TY - JOUR
T1 - Extracellular charge adsorption influences intracellular electrochemical homeostasis in amphibian skeletal muscle
AU - Mehta, Arpan R
AU - Huang, Christopher L-H
AU - Skepper, Jeremy N
AU - Fraser, James A
N1 - © 2008 The Biophysical Society. Published by Elsevier Inc.
PY - 2008/6
Y1 - 2008/6
N2 - The membrane potential measured by intracellular electrodes, E(m), is the sum of the transmembrane potential difference (E(1)) between inner and outer cell membrane surfaces and a smaller potential difference (E(2)) between a volume containing fixed charges on or near the outer membrane surface and the bulk extracellular space. This study investigates the influence of E(2) upon transmembrane ion fluxes, and hence cellular electrochemical homeostasis, using an integrative approach that combines computational and experimental methods. First, analytic equations were developed to calculate the influence of charges constrained within a three-dimensional glycocalyceal matrix enveloping the cell membrane outer surface upon local electrical potentials and ion concentrations. Electron microscopy confirmed predictions of these equations that extracellular charge adsorption influences glycocalyceal volume. Second, the novel analytic glycocalyx formulation was incorporated into the charge-difference cellular model of Fraser and Huang to simulate the influence of extracellular fixed charges upon intracellular ionic homeostasis. Experimental measurements of E(m) supported the resulting predictions that an increased magnitude of extracellular fixed charge increases net transmembrane ionic leak currents, resulting in either a compensatory increase in Na(+)/K(+)-ATPase activity, or, in cells with reduced Na(+)/K(+)-ATPase activity, a partial dissipation of transmembrane ionic gradients and depolarization of E(m).
AB - The membrane potential measured by intracellular electrodes, E(m), is the sum of the transmembrane potential difference (E(1)) between inner and outer cell membrane surfaces and a smaller potential difference (E(2)) between a volume containing fixed charges on or near the outer membrane surface and the bulk extracellular space. This study investigates the influence of E(2) upon transmembrane ion fluxes, and hence cellular electrochemical homeostasis, using an integrative approach that combines computational and experimental methods. First, analytic equations were developed to calculate the influence of charges constrained within a three-dimensional glycocalyceal matrix enveloping the cell membrane outer surface upon local electrical potentials and ion concentrations. Electron microscopy confirmed predictions of these equations that extracellular charge adsorption influences glycocalyceal volume. Second, the novel analytic glycocalyx formulation was incorporated into the charge-difference cellular model of Fraser and Huang to simulate the influence of extracellular fixed charges upon intracellular ionic homeostasis. Experimental measurements of E(m) supported the resulting predictions that an increased magnitude of extracellular fixed charge increases net transmembrane ionic leak currents, resulting in either a compensatory increase in Na(+)/K(+)-ATPase activity, or, in cells with reduced Na(+)/K(+)-ATPase activity, a partial dissipation of transmembrane ionic gradients and depolarization of E(m).
KW - Adsorption
KW - Animals
KW - Anura/physiology
KW - Computer Simulation
KW - Extracellular Fluid/metabolism
KW - Homeostasis/physiology
KW - Ion Channels/physiology
KW - Membrane Potentials/physiology
KW - Models, Biological
KW - Muscle, Skeletal/physiology
UR - https://www.scopus.com/record/display.uri?eid=2-s2.0-44849138875&origin=inward
UR - https://dundee.primo.exlibrisgroup.com/discovery/fulldisplay?docid=cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_2480687&context=PC&vid=44DUN_INST:dun&lang=en&search_scope=MyInst_and_CI&adaptor=Primo%20Central&tab=Everything&query=any,contains,Extracellular%20charge%20adsorption%20influences%20intracellular%20electrochemical%20homeostasis%20in%20amphibian%20skeletal%20muscle
U2 - 10.1529/biophysj.107.128587
DO - 10.1529/biophysj.107.128587
M3 - Article
C2 - 18310253
SN - 0006-3495
VL - 94
SP - 4549
EP - 4560
JO - Biophysical Journal
JF - Biophysical Journal
IS - 11
ER -