Summary
Tracheobronchial epithelium, thyroid organ, thymus, of the developing rats were examined by immunohistochemistry using anti-spot 35 calbindin-antiserum. At E 14, weak to moderate immunoreactivity for spot 35-calbindin was detected in the airway epithelia of the distal half of the trachea and the extrapulmonary bronchus. The immunoreactive cells increased in intensity at E 16–E 21, but decreased markedly after birth. These cells were non-ciliated cells and comprised a majority of the epithelial cells especially in the ventral/cartilaginous portion of the airway. They were characterized by microvilli, vacuoles, granular and agranular endoplasmic reticulum. Typical ciliated cells, which were much less numerous than the immunopositive non-ciliated cells, were immunonegative. In thyroid gland, calbindin-immunoreactive cells first appeared at E 18. They increased in number at E 20-P 1 and decreased gradually after P 7. These cells were the parafollicular cells characterized by numerous secretory granules and situated in close proximity to the basal surface of the follicular cells. In the thymus, immunoreactive cells appeared in the thymic medulla at E 20. They increased in number at P 1, but decreased gradually after P 7. They were stellate in shape and had vesicles, vacuoles, intermediate filaments and represented a subpopulation of thymic reticular epithelial cells. Such a transient appearance of spot 35-calbindin in these cells suggests that this protein may be involved in the regulation of differentiation or may be involved in the process of secretion during the limited developmental period.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abe H, Amano O, Yamakuni T, Takahashi Y, Kondo H (1990) Localization of spot 35-calbindin (rat cerebellar calbindin) in the anterior pituitary of the rat: developmental and sexual differences. Arch Histol Cytol 53:585–591
Abe H, Amano O, Yamakuni T, Kuwano R, Takahashi Y, Kondo H (1991) Transient expression of a calcium-binding protein (spot 35-calbindin) and its mRNA in the immature pituicytes of embryonic rats. Cell Tissue Res 266:325–330
Carafoli E (1987) Intracellular calcium homeostasis. Ann Rev Biochem 56:395–433
Douglas WW (1974) Exocytosis and the exocytosis-vesiculation sequence: with special reference to neurohypophysis, chromaffine and mast cells, calcium and calcium ionophores. In: Thorn NA, Peterson OH (eds) Secretory mechanisms of exocrine glands. Munksgaard, Copenhagen, pp 116–133
Evans MJ, Cabral-Anderson LJ, Freeman G (1978) Role of the Clara cell in renewal of the bronchiolar epithelium. Lab Invest 38:648–655
Hunziker W, Schrickel S (1988) Rat brain calbindin D28: six domain structure and extensive amino acid homology with chicken calbindin D28. Mol Endocrinol 2:465–473
Inpanbutr N, Taylor AN, Deftos LJ (1987) Calbindin-D28k distribution in chick ultimobranchial and rat thyroid glands. In: Norman AW, Vanaman TC, Means AR (eds) Calcium-binding proteins in health and disease. Academic Press, San Diego, pp 609–611
Kameda Y, Ikeda A (1980) Immunohistochemical study of the C-cell complex of dog thyroid glands with reference to the reactions of calcitonin, C-thyroglobulin and 19S thyroglobulin. Cell Tissue Res 208:405–415
Kawamata S, Fujita H (1983) Fine structural aspects of the development and aging of the tracheal epithelium of mice. Arch Histol Jpn 46:355–372
Kondo H, Yamamoto M, Yamakuni T, Takahashi Y (1988) An immunohistochemical study of the ontogeny of the horizontal cell in the rat retina using an antiserum against spot 35 protein, a novel Purkinje cell-specific protein, as a marker. Anat Rec 222:103–109
King MW, Norman AW (1986) Analysis of the mRNA coding for the chick vitamin D-induced calbindin and its regulation by 1,25-dihydroxyvitamin D3. Arch Biochem Biophys 248:612–619
Larsson L-I (1985) Differential changes in calcitonin, somatostatin and gastrin/cholecystokinin-like immunoreactivities in rat thyroid parafollicular cells during ontogeny. Histochemistry 82:121–130
McDowell EM, Newkirk C, Coleman B (1985) Development of hamster tracheal epithelium: I. A quantitative morphologic study in the fetus. Anat Rec 213:429–447
McMillan PJ, Hooker WM, Deftos LJ (1974) Distribution of calcitonin-containing cells in the human thyroid. Am J Anat 140:73–80
Moore DCP, Stanisstreet M (1986) Calcium requirement for neural fold elevation in rat embryos. Cytobios 47:167–177
Pack RJ, Al-Ugaily LH, Morris G, Widdicombe JG (1980) The distribution and structure of cells in the tracheal epithelium of the mouse. Cell Tissue Res 208:65–84
Parmentier M, Lawson DEM, Vassart G (1987) Human 27-kDa calbindin complementary DNA sequence. Evolutionary and functional implications. Eur J Biochem 170:207–215
Pearse AGE, Polak JM (1971) Cytochemical evidence for the neural crest origin of mammalian ultimobranchial C cells. Histochemie 27:96–102
Smedley MJ, Stanisstreet M (1985) Calcium and neurulation in mammalian embryos. J Embryol Exp Morphol 89:1–14
Smolich JJ, Stratford BF, Moloney JE, Ritchie BC (1967) Postnatal development of the epithelium of larynx and trachea in the rat: scanning electron microscopy. J Anat 124:657–673
Taira K, Shibasaki S (1978) A fine structure study of the non-ciliated cells in the mouse tracheal epithelium with special reference to the relation of “brush cells” and “endocrine cells”. Arch Histol Jpn 41:351–366
Varghese S, Lee S, Huang Y-C, Christakos S (1988) Analysis of rat vitamin D-dependent calbindin-D28k gene expression. J Biol Chem 263:9776–9784
Wasserman RH, Taylor AN (1966) Vitamin D3-induced calcium-binding protein in chick intestinal mucosa. Science 152:791–793
Weiss L (1988) Cell and tissue biology. A textbook of histology. (6th edn) Urban & Schwarzenberg, Baltimore, USA, pp 490–491
Yamakuni T, Usui H, Iwanaga T, Kondo H, Odani S, Takahashi Y (1984) Isolation and immunohistochemical localization of a cerebellar protein. Neurosci Lett 45:235–240
Yamakuni T, Araki K, Takahashi Y (1985) The developmental changes of mRNA levels for a cerebellar protein (spot 35 protein) in rat brains. FEBS Lett 188:127–130
Yamakuni T, Kuwano R, Odani S, Miki N, Yamaguchi K, Takahashi Y (1987) Molecular cloning of cDNA to mRNA for a cerebellar spot 35 protein. J Neurochem 48:1590–1596
Yamamoto M, Yamakuni T, Takahashi Y, Kondo H (1991) Transient appearance of immunoreactivity for Ca-binding protein (spot 35-calbindin) in small principal neurons in the superior cervical ganglion of pre-weanling rats. J Autonom Nerv Syst 35:25–32
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Abe, H., Watanabe, M. & Kondo, H. Transient appearance of Ca-binding protein (spot 35-calbindin) in bronchial epithelial cells, thyroid parafollicular cells and thymic epithelial cells during the development of rats. Histochemistry 97, 155–160 (1992). https://doi.org/10.1007/BF00267306
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00267306