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Crustacean Models for Studying Calcium Transport: The Journey from Whole Organisms to Molecular Mechanisms

Published online by Cambridge University Press:  11 May 2009

Michele G. Wheatly
Affiliation:
Department of Biological Sciences, Wright State University, Dayton, Ohio, USA
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The crustacean moult cycle is a convenient model system in which to study calcium (Ca) homeostasis as vectorial movement across Ca transporting epithelia (gills, gastric epithelium, cuticular hypodermis, antennal gland) which occurs in either direction at different stages of the moulting cycle. Intermoult crustaceans are in relative Ca balance. During premoult, at the same time as the cuticle decalcifies, epithelia involved in Ca storage (e.g. gastric) calcify and/or increase their intracellular Ca stores. Premoult Ca balance is typically negative as Ca is excreted. During postmoult the soft new cuticle is remineralized largely with external Ca taken up across the gills and gastric epithelium (positive Ca balance); conversely during this time internally stored Ca is remobilized. This review (1) compares the relative roles of Ca transporting epithelia in Ca balance for crustaceans from different habitats; (2) proposes up-to-date cellular models for both apical to basolateral and basolateral to apical Ca transport in both noncalcifying and calcifying epithelia; (3) compares kinetics of the Ca pump and exchanger during intermoult; (4) presents new data on specific activity of calcium adenosinetriphosphatase (Ca2+ATPase) during the moult cycle of crayfish and (5) characterizes a partial cDNA sequence for the crayfish sarcoplasmic reticular Ca2+ATPase and documents its expression in gill, kidney and muscle of intermoult crayfish. The physiological and molecular characterization of Ca transporters in crustaceans will provide insight into the function, regulation and molecular evolution of mechanisms common to all eukaryotic cells.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 1997

References

Ahearn, G.A., 1978. Allosteric cotransport of sodium, chloride and calcium by the intestine of freshwater prawns. Journal of Membrane Biology, 42, 281300.CrossRefGoogle Scholar
Ahearn, G.A. & Franco, P., 1993. Ca transport pathways in brush border membrane vesicles of crustacean antennal glands. American Journal of Physiology, 264, 12061213.Google ScholarPubMed
Ahearn, G.A. & Zhuang, Z., 1996. Cellular mechanisms of calcium transport in crustaceans. Physiological Zoology, 69, 383402.CrossRefGoogle Scholar
Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J., 1990. Basic local alignment search tool. Journal of Molecular Biology, 215, 403410.CrossRefGoogle ScholarPubMed
Becker, G.L., Chen, C.H., Greenawalt, J.W. & Lehninger, A.L., 1974. Calcium phosphate granules in the hepatopancreas of the blue crab Callinectes sapidus. Journal of Cell Biology, 61, 316326.CrossRefGoogle ScholarPubMed
Brandl, C.J., Green, N.M., Korczak, B. & Maclennan, D.H., 1986. Two Ca2t ATPase genes: homologies and mechanistic implications of deduced amino acid sequences. Cell, 44, 597607.CrossRefGoogle Scholar
Cameron, J.N., 1989. Post-moult calcification in the blue crab Callinectes sapidus: timing and mechanism. Journal of Experimental Biology, 143, 285304.CrossRefGoogle Scholar
Cameron, J.N. & Wood, C.M., 1985. Apparent H+excretion and CO2 dynamics accompanying carapace mineralization in the blue crab (Callinectes sapidus) following moulting. Journal of Experimental Biology, 114, 181196.CrossRefGoogle Scholar
