Summary
The localization of the proenkephalin A-derived octapeptide, Met5-enkephalin-Arg6-Gly7-Leu8 (MEAGL), was studied in the major salivary glands of Sprague-Dawley and Wistar rats with the indirect immunofluorescence method. MEAGL-immunoreactive nerve fibers were found around the acini, along intra-and interlobular salivary ducts and in close contact with blood vessels. In the parotid and submandibular glands tyrosine hydroxylase (TH) immunoreactivity was observed in nerve fibers around the acini, in association with intra- and interlobular salivary ducts and around blood vessels, while in the sublingual gland TH-immunoreactive nerve fibers were only seen around blood vessels. Parasympathetic neurons in submandibular ganglia contained MEAGL immunoreactivity. Moderate TH immunoreactivity was seen in some neurons of the submandibular ganglia. A subpopulation of sympathetic principal neurons in the superior cervical ganglion were immunoreactive for both MEAGL and TH. In the trigeminal ganglion, no MEAGL-immunoreactive sensory neurons or nerve fibers were observed. Superior cervical ganglionectomies resulted in a complete disappearance of TH-immunoreactive nerve fibers, while MEAGL-immunoreative nerve fibers were still present in the glands. The presence of MEAGL immunoreactivity in neurons of both sympathetic superior cervical ganglia and parasympathetic submandibular ganglia and the results of superior cervical ganglionectomies suggest, that MEAGL-immunoreactive nerve fibers in the major salivary glands of the rat have both sympathetic and parasympathetic origin.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Björklund H, Hoffer B, Olson L, Palmer M Seiger Å (1984) Enkephalin immunoreactivity in iris nerves: distribution in normal and grafted irides, persistence and enhanced fluorescence after denervations. Histochemistry 80:1–7
Bowers CW, Zigmond RE (1979) Localization of neurons in the rat superior cervical ganglion that project into different post-ganglionic trunks. J Comp Neurol 185:381–391
Dingledine R (1985) Opioid peptides: central nervous system. In: Rogawsky MA, Barker JL (eds) Neurotransmitter actions in the vertebrate nervous system. Plenum Publishing Corporation, pp 341–364
Di Giulio AM, Yang H-YT, Lutold B, Fratta W, Hong J, Costa E (1978) Characterization of enkephalin-like material extracted from sympathetic ganglia. Neuropharmacology 17:989–992
Erichsen JT, Karten HJ, Eldred WD, Brecha NC (1982) Localization of substance P-like and enkephalin-like immunoreactivity within preganglionic terminals of the avian ciliary ganglion: light and electron microscopy. J Neurosci 2:994–1003
Häppölä O, Soinila S, Päivärinta H, Panula P (1987) Met5-Enkephalin-Arg6-Phe7- and Met5-Arg6-Gly7-Leu8-immunoreactive nerve fibers and neurons in the superior cervical ganglion of the rat. Neuroscience 21:283–295
Hughes J, Kosterlitz HW, Smith TW (1977) The distribution of methionine-enkephalin and leucine-enkephalin in the brain and peripheral tissues. Br J Pharmacol 61:639–647
Ikeda Y, Nakao K, Yoshimasa T, Yanaihara N, Numa S, Imura H (1982) Existence of Met-enkephalin-Arg6-Gly7-Leu8 with Met-enkephalin, Leu-enkephalin and Met-enkephalin-Arg6-Phe7 in the brain of guinea pig, rat and golden hamster. Biochem Biophys Res Commun 107:656–662
Joh TH, Geghman C, Reis DJ (1973) Immunochemical demonstration of increased accumulation of tyrosine hydroxylase protein in sympathetic ganglia and adrenal medulla elicited by reserpine. Proc Natl Acad Sci USA 70:2767–2773
Joh TH, Ross ME (1983) Preparation of catecholamine-synthesizing enzymes as immunogens for immunohistochemistry. In: Cuello AC (ed) Immunohistochemistry. Wiley, Chichester, pp 121–138
Kawa K, Roper S (1984) On the two subdivisions and intrinsic synaptic connections in the submandibular ganglion of the rat. J Physiol 346:301–320
Kobayashi S, Uchida T, Ohashi T, Fujita T, Imura H, Mochizuki T, Yanaihara C, Yanaihara N (1983a) Met-enkephalin-Arg-Gly-Leu-like immunoreactivity in adrenal chromaffin cells and carotid body chief cells of the dog and monkey. Biomed Res 4:201–210
Kobayashi S, Uchida T, Ohashi T, Fujita T, Nakao K, Yoshimasa T, Imura H, Mochizuki T, Yanaihara C, Yanaihara N, Verhofstad AAJ (1983b) Immunocytochemical demonstration of the co-storage noradrenaline with Met-enkephalin-Arg6-Phe7 and Met-enkephalin-Arg6-Gly7-Leu8 in the carotid body chief cells of the dog. Arch Histol Jpn 46:713–722
Kondo H, Yamamoto M, Yanaihara N, Nagatsu I (1988) Transient involvement of enkephalins in both the sympathetic and parasympathetic innervations of the submandibular gland of rats. Light- and electron microscopic immunocytochemical study. Cell Tissue Res 253:529–537
Konishi S (1985) Opioid peptides: peripheral nervous system. In: Rogawsky MA, Barker JL (eds) Neurotransmitter actions in the vertebrate nervous system. Plenum Publishing Corporation, pp 365–383
Lichtman JW (1977) The reorganization of synaptic connexions in the rat submandibular ganglion during postnatal development. J Physiol 273:155–177
Lindberg I, Yang H-YT (1984) Distribution of Met5-enkephalin-Arg6-Gly7-Leu8 immunoreactive peptides in rat brain: presence of multiple molecular forms. Brain Res 330:127–134
Lundberg JM, Martling C-R, Hökfelt T (1988) Airways, oral cavity and salivary glands: classical transmitters and peptides in sensory and autonomic motor neurons. In: Björklund A, Hökfelt T, Owman C (eds) Handbook of chemical neuroanatomy. Elsevier, Amsterdam New York Oxford, pp 391–444
Miller RJ, Pickel VM (1980) The distribution and functions of the enkephalins. J Histochem Cytochem 28:903–917
Reiner A (1987) A VIP-like peptide co-occurs with substance P and enkephalin in cholinergic preganglionic terminals of the avian ciliary ganglion. Neurosci Lett 78:22–28
Rossier J, Audigier Y, Ling N, Cros J, Udenfriend S (1980) Metenkephalin-Arg6-Phe7, present in high amounts in brain of rat, cattle and man, is an opioid agonist. Nature 288:88–90
Shimosegawa T, Koizumi M, Toyota T, Goto Y, Yanaihara C, Yanaihara N (1987) An immunohistochemical study of methionine-enkephalin-Arg6-Gly7-Leu8-like immunoreactivity containing neurons in the parasympathetic preganglionic regions of the rat spinal cord. Brain Res 406:341–347
Schultzberg M, Hökfelt T, Terenius L, Elfin L-G, Lundberg JM, Brandt J, Elde RP, Goldstein M (1979) Enkephalin immunoreactive nerve terminals and cell bodies in sympathetic ganglia of the guinea pig and rat. Neuroscience 4:249–270
Wharton J, Polak JM, Bryant MG, Van Noorden S, Bloom SR, Pearse AGE (1979) Vasoactive intestinal polypeptide (VIP)-like immunoreactivity in the salivary glands. Life Sci 25:273–280
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Soinila, J., Salo, A., Uusitalo, H. et al. Met5-enkephalin-Arg6-Gly7-Leu8-immunoreactive nerve fibers in the major salivary glands of the rat: evidence for both sympathetic and parasympathetic origin. Cell Tissue Res 264, 15–22 (1991). https://doi.org/10.1007/BF00305718
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00305718