Summary
Tubular channels from mitochondria to catecholamine-storage vesicles have been demonstrated in thick sections of adrenal medullary tissue from hypoglycemia-stressed rats by the use of the high voltage electron microscope. The function of these connections is not presently known although they may serve as channels for the transport of materials such as high-energy nucleotides from one organelle to the other. The present study has examined only the adrenal medulla, but it should be considered that such connections may also exist in other neural cells and possibly other cells in which there is intracellular transport of ATP.
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References
Agostini, B., Taugner, G.: The membrane of the catecholamine storage vesicles of the adrenal medulla. Histochemie 33, 255–272 (1973)
Agrell, I.P.S.: Continuity of the membrane systems in the cells of imaginal discs. Z. Zellforsch. 72, 22–29 (1966)
Andersson-Cedergren: Ultrastructure of motor end plate and sarcoplasmic components of mouse skeletal muscle fiber as revealed by three-dimensional reconstructions from serial sections. J. Ultrastruct. Res. S1, 1–181 (1959)
André, J.: Etude au microscope électronique de l'évolution du chondriome pendant la spermatogénèse du Scorpion Euscorpius flavicaudis. J. Ultrastruct Res. 2, 288–308 (1959)
Bernhard, W., Rouiller, C.: Close topographical relationship between mitochondria and ergastoplasm of liver cells in a definite phase of cellular activity. J. biophys. biochem. Cytol. 2, Suppl. (1956)
Bowman, R.W.: Mitochondrial connections in canine myocardium. Tex. Rep. Biol. Med. 25, 517–524 (1967)
Bracker, C.E., Grove, N.: Continuity between cytoplasmic endomembranes and outer mitochondrial membranes in fungi. Protoplasma 73, 15–34 (1971)
Brandt, P.W., Pappas, G.D.: Mitochondria, II. The Nuclearmitochondrial relationship in Pelomxya carolinensis Wilson (Chaos chaos L.). J. biophys. biochem. Cytol. 6, 91–95 (1959)
Burnstock, G.: Purinergic Nerves. Pharmacol. Rev. 24, 509–581 (1972)
Carlsson, A., Hillarp, N.A.: Release of adenosine triphosphate along with adrenaline and noradrenaline following stimulation of the adrenal medulla. Acta physiol. scand. 36, 235–239 (1956)
Carlsson, A., Hillarp, N.A., Waldeck, B.: Analysis of the Mg-ATP dependent storage mechanism in the amine granules of the adrenal medulla. Acta physiol. scand. 59, Suppl. 215, 1–38(1963)
Carmichael, S.W.: Fluorescence microscopy of the adrenal medulla of the newborn puppy after asphyxia and hypothermia. Acta anat. (Basel) 87, 131–140 (1974)
Coupland, R.E.: Electron microscopic observations on the structure of the rat adrenal medulla I. The ultrastructure and organization of chromaffin cells in the normal adrenal medulla. J. Anat. (Lond.) 99, 231–254 (1965)
Diers, L.: On the plastids, mitochondria, and other cell constituents during oogenesis of a plant. J. Cell Biol. 28, 527–543 (1966)
Droz, B.: Synthetic machinery and axoplasmic transport: maintenance of neural connectivity. D.B. Tower (Ed.), The nervous system, Vol I, The basic neurosciences, pp. 111–127. 1975. New York: Raven Press
Droz, B., Koenig, H.L., Giamberardino, L.D.: Axonal migration of protein and glycoprotein to nerve endings. I. Radioautographic analysis of the renewal of protein in nerve endings of chicken ciliary ganglion after intracerebral injection of (3H) lycine. Brain Res. 60, 93–127 (1973)
Forbes, M.S., Sperelakis, N.: Spheroidal bodies in the junctional sarcoplasmic reticulum of lizard myocardial cells. J. Cell Biol. 60, 602–615 (1974)