Chen, C.H., Greenawalt, J.W. & Lehninger, A.L., 1974. Biochemical and ultrastructural aspects of Ca2+ transport by mitochondria of the hepatopancreas of the blue crab Callinectes sapidus. Journal of Cell Biology, 61, 301315.CrossRefGoogle ScholarPubMed
Clarke, D.M., Loo, T.W., Inesi, G. & Maclennan, D.H., 1989. Location of high affinity Ca2+ binding sites within the predicted transmembrane domain of the sarcoplasmic reticulum Ca2+-ATPase. Nature, London, 339, 476478.CrossRefGoogle ScholarPubMed
Compere, P.H. & Goffinet, G., 1987. Elaboration and ultrastructural changes in the pore canal system of the mineralized cuticle of Carcinus maenas during the moulting cycle. Tissue and Cell, 19, 859875.CrossRefGoogle ScholarPubMed
Flik, G., Klaren, P.H.M., Schoenmakers, T.J.M., Bijvelds, M.J.C., Verbost, P.M. & Wendelaar, Bonga S.E., 1996. Cellular calcium transport in fish: unique and universal mechanisms. Physiological Zoology, 69, 403417.CrossRefGoogle Scholar
Flik, G., Schoenmakers, T.J.M., Groot, J.A., Van Os, C.H. & Wendelaar, Bonga S.E., 1990. Calcium absorption by fish intestine: the involvement of ATP- and sodium-dependent calcium extrusion mechanisms. Journal of Membrane Biology, 113, 1322.CrossRefGoogle ScholarPubMed
Flik, G., Van Rijs, J.H. & Wendelaar, Bonga S.E., 1985. Evidence for high-affinity Ca+2-ATPase activity and ATP-driven Ca+2-transport in membrane preparations of the gill epithelium of the cichlid fish Oreochromis mossambicus. Journal of Experimental Biology, 119, 335347.CrossRefGoogle Scholar
Flik, G. & Verbost, P.M., 1993. Calcium transport in fish gills and intestine. Journal of Experimental Biology, 184, 1729.CrossRefGoogle Scholar
Flik, G., Verbost, P.M., Atsma, W. & Lucu, C., 1994. Calcium transport in gill plasma membranes of the crab Carcinus maenas: evidence for carriers driven by ATP and a Na+ gradient. Journal of Experimental Biology, 195, 109122.CrossRefGoogle Scholar
Flik, J., Wendelaar, sBonga S.E. & Fenwick, J.C., 1983. Ca+2 dependent phosphatase and ATPase activities in eel gill plasma membranes. I. Identification of Ca+2-activated ATPase activities with nonspecific phosphatase activities. Comparative Biochemistry and Physiology, 76B, 745754.Google Scholar
Fox, F.R. & Ranga, Rao K., 1978. Characteristics of Ca+2-activated ATPase from the hepatopancreas of the blue crab Callinectes sapidus. Comparative Biochemistry and Physiology, 59B, 327331.Google Scholar
Ghijsen, W.E.J.M., De Jong, M.D. & Van Os, C.H., 1980. Dissociation between Ca2+ ATPase and alkaline phosphatase activities in plasma membranes of rat duodenum. Biochimica et Biophysica Ada, 599, 538551.CrossRefGoogle ScholarPubMed
Graf, F., 1971. Dynamique du calcium dans l'épithélium des caecums postérieurs d'Orchestia cavimana Heller (Crustacé: Amphipode). Rôle de l'espace intercellulaire. Comptes Rendus de l'Académie des Sciences. Paris, 273, 18281831.Google Scholar
Graf, F. & Meyran, J.C., 1985. Calcium reabsorption in the posterior caeca of the midgut in a terrestrial crustacean, Orchestia cavimana. Cell and Tissue Research, 242, 8395.CrossRefGoogle Scholar
Greenaway, P., 1974. Calcium balance at the postmoult stage of the freshwater crayfish Austropotamobius pallipes (Lereboullet). Journal of Experimental Biology, 61, 3545.CrossRefGoogle ScholarPubMed
Greenaway, P., 1976. The regulation of haemolymph calcium concentration of the crab Carcinus maenas (L.). Journal of Experimental Biology, 64, 149157.CrossRefGoogle ScholarPubMed
Greenaway, P., 1983. Uptake of calcium at the postmoult stage by the marine crabs Callinectes sapidus and Carcinus maenas. Comparative Biochemistry and Physiology, 75A, 181184.CrossRefGoogle Scholar
