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Endocytosis and multivesicular body formation in rabbit luteal cells during pseudopregnancy

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Summary

Horseradish peroxidase (HBP) was injected directly into the corpora lutea of rabbits on different days of pseudopregnancy. Young luteal cells have also been incubated “in vitro” in a medium containing horseradish peroxidase. In the “in vivo” experiments the 5 to 9 days old luteal cells take up far more horseradish peroxidase than the older ones (14–20 days). Different types of endocytic vacuoles, MvB's and also some DB's are already peroxidase positive shortly (15–20 min) after injection of the tracer. In the “in vitro” experiments the cells are more heavily loaded.

The normal morphology of pale, dense and terminal MvB's is also described and staining with PTA at low pH provides further information on changes occurring in the MvB's.

The various findings on multivesicular bodies are compared and two possible pathways for endocytic vacuoles are proposed: one to DB's the other to MvB's.

The related phenomena of the uptake of material and the internalization of plasma membrane are discussed in the light of the possible function of endocytosis in luteal cells.

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References

  • Abrahams, S. J., Holzman, E.: Secretion and endocytosis in insulin-stimulated rat adrenal medulla cells. J. Cell Biol. 56, 540–558 (1973)

    Google Scholar 

  • Adams, E. C., Hertig, A. T.: Studies on the human corpus luteum. I. Observations on the ultrastructure of development and regression of the luteal cells during the menstrual cycle. J. Cell Biol. 41, 696–715 (1969)

    Google Scholar 

  • Anderson, W. A.: The use of exogenous myoglobin as an ultrastructural tracer. Reabsorption and translocation of protein by the renal tubule. J. Histochem. Cytochem. 20, 672–684 (1972)

    Google Scholar 

  • Antheunis, A.: Origin and fate of the multivesicular bodies in PHA stimulated lymphocytes. Cell Tiss. Res. 149, 497–511 (1974)

    Google Scholar 

  • Arstila, A. V., Jauregui, H. O., Chang, J., Trump, B. F.: Studies on cellular autophagocytosis.Relationship between heterophagy and autophagy in HeLa cells. Lab. Invest. 24, 162–174 (1971)

    Google Scholar 

  • Biberfeld, P.: Endocytosis and lysosome formation in blood lymphocytes transformed by phytohemagglutinin. J. Ultrastruct. Res. 36, 41–68 (1971)

    Google Scholar 

  • Cornell, R., Walker, W. A., Isselbacher, K. J.: Small intestinal absorption of horseradish peroxidase. A cytochemical study. Lab. Invest. 25, 42–48 (1971)

    Google Scholar 

  • Cotran, R. S., Karnovsky, M. J.: Ultrastructural studies on the permeability of the mesothelium to horseradish peroxidase. J. Cell Biol. 37, 123–137 (1968)

    Google Scholar 

  • Creemers, J., Jacques, P. J.: Endocytic uptake and vesicular transport of injected horseradish peroxidase in the vacuolar apparatus of rat liver cells. Exp. Cell Res. 67, 188–203 (1971)

    Google Scholar 

  • Daems, W. Th., Wisse, E., Brederoo, P.: Electron microscopy of the vacuolar apparatus. In: Lysosomes in biology and pathology (Dingle, J. T. and Fell, H. B., eds.), vol. 1, p. 64–112. Amsterdam: North-Holland Publ. 1969

    Google Scholar 

  • Dawson, R. M. C., Elliott, D.C., Elliott, W. H., Jones, K. M., eds.: Data for biochemical research. Oxford: Clarendon Press 1969

    Google Scholar 

  • De Duve, C., Wattiaux, R.: Functions of lysosomes. Ann. Rev. Physiol. 28, 435–492 (1966)

    Google Scholar 

  • Enders, A. C., Winsatt, W. A.: Transport and barrier function in the chorioallantoic placenta of the bat, Myotis lucifugus. Anat. Rec. 170, 381–400 (1971)

    Google Scholar 

  • Ericsson, J. L. E.: Transport and digestion of hemoglobin in the proximal tubule. II. Electron microscopy. Lab. Invest. 14, 16–39 (1965)