Franke, W.W., Kartenbeck, J.: Outer mitochondrial membrane continuous with endoplasmic reticulum. Protoplasma 73, 35–41 (1971)
Ghidoni, J.J., Thomas, H.: Connection between a mitochondrion and endoplasmic reticulum in liver. Experientia (Basel) 25, 632–633 (1969)
Goeckermann, J.A., Vigil, E.L.: Peroxisome development in the metanephric kidney of the mouse. J. Histochem. Cytochem. 23, 957–973 (1975)
Hillarp, N.A., Nilson, B., Hogberg, B., Leo, A.B.: Adenosine triphosphate in the adrenal medulla of the cow. Nature (Lond). 176, 1032–1033 (1955)
Jamieson, J.D., Palade, G.E.: Specific granules in atrial muscle cells. J. Cell Biol. 23, 155 (1964)
Kessel, R.G.: Cytodifferentiation in the Rana pipiens oocyte, II, Intramitochondrial yolk. Z. Zellforsch. 112, 313–332 (1971)
Kirshner, N.: Uptake of catecholamines by a particulate fraction of the adrenal medulla. J. biol. Chem. 237, 2311–2317 (1962)
Klingenberg, M.: The ADP-ATP carrier in mitochondrial membranes. A. Martonosi (Ed.), The enzymes of biological membranes, pp. 383–437 (1976)
Kostron, H., Winkler, H., Peer, L.J., Konig, P.: Uptake of adenosine triphosphate by isolated adrenal chromaffin granules: A carrier-mediated transport. Neurosci. 2, 159–166 (1977)
Moore, D.J., Merrit, W.D., Lembi, C.A.: Connections between mitochondria and endoplasmic reticulum in rat liver and onion stem. Protoplasma 73, 43–49 (1971)
Norberg, H.S.: The morphological relationship between mitochondria and cytoplasmic membranes of the follicular oocyte in domestic pig. Z. Zellforsch. 124, 520–531 (1972)
Nunez, E.A.: Secretory processes in follicular cells of the bat thyroid, II. The occurrence of organelle-associated intercellular junctions during late hibernation. Amer. J. Anat. 131, 227–240 (1971)
Palade, G.E.: The fine structure of mitochondria. Anat. Rec. 114, 427–451 (1952)
Pannese, E.: Expansive growth of the nuclear envelope and formation of mitochondria in ganglionic neuroblasts. Z. Zellforsch. 72, 295–324 (1966)
Paulin, J.J.: The chondriome of selected trypanosomatids. J. Cell Biol. 66, 404–413 (1975)
Peer, L.J., Winkler, H., Snider, S.R., Gibb, J.W., Baumgartner, H.: Synthesis of nucleotides in adrenal medulla and their uptake into chromaffin granules. Biochem. Pharmacol. 25, 311–316 (1976)
Poisner, A.M., Trifaro, J.M.: The role of ATP and ATPase in the release of catecholamines from the adrenal medulla: I. ATP-evoked release of catecholamines, ATP, and protein from isolated chromaffin granules. Molec. Pharmacol. 3, 561–571 (1967)
Pollard, H.B., Miller, A., Cox, G.C.: Synaptic vesicles; structure of chromaffin granule membranes. J. Supramol. Struct. 1, 295–306 (1973)
Reiter, W.: Über das Raumsystem des endoplasmatischen Retikulums von Hautnervenfasern. Untersuchungen an Serienschnitten. Z. Zellforsch. 72, 446–461 (1966)
Robertson, J.D.: Interrelationships between mitochondria and the endoplasmic reticulum bearing on a theory of the origin of mitochondria. J. Physiol. (Lond.) 153, 58–59P (1961)
Robinson, R.L., Watts, D.T.: An automated trihydroxyindole procedure for the differential analysis of catecholamines. Clin. Chem. 11, 986–997 (1965)
Ruby, J.R., Dyer, R.F., Skalko, R.G.: Continuities between mitochondria and endoplasmic reticulum in the mammalian ovary. Z. Zellforsch. 97, 30–37 (1969)
Schmekel, L., Fioroni, P.: Cell differentiation during early development of Nassarius reticulatus L. (Gastropoda Prosobranchia). I. Zygote to 16-cell stage. Cell Tiss. Res. 159, 503–522 (1975)
Siebert, G.: The biochemical environment of the mammalian nucleus. Subcell. Biochem. 1, 277–292 (1972)
