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. 1981 Feb 1;88(2):301–311. doi: 10.1083/jcb.88.2.301

Control of exocytotic processes: cytological and physiological studies of trichocyst mutants in Paramecium tetraurelia

PMCID: PMC2111747  PMID: 7204496

Abstract

The trichocysts of Paramecium tetraurelia constitute a favorable system for studying secretory process because of the numerous available mutations that block, at various stages, the development of these secretory vesicles, their migration towards and interaction with the cell surface, and their exocytosis. Previous studies of several mutants provided information (a) on the assembly and function of the intramembranous particles arrays in the plasma membrane at trichocyst attachment sites, (b) on the autonomous motility of trichocysts, required for attachment to the cortex, and (c) on a diffusible cytoplasmic factor whose interaction with both trichocyst and plasma membrane is required for exocytosis to take place. We describe here the properties of four more mutants deficient in exocytosis ability, nd6, nd7, tam38, and tam6, which were analyzed by freeze-fracture, microinjection of trichocysts, and assay for repair of the mutational defect through cell-cell interaction during conjugation with wild-type cells. As well as providing confirmation of previous conclusions, our observations show that the mutations nd6 and tam6 (which display striking abnormalities in their plasma membrane particle arrays and are reparable through cell-cell contact but not by microinjection of cytoplasm) affect two distinct properties of the plasma membrane, whereas the other two mutations affect different properties of the trichocysts. Altogether, the mutants so far analyzed now provide a rather comprehensive view of the steps and functions involved in secretory processes in Paramecium and demonstrate that two steps of these processes, trichocyst attachment to the plasma membrane and exocytosis, depend upon specific properties of both the secretory vesicle and the plasma membrane.

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Selected References

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  1. Allen R. D., Hausmann K. Membrane behavior of exocytic vesicles. I. The ultrastructure of Paramecium trichocysts in freeze-fracture preparations. J Ultrastruct Res. 1976 Feb;54(2):224–234. doi: 10.1016/s0022-5320(76)80152-9. [DOI] [PubMed] [Google Scholar]
  2. Aufderheide K. J. Genetic aspects of intracellular motility: cortical localization and insertion of trichocysts in Paramecium tetraurelia. J Cell Sci. 1978 Jun;31:259–273. doi: 10.1242/jcs.31.1.259. [DOI] [PubMed] [Google Scholar]
  3. Aunis D., Hesketh J. E., Devilliers G. Freeze-fracture study of the chromaffin cell during exocytosis: evidence for connections between the plasma membrane and secretory granules and for movements of plasma membrane-associated particles. Cell Tissue Res. 1979 Apr 12;197(3):433–441. doi: 10.1007/BF00233568. [DOI] [PubMed] [Google Scholar]
  4. Bannister L. H. The structure of trichocysts in Paramecium caudatum. J Cell Sci. 1972 Nov;11(3):899–929. doi: 10.1242/jcs.11.3.899. [DOI] [PubMed] [Google Scholar]
  5. Beisson J., Cohen J., Lefort-Tran M., Pouphile M., Rossignol M. Control of membrane fusion in exocytosis. Physiological studies on a Paramecium mutant blocked in the final step of the trichocyst extrusion process. J Cell Biol. 1980 May;85(2):213–227. doi: 10.1083/jcb.85.2.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Beisson J., Lefort-Tran M., Pouphile M., Rossignol M., Satir B. Genetic analysis of membrane differentiation in Paramecium. Freeze-fracture study of the trichocyst cycle in wild-type and mutant strains. J Cell Biol. 1976 Apr;69(1):126–143. doi: 10.1083/jcb.69.1.126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Berger J. D. Gene expression and phenotypic change in Paramecium tetraurelia exconjugants. Genet Res. 1976 Apr;27(2):123–134. doi: 10.1017/s0016672300016335. [DOI] [PubMed] [Google Scholar]
  8. Burridge K., Phillips J. H. Association of actin and myosin with secretory granule membranes. Nature. 1975 Apr 10;254(5500):526–529. doi: 10.1038/254526a0. [DOI] [PubMed] [Google Scholar]
  9. Creutz C. E., Pazoles C. J., Pollard H. B. Identification and purification of an adrenal medullary protein (synexin) that causes calcium-dependent aggregation of isolated chromaffin granules. J Biol Chem. 1978 Apr 25;253(8):2858–2866. [PubMed] [Google Scholar]
  10. Creutz C. E., Pazoles C. J., Pollard H. B. Self-association of synexin in the presence of calcium. Correlation with synexin-induced membrane fusion and examination of the structure of synexin aggregates. J Biol Chem. 1979 Jan 25;254(2):553–558. [PubMed] [Google Scholar]
  11. Hiwatashi K., Haga N., Takahashi M. Restoration of membrane excitability in a behavioral mutant of Paramecium caudatum during conjugation and by microinjection of wild-type cytoplasm. J Cell Biol. 1980 Feb;84(2):476–480. doi: 10.1083/jcb.84.2.476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jockusch B. M., Burger M. M., DaPrada M., Richards J. G., Chaponnier C., Gabbiani G. alpha-Actinin attached to membranes of secretory vesicles. Nature. 1977 Dec 15;270(5638):628–629. doi: 10.1038/270628a0. [DOI] [PubMed] [Google Scholar]
  13. Knowles J. K. An improved microinjection technique in Paramecium aurelia. Transfer of mitochondria conferring erythromycin-resistance. Exp Cell Res. 1974 Sep;88(1):79–87. doi: 10.1016/0014-4827(74)90620-x. [DOI] [PubMed] [Google Scholar]
  14. Koizumi S. Microinjection and transfer of cytoplasm in Paramecium. Experiments on the transfer of kappa particles into cells at different stages. Exp Cell Res. 1974 Sep;88(1):74–78. doi: 10.1016/0014-4827(74)90619-3. [DOI] [PubMed] [Google Scholar]
  15. Novick P., Field C., Schekman R. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell. 1980 Aug;21(1):205–215. doi: 10.1016/0092-8674(80)90128-2. [DOI] [PubMed] [Google Scholar]
  16. Perasso R., Adoutte A. The process of selection of erythromycin-resistant mitochondria by erythromycin in Paramecium. J Cell Sci. 1974 May;14(3):475–497. doi: 10.1242/jcs.14.3.475. [DOI] [PubMed] [Google Scholar]
  17. Plattner H., Miller F., Bachmann L. Membrane specializations in the form of regular membrane-to-membrane attachment sites in Paramecium. A correlated freeze-etching and ultrathin-sectioning analysis. J Cell Sci. 1973 Nov;13(3):687–719. doi: 10.1242/jcs.13.3.687. [DOI] [PubMed] [Google Scholar]
  18. Plattner H., Reichel K., Matt H. Bivalent-cation-stimulated ATPase activity at preformed exocytosis sites in Paramecium coincides with membrane-intercalated particle aggregates. Nature. 1977 Jun 23;267(5613):702–704. doi: 10.1038/267702a0. [DOI] [PubMed] [Google Scholar]
  19. Pollack S. Mutations affecting the trichocysts in Paramecium aurelia. I. Morphology and description of the mutants. J Protozool. 1974 May;21(2):352–362. doi: 10.1111/j.1550-7408.1974.tb03669.x. [DOI] [PubMed] [Google Scholar]
  20. Ruiz F., Adoutte A., Rossignol M., Beisson J. Genetic analysis of morphogenetic processes in Paramecium. I. A mutation affecting trichocyst formation and nuclear division. Genet Res. 1976 Apr;27(2):109–122. doi: 10.1017/s0016672300016323. [DOI] [PubMed] [Google Scholar]

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