Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1991 Dec;444:213–240. doi: 10.1113/jphysiol.1991.sp018874

Three types of bovine chromaffin cell Ca2+ channels: facilitation increases the opening probability of a 27 pS channel.

C R Artalejo 1, D J Mogul 1, R L Perlman 1, A P Fox 1
PMCID: PMC1179929  PMID: 1726596

Abstract

1. Cell-attached patch recordings from bovine chromaffin cells were performed with 90 mM-Ba2+ in the patch pipette and with isotonic potassium aspartate in the bathing solution to zero the membrane potential. Three different types of unitary Ca2+ channel activity could be distinguished in these recordings. 2. A 27 pS Ca2+ channel was distinguished by constructing amplitude histograms and measuring slope conductance. This channel activated over a broad range of potentials (depolarizations greater than -10 mV). 3. A second Ca2+ channel with a slope conductance of 14 pS could also be detected with amplitude histograms. This channel activated with depolarizations greater than -20 mV. 4. An 18 pS Ca2+ channel was observed infrequently indicating that this channel may carry only a small amount of the whole-cell current. This 18 pS channel was sensitive to changes in holding potential. Depolarizing the patch to +10 mV from a holding potential of -80 mV elicited robust unitary activity. Changing the patch holding potential to -40 mV while maintaining test depolarizations to +10 mV completely inactivated the 18 pS channel. Neither the 25 pS nor the 14 pS Ca2+ channels were affected by changes in holding potential in the range from -80 mV to -40 mV, indicating the 18 pS channel was a different type of channel. As the 18 pS channel was observed so infrequently, no detailed studies of it were possible. 5. Chromaffin cell Ca2+ currents exhibited facilitation. Large pre-depolarizations greatly augmented whole-cell currents observed in these cells. Whole-cell currents could double or triple after recruiting facilitation. The application of large pre-depolarizations altered the gating behaviour of the 27 pS Ca2+ channel manifested as dramatically increased channel opening probabilities measured during subsequent test pulses. Large pre-depolarizations induced unitary activity in the 27 pS Ca2+ channel similar to the long-lived openings exhibited by L-type Ca2+ channels in the presence of Bay K 8644. Large pre-depolarizations did not change the gating behaviour of the 14 pS Ca2+ channel. 6. Repetitive depolarizations in the physiological range could also induce facilitation. At the single-channel level facilitation was manifested as a striking increase in opening probability of the 27 pS Ca2+ channel. No effect of repetitive activity was observed on 14 pS channel gating. At the whole-cell level, repetitive depolarizations dramatically increased the current observed. 7. Facilitation of 27 pS Ca2+ channel activity could be induced by changing the holding potential to a depolarized level (greater than or equal to -10 mV).(ABSTRACT TRUNCATED AT 400 WORDS)

