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, Jill Thompson, R. Stephen Munger, Chris M. Wood

Research output: Contribution to journalArticle

15 Scopus citations

Abstract

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 5×10-6 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, ṀCO2 and ṀO2 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 ṀCO2 (relative to stable ṀO2) and elevation in secretion PCO2 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, PCO2 and HCO 3- 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 PCO2 extracellular HCO 3-, 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.

Original languageEnglish (US)
Pages (from-to)4701-4716
Number of pages16
JournalJournal of Experimental Biology
Volume209
Issue number23
DOIs
StatePublished - Dec 1 2006
Externally publishedYes

Keywords

  • Acetazolamide
  • Acidosis
  • Alkalosis
  • Chloride secretion
  • CO excretion
  • Gas exchange ratio
  • O consumption
  • pHe
  • pHi
  • Shark

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Agricultural and Biological Sciences (miscellaneous)

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