Abstract
Calcium ions affect the gating of Ca currents. Surface charge is involved but to what extent is unknown. We have examined this, using isolated nerve cell bodies of Helix aspersa and the combined microelectrode-suction pipette method for voltage-clamp and internal perfusion. We found that Ba and Sr currents produced by substitution of these ions for extracellular Ca ions are activated at less positive potentials than Ca currents. Mg ions do not permeate the Ca channel and changes in [Mg]o produce shifts in the activation-potential curves that are comparable to the effects of changes in [Ba]o or [Sr]o. Inactivation of Ba currents also occurs at less positive potentials. Perfusion intracellularly with EGTA reduced inactivation of Ca currents as a function of potential, but did not shift the inactivation-potential curve. Hence, Ca current-dependent inactivation which is blocked by intracellular EGTA probably does not involve a similar change of intracellular surface potential. The voltage shifts of activation and inactivation produced by extracellular divalent cations used singly or in mixtures can be described by the Gouy-Chapman theory for the diffuse double layer with binding (Gilbert & Ehrenstein, 1969; McLaughlin, Szabo & Eisenman, 1971). From the surface potential values and the Boltzman distribution, we have computed surface concentrations that predict the following experimental observations: 1) saturation of current-concentration relationships when surface potential is changing maximally; 2) the increase in peak current when Ca ions are replaced by Sr or Ba ions; and 3) the greater inhibitory effect of Mg on IBa than ICa. Theory indicates that surface charge cannot be screened completely even at 1 M [Mg]o and thus that Ca channel properties must be evaluated in the light of surface charge effects. For example, after correction for surface charge effects the relative permeabilities of Ca, Ba and Sr ions are equivalent. In the presence of Co ions, however, Ca ions are more permeable than Ba ions suggesting a channel binding site may be involved.
MeSH Terms
Animals
Biological Transport, Active
Biotransformation
Calcium/physiology
Helix, Snails/metabolism
In Vitro Techniques
Ion Channels/metabolism
Magnesium/pharmacology
Membrane Potentials
Neurons/metabolism
Surface Properties
Chemicals
Ion Channels
Magnesium
Calcium
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Wilson D L
Morimoto K
Tsuda Y
Brown A M
References (31)
31 references, click to expand
-
Magnitude and location of surface charges on Myxicola giant axons.
J Gen Physiol. 1975 Jul;66(1):47-65
PMID: 1159402
-
Interactions of divalent cations with negatively charged membrane surfaces. I. Discrete charge potential.
J Theor Biol. 1979 Nov 21;81(2):157-79
PMID: 537365
-
Calcium current-dependent and voltage-dependent inactivation of calcium channels in Helix aspersa.
J Physiol. 1981 Nov;320:193-218
PMID: 6275075
-
Surface potential reflected in both gating and permeation mechanisms of sodium and calcium channels of the tunicate egg cell membrane.
J Physiol. 1977 May;267(2):429-63
PMID: 17734
-
The calcium current of Helix neuron.
J Gen Physiol. 1978 May;71(5):509-31
PMID: 660160
-
Calcium-mediated inactivation of calcium current in Paramecium.
J Physiol. 1980 Sep;306:193-203
PMID: 6257894
-
Calcium inward current and related charge movements in the membrane of snail neurones.
J Physiol. 1981 Jan;310:403-21
PMID: 6262506
-
Discrete membrane surface charge distributions. Effect of fluctuations near individual channels.
Biophys J. 1978 Dec;24(3):869-75
PMID: 737290
-
Adsorption of monovalent cations to bilayer membranes containing negative phospholipids.
Biochemistry. 1979 Nov 13;18(23):5213-23
PMID: 115493
-
Calcium channel.
Annu Rev Neurosci. 1981;4:69-125
PMID: 6261668
-
Calcium currents in internally perfused nerve cell bodies of Limnea stagnalis.
J Physiol. 1982 Jan;322:503-28
PMID: 7069629
-
The suction pipette method for internal perfusion and voltage clamp of small excitable cells.
J Neurosci Methods. 1980 Feb;2(1):51-78
PMID: 7329091
-
A quantitative description of membrane current and its application to conduction and excitation in nerve.
J Physiol. 1952 Aug;117(4):500-44
PMID: 12991237
-
Potassium activation associated with intraneuronal free calcium.
Science. 1978 Apr 28;200(4340):437-9
PMID: 644308
-
Adsorption of divalent cations to bilayer membranes containing phosphatidylserine.
J Gen Physiol. 1981 Apr;77(4):445-73
PMID: 7241089
-
Effect of divalent cations on potassium conductance of squid axons: determination of surface charge.
Biophys J. 1969 Mar;9(3):447-63
PMID: 5780717
-
Ionic selectivity, saturation, and block in sodium channels. A four-barrier model.
J Gen Physiol. 1975 Nov;66(5):535-60
PMID: 1194886
-
Effect of surface charge on the steady-state potassium conductance of nodal membrane.
Nature. 1970 Oct 10;228(5267):164-5
PMID: 5460015
-
Inactivation of Ca conductance dependent on entry of Ca ions in molluscan neurons.
Proc Natl Acad Sci U S A. 1979 Mar;76(3):1497-500
PMID: 286336
-
Effects of internal divalent cations on voltage-clamped squid axons.
J Gen Physiol. 1974 Jun;63(6):675-89
PMID: 4829524
-
Membrane surface charge: discrete and uniform modelling.
Prog Biophys Mol Biol. 1974;28:341-70
PMID: 4617249
-
The action of calcium on the electrical properties of squid axons.
J Physiol. 1957 Jul 11;137(2):218-44
PMID: 13449874
-
Divalent ions and the surface potential of charged phospholipid membranes.
J Gen Physiol. 1971 Dec;58(6):667-87
PMID: 5120393
-
The electrical double layer and the theory of electrocapillarity.
Chem Rev. 1947 Dec;41(3):441-501
PMID: 18895519
-
Calcium currents in snail neurones. II. The effect of external calcium concentration on the calcium inward current.
Pflugers Arch. 1974 Apr 11;348(2):95-104
PMID: 4859233
-
Effects of surface charge on the conductance of the gramicidin channel.
Biochim Biophys Acta. 1979 Apr 19;552(3):369-78
PMID: 87221
-
Negative surface charge near sodium channels of nerve: divalent ions, monovalent ions, and pH.
Philos Trans R Soc Lond B Biol Sci. 1975 Jun 10;270(908):301-18
PMID: 238230
-
Calcium ionic channels in electrically excitable membrane.
Neuroscience. 1980;5(6):945-59
PMID: 6250097
-
Sodium permeability in toad nerve and in squid nerve.
J Physiol. 1960 Jun;152:159-66
PMID: 13824559
-
The effect of changing the internal solution on sodium inactivation and related phenomena in giant axons.
J Physiol. 1965 Oct;180(4):821-36
PMID: 5880364
-
Ionic currents through the membrane of the mammalian oocyte and their comparison with those in the tunicate and sea urchin.
J Physiol. 1977 May;267(2):465-95
PMID: 559759