Skip to main content
Log in

Schwann cell proliferation in the sciatic nerve of hypothyroid chick embryos studied by autoradiography and image analysis

  • Published:
Journal of Neurocytology

Summary

The proliferation of Schwann cells in the sciatic nerve of chick was studied from day 11 to day 27 of development in control and thyroid-deficient embryos. Hypothyroidism was induced by tetramethylthiourea injection on days 8 and 19 of incubation. The parameters of the cell cycle were determined using autoradiographs (tritiated thymidine) and by image analysis of Feulgen-stained nuclear smears. The duration of the cell cycle was lengthened and the growth fraction was reduced in hypothyroid animals, at 11 and 15 days of incubation. At later stages (days 21 and 27), these parameters were not significantly different from the controls as if the sensitivity of Schwann cells to thyroid hormones was scheduled to occur during a limited period of development. The total number of axons was the same in control and hypothyroid animals suggesting that the slowing down of Schwann cell proliferation is not a consequence of neuronal cell death. The consequence of that slowing down is a delay in the isolation of promyelin axons and a reduction in the proportion of myelinated axons at all the stages studied.

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

  • Allt, G. (1969) Ultrastructural features of the immature peripheral nerve.Journal of Anatomy 105, 283–93.

    Google Scholar 

  • Almazan, G., Honegger, P. &Matthieu, J. M. (1985) Triiodothyronine stimulation of oligodendroglial differentiation and myelination. A development study.Developmental Neuroscience 7, 45–54.

    Google Scholar 

  • Al Nachawati, I. (1985) Processus de classification séquentiels non arborescents pour l'aide au diagnostic. PhD thesis in Applied Mathematics. Universié Scientifique Technologique et Médicale de Grenoble, France.

    Google Scholar 

  • Asbury, A. K. (1967) Schwann cell proliferation in developing mouse sciatic nerve. A radioautographic study.Journal of Cell Biology 34, 735–43.

    Google Scholar 

  • Astier, H. S., Daniel, J. H. &Jallageas, M. (1978) Estimation of plasma concentration in ducks in relation to different environmental and experimental conditions.Experientia 34, 1228–9.

    Google Scholar 

  • Bacou, F., Jallageas, M., Nougues, J. &Vigneron, P. (1979) Différences sexuelles de l'évolution de la thyroxinémie chez l'embryon et le jeune poulet.Comptes Rendus Académie des Sciences de Paris 288, 1228–9.

    Google Scholar 

  • Balazs, R., Brooksbank, B. W. L., Davison, A. N., Eayrs, J. T. &Zilson, D. A. (1969) The effects of neonatal thyroidectomy on myelination in the rat brain.Brain Research 15, 219–32.

    Google Scholar 

  • Balazs, R., Kovacs, S., Cocks, W. A., Johnson, A. L. &Eayrs, J. T. (1971) Effect of thyroid hormone on the biochemical maturation of rat brain. Postnatal cell formation.Brain Research 25, 555–70.

    Google Scholar 

  • Bouvet, J. &Saxod, R. (1984) Analyse ultrastructurale quantitative du développement des nerfs cutanés chez le poulet hypothyroidien.Archives d'Anatomie Microscopique et Morphologie Expérimentale 73, 27–43.

    Google Scholar 

  • Brugal, G. (1984) Image analysis of microscopic preparations. InMethods and Achievements in Experimental Pathology (edited byJasmin, G. &Proscheck, L.)11, pp. 1–33. Basel: Karger.

    Google Scholar 

  • Brugal, G., Giroud, F. &Gabriel, A. (1985) Analysis of cell kinetics during planarian regeneration by means of SAMBA 200 cell image processor.Roux's Archives of Developmental Biology 194, 148–54.

    Google Scholar 

  • Cassel, D., Wood, P. M., Bunge, R. P. &Glaser, L. (1982) Mitogenicity of brain axolemma membranes and soluble factors for dorsal root ganglion Schwann cells.Journal of Cellular Biochemistry 18, 433–45.

    Google Scholar 

  • Cleaver, J. E. (1967) Thymidine metabolism and cell kinetics. InFrontiers of Biology (edited byNeuberger, A. &Tatum, E. L.)6, pp. 116–18. Amsterdam: North-Holland Publishing Company.

    Google Scholar 

  • Clos, J. (1980) Influence de l'état hypothyroidien et de la sous-alimentation sur les interactions cellulaires au cours du développement du cervelet du rat. Analyse morphologique, histochimique et biochimique. Thesis, Doctorat és-Sciences, Université de Montpellier II

  • Dalal, K. B., Valcana, T., Timiras, P. S. &Einstein, E. R. (1971) Regulatory role of thyroxine on myelinogenesis in the developing rat.Neurobiology 1, 211–18.

