Skip to main content Accessibility help

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

  • Michele G. Wheatly (a1)


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.



Hide All
Ahearn, G.A., 1978. Allosteric cotransport of sodium, chloride and calcium by the intestine of freshwater prawns. Journal of Membrane Biology, 42, 281300.
Ahearn, G.A. & Franco, P., 1993. Ca transport pathways in brush border membrane vesicles of crustacean antennal glands. American Journal of Physiology, 264, 12061213.
Ahearn, G.A. & Zhuang, Z., 1996. Cellular mechanisms of calcium transport in crustaceans. Physiological Zoology, 69, 383402.
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.
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.
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.
Cameron, J.N., 1989. Post-moult calcification in the blue crab Callinectes sapidus: timing and mechanism. Journal of Experimental Biology, 143, 285304.
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.
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.
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.
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.
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.
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.
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.
Flik, G. & Verbost, P.M., 1993. Calcium transport in fish gills and intestine. Journal of Experimental Biology, 184, 1729.
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.
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.
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.
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.
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.
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.
Greenaway, P., 1974. Calcium balance at the postmoult stage of the freshwater crayfish Austropotamobius pallipes (Lereboullet). Journal of Experimental Biology, 61, 3545.
Greenaway, P., 1976. The regulation of haemolymph calcium concentration of the crab Carcinus maenas (L.). Journal of Experimental Biology, 64, 149157.
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.
Greenaway, P., 1985. Calcium balance and moulting in the Crustacea. Biological Reviews, 60, 425454.
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.
Greenaway, P., 1989. Sodium balance and adaptation to freshwater in the amphibious crab Cardisoma hirtipes. Physiological Zoology, 62, 639653.
Greenaway, P., 1993. Calcium and magnesium balance during moulting in land crabs. Journal of Crustacean Biology, 13, 191197.
Greenaway, P. & Farrelly, C., 1991. Trans-epidermal transport and storage of calcium in Holthuisana transversa (Brachyura; Sundathelphusidae) during premoult. Ada Zoologica, 72, 2940.
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.
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.
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.
Hopkins, P.M., 1992. Hormonal control of the molt cycle in the fiddler crab Uca pugilator. American Zoologist, 32, 450458.
Huxley, T.H., 1896. The crayfish: an introduction to the study of zoology 6th ed., London: Kegan Paul, Trench, Trubner & Co.
Inesi, G., 1985. Mechanism of calcium transport. Annual Review of Physiology, 47, 573601.
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.
Lowenstam, H.A. & Weiner, S., 1989. On biomineralization. New York: Oxford University Press.
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.
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.
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.
Mizuhira, V. & Ueno, M., 1983. Calcium transport mechanism in molting crayfish revealed by microanalysis. Journal of Histochemistry and Cytochemistry, 31, 214218.
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.
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.
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.
Neufeld, D.S. & Cameron, J.N., 1993. Transepithelial movement of calcium in crustaceans. Journal of Experimental Biology, 184, 116.
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.
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.
Pederson, P.L. & Carafoli, E., 1987. Ion motive ATPases. I. Ubiquity, properties and significance to cell function. Trends in Biochemical Science, 12, 146150.
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.
Roer, R.D. & Dillaman, R., 1984. The structure and calcification of the crustacean cuticle. American Zoologist, 24, 893909.
Serrano, R., 1988. Structure and function of proton translocating ATPases in plasma membranes of plants and fungi. Biochimica et Biophysica Ada, 947,128.
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.
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.
Shull, G.E. & Lingrel, J.B., 1986. Molecular cloning of the rat stomach (H++K+-ATPase). Journal of Biological Chemistry, 261, 1678816791.
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.
Simkiss, K., 1974. Calcium translocation by cells. Endeavour, 33, 119124.
Simkiss, K. & Wilbur, K.M., 1989. Biomineralization. San Diego: Academic Press.
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.
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.
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.
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.
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.
Ueno, M., 1980. Calcium transport in crayfish gastrolith disc: morphology of gastrolith disc and ultrahistochemical demonstration of calcium. Journal of Experimental Zoology, 213, 161171.
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.
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.
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.
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.
Wheatly, M.G., 1996. An overview of calcium balance in crustaceans. Physiological Zoology, 69, 351382.
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.
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.
Wheatly, M.G. & Gannon, A.T., 1995. Ion regulation in crayfish: freshwater adaptations and the problem of moulting. American Zoologist, 35, 4959.
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.
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.
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.
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.
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.
Wolcott, T.G. & Wolcott, D.L., 1991. Ion conservation by reprocessing of urine in the land crab Gecarcinus lateralis (Freminville). Physiological Zoology, 64, 344361.
Zanders, I.P., 1980. Regulation of blood ions in Carcinus maenas (L.). Comparative Biochemistry and Physiology, 65A, 97108.
Zhuang, Z. & Ahearn, G.A., 1996. Ca2+ transport processes of lobster hepatopancreas brush-border membrane vesicles. Journal of Experimental Biology, 199, 11951208.

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

  • Michele G. Wheatly (a1)


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed