Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 2001 Mar;80(3):1220–1229. doi: 10.1016/S0006-3495(01)76098-5

Voltage-dependent membrane capacitance in rat pituitary nerve terminals due to gating currents.

G Kilic 1, M Lindau 1
PMCID: PMC1301317  PMID: 11222286

Abstract

We investigated the voltage dependence of membrane capacitance of pituitary nerve terminals in the whole-terminal patch-clamp configuration using a lock-in amplifier. Under conditions where secretion was abolished and voltage-gated channels were blocked or completely inactivated, changes in membrane potential still produced capacitance changes. In terminals with significant sodium currents, the membrane capacitance showed a bell-shaped dependence on membrane potential with a peak at approximately -40 mV as expected for sodium channel gating currents. The voltage-dependent part of the capacitance showed a strong correlation with the amplitude of voltage-gated Na+ currents and was markedly reduced by dibucaine, which blocks sodium channel current and gating charge movement. The frequency dependence of the voltage-dependent capacitance was consistent with sodium channel kinetics. This is the first demonstration of sodium channel gating currents in single pituitary nerve terminals. The gating currents lead to a voltage- and frequency-dependent capacitance, which can be well resolved by measurements with a lock-in amplifier. The properties of the gating currents are in excellent agreement with the properties of ionic Na+ currents of pituitary nerve terminals.

Full Text

The Full Text of this article is available as a PDF (109.8 KB).

