Hostname: page-component-848d4c4894-8bljj Total loading time: 0 Render date: 2024-06-26T01:29:43.286Z Has data issue: false hasContentIssue false

The cell cortex during ciliate morphogenesis and ciliogenesis

Published online by Cambridge University Press:  19 September 2011

Linda A. Hufnagel
Affiliation:
Department of Microbiology, University of Rhode Island, Kingston, RI 02881, U.S.A.
Get access

Abstract

The cell cortex of a ciliated protozoan contains most of the structure that defines the shape and pattern of the organism. The ciliate cell cortex is composed of both cytoskeletal and membranous components. While the assembly of the cytoskeleton is believed to account for the major part of the development of shape and pattern in this cell (as in all eukaryotic cells), the contribution of membranes to the development of cellular architecture in ciliates is poorly understood. Also, how the cortical membranes are assembled and how this assembly is coordinated with cytoskeletal assembly are virtually unknown. Furthermore, membranes have several unique properties which could be useful in the storage and utilization of blueprints for cellular architecture. Freeze-fracture and freeze-etch electron microscopy provide ways to characterize the molecular architecture and assembly of membranes during development. Efforts are being made to apply these methods to an analysis of morphogenesis and ciliogenesis in Tetrahymena. The results of these studies ar summarized and their possible implications regarding the role of membranes in ciliate morphogenesis are discussed.

Résumé

Le cortex cellulaire des protozoaires ciliés contient la plupart des structures qui définissent la forme et le motif de l'organisme. Le cortex cellulaire des ciliés est composé à la fois d'éléments cytosquelettaux et membranaires. Alors que 'on pense que l'assemblement du cytosquelette joue un rôle dans la majeure partie du développement de la forme et du motif de ces cellules (comme dans toutes les cellules eucaryotes), la contribution des membranes au développement de l'architecture cellulaire chez les ciliés est mal connue. De mème, la maniere dont les membranes corticales sont assemblées et la manière dont cet assemblement est coordonné avec l'assemblement du cytosquelette sont virtuellement inconnues. De plus, les membranes ont plusieurs propriétés particulières qui pourraient être utiles au stockage et à l'utilisation des plans de l'architecture cellulaire. La microscopie électronique de ‘freeze-fracture’ et de ‘freeze-etch’ fournit des moyens pour caractériser l'architecture moléculaire et l'assemblement des membranes durant le développment. Des efforts sont mis en oeuvre pour appliquer ces méthodes à l'analyse de la morphogenése et de la ciliogenèse chez Tetrahymena. Les résultats de ces études sont résumés et leurs possibles implications quant au rôle des membranes dans la morphogenèse des ciliés sont discutées.

Type
Research Article
Copyright
Copyright © ICIPE 1986

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Allen, R. D. (1978a) Particle arrays in the surface membrane of Paramecium: junctional and possible sensory sites. J. Ultrastruct. Res. 63, 6478.CrossRefGoogle ScholarPubMed
Allen, R. D. (1978b) Membranes of ciliates: ultrastructure, biochemistry and fusion. In Membrane Fusion (Edited by Poste, G. and Nicolson, G. L.), pp. 657763. Elsevier/North-Holland Biomedical Press, New York.Google Scholar
Allen, R. D. and Wolfe, R. W. (1974) The cytoproct of Paramecium caudatum: structure and function, microtubules, and the fate of food vacuole membranes. J. Cell Sci. 14, 611631.CrossRefGoogle ScholarPubMed
Allen, R. D. and Wolfe, R. W. (1979) Membrane recycling at the cytoproct of Telrahymena. J. Cell Sci. 35, 217227.CrossRefGoogle Scholar
Aufderheide, K. J., Frankel, J. and Williams, N. E. (1980) Formation and positioning of surface-related structures in Protozoa. Microbiol. Rev. 44, 252302.CrossRefGoogle ScholarPubMed
Barbosa, M. L. F. and Pinto da Silva, P. (1983) Restriction of glycolipids to the outer half of a plasma membrane: Concanavalin A labeling of membrane halves in Acanthamoeba castellanii. Cell 33, 959966.CrossRefGoogle Scholar
Bardele, C. F. (1983) Mapping of highly ordered membrane domains in the plasma membrane of the ciliate Cyclidium glaucoma. J. Cell Sci. 61, 130.CrossRefGoogle ScholarPubMed
Beisson, J. and Sonneborn, T. M. (1965) Cytoplasmic inheritance of the organization of the cell cortex in Paramecium aurelia. Proc. natn. Acad. Sci. U.S.A. 53, 275282.Google Scholar
Deterra, N. (1982) Self-assembly mechanisms and control of development in Stentor and Paramecium. In Developmental Order: Its Origin and Regulation, pp. 165182. Alan R. Liss, New York.Google Scholar
Frankel, J. (1970) The synchronization of oral development without cell division in Tetrahymena pyriformis GL-C. J. exp. Zool. 173, 79100.Google Scholar
Frankel, J. (1979) An analysis of cell-surface patterning in Tetrahymena. In Determinants of Spatial Organization (Edited by Subtelney, S. and Konigsberg, I. R.), pp. 215246. Academic Press, New York.Google Scholar
Frankel, J. (1984) Pattern formation in ciliated protozoa. In Pattern formation. A Primer in Developmental Biology (Edited by Malacinski, G. M. and Bryant, S. V.), pp. 163196. Macmillan, New York.Google Scholar
Frankel, J. and Jenkins, L. M. (1979) A mutant of Tetrahymena thermophila with a partial mirror-image duplication of cell surface pattern II. Nature of genie control. J. Embryol. expl. Morph. 49, 203227.Google Scholar
Gershon, W. D., Demsey, A. and Stackpole, C. W. (1979) Analysis of local order in the spatial distribution of cell surface molecular assemblies. Expl Cell Res. 122, 115126.Google Scholar
Gilula, N. B. and Satir, P. (1972) The ciliary necklace: a ciliary membrane specialization. J. Cell Biol. 53, 494509.Google Scholar
Golinska, K. (1984) Diminution of microtubular organelles after experimental reduction in cell size in the ciliate, Dileptus. J. Cell Sci. 70, 2539.CrossRefGoogle ScholarPubMed
Heuser, J. E. and Cooke, R. (1983) Actin-myosin interactions visualized by the quick-freeze, deep-etch replica technique. J. molec. Biol. 169, 97122.CrossRefGoogle ScholarPubMed
Heuser, J. E., Reese, T. S., Dennis, M. J., Jan, Y., Jan, L. and Evans, L. (1979) Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J. Cell Biol. 81, 275300.Google Scholar
Hufnagel, L. A. (1981a) Particle assemblies in the plasma membrane of Tetrahymena: relationship to cell surface topography and cellular morphogenesis. J. Protozool. 28, 192203.CrossRefGoogle Scholar
Hufnagel, L. A. (1981b) External manifestation of plate-like particle arrays in the plasma membrane of Tetrahymena. Cell Biol. Int. Rept. 5, 581586.CrossRefGoogle ScholarPubMed
Hufnagel, L. A. (1981c) Freeze-fracture analysis of a morphologically disorganized mutant of Tetrahymena thermophila. J. Cell Biol. 90, 105a.Google Scholar
Hufnagel, L. A. (1982a) Mechanisms for assembly of membrane structure during morphogenesis in Tetrahymena: Freeze-fracture evidence. J. Cell Biol. 95, 269a.Google Scholar
Hufnagel, L. A. (1982b) Some membrane structural changes accompanying morphogenetic changes in Tetrahymena. Biol. Bull. 163, 359.Google Scholar
Hufnagel, L. A. (1983a) Freeze-fracture analysis of membrane events during early neogenesis of cilia in Tetrahymena: changes in fairyring morphology and membrane topography. J. Cell Sci. 60, 137156.Google Scholar
Hufnagel, L. A. (1983b) Automated image analysis applied to freeze-fracture replicas of Tetrahymena. Proceedings of the 41st Annual Meeting EMSA, pp. 638639.CrossRefGoogle Scholar
Hufnagel, L. A. (1983c) Fully automated image analysis can be used to study intramembranous particle (IMP) behavior during development in Tetrahymena. Biol. Bull. 165, 491492.Google Scholar
