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. 1998 Aug;75(2):704–713. doi: 10.1016/S0006-3495(98)77560-5

The voltage-gating process of the voltage-dependent anion channel is sensitive to ion flow.

M Zizi 1, C Byrd 1, R Boxus 1, M Colombini 1
PMCID: PMC1299745  PMID: 9675172

Abstract

The voltage-dependent anion channel (VDAC) is a voltage-gated channel from the mitochondrial outer membrane. It has two gating processes: one at positive potentials and the other at negative potentials. The energetics of VDAC gating are quite different when measured in the presence or absence of an ion gradient. A positive potential on the high-salt side results in channel closure at lower transmembrane potentials. The midpoint potential (V0) shifted from 25 to 5.7 mV, with an activity gradient for KCl of 0.6 versus 0.06. The opposite occurred for negative potentials on the high-salt side (V0 shifted from -25 to -29 mV). Thus the salt gradient favored closure for one gating process and opening for the other. These results could be explained if part of the electrochemical potential of the gradients present were transferred to the gating mechanism. If the kinetic energy of the ion flow were coupled to the gating process, the effects of the gradient would depend on the mass and velocities of these ions. This was tested by using a series of different salts (KCl, NaCl, LiCl, KBr, K acetate, Na butyrate, and RbBr) under an identical activity gradient. The kinetic energy correlated very well with the measured shifts in free energy of the channel gating. This was true for both polarities. Thus the gating of VDAC is influenced by ion flow. These results are consistent in sign and direction with the voltage gating process in VDAC, which is believed to involve the movement of a positively charged portion of the wall of the channel out of the membrane.

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Selected References

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

  1. Colombini M. A candidate for the permeability pathway of the outer mitochondrial membrane. Nature. 1979 Jun 14;279(5714):643–645. doi: 10.1038/279643a0. [DOI] [PubMed] [Google Scholar]
  2. Colombini M. Characterization of channels isolated from plant mitochondria. Methods Enzymol. 1987;148:465–475. doi: 10.1016/0076-6879(87)48045-2. [DOI] [PubMed] [Google Scholar]
  3. Ehrenstein G., Lecar H., Nossal R. The nature of the negative resistance in bimolecular lipid membranes containing excitability-inducing material. J Gen Physiol. 1970 Jan;55(1):119–133. doi: 10.1085/jgp.55.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Mannella C. A. Structure of the outer mitochondrial membrane: ordered arrays of porelike subunits in outer-membrane fractions from Neurospora crassa mitochondria. J Cell Biol. 1982 Sep;94(3):680–687. doi: 10.1083/jcb.94.3.680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Merrill A. R., Cramer W. A. Identification of a voltage-responsive segment of the potential-gated colicin E1 ion channel. Biochemistry. 1990 Sep 18;29(37):8529–8534. doi: 10.1021/bi00489a004. [DOI] [PubMed] [Google Scholar]
  6. Montal M., Mueller P. Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. Proc Natl Acad Sci U S A. 1972 Dec;69(12):3561–3566. doi: 10.1073/pnas.69.12.3561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Peng S., Blachly-Dyson E., Forte M., Colombini M. Large scale rearrangement of protein domains is associated with voltage gating of the VDAC channel. Biophys J. 1992 Apr;62(1):123–135. doi: 10.1016/S0006-3495(92)81799-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Rosenberg P. A., Finkelstein A. Interaction of ions and water in gramicidin A channels: streaming potentials across lipid bilayer membranes. J Gen Physiol. 1978 Sep;72(3):327–340. doi: 10.1085/jgp.72.3.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Schein S. J., Colombini M., Finkelstein A. Reconstitution in planar lipid bilayers of a voltage-dependent anion-selective channel obtained from paramecium mitochondria. J Membr Biol. 1976 Dec 28;30(2):99–120. doi: 10.1007/BF01869662. [DOI] [PubMed] [Google Scholar]
  10. Thomas L., Blachly-Dyson E., Colombini M., Forte M. Mapping of residues forming the voltage sensor of the voltage-dependent anion-selective channel. Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5446–5449. doi: 10.1073/pnas.90.12.5446. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Thomas L., Kocsis E., Colombini M., Erbe E., Trus B. L., Steven A. C. Surface topography and molecular stoichiometry of the mitochondrial channel, VDAC, in crystalline arrays. J Struct Biol. 1991 Apr;106(2):161–171. doi: 10.1016/1047-8477(91)90085-b. [DOI] [PubMed] [Google Scholar]
  12. Zambrowicz E. B., Colombini M. Zero-current potentials in a large membrane channel: a simple theory accounts for complex behavior. Biophys J. 1993 Sep;65(3):1093–1100. doi: 10.1016/S0006-3495(93)81148-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Zimmerberg J., Parsegian V. A. Polymer inaccessible volume changes during opening and closing of a voltage-dependent ionic channel. Nature. 1986 Sep 4;323(6083):36–39. doi: 10.1038/323036a0. [DOI] [PubMed] [Google Scholar]

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