Cell and Tissue Research

, Volume 259, Issue 3, pp 443–454 | Cite as

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

  • Emmanuelle Boisvieux-Ulrich
  • Marie-Christine Lainé
  • Daniel Sandoz


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.

Key words

Ciliogenesis Actin Microfilaments Cytochalasin D Coturnix coturnix japonica (Aves) 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Boisvieux-Ulrich E, Sandoz D, Chailley B (1977) A freeze-fracture and thin section study of the ciliary necklace in quail oviduct. Biol Cell 30:245–252Google Scholar
  2. Boisvieux-Ulrich E, Lainé M-C, Sandoz D (1984) Effets de la cytochalasine D sur la ciliogénèse dans l'oviducte de caille. Biol Cell 52:66aGoogle Scholar
  3. Boisvieux-Ulrich E, Lainé M-C, Sandoz D (1987) In vitro effects of benzodiazepines on ciliogenesis in the quail oviduct. Cell Motil Cytoskeleton 8:333–344PubMedGoogle Scholar
  4. Boisvieux-Ulrich E, Lainé M-C, Sandoz D (1989a) In vitro effects of taxol on ciliogenesis in the quail oviduct. J Cell Sci 92:9–20PubMedGoogle Scholar
  5. Boisvieux-Ulrich E, Lainé M-C, Sandoz D (1989b) In vitro effects of colchicine and nocodazole on ciliogenesis in the quail oviduct. Biol Cell 67:67–79PubMedGoogle Scholar
  6. Bornens M, Karsenti E (1984) The centrosome. In: Bittar EE (ed) Membrane, structure and function, vol 6. Wiley, New York, pp 100–171Google Scholar
  7. Brett JG, Godman GC (1984a) Macrovacuolation induced by cytochalasin: its relation to the cytoskeleton; morphological and cytochemical observations. Tissue Cell 16:311–324PubMedGoogle Scholar
  8. Brett JG, Godman GC (1984b) Membrane cycling and macrovacuolation under the influence of cytochalasin: kinetic and morphometric studies. Tissue Cell 16:325–335PubMedGoogle Scholar
  9. Brett JG, Godman GC (1986) Cytoskeletal organization affects cellular responses to cytochalasins: comparison of a normal line and its transformant. Tissue Cell 18:175–199PubMedGoogle Scholar
  10. 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 53:195–198PubMedGoogle Scholar
  11. 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 18:383–400Google Scholar
  12. Chailley B, Boisvieux-Ulrich E, Sandoz D (1982) Ciliary events during ciliogenesis in quail oviduct. Biol Cell 46:51–64Google Scholar
  13. Chailley B, Bork K, Gounon P, Sandoz D (1986) Immunological detection of actin in isolated cilia from quail oviduct. Biol Cell 58:43–52PubMedGoogle Scholar
  14. 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 93:683–690PubMedGoogle Scholar
  15. Chailley B, Nicolas G, Lainé M-C (1989b) Organization of actin microfilaments in the apical border of oviduct ciliated cells. Biol Cell 67:81–90PubMedGoogle Scholar
  16. Cooper JA (1987) Effects of cytochalasin and phalloidin on actin. Minireview. J Cell Biol 105:1473–1478PubMedGoogle Scholar
  17. 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 18:685–700PubMedGoogle Scholar
  18. 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 10:451–462PubMedGoogle Scholar
  19. Dentler WL (1980) Structures linking the tips of ciliary and flagellar microtubules to the membrane. J Cell Sci 42:207–220PubMedGoogle Scholar
  20. Dentler WL (1984) Attachment of the cap to the central microtubules ofTetrahymena cilia. J Cell Sci 66:167–178PubMedGoogle Scholar
  21. 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 2:549–572PubMedGoogle Scholar
  22. 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 74:747–759PubMedGoogle Scholar
  23. Euteneuer U, Schliwa M (1985) Evidence for an involvement of actin in the positioning and motility of centrosomes. J Cell Biol 101:96–103PubMedGoogle Scholar
  24. 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 22:733–744PubMedGoogle Scholar
  25. 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 22:745–754PubMedGoogle Scholar
  26. Gordon RE, Lane BP, Miller F (1980) Identification of contractile proteins in basal bodies of ciliated tracheal epithelial cells. J Histochem Cytochem 28:1189–1197PubMedGoogle Scholar
