Portal de Periódicos da CAPES

Mechanisms of acid-base excretion across the gills of a marine fish

1997; Wiley; Volume: 279; Issue: 5 Linguagem: Inglês

10.1002/(sici)1097-010x(19971201)279

1097-010X

James B. Claiborne, Erin Perry, Shenna Bellows, J. Campbell,

Environmental Toxicology and Ecotoxicology

Journal of Experimental ZoologyVolume 279, Issue 5 p. 509-520 Comparative Physiology and Biochemistry Mechanisms of acid-base excretion across the gills of a marine fish James B. Claiborne, Corresponding Author James B. Claiborne [email protected] Department of Biology, Georgia Southern University, Statesboro, Georgia 30460 The Mount Desert Island Biological Laboratory, Salsbury Cove, Maine 04672Department of Biology, Georgia Southern University, Statesboro, GA 30460===Search for more papers by this authorErin Perry, Erin Perry The Mount Desert Island Biological Laboratory, Salsbury Cove, Maine 04672Search for more papers by this authorShenna Bellows, Shenna Bellows The Mount Desert Island Biological Laboratory, Salsbury Cove, Maine 04672Search for more papers by this authorJennifer Campbell, Jennifer Campbell Department of Biology, Georgia Southern University, Statesboro, Georgia 30460 The Mount Desert Island Biological Laboratory, Salsbury Cove, Maine 04672Search for more papers by this author James B. Claiborne, Corresponding Author James B. Claiborne [email protected] Department of Biology, Georgia Southern University, Statesboro, Georgia 30460 The Mount Desert Island Biological Laboratory, Salsbury Cove, Maine 04672Department of Biology, Georgia Southern University, Statesboro, GA 30460===Search for more papers by this authorErin Perry, Erin Perry The Mount Desert Island Biological Laboratory, Salsbury Cove, Maine 04672Search for more papers by this authorShenna Bellows, Shenna Bellows The Mount Desert Island Biological Laboratory, Salsbury Cove, Maine 04672Search for more papers by this authorJennifer Campbell, Jennifer Campbell Department of Biology, Georgia Southern University, Statesboro, Georgia 30460 The Mount Desert Island Biological Laboratory, Salsbury Cove, Maine 04672Search for more papers by this author First published: 07 December 1998 https://doi.org/10.1002/(SICI)1097-010X(19971201)279:5 3.0.CO;2-2Citations: 24AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Abstract Na+/H+ and Cl–/HCO3–exchanges in the branchial epithelium are thought to be primarily responsible for acid-base transfers in fish. Several different cellular mechanisms have been proposed to drive these exchanges in fresh water and marine species. We measured the acid-base balance and net H+ transfers (ΔH+) in the marine long-horned sculpin (Myoxocephalus octodecimspinosus) following acidosis. ΔH+ was determined in different groups of acid loaded (2–3 meq kg–1) animals which were: 1) adapted to seawater (SW); 2) adapted to 20% SW; 3) exposed to water with artificially low [Na+] or [Cl–]; 4) exposed to water containing 1 × 10–4 M amiloride, 5-(N,N-hexamethylene)-amiloride (HMA), or 4,4′-diisothiocyanatostilbene-2,2′-disulfonic acid (DIDS). Both seawater and 20% SW adapted fish were able to completely compensate for the infused load and over 24 hours typically over-excreted more than 2× the amount infused. A 30% decrease in plasma PCO2 following the metabolic acidosis in sculpin adpated to 20% SW (presumably secondary to respiratory alterations) contributed to the rapid recovery of blood pH. Low ambient [Na+] reversed normal acid excretion to an uptake (HCO3– loss; even after acid infusion). 