Summary
The cortical cell of the interrenal gland of the American bullfrog, Rana catesbeiana, was examined in the electron microscope. These cells occur in small groups and cords and are quite irregular in shape. The cortical cell is reminiscent of adrenal cortical cells from other vertebrates. Liposomes are variable in size and density. Smooth endoplasmic reticulum is scant in amount and predominantly of the fine tubular type. Mitochondria have vesicular cristae, a dense matrix, and occasionally have blebs, vacuoles, and myelin-like whorls at their surfaces. Intimate morphological relationships are found among the Golgi apparatus, lysosomes, and liposomes, and among Golgi vacuoles, mitochondria, and liposomes. In addition microfibrils are a prominent feature of the cortical cell. The biochemical events of steroidogenesis in amphibia and other vertebrates are discussed in relationship to the organellar interrelations found in the bullfrog interrenal cortical cells. Based on the available chemical and morphological information a scheme is proposed of movement of the steroidal intermediates through the cell that tentatively identifies the localizations of the various enzyme systems involved in corticosteroidogenesis from acetate to corticosterone and aldosterone.
Similar content being viewed by others
Bibliography
Berchtold, J. P.: Effets de l'hypophysectomie sur la structure fine des cellules interrénales de l'urodele Triturus cristatus. C. R. Acad. Sci. (Paris) (D) 268, 2262–2264 (1969a).
—: Aspects ultrastructuraux des cellules interrénales de salamandres (Salamandra salamandra L.) atteintes d'une maladie mycosique. C.R. Acad. Sci. (Paris) (D) 268, 1742–1744 (1969b).
Beyer, K. F., Samuels, L. T.: Distribution of steroid-3β-ol-dehydrogenase in cellular structures of the adrenal gland. J. biol. Chem. 219, 69–76 (1956).
Brownie, A. C., Grant, J. K.: The in vitro hydroxylation of steroid hormones. I. Factors influencing the enzymic 11β-hydroxylation of 11-deoxycorticosterone. Biochem. J. 57, 255–263 (1954).
Bunt, A. H.: Fine structure of the pars distalis and interrenals of Taricha torosa after administration of metopirone (SU-4885). Gen. comp. Endocr. 12, 134–147 (1969).
Burgos, M. H.: Histochemistry and electron microscopy of the three cell types in the adrenal gland of the frog. Anat. Rec. 133, 163–185 (1959).
Caro, L. G., Palade, G. E.: Protein synthesis, storage, and discharge in the pancreatic exocrine cell. An autoradiographic study. J. Cell Biol. 20, 473–495 (1964).
Carstensen, H., Burgers, A. C. J., Li, C. H.: Demonstration of aldosterone and corticosterone as the principal steroids formed in incubates of adrenals of the American bullfrog (Rana catesbeiana) and stimulation of their production by mammalian adrenocorticotropin. Gen. comp. Endocr. 1, 37–50 (1961).
Cater, D. B., Lever, J. D.: The zona intermedia of the adrenal cortex. A correlation of possible functional significance with development, morphology, and histochemistry. J. Anat. (Lond.) 88, 437–454 (1954).
Chan, S. W. C., Vinson, G. P., Phillips, J. G.: Pathways for the biosynthesis of corticosteroids from pregnenolone by adrenal tissue of the frog, Rana rugulosa. Gen. comp. Endocr. 12, 644–650 (1969).
Essner, E., Novikoff, A. B.: Cytological studies on two functional hepatomas. Interrelations of endoplasmic reticulum, Golgi apparatus, and lysosomes. J. Cell Biol. 15, 289–312 (1962).
Friend, D. S., Brassil, G. E.: Osmium staining of endoplasmic reticulum and mitochondria in the rat adrenal cortex. J. Cell Biol. 46, 252–266 (1970).
Fujimura, W., Nishiki, T., Ueyama, S., Koishi, T., Mori, K.: Electron microscope studies on the adrenal glands of amphibia. Med. Ass. J. (Nara, Japan) 10, 203–209 (1959).
