Skip to main content
Log in

Cytoskeleton-membrane interactions in the cnidocil complex of hydrozoan nematocytes

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Each cnidocil complex of the hydrozoans Tubularia larynx and Hydra vulgaris consists of 9 or 7–10 large stereovilli (=stereocilia), respectively, and a modified cilium, the cnidocil. The cnidocils comprise the regular 9 microtubule doublets, up to 30 additional microtubules, as well as a central filament body. Adjacent stereovilli are linked together by intermembrane connectors forming the stereovillar cone. The distal tips of the stereovilli surround the cnidocil in a closed tubular arrangement measuring up to 0.7 μm in length. Within this contact region the cnidocil is linked to the stereovillar tube by another set of intermembrane connectors, which seem to hold the cnidocil in a central position within the stereovillar cone. Stereovillar membrane and actin core are linked by 16-nm long cross bridges, which display a periodicity of 16 nm and emerge from the actin core. Within the cnidocils periodically arranged membrane-cytoskeleton bridges are uniformly restricted to the contact region. Here, 24-nm long cross bridges, which are spaced by a regular distance of 20 nm, interconnect the A-tubules of the microtubule doublets and the membrane. The cnidociliary membrane is differentiated into distinct domains as revealed by freeze-fracturing. Within the contact region of the nematocytes of Tubularia larynx, intramembrane particles are arranged in 9 rows of 700 nm length and 50 nm width, separated by particlefree areas. Intramembrane particles are irregularly distributed distal to the contact region. Considering recent physiological results we presume that the latter represent chemoreceptor units, while mechanical stimuli are transmitted via the intermembrane connectors and the microtubule-membrane bridges to mechanosensitive channels within the domain of the cnidociliary membrane in the contact region.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bone Q, Ryan KP (1978) Cupular sense organs in Ciona (Tunicata: Ascidiacea). J Zool 186:417–429

    Google Scholar 

  • Cormier SM, Hessinger DA (1980) Cnidocil apparatus: Sensory receptor of Physalia nematocytes. J Ultrastruct Res 72:13–19

    Google Scholar 

  • Ehlers U, Ehlers B (1977) Monociliary receptors in interstitial Proseriata and Neorhabdocoela (Turbellaria Neoophora). Zoomorphology 86:197–222

    Google Scholar 

  • Flock A (1971) Sensory transduction in hair cells. In: Evans EF, Wilson JP (eds) Handbook of sensory physiology of hearing. Academic Press, New York London,pp 17–25

    Google Scholar 

  • Gibbons IR (1981) Cilia and flagella of eukaryotes. J Cell Biol 91:107s-124s

    Google Scholar 

  • Gnatzy W, Tautz J (1980) Ultrastructure and mechanical properties of an insect mechanoreceptor: stimulus transmitting structures and sensory apparatus of the cercal filiform haris of Gryllus. Cell Tissue Res 213:441–463

    Google Scholar 

  • Golz R, Thurm U (1988) Membrane-cytoskeleton interactions in the cnidocil apparatus of Tubularia larynx (Hydroidea). Verh Dtsch Zool Ges 81:291–292

    Google Scholar 

  • Golz R, Thurm U (1990) Cnidocil regeneration in nematocytes of Hydra. Protoplasma 155:95–105

    Google Scholar 

  • Grain J (1986) The cytoskeleton in protists: nature, structure, and functions. Int Rev Cytol 104:153–249

    Google Scholar 

  • Gray EG (1960) The fine structure of the insect ear. Philos Trans R Soc Lond [Biol] 243:75–94

    Google Scholar 

  • Hausmann K, Holstein T (1985) Bilateral symmetry in the cnidocilnematost complex of the freshwater medusa Craspedacusta sowerbii Lankester (Hydrozoa, Limnomedusae). J Ultrastruct Res 90:89–104

    Google Scholar 

  • Herna'di L, Röhlich P (1988) Freeze-fracture study of the receptor membranes in the olfactory organ of Alburnus alburnus (Teleostei). Zoomorphology 108:41–46

    Google Scholar 

  • Hessinger DA, Ford MT (1988) Ultrastructure of the small cnidocyte of the Portuguese man-of-war (Physalia physalis) tentacle. In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts. Academic Press, New York, pp 75–94

    Google Scholar 

  • Holstein T, Hausmann K (1988) The cnidocil apparatus of hydrozoans: a progenitor of higher metazoan mechanoreceptors. In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts. Academic Press, New York, pp 53–73

    Google Scholar 

  • Holstein T, Tardent P (1984) An ultrahigh-speed analysis of exocytosis: nematocyst discharge. Science 223:830–833

    Google Scholar 

  • Hudspeth AJ (1985) The cellular basis of hearing: the biophysics of hair cells. Science 230:745–752

    Google Scholar 

  • Lenhoff HM (1983) Culturing large numbers of Hydra. In: Lenhoff HM (ed) Hydra: research methods. Plenum Press, New York London, pp 53–62

    Google Scholar 

  • Little KF, Neugebauer D-Ch (1985) Interconnections between the stereovilli of the fish inner ear. II. Systematic investigations of saccular hair bundles from Rutilus rutilus (Teleostei). Cell Tissue Res 242:427–432