20–30 mM Na+ in the water was necessary to induce a positive ΔH+. A reversible inhibition of ΔH+ was also observed in sculpin exposed to either amiloride or HMA during the acidosis. In contrast, low [Cl–] or DIDS enhanced ΔH+ excretion. We conclude that net H+ excretion measured following acidosis in these seawater or brackish water adapted animals is the sum of parallel (and counter acting) apical gill Na+/H+ and Cl–/HCO3– exchanges. The Na+/H+ transfers are most likely via an antiporter of the NHE family and occur on the background of continued "band-3" Cl–/HCO3– exchange. J. Exp. Zool. 279:509–520, 1997.© 1997 Wiley-Liss, Inc. Literature Cited Benos, D. J. (1988) Amiloride: Chemistry, kinetics and structure-activity relationships. In: Na+/H+ Exchange. S. Grinstein, ed. CRC Press, Boca Raton, pp. 121– 136. Bianchini, L., and J. Pouyssegur (1994) Molecular structure and regulation of vertebrate Na+/H+ exchangers. J. Exp. Biol., 196: 337– 345. Blackston, C., W. Hollimon, and J. B. Claiborne (1997) Isoforms of the Na+/H+ antiporter (NHE), in gill mRNA from the marine long-horned sculpin (Myoxocephalus octodecimspinosus). Bull. Mt. Desert Is. Biol. Lab. 36: 22. Borgese, F., C. Sardet, M. Cappadoro, J. Pouyssegur, and R. Motais (1992) Cloning and expressing a cAMP-activated Na+/H+ exchanger; evidence that the cytoplasmic domain mediates hormonal regulation. Proc. Natl. Acad. Sci. USA, 89: 6768– 6769. Bornancin, M., G. De Renzis, and R. Naon (1980) Cl− HCO3-ATPase in gills of the rainbow trout: Evidence for its microsomal localization. Am. J. Physiol. 238: R251– R259. Brosius, F. C., S. L. Alper, A. M. Garcia, and H. F. Lodish (1989) The major kidney band 3 gene transcript predicts an animoterminated truncated band 3 polypeptide. J. Biol. Chem., 264: 7784– 7787. Claiborne, J. B. (1997) Acid-base regulation. In: The Physiology of Fishes. D. H. Evans, ed. CRC Press, Boca Raton. In press. Campbell, J., I. Darko, and J. B. Claiborne (1997) Evidence for a DIDS sensitive gill Cl−/HCO3- in the marine longhorned sculpin (Myoxocephalus octodecimspinosus) adapted to dilute seawater. Bull. Mt. Desert Is. Biol. Lab. 36: 63– 64. Claiborne, J. B., D. Compton-McCullough and J. S. Walton (1998) Branchial acid transfers in the euryhaline toadfish (Opsanus tau) during exposure to low salinities. J. Exp. Biol. submitted. Claiborne, J. B. and D. H. Evans (1988) Ammonia and acidbase balance during high ammonia exposure in a marine teleost (Myoxocephalus octodecimspinosus). J. Exp. Biol., 140: 89– 105. Claiborne, J. B. and D. H. Evans (1992) Acid-base balance and ion transfers in the spiny dogfish (Squalus acanthias) during hypercapnia: a role for ammonia excretion. J. Exp. Zool., 261: 9– 17. Claiborne, J. B., D. H. Evans, and L. Goldstein (1982) Fish branchial Na+/NH4+ exchange is via basolateral Na+-K+ activated ATPase. J. Exp. Biol., 96: 431– 434. Claiborne, J. B., J. S. Walton, and D. Compton-McCullough (1994) Acid-base regulation, branchial transfers and renal output in a marine teleost fish (the long-horned sculpin; Myoxocephalus octodecimspinosus) during exposure to low salinities. J. Exp. Biol., 193: 79– 95. Evans, D. H. (1982) Mechanisms of acid extrusion by two marine fishes: the teleost, Opsanus beta, and the elasmobranch, Squalus acanthias. J. Exp. Biol., 97: 289– 299. Evans, D. H. (1984) The roles of gill permeability and transport mechanisms in euryhalinity. In: Fish Physiology. W. S. Hoar and D. J. Randall, eds. Academic Press, New York, pp. 239– 283. Goss, G., S. Perry, J. Fryer, and P. Laurent (1997) Gill morphology and acid-base regulation in freshwater fishes. Comp. Biochem. Physiol. In press. Goss, G. G. and C. M. Wood (1990) Na and Cl uptake kinetics, diffusive effluxes and acidic equivalent fluxes across the gills of rainbow trout. I. Responses to environmental hyperoxia. J. Exp. Biol., 152: 521– 548. Harris, S. P., J. B. Claiborne, J. Pouyssegur, and D. C. Dawson (1993) Transcripts homologous to Na/H antiporter isoform, NHE-1, in mRNA from the long horned sculpin (Myoxocephalus octodecimspinosus) and