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Electrophysiology of Gastric Ion Transport

Jeffrey R. Demarest, Terry E. Machen

10.1002/cphy.cp060310

Source: Supplement 18: Handbook of Physiology, The Gastrointestinal System, Salivary, Gastric, Pancreatic, and Hepatobiliary Secretion

Originally published: 1989

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Structure of Gastric Mucosa
2 Voltage, Current, Ionic Flux, and Resistance
3 Membrane Permeability and Transport Properties
3.1 Cation and Anion Requirements for Acid Secretion
3.2 Sodium Absorption by Surface Cells and Chloride Secretion by Oxyntic Cells
3.3 Potassium Transport
3.4 Bicarbonate Secretion
3.5 Cell Membrane Potentials and Intracellular Ion Activities
3.6 Equivalent Circuit Analysis With Microelectrodes
3.7 Equivalent Circuit Analysis from Impedance Measurements
3.8 Segregation of Transport Functions and Associated Shunt Pathways
3.9 Electroneutral Hydrogen and Electrogenic Chloride Transport by Oxyntic Cells
4 Summary
Figure 1. Figure 1.

Vibrating‐probe measurement of current emerging from a surface epithelial cell (SEC) during control conditions and during amiloride 10−6 M, mucosal) treatment. Height of probe above epithelium (measured to midpoint of probe's excursion) and open‐circuit (OC) or short‐circuit (SC) conditions are indicated across top. Black bars, time periods when transepithelial voltage was clamped to ‐20 mV, mucosal negative. Resistance of this SEC (including the shunt pathway) was ∼5,000 Ω·cm2 20 mV·4 μA−1·cm−2) during control conditions and 15,000 Ω·cm2 20 mV·1.33 μA−1·cm−2) during amiloride treatment.

From Demarest et al. 25
Figure 2. Figure 2.

Example of a basolateral impalement of an oxyntic cell (OC) in a stimulated (.1 mM histamine) mucosa. Record starts with microelectrode in serosal bath registering a potential of 0 mV (lower trace). IN arrow, OC was impaled, and basolateral membrane potential (Vcs) of ‐62 mV was recorded. Upper trace, transepithelial potential (Vms) of ‐38 mV prior to impalement and apical membrane potential (Vmc) (= Vms ‐ Vcs) of 24 mV after impalement. Repeated downward deflections in traces were due to transepithelial current pulses (amplitude = 20 μA/cm2; duration = 1 s; frequency = 12/min) used to determine transepithelial resistance, RT = ΔVms·20 μA−1·cm−2, and ratio of apical to basolateral membrane resistances, Ra/Rb = ΔVmc/ΔVcs. At ∼45 s after impalement, serosal solution [K+] was raised from 5 to 50 mM (black bar), causing a rapid and reversible depolarization of both membrane potentials and a decrease in relative resistance of the basolateral membrane, i.e., an increase in Ra/Rb. After return to 5 mM serosal [K+], microelectrode was withdrawn from cell at OUT arrow.

From Demarest and Machen 22
Figure 3. Figure 3.

Time course of stimulation followed continuously in a single OC in each of 5 mucosae. Values for time 0 were determined immediately before switching serosal superfusate to a superfusate containing 0.1 mM histamine. Vms and Vcs, transepithelial and basolateral membrane potential differences referred to serosal solution. Rt, transepithelial resistance; Rs/Rb, ratio of apical to basolateral membrane resistances. *, P < 0.05; **, P < 0.005; ***, P < 0.001.

From Demarest and Machen 22
Figure 4. Figure 4.

Equivalent circuit models of epithelia. M, mucosal compartment; C, cellular compartment; S, serosal compartment. Apical and basolateral cell membranes are represented by electromotive forces Ea and Eb, in series with resistances Ra and Rb. Rs, shunt pathway; electromotive force across this resistance was assumed to be 0. Horizontal dashed lines connect transepithelial (Vms), apical (Vmc), and basolateral (Vcs) membrane potentials to points in circuit from which they are measured. Curved arrow, current (Ic) that circulates within epithelium under open‐circuit conditions. A: simple circuit for flat epithelium with only 1 cell type. B: more realistic circuit for gastric mucosa that represents 2 cell types (oc, oxyntic cells; sec, surface epithelial cells, each with a paracellular shunt).
Figure 5. Figure 5.

Models for H+ and Cl− transport by secreting (A) and resting (B) OC. Apical membrane contains H+‐K+ pump and conductive pathways for K+ and Cl−. Basolateral membrane contains Na+‐K+ pump, K+ conductance, and separate Na+‐H+ and Cl−‐HCO3− exchangers (ex). Mechanisms surrounded with dotted lines in A can account for HCl secretion by stimulated OC; mechanisms surrounded with dotted lines in B can account for Cl secretion by resting OC.

From Reenstra et al. 89
Figure 6. Figure 6.