    Google Scholar 

  • Mariscal RN, Bigger CH (1976) A comparison of putative sensory receptors associated with nematocysts in an anthozoan and a scyphozoan. In: Mackie GO (ed) Coelenterate ecology and behavior. Plenum Press, New York, pp 559–568

    Google Scholar 

  • Matsudaira PT, Burgess DR (1982) Organization of the cross-filaments in intestinal microvilli. J Cell Biol 92:657–664

    Google Scholar 

  • Menco BPM (1984) Ciliated and microvillous structures of rat olfactory and nasal respiratory epithelia. A study using ultrarapid cryo-fixation followed by freeze-substitution or freezeetching. Cell Tissue Res 235:225–241

    Google Scholar 

  • Menco BPM, Van der Wolk FM (1982) Freeze-fracture characteristics of insect gustatory and olfactory sensilla. I. A comparison with vertebrate olfactory receptor cells with special reference to ciliary components. Cell Tissue Res 223:1–27

    Google Scholar 

  • Neugebauer D-C, Thurm U (1984) Intra-and extracellular membrane connections in stereovilli from fish inner ear. An electron microscopic study. Verh Dtsch Zool Ges 77:313

    Google Scholar 

  • Neugebauer D-C, Thurm U (1987) Surface charges of the membane and cell adhesion substances determine the structural integrity of hair bundles from the inner ear of fish. Cell Tissue Res 249:199–207

    Google Scholar 

  • Osborne MP, Comis SD, Pickles JO (1984) Morphology and crosslinkage of stereocilia in the guinea pig labyrinth examined without the use of osmium as a fixative. Cell Tissue Res 237:43–48

    Google Scholar 

  • Pantin CFA (1942) The excitation of nematocysts. J Exp Biol 19:294–310

    Google Scholar 

  • Rüsch A, Thurm U (1988) Voltage-induced deflections of vestibular hair bundles: motor activity of the kinocilium? Pflügers Arch 411:R168

  • Rüsch A, Thurm U (1990) Spontaneous and electrically induced movements of ampullary kinocilia and stereovilli. Hear Res 48:247–264

    Google Scholar 

  • Schmidt B, Thurm U (1984) Structures transmitting stimulatory force to the sensory hairs (stereovilli) of the frog sacculus. Verh Dtsch Zool Ges 77:326

    Google Scholar 

  • Slauterback DB (1967) The cnidoblast-musculoepithelial cell complex in the tentacles of Hydra. Z Zellforsch 79:296–318

    Google Scholar 

  • Steinbrecht RA (1980) Cryofixation without cyroprotectants. Freeze substitution and freeze etching of an insect olfactory receptor. Tissue Cell 12:73–100

    Google Scholar 

  • Stidwill RP, Honegger TG (1989) A single layer of microtubules in the part of a complex cytoskeleton in mature nematocytes of Hydra. Tissue Cell 21:179–188

    Google Scholar 

  • Stidwill RP, Honegger TG, Tardent P (1988) Polymerized actin in the apical region of Hydra nematocytes. In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts. Academic Press, New York, pp 567–574

    Google Scholar 

  • Takumida M, Wersäll J, Bagger-Sjöbäck D (1988) Stereociliary glycocalyx and interconnections in the guinea pig vestibular organs. Acta Otolaryngol 106:130–139

    Google Scholar 

  • Teuchert G (1976) Sinneseinrichtungen bei Turbanella cornuta Remane (Gastrotricha). Zoomorphology 83:193–207

    Google Scholar 

  • Thorington GU, Hessinger DA (1988) Control of discharge: factors affecting discharge of cnidae. In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts. Academic Press, New York, pp 233–253

    Google Scholar 

  • Thurm U (1964) Mechanoreceptors in the cuticule of the honey bee: fine structure and stimulus mechanism. Science 145:1063–1065

    Google Scholar 

  • Thurm U (1983) Mechano-electrical transduction. In: Hoppe W, Lohmann W, Markl H, Ziegler H (eds) Biophysics. Springer, Berlin Heidelberg New York, pp 666–671

    Google Scholar 

  • Thurm U, Lawonn P (1990) The sensory properties of the cnidocil-aparatus as a basis for prey capture in Hydra attenuata. Verh Dtsch Zool Ges 83:431–432

    Google Scholar 

  • Thurm U, Erler G, Gödde J, Kastrup H, Keil Th, Völker W, Vohwinkel B (1983) Cilia specialized for mechanoreception. J Submicrosc Cytol 15:151–155

    Google Scholar 

  • Travis JL, Allen RD (1981) Studies on the motility of the Foraminifera. I. Ultrastructure of the reticulopodial network of Allogromia laticollaris (Arnold). J Cell Biol 90:211–221

    Google Scholar 

  • Watson GM, Hessinger DA (1988) Localization of a purported chemoreceptor involved in triggering cnida in sea anemones. In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts. Academic Press, New York, pp 255–272

    Google Scholar 

  • Westfall JA (1970) The nematocyte complex in hydromedusan, Gonionemus vertens. Z Zellforsch 110:457–470

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Golz, R., Thurm, U. Cytoskeleton-membrane interactions in the cnidocil complex of hydrozoan nematocytes. Cell Tissue Res 263, 573–583 (1991). https://doi.org/10.1007/BF00327291

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00327291

Key words

Navigation