Skip to main content
SpringerLink
Log in

Prolactin-induced cytologic changes in the mucosa of the pigeon crop during crop-“milk” formation

  • Published:
Zeitschrift für Zellforschung und Mikroskopische Anatomie Aims and scope Submit manuscript

Summary

Light and electron microscope observations reveal two basic histo- and cytologic changes which take place in the pigeon crop during the course of prolaction administration to both sexes; (1) an increase in mitotic activity resulting in hyperplasia of the lateral lobes of the crop and (2) the accumulation of lipid in cells of these lobes. The latter process begins about twelve hours following prolactin injection. Histologic and cytochemical tests, as well as thin layer chromatographic analysis, reveal that these lipids may be classified as neutral unsaturated triglycerides. Tissues of control and prolactin-treated groups examined during the course of this study do not reveal any striking changes in organelle systems — aside from the accumulation of large lipid droplets. It does appear, however, that while ribosomes exist primarily as single units in non-stimulated cells, they appear primarily as polysomes in stimulated cells actively engaged in lipid synthesis. The origin of the cytoplasmic lipid inclusions is of interest. Morphologic evidence suggests that (1) they are not the result of cyto-pathologic changes, (2) they do not result from mitochondrial transformation and (3) they are not incorporated as discrete triglyceride micelles into these cells. The availability of precursors to the cell is dicussed in light of the observation that intercellular channels increase in width, and microvilli and desmosomes decrease in number throughout the experimental series. The incorporation of possible precursors into the cytoplasm may occur via two distinct classes of vesicles. One class is thought to arise through micropinocytotic activity. These vesicles have filamentous boundaries which are thought to render them specific for certain classes of compounds. The second class is somewhat larger in size and differs morphologically from micropinocytotic vesicles. These are thought to arise by the fusion of tips of microvilli and the plasma membrane, thus inpounding and internalizing materials from the intercellular canals into the cytoplasm.

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

  • Anderson, E.: Oocyte differentiation and vitellogenessis in the roach Periplaneta americana. J. Cell Biol. 20, 131–155 (1964).

    Google Scholar 

  • Barrnett, J. J., and E. G. Ball: Metabolic and ultrastructural changes induced in adipose tissue by insulin. J. biophys. biochem. Cytol. 8, 83–101 (1960).

    Google Scholar 

  • Beams, H. W., and R. K. Meyer: The formation of pigeon “milk”. Physiol. Zool. 4, 486–500 (1931).

    Google Scholar 

  • Bennett, H. S.: Morphological aspects of extracellular polysaccharides. J. Histochem. Cytochem. 11, 14–23 (1963).

    Google Scholar 

  • Bernard, C.: Dixième Leçons. Leçon sur les propriétés physiologiques et les altérations pathologiques des liquides de l'organisme, vol. 2, p. 220–238 (1859).

    Google Scholar 

  • Brachet, J.: La localisation des acides pentose nucléiques dans les tissues animaux et dans les oeufs d'amphibiens en voie de development. Arch. Biol (Liége) 53, 207–257 (1941).

    Google Scholar 

  • Burgos, H. H., and G. B. Wislocki: Cyclical changes in the guinea pigs' uterus, cervix, vagina, and sexual skin investigated with histological and histochemical means. Endocrinology 59, 93–118 (1956).

    Google Scholar 

  • Cain, J.: The use of nile blue in the examination of lipoids. Quart. J. micr. Sci. 88, 383–392 (1947).

    Google Scholar 

  • Charbonnel-Salle et Phisalix: Sécretion lactée du jabot des pigeons en incubation. C. R. Acad. Sci. (Paris) 103, 286–289 (1886).

    Google Scholar 

  • Clever, U., u. P. Karlson: Induktion von Puff-Veränderungen in den Speicheldrüsenchromosomen von Chironomus tentans durch Ecdyson. Exp. Cell Res. 20, 623–626 (1960).

    Google Scholar 

  • Deane, H., and K.R. Porter: A comparative study of cytoplasmic basophilia and the population density of ribosomes in the secretory cells of mouse seminal vesicle. Z. Zellforsch. 52, 697–711 (1960).

