammonium blockade of apamin-sensitive and insensitive Ca2(+)-activated K+ channels in a pituitary cell line. J Physiol. 1990 Jun;425:117–132. doi: 10.1113/jphysiol.1990.sp018095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lechleiter J. D., Dartt D. A., Brehm P. Vasoactive intestinal peptide activates Ca2(+)-dependent K+ channels through a cAMP pathway in mouse lacrimal cells. Neuron. 1988 May;1(3):227–235. doi: 10.1016/0896-6273(88)90143-2. [DOI] [PubMed] [Google Scholar]
  24. Levitan I. B. Phosphorylation of ion channels. J Membr Biol. 1985;87(3):177–190. doi: 10.1007/BF01871217. [DOI] [PubMed] [Google Scholar]
  25. Livett B. G. Adrenal medullary chromaffin cells in vitro. Physiol Rev. 1984 Oct;64(4):1103–1161. doi: 10.1152/physrev.1984.64.4.1103. [DOI] [PubMed] [Google Scholar]
  26. Marty A., Neher E. Potassium channels in cultured bovine adrenal chromaffin cells. J Physiol. 1985 Oct;367:117–141. doi: 10.1113/jphysiol.1985.sp015817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. McManus O. B. Calcium-activated potassium channels: regulation by calcium. J Bioenerg Biomembr. 1991 Aug;23(4):537–560. doi: 10.1007/BF00785810. [DOI] [PubMed] [Google Scholar]
  28. Neely A., Lingle C. J. Effects of muscarine on single rat adrenal chromaffin cells. J Physiol. 1992;453:133–166. doi: 10.1113/jphysiol.1992.sp019221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Neely A., Lingle C. J. Two components of calcium-activated potassium current in rat adrenal chromaffin cells. J Physiol. 1992;453:97–131. doi: 10.1113/jphysiol.1992.sp019220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Park Y. B. Ion selectivity and gating of small conductance Ca(2+)-activated K+ channels in cultured rat adrenal chromaffin cells. J Physiol. 1994 Dec 15;481(Pt 3):555–570. doi: 10.1113/jphysiol.1994.sp020463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pennefather P., Lancaster B., Adams P. R., Nicoll R. A. Two distinct Ca-dependent K currents in bullfrog sympathetic ganglion cells. Proc Natl Acad Sci U S A. 1985 May;82(9):3040–3044. doi: 10.1073/pnas.82.9.3040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rae J., Cooper K., Gates P., Watsky M. Low access resistance perforated patch recordings using amphotericin B. J Neurosci Methods. 1991 Mar;37(1):15–26. doi: 10.1016/0165-0270(91)90017-t. [DOI] [PubMed] [Google Scholar]
  33. Reinhart P. H., Chung S., Martin B. L., Brautigan D. L., Levitan I. B. Modulation of calcium-activated potassium channels from rat brain by protein kinase A and phosphatase 2A. J Neurosci. 1991 Jun;11(6):1627–1635. doi: 10.1523/JNEUROSCI.11-06-01627.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Ritchie A. K. Two distinct calcium-activated potassium currents in a rat anterior pituitary cell line. J Physiol. 1987 Apr;385:591–609. doi: 10.1113/jphysiol.1987.sp016509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Role L. W., Perlman R. L. Purification of adrenal medullary chromaffin cells by density gradient centrifugation. J Neurosci Methods. 1980 Jun;2(3):253–265. doi: 10.1016/0165-0270(80)90014-x. [DOI] [PubMed] [Google Scholar]
  36. Solaro C. R., Lingle C. J. Trypsin-sensitive, rapid inactivation of a calcium-activated potassium channel. Science. 1992 Sep 18;257(5077):1694–1698. doi: 10.1126/science.1529355. [DOI] [PubMed] [Google Scholar]
  37. White R. E., Schonbrunn A., Armstrong D. L. Somatostatin stimulates Ca(2+)-activated K+ channels through protein dephosphorylation. Nature. 1991 Jun 13;351(6327):570–573. doi: 10.1038/351570a0. [DOI] [PubMed] [Google Scholar]
  38. Yellen G. Ionic permeation and blockade in Ca2+-activated K+ channels of bovine chromaffin cells. J Gen Physiol. 1984 Aug;84(2):157–186. doi: 10.1085/jgp.84.2.157. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES