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Histochemically demonstrable catecholamines and cholinesterases in nerve fibres of rat dorsal skin

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Histochemically demonstrable cholinesterases of rat skin and cutaneous nerves hydrolyze acetylthiocholine iodide and butyrylthiocholine iodide. Cholinesterase activity of the skin was located in the epidermis, in the hair follicles at the level of the sebaceous glands, in adjacent parts of the sebaceous glands, in erector pili muscles and their nerves, in cutaneous and subcutaneous nerves and nerve trunks, including some nerves accompanying cutaneous blood vessels, and in the membranes of fat cells. No encapsulated nerve endings were found. In the nerves of erector pili muscles there was some neurilemmal non-specific cholinesterase activity, demonstrated in the presence of 10−5 M BW 284C 51, and specific acetylcholinesterase activity resistant to 10−5 M iso-OMPA. The cholinesterase activity in other cutaneous nerves was inhibited by 10−5 M iso-OMPA but was resistant to 10−5 M BW284 C 51, thus representing mainly non-specifc cholinesterase (nsChE) activity.

The adrenergic nerves of the dorsal skin, as revealed by glyoxylic acid-induced fluorescence (GIF), were located in association with erector pili muscles and surrounded arteries and arterioles. Small fluorescent nerves were situated in subcutaneous nsChE-positive nerve trunks.

Using GIF and cholinesterase techniques performed either simultaneously or consecutively, it was found that the nsChE-positive, probably sensory, nerves accompanying blood vessels were fewer in number than the fluorescent adrenergic nerves and ran a course independent of them. No cholinesterase reaction was seen in the fluorescent adrenergic nerves when short incubation times were used. When the incubation time was prolonged overnight, the nsChE reaction closely followed the course of fluorescent adrenergic nerves.

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References

  • Adams, C.W.M., Grant, R.T., Baylis, O.B.: Cholinesterases in peripheral nervous system. I Mixed motor and sensory trunks. Brain Res. 5, 366–376 (1967)

    Google Scholar 

  • Allen, J.M., Eränkö, O., Hunter, R.L.: A histochemical study of the esterases of the adrenal medulla of the rat. Amer J. Anat. 102, 93–115 (1958)

    Google Scholar 

  • Allen, J.M., Eränkö, O., Hunter, R.L.: A cytochemical study of cholinesterase activity in the adrenal medulla of the rat. Anat. Rec. 128, 514–515 (1957)

    Google Scholar 

  • Akoev, G.N., Chelyshev, Yu.A., Elman, S.J.: Effect of acetylcholine and catecholamines on excitability of Paccinian corpuscles in Progress in Brain Res. (Iggo, A and Ilyinsky, O.B. eds.), 43, 187–193, Amsterdam: Elsevier Publ. 1976

    Google Scholar 

  • Beckett, E.B., Bourne, G.H., Montahna, W.: Histology and cytochemistry of human skin. The distribution of cholinesterase in the finger of the embryo and the adult. J. Physiol. 134, 202–206 (1956)

    Google Scholar 

  • Bell, C., McLean, J.R.: Localization of norepinephrine and acetylcholinesterase in separate neurons supplying the guinea pig vas defferens. J. Pharmacol. Exp. Ther. 157, 69–73 (1967)

    Google Scholar 

  • Bourlond, A.: Cutaneous innervation. J. Invest. Dermatol. 67, 106–109 (1976)

    Google Scholar 

  • Brown, L.G., Gray, J.A.B.: Some effects of nicotine-like substances and their relation to sensory nerve endings. J. Physiol. 107, 306–317 (1948)

    Google Scholar 

  • Burt, A.M., Debart, W-D.: A histochemical study of the distribution of choline acetyl transferease activity in sensory ganglia and nerve roots in the bull frog. Histochem. J. 4, 401–411 (1972)

    Google Scholar 

  • Cauna, N.: The distribution of cholinesterase in the cutaneous receptor organs, especially touch corpuscles of human finger. J. Histochem. Cytochem. 8, 367–375 (1960)