    Google Scholar 

  • Fahimi, H. D., Drochmans, P.: Essais de standardisation de la fixation au glutaraldéhyde. I. Purification et détermination de la concentration du glutaraldéhyde. J. Microscopie 4, 725–736 (1965)

    Google Scholar 

  • Friend, D. S.: Cytochemical staining of multivesicular body and Golgi vesicles. J. Cell Biol. 41, 269–279 (1969)

    Google Scholar 

  • Friend, D. S., Farquhar, H. G.: Functions of coated vesicles during protein absorption in the rat vas deferens. J. Cell Biol. 35, 357–376 (1967)

    Google Scholar 

  • Geuze, J. J., Poort, C.: Cell membrane resorption in the rat exocrine pancreas cell after invivo stimulation of the secretion, as studied by in vitro incubation with the extracellular space markers. J. Cell Biol. 57, 159–174 (1973)

    Google Scholar 

  • Goebel, F.D., Dennhardt, R.: Über den Peroxydasetransport im Darmepithel der Ratte. Z. Zellforsch. 134, 403–410 (1972)

    Google Scholar 

  • Goldfischer, S., Novikoff, A. B., Albala, A., Biempica, L.: Hemoglobin uptake by rat hepatocytes and its breakdown within lysosomes. J. Cell Biol. 44, 513–529 (1970)

    Google Scholar 

  • Graham, R. C., Karnovsky, M. J.: The early stage of absorption of injected horseradish peroxidase in the proximal tubule of the mouse kidney: ultrastructural cytochemistry by a new technique. J. Histochem. Cytochem. 14, 291–302 (1966)

    Google Scholar 

  • Graham, R. C., Limpert, S., Kellenmeyer, R. W.: The uptake and transport of exogenous proteins in mouse liver. Ultrastructural cytochemical studies with peroxidase tracers. Lab. Invest. 20, 298–304 (1969)

    Google Scholar 

  • Greene, W. B., Spicer, S. S.: Cytochemistry of multivesicular bodies in human term placentas. J. Histochem. Cytochem. 18, 687 (abstr.) (1970)

    Google Scholar 

  • Holtzman, E., Dominitz, R.: Cytochemical studies of lysosomes, Golgi apparatus and endoplasmic reticulum in secretion and protein uptake by adrenal medulla cells of the rat. J. Histochem. Cytochem. 16, 320–336 (1968)

    Google Scholar 

  • Holtzman, E., Novikoff, A.B., Villaverde, H.: Lysosomes and GERL in normal and chromatolytic neurons of rat ganglion nodosum. J. Cell Biol. 33, 419–435 (1967)

    Google Scholar 

  • Holtzman, E., Teichberg, S., Abrahams, S. J., Citkowitz, E., Grain, S. M., Kawai, N., Peterson, E. R.: Notes on synaptic vesicles and related structures, endoplasmic reticulum, lysosomes and peroxisomes in nervous tissue and the adrenal medulla. J. Histochem. Cytochem. 21, 349–385 (1973)

    Google Scholar 

  • Hugon, J., Borgers, M.: Absorption of horseradish peroxidase by the mucosal cells of the duodenum of mouse. I. The fasting animal. J. Histochem. Cytochem. 16, 229–236 (1968)

    Google Scholar 

  • King, B. F., Enders, A. C.: Protein absorption by the guinea pig chorioallantoic placenta. Amer. J. Anat. 130, 409–430 (1971)

    Google Scholar 

  • Kwan, P., Curtis, J. C.: Lysosomes and multivesicular bodies in fasciculata cells in the rat adrenal. J. Cell Biol. 59, 181 a (1973)

    Google Scholar 

  • Lagunoff, D., Curran, D. E.: Role of bristle-coated membrane in the uptake of ferritin by rat macrophages. Exp. Cell Res. 75, 337–346 (1972)

    Google Scholar 

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

    Google Scholar 

  • Ma, M. H., Laird, W. A., Scott, H.: Cytopempsis of horseradish peroxidase in the hepatocytes. J. Histochem. Cytochem. 22, 160–169 (1974)