Greenaway, P., 1985. Calcium balance and moulting in the Crustacea. Biological Reviews, 60, 425454.CrossRefGoogle Scholar
Greenaway, P., 1988. Ion and water balance. In Biology of the land crabs (ed. W.W., Burggren and B.R., McMahon), pp. 211248. New York: Cambridge University Press.CrossRefGoogle Scholar
Greenaway, P., 1989. Sodium balance and adaptation to freshwater in the amphibious crab Cardisoma hirtipes. Physiological Zoology, 62, 639653.CrossRefGoogle Scholar
Greenaway, P., 1993. Calcium and magnesium balance during moulting in land crabs. Journal of Crustacean Biology, 13, 191197.CrossRefGoogle Scholar
Greenaway, P. & Farrelly, C., 1991. Trans-epidermal transport and storage of calcium in Holthuisana transversa (Brachyura; Sundathelphusidae) during premoult. Ada Zoologica, 72, 2940.CrossRefGoogle Scholar
Greenaway, P., Taylor, H.H. & Morris, S., 1990. Adaptations to a terrestrial existence by the robber crab Birgus latro. VI. The role of the excretory system in fluid balance. Journal of Experimental Biology, 152, 505519.CrossRefGoogle Scholar
Harris, R.R., 1977. Urine production rate and water balance in the terrestrial crabs Gecarcinus lateralis and Cardisoma guanhumi. Journal of Experimental Biology, 68, 5767.CrossRefGoogle ScholarPubMed
Henry, R.P. & Kormanik, G.A., 1985. Carbonic anhydrase activity and calcium deposition during the moult cycle of the blue crab, Callinectes sapidus. Journal of Crustacean Biology, 5, 234241.CrossRefGoogle Scholar
Hopkins, P.M., 1992. Hormonal control of the molt cycle in the fiddler crab Uca pugilator. American Zoologist, 32, 450458.CrossRefGoogle Scholar
Huxley, T.H., 1896. The crayfish: an introduction to the study of zoology 6th ed., London: Kegan Paul, Trench, Trubner & Co.CrossRefGoogle Scholar
Inesi, G., 1985. Mechanism of calcium transport. Annual Review of Physiology, 47, 573601.CrossRefGoogle ScholarPubMed
Kormanik, G.A. & Harris, R.R., 1981. Salt and water balance and antennal gland function in three Pacific species of terrestrial crab (Gecarcoidea lalandii, Cardisoma carnifex, Birgus latro). Journal of Experimental Zoology, 218, 97105.CrossRefGoogle Scholar
Lowenstam, H.A. & Weiner, S., 1989. On biomineralization. New York: Oxford University Press.CrossRefGoogle Scholar
Maclennan, D.H., Brandl, C.J., Korczak, B. & Green, N.M., 1985. Amino acid sequence of a Ca2+ + Mg2+-dependent ATPase from rabbit muscle sarcoplasmic reticulum, deduced from its complementary DNA sequence. Nature, London, 316, 696700.CrossRefGoogle ScholarPubMed
Meyran, J.-C., Graf, F. & Nicaise, G., 1984. Calcium pathway through a mineralizing epithelium in the crustacean Orchestia in premoult: ultrastructural cytochemistry and X-ray microanalysis. Tissue and Cell, 16, 269286.CrossRefGoogle Scholar
Meyran, J.-C., Graf, F. & Nicaise, G., 1986. Pulse discharge of calcium through a demineralizing epithelium in the crustacean Orchestia: ultrastructural cytochemistry and X-ray microanalysis. Tissue and Cell, 18, 267283.CrossRefGoogle Scholar
Mizuhira, V. & Ueno, M., 1983. Calcium transport mechanism in molting crayfish revealed by microanalysis. Journal of Histochemistry and Cytochemistry, 31, 214218.CrossRefGoogle ScholarPubMed
Morris, M.A. & Greenaway, P., 1992. High affinity, Ca2+specific ATPase and Na+K+-ATPase in the gills of a supralittoral crab Leptograpsus variegatus. Comparative Biochemistry and Physiology, 102A, 1518.CrossRefGoogle ScholarPubMed
Morris, S., Taylor, H.H. & Greenaway, P., 1991. Adaptations to a terrestrial existence by the robber crab Birgus latro. VII. The branchial chamber and its role in urine reprocessing. Journal of Experimental Biology, 161, 315331.CrossRefGoogle Scholar