    Google Scholar 

  • Duve, C. De: The lysosome concept. In: Lysosomes, ed. by A. V. S. de Reuck and M. P. Cameron, p. 1–35. Boston: Little, Brown & Co. (1963).

    Google Scholar 

  • Estable, C., and R. J. Sotelo: Fine structure of cells, Symposium at the 8th Cong. of cell biol. p. 170–190. New York: Interscience Publishers, Inc. (1955).

    Google Scholar 

  • Fawcett, D. W.: Structural specializations of the cell surface. In: Frontiers in cytology, ed. by S. L. Palay, p. 19–41. New Haven: Yale University Press (1958).

    Google Scholar 

  • —, and J. Wittenberg: Structural specializations of endothelial cell junctions. Abstr. Anat. Rec. 142, 231 (1962).

    Google Scholar 

  • Folch, J. M., Lees, S. Stanley: A simple method for the isolation and purification of total lipids from animals tissue. J. biol. Chem. 226, 497–509 (1957).

    Google Scholar 

  • Hunter, J.: Über eine Absonderung im Kröpfe brütender Tauben zur Ernährung ihrer Jungen. In: Über die tierische Ökonomie. Braunschweig 1786. Zit. from Litwer (1926).

  • Ihnen, K.: Beiträge zur Physiologie des Kropfes bei Huhn und Taube. Pflügers Arch. Ges. Physiol. 218, 767–782 (1928).

    Google Scholar 

  • Ito, S.: Light and electron microscopic study of membranous cytoplasmic organelles. In: The interpretation of ultrastructure, ed. by R. J. C. Harris, p. 129–148. New York: Academic Press (1962).

    Google Scholar 

  • —, and R. J. Winchester: The fine structure of the gastric mucosa in the bat. J. Cell Biol. 16, 541–578 (1963).

    Google Scholar 

  • Lahr, E. L., and O. Riddle: Proliferation of crop-sac epithelium in incubating and prolactin-injected pigeons studied with the colchicine method. Amer. J. Physiol. 123, 614–619 (1938).

    Google Scholar 

  • Lewis, W. H.: Observations on cells in tissue-cultures with dark-field illumination. Anat. Rec. 26, 15–29 (1923).

    Google Scholar 

  • Lison, L.: Histochimie Animale, Paris 1936.

  • Littau, V., G. Allfrey, J. Frenster, and A. Mirsky: Active and inactive regions of nuclear chromatin as revealed by electron microscopy autoradiography. Proc. nat. Acad. Sci. (Wash.) 52, 93–100 (1964).

    Google Scholar 

  • Litwer, G.: Die histologischen Veränderungen der Kropfwandung bei Tauben, zur Zeit der Brütung und Ausfütterung ihrer Jungen. Z. Zellforsch. 3, 695–722 (1926).

    Google Scholar 

  • Loewenstein W. R., and Y. Kano: Studies on epithelial (gland) cell junction. I. Modifications of surface membrane permeability. J. Cell Biol. 22, 565–586 (1964).

    Google Scholar 

  • Ludford, R. J.: Pathological aspects of cytology. In: Cytology and cell physiology, ed. by G. H. Bourne, p. 373–418. Oxford: Clarendon Press (1951).

    Google Scholar 

  • Luft, J. H.: Improvements in epoxy resin embedding techniques. J. biophys. biochem. Cytol. 9, 409–414 (1961).

    Google Scholar 

  • Masahito, D., and T. Fujii: Histology of pigeon crop-sac, with special reference to the early changes evoked by prolactin. J. Fac. Sci. Univ. Tokyo 7, 410–419 (1955).

    Google Scholar 

  • Napolitano, L., and D. W. Fawcett: The fine structure of brown adipose tissue in the newborn mouse and rat. J. biophys. biochem. Cytol. 4, 685–692 (1958).

    Google Scholar 

  • Novikoff, A. B.: Lysosomes and related particles. In: The cell, ed. by J. Brachet and A. Mirsky, vol. 2, p. 423–488. New York: Academic Press 1961 a.

    Google Scholar 

  • —: Mitochondria (chondrisomes). In: The cell, ed. by J. Brachet and A. Mirsky, vol. 2, p.299–422. New York: Academic Press 1961 b.

