Differential distribution of calcium stores in Paramecium cells. Occurrence of a subplasmalemmal store with a calsequestrin-like protein

European Journal of Cell Biology

Volumn 72, Issue 4, 1997, Pages 297-306

  Plattner, Helmut ^a   Habermann, Anja ^a   Kissmehl, Roland ^a   Klauke, Norbert ^a   Majoul, Irina ^b   Söling, Hans Dieter ^b  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Calcium; Calreticulin; Calsequestrin; Exocytosis; Paramecium

Indexed keywords

CALCIUM; CALCIUM BINDING PROTEIN; CALRETICULIN; CALSEQUESTRIN;

AFFINITY CHROMATOGRAPHY; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOGOLD STAINING; LIVER; NONHUMAN; PARAMECIUM; PRIORITY JOURNAL; RAT; SARCOPLASMIC RETICULUM; SKELETAL MUSCLE;

EID: 0030971213     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (59)

1. Allen, R. D.: Cytology. In: H. D. Görtz (ed.): Paramecium. pp. 4-40. Springer-Verlag. Berlin, Heidelberg, New York 1988.
2. Beisson, J., M. Lefort-Tran, M. Pouphile, M. Rossignol, B. Satir: Genetic analysis of membrane differentiation in Paramecium. Freeze-fracture study of the trichocyst cycle in wild-type and mutant strains. J. Cell Biol. 69, 126-143 (1976).
3. Berridge, M. J.: Capacitative calcium entry. Biochem. J. 312, 1-11 (1995).
4. Bittermann, A. G., G. Knoll, A. Németh, H. Plattner: Quantitative immuno-gold labelling and ultrastructural preservation after cryo-fixation (combined with different freeze-substitution and embedding protocols) and after chemical fixation and cryosectioning. Analysis of the secretory organelle matrix of Paramecium trichocysts. Histochemistry 97, 421-429 (1992).
5. Buchanan, R. A., R. D. Leapmen, M. F. O'Connell, T. S. Reese, S. B. Andrews: Quantitative scanning transmission electron microscopy of ultrathin cryosections: subcellular organelles in rapidly frozen liver and cerebellar cortex. J. Struct. Biol. 110, 244-255 (1993).
6. Burgoyne, R. D., A. Morgan: Regulated exocytosis. Biochem. J. 293, 305-316 (1993).
7. Cala, S. E., L. R. Jones: Rapid purification of calsequestrin from cardiac and skeletal muscle sarcoplasmic reticulum vesicles by Ca2+-dependent elution from phenyl-Sepharose. J. Biol. Chem. 258, 11932-11936 (1983).
8. Campbell, K. P., D. H. MacLennan, A. O. Jorgensen: Staining of the Ca2+-binding proteins, calsequestrin, calmodulin, troponin C, and S-100, with the cationic carbocyanide dye "stains all". J. Biol. Chem. 258, 11267-11273 (1983).
9. Carlemalm, E., W. Villiger: Low temperature embedding. In: G. R. Bullock, P. Petrusz (eds.): Techniques in Immunocytochemistry. Vol. 4. pp. 29-45. Academic Press. London 1989.
10. Cheek, T. R., A. J. O'Sullivan, R. B. Moreton, M. J. Berridge, R. D. Burgoyne: The caffeine-sensitive Ca2+ store in bovine adrenal chromaffin cells: an estimation of its role in triggering secretion and Ca2+ homeostasis. FEBS Lett. 266, 91-95 (1990).
11. Clapham, D. E.: Calcium signaling. Cell 80, 259-268 (1995).
12. Damiani, E., A. Margreth: Characterization study of the ryanodine receptor and of calsequestrin isoforms of mammalian skeletal muscles in relation to fibre types. J. Muscle Res. Cell Motil. 15, 86-101 (1994).
13. Erxleben, C., H. Plattner: Ca2+ release from subplasmalemmal stores as a primary event during exocytosis in Paramecium cells. J. Cell Biol. 127, 935-945 (1994).
14. Fauré-Fermiet, E., J. André, M. C. Ganier: Calcification tégumentaire chez les ciliés du genre Coleps Nitzsch. J. Microsc. (Paris) 7, 693-704 (1968).
15. Fleischer, S., M. Inui: Biochemistry and biophysics of excitation-coupling. Annu. Rev. Biophys. Biophys. Chem. 18, 333-364 (1989).
16. Franceschi, V. R., X. Li, D. Zhang, T. W. Okita: Calsequestrin-like calcium-binding protein is expressed in calcium-accumulating cells of Pistia stratiotes. Proc. Natl. Acad. Sci. USA 90, 6986-6990 (1993).
17. Franzini-Armstrong, C., A. O. Jorgensen: Structure and development of E-C coupling units in skeletal muscle. Annu. Rev. Physiol. 56, 509-534 (1994).
18. Hincke, M. T.: Conditions for improved adsorption of calmodulin to nitrocellulose: detection by 45Ca binding. Electrophoresis 9, 303-306 (1988).
