Summary
The coexistence of met5- and leu5-enkephalinlike immunoreactivities with catecholamines in the rat adrenal medulla was studied with combined fluorescence microscopy and immunocytochemistry. Both met5- and leu5-enkephalin-like immunoreactivities were localized in few heavily stained adrenaline cells and in a population of nerves innervating adrenaline cells and as well as ganglion cells among the adrenaline cells. Only occasionally single noradrenaline cells exhibited light immunostaining for both enkephalins but no positive fibers could be found around the noradrenaline cells. In electron microscope the immunoreaction was seen in the granules of the adrenaline cells and in the large synaptic vesicles of the nerve terminals around the adrenaline cells. The present findings suggest that enkephalin-like immunoreactivity coexists mainly with adrenaline in rat adrenal medulla and that the enkephalin immunoreactive terminals regulate secretion of adrenaline from rat adrenal medulla.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altschuler R, Fex J, Parakkal M, Eckenstein F (1984) Colocalization of enkephalin-like and choline acetyltransferase-like immunorcactivities in olivocochlear neurons of the guinea pig. J Histochem Cytochem 32:839–843
Bloch B, Milner R, Baird A, Gubler U, Reymond C, Bohlen P, Le Guellec D, Bloom F (1984) Detection of the messenger RNA coding for preproenkephalin A in bovine adrenal by in situ hybridization. Regul Peptides 8:345–354
Bohn M, Kessler L, Golightly L, Black I (1983) Appearance of enkephalin-immunoreactivity in rat adrenal medulla following treatment with nicotinic antagonist or reserpine. Cell Tissue Res 231:496–479
Coupland RE (1965) The natural history of the chrommaffin cell. Longmans. London
Coupland RE (1972) The chrommaffin system. In: Blaschko H, Muscholl E (eds) Catecholamines. Springer, Berlin Heidelberg New York, pp 16–45
Dalsgard C-J, Hökfelt T, Elfin L-G, Terenius L (1982) Enkephalincontaining sympathetic preganglionic neurons projecting to the inferior mesenteric ganglion: evidense from combined retrograde tracing and immunohistochemistry. Neuroscience 7:2039–2050
Eränkö O (1955a) Distribution of fluorescing islets, adrenaline and noradrenaline in the adrenal medulla of the hamster. Acta Endocrinol 18:174–179
Eränkö O (1955b) Fluorescing islets, adrenaline and noradrenaline in adrenal medulla of some common laboratory animals. Ann Med Exp Fenn 33:278
Feldberg W, Minz B, Tsudzimura H (1934) The mechanism of the nervous discharge of adrenaline. J Physiol (Lond) 81:286–304
Furness, JB, Costa M, Wilson AJ (1977) Water stable fluorophores, produced by reaction with aldehyde solutions, for histochemical localization of catechol- and indolethylamines. Histochemistry 52:159–170
Glazer E, Basbaum A (1981) Immunohistochemical localization of leusine-enkephalinin the spinal cord of the cat: enkephalincontaining marginal neurons and pain modulation. J Comp Neurol 196:377–389
Hervonen A, Pelto-Huikko M, Linnoila I (1980) Ultrastructural localization of enkephalin-like immunoreactivity in the rat adrenal gland. Am J Anat 157:445–448
Hökfelt T, Fuxe K, Goldstein M, Joh T (1972) Immunohistochemical localization of three catecholamine synthetizing enzymes: Aspects on methodology. Histochemie 33:231–254
Hökfelt T, Elde R, Johansson O, Terenius L, Stein L (1977) The distribution of enkephalin immunoreactive cell bodies in the rat central nervous system. Neurosci Lett 5:25–31
Jessel T, Iversen L (1977) Opiate analgesics inhibit substance P release from rat trigeminal nucleus. Nature 268:549–551
Kobayashi S, Ohashi T, Fujita T, Nakao K, Yoshimasa T, Imura H, Mochizuki T, Yanaihara C, Yanaihara N, Verhofstad A (1983) An immunohistochemical study on the co-storage of met-enkephalin-arg6-gly7-leu8 and met-enkephalin-arg6-phe7 with adrenaline and/or noradrenaline in the adrenal chromaffin cells of the rat, dog and cat. Biomed Res 4:433–442
