Crossref journal-article
The Company of Biologists
Journal of Experimental Biology (237)
Abstract

SUMMARYIn terrestrial isopods, large amounts of Ca2+ are transported across anterior sternal epithelial cells during moult-related deposition and resorption of CaCO3 deposits. Because of its toxicity and function as a second messenger, resting cytosolic Ca2+ levels must be maintained below critical concentrations during epithelial Ca2+transport, raising the possibility that organelles play a role during Ca2+ transit. We therefore studied the uptake of Ca2+into Ca2+-sequestering organelles by monitoring the formation of birefringent calcium oxalate crystals in permeabilised anterior and posterior sternal epithelium cells of Porcellio scaber during Ca2+-transporting and non-transporting stages of the moulting cycle using polarised-light microscopy. The results indicate ATP-dependent uptake of Ca2+ into organelles. Half-maximal crystal growth at a Ca2+ activity, aCa, of 0.4 μmol l-1 and blockade by cyclopiazonic acid suggest Ca2+uptake into the smooth endoplasmic reticulum by the smooth endoplasmic reticulum Ca2+-ATPase. Analytical electron microscopical techniques support this interpretation by revealing the accumulation of Ca2+-containing crystals in smooth membranous intracellular compartments. A comparison of different moulting stages demonstrated a virtual lack of crystal formation in the early premoult stage and a significant fivefold increase between mid premoult and the Ca2+-transporting stages of late premoult and intramoult. These results suggest a contribution of the smooth endoplasmic reticulum as a transient Ca2+ store during intracellular Ca2+ transit.

Bibliography

Hagedorn, M., & Ziegler, A. (2002). Analysis of Ca2+ uptake into the smooth endoplasmic reticulum of permeabilised sternal epithelial cells during the moulting cycle of the terrestrial isopodPorcellio scaber. Journal of Experimental Biology, 205(13), 1935–1942.

Authors 2
  1. Monica Hagedorn (first)
  2. Andreas Ziegler (additional)
References 38 Referenced 26
  1. Ahearn, G. A. and Franco, P. (1990). Sodium and calcium share the electrogenic 2Na+-1H+ antiporter in crustacean antennal glands. Am. J. Physiol.259,F758-F767.
  2. Ahearn, G. A. and Franco, P. (1993). Ca2+ transport pathways in brush-border membrane vesicles of crustacean antennal glands. Am. J. Physiol.264,1206-1213. (10.1152/ajpregu.1993.264.6.R1206)
  3. Ahearn, G. A. and Zhuang, Z. (1996). Cellular mechanisms of calcium transport in crustaceans. Physiol. Zool.69,383-402. (10.1086/physzool.69.2.30164191)
  4. Baumann, O. and Walz, B. (1989). Calcium- and inositol polyphosphate-sensitivity of the calcium-sequestering endoplasmic reticulum in the photoreceptor cells of the honeybee drone. J. Comp. Physiol. A165,627-636. (10.1007/BF00610994)
  5. Baumann, O., Walz, B., Somlyo, A. V. and Somlyo, A. P.(1991). Electron probe microanalysis of calcium release and magnesium uptake by endoplasmic reticulum in bee photoreceptors. Proc. Natl. Acad. Sci. USA88,741-744. (10.1073/pnas.88.3.741)
  6. Berridge, M. J. (1993). Inositol trisphosphate and calcium signalling. Nature361,315-325. (10.1038/361315a0)
  7. Drobne, D. and Štrus, J. (1996). Moult frequency of the isopod Porcellio scaber, as a measure of zinc-contaminated food. Env. Toxicol. Chem.15,126-130. (10.1002/etc.5620150209)
  8. Escalante, R. and Sastre, L. (1993). Similar alternative splicing events generate two sarcoplasmic or endoplasmic reticulum Ca-ATPase isoforms in the crustacean Artemia franciscana and in vertebrates. J. Biol. Chem.268,14090-14095. (10.1016/S0021-9258(19)85212-2)
  9. Feher, J. J., Fullmer, C. S. and Fritzsch, G. K.(1989). Comparison of the enhanced steady-state diffusion of calcium by calbindin-D9K and calmodulin: possible importance in intestinal calcium absorption. Cell Calcium10,189-203. (10.1016/0143-4160(89)90002-X)
