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First published online November 17, 2006
Journal of Experimental Biology 209, 4701-4716 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02564

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A critical analysis of carbonic anhydrase function, respiratory gas exchange, and the acid-base control of secretion in the rectal gland of Squalus acanthias

Trevor J. Shuttleworth^1,2, Jill Thompson^1,2, R. Stephen Munger^2,3,4 and Chris M. Wood^2,4,*

¹ Department of Pharmacology and Physiology, University of Rochester School of Medicine and Dentistry, Rochester, NY 14642, USA
² Bamfield Marine Sciences Centre, 100 Pachena Drive, Bamfield, British Columbia, VOR 1BO, Canada
³ Canadian Nuclear Safety Commission, PO Box 1046, Station B, 280 Slater Street, Ottawa, Ontario, K1P 5S9, Canada
⁴ Department of Biology, McMaster University, 1280 Main St. West, Hamilton, Ontario, L8S 4K1, Canada

^* Author for correspondence (e-mail: woodcm{at}mcmaster.ca)

Accepted 27 September 2006

We compared in vivo responses of rectal gland secretion to carbonic anhydrase (CA) inhibition (10^-4 mol l^-1 acetazolamide) in volume-loaded dogfish with in vitro responses in an isolated-perfused gland stimulated with 5x10^-6 mol l^-1 forskolin and removed from systemic influences. We also measured respiratory gas exchange in the perfused gland, described the acid-base status of the secreted fluid, and determined the relative importance of various extracellular and intracellular acid-base parameters in controlling rectal gland secretion in vitro. In vivo, acetazolamide inhibited Cl^- secretion and decreased pHi in the rectal gland, but interpretation was confounded by an accompanying systemic respiratory acidosis, which would also have contributed to the inhibition. In the perfused gland, and increased in linear relation to increases in Cl^- secretion rate. CA inhibition (10^-4 mol l^-1 acetazolamide) had no effect on Cl^- secretion rate or pHi in the perfused gland, in contrast to in vivo, but caused a transitory 30% inhibition of (relative to stable ) and elevation in secretion P_CO2 effects, which peaked at 2 h and attenuated by 3.5-4 h. Secretion was inhibited by acidosis and stimulated by alkalosis; the relationship between relative Cl^- secretion rate and pHe was almost identical to that seen in vivo. Experimental manipulations of perfusate pH, P_CO2 and HCO₃^- concentration, together with measurements of pHi, demonstrated that these responses were most strongly correlated with changes in pHe, and were not related to changes in P_CO2, extracellular HCO₃^-, or intracellular HCO₃^- levels, though changes in pHi may also have played a role. The acid-base status of the secreted fluid varied with that of the perfusate, secretion pH remaining about 0.3-0.5 units lower, and changing in concert with pHe rather than pHi; secretion HCO₃^- concentrations remained low, even in the face of greatly elevated perfusate HCO₃^- concentrations. We conclude that pH effects on rectal gland secretion rate are adaptive, that CA functions to catalyze the hydration of CO₂, thereby maintaining a gradient for diffusive efflux of CO₂ from the working cells, and that differences in response to CA inhibition likely reflect the higher perfusion-to-secretion ratio in vitro than in vivo.

Key words: chloride secretion, O₂ consumption, CO₂ excretion, gas exchange ratio, pHi, pHe, acidosis, alkalosis, shark, acetazolamide

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