Neufeld, D.S. & Cameron, J.N., 1992. Postmoult uptake of calcium by the blue crab (Callinectes sapidus) in water of low salinity. Journal of Experimental Biology, 171, 283299.CrossRefGoogle Scholar
Neufeld, D.S. & Cameron, J.N., 1993. Transepithelial movement of calcium in crustaceans. Journal of Experimental Biology, 184, 116.CrossRefGoogle ScholarPubMed
Neufeld, D.S. & Cameron, J.N., 1994. Effect of the external concentration of calcium on the postmoult uptake of calcium in blue crabs (Callinectes sapidus). Journal of Experimental Biology, 188, 19.CrossRefGoogle ScholarPubMed
Palmero, I. & Sastre, L., 1989. Complementary DNA cloning of a protein highly homologous to mammalian sarcoplasmic reticulum Ca-ATPase from the crustacean Artemia. Journal of Molecular Biology, 210, 737748.CrossRefGoogle ScholarPubMed
Pederson, P.L. & Carafoli, E., 1987. Ion motive ATPases. I. Ubiquity, properties and significance to cell function. Trends in Biochemical Science, 12, 146150.CrossRefGoogle Scholar
Roer, R.D., 1980. Mechanisms of resorption and deposition of calcium in the carapace of the crab Carcinus maenas. Journal of Experimental Biology, 88, 205218.CrossRefGoogle Scholar
Roer, R.D. & Dillaman, R., 1984. The structure and calcification of the crustacean cuticle. American Zoologist, 24, 893909.CrossRefGoogle Scholar
Serrano, R., 1988. Structure and function of proton translocating ATPases in plasma membranes of plants and fungi. Biochimica et Biophysica Ada, 947,128.CrossRefGoogle ScholarPubMed
Shull, G.E. & Greeb, J., 1988. Molecular cloning of two isoforms of the plasma membrane Ca2+ transporting ATPase from rat brain. Journal of Biological Chemistry, 263, 86468657.CrossRefGoogle ScholarPubMed
Shull, G.E., Greeb, J. & Lingrel, J.B., 1986. Molecular cloning of three distinct forms of the Na+/K+ATPase alpha subunit from rat brain. Biochemistry, 25, 81258132.CrossRefGoogle ScholarPubMed
Shull, G.E. & Lingrel, J.B., 1986. Molecular cloning of the rat stomach (H++K+-ATPase). Journal of Biological Chemistry, 261, 1678816791.CrossRefGoogle ScholarPubMed
Shull, G.E., Schwartz, A. & Lingrel, J.B., 1985. Amino-acid sequence of the catalytic subunit of the (Na+ + K+) ATPase deduced from a complementary DNA. Nature, London, 316, 691695.CrossRefGoogle ScholarPubMed
Simkiss, K., 1974. Calcium translocation by cells. Endeavour, 33, 119124.CrossRefGoogle ScholarPubMed
Simkiss, K. & Wilbur, K.M., 1989. Biomineralization. San Diego: Academic Press.Google Scholar
Sparkes, S. & Greenaway, P., 1984. The haemolymph as a storage site for cuticular ions during premoult in the freshwater/land crab Holthusiana transversa. Journal of Experimental Biology, 113, 4354.CrossRefGoogle Scholar
Steel, C.G.H., 1982. Stages of the intermoult cycle in the terrestrial isopod Oniscus asellus and their relationship to biphasic cuticle secretion. Canadian Journal of Zoology, 60, 429437.CrossRefGoogle Scholar
Towle, D.W. & Mangum, C.P., 1985. Ionic regulation and transport ATPase activities during the moult cycle in the blue crab Callinectes sapidus. Journal of Crustacean Biology, 5, 216222.CrossRefGoogle Scholar
Travis, D.F., 1963. Structural features of mineralization from tissues to macromolecular levels of organization in the decapod Crustacea. Annals of the New York Academy of Sciences, 109, 177245.CrossRefGoogle ScholarPubMed
Tyler-Jones, R. & Taylor, E.W., 1986. Urine flow and the role of the antennal glands in water balance during aerial exposure in the crayfish Austropotamobius pallipes (Lereboullet). Journal of Comparative Physiology, 156B, 529535.CrossRefGoogle Scholar