  10. Flik, G., Verbost, P. M. and Atsma, W. (1994). Calcium transport in gill plasma membranes of the crab Carcinus maenas: evidence for carriers driven by ATP and a Na+gradient. J. Exp. Biol.195,109-122. (10.1242/jeb.195.1.109)
  11. Franklin, I., Winz, R. and Hubbard, M. (2001). Endoplasmic reticulum Ca-ATPase pump is up-regulated in calcium-transporting dental enamel cells: a non-housekeeping role for SERCA2b. Biochem. J.358,217-224. (10.1042/bj3580217)
  12. Frixione, E. and Ruiz, L. (1988). Calcium uptake by smooth endoplasmic reticulum of peeled retinal photoreceptors of the crayfish. J. Comp. Physiol. A162,91-100. (10.1007/BF01342706)
  13. Glötzner, J. and Ziegler, A. (2000). Morphometric analysis of the plasma membranes in the calcium transporting sternal epithelium of the terrestrial isopods Ligia oceanica, Ligidium hypnorum and Porcellio scaber.Arthropod Struct. Dev.29,241-257. (10.1016/S1467-8039(00)00030-X)
  14. Greenaway, P. (1985). Calcium balance and moulting in the Crustacea. Biol. Rev.60,425-454. (10.1111/j.1469-185X.1985.tb00424.x)
  15. Greenaway, P., Dillaman, R. M. and Roer, R. D.(1995). Quercitin-dependent ATPase activity in the hypodermal tissue of Callinectes sapidus, during the moult cycle. Comp. Biochem. Physiol.111A,303-312. (10.1016/0300-9629(94)00205-8)
  16. Hubbard, M. J. (1996). Abundant calcium homeostasis machinery in rat dental enamel cells. Up-regulation of calcium store proteins during enamel mineralization implicates the endoplasmic reticulum in calcium transcytosis. Eur. J. Biochem.239,611-623. (10.1111/j.1432-1033.1996.0611u.x)
  17. Jorgensen, A. O., Broderick, R., Somlyo, A. P. and Somlyo, A. V. (1988). Two structurally distinct calcium storage sites in rat cardiac sarcoplasmic reticulum: an electron microprobe analysis study. Circ. Res.63,1060-1069. (10.1161/01.RES.63.6.1060)
  18. Messner, B. (1965). Ein morphologisch-histologischer Beitrag zur Häutung von Porcellio scaber Latr. und Oniscus asellus I. (Isopoda Terrestria). Crustaceana9,285-301.
  19. Nemere, I. (1992). Vesicular calcium transport in chick intestine. J. Nutr.122,657-661. (10.1093/jn/122.suppl_3.657)
  20. Neufeld, D. S. and Cameron, J. N. (1993). Transepithelial movement of calcium in crustaceans. J. Exp. Biol.184,1-16. (10.1242/jeb.184.1.1)
  21. Roer, R. D. (1980). Mechanisms of resorption and deposition of calcium in the carapace of the crab Carcinus maenas.J. Exp. Biol.88,205-218. (10.1242/jeb.88.1.205)
  22. Rogers, J. V. and Wheatly, M. G. (1997). Accumulation of calcium in the antennal gland during the molting cycle of the freshwater crayfish Procambarus clarkii.Invert. Biol.116,248-254. (10.2307/3226901)
  23. Simkiss, K. (1996). Calcium transport across calcium-regulated cells. Physiol. Zool.69,343-350. (10.1086/physzool.69.2.30164189)
  24. Somlyo, A. P. and Walz, B. (1985). Elemental distribution in Rana pipiens retinal rods: quantitative electron probe analysis. J. Physiol., Lond.358,183-195. (10.1113/jphysiol.1985.sp015547)
  25. Somlyo, A. V., Gonzalez-Serratos, H., Shuman, H., McClellan, G. and Somlyo, A. P. (1981). Calcium release and ionic changes in the sarcoplasmic reticulum of tetanized muscle: an electron-probe study. J. Cell Biol.90,577-594. (10.1083/jcb.90.3.577)
  26. Steel, C. G. H. (1993). Storage and translocation of integumentary calcium during the moult cycle of the terrestrial isopod Oniscus asellus (L.). Can. J. Zool.71,4-10. (10.1139/z93-002)
  27. Tsien, R. Y. and Rink, T. J. (1980). Neutral carrier ion-selective microelectrodes for measurement of intracellular free calcium. Biochim. Biophys. Acta599,623-638. (10.1016/0005-2736(80)90205-9)
  28. Ueno, M. (1980). Calcium transport in crayfish gastrolith disc: morphology of gastrolith disc and ultrahistochemical demonstration of calcium. J. Exp. Zool.213,161-171. (10.1002/jez.1402130202)
  29. Walz, B. (1982). Ca2+-sequestering smooth endoplasmic reticulum in an invertebrate photoreceptor. II. Its properties as revealed by microphotometric measurements. J. Cell Biol.93,849-859.