  27. 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 103:613–620PubMedGoogle Scholar
  28. LeCluyse EL, Dentler WL (1984) Asymmetrical microtubule capping structures in frog palate cilia. J Ultrastruct Res 86:75–78PubMedGoogle Scholar
  29. 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 16:47–48Google Scholar
  30. Lemullois M, Gounon P, Sandoz D (1987a) Relationship between cytokeratin filaments and centriolar derivatives in the quail oviduct. Biol Cell 61:39–49PubMedGoogle Scholar
  31. Lemullois M, Klotz C, Sandoz D (1987b) Immunocytochemical localization of myosin during ciliogenesis in quail oviduct. Eur J Cell Biol 43:429–437PubMedGoogle Scholar
  32. 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 63:195–208PubMedGoogle Scholar
  33. Miranda AF, Godman GC, Tannenbaum SW (1974) Action of cytochalasin D on cells of established lines. II. Cortex and microfilaments. J Cell Biol 62:406–423PubMedGoogle Scholar
  34. 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–112sGoogle Scholar
  35. 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 103:1751–1765PubMedGoogle Scholar
  36. 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 104:1527–1537PubMedGoogle Scholar
  37. 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 177–185Google Scholar
  38. Piperno G, Luck DJL (1979) An actin-like protein is a component of axonemes fromChlamydomonas flagella. J Biol Chem 254:2187–2190PubMedGoogle Scholar
  39. Portman RW, LeCluyse EL, Dentler WL (1987) Development of microtubule capping structures in ciliated epithelial cells. J Cell Sci 87:85–94PubMedGoogle Scholar
  40. Remillard SP, Witman GB (1982) Synthesis, transport, and utilization of specific flagellar proteins during flagellar regeneration inChlamydomonas. J Cell Biol 93:615–631PubMedGoogle Scholar
  41. 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 79:3198–3202PubMedGoogle Scholar
  42. 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 63:183–193PubMedGoogle Scholar
  43. 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 11:248–259PubMedGoogle Scholar
  44. Schliwa M (1982) Action of cytochalasin D on skeletal networks. J Cell Biol 92:79–81PubMedGoogle Scholar
  45. Schliwa M, Pryzwansky KB, Euteneuer U (1982) Centrosome splitting in neutrophils: an unusual phenomenon related to cell activation and motility. Cell 31:705–717PubMedGoogle Scholar
  46. Stephens RE, Oleszko-Szuts S, Linck RW (1989) Retention of ciliary ninefold structure after removal of microtubules. J Cell Sci 92:391–402PubMedGoogle Scholar
  47. Tamm S, Tamm SL (1986) Centriole migration, actin bundles, and formation of macrocilia in the ctenophoreBeroë. J Cell Biol 103:281aGoogle Scholar
  48. Tamm S, Tamm SL (1988a) Development of macrociliary cells inBeroë. I. Actin bundles and centriole migration. J Cell Sci 89:67–80PubMedGoogle Scholar
  49. Tamm SL, Tamm S (1988b) Development of macrociliary cells inBeroë. II. Formation of macrocilia. J Cell Sci 89:81–95PubMedGoogle Scholar
  50. 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 102:285–297PubMedGoogle Scholar
  51. Witman GB (1975) The site of in vivo assembly of flagellar microtubules. Ann NY Acad Sci 253:178–191PubMedGoogle Scholar
  52. Woda R, Godman G, Berl S (1977) Cytochalasin D-induced redistribution of actin in normal and neoplastic cells. J Histochem Cytochem 25:238aGoogle Scholar
  53. Wrenn TJ, Wessels NK (1970) Cytochalasin B: effects upon microfilaments involved in morphogenesis of estrogen-induced glands of oviduct. Proc Natl Acad Sci USA 66:904–908PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • Emmanuelle Boisvieux-Ulrich
    • 1
  • Marie-Christine Lainé
    • 1
  • Daniel Sandoz
    • 1
  1. 1.Paris and Centre de Biologie Cellulaire, CNRSUniversité Pierre et Marie CurieIvrysur-Seine CedexFrance

Personalised recommendations