    Google Scholar 

  • Daugeras-Bernard, N., Leloup, J. &Lachiver, F. (1976) Evolution de la thyroxinémie au cours du développement de l'embryon de poulet. Influence de l'hypophysectomie.Comptes Rendus Académie des Sciences de Paris 283, 1325–7.

    Google Scholar 

  • Diamond, L. W., Dennis, D. W. &Rappaport, H. (1981) The relationship between lymphocyte nuclear morphology and cell cycle stage in lymphoid neoplasia.American Journal of Hematology 11, 165–73.

    Google Scholar 

  • Friede, R. L. &Samorajski, T. (1968) Myelin formation in the sciatic nerve of rat. A quantitative electron, histochemical and radioautographic study.Journal of Neuropathology and Experimental Neurology 27, 546–70.

    Google Scholar 

  • Giroud, F. (1982) Cell nucleus pattern analysis. Geometric and densitometric featuring automatic cell phase identification.Biology of the Cell 44, 177–88.

    Google Scholar 

  • Honegger, P. &Lenoir, D. (1980) Triiodothyronine enhancement of neuronal differentiation in aggregating fetal rat brain cells cultured in a chemically defined medium.Brain Research 199, 425–34.

    Google Scholar 

  • Kameda, Y. (1984) Immunocytochemical studies on differentiation of the thyroid gland in rabbit fetuses and chick embryos.Histochemistry 80, 23–9.

    Google Scholar 

  • Lawson, S., Caddy, K. &Biscoe, T. (1974) Development of rat dorsal root ganglion neurones: studies of cell birthdays and changes in mean cell diameter.Cell and Tissue Research 153, 399–413.

    Google Scholar 

  • Legrand, J. (1984) Effects of thyroid hormones on central nervous system development. InNeurobehavioural Teratology (edited byYanai, J.), pp. 331–63. Amsterdam: Elsevier Science Publishers.

    Google Scholar 

  • Martin, J. R. &Webster, H. De F. (1973) Mitotic Schwann cells in developing nerve: their changes in shape, fine structure and axon relationships.Developmental Biology 32, 417–31.

    Google Scholar 

  • Matthieu, J. M., Reier, P. J. &Sawchak, J. A. (1975) Proteins of rat brain myelin in neonatal hypothyroidism.Brain Research 84, 443–51.

    Google Scholar 

  • Meador-Woodruff, J. H., Yoshino, J. E., Bigbee, J. W., Lewis, B. L. &DeVries, G. H. (1985) Differential proliferative response of cultured Schwann cells to axolemma and myelin-enriched fractions. II. Morphological studies.Journal of Neurocytology 14, 619–35.

    Google Scholar 

  • Moustafa, Y. &Brugal, G. (1984) Image analysis of cell proliferation and differentiation in the thymus of the newtPleurodeles waltlii Michah. by SAMBA 200 cell image processing.Roux's Archives of Developmental Biology 193, 139–48.

    Google Scholar 

  • Nunez, J. (1984) Effects of thyroid hormones during brain differentiation.Molecular and Cellular Endocrinology 37, 125–32.

    Google Scholar 

  • Ockleford, E. M. &Vince, M. A. (1980) Effects of thyroxine on prehatching developmental rate and behaviour in the chick.Journal of Comparative and Physiological Psychology 94, 280–8.

    Google Scholar 

  • Peters, A. &Muir, A. R. (1959) The relationship between axons and Schwann cells during the development of peripheral nerves in the rat.Quarterly Journal of Experimental Physiology and Cognate Medical Sciences 44, 117–90.

    Google Scholar 

  • Puymirat, J., Barret, A., Picart, R., Vigay, A., Faivre-Bauman, A. &Tixier-Vidal, A. (1983) Triiodothyronine enhances the morphological maturation of dopaminergic neurons from fetal mouse hypothalamus cultured in serum-free medium.Neuroscience 10, 801–10.

    Google Scholar 

  • Reier, P. J. &Hughes, A. F. (1972) An effect of radiothyroidectomy upon non-myelinated axons and associated Schwann cells during maturation of the mouse sciatic nerve.Brain Research 41, 263–82.

    Google Scholar 

  • Romijn, H. J., Habets, A. M. M. C., Mud, M. T. &Wolters, P. S. (1982) Nerve outgrowth, synaptogenesis and bioelectric activity in fetal rat cerebellar cortex cultured in serum-free, chemically defined medium.Developmental Brain Research 2, 583–9.