  30. Walz, B. and Baumann, O. (1989). Calcium-sequestering cell organelles: in situ localization,morphological and functional characterization. Progr. Histochem. Cytochem.20,1-47.
  31. Wheatly, M. G. (1997). Crustacean models for studying calcium transport: the journey from whole organisms to molecular mechanisms. J. Mar. Biol.77,107-125. (10.1017/S0025315400033816)
  32. Zhang, Z., Chen, D. and Wheatly, M. G. (2000). Cloning and characterization of sarco/endoplasmic reticulum Ca2+-ATPase (SERCA) from crayfish axial muscle. J. Exp. Biol.203,1-13. (10.1242/jeb.203.22.3411)
  33. Ziegler, A. (1994). Ultrastructure and electron spectroscopic diffraction analysis of the sternal calcium deposits of Porcellio scaber Latr. (Isopoda, Crustacea). J. Struct. Biol.112,110-116. (10.1006/jsbi.1994.1012)
  34. Ziegler, A. (1996). Ultrastructural evidence for transepithelial calcium transport in the anterior sternal epithelium of the terrestrial isopod Porcellio scaber (Crustacea) during the formation and resorption of CaCO3 deposits. Cell Tissue Res.284,459-466. (10.1007/s004410050606)
  35. Ziegler, A. (1997). Immunocytochemical localization of Na+,K+-ATPase in the calcium-transporting sternal epithelium of the terrestrial isopod Porcellio scaber Latr. (Crustacea). J. Histochem. Cytochem.45,437-446. (10.1177/002215549704500311)
  36. Ziegler, A. (2002). X-ray microprobe analysis of epithelial calcium transport. Cell Calcium (in press). (10.1016/S0143-4160(02)00060-X)
  37. Ziegler, A. and Scholz, F. H. E. (1997). The ionic hemolymph composition of the terrestrial isopod Porcellio scaber Latr. during molt. J. Comp. Physiol. B167,536-542. (10.1007/s003600050106)
  38. Ziegler, A., Weihrauch, D. and Towle, D. W.(2001). Increased expression of the Ca2+-ATPase and the Na+/Ca2+-exchanger in the anterior sternal tissue of Porcellio scaber (Isopoda, Crustacea) during premolt. Zoology104, Suppl. IV,67.
Dates
Type When
Created 4 years, 4 months ago (April 25, 2021, 12:52 a.m.)
Deposited 1 year, 9 months ago (Nov. 2, 2023, 1:55 p.m.)
Indexed 1 year, 3 months ago (May 9, 2024, 12:38 a.m.)
Issued 23 years, 1 month ago (July 1, 2002)
Published 23 years, 1 month ago (July 1, 2002)
Published Print 23 years, 1 month ago (July 1, 2002)
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@article{Hagedorn_2002, title={Analysis of Ca2+ uptake into the smooth endoplasmic reticulum of permeabilised sternal epithelial cells during the moulting cycle of the terrestrial isopodPorcellio scaber}, volume={205}, ISSN={0022-0949}, url={http://dx.doi.org/10.1242/jeb.205.13.1935}, DOI={10.1242/jeb.205.13.1935}, number={13}, journal={Journal of Experimental Biology}, publisher={The Company of Biologists}, author={Hagedorn, Monica and Ziegler, Andreas}, year={2002}, month=jul, pages={1935–1942} }