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Journal of Experimental Biology, Vol 172, Issue 1 289-309, Copyright © 1992 by Company of Biologists
JOURNAL ARTICLES |
BJ Harvey
Departement de Biologie Cellulaire et Moleculaire, Commissariat a l'Energie Atomique, Laboratoire Jean Maetz, Villefranche-sur-mer, France.
The frog skin in vivo is capable of active transepithelial H+ secretion (JH) which is matched by Na+ absorption (JNa). Studies in vitro demonstrate that JH is generated by an H(+)-ATPase pump localized in apical membranes of mitochondria-rich (MR) cells, whereas JNa occurs through an amiloride-sensitive pathway in principal (P) cells. The H+ pump is sensitive to inhibitors of carbonic anhydrase (e.g. acetazolamide) and to specific inhibitors of mitochondrial F1F0 H(+)-ATPase (oligomycin) and vacuolar (V)-type H(+)-ATPase (N-ethylmaleimide) and to inhibitors of both these types of H(+)-ATPases (dicyclohexylcarbodiimide, DCCD). JH is independent of external K+, which differentiates it from gastric H+/K(+)-ATPase and is strictly dependent on aerobic metabolism. The proton pump is primarily implicated in whole-body acid-base regulation. Acute stimulation of JH in response (seconds-minutes) to an acid load involves insertion of H+ pumps (exocytosis) from a cytosolic pool into the apical membrane. The chronic response (days) to metabolic acid load involves morphological changes (increased apical membrane surface area and number of MR cells). Whole-cell patch-clamp recordings of membrane capacitance and current fluctuations from MR cells demonstrate that a respiratory acid load and aldosterone produce rapid exocytotic insertion of DCCD-sensitive conductive membrane. A secondary role of the H+ pump is to energize sodium absorption (JNa) via principal cells from dilute solutions in the absence of a permeant anion under open-circuit conditions. The apparent 1:1 stoichiometry between JH and JNa is a result of transepithelial electrical coupling between these electrogenic fluxes. The H+ pump in MR cells generates a transepithelial current (serosa to apical) which acts as a physiological voltage-clamp to hyperpolarize the apical membrane of P cells. This hyperpolarization can facilitate passive Na+ entry across the apical membrane against a threefold chemical gradient. Since both JH and JNa are sensitive to membrane potential, inhibition or activation of one will produce similar effects on the transport of the other ion. For example, inhibition of JH by ethoxzolamide will reduce JNa. Conversely, blocking JNa with amiloride also inhibits JH. These effects can be avoided or reversed if variations in membrane potential are prevented by voltage-clamping the epithelium. A paradoxical activation of JNa is observed when JH is stimulated by an acid load (CO2), despite inhibition of Na+ channel activity by H+ in P cells.(ABSTRACT TRUNCATED AT 400 WORDS)
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