The Journal of General Physiology, Vol 99, 297-316, Copyright © 1992 by The Rockefeller University Press
Pseudo-streaming potentials in Necturus gallbladder epithelium. I. Paracellular origin of the transepithelial voltage changes
L Reuss, B Simon and Z Xi
Department of Physiology and Biophysics, University of Texas Medical Branch, Galveston 77550.
Apparent streaming potentials were elicited across Necturus gallbladder
epithelium by addition or removal of sucrose from the apical bathing
solution. In NaCl Ringer's solution, the transepithelial voltage (Vms)
change (reference, basolateral solution) was positive with sucrose addition
and negative with sucrose removal. Bilateral Cl- removal (cyclamate
replacement) had no effect on the polarity or magnitude of the Vms change
elicited by addition of 100 mM sucrose. In contrast, bilateral Na+ removal
(tetramethylammonium [TMA+] replacement) inverted the Vms change (from 2.7
+/- 0.3 to -3.2 +/- 0.2 mV). Replacement of Na+ and Cl- with TMA+ and
cyclamate, respectively, abolished the change in Vms. Measurements of cell
membrane voltages and relative resistances during osmotic challenges
indicate that changes in cell membrane parameters do not explain the
transepithelial voltage changes. The initial changes in Vms were slower
than expected from concomitant estimates of the time course of sucrose
concentration (and hence osmolality) at the membrane surface. Paired
recordings of the time courses of paracellular bi-ionic potentials (partial
substitution of apical Na+ with tetrabutylammonium [TBA+]) revealed much
faster time courses than those produced by sucrose addition, although the
diffusion coefficients of sucrose and TBACl are similar. Hyperosmotic and
hypoosmotic challenges yielded initial Vms changes at the same rate;
thereafter, the voltage increased with hypoosmotic solution and decreased
with hyperosmotic solution. These late voltage changes appear to result
from changes in width of the lateral intercellular spaces. The early time
courses of the Vms changes produced by osmotic challenge are inconsistent
with the expectations for water-ion flux coupling in the junctions. We
propose that they are pseudo-streaming potentials, i.e., junctional
diffusion potentials caused by salt concentration changes in the lateral
intercellular spaces secondary to osmotic water flow.