Reciprocal expression of gill Na+/K+-ATPaseα-subunit isoforms α1a and α1b during seawater acclimation of three salmonid fishes that vary in their salinity tolerance

Journal of Experimental Biology - Tập 209 Số 10 - Trang 1848-1858 - 2006
Jason S. Bystriansky1, Jeffrey G. Richards2, Patricia M. Schulte2, James S. Ballantyne1
1Department of Integrative Biology, University of Guelph, Guelph, Ontario N1G 2W1, Canada
2Department of Zoology, University of British Columbia, Vancouver, British Columbia, V6T 1Z4, Canada

Tóm tắt

SUMMARYThe upregulation of gill Na+/K+-ATPase activity is considered critical for the successful acclimation of salmonid fishes to seawater. The present study examines the mRNA expression of two recently discovered α-subunit isoforms of Na+/K+-ATPase(α1a and α1b) in gill during the seawater acclimation of three species of anadromous salmonids, which vary in their salinity tolerance. Levels of these Na+/K+-ATPase isoforms were compared with Na+/K+-ATPase activity and protein abundance and related to the seawater tolerance of each species. Atlantic salmon (Salmo salar) quickly regulated plasma Na+, Cl– and osmolality levels within 10 days of seawater exposure, whereas rainbow trout(Oncorhynchus mykiss) and Arctic char (Salvelinus alpinus)struggled to ionoregulate, and experienced greater perturbations in plasma ion levels for a longer period of time. In all three species, mRNA levels for theα1a isoform quickly decreased following seawater exposure whereasα1b levels increased significantly. All three species displayed similar increases in gill Na+/K+-ATPase activity during seawater acclimation, with levels rising after 10 and 30 days. Freshwater Atlantic salmon gill Na+/K+-ATPase activity and protein content was threefold higher than those of Arctic char and rainbow trout, which may explain their superior seawater tolerance. The role of the α1b isoform may be of particular importance during seawater acclimation of salmonid fishes. The reciprocal expression of Na+/K+-ATPase isoforms α1a and α1b during seawater acclimation suggests they may have different roles in the gills of freshwater and marine fishes; ion uptake in freshwater fish and ion secretion in marine fishes.

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Tài liệu tham khảo

Aas-Hansen, O., Vijayan, M. M., Johnsen, H. K., Cameron, C. and Jorgensen, E. H. (2005). Resmoltification in wild,anadromous Arctic char (Salvelinus alpinus): a survey of osmoregulatory, metabolic, and endocrine changes preceding annual seaward migration. Can. J. Fish. Aquat. Sci.62,195-204.

Applied Biosystems Inc. (2001). User bulletin #2: ABI Prism 7700 sequence detection system, pp.1-36.

Arnesen, A. M., Halvorsen, M. and Nilssen, K. J.(1992). Development of hypoosmoregulatory capacity in Arctic char(Salvelinus alpinus) reared under either continuous light or natural photoperiod. Can. J. Fish. Aquat. Sci.49,229-237.

Avella, M. and Bornancin, M. (1989). A new analysis of ammonia and sodium transport through the gills of the freshwater rainbow trout (Salmo gairdneri). J. Exp. Biol.142,155-175.

Besner, M. and Pelletier, D. (1991). Adaptation of the brook trout, Salvelinus fontinalis, to direct transfer to sea water in spring and summer. Aquaculture97,217-230.

Black, V. S. (1951). Changes in body chloride,density, and water content of chum (Oncorhynchus keta) and coho(O. kisutch) salmon fry when transferred from fresh water to sea water. J. Fish. Res. Board Can.8, 161-177.

Bystriansky, J. S. (2005). Regulation of gill Na+, K+-ATPase during salinity acclimation of salmonid fishes. PhD thesis, University of Guelph, Guelph,Canada.

Chomczynski, P. and Sacchi, N. (1987). Single-step method of RNA isolation by acid quanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem.162,156-159.

Conte, F. P. and Lin, D. H. Y. (1967). Kinetics of cellular morphogenesis in gill epithelium during sea water adaptation of Oncorhynchus (Walbaum). Comp. Biochem. Physiol.23,945-957.

D'Cotta, H., Valotaire, C., Le Gac, F. and Prunet, P.(2000). Synthesis of gill Na+-K+-ATPase in Atlantic salmon smolts: differences in α-mRNA and α-protein levels. Am. J. Physiol.278,R101-R110.

Else, P. L. and Wu, B. J. (1999). What role for membranes in determining the higher sodium pump molecular activity of mammals compared to ectotherms? J. Comp. Physiol.169B,296-302.

Evans, D. H., Piermarini, P. M. and Choe, K. P.(2005). The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol. Rev.85,97-177.

Folmar, L. C. and Dickhoff, W. W. (1980). The parr-smolt transformation (smoltification) and seawater adaptation in salmonids. A review of selected literature. Aquaculture21,1-37.

Gibbs, A. and Somero, G. N. (1990). Na+-K+-adenosine triphosphatase activities in gills of marine teleost fishes: changes with depth, size and locomotory activity level. Mar. Biol.106,315-321.

Gjedrem, T. (1975). Survival of Arctic char in the sea during fall and winter. Aquaculture6, 189-190.

Hirata, T., Kaneko, T., Ono, T., Nakazato, T., Furukawa, N.,Hasegawa, S., Wakabayashi, S., Shigekawa, M., Chang, M., Romero, M. F. et al. (2003). Mechanism of acid adaptation of a fish living in a pH 3.5 lake. Am. J. Physiol.284,R1199-R1212.