Sinha, A.A., Seal, U.S., Doe, R.P.: Fine structure of the corpus luteum of the raccoon during pregnancy. Z. Zellforsch. 117, 35–45 (1971)
Sjöstrand, F.S.: Electron microscopy of mitochondria and cytoplasmic double membranes. Nature (Lond.) 171, 30–32 (1953)
Stevens, P., Robinson, R.L., Van Dyke, K., Stitzel, R.: The temperature dependence of (8-3H) adenosine labelling of the perfused bovine and canine adrenal gland. J. Pharm. Pharmacol. 27, 864 (1975)
Stormorken, H.: The release reaction of secretion. Scand. J. Haematol. 9, Suppl., 3–24 (1969)
Sybers, H.D., Ashraf, M.: Scanning electron microscopy of cardiac muscle. Lab. Invest. 30, 441–450 (1974)
Szöllösi, D., Hunter, R.H.F.: A special attachment complex between the rough endoplasmic reticulum and mitochondria in porcine oocytes. J. Microsc. 15, 105–110 (1973)
Tedeschi, H., Harris, D.L.: The osmotic behavior and permeability to non-electrolytes of mitochondria. Arch. Biochem. Biophys. 58, 52–67 (1955)
Thiéry, G., Rambourg, A.: A new staining technique for studying thick sections in the electron microscope. J. Microscopie Biol. Cell 26, 103–196 (1976)
Threadgold, L.T., Lasker, R.: Mitochondriogenesis in integumentary cells of the larval sardine (Sardinops caerulea). J. Ultrastruct. Res. 19, 238–249 (1967)
Trifaró, J.M., Dworkind, J.: Phosphorylation of membrane components of adrenal chromaffin granules by adenosine triphosphate. Molec. Pharmacol. 7, 52–65 (1971)
Trifarò, J.M., Dworkind, J.: Phosphorylation of the membrane components of chromaffin granules synthesis of diphosphatidylinositol and presence of phosphatidylinositol kinase in granule membranes. Canad. J. Physiol. Pharmacol. 53, 479–492 (1975)
Trifaró, J.M., Poisner, A.M.: The role of ATP and ATPase in the release of catecholamines from the adrenal medulla; II. ATP-evoked fall in optical density of isolated chromaffin granules. Molec. Pharmacol. 3, 572–580 (1967)
Volk, T.L.: Mitochondrial-tubular membrane interconnections in the rat adrenal cortex. Lab. Invest. 25, 349–355 (1971)
Walker, S.M., Schrodt, G.: Evidence for structural connections between mitochondria and intermediate elements of triads. Phys. Med. 45, 26–44 (1966)
Wassermann, D., Wassermann, M.: The fine structure of adrenal zona glomerulosa in the adult rat. Cell Tiss. Res. 149, 235–243 (1974)
Waugh, R.A., Sommer, J.R., Peachey, L.D.: Cardiac sarcoplasmic reticulum: distribution and ultrastructure revealed by selective staining. Abstracts of the 47th Scientific Sessions. Circulation Suppl. III. 13–49 & 50
Weakley, B.S.: Specializations of the outer mitochondrial membrane during oocyte development. Cell Tiss. Res. 180, 515–528 (1977)
Winkler, H., Smith, A.D.: The chromaffin granule and the storage of catecholamines. G. Sayers, H. Blaschko, A. Smith (Eds.), Handbook of Physiology, Vol. VI., Washington: Amer. Physiol. 19
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This work was supported by NIH DRR 70-4136, WVU Medical Corporation Research Grants, Biomedical Research Support Grant 5 SOI RR05433, WVU Senate Research Grant, and West Virginia Heart Association Research Grant. We wish to thank Barbara Coalgate, Billie Pack, and the staffs of the HVEM laboratories at U.S. Steel and University of Colorado.
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Carmichael, S.W., Smith, D.J. Direct connections between mitochondria and catecholamine-storage vesicles demonstrated by high voltage electron microscopy in rat adrenal medulla. Cell Tissue Res. 191, 421–432 (1978). https://doi.org/10.1007/BF00219806
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DOI: https://doi.org/10.1007/BF00219806