Geyer, G.: Histochemische und elektronenmikroskopische Untersuchungen an der Nebenniere von Rana esculenta. Acta histochem. (Jena) 8, 234–288 (1959).
Gibbons, I. R., Grimstone, A. V.: On flagellar structure in certain flagellates. J. biophys. biochem. Cytol. 7, 697–716 (1960).
Grant, J. K.: The biosynthesis of adrenocortical steroids. J. Endocr. 41, 111–135 (1968).
Halkerston, I. D. K., Eichhorn, J., Hechter, O.: TPNH requirement for cholesterol side chain cleavage in adrenal cortex. Arch. Biochem. 85, 287–289 (1959).
Harrison, G.: Some aspects of the comparative ultrastructure of interrenal tissue in amphibians, reptiles, and birds. Dissertation, Boston University, Boston, Massachusetts 1963.
Ichii, S., Kobayashi, S., Yago, N., Omata, S.: Role of plasma cholesterol in rat adrenal corticosteroidogenesis in vitro. Endocr. jap. 14, 138–142 (1967).
—, Okada, N., Ikeda, A.: Effect of ACTH on the interconversion of ester and free cholesterol and corticosterone biosynthesis in rat adrenal glands. Endocr. jap. 17, 83–87 (1970).
Idelman, S.: Contribution à la cytophysiologie infrastructurale de la corticosurrénale chez le rat albinos. Ann. Sci. Nat. Zool. Biol. Animale 8, 205–362 (1966).
—: Ultrastructure of the mammalian adrenal cortex. Int. Rev. Cytol. 27, 181–281 (1970).
Johnston, C. I., Davis, J. O., Brown, T. C., Wright, F., Howards, S.: Effects of ACTH and renin on in vivo aldosterone production in the frog. Fed. Proc. 25, 494 (1966).
—, Wright, F. S., Howards, S. S.: Effects of renin and ACTH on adrenal steroid secretion in the American bullfrog. Amer. J. Physiol. 213, 393–399 (1967).
Kemenade, J. A. M., van: Effect of ACTH and hypophysectomy on the interrenal tissue in the common frog, Rana temporaria. Z. Zellforsch. 92, 549–566 (1968).
—, Dongen, W. J., van: Adrenal cortical activity in the common frog, Rana temporaria. Gen. comp. Endocr. 5, 712 (1965).
Kjaerheim, A.: Studies of adrenocortical ultrastructure. 4. Effects of ACTH on interrenal cells of the domestic fowl. J. Microscopie 7, 715–738 (1968).
Lentz, T. L.: Rhabdite formation in planaria: The role of microtubules. J. Ultrastruct. Res. 17, 114–126 (1967).
Millonig, G.: Advantages of a phosphate buffer OsO4 solutions in fixation. J. appl. Phys. 32, 1637 (1961).
Morris, M. D., Chaikoff, I. L.: The origin of cholesterol in liver, small intestine, adrenal gland, and testis of the rat: Dietary versus endogenous contributions. J. biol. Chem. 234, 1095–1097 (1959).
Moses, H. L., Davis, W. W., Rosenthal, A. S., Garren, L. D.: Adrenal cholesterol: Localization by electron-microscope autoradiography. Science 163, 1203–1205 (1969).
Ogawa, M.: Fine structure of the corpuscles of Stannius and the interrenal tissue in goldfish. Carassius auratus. Z. Zellforsch. 81, 174–189 (1967).
Palay, S. L., Sotelo, C., Peters, A., Orkand, P. M.: The axon hillock and the initial segment. J. Cell Biol. 38, 193–201 (1968).
Pehlemann, F. W., Hanke, W.: Funktionsmorphologie des Interrenalorgans von Rana temporaria L. Z. Zellforsch. 89, 281–302 (1968).
Piezzi, R. S., Burgos, M. H.: The toad adrenal gland. 1. Cortical cells during summer and winter. Gen. comp. Endocr. 10, 344–354 (1968).
Raman, P. B., Sharma, D. C., Dorfman, R. I.: Studies on aldosterone biosynthesis in vitro. Biochemistry 5, 1795–1804 (1966).
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).
Roth, L. E., Pihlaja, D. J., Shigenaka, Y.: Microtubules in the heliozoan axopodium. 1. The gradion hypothesis of allosterism in structural proteins. J. Ultrastruct. Res. 30, 7–37 (1970).
Ryan, K. J., Engel, L. L.: Hydroxylation of steroids at carbon 21. J. biol. Chem. 225, 103–114 (1957).
Sabatini, D. D., DeRobertis, E. D., Bleichmar, H. B.: Submicroscopic study of the pituitary action on the adrenocortex of the rat. Endocrinology 70, 390–406 (1962).
Sandborn, E., Koen, P. F., McNabb, J. D., Moore, G.: Cytoplasmic microtubules in mammalian cells. J. Ultrastruct. Res. 11, 123–138 (1964).
Schwarz, W., Merker, H. J., Suchowsky, G.: Elektronenmikroskopische Untersuchungen über die Wirkungen von ACTH und Stress auf die Nebennierenrinde der Ratte. Virchows Arch. path. Anat. 335, 165–179 (1962).
—, Suchowsky, G. K.: Die Wirkung von Metopiron und Amphenon B auf die Nebennierenrinde der Ratte. Virchows Arch. path. Anat. 337, 270–278 (1963).
Sheridan, M. N., Belt, W. D.: Fine structure of the interrenal cells in the salamander, Necturus maculosus. Anat. Rec. 148, 402 (1964a).
—: Fine structure of the guinea pig adrenal cortex. Anat. Rec. 149, 73–97 (1964b).
Smith, R. E., Farquhar, M. G.: Lysosome function in the regulation of the secretory process in cells of the anterior pituitary gland. J. Cell Biol. 31, 319–347 (1966).
Stilling, H.: Zur Anatomie der Nebennieren. Arch. mikr. Anat. 52, 176–195 (1898).
Sweat, M. L.: Enzymatic synthesis of 17-hydroxycorticosterone. J. Amer. chem. Soc. 73, 4056 (1951).
Volk, T. L.: Mitochondrial-tubular membrane interconnections in the rat adrenal cortex. Lab. Invest. In press (1971 a).
- Alterations of the adrenal cortex of rats treated with progesterone. Virchows Arch. path. Anat. In press (1971 b).
Volk, T. L.: Morphologic observations on the summer cell of Stilling in the interrenal gland of the American bullfrog (Rana catesbeiana). Submitted for publication (1971 c).
- Ultrastructure of the chromaffin cell of the interrenal gland of the Americal bullfrog (Rana catesbeiana). In preparation (1971 d).
—, Scarpelli, D. G.: Alterations of fine structure of the rat adrenal cortex after the administration of triparanol. Lab. Invest. 13, 1205–1214 (1964).
Werbin, H., Chaikoff, I. L.: Utilization of adrenal gland cholesterol for synthesis of cortisol by the intact normal and the ACTH-treated guinea pig. Arch. Biochem. 93, 476–482 (1961).
Yoshimura, F., Harumiya, K.: Electron microscopy of adrenal cortex cells in the hypophysectomized and ACTH administered bullfrogs. Sixth Int. Congr. Electron Microscopy, Kyoto, vol. II, p. 545–546 (1966).
Author information
Authors and Affiliations
Additional information
Supported in part by N.I.H. Grant RR 06138. Health Sciences Advancement Award.
Rights and permissions
About this article
Cite this article
Volk, T.L. Ultrastructure of the cortical cell of the interrenal gland of the American bullfrog (Rana catesbeiana). Z. Zellforschung 123, 470–485 (1972). https://doi.org/10.1007/BF00335543
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00335543