Hufnagel, L. A. (1984a) Membrane particle (IMP) frequency and distribution in starved versus fed Tetrahymena plasma membranes using fully automated computerassisted image analysis. International Cell Biology 1984 (abstr. of the Third International Congress on Cell Biology, Tokyo, Japan), p. 299.Google Scholar
Hufnagel, L. A. (1984b) Analysis of freeze-fracture (FF) replicas of developing cells using computer assisted, fully automated image analysis. Eur. J. Cell Biol. 33, 11.Google Scholar
Hufnagel-Zackroff, L. A. (1984) Small intramembranous particle (IMP) rosettes in the ciliary plasma membrane of Tetrahymena thermophila. J. Cell Biol. 99, 285a.Google Scholar
Jerka-Dziadosz, M. (1976) The proportional regulation of cortical structures in a hypotrich ciliate Paraurostyla weissei. J. exp. Zool. 195, 114.Google Scholar
Johansson, L. B.-A. and Lindblom, G. (1980) Orientation and mobility of molecules in membranes studied by polarized light spectroscopy. Q. Rev. Biophys. 13, 63118.CrossRefGoogle ScholarPubMed
Kaczanowska, J. and Dubielecka, B. (1983) Pattern determination and pattern regulation in Paramecium tetraurelia. J. Embryol. exp. Morph. 74, 4768.Google Scholar
Kitajima, Y. and Thompson, G. A. Jr (1977) Tetrahymena strives to maintain the fluidity interrelationship of all its membranes constant. Electron microscope evidence. J. Cell Biol. 72, 744755.CrossRefGoogle ScholarPubMed
McCloskey, M. and Poo, M.-M. (1984) Protein diffusion in cell membranes: some biological implications. Int. Rev. Cytol. 87, 1981.CrossRefGoogle ScholarPubMed
Nilsson, J. R. and Behnke, O. (1971) Studies on a surface coat of Tetrahymena. J. Ultrastruct. Res. 36, 542544.Google Scholar
Pinto da Silva, P., Kachar, B., Torrisi, M. R., Brown, C. and Parkinson, C. (1981) Freeze-fracture cytochemistry: replicas of critical point dried cells and tissues after ‘fracture-label’. Science U.S.A. 213, 230233.Google Scholar
Pitelka, D. R. (1965) New observations on cortical ultrastructure in Paramecium. J. Microsc. 4, 373394.Google Scholar
Plattner, H. (1975) Ciliary granule plaques: membraneintercalated particle aggregates associated with Ca2+-binding sites in Paramecium. J. Cell Sci. 18, 257269.CrossRefGoogle ScholarPubMed
Plattner, H., Reichel, K., Matt, H., Beisson, J., Lefort-Tran, M. and Pouphile, M. (1980) Genetic disection of the final exocytosis steps in Paramecium tetraurelia cells: cytochemical determination of Ca2+-ATPase activity over preformed exocytosis sites. J. Cell Sci. 46, 1740.CrossRefGoogle Scholar
Rash, J. E. and Hudson, C. S. (Eds) (1979) Freeze-Fracture: Methods, Artifacts, and Interpretations. Raven Press, New York.Google Scholar
Rash, J. E., Johnson, T. J. A., Hudson, C. S., Giddings, F. D., Graham, W. F. and Eldefrawi, M. E. (1982) Labelledreplica techniques: post-shadow labelling of intramembrane particles in freeze-fracture replies. J. Microsc. 128, 121138.Google Scholar
Rosenbaum, J. L. and Carlson, K. (1969) Cilia regeneration in Tetrahymena and its inhibition by colchicine. J. Cell Biol. 40, 415425.Google Scholar
Satir, B. H. (1977) Dibucaine-induced synchronous mucocyst secretion in Tetrahymena. Cell Biol. Int. Rept. 1, 6973.CrossRefGoogle ScholarPubMed
Satir, B. H. and Oberg, S. G. (1978) Paramecium fusion rosettes: possible function as Ca2+ gates. Science U.S.A. 199, 536538.Google Scholar
Satir, B., Sale, W. S. and Satir, P. (1976) Membrane renewal after dibucaine deciliation of Tetrahymena. Exp. Cell Res. 97, 8391.CrossRefGoogle ScholarPubMed
Satir, B., Schooley, C. and Satir, P. (1972) Membrane reorganization during secretion in Tetrahymena. Nature, Lond. 235, 5354.Google Scholar
Scott, S. M. and Hufnagel, L. A. (1983) The effect of Concanavalin A on egestion of food vacuoles in Tetrahymena. Expl Cell Res. 144, 429441.CrossRefGoogle ScholarPubMed
Singer, S. J. and Nicolson, G. L. (1972) The fluid mosaic model of the structure of cell membranes. Science, Wash. D.C. 175, 720731.CrossRefGoogle ScholarPubMed
Thompson, G., Baugh, L. and Walker, L. (1974) Non-lethal deciliation of Tetrahymena by a local anaesthetic and its utility as a tool for studying cilia regeneration. J. Cell Biol. 61, 253257.CrossRefGoogle Scholar
Tucker, J. B. (1977) Shape and pattern specification during microtubule bundle assembly. Nature 266, 2226.Google Scholar
Williams, N. E., Subbaiah, P. V. and Thompson, G. A. Jr (1980) Studies of membrane formation in Tetrahymena. J. biol. Chem. 255, 296303.CrossRefGoogle ScholarPubMed
Williams, N. E., Vaudaux, P. E. and Skriver, L. (1979) Cytoskeletal proteins of the cell surface in Tetrahymena. I. Identification and localization of major proteins. Expl Cell Res. 123, 311320.CrossRefGoogle ScholarPubMed
Wolfe, J. and Grimes, G. W. (1979) Tip transformation in Tetrahymena: a morphogenetic response to interactions between mating types. J. Protozool. 26, 8289.CrossRefGoogle Scholar
Wunderlich, F. and Ronai, A. (1975) Adaptive lowering of the lipid clustering temperature within Tetrahymena membranes. FEBS Lett. 55, 237241.CrossRefGoogle ScholarPubMed
Wunderlich, F. and Speth, V. (1972) Membranes in Tetrahymena. I. The cortical pattern. J. Ultrastruct. Res. 41, 258269.Google Scholar