Skip to main content
SpringerLink
Log in

Cytochalasin D inhibits basal body migration and ciliary elongation in quail oviduct epithelium

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

Summary

The effects of cytochalasin D (CD) were studied by scanning (SEM) and transmission (TEM) electron-microscopic examination at different stages of ciliary differentiation in epithelial cells of quail oviduct. Immature quails were prestimulated by estradiol benzoate injections to induce ciliogenesis in the undifferentiated oviduct. After 24 h of CD culture, SEM study revealed inhibition of ciliogenesis and dilation of the apex of non-ciliated cells. TEM study showed that 2 h of CD treatment produced dilation of lateral intercellular spaces, after 6 h of treatment, this resulted in intracellular macrovacuolation. Vacuoles were surrounded by aggregates of dense felt-like material. CD also induced the disappearance of microvilli, and rounding of the apical surface of undifferentiated cells and those blocked in ciliogenesis. Centriologenesis was not inhibited by CD; basal bodies assembled in generative complexes in the supranuclear region after 24 h of treatment. However, the migration of mature basal bodies towards the apical surface was impaired. Instead, they anchored onto the membrane of intracellular vacuoles; growth of cilia was induced in the vacuole lumen. Cilium elongation was disturbed, giving abnormally short cilia with a dilated tip; microtubules failed to organize correctly.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Boisvieux-Ulrich E, Sandoz D, Chailley B (1977) A freeze-fracture and thin section study of the ciliary necklace in quail oviduct. Biol Cell 30:245–252

    Google Scholar 

  • Boisvieux-Ulrich E, Lainé M-C, Sandoz D (1984) Effets de la cytochalasine D sur la ciliogénèse dans l'oviducte de caille. Biol Cell 52:66a

    Google Scholar 

  • Boisvieux-Ulrich E, Lainé M-C, Sandoz D (1987) In vitro effects of benzodiazepines on ciliogenesis in the quail oviduct. Cell Motil Cytoskeleton 8:333–344

    PubMed  Google Scholar 

  • Boisvieux-Ulrich E, Lainé M-C, Sandoz D (1989a) In vitro effects of taxol on ciliogenesis in the quail oviduct. J Cell Sci 92:9–20

    PubMed  Google Scholar 

  • Boisvieux-Ulrich E, Lainé M-C, Sandoz D (1989b) In vitro effects of colchicine and nocodazole on ciliogenesis in the quail oviduct. Biol Cell 67:67–79

    PubMed  Google Scholar 

  • Bornens M, Karsenti E (1984) The centrosome. In: Bittar EE (ed) Membrane, structure and function, vol 6. Wiley, New York, pp 100–171

    Google Scholar 

  • Brett JG, Godman GC (1984a) Macrovacuolation induced by cytochalasin: its relation to the cytoskeleton; morphological and cytochemical observations. Tissue Cell 16:311–324

    PubMed  Google Scholar 

  • Brett JG, Godman GC (1984b) Membrane cycling and macrovacuolation under the influence of cytochalasin: kinetic and morphometric studies. Tissue Cell 16:325–335

    PubMed  Google Scholar 

  • Brett JG, Godman GC (1986) Cytoskeletal organization affects cellular responses to cytochalasins: comparison of a normal line and its transformant. Tissue Cell 18:175–199

    PubMed  Google Scholar 

  • Busson-Mabillot S, Chambaut-Guérin A-M, Huleux-Maurs C, Ovtracht L, Rossignol B (1985) Cytochalasin D suppressesβ-induced protein discharge without inhibiting membrane fusion. Biol Cell 53:195–198

    PubMed  Google Scholar 

  • Carasso N, Favard P, Bourguet J (1973) Action de la cytochalasin B sur la réponse hydrosmotique et l'ultrastructure de la vessie de grenouille. J Miscrosc 18:383–400

    Google Scholar 

  • Chailley B, Boisvieux-Ulrich E, Sandoz D (1982) Ciliary events during ciliogenesis in quail oviduct. Biol Cell 46:51–64

    Google Scholar 

  • Chailley B, Bork K, Gounon P, Sandoz D (1986) Immunological detection of actin in isolated cilia from quail oviduct. Biol Cell 58:43–52

    PubMed  Google Scholar 

  • Chailley B, Frappier T, Regnouf F, Lainé M-C (1989a) Immunological detection of spectrin during differentiation and in mature ciliated cells from quail oviduct. J Cell Sci 93:683–690

    PubMed  Google Scholar 

  • Chailley B, Nicolas G, Lainé M-C (1989b) Organization of actin microfilaments in the apical border of oviduct ciliated cells. Biol Cell 67:81–90