    Google Scholar 

  • Cauna, N.: The free penicillate nerve endings of the human hairy skin. J. Anat. 115, 277–288 (1973)

    Google Scholar 

  • Cunningham, F.O., Fitzgerald, M.J.: Bulbous corpuscles in the hairy skin of laboratory mammals. J. Anat. 111, 345 (1972a)

    Google Scholar 

  • Cunningham, F.D., Fitzgerald, M.J.: Encapsulated nerve endings in hairy skin. J. Anat. 112, 93–97 (1972b)

    Google Scholar 

  • Dimond, R.L., Montagna, W.: Histology and cytochemistry of human skin XXXVI. The nose and lips. Arch. Dermatol. 112, 1235–1244 (1976)

    Google Scholar 

  • Douglas, W.W., Gray, J.A.B.: The excitant action of acetylcholine and other substances on cutaneous sensory pathways and its prevention by hexamethonium and α-Tubocurarine. J. Physiol. 119, 118–128 (1953)

    Google Scholar 

  • Douglas, W.W., Ritchie, J.M.: The excitatory action of acetylcholine on cutaneous non-myelinated fibers. J. Physiol. 150, 501–504 (1960)

    Google Scholar 

  • Edvinsson, L., Nielsen, K.C., Owman, Ch., Sporrong, B.: Cholinergic mechanisms in pial vessels. Histochemistry, electromicroscopy and pharmacology. Z. Zellforsch. 134, 311–325 (1972)

    Google Scholar 

  • Edvinsson, L., Owman, C., Sjöberg, N-O.: Autonomic nerves, mast cells, and amine receptors in human brain vessels. A histochemical and pharmacological study. Brain Res 115, 377–393 (1976)

    Google Scholar 

  • El-Badawi, A., Schenk, E.A.: Histochemical methods for separate, consecutive and simultaneous demonstration of acetylcholinesterase and norepinephrine in cryostat sections. J. Histochem. Cytochem. 15, 580–588 (1967)

    Google Scholar 

  • Ehinger, B., Falck, B.: Noradrenaline and cholinesterases in concomitant nerve fibres in the rat iris. Life Sci 4, 2097–2100 (1965)

    Google Scholar 

  • Ehinger, B., Falck, B.: Concomitant adrenergic and parasympathetic fibres in the rat iris. Acta physiol. Scand. 67, 201–207 (1966)

    Google Scholar 

  • Ellison, J-P., Olander, K.W.: Simultaneous demonstration of catecholamines and acetylcholinesterase in peripheral autonomic nerves. Amer. J. Anat. 135, 23–32 (1972)

    Google Scholar 

  • Eränkö, O.: Distribution of fluorescing islets, adrenalin and noradrenalin in the adrenal nedulla of the hamster. Acta endocrinol. (Kbh) 18, 174–179 (1955)

    Google Scholar 

  • Eränkö, O.: Specific demonstration of acetylcholinesterase and nonspecific cholinesterase in the adrenal gland of the rat. Histochemie 1, 257–267 (1959)

    Google Scholar 

  • Eränkö, O.: Demonstration of catecholamines and cholinesterases in the same section. Pharmacol. Rev. 18, 353–358 (1966)

    Google Scholar 

  • Eränkö, O.: The practical histochemical demonstration of catecholamines by formaldehyde-induced fluorescence. J. roy Microsc. Soc. 87, 259–276 (1967)

    Google Scholar 

  • Eränkö, O., Härkönen, M.: Noradrenaline and acetylcholinesterase in sympathetic ganglion cells of the rat. Acta physiol. Scand. 61, 299–300 (1964)

    Google Scholar 

  • Eränkö, O., Hopsu, V., Räisänen, L.: Changes induced by prolonged administration of nicotine in the distributions of cholinesterases and acid phosphatase in the adrenal medulla of the rat. J. Neurochem. 4, 332–337 (1959)

    Google Scholar 

  • Eränkö, O., Räisänen, L.: Fibers containing both noradrenaline and acetylcholinesterases in the nerve net of the rat iris. Acta physiol. Scand. 63, 505–506 (1965)