Selected References

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

  1. Adrian R. H., Almers W. The voltage dependence of membrane capacity. J Physiol. 1976 Jan;254(2):317–338. doi: 10.1113/jphysiol.1976.sp011234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Almers W., McCleskey E. W. Non-selective conductance in calcium channels of frog muscle: calcium selectivity in a single-file pore. J Physiol. 1984 Aug;353:585–608. doi: 10.1113/jphysiol.1984.sp015352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Armstrong C. M., Bezanilla F. Charge movement associated with the opening and closing of the activation gates of the Na channels. J Gen Physiol. 1974 May;63(5):533–552. doi: 10.1085/jgp.63.5.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Armstrong C. M., Bezanilla F. Currents related to movement of the gating particles of the sodium channels. Nature. 1973 Apr 13;242(5398):459–461. doi: 10.1038/242459a0. [DOI] [PubMed] [Google Scholar]
  5. Armstrong C. M., Bezanilla F. Inactivation of the sodium channel. II. Gating current experiments. J Gen Physiol. 1977 Nov;70(5):567–590. doi: 10.1085/jgp.70.5.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Austin R. H., Beeson K. W., Eisenstein L., Frauenfelder H., Gunsalus I. C. Dynamics of ligand binding to myoglobin. Biochemistry. 1975 Dec 2;14(24):5355–5373. doi: 10.1021/bi00695a021. [DOI] [PubMed] [Google Scholar]
  7. Bezanilla F., Perozo E., Papazian D. M., Stefani E. Molecular basis of gating charge immobilization in Shaker potassium channels. Science. 1991 Nov 1;254(5032):679–683. doi: 10.1126/science.1948047. [DOI] [PubMed] [Google Scholar]
  8. Bezanilla F., Taylor R. E., Fernández J. M. Distribution and kinetics of membrane dielectric polarization. 1. Long-term inactivation of gating currents. J Gen Physiol. 1982 Jan;79(1):21–40. doi: 10.1085/jgp.79.1.21. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bielefeldt K., Rotter J. L., Jackson M. B. Three potassium channels in rat posterior pituitary nerve terminals. J Physiol. 1992 Dec;458:41–67. doi: 10.1113/jphysiol.1992.sp019405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cazalis M., Dayanithi G., Nordmann J. J. Hormone release from isolated nerve endings of the rat neurohypophysis. J Physiol. 1987 Sep;390:55–70. doi: 10.1113/jphysiol.1987.sp016686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Debus K., Hartmann J., Kilic G., Lindau M. Influence of conductance changes on patch clamp capacitance measurements using a lock-in amplifier and limitations of the phase tracking technique. Biophys J. 1995 Dec;69(6):2808–2822. doi: 10.1016/S0006-3495(95)80154-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fernández J. M., Bezanilla F., Taylor R. E. Distribution and kinetics of membrane dielectric polarization. II. Frequency domain studies of gating currents. J Gen Physiol. 1982 Jan;79(1):41–67. doi: 10.1085/jgp.79.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fernández J. M., Taylor R. E., Bezanilla F. Induced capacitance in the squid giant axon. Lipophilic ion displacement currents. J Gen Physiol. 1983 Sep;82(3):331–346. doi: 10.1085/jgp.82.3.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gilly W. F., Armstrong C. M. Gating current and potassium channels in the giant axon of the squid. Biophys J. 1980 Mar;29(3):485–492. doi: 10.1016/S0006-3495(80)85147-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Giovannucci D. R., Stuenkel E. L. Regulation of secretory granule recruitment and exocytosis at rat neurohypophysial nerve endings. J Physiol. 1997 Feb 1;498(Pt 3):735–751. doi: 10.1113/jphysiol.1997.sp021898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Horrigan F. T., Bookman R. J. Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron. 1994 Nov;13(5):1119–1129. doi: 10.1016/0896-6273(94)90050-7. [DOI] [PubMed] [Google Scholar]
  17. Hsu S. F., Jackson M. B. Rapid exocytosis and endocytosis in nerve terminals of the rat posterior pituitary. J Physiol. 1996 Jul 15;494(Pt 2):539–553. doi: 10.1113/jphysiol.1996.sp021512. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jackson M. B., Zhang S. J. Action potential propagation and propagation block by GABA in rat posterior pituitary nerve terminals. J Physiol. 1995 Mar 15;483(Pt 3):597–611. doi: 10.1113/jphysiol.1995.sp020609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kilic G., Stolpe A., Lindau M. A slowly activating voltage-dependent K+ current in rat pituitary nerve terminals. J Physiol. 1996 Dec 15;497(Pt 3):711–725. doi: 10.1113/jphysiol.1996.sp021802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lemos J. R., Nowycky M. C. Two types of calcium channels coexist in peptide-releasing vertebrate nerve terminals. Neuron. 1989 May;2(5):1419–1426. doi: 10.1016/0896-6273(89)90187-6. [DOI] [PubMed] [Google Scholar]
  21. Lim N. F., Nowycky M. C., Bookman R. J. Direct measurement of exocytosis and calcium currents in single vertebrate nerve terminals. Nature. 1990 Mar 29;344(6265):449–451. doi: 10.1038/344449a0. [DOI] [PubMed] [Google Scholar]
  22. Lindau M., Neher E. Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflugers Arch. 1988 Feb;411(2):137–146. doi: 10.1007/BF00582306. [DOI] [PubMed] [Google Scholar]
  23. Lindau M., Stuenkel E. L., Nordmann J. J. Depolarization, intracellular calcium and exocytosis in single vertebrate nerve endings. Biophys J. 1992 Jan;61(1):19–30. doi: 10.1016/S0006-3495(92)81812-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lindau M. Time-resolved capacitance measurements: monitoring exocytosis in single cells. Q Rev Biophys. 1991 Feb;24(1):75–101. doi: 10.1017/s0033583500003279. [DOI] [PubMed] [Google Scholar]
  25. Neher E., Marty A. Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6712–6716. doi: 10.1073/pnas.79.21.6712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sigg D., Qian H., Bezanilla F. Kramers' diffusion theory applied to gating kinetics of voltage-dependent ion channels. Biophys J. 1999 Feb;76(2):782–803. doi: 10.1016/S0006-3495(99)77243-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Taylor R. E., Bezanilla F. Comments on the measurement of gating currents in the frequency domain. Biophys J. 1979 May;26(2):338–340. doi: 10.1016/S0006-3495(79)85255-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Thorn P. J., Wang X. M., Lemos J. R. A fast, transient K+ current in neurohypophysial nerve terminals of the rat. J Physiol. 1991 Jan;432:313–326. doi: 10.1113/jphysiol.1991.sp018386. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Wang G., Dayanithi G., Kim S., Hom D., Nadasdi L., Kristipati R., Ramachandran J., Stuenkel E. L., Nordmann J. J., Newcomb R. Role of Q-type Ca2+ channels in vasopressin secretion from neurohypophysial terminals of the rat. J Physiol. 1997 Jul 15;502(Pt 2):351–363. doi: 10.1111/j.1469-7793.1997.351bk.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wang G., Dayanithi G., Newcomb R., Lemos J. R. An R-type Ca(2+) current in neurohypophysial terminals preferentially regulates oxytocin secretion. J Neurosci. 1999 Nov 1;19(21):9235–9241. doi: 10.1523/JNEUROSCI.19-21-09235.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wang G., Thorn P., Lemos J. R. A novel large-conductance Ca(2+)-activated potassium channel and current in nerve terminals of the rat neurohypophysis. J Physiol. 1992 Nov;457:47–74. doi: 10.1113/jphysiol.1992.sp019364. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wang X., Treistman S. N., Lemos J. R. Two types of high-threshold calcium currents inhibited by omega-conotoxin in nerve terminals of rat neurohypophysis. J Physiol. 1992 Jan;445:181–199. doi: 10.1113/jphysiol.1992.sp018919. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES