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On the ultrastructure of granulosa lutein cells in porcine corpus luteum

With special reference to endoplasmic reticulum and steroid hormone synthesis

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Summary

In young corpora lutea the endoplasmic reticulum membranes are sparse. A marked increase of smooth membranes then follows up to the peak of dioestrus. Continuities between smooth and rough endoplasmic reticulum are obvious during the same period. These observations suggest that the agranular membranes develop from the granular ones.

During the most intense development of the endoplasmic reticulum the membranes show a tendency to be arranged in whorls. Since these are numerous only during the period of high progesterone secretion, a multitude of whorls constitutes a useful morphologic sign of high functional activity in the porcine granulosa lutein cells.

During the first half of the oestrous cycle the increase in endoplasmic reticulum in general also parallels the increase in progesterone secretion. However, this secretion as well as Δ5-3β-hydroxysteroid dehydrogenase activity declines earlier and more rapidly than the endoplasmic reticulum regresses. Steroid hormone synthesis may therefore be lacking although the agranular membranes appear morphologically normal.

The mechanisms of induction of the endoplasmic reticulum membranes and enzymes active in steroid synthesis are discussed and it is suggested that luteinizing hormone (LH) may act as a trigger by increasing transport across membranes.

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References

  • Adams, C. W. M.: Osmium tetroxide and the Marchi method: Reactions with polar and nonpolar lipids, protein and polysaccharide. J. Histochem. Cytochem.8, 262–267 (1960).

    Google Scholar 

  • —: Cerebral storage diseases. In: Neurohistochemistry (C. W. M. Adams, editor), p. 488–517. Amsterdam-London-New York: Elsevier Publ. Co. 1965a.

    Google Scholar 

  • —: Histochemistry of lipids. In: Neurohistochemistry (C. W. M. Adams, editor), p. 6–66. Amsterdam-London-New York: Elsevier Publ. Co. 1965b.

    Google Scholar 

  • Armstrong, D. T.: Comparative studies of the action of luteinizing hormone upon ovarian steroidogenesis. J. Reprod. Fertil., Suppl.1, 101–112 (1966).

    Google Scholar 

  • Ashworth, Ch. T., G. J. Race, andH. H. Mollenhauer: Study of functional activity of adrenocortical cells with electron microscopy. Amer. J. Path.35, 425–437 (1959).

    PubMed  Google Scholar 

  • Bahr, G. F.: Osmium tetroxide and ruthenium tetroxide and their reactions with biologically important substances. Electron stains III. Exp. Cell Res.7, 457–479 (1954).

    PubMed  Google Scholar 

  • Baker, J. R.: The structure and chemical composition of the Golgi element. Quart. J. micr. Sci.85, 1–71 (1944).

    Google Scholar 

  • Ball, J. H., andB. Kadis: Steroid hydroxylations. II. Intracellular location of 17 α-hydroxylase and its substrate specificity in sow ovary. Arch. Biochem.110, 427–431 (1965).

    PubMed  Google Scholar 

  • Barker, W. L.: A cytochemical study of lipids in sows' ovaries during the estrous cycle. Endocrinology48, 772–785 (1951).

    PubMed  Google Scholar 

  • Bennett, H. S., andJ. H. Luft: s-Collidine as a basis for buffering fixatives. J. biophys. biochem. Cytol.6, 113–114 (1959).

    PubMed  Google Scholar 

  • Bjersing, L.: The ultrastructure of corpus luteum, ovarian follicles and isolated granulosa cells. Acta path, microbiol. scand.66, 270 (1966).

    Google Scholar 

  • —: On the ultrastructure of follicles and isolated follicular granulosa cells of porcine ovary. Z. Zellforsch.82, 173–186 (1967a).

    PubMed  Google Scholar 

  • —: Histochemical demonstration of Δ5-3β- and 17β-hydroxysteroid dehydrogenase activities in porcine ovary. Histochemie10, 295–304 (1967b).

    PubMed  Google Scholar 

  • —, andH. Carstensen: The role of the granulosa cell in the biosynthesis of ovarian steroid hormones. Biochim. biophys. Acta (Amst.)86, 639–640 (1964).

    Google Scholar 

  • — —: Biosynthesis of steroids by granulosa cells of the porcine ovaryin vitro. J. Reprod. Fertil.14, 101–111 (1967).

    PubMed  Google Scholar 

  • Blanchette, E. J.: Ovarian steroid cells. II. The lutein cell. J. Cell Biol.81, 517–542 (1966).

    Google Scholar 

  • Bloor, W. R., R. Okey, andG. W. Corner: The relation of the lipids to physiological activity. I. The changes in the lipid content of the corpus luteum of the sow. J. biol. Chem.86, 291–306 (1930).

    Google Scholar 

  • Boyd, E. M., andC. A. Elden: The relation of lipids to oestrin and progestin in the corpus luteum of the sow. Endocrinology19, 599–602 (1935).

    Google Scholar 

  • Brinkley, H. J., andE. P. Young:In vivo progesterone secretion by swine ovaries. J. Animal Sci.24, 914 (1965).

    Google Scholar 

  • Carr, I., andJ. Carr: Membranous whorls in the testicular interstitial cell. Anat. Rec.144, 143–147 (1962).

    PubMed  Google Scholar 

  • Channing, C. P., andC. A. Villee: Luteinizing hormone: Effects on uptake and metabolism of hexoses by luteinized rat ovaries. Biochim. biophys. Acta (Amst.)115, 205–218 (1966).

    Google Scholar 

  • Christensen, A. K.: The fine structure of testicular interstitial cells in guinea pigs. J. Cell Biol.26, 911–935 (1965).

    Google Scholar 

  • —, andD. W. Fawcett: The normal fine structure of opossum testicular interstitial cells. J. biophys. biochem. Cytol.9, 653–670 (1961).

    PubMed  Google Scholar 

  • — —: The fine structure of testicular interstitial cells in mice. Amer. J. Anat.118, 551–572 (1966).

    PubMed  Google Scholar 

  • Corner, G. W.: On the origin of the corpus luteum of the sow from both granulosa and theca interna. Amer. J. Anat.26, 117–183 (1919).

    Google Scholar 

  • —: Cyclic changes in the ovaries and uterus of the sow, and their relation to the mechanism of implantation. Contr. Embryol. Carneg. Instn13, 117–146 (1921).

    Google Scholar 

  • —: Alkaline phosphatase in the ovarian follicle and in the corpus luteum. Contr. Embryol. Carneg. Instn32, 1–8 (1948).

    Google Scholar 

  • Cotte, G.: Quelques problèmes posés par l'ultrastructure des lipides de la cortico-surrénale. J. Ultrastruct. Res.8, 186–209 (1959).

    Google Scholar 

  • Deane, H. W.: Intracellular lipides: Their detection and significance. In: Frontiers in cytology (S. L. Palay, editor), p. 227–263. New Haven: Yale University Press 1958.

    Google Scholar 

  • —, andW. L. Barker: A cytochemical study of lipids in the ovaries of the rat and sow during the estrous cycle. In: Studies on testis and ovary, eggs and sperm (E. T. Engle, editor), p. 176–195. Springfield (Ill.): Ch. C. Thomas 1952.

    Google Scholar 

  • —, andR. V. Short: The corpus luteum of the sheep: Relationships between morphology and function during the oestrous cycle. Acta endocr. (Kbh.)51, 245–263 (1966).

    Google Scholar 

  • Deenan, L. L. M. van: Phospholipids and biomembranes. In: Progress in the chemistry of fats and other lipids (R. T. Holman, editor), vol. 8, part 1, p. 1–127. London: Pergamon Press 1965.

    Google Scholar 

  • Dixon, M., andE. C. Webb: Enzymes, 2 ed. London: Longmans, Green & Co. Ltd 1964.

    Google Scholar 

  • Doreman, R. I., andF. Ungar: Metabolism of steroid hormones. London: Academic Press 1965.

    Google Scholar 

  • Duncan, G. W., A. M. Bowerman, W. R. Hearn, andR. M. Melampy:In vitro synthesis of progesterone by swine corpora lutea. Proc. Soc. exp. Biol. (N.Y.)104, 17–19 (1960).

    Google Scholar 

  • Enders, A. C.: Observations on the fine structure of lutein cells. J. Cell Biol.12, 101–113 (1962).

    PubMed  Google Scholar 

  • —, andW. R. Lyons: Observations on the fine structure of lutein cells. II. The effects of hypophysectomy and mammotrophic hormone in the rat. J. Cell Biol.22, 127–141 (1964).

    PubMed  Google Scholar 

  • Fawcett, D. W.: Structural and functional variations in the membranes of the cytoplasm. In: Intracellular membranous structure (S. Seno andE. V. Cowdry, editors), p. 15–40. Okayama: Japan Society for Cell Biology 1965.

    Google Scholar 

  • —: The cell. Its organelles and inclusions. Philadelphia and London: W. B. Saunders Co. 1966.

    Google Scholar 

  • Fleischer, S., andG. Brierley: Solubilization of cholesterol in phospholipid micelles in water. Biochem. biophys. Res. Commun.5, 367–372 (1961).

    Google Scholar 

  • Gabe, M., andL. Arvy: Gland cells. In: The cell (J. Brachet andA. E. Mirsky, editors), vol. V, p. 1–88. London: Academic Press 1961.

    Google Scholar 

  • Giacomelli, F., J. Wiener, andD. Spiro: Cytological alterations related to stimulation of the zona glomerulosa of the adrenal gland. J. Cell Biol.26, 499–522 (1965).

    PubMed  Google Scholar 

  • Gomes, W. R., R. C. Herschler, andR. E. Erb: Progesterone levels in ovarian venous effluent of the nonpregnant sow. J. Animal Sci.24, 722–725 (1965).

    Google Scholar 

  • Goodman, P., J. S. Latta, R. B. Wilson, andB. Kadis: Massive smooth endoplasmic reticulum in porcine granulosa lutein cells. Anat. Rec.157, 249–250 (1967).

    Google Scholar 

  • Haguenau, F.: The ergastoplasm: Its history, ultrastructure, and biochemistry. Int. Rev. Cytol.7, 425–483 (1958).

    Google Scholar 

  • Hall, P. F., andS. B. Koritz: The conversion of cholesterol and 20α-hydroxycholesterol to steroids by acetone powder of particles from bovinecorpus luteum. Biochemistry3, 129–134 (1964).

    Google Scholar 

  • Hay, M. F., andH. W. Deane: Attempts to demonstrate 3β- and 17β-hydroxysteroid dehydrogenases histochemically in the testes of the stallion, boar, ram and bull. J. Reprod Fertil.12, 551–560 (1966).

    PubMed  Google Scholar 

  • Hirschfield, I. N., andS. B. Koritz: Pregnenolone synthesis stimulation in the large particles from bovine adrenal cortex and bovine corpus luteum. Endocrinology78, 165–168 (1966).

    PubMed  Google Scholar 

  • Kessel, R. G.: Intranuclear and cytoplasmic annulate lamellae in tunicate oocytes. J. Cell Biol.24, 471–487 (1965).

    Google Scholar 

  • Korn, E. D.: III. Modification of oleic acid during fixation of amoebae by osmium tetroxide. Biochim. biophys. Acta (Amst.)116, 325–335 (1966).

    Google Scholar 

  • —, andR. A. Weisman: I. Loss of lipids during preparation of amoebae for electron microscopy. Biochim. biophys. Acta (Amst.)116, 309–316 (1966).

    Google Scholar 

  • Ladman, A. J., H. A. Padykula, andE. W. Strauss: A morphological study of fat transport in the normal human jejunum. Amer. J. Anat.112, 389–419 (1963).

    PubMed  Google Scholar 

  • Laguesse, E.: J. Anat. (Paris)30, 591 (1894). (Quoted fromGabe andArvy 1961.)

    Google Scholar 

  • Leak, L. V., andV. J. Rosen jr.: Early ultrastructural alterations in proximal tubular cells after unilateral nephrectomy and x-irradiation. J. Ultrastruct. Res.15, 326–348 (1966).

    PubMed  Google Scholar 

  • Maeir, D. M.: Species variation in testicular Δ5-3β-hydroxysteroid dehydrogenase activity: Absence of activity in primate Leydig cells. Endocrinology76, 463–469 (1965).

    PubMed  Google Scholar 

  • Masuda, H., L. L. Anderson, D. M. Henricks, andR. M. Melampy: Progesterone in ovarian venous plasma and corpora lutea of cycling, pregnant and hysterectomized pigs. Fed. Proc.25, 444 (1966).

    Google Scholar 

  • Meldolesi, J., F. Clementi, E. Chiesara, andF. Conti: Alterations of the endoplasmic reticulum in liver cells produced by ethionine and adenine — ultrastructural and biochemical study. In: Electron microscopy, vol. 2, p. 623–624. Proc. VI Internat. Congr. Electron Microscopy, Kyoto 1966. Tokyo: Maruzen Co. 1966.

    Google Scholar 

  • Millonig, G.: Advantages of a phosphate buffer for OsO4 solutions in fixation. J. appl. Phys.32, 1637 (1961).

    Google Scholar 

  • Murakami, M.: An electron microscopic observation of the testicular interstitial tissue in the rat with special reference to the morphological changes of the interstitial cells. In: Electron microscopy, vol. 2, p. 547–548. Proc. VI Internat. Congr. Electron Microscopy, Kyoto 1966. Tokyo: Maruzen Co. 1966.

    Google Scholar 

  • —, u.Tonutti: Submikroskopische Veränderungen der Leydig-Zellen des Rattenhodens nach Behandlung mit Östrogenen und nach Gonadotropinzufuhr. Endokrinologie50, 231–250 (1966).

    PubMed  Google Scholar 

  • Nagano, T.: Some observations on the fine structure of the Sertoli cell in the human testis. Z. Zellforsch.73, 89–106 (1966).

    PubMed  Google Scholar 

  • Nilsson, O., andK. Fuxe: Morphologic changes in the mouse uterine epithelium during decomposition of lipid granules. In: Methods and achievements in experimental pathology. An introduction to experimental pathology (E. Bajusz andG. Jasmin, editors), vol. 1, p. 271–297. Basel: S.Karger 1966.

    Google Scholar 

  • Nishikawa, M., I. Murone, andT. Sato: Electron microscopic investigations of the adrenal cortex. Endocrinology72, 197–209 (1963).

    PubMed  Google Scholar 

  • Onoé, T., andK. Ohno: Role of endoplasmic reticulum in fat absorption. In: Intracellular membranous structure (S. Seno andE. V. Cowdry, editors), p. 559–568. Okayama: Japan Society for Cell Biology 1965.

    Google Scholar 

  • Orrenius, S.: Studies on the drug-hydroxylating enzyme system of rat liver microsomes. Thesis, Karolinska Institutet, Stockholm, 1965.

    Google Scholar 

  • —, andJ. L. E. Ericsson: Enzyme-membrane relationship in phenobarbital induction of synthesis of drug-metabolizing enzyme system and proliferation of endoplasmic membranes. J. Cell Biol.28, 181–198 (1966).

    PubMed  Google Scholar 

  • Orrenius, S., J. L. E. Ericsson, andL. Ernster: Phenobarbital-induoed synthesis of the microsomal drug-metabolizing enzyme system and its relationship to the proliferation of endoplasmic membranes. J. Cell Biol.25, 627–639 (1965).

    PubMed  Google Scholar 

  • Ortega, P.: Light and electron microscopy of dichlorodiphenyltrichloroethane (DDT) poisoning in the rat liver. Lab. Invest.15, 657–679 (1966).

    PubMed  Google Scholar 

  • Porter, K. R.: The ground substance; observations from electron microscopy. In: The cell (J. Brachet andA. E. Mirsky, editors), vol. 2, p. 621–675. London: Academic Press 1961.

    Google Scholar 

  • Reimer, L.: Elektronenmikroskopische Untersuchungs- und Präparationsmethoden, 2. Aufl. Berlin-Heidelberg-New York: Springer 1967.

    Google Scholar 

  • Rennels, E. G.: Observations on the ultrastructure of luteal cells from PMS and PMS-HCG treated immature rats. Endocrinology79, 373–386 (1966).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Rotschild, J.: The isolation of microsomal membranes. In: Biochemical Society Symposia No 22 (D. J. Bell andJ. K. Grant, editors), p. 4–31. Cambridge: Cambridge University Press 1963.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Schelin, U.: Chromophobe and acidophil adenomas of the human pituitary gland. A light and electron microscopic study. Acta path. microbiol. scand., Suppl.168, 1–80 (1962).

    Google Scholar 

  • Schwarz, W., u.H.-J. Merker: Die Hodenzwischenzellen der Ratte nach Hypophysektomie und nach Behandlung mit Choriongonadotropin und Amphenon B. Z. Zellforsch.65, 272–284 (1965).

    PubMed  Google Scholar 

  • — —, u.G. Suchowsky: Elektronenmikroskopische Untersuchungen über die Wirkungen von ACTH und Stress auf die Nebennierenrinde der Ratte. Virchows Arch. path. Anat.335, 165–179 (1962).

    Google Scholar 

  • Shymala, G., W. J. Lossow, andI. L. Chaikoff: Esterification of cholesterol by rat adrenal gland homogenates and subcellular components. Biochim. biophys. Acta (Amst.)116, 543–554 (1966).

    Google Scholar 

  • Siekevitz, P.: Protoplasma: Endoplasmic reticulum and microscomes and their properties. Ann. Rev. Physiol.25, 15–40 (1963).

    Google Scholar 

  • Steiner, J. W., K. Miyai, andM. J. Phillips: Electron microscopy of membrane-particle arrays in liver cells of ethionine-intoxicated rats. Amer. J. Path.44, 169–213 (1964).

    PubMed  Google Scholar 

  • Stenger, R. J.: Hepatic parenchymal cell alterations after long-term carbon tetrachloride administration. A light and electron microscopic study. Amer. J. Path.43, 867–895 (1963).

    PubMed  Google Scholar 

  • Toren, D., K. M. J. Menon, E. Forohielli, andR. I. Dorfman:In vitro enzymatic cleavage of the cholesterol side chain in rat testis preparations. Steroids3, 381–390 (1964).

    Google Scholar 

  • Trump, B. F., andJ. L. E. Ericsson: Some ultrastructural and biochemical consequences of cell injury. In: The inflammatory process (B. W. Zweifach, L. Grant andR. T. McCluskey, editors), p. 35–120. London: Academic Press 1965.

    Google Scholar 

  • —, andE. P. Benditt: A method for staining epoxy sections for light microscopy. J. ultrastruct. Res.5, 343–348 (1961).

    PubMed  Google Scholar 

  • Venable, J. H., andR. Coggeshall: A simplified lead citrate stain for use in electron microscopy. J. Cell Biol.25, 407–408 (1965).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Werthessen, N. T., E. Schwenk, andC. Baker: Biosynthesis of estrone andβ-estradiol in the perfused ovary. Science117, 380–381 (1953).

    PubMed  Google Scholar 

  • Winbladh, L.: Light microscopical and ultrastructural studies of the pancreatic islet tissue of the lamprey (Lampetra fluviatilis). Gen. comp. Endocr.6, 534–543 (1966).

    PubMed  Google Scholar 

  • Zachariae, F.: Studies on the mechanism of ovulation. Permeability of the blood-liquor barrier. Acta endocr. (Kbh.)27, 339–342 (1958).

    Google Scholar 

  • Zetterqvist, H.: The ultrastructural organization of the columnar absorbing cells of the mouse jejunum. Thesis, Karolinska Institutet, Stockholm, 1956.

    Google Scholar 

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  1. Institute of Pathology, University of Umeå, Umeå 6, Sweden

    Lars Bjersing

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Read at the Meeting of the Swedish Society for Pathology in Umeå, September 25, 1965 (Bjersing, 1966).

This investigation was supported by grants from the Swedish Medical Research Council (Projects No. 13 X-78-01, 12 X-78-02, and 12 X-78-03).

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Bjersing, L. On the ultrastructure of granulosa lutein cells in porcine corpus luteum. Z.Zellforsch 82, 187–211 (1967). https://doi.org/10.1007/BF01901701

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