19. Jorgensen, A. O., R. Broderick, A. P. Somlyo, A. V. Somlyo: Two structurally distinct calcium storage sites in rat cardiac sarcoplasmic reticulum: an electron microprobe analysis study. Circ. Res. 63, 1060-1069 (1988).
20. Kersken, H., J. Vilmart-Seuwen, M. Momayezi, H. Plattner: Filamentous actin in Paramecium cells: mapping by phalloidin affinity labeling in vivo and in vitro. J. Histochem. Cytochem. 34, 443-454 (1986).
21. Knoll, G., C. Braun, H. Plattner: Quenched flow analysis of exocytosis in Paramecium cells: Time course, changes in membrane structure, and calcium requirements revealed after rapid mixing and rapid freezing of intact cells. J. Cell Biol. 113, 1295-1304 (1991).
22. Knoll, G., A. Grässle, C. Braun, W. Probst, B. Höhne-Zell, H. Plattner: A calcium influx is neither strictly associated with nor necessary for exocytotic membrane fusion in Paramecium cells. Cell Calcium 14, 189-199 (1993).
23. Knoll, G., D. Kerboeuf, H. Plattner: A rapid calcium influx during exocytosis in Paramecium cells is followed by a rise in cyclic GMP within 1 s. FEBS Lett. 304, 265-268 (1992).
24. Krause, K. H., M. Chou, M. A. Thomas, R. D. Sjolund, K. P. Campbell: Plant cells contain calsequestrin. J. Biol. Chem. 264, 4269-4272 (1989).
25. Kyhse-Andersen, J.: Multi-chamber apparatus for preparative isoelectric focusing. Electrophoresis 10, 6-10 (1989).
26. Länge, S., N. Klauke, H. Plattner: Subplasmalemmal Ca2+ stores of probable relevance for exocytosis in Paramecium. Alveolar sacs share some but not all characteristics with sarcoplasmic reticulum. Cell Calcium 17, 335-344 (1995).
27. Lebeche, D., B. Kaminer: Characterization of a calsequestrin-like protein from sea-urchin eggs. Biochem. J. 287, 741-747 (1992).
28. Lumpert, C. J., H. Kersken, H. Plattner: Cell surface complexes ('cortices') isolated from Paramecium tetraurelia cells as a model system for analysing exocytosis in vitro in conjunction with microinjection studies. Biochem. J. 269, 639-645 (1990).
29. Maruyama, K., T. Mikawa, S. Ebashi: Detection of calcium binding proteins by 45Ca autoradiography on nitrocellulose membrane after sodium dodecyl sulfate gel electrophoresis. J. Biochem. 95, 511-519 (1984).
30. Matsuoka, K., K. Seta, Y. Yamakawa, T. Okuyama, T. Shinoda, T. Isobe: Covalent structure of bovine brain calreticulin. Biochem. J. 298, 435-442 (1994).
31. Meldolesi, J., E. Clementi, C. Fasolato, D. Zacchetti, T. Pozzan: Ca2+ influx following receptor activation. Trends Pharmacol. Sci. 12, 289-292 (1991).
32. Meldolesi, J., L. Madeddu, T. Pozzan: Intracellular Ca2+ storage organelles in non-muscle cells: heterogeneity and functional assignment. Biochim. Biophys. Acta 1055, 130-140 (1990).
33. Menegazzi, P., F. Guzzo, B. Baldan, P. Mariani, S. Treves: Purification of calreticulin-like protein(s) from spinach leaves. Biochem. Biophys. Res. Commun. 190, 1130-1135 (1993).
34. Michalak, M., S. Baksh, M. Opas: Identification and immunolocalization of calreticulin in pancreatic cells: No evidence for "calciosomes". Exp. Cell Res. 197, 91-99 (1991).
35. Michalak, M., R. E. Milner, K. Burns, M. Opas: Calreticulin. Biochem. J. 285, 681-692 (1992).
36. Milner, R. E., K. S. Famulski, M. Michalak: Calcium binding proteins in the sarcoplasmic/endoplasmic reticulum of muscle and non-muscle cells. Mol. Cell. Biochem. 112, 1-13 (1992).
37. Momayezi, M., A. W. Habermann, J. J. Sokolova, R. Kissmehl, H. Plattner: Ultrastructural and antigenic preservation of a delicate structure by cryopreparation: identification and immunogold localization during biogenesis of a secretory component (membrane-matrix connection) in Paramecium trichocysts. J. Histochem. Cytochem. 41, 1669-1677 (1992).
38. Muto, Y., Y. Nozawa: Ca2+ transport studied with arsenazo III in Tetrahymena microscomes. Effect of calcium ionophore A23187 and trifluoperazine. Biochim. Biophys. Acta 815, 410-416 (1985).
39. Nguyen Van, P., F. Peter, H.-D. Söling: Four intracisternal calcium-binding glycoproteins from rat liver microsomes with high affinity for calcium. No indication for calsequestrin-like proteins in inositol 1,4,5-trisphosphate-sensitive calcium sequestering rat liver vesicles. J. Biol. Chem. 264, 17494-17501 (1989).