    Google Scholar 

  • Falck, B.: Observations on the possibilities of the cellular localization of monoamines by a fluorescence method. Acta physiol. scand. Suppl. 197, 56, 1–25 (1962)

    Google Scholar 

  • Falck, B., Rorsman, H.: Observation on the adrenergic innervation of the skin. Experientia (Basel) 19, 205 (1963)

    Google Scholar 

  • Fitzgerald, G.G., Cooper, J.R.: Acetylcholine as a possible sensory mediator in rabbit corneal epithelium. Biochem. Pharmacol. 20, 2741–48 (1971)

    Google Scholar 

  • Furness, J.B., Costa, M.: The use of glyoxylic acid for the fluorescence histochemical demonstration of peripheral stores of noradrenaline and 5-hydroxytryptamine in whole mounts. Histochemistry 41, 335–352 (1975)

    Google Scholar 

  • Fuxe, K., Nilson, B.Y.: Mechanoreceptors and adrenergic nerve terminal. Experientia (Basel) 21, 641 (1965)

    Google Scholar 

  • Gomori, G.: Enzymes In: Microscopic histochemistry principles and practice, p. 137–221 Chicago: University of Chicago Press 1952

    Google Scholar 

  • Grant, R.T., Baylis, O.B., Adams, C.W.M.: Cholinesterases in peripheral nervous system. II The motor, sensory and sympathetic nerves in the rabbit ear perichondrium and cat cremaster muscle. Brain Res. 6, 457–474 (1967)

    Google Scholar 

  • Gray, J.A.B., Diamond, J.: Pharmacological properties of sensory receptors and their relation to those of the autonomic nervous system. Brit med bull 13, 185–188 (1957)

    Google Scholar 

  • Gruber, H., Zenker, W.: Acetylcholinesterase: histochemical differentiation between motor and sensory nerve fibers. Brain Res. 51, 207–214 (1973)

    Google Scholar 

  • Haegerstam, G., Olgart, L., Edwall, L.: The excitatory action of Acetylcholine on intradental sensory units. Acta physiol. scand. 93, 113–118 (1975)

    Google Scholar 

  • Hebb, C., Hill, K.J.: Distribution of cholinesterases in the mammalian pancreas. Quart. J. exp. Physiol. 40, 168–175 (1955)

    Google Scholar 

  • Hebb, C., Hill, K.J.: Pseudocholinesterase in paccinian corpuscles. Nature (London) 175, 597 (1955)

    Google Scholar 

  • Hellman, K.: Cholinesterase and amine oxidase in the skin. A histochemical investigation. J. Physiol. 129, 454–463 (1955)

    Google Scholar 

  • Hervonen, H., Rechardt, L.: Light and electronmicroscopic demonstration of cholinesterases of the cultured sympathetic ganglia of the chick embryo. Histochemistry 39, 129–142 (1974)

    Google Scholar 

  • Hurley, H.J.: Non-specific cholinesterase in specialized sensory nerve-endings of human genital skin. Brit. J. Dermatol. 70, 284–287 (1958)

    Google Scholar 

  • Hurley, H., Koelle, G.B.: The effect of inhibition of non-specific cholinesterase on perception of tactile sensation in human volar skin. J. Invest. Dermatol. 31, 243–245 (1958)

    Google Scholar 

  • Hökfelt, T., Elde, R., Johansson, O., Luft, R., Arimura, A.: Immunohistochemical evidence for the presence of somatostatin a powerful inhibitory peptide in some primary sensory neurons. Neurosci. Lett. 1, 231–235 (1975a)

    Google Scholar 

  • Hökfelt, T., Kellerth, J.O., Nilsson, G., Pernow, B.: Substance P localization in the central nervous system and in some primary sensory neurons. Science 190, 889–890 (1975b)

    Google Scholar 

  • Hökfelt, T., Elde, R., Johanssson, O., Luft, R., Nilsson, G., Arimura, A.: Immunohistochemical evidence for separate populations of somatostatin-containing and substance P containing primary afferent neurons in the rat. Neuroscience 1, 131–136 (1976)