Full text

PDF
213

Selected References

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

  1. Artalejo A. R., García A. G., Montiel C., Sánchez-García P. A dopaminergic receptor modulates catecholamine release from the cat adrenal gland. J Physiol. 1985 May;362:359–368. doi: 10.1113/jphysiol.1985.sp015683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Artalejo C. R., Ariano M. A., Perlman R. L., Fox A. P. Activation of facilitation calcium channels in chromaffin cells by D1 dopamine receptors through a cAMP/protein kinase A-dependent mechanism. Nature. 1990 Nov 15;348(6298):239–242. doi: 10.1038/348239a0. [DOI] [PubMed] [Google Scholar]
  3. Artalejo C. R., Dahmer M. K., Perlman R. L., Fox A. P. Two types of Ca2+ currents are found in bovine chromaffin cells: facilitation is due to the recruitment of one type. J Physiol. 1991 Jan;432:681–707. doi: 10.1113/jphysiol.1991.sp018406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ballesta J. J., Palmero M., Hidalgo M. J., Gutierrez L. M., Reig J. A., Viniegra S., Garcia A. G. Separate binding and functional sites for omega-conotoxin and nitrendipine suggest two types of calcium channels in bovine chromaffin cells. J Neurochem. 1989 Oct;53(4):1050–1056. doi: 10.1111/j.1471-4159.1989.tb07394.x. [DOI] [PubMed] [Google Scholar]
  5. Bean B. P. Classes of calcium channels in vertebrate cells. Annu Rev Physiol. 1989;51:367–384. doi: 10.1146/annurev.ph.51.030189.002055. [DOI] [PubMed] [Google Scholar]
  6. Bean B. Calcium channels. Gating for the physiologist. Nature. 1990 Nov 15;348(6298):192–193. doi: 10.1038/348192a0. [DOI] [PubMed] [Google Scholar]
  7. Brooks J. C. The isolated bovine adrenomedullary chromaffin cell: a model of neuronal excitation-secretion. Endocrinology. 1977 Nov;101(5):1369–1378. doi: 10.1210/endo-101-5-1369. [DOI] [PubMed] [Google Scholar]
  8. Callewaert G., Hanbauer I., Morad M. Modulation of calcium channels in cardiac and neuronal cells by an endogenous peptide. Science. 1989 Feb 3;243(4891):663–666. doi: 10.1126/science.2536955. [DOI] [PubMed] [Google Scholar]
  9. Chern Y. J., Kim K. T., Slakey L. L., Westhead E. W. Adenosine receptors activate adenylate cyclase and enhance secretion from bovine adrenal chromaffin cells in the presence of forskolin. J Neurochem. 1988 May;50(5):1484–1493. doi: 10.1111/j.1471-4159.1988.tb03034.x. [DOI] [PubMed] [Google Scholar]
  10. Douglas W. W., Rubin R. P. The mechanism of catecholamine release from the adrenal medulla and the role of calcium in stimulus-secretion coupling. J Physiol. 1963 Jul;167(2):288–310. doi: 10.1113/jphysiol.1963.sp007150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Fenwick E. M., Marty A., Neher E. Sodium and calcium channels in bovine chromaffin cells. J Physiol. 1982 Oct;331:599–635. doi: 10.1113/jphysiol.1982.sp014394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fox A. P., Nowycky M. C., Tsien R. W. Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones. J Physiol. 1987 Dec;394:149–172. doi: 10.1113/jphysiol.1987.sp016864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fox A. P., Nowycky M. C., Tsien R. W. Single-channel recordings of three types of calcium channels in chick sensory neurones. J Physiol. 1987 Dec;394:173–200. doi: 10.1113/jphysiol.1987.sp016865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Greenberg A., Zinder O. Alpha- and beta-receptor control of catecholamine secretion from isolated adrenal medulla cells. Cell Tissue Res. 1982;226(3):655–665. doi: 10.1007/BF00214792. [DOI] [PubMed] [Google Scholar]
  16. Hess P., Lansman J. B., Tsien R. W. Different modes of Ca channel gating behaviour favoured by dihydropyridine Ca agonists and antagonists. Nature. 1984 Oct 11;311(5986):538–544. doi: 10.1038/311538a0. [DOI] [PubMed] [Google Scholar]
  17. Hirning L. D., Fox A. P., McCleskey E. W., Olivera B. M., Thayer S. A., Miller R. J., Tsien R. W. Dominant role of N-type Ca2+ channels in evoked release of norepinephrine from sympathetic neurons. Science. 1988 Jan 1;239(4835):57–61. doi: 10.1126/science.2447647. [DOI] [PubMed] [Google Scholar]
  18. Hoshi T., Rothlein J., Smith S. J. Facilitation of Ca2+-channel currents in bovine adrenal chromaffin cells. Proc Natl Acad Sci U S A. 1984 Sep;81(18):5871–5875. doi: 10.1073/pnas.81.18.5871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hoshi T., Smith S. J. Large depolarization induces long openings of voltage-dependent calcium channels in adrenal chromaffin cells. J Neurosci. 1987 Feb;7(2):571–580. doi: 10.1523/JNEUROSCI.07-02-00571.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kokubun S., Reuter H. Dihydropyridine derivatives prolong the open state of Ca channels in cultured cardiac cells. Proc Natl Acad Sci U S A. 1984 Aug;81(15):4824–4827. doi: 10.1073/pnas.81.15.4824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lester H. A., Snutch T. P., Leonard J. P., Nargeot J., Dascal N., Curtis B. M., Davidson N. Expression of mRNA encoding voltage-dependent Ca channels in Xenopus oocytes. Review and progress report. Ann N Y Acad Sci. 1989;560:174–182. doi: 10.1111/j.1749-6632.1989.tb24094.x. [DOI] [PubMed] [Google Scholar]
  22. Llinás R. R., Sugimori M., Cherksey B. Voltage-dependent calcium conductances in mammalian neurons. The P channel. Ann N Y Acad Sci. 1989;560:103–111. doi: 10.1111/j.1749-6632.1989.tb24084.x. [DOI] [PubMed] [Google Scholar]
  23. Marriott D., Adams M., Boarder M. R. Effect of forskolin and prostaglandin E1 on stimulus secretion coupling in cultured bovine adrenal chromaffin cells. J Neurochem. 1988 Feb;50(2):616–623. doi: 10.1111/j.1471-4159.1988.tb02955.x. [DOI] [PubMed] [Google Scholar]
  24. Morita K., Dohi T., Kitayama S., Koyama Y., Tsujimoto A. Enhancement of stimulation-evoked catecholamine release from cultured bovine adrenal chromaffin cells by forskolin. J Neurochem. 1987 Jan;48(1):243–247. doi: 10.1111/j.1471-4159.1987.tb13154.x. [DOI] [PubMed] [Google Scholar]
  25. Nowycky M. C., Fox A. P., Tsien R. W. Long-opening mode of gating of neuronal calcium channels and its promotion by the dihydropyridine calcium agonist Bay K 8644. Proc Natl Acad Sci U S A. 1985 Apr;82(7):2178–2182. doi: 10.1073/pnas.82.7.2178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nowycky M. C., Fox A. P., Tsien R. W. Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature. 1985 Aug 1;316(6027):440–443. doi: 10.1038/316440a0. [DOI] [PubMed] [Google Scholar]
  27. Pietrobon D., Hess P. Novel mechanism of voltage-dependent gating in L-type calcium channels. Nature. 1990 Aug 16;346(6285):651–655. doi: 10.1038/346651a0. [DOI] [PubMed] [Google Scholar]
  28. Rosario L. M., Soria B., Feuerstein G., Pollard H. B. Voltage-sensitive calcium flux into bovine chromaffin cells occurs through dihydropyridine-sensitive and dihydropyridine- and omega-conotoxin-insensitive pathways. Neuroscience. 1989;29(3):735–747. doi: 10.1016/0306-4522(89)90145-0. [DOI] [PubMed] [Google Scholar]
  29. Tsien R. W., Lipscombe D., Madison D. V., Bley K. R., Fox A. P. Multiple types of neuronal calcium channels and their selective modulation. Trends Neurosci. 1988 Oct;11(10):431–438. doi: 10.1016/0166-2236(88)90194-4. [DOI] [PubMed] [Google Scholar]
  30. Wilson S. P. Vasoactive intestinal peptide elevates cyclic AMP levels and potentiates secretion in bovine adrenal chromaffin cells. Neuropeptides. 1988 Jan;11(1):17–21. doi: 10.1016/0143-4179(88)90023-6. [DOI] [PubMed] [Google Scholar]

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

RESOURCES