    Google Scholar 

  • Martin, B. J., Spicer, S. S.: Multivesicular bodies and related structures of the syncytiotrophoblast of human term placenta. Anat. Rec. 175, 15–36 (1973)

    Google Scholar 

  • Matter, A., Orci, L., Rouiller, Gh.: A study on the permeability barriers between Disse's space and the bile canaliculus. J. Ultrastruct. Res., Suppl. 11, 1–71 (1969)

    Google Scholar 

  • Maunsbach, A. B.: Absorption of ferritin by rat kidney proximal tubule cells. Electron microscopic observation of the initial uptake phase in cells of microperfused single proximal tubules. J. Ultrastruct. Res. 16, 1–12 (1966)

    Google Scholar 

  • Orci, L., Malaisse-Lagae, F., Ravazzola, M., Amherdt, M., Renold, A. E.: Exocytosis-endocytosis coupling in the pancreatic beta cell. Science (Wash.) 181, 561–562 (1973)

    Google Scholar 

  • Quatacker, J.: De luteale cellen van net pseudozwangere konijn. Thesis, Ph. D. Gent: Rijksuniversiteit 1973

    Google Scholar 

  • Quatacker, J.: Les contacts “ septate-like ” des cellules lutéales traitées au lanthane colloïdal. J. Microscopie 20, 83a (1974)

  • Quatacker, J.: Cell contacts in rabbit corpora lutea. J. Ultrastruct. Res. 50 (1975)

  • Rambourg, A.: Détection des glycoprotéïnes en microscopie électronique: coloration de la surface cellulaire et de l'appareil de Golgi par un mélange acide chromique-phosphotungstique. C. R. Acad. Sci. (Paris) 265, 1426–1428 (1967)

    Google Scholar 

  • Rosenbluth, J., Wissig, S. L.: The distribution of exogenous ferritin in toad spinal ganglia and the mechanism of its uptake by neurons. J. Cell Biol. 23, 307–325 (1964)

    Google Scholar 

  • Schneeberger-Keeley, E. E., Karnovsky, M. J.: The ultrastructural basis of alveolar-capillary membrane permeability to peroxidase as a tracer. J. Cell Biol. 37, 781–793 (1968)

    Google Scholar 

  • Seljelid, R.: Endocytosis in thyroid follicle cells. II. A microinjection study of the origin of colloid droplets. J. Ultrastruct. Res. 17, 401–420 (1967)

    Google Scholar 

  • Slautterback, D. B.: Coated vesicles in absorptive cells of Hydra. J. Cell Sci. 2, 563–572 (1967)

    Google Scholar 

  • Steinman, R. M., Cohn, Z. A.: The interaction of soluble horseradish peroxidase with the mouse peritoneal macrophages in vitro. J. Cell Biol. 55, 186–204 (1972)

    Google Scholar 

  • Steinman, R. M., Silver, J. M., Cohn, Z. A.: Pinocytosis in fibroblasts. Quantitative studies in vitro. J. Cell. Biol. 63, 949–969 (1974)

    Google Scholar 

  • Thiery, J. P.: Cytochimie sur coupe fine des mucopolysaccharides acides après inclusion dans les resines Epoxy. Septième congrès international de microscopie électronique, Grenoble, vol.1, 557–578 (1970)

    Google Scholar 

  • Walker, W. A., Cornell, R., Davenport, L. M., Isselbacher, K. J.: Macromolecular absorption: mechanism of horseradish peroxidase uptake and transport in adult and neonatal rat intestine. J. Cell Biol. 54, 195–205 (1972)

    Google Scholar 

  • Wollman, S. H.: Secretion of thyroid hormones. In: Lysosomes in biology and pathology (Dingle, J. T. and Fell, H. B., eds.), vol. 2, 483–508. Amsterdam: North-Holland Publ. 1969

    Google Scholar 

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  1. Department of Pathology, Akademisch Ziekenhuis, State University, Gent, Belgium

    J. Quatacker

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Quatacker, J. Endocytosis and multivesicular body formation in rabbit luteal cells during pseudopregnancy. Cell Tissue Res. 161, 541–553 (1975). https://doi.org/10.1007/BF00224143

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  • DOI: https://doi.org/10.1007/BF00224143

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