    Google Scholar 

  • Palade, G. E.: A study of fixation of tissues for electron microscopy. J. exp. Med. 95, 285–298 (1952).

    Google Scholar 

  • —, and P. Siekevitz: Pancreatic microsomes. An integrated morphological and biochemical study. J. biophys. biochem. Cytol. 2, 671–690 (1956).

    Google Scholar 

  • Palay, S. L.: Alveolate vesicles in Purkinje cells of the rat's cerebellum. Abstr. J. Cell Biol. 19, 89A (1963).

    Google Scholar 

  • Patel, M. D.: The physiology of the formation of “pigeon's milk”. Physiol. Zool. 9, 129–152 (1936).

    Google Scholar 

  • Pearse, A.: Histochemistry, theoretical and applied. Boston: Little Brown & Co. 1961.

    Google Scholar 

  • Reynolds, E.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963).

    Google Scholar 

  • Rich, A., J. R. Warner, and H. M. Goodman: The structure and function of polyribosomes. In: Cold Spr. Harb. Symp. quant. Biol. 28, 269–285 (1963).

    Google Scholar 

  • Riddle, O.: Prolactin in vertebrate function and organization. J. nat. Cancer Inst. 31, 1039–1110 (1963).

    Google Scholar 

  • —, R. W. Bates, and S. W. Dykshorn: A new hormone of the anterior pituitary. Proc. Soc. exp. Biol. (N. Y.) 29, 1211–1212 (1932).

    Google Scholar 

  • —: The preparation, identification and assay of prolactin — a hormone of the anterior pituitary. Amer. J. Physiol. 105, 191–216 (1933).

    Google Scholar 

  • —, and P. F. Braucher: Studies on physiology of reproduction in birds; control of special secretions of the crop-gland in pigeons by an anterior pituitary hormone. Amer. J. Physiol. 97, 617–625 (1931).

    Google Scholar 

  • Roth, T., and K. R. Porter: Yolk protein uptake in the oocyte of the mosquito, Aedes aegypti L. J. Cell Biol. 20, 313–332 (1964).

    Google Scholar 

  • Sabatini, D., K. Bensch, and R. Barrnett: Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J. Cell Biol. 17, 19–58 (1963).

    Google Scholar 

  • Teichmann, M.: Der Kropf der Taube. Arch. mikr. Anat. 34, 235–247 (1889).

    Google Scholar 

  • Watson, M.: Staining of tissue sections for electron microscopy with heavy metals. J. biophys. biochem. Cytol. 4, 475–478 (1958).

    Google Scholar 

  • Weber, W.: Zur Histologie und Cytologie der Kropfmilchbildung der Taube. Z.Zellforsch. 56, 247–276 (1962).

    Google Scholar 

  • Williamson, J. R.: Adipose tissue: morphological changes associated with lipid mobilization. J. Cell Biol. 20, 57–74 (1964).

    Google Scholar 

  • Zelander, T.: Ultrastructure of mouse adrenal cortex: An electron microscopical study of intact and hydrocortisone-treated male adults. J. Ultrastruct. Res., Suppl. 2, 1–111 (1959).

    Google Scholar 

  • Zollner, N., u. G. Wolfram: Dünnschichtchromatographische Systeme zur Trennung der Plasmalipoide. Klin. Wschr. 21, 1101–1107 (1962).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, The University of Massachusetts, Amherst, Massachusetts, USA

    James N. Dumont

Authors
  1. James N. Dumont
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

The author is indebted to Dr. Everett Anderson for his valuable criticism and encouragement offered during the course of this work. The investigation was supported in part by a Pre-Doctoral Fellowship (1-F1-GM-20, 296-01) from the National Institutes of Health and in part by grant GM-08776 from the National Institutes of Health awarded to Dr. Everett Anderson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dumont, J.N. Prolactin-induced cytologic changes in the mucosa of the pigeon crop during crop-“milk” formation. Zeitschrift für Zellforschung 68, 755–782 (1965). https://doi.org/10.1007/BF00343930

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00343930

Keywords

Search

Navigation