Kondo H, Yui R (1984) Co-existence of enkephalin and adrenalin in the frog adrenal gland. Histochemistry 80:243–246
Konishi S, Tsunoo A, Otsuka M (1979) enkephalins presynaptically inhibit cholinergic transmission in sumpathetic ganglia. Nature 282:515–516
Konishi S, Tsunoo A, Otsuka M (1981) Enkephalin as a transmitter for presynaptic inhibition in sympathetic ganglia. Nature 294:80–82
Kumakura K, Guidotti A, Yang H-Y, Saiani L, Costa E (1980) A role for the opiate peptides that presumably coexist with acetylcholine in splanchnic nerves. In: Costa E, Trabucchi M (eds) Neural peptides and neuronal communication. Raven Press, New York, pp 570–580
LaGamma E, Adler, J, Black I (1984) Impulse activity differentially regulates (leu)enkephalina and catecholamine characters in the rat adrenal medulla. Science 224:1102–1104
Lang R, Taugner G, Gaida W, Ganten D, Kraft K, Unger T, Wunderlich I (1983) Evidence against co-storage of enkephalins with noradrenaline in bovine adrenal medullary granules. Eur J Pharmacol 86:117–120
Lewis R, Stern A, Kilpatrick D, Gerber L, Rossier J, Stein S, Udenfriend S (1981) Marked increase in large enkephalin-containing polypeptides in the rat adrenal gland following denervation. J Neurosci 1:80–82
Linnoila I, DiAugustine RP, Hervonen A, Miller R (1980) Distribution of (leu5) and (met5) enkephalin-, VIP- and SP-like immunoreactivity in human adrenal glands. Neuroscience 5:2247–2259
Livett B, Day R, Elde R, Howe P (1982) Co-storage of enkephalins and adrenaline in the bovine adrenal medulla. Neuroscience 7:1323–1332
Lundberg JM, Hamberger B, Schultzberg M, Hökfelt T, Granberg P-O, Efendie S, Terenius L, Goldstein M, Luft R (1979) Enkephalin-and smatostatin-like immunoreactivities in human adrenal medulla and pheochromocytoma. Proc Natl Acad Sci USA 76:4079–4083
Matsui H (1984) Adrenal medullary secretion in response to diencephalic stimulation in the rat. Neuroendocrinology 38:164–168
Miller R, Chang K-J, Cooper B, Cuatrecasas P (1978) Radioimmunoassay and characterization of enkephalins in rat tissues. J Biol Chem 253:531–538
Pelto-Huikko M, Salminen T, Hervonen A (1982) Enkephalin-like immunoreactivity is restricted to the adrenaline cells in hamster adrenal medulla. Histochemistry 73:493–497
Pelto-Huikko M, Salminen T, Partanen M, Toivanen M, Hervonen A (1985) Immunohistochemical localization of neurotensin in hamster adrenal medulla. Anat Rec 211:(in press)
Pickel VM, Joh TH, Reis DJ, Leeman SE, Miller RJ (1979) Electron-microscopic localization of substance-P and enkephalin in axon terminals related to dendrites of catecholaminergic neurons. Brain Res 160:387–400
Robinson RL, Gulberson, JL, Carmichael SW (1983) Influence of hypothalamic stimulation on the secretion of adrenal medullary catecholamines. J Autonom Nerv Syst 8:889–896
Roisin M, Artola A, Henry J, Rossier J (1983) Enkephalins are associated with adrenergic granules in bovine adrenal medulla. Neuroscience 10:83–88
Schultzberg M, Lundberg JM, Hökfelt T, Terenius L, Brandt J, Elde R, Goldstein M (1978) Enkephalin-like immunoreactivity in gland cells and nerve terminals of the adrenal medulla. Neuroscience 3:1169–1186
Sternberger LA (1979) Immunocytochemistry. 2nd edn. John Wiley & Sons, New York
Varndell IM, Tapia FJ, De Mey J, Rush RA, Bloom SR, Polak JM (1982) Electron immunocytochemical localization of enkephalin-like material in catecholamine-containing cells of the carotid body, the adrenal medulla, and in pheochromocytomas of man and other mammals. J Histochem Cytochem 30:682–690
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Pelto-Huikko, M., Salminen, T. & Hervonen, A. Localization of enkephalins in adrenaline cells and the nerves innervating adrenaline cells in rat adrenal medulla. Histochemistry 82, 377–383 (1985). https://doi.org/10.1007/BF00494067
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00494067