    PubMed  Google Scholar 

  • Cooper JA (1987) Effects of cytochalasin and phalloidin on actin. Minireview. J Cell Biol 105:1473–1478

    PubMed  Google Scholar 

  • Davis WL, Goodman BP (1986) Antidiuretic hormone response in the amphibian urinary bladder: time course of cytochalasininduced vacuole formation, an ultrastructural study employing ruthenium red. Tissue Cell 18:685–700

    PubMed  Google Scholar 

  • Davis WL, Goodman DBP, Jones RG, Rasmussen H (1978) The effects of cytochalasin B on the surface morphology of the toad urinary bladder epithelium: a scanning electron microscopic study. Tissue Cell 10:451–462

    PubMed  Google Scholar 

  • Dentler WL (1980) Structures linking the tips of ciliary and flagellar microtubules to the membrane. J Cell Sci 42:207–220

    PubMed  Google Scholar 

  • Dentler WL (1984) Attachment of the cap to the central microtubules ofTetrahymena cilia. J Cell Sci 66:167–178

    PubMed  Google Scholar 

  • Dentler WL, LeCluyse EL (1982) Microtubule capping structures at the tips of tracheal cilia: evidence for their firm attachment during ciliary bend formation and the restriction of microtubule sliding. Cell Motil 2:549–572

    PubMed  Google Scholar 

  • Dentler WL, Rosenbaum JL (1977) Flagellar elongation and shortening inChlamydomonas. III. Structures attached to the tips of flagellar microtubules and their relationship to the directionality of flagellar microtubule assembly. J Cell Biol 74:747–759

    PubMed  Google Scholar 

  • Euteneuer U, Schliwa M (1985) Evidence for an involvement of actin in the positioning and motility of centrosomes. J Cell Biol 101:96–103

    PubMed  Google Scholar 

  • Godman G, Woda B, Kolberg R (1980a) Redistribution of contractile and cytoskeletal components induced by cytochalasin. I. In Hmf cells, a nontransformed fibroblastoid line. Eur J Cell Biol 22:733–744

    PubMed  Google Scholar 

  • Godman G, Woda B, Kolberg R (1980b) Redistribution of contractile and cytoskeletal components induced by cytochalasin. II. In HeLa and HEp2 cells. Eur J Cell Biol 22:745–754

    PubMed  Google Scholar 

  • Gordon RE, Lane BP, Miller F (1980) Identification of contractile proteins in basal bodies of ciliated tracheal epithelial cells. J Histochem Cytochem 28:1189–1197

    PubMed  Google Scholar 

  • Klotz C, Bordes N, Lainé M-C, Sandoz D, Bornens M (1986) Myosin at the apical pole of the ciliated epithelial cells as revealed by a monoclonal antibody. J Cell Biol 103:613–620

    PubMed  Google Scholar 

  • LeCluyse EL, Dentler WL (1984) Asymmetrical microtubule capping structures in frog palate cilia. J Ultrastruct Res 86:75–78

    PubMed  Google Scholar 

  • Lemullois M, Gounon P, Lainé M-C, Nicolas G, Klotz C, Sandoz D (1984) Differentiation of cytoskeleton during ciliogenesis in quail oviduct. J Submicrosc Cytol 16:47–48

    Google Scholar 

  • Lemullois M, Gounon P, Sandoz D (1987a) Relationship between cytokeratin filaments and centriolar derivatives in the quail oviduct. Biol Cell 61:39–49

    PubMed  Google Scholar 

  • Lemullois M, Klotz C, Sandoz D (1987b) Immunocytochemical localization of myosin during ciliogenesis in quail oviduct. Eur J Cell Biol 43:429–437

    PubMed  Google Scholar 

  • Lemullois M, Boisvieux-Ulrich E, Lainé M-C, Chailley B, Sandoz D (1988) Development and functions of the cytoskeleton during ciliogenesis in metazoa. Biol Cell 63:195–208

    PubMed  Google Scholar 

  • Miranda AF, Godman GC, Tannenbaum SW (1974) Action of cytochalasin D on cells of established lines. II. Cortex and microfilaments. J Cell Biol 62:406–423

    PubMed  Google Scholar 

  • Mooseker MS, Bonder EM, Conzelman KA, Fishkind DJ, Howe CJ, Keller TCS (1984) The brush border cytoskeleton and integration of cellular functions. J Cell Biol 99:104s–112s

    Google Scholar 

  • Nelson WJ, Veshnock PJ (1986) Dynamics of membrane-skeleton (fodrin) organization during development of polarity in Madin-Darby canine kidney epithelial cells. J Cell Biol 103:1751–1765