Hoar, W. S. (1976). Smolt transformation:evolution, behavior, and physiology. J. Fish. Res. Board Can.33,1234-1252.

Hoar, W. S. (1988). The physiology of smolting salmonids. In Fish Physiology: Vol. XI, The Physiology of Developing Fish, Part B, Viviparity and Posthatching Juveniles (ed. W. S. Hoar and D. J. Randall), pp.275-343. San Diego: Academic Press.

Houston, A. H. (1959). Osmoregulatory adaptation of steelhead trout (Salmo gairdneri Richardson) to sea water. Can. J. Zool.37,729-748.

Leray, C., Colin, D. A. and Florentz, A.(1981). Time course of osmotic adaptation and gill energetics of rainbow trout (Salmo gairdneri R.) following abrupt changes in external salinity. J. Comp. Physiol.144,175-181.

Lingrel, J. B. and Kuntzweiler, T. (1994). Na+/K+-ATPase. J. Biol. Chem.269,19659-19662.

Madsen, S. S., Jensen, M. K., Nohr, J. and Kristiansen, K.(1995). Expression of Na+-K+-ATPase in the brown trout Salmo trutta: in vivo modulation by hormones and seawater. Am. J. Physiol.269,R1339-R1345.

McCormick, S. D. and Saunders, R. L. (1987). Preparatory physiological adaptations for marine life of salmonids:osmoregulation, growth, and metabolism. Am. Fish. Soc. Symp.1,211-229.

Mobasheri, A., Avila, J., Cozar-Castellano, I., Brownleader, M. D., Trevan, M., Francis, M. J. O., Lamb, J. F. and Martin-Vasallo,P. (2000). Na+/K+-ATPase isozyme diversity; comparative biochemistry and physiological implications of novel functional interactions. Biosci. Rep.20, 51-91.

Miles, H. M. and Smith, L. S. (1968). Ionic regulation in migrating juvenile Coho salmon, Oncorhynchus kisutch.Comp. Biochem. Physiol.26,381-398.

Pagliarani, A., Ventrella, V., Ballestrazzi, R., Trombetti, F.,Pirini, M. and Trigari, G. (1991). Salinity-dependence of the properties of gill (Na+ + K+)-ATPase in rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol.100B,229-236.

Piermarini, P. M. and Evans, D. H. (2001). Immunochemical analysis of the vacuolar proton-ATPase B-subunit in the gills of a euryhaline stingray (Dasyatis sabina): effects of salinity and relation to Na+/K+-ATPase. J. Exp. Biol.204,3251-3259.

Prunet, P. and Boeuf, G. (1985). Plasma prolactin level during transfer of rainbow trout (Salmo gairdneri)and Atlantic salmon (Salmo salar) from fresh water to sea water. Aquaculture45,167-176.

Reid, S. D., Hawkings, G. S., Galvez, F. and Goss, G. G.(2003). Localization and characterization of phenamil-sensitive Na+ influx in isolated rainbow trout gill epithelial cells. J. Exp. Biol.206,551-559.

Richards, J. G., Semple, J. W., Bystriansky, J. S. and Schulte,P. M. (2003). Na+/K+-ATPaseα-isoform switching in gills of rainbow trout (Oncorhynchus mykiss) during salinity transfer. J. Exp. Biol.206,4475-4486.

Roberts, R. A. (1971). Preliminary observations on the ionic regulation of the Arctic char Salvelinus alpinus.J. Exp. Biol.55,213-222.

Saunders, R. L. and Henderson, E. B. (1978). Changes in gill ATPase activity and smolt status of Atlantic salmon (Salmo salar). J. Fish. Res. Board Can.27,1295-1311.

Seidelin, M., Madsen, S. S., Blenstrup, H. and Tipsmark, C. K. (2000). Time-course changes in the expression of Na+/K+-ATPase in gills and pyloric caeca of brown trout(Salmo trutta) during acclimation to seawater. Physiol. Biochem. Zool.73,446-453.

Silva, P., Soloman, R., Spokes, K. and Epstein, F. H.(1977). Ouabain inhibition of gill Na-K-ATPase: relationship to active chloride transport. J. Exp. Zool.199,419-426.

Singer, T. D., Clements, K. M., Semple, J. W., Schulte, P. M.,Bystriansky, J. S., Finstad, B., Fleming, I. A. and McKinley, R. S.(2002). Seawater tolerance and gene expression in two strains of Atlantic salmon smolts. Can. J. Fish. Aquat. Sci.59,125-135.

Staurnes, M., Sigholt, T., Lysfjord, G. and Gulseth, O. A.(1992). Difference in the seawater tolerance of anadromous and landlocked populations of Arctic char (Salvelinus alpinus). Can. J. Fish. Aquat. Sci.49,443-447.

Tipsmark, C. K., Madsen, S. S., Seidelin, M., Christensen, A. S., Cutler, C. P. and Cramb, G. (2002). Dynamics of Na+/K+,2Cl– cotransporter and Na+/K+-ATPase expression in the branchial epithelium or brown trout (Salmo trutta) and Atlantic Salmon (Salmo salar). J. Exp. Zool.293,106-118.

Zaugg, W. S. and Wagner, H. H. (1973). Gill ATPase activity related to the parr-smolt transformation and migration in steelhead trout (Salmo gairdneri): influence of photoperiod and temperature. Comp. Biochem. Physiol.45,955-965.

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Journal of Experimental Biology

Tập 209 Số 10

1848-1858

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