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

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.

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References

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

    Google Scholar 

  2. 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 

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

    Google Scholar 

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

    Google Scholar 

  5. 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 

  6. 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 

  7. 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 

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

    Google Scholar 

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

    Google Scholar 

  10. 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 

  11. 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 

  12. 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 

  13. 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 

  14. 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 

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

    Google Scholar 

  16. 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 

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

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

    Google Scholar 

  19. 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 

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

    Google Scholar 

  21. 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 

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

    Google Scholar 

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

  24. 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 

  25. 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 

  26. 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 

  27. 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 

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

    Google Scholar 

  29. 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 

  30. 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 

  31. 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 

  32. —: 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 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  38. 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 

  39. 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 

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

    Google Scholar 

  41. —, 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 

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

    Google Scholar 

  43. —, 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 

  44. 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 

  45. 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 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  50. 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 

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

    Google Scholar 

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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.

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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

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Keywords

  • Prolactin
  • Electron Microscope Observation
  • Lateral Lobe
  • Thin Layer Chromatographic Analysis
  • Large Lipid