    PubMed  Google Scholar 

  • Nelson WJ, Veshnock PJ (1987) Modulation of fodrin (membrane skeleton) stability by cell-cell contact in Madin Darby canine kidney epithelial cells. J Cell Biol 104:1527–1537

    PubMed  Google Scholar 

  • Nève P, Rocmans P, Ketelbant-Balasse P (1975) Microtubules and microtubule inhibitors and cytochalasin in the thyroid gland. In: Borgers M, DeBrabander (eds) Microtubules and microtubule inhibitors. North-Holland, Amsterdam, pp 177–185

    Google Scholar 

  • Piperno G, Luck DJL (1979) An actin-like protein is a component of axonemes fromChlamydomonas flagella. J Biol Chem 254:2187–2190

    PubMed  Google Scholar 

  • Portman RW, LeCluyse EL, Dentler WL (1987) Development of microtubule capping structures in ciliated epithelial cells. J Cell Sci 87:85–94

    PubMed  Google Scholar 

  • Remillard SP, Witman GB (1982) Synthesis, transport, and utilization of specific flagellar proteins during flagellar regeneration inChlamydomonas. J Cell Biol 93:615–631

    PubMed  Google Scholar 

  • Sandoz D, Gounon P, Karsenti E, Sauron M-E (1982) Immunocytochemical localization of tubulin, actin, and myosin in axonemes of ciliated cells from quail oviduct. Proc Natl Acad Sci USA 79:3198–3202

    PubMed  Google Scholar 

  • Sandoz D, Chailley B, Boisvieux-Ulrich E, Lemullois M, Lainé M-C, Bautista-Harris G (1988) Organization and functions of cytoskeleton in metazoan ciliated cells. Biol Cell 63:183–193

    PubMed  Google Scholar 

  • Schatten H, Walter M, Biessmann H, Schatten G (1988) Microtubules are required for centrosome expansion and positioning while microfilaments are required for centrosome separation in sea urchin eggs during fertilization and mitosis. Cell Motil Cytoskeleton 11:248–259

    PubMed  Google Scholar 

  • Schliwa M (1982) Action of cytochalasin D on skeletal networks. J Cell Biol 92:79–81

    PubMed  Google Scholar 

  • Schliwa M, Pryzwansky KB, Euteneuer U (1982) Centrosome splitting in neutrophils: an unusual phenomenon related to cell activation and motility. Cell 31:705–717

    PubMed  Google Scholar 

  • Stephens RE, Oleszko-Szuts S, Linck RW (1989) Retention of ciliary ninefold structure after removal of microtubules. J Cell Sci 92:391–402

    PubMed  Google Scholar 

  • Tamm S, Tamm SL (1986) Centriole migration, actin bundles, and formation of macrocilia in the ctenophoreBeroë. J Cell Biol 103:281a

    Google Scholar 

  • Tamm S, Tamm SL (1988a) Development of macrociliary cells inBeroë. I. Actin bundles and centriole migration. J Cell Sci 89:67–80

    PubMed  Google Scholar 

  • Tamm SL, Tamm S (1988b) Development of macrociliary cells inBeroë. II. Formation of macrocilia. J Cell Sci 89:81–95

    PubMed  Google Scholar 

  • Weber K, Rathke PC, Osborn M, Franke WW (1976) Distribution of actin and tubulin in cells and in glycerinated cell models after treatment with cytochalasin B (CB). Exp Cell Res 102:285–297

    PubMed  Google Scholar 

  • Witman GB (1975) The site of in vivo assembly of flagellar microtubules. Ann NY Acad Sci 253:178–191

    PubMed  Google Scholar 

  • Woda R, Godman G, Berl S (1977) Cytochalasin D-induced redistribution of actin in normal and neoplastic cells. J Histochem Cytochem 25:238a

    Google Scholar 

  • Wrenn TJ, Wessels NK (1970) Cytochalasin B: effects upon microfilaments involved in morphogenesis of estrogen-induced glands of oviduct. Proc Natl Acad Sci USA 66:904–908

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Paris and Centre de Biologie Cellulaire, CNRS, Université Pierre et Marie Curie, 67 rue Maurice Günsbourg, F-94205, Ivrysur-Seine Cedex, France

    Emmanuelle Boisvieux-Ulrich, Marie-Christine Lainé & Daniel Sandoz

Authors
  1. Emmanuelle Boisvieux-Ulrich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marie-Christine Lainé
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daniel Sandoz
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Boisvieux-Ulrich, E., Lainé, MC. & Sandoz, D. Cytochalasin D inhibits basal body migration and ciliary elongation in quail oviduct epithelium. Cell Tissue Res. 259, 443–454 (1990). https://doi.org/10.1007/BF01740770

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01740770

Key words

Search

Navigation