Ueno, M., 1980. Calcium transport in crayfish gastrolith disc: morphology of gastrolith disc and ultrahistochemical demonstration of calcium. Journal of Experimental Zoology, 213, 161171.CrossRefGoogle Scholar
Ueno, M. & Mizuhira, V., 1984. Calcium transport mechanism in crayfish gastrolith epithelium correlated with the moulting cycle. II. Cytochemical demonstration of Ca ATPase and Mg ATPase. Histochemistry, 80, 213217.CrossRefGoogle Scholar
Welinder, B.S., 1975. The crustacean cuticle. II. Deposition of organic and inorganic material in the cuticle of Astacus fluviatilis in the period after moulting. Comparative Biochemistry and Physiology, 51B, 409416.Google ScholarPubMed
Wheatly, M.G., 1985. The role of the antennal gland in ion and acid-base regulation during hyposaline exposure of the Dungeness crab Cancer magister (Dana). Journal of Comparative Physiology, 155B, 445454.CrossRefGoogle Scholar
Wheatly, M.G., 1989. Physiological responses of the crayfish Pacifastacus leniusculus (Dana) to environmental hyperoxia. I. Extracellular acid-base and electrolyte status and transbranchial exchange. Journal of Experimental Biology, 143, 3351.CrossRefGoogle Scholar
Wheatly, M.G., 1996. An overview of calcium balance in crustaceans. Physiological Zoology, 69, 351382.CrossRefGoogle Scholar
Wheatly, M.G. & Ayers, J., 1995. Scaling of calcium, inorganic and organic contents to body mass during the moulting cycle of the freshwater crayfish Procambarus clarkii (Girard). Journal of Crustacean Biology, 15, 409417.CrossRefGoogle Scholar
Wheatly, M.G. & Gannon, A.T., 1993. The effect of external electrolytes an postmoult calcification and associated ions fluxes in the freshwater crayfish Procambarus clarkii (Girard). In Freshwater crayfish, vol. 9 (ed. D.M., Holdich and G.F., Warner), pp. 200212. Lafayette: University of Southwestern Louisiana.Google Scholar
Wheatly, M.G. & Gannon, A.T., 1995. Ion regulation in crayfish: freshwater adaptations and the problem of moulting. American Zoologist, 35, 4959.CrossRefGoogle Scholar
Wheatly, M.G. & Ignaszewski, L.A., 1990. Electrolyte and gas exchange during the moulting cycle of a freshwater crayfish. Journal of Experimental Biology, 151, 469483.CrossRefGoogle Scholar
Wheatly, M.G. & Toop, T., 1989. Physiological responses of the crayfish Pacifastacus leniusculus to environmental hyperoxia. II. The role of the antennal gland in acid base and ion regulation. Journal of Experimental Biology, 143, 5370.CrossRefGoogle Scholar
Wheatly, M.G., Toop, T., Morrison, R.J. & Yow, L.C., 1991. Physiological responses of the crayfish Pacifastacus leniusculus (Dana) to environmental hyperoxia. III. Intracellular acid-base balance. Physiological Zoology, 64, 323343.CrossRefGoogle Scholar
Whiteley, N.M. & Taylor, E.W., 1992. Oxygen and acid-base disturbances in the haemolymph of the lobster Homarus gammarus during commercial transport and storage. Journal of Crustacean Biology, 12, 1930.CrossRefGoogle Scholar
Wolcott, T.G. & Wolcott, D.L., 1985. Extrarenal modification of urine for ion conservation in ghost crabs, Ocypode quadrata (Fabricius). Journal of Experimental Marine Biology and Ecology, 91, 93107.CrossRefGoogle Scholar
Wolcott, T.G. & Wolcott, D.L., 1991. Ion conservation by reprocessing of urine in the land crab Gecarcinus lateralis (Freminville). Physiological Zoology, 64, 344361.CrossRefGoogle Scholar
Zanders, I.P., 1980. Regulation of blood ions in Carcinus maenas (L.). Comparative Biochemistry and Physiology, 65A, 97108.CrossRefGoogle Scholar
Zhuang, Z. & Ahearn, G.A., 1996. Ca2+ transport processes of lobster hepatopancreas brush-border membrane vesicles. Journal of Experimental Biology, 199, 11951208.CrossRefGoogle Scholar