winter flounder (Pseudopheuronectes americanus). Bull. Mt. Desert Is. Biol. Lab., 32: 128– 130. Heisler, N. (1993) Acid-base regulation. In: The Physiology of Fishes. D. H. Evans, ed. CRC Press, Boca Raton, pp. 343– 378. Klungsoyr, L. (1987) Magnesium ion activated ATPase and proton transport in vesicles from the gill of rainbow trout (Salmo gairdneri). Comp. Biochem. Physiol., 88B: 1125– 1134. Lin, H., D. C. Pfeiffer, A. W. Vogl, J. Pan, and D. J. Randall (1994) Immunolocalization of proton-ATPase in the gill epithelia of rainbow trout. J. Exp. Biol., 195: 169– 183. Lin, H., and D. J. Randall (1991) Evidence for the presence of an electrogenic proton pump on the trout gill epithelium. J. Exp. Biol., 161: 119– 134. Lin, H., and D. J. Randall (1993) H+-ATPase activity in crude homogenates of fish gill tissue-inhibitor sensitivity and environmental and hormonal regulation. J. Exp. Biol., 180: 163– 174. Lin, H., and D. J. Randall (1995) Proton pumps in fish gills. In: Cellular and Molecular Approaches to Fish Ionic Regulation. C. M. Wood and T. J. Shuttleworth, eds. Academic Press, San Diego. McDonald, D. G., V. Cavdek, L. Calvert, and C. L. Milligan (1991) Acid base regulation in the atlantic hagfish Myxine glutinosa. J. Exp. Biol., 161: 201– 215. McDonald, D. G., R. L. Walker, P. R. H. Wilkes and C. M. Wood (1982) H+ excretion in the marine teleost Parophrys vetulus. J. Exp. Biol., 98: 403– 414. Milligan, C. L., D. G. McDonald, and T. Prior (1991) Branchial acid and ammonia fluxes in response to alkalosis and acidosis in 2 marine teleosts — coho salmon (Oncorhynchus-kisutch) and starry flounder (Platichthys-stellatus). Physiol. Zool., 64: 169– 192. Nonnotte, G., and J. P. Truchot (1990) Time-course of extracellular acid-base adjustments under hypo- or hyperosmotic conditions in the euryhaline fish, Platichthys flesus. J. Fish Biol., 98: 403– 414. Pärt, P. and C. M. Wood (1996) Na+/H+ exchange in cultured epithelial cells from fish gills. J. Comp. Physiol., 166: 37– 45. Smith, H. W. (1930) The absorption and excretion of salts by marine teleosts. Am. J. Physiol., 93: 480– 505. Solorzano, L. (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol. Oceanogr., 14: 799– 801. Sullivan, G. V., J. N. Fryer, and S. F. Perry (1996) Localization of mRNA for proton pump (H+ ATPase) and Cl−/HCO3− exchanger in rainbow trout gill. Can. J. Zool., 74: 2095– 2103. Tang, Y., D. G. McDonald, and R. G. Boutilier (1989) Acidbase regulation following exhaustive exercise: a comparison between freshwater- and seawater-adapted rainbow trout (Salmo gairdneri). J. Exp. Biol., 141: 407– 418. Tang, Y., S. Nolan, and R. G. Boutilier (1988) Acid-base regulation following acute acidosis in seawater-adapted rainbow trout, Salmo gairdneri: A possible role for catecholamines. J. Exp. Bio., 134: 297– 312. Tse, M., S. Levine, C. Yun, S. Brant, L. T. Counillon, J. Pouyssegur, and M. Donowitz (1993) Structure/function studies of the epithelial isoforms of the mammalian Na+/H+ exchanger gene family. J. Mem. Biol., 135: 93– 108. Wilkie, M. P. (1997) Mechanisms of ammonia excretion across fish gills. J. Comp. Biochem. Physiol. A., 118: 39– 50. Wilson, R., K. M. Gilmour, R. P. Henry, and C. M. Wood (1996) Intestinal base excretion in the seawater-adapted rainbow trout: a role in acid-base balance? J. Exp. Biol., 199: 2331– 2343. Zadunaisky, J. A., S. Cardona, L. Au, D. M. Roberts, E. Fisher, B. Lowenstein, E. J. Cragoe, and K. R. Spring (1995) Chloride transport activation by plasma osmolarity during rapid adaptation to high salinity of Fundulus heteroclitus. J. Mem. Biol., 143: 207– 217. Citing Literature Volume279, Issue5Special Issue: Cellular and Molecular Membrane Transport–A Symposium in Honor of Arnost Kleinzeller1 December 1997Pages 509-520 ReferencesRelatedInformation