    Google Scholar 

  • Jacobowitz, D., Koelle, G.B.: Demonstration of both acetylcholinesterase (AChE) and catecholamines in same nerve trunk. Pharmacologist 5, 270 (1963)

    Google Scholar 

  • Jacobowitz, D., Koelle, G.B.: Histochemical correlations of acetylcholinesterase and catecholamines in postganglionic autonomic nerves of the cat, rabbit and guinea pig. J. pharmacol. Exp. Therap. 148, 225–237 (1965)

    Google Scholar 

  • Jenkinson, D., Sengupta, B., Blackburn, P.: The distribution of nerves monoamine oxidase and cholinesterase in the skin of cattle. J. Anat. 100, 593–613 (1966)

    Google Scholar 

  • Jenkinson, D.M., Thompson, G.E., Kenny, J.D., Pearson, J.M.: Histochemical studies on mast cells in cattle skin. Histochem. J. 2, 419–424 (1970)

    Google Scholar 

  • Johnson, J.L.: Glutamic acid as a synaptic transmitter in the nervous system. A review. Brain Res. 37, 1–19 (1972)

    Google Scholar 

  • Johnson, J.L., Aprison, M.H.: The distribution of glutamic acid, a transmitter candidate, and other amino acids in the dorsal sensory neuron of the cat. Brain Res. 24, 285–292 (1970)

    Google Scholar 

  • Karnovsky, M.J., Roots, L.: A “direct-coloring” thiocholine method for cholinesterase. J. Histochem. Cytochem. 12, 219–221 (1964)

    Google Scholar 

  • Koelle, G.B.: The elimination of enzymatic diffusion artifacts in the histochemical localization of cholinesterases and a survey of their cellular distribution. J. Pharmacol. Exp. Ther. 103, 153–171 (1951)

    Google Scholar 

  • Koelle, G.B.: A new general concept of the neurohumoral functions of acetylcholine and acetylcholinesterase. J. Pharmacy Pharmacol. 14, 65–90 (1962)

    Google Scholar 

  • Koelle, G.B., Friedenwald, J.S.: A histochemical method for localizing cholinesterase activity. Proc. Soc. Exp. Biol. Med. 70, 617–622 (1949)

    Google Scholar 

  • Leela, K., Kanagasuntheram, R., Ahmed, M.M.: Innervation of the nasopharynx in macaca fascicularis. J. Anat. 110, 49–56 (1971)

    Google Scholar 

  • Lewis, P.R., Shute, C.C.D.: The distribution of cholinesterase in cholinergic neurons demonstrated with the electron microscope. J. Cell Sci. 1, 381–390 (1966)

    Google Scholar 

  • Lindvall, O., Björklund, A.: The glyoxylic acid fluorescence histochemical method: a detailed account of the methodology for the visualization of central catecholamine neurons. Histochemistry 39, 97–127 (1974)

    Google Scholar 

  • Loewenstein, W.R., Molins, D.: Cholinesterase in a receptor. Science 128, 1284 (1958)

    Google Scholar 

  • Montagna, W., Beckett, E.B.: Cholinesterase and alpha esterase in the lip of the rat. Acta anat. 32, 256–261 (1958)

    Google Scholar 

  • Montagna, W., Ford, D.: Histology and cytochemistry of human skin. The eyelid. Arch Dermatol. 100, 328–335 (1969)

    Google Scholar 

  • Montagna, W., MacPherson, E.: Similarities in cutaneous nerve receptors. Arch. Dermatol. 107, 383–385 (1973)

    Google Scholar 

  • Montagna, W., Parakkal, P.F.: Cutaneous innervation In: the structure and function of skin. Third edition p. 157–171, New York and London: Academic Press 1974

    Google Scholar 

  • Morishima, T.: Histochemical studies on the monoaminergic nerves in the skin chiefly by mans of the fluorescence method of Falck and Hillarp. Acta Dermatovener (Stockholm) 50, 329–337 (1970)

    Google Scholar 

  • Nachmanson, D.: Sequence of energy transformations In: chemical and molecular basis of nerve activity ed. (Nachmanson D) p. 69–99. New York, San Francisco, London: Academic Press 1975)