40. Nigam, S. K., T. Towers: Subcellular distribution of calcium-binding proteins and a calcium-ATPase in canine pancreas. J. Cell Biol. 111, 197-200 (1990).
41. Osborn, M., K. Weber: Immunofluorescence and immunocytochemical procedures with affinity purified antibodies: tubulin-containing structures. In: L. Wislon (ed.): Methods in Cell Biology. Vol. 24. pp. 98-132. Academic Press. New York 1982.
42. Pape, R., H. Plattner: Secretory organelle docking at the cell membrane of Paramecium cells: dedocking and synchronized redocking of trichocysts. Exp. Cell Res. 191, 263-272 (1990).
43. Parys, J. B., S. M. McPherson, L. Mathews, K. P. Campbell, F. J. Longo: Presence of inositol 1,4,5-trisphosphate receptor, calreticulin, and calsequestrin in eggs of sea urchins and Xenopus laevis. Dev. Biol. 161, 466-476 (1994).
44. Plattner, H.: Regulation of membrane fusion during exocytosis. Int. Rev. Cytol. 119, 197-286 (1989).
45. Plattner, H., G. Knoll, R. Pape: Synchronization of different steps of the secretory cycle in Paramecium tetraurelia: trichocyst exocytosis, exocytosis-coupled endocytosis, and intracellular transport. In: H. Plattner (ed.): Membrane Traffic in Protozoa. pp. 123-148. JAI Press Inc. Greenwich (CT), London 1993.
46. Platter, H., C. J. Lumpert, G. Knoll, R. Kissmehl, B. Höhne, M. Momayezi, R. Glas-Albrecht: Stimulus-secretion coupling in Paramecium cells. (Review Article.) Eur. J. Cell Biol. 55, 3-16 (1991).
47. Plattner, H., H. Matt, H. Kersken, B. Haacke, R. Stürzl: Synchronous exocytosis in Paramecium cells. I. A novel approach. Exp. Cell Res. 151, 6-13 (1984).
48. Pozzan, T., R. Rizzuto, P. Volpe, J. Meldolesi: Molecular and cellular physiology of intracellular calcium stores. Physiol. Rev. 74, 595-636 (1994).
49. Schmitz, M., K. Zierold: X-ray microanalysis of ion changes during fast processes of cells, as exemplified by trichocyst exocytosis of Paramecium caudatum. In: H. Plattner (ed.): Electron Microscopy of Subcellular Dynamics. pp. 325-339. CRC Press Inc. Boca Raton (FL) 1989.
50. Smith, M. J., G. L. E. Koch: Multiple zones in the sequence of calreticulin (CRP55, calregulin, HACBP), a major calcium binding ER/SR protein. EMBO J. 8, 3581-3586 (1989).
51. Somlyo, A. P., M. Bond, A. V. Somlyo: Calcium content of mitochondria and endoplasmic reticulum in liver frozen rapidly in vivo. Nature 314, 622-625 (1985).
52. Stelly, N., J. P. Mauger, G. Kéryer, M. Claret, A. Adoutte: Cortical alveoli of Paramecium: a vast submembranous calcium storage compartment. J. Cell Biol. 113, 103-112 (1991).
53. Takei, K., H. Stukenbrok, A. Metcalf, G. A. Mignery, T. C. Südhof, P. Volpe, P. De Camilli: Ca2+ stores in Purkinje neurons: endoplasmic reticulum subcompartments demonstrated by the heterogeneous distribution of the InsP3 receptor, Ca2+-ATPase, and calsequestrin. J. Neurosci. 12, 489-505 (1992).
54. Terasaki, M.: Probes for the endoplasmic reticulum: In: W. T. Mason (ed.): Fluorescent and Luminescent Probes for Biological Activity. pp. 120-123. Academic Press. London, San Diego, New York 1993.
55. Treptau, T., R. Kissmehl, J.-D. Wissmann, H. Plattner: A 63 kDa phosphoprotein undergoing rapid dephosphorylation during exocytosis in Paramecium cells shares biochemical characteristics with phosphoglucomutase. Biochem. J. 309, 557-567 (1995).
56. Treves, S., M. De Mattei, M. Lanfredi, A. Villa, N. M. Green, D. H. MacLennan, J. Meldolesi, T. Pozzan: Calreticulin is a candidate for a calsequestrin-like function in Ca2+-storage compartments (calciosomes) of liver and brain. Biochem. J. 271, 473-480 (1990).
57. Villa, A., P. Podini, D. O. Clegg, T. Pozzan, J. Meldolesi: Intracellular Ca2+ stores in chicken Purkinje neurons: differential distribution of the low affinity-high capacity Ca2+ binding protein, calsequestrin, of Ca2+ ATPase and of the ER lumenal protein, Bip. J. Cell Biol. 113, 778-791 (1991).
58. Volpe, P., L. Gorza, M. Brini, R. Sacchetto, S. Ausoni, D. O. Clegg: Expression of the calsequestrin gene in chicken cerebellum Purkinje neurons. Biochem. J. 294, 487-490 (1993).
59. Volpe, P., A. Villa, E. Damiani, A. H. Sharp, P. Podini, S. H. Snyder, J. Meldolesi: Heterogeneity of microsomal Ca2+ stores in chicken Purkinje neurons. EMBO J. 10, 3183-3189 (1991).