Summary
The tentacles of the suctorian protozoonDiscophrya collini are stimulated to contract by externally applied Ca2+. The role of extracellular Ca2+ in tentacle contraction was studied by monitoring45Ca2+ uptake, using ionophore A23187 to facilitate membrane transport of calcium and ruthenium red (RR) as an inhibitor of transport. The degree of tentacle retraction was dependent upon external Ca2+ concentration and studies with45Ca2+ using scintillation counting indicated a linear relationship between external Ca2+ concentration and Ca2+ uptake. Uptake of Ca2+ was enhanced in the presence of the ionophore while RR caused little inhibition.45Ca2+ uptake was only partially inhibited by RR when cells were subjected to a Ca2+, ionophore and RR mixture. Grain counts from light microscope autoradiographs after treatment of cells with45Ca2+/ionophore,45Ca2+/RR or45Ca2+ alone showed heavy, light and intermediate labelling respectively. In all instances the grains were evenly distributed within the cell.
These observations are interpreted as supporting the suggestion that the ionophore enhances both the uptake of extracellular Ca2+ and release of Ca2+from an internal source, while the RR could only partially prevent movement of Ca2+ through the plasma mebrane. A model is presented suggesting that tentacle retraction is mediated by cytosolic Ca2+ levels which are determined by the fluxing of Ca2+ across the plasma membrane and the membrane of elongate dense bodies which act as internal Ca2+ reservoirs.
Similar content being viewed by others
References
Al-Khazzar, A. R., Butler, R. D., Earnshaw, M. J., 1983: The effect of ionophore A23187 and ruthenium red on tentacle contraction and ultrastructure inDiscophrya collini: Evidence of calcium fluxing from intracellular reservoirs. Protoplasma117, 158–166.
Becker, G. L., Chen, C. H., Greenwalt, J. W., Lehninger, A. L., 1974: Calcium phosphate granules in the hepatopancreas of the blue crabCallinectes sapidus. J. Cell Biol.61, 316–326.
Borle, A. B., Studer, R., 1978: Effect of calcium ionophores on the transport and distribution of calcium in isolated cells and in liver and kidney slices. J. Memb. Biol.38, 51–72.
Burton, R. L., 1972: The storage of calcium and magnesium phosphates and of calcite in the digestive gland of thePulmonata (Gastropoda). Comp. Biochem. Physiol.43 A, 655–663.
Bygrave, F. L., 1977: Mitochondrial calcium transport. In: Current topics in bioenergetics, Vol. 6 (Sanadi, D. R., ed.), pp. 259–318. New York: Academic Press.
Carafoli, E., Crompton, M., 1978: The regulation of intracellular Ca2+. Current topics in membranes and transport10, 151–216.
Curry, A., Butler, R. D., 1976: The ultrastructure, function and morphogenesis of the tentacle inDiscophrya sp. (Suctorida)Cileatea. J. Ultrastruct. Res.56, 164–176.
Desmedt, J. E., Hainaut, K., 1976: The effect of A23187 ionophore on calcium movement and contraction processes in single barnacle muscle fibres. J. Physiol.257, 87–107.
Dziak, R., Stern, P., 1975: Parathyrominetic effects of the ionophore, A23187, on bone cells and organ cultures. Biochem. biophys. Res. Commun.65, 1343–1349.
Geldard, B., 1977: Cytological and physiological studies ofDendro-cometes paradoxus (Stein). Ph.D. Thesis, University of Manchester.
Grinstein, S., Erlij, D., 1976: Action of insulin and cell calcium: Effect of ionophore A23187. J. Memb. Biol.29, 313–328.
Hackney, C. M., Al-Khazzar, A. R., Butler, R. D., 1982: Tentacle contraction and ultrastructure inDiscophrya collini: The response to cations. Protoplasma112, 92–100.
—,Butler, R. D., 1981a: Tentacle contraction in glycerinatedDiscophrya collini and the localization of HMM-binding filaments. J. Cell Sci.47, 65–75.
— —, 1981 b: Distribution of calcium in the suctorianDiscophrya collini: An X-ray microanalytical study. Tissue and Cell13, 453–459.
— —, 1981c: Electrically-induced tentacle retraction in the suctorian protozoonDiscophrya collini (Root). J. Protozool.28, 151–157.
Howard, B., Mitchell, P. C. H., Ritchie, A., Simkiss, K., Taylor, M., 1981: The composition of intracellular granules from the metal accumulating cells of the garden snailHelix aspersa. ]Biochem. J.194, 507–511.
Massini, P., Lüscher, E. F., 1974: Some effects of ionophores for divalent cations on blood platelets. Biochim. biophys. Acta372, 109–121.
Okajima, A., 1957: Protoplasmic contraction observed on the tentacles of the suctorian. I. Effects of electrolytes in the medium. Annot. Zool. Japanensis30, 51–62.
Pfeiffer, D. R., Taylor, R. W., Lardy, H. A., 1978: Ionophore A23187. Cation binding and transport properties. Ann. N.Y. Acad. Sci.307, 402–421.
Prince, W. T., Rasmussen, H., Berridge, M. J., 1973: The role of calcium in fly salivary gland secretion analyzed with the ionophore A23187. Biochim. biophys. Acta329, 98–107.
Reed, K. C., Bygrave, F. L., 1974: The inhibition of mitochondrial calcium transport by lanthanides and ruthenium red. Biochem. J.140, 143–155.
Reed, P. W., Lardy, H. A., 1972: A23187: A divalent cation ionophore. J. biol. Chem.247, 6970–6977.
Rose, B., Lowenstein, W. R., 1976: Permeability of a cell junction and the local cytoplasmic free ionized calcium concentrations: A study with aequorin. J. Memb. Biol.28, 87–119.
Sabri, A. W., 1977: Cytological studies of suctorian protozoans. Ph.D. Thesis, University of Manchester.
Schudt, C., Pette, D., 1975: Influence of the ionophore A23187 on myogenic cell fusion. FEBS Lett.59, 36–38.
Segal, J., Ingbar, S. H., 1982: A postulated mechanism for the coordinate effect of ionophore A23187 on calcium uptake and cell viability in rat thymocytes. Biochim. biophys. Acta684, 7–11.
Watson, E. L., Vicenzi, F. F., Davis, P. W., 1971: Ca2+-activated membrane ATPase: Selective inhibition by ruthenium red. Biochim. biophys. Acta249, 606–610.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Al-Khazzar, A.R., Earnshaw, M.J., Butler, R.D. et al. Tentacle contraction inDiscophrya collini: The effects of ionophore A23187 and ruthenium red on Ca2+-induced contraction and uptake of extracellular calcium. Protoplasma 122, 125–131 (1984). https://doi.org/10.1007/BF01279445
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01279445