    Google Scholar 

  • Orfanos, C.E., Mahrle, G.: Ultrastructure and cytochemistry of human cutaneous nerves, with special reference to the ultrastructural localization of specific and nonspecific cholinesterases in human skin. J. Invest. Dermatol. 61, 108–120 (1973)

    Google Scholar 

  • Pospišil, M.: Distribution of acetylcholine esterase in the skin of experimental animals. Collection of scientific works of the faculty of Charles University at Hradel Kralove 2, 274–278 (1959)

    Google Scholar 

  • Rauanheimo, L., Eränkö, O.: Simultaneous histochemical demonstration of acetylcholinesterase and noradrenaline in autonomic nerve fibers. Scand. J. Clin. Lab. Invest. 21, Suppl. 101, 44–45 (1968)

    Google Scholar 

  • Rollinson, D.H., Injidi, M.H.: The distribution of nerves, monoamine oxidase and cholinesterase in the skin of the camel (camelus dromedarius). Res. Vet. Sci 13, 304–5 (1972)

    Google Scholar 

  • Svengaard, N-A., Björklund, A., Stenevi, U.: Regeneration of central cholinergic neurones in the adult rat brain. Brain Res. 102, 1–22 (1976)

    Google Scholar 

  • Tervo, T.: Consecutive demonstration of nerves containing catecholamine and acetylcholinesterase in the rat cornea. Histochemistry 50, 291–299 (1977)

    Google Scholar 

  • Thompson, G.E., Robertshaw, D., Findlay, J.D.: Noradrenergic innervation of the arrectores pilorum muscles of the ox (Bos taurus). Can. J. Physiol. Pharmacol. 47, 310–311 (1969)

    Google Scholar 

  • Tseraidis, G.S., Bavykina, E.A.: Cholinergic innervation of the normal human skin. Vestn. Dermatol. Veneroll. 6, 3 (1973)

    Google Scholar 

  • Uno, H., Montagna, W.: Catecholamine-containing nerve terminals of eccerine sweat glands of macaques. Cell Tissue Res. 158, 1–13 (1975)

    Google Scholar 

  • Walter, P., Hebell, R.: Zur morphologie sensibler receptoren. Anat. Anz. 118, 436–43 (1966)

    Google Scholar 

  • Waris, T., Partanen, S.: Demonstration of catecholamines in peripheral adrenergic nerves in stretch preparations with fluorescence induced by aqueous solution of glyoxylic acid. Histochemistry 41, 369–372 (1975)

    Google Scholar 

  • Waris, T., Korkala, O.: The simultaneous or consecutive demonstration of glyoxylic acid induced fluorescence and acetylcholinesterase reaction in the glomus cells of the carotid body of the rat. Light microscopic study. Histochemistry and Cytochemistry, p. 366–367 (1976) (Proc. V Int. Congress of Histochem. and Cytochem. Bucharest)

  • Waris, T., Rechardt, L.: The demonstration of glyoxylic acid induced fluorescence and cholinesterase reaction in peripheral nerves in the same specimen. Histochemistry and Cytochemistry p. 367 (1976) (Proc. V Int. Congress of Histochem. and Cytochem. Bucharest)

  • Winkelman, R.K., Schmit, R.W.: Cholinesterase in the skin of the rat, dog, cat, guinea pig and rabbit. J. Invest. Dermatol. 33, 185–130 (1959)

    Google Scholar 

  • Yamauchi, A., Lever, J.D.: Formol fluorescence and acetylcholinesterase (AChE) staining in the rat superior cervical ganglion. J. Anat. 109, 340 (1971a)

    Google Scholar 

  • Yamauchi, A., Lever, J.D.: Correlations between formol fluorescence and acetylcholinesterase (AChE) staining in the superior cervical ganglion of normal rat, pig and sheep. J. Anat. 110, 435–443 (1971b)

    Google Scholar 

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Waris, T., Rechardt, L. Histochemically demonstrable catecholamines and cholinesterases in nerve fibres of rat dorsal skin. Histochemistry 53, 203–216 (1977). https://doi.org/10.1007/BF00511076

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