Ion‐transport pathways in SEC and OC. Filled circles, ATP‐driven pumps (Na+‐K+‐ and H+‐K+‐ATPases). Open circles, coupled exchangers (Na+‐H+ and Cl−‐HCO3−). Open cylinders, conductance channels (K+ and Cl−). Known intracellular concentrations and effects of inhibitors are indicated. Value for [Na+]i in SEC is taken from unpublished measurements by T. Zeuthen and T. E. Machen.


Figure 1.

Vibrating‐probe measurement of current emerging from a surface epithelial cell (SEC) during control conditions and during amiloride 10−6 M, mucosal) treatment. Height of probe above epithelium (measured to midpoint of probe's excursion) and open‐circuit (OC) or short‐circuit (SC) conditions are indicated across top. Black bars, time periods when transepithelial voltage was clamped to ‐20 mV, mucosal negative. Resistance of this SEC (including the shunt pathway) was ∼5,000 Ω·cm2 20 mV·4 μA−1·cm−2) during control conditions and 15,000 Ω·cm2 20 mV·1.33 μA−1·cm−2) during amiloride treatment.

From Demarest et al. 25


Figure 2.

Example of a basolateral impalement of an oxyntic cell (OC) in a stimulated (.1 mM histamine) mucosa. Record starts with microelectrode in serosal bath registering a potential of 0 mV (lower trace). IN arrow, OC was impaled, and basolateral membrane potential (Vcs) of ‐62 mV was recorded. Upper trace, transepithelial potential (Vms) of ‐38 mV prior to impalement and apical membrane potential (Vmc) (= Vms ‐ Vcs) of 24 mV after impalement. Repeated downward deflections in traces were due to transepithelial current pulses (amplitude = 20 μA/cm2; duration = 1 s; frequency = 12/min) used to determine transepithelial resistance, RT = ΔVms·20 μA−1·cm−2, and ratio of apical to basolateral membrane resistances, Ra/Rb = ΔVmc/ΔVcs. At ∼45 s after impalement, serosal solution [K+] was raised from 5 to 50 mM (black bar), causing a rapid and reversible depolarization of both membrane potentials and a decrease in relative resistance of the basolateral membrane, i.e., an increase in Ra/Rb. After return to 5 mM serosal [K+], microelectrode was withdrawn from cell at OUT arrow.

From Demarest and Machen 22


Figure 3.

Time course of stimulation followed continuously in a single OC in each of 5 mucosae. Values for time 0 were determined immediately before switching serosal superfusate to a superfusate containing 0.1 mM histamine. Vms and Vcs, transepithelial and basolateral membrane potential differences referred to serosal solution. Rt, transepithelial resistance; Rs/Rb, ratio of apical to basolateral membrane resistances. *, P < 0.05; **, P < 0.005; ***, P < 0.001.

From Demarest and Machen 22


Figure 4.

Equivalent circuit models of epithelia. M, mucosal compartment; C, cellular compartment; S, serosal compartment. Apical and basolateral cell membranes are represented by electromotive forces Ea and Eb, in series with resistances Ra and Rb. Rs, shunt pathway; electromotive force across this resistance was assumed to be 0. Horizontal dashed lines connect transepithelial (Vms), apical (Vmc), and basolateral (Vcs) membrane potentials to points in circuit from which they are measured. Curved arrow, current (Ic) that circulates within epithelium under open‐circuit conditions. A: simple circuit for flat epithelium with only 1 cell type. B: more realistic circuit for gastric mucosa that represents 2 cell types (oc, oxyntic cells; sec, surface epithelial cells, each with a paracellular shunt).



Figure 5.

Models for H+ and Cl− transport by secreting (A) and resting (B) OC. Apical membrane contains H+‐K+ pump and conductive pathways for K+ and Cl−. Basolateral membrane contains Na+‐K+ pump, K+ conductance, and separate Na+‐H+ and Cl−‐HCO3− exchangers (ex). Mechanisms surrounded with dotted lines in A can account for HCl secretion by stimulated OC; mechanisms surrounded with dotted lines in B can account for Cl secretion by resting OC.

From Reenstra et al. 89


Figure 6.

Ion‐transport pathways in SEC and OC. Filled circles, ATP‐driven pumps (Na+‐K+‐ and H+‐K+‐ATPases). Open circles, coupled exchangers (Na+‐H+ and Cl−‐HCO3−). Open cylinders, conductance channels (K+ and Cl−). Known intracellular concentrations and effects of inhibitors are indicated. Value for [Na+]i in SEC is taken from unpublished measurements by T. Zeuthen and T. E. Machen.

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Article Title: Electrophysiology of Gastric Ion Transport
 

How to Cite

Jeffrey R. Demarest, Terry E. Machen. Electrophysiology of Gastric Ion Transport. Compr Physiol 2011, Supplement 18: Handbook of Physiology, The Gastrointestinal System, Salivary, Gastric, Pancreatic, and Hepatobiliary Secretion: 185-205. First published in print 1989. doi: 10.1002/cphy.cp060310