    Google Scholar 

  • Salzer, J. L. &Bunge, R. P. (1980a) Studies of Schwann cell proliferation. I. An analysis of proliferation during development. Wallerian degeneration and direct injury.Journal of Cell Biology 84, 739–52.

    Google Scholar 

  • Lzer, J. L. &Bunge, R. P. (1980b) Studies of Schwann cell proliferation. III. Evidence for the surface localization of the neurite mitogen.Journal of Cell Biology 84, 767–78.

    Google Scholar 

  • Salzer, J. L., Williams, A. K., Glaser, L. &Bunge, R. P. (1980) Studies of Schwann cell proliferation. II. Characterization of the stimulation and specificity of the response to a neurite membrane fraction.Journal of Cell Biology 84, 753–66.

    Google Scholar 

  • Saxod, R. (1978) Combination of cholinesterase staining of nerves and stereoscopic viewing for three-dimensional study of skin innervation on whole mounts.Journal of Investigative Dermatology 70, 95–7.

    Google Scholar 

  • Saxod, R. &Bouvet, J. (1982a) Effets de la déficience thyroidienne sur le développement des nerfs cutanés du poulet.Comptes Rendus Académie des Sciences de Paris 294, 19–24.

    Google Scholar 

  • Saxod, R. &Bouvet, J. (1982b) Quantitative analysis of growth and myelination of cutaneous nerve fibers in the chick.Developmental Neuroscience 5, 143–55.

    Google Scholar 

  • Schulte, E. (1986) Hematoxylin and Feulgen reagent in nuclear staining. InStandardization and Quantitation of Diagnostic Staining in Cytology (edited byBoon, M. E. &Kok, L. P.), pp. 15–26. Leyden: Coulomb Press Leyden.

    Google Scholar 

  • Sobue, G. &Pleasure, D. (1985) Adhesion of axolemmal fragment to Schwann cells: a signal- and target-specific process closely linked to axolemmal induction of Schwann cell mitosis.Journal of Neuroscience 5, 379–87.

    Google Scholar 

  • Stelmack, B. M. &Kiernan, J. A. (1977) Effects of triiodothyronine on the normal and regenerating facial nerve of the rat.Acta Neuropathologica 40, 151–5.

    Google Scholar 

  • Swanson, J. W., Kelly, J. J. &Mcconahey, W. M. (1981) Neurologic aspects of thyroid dysfunction.Mayo Clinic Proceedings 56, 504–12.

    Google Scholar 

  • Tezlaff, W. (1978) The development of zonula ocludens in peripheral myelin of the chick embryo. A freeze fracture study.Cell and Tissue Research 189, 187–201.

    Google Scholar 

  • Usson, Y. (1985) Prolifération des cellules de Schwann du nerf sciatique de l'embryon de poulet normal et hypothy-roïdien: quantification par morphométrie ultrastructurale et analyse d'image. PhD thesis in Cellular and Molecular Biology, Université Scientifique Technologique et Médicale de Grenoble, France, 20 December 1985.

    Google Scholar 

  • Uyemura, K., Horie, K., Kitamura, K., Suzuki, M. &Uehara, S. (1979) Developmental changes of myelin proteins in the chick peripheral nerve.Journal of Neurochemistry 32, 778–88.

    Google Scholar 

  • Verna, J. M. &Saxod, R. (1979) Développement de l'innervation cutanée chez le poulet: analyse ultrastructurale et quantitative.Archives d'Anatomie Microscopique et Morphologie Expérimentale 68, 1–16.

    Google Scholar 

  • Webster, H. De F., Martin, J. R. &O'Connell, M. F. (1973) The relationships between interphase Schwann cells and axons before myelination: a quantitative electron microscopic study.Developmental Biology 32, 401–16.

    Google Scholar 

  • Wimber, D. E. (1963) Methods for studying cell proliferation with emphasis on DNA labels. InCell Proliferation (edited byLamerton, L. F. &Fry, R. J. M.), pp. 1–12. Oxford: Blackwell Scientific.

    Google Scholar 

  • Wood, P. M. &Bunge, R. P. (1975) Evidence that sensory axons are mitogenic for Schwann cells.Nature 256, 661–4.

    Google Scholar 

  • Wysacki, S. J. &Segal, W. (1972) Influence of thyroid hormones on enzyme activities of myelinating rat central nervous tissues.European Journal of Biochemistry 28, 183–9.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Usson, Y., Saxod, R. Schwann cell proliferation in the sciatic nerve of hypothyroid chick embryos studied by autoradiography and image analysis. J Neurocytol 17, 639–648 (1988). https://doi.org/10.1007/BF01260991

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01260991

Keywords

Navigation