Summary
The morphological relationship between sensory and sympathetic nerves was studied in tissues of the eye and the oral cavity following chronic sympathetic or sensory denervation. Immunoreactivities for calcitonin gene-related peptide (CGRP) and tyrosine hydroxylase (TH) were used as indexes to assess the changes of the two nerve populations after denervation.
Following surgical sympathectomy, a marked increase of CGRP-containing fibres was seen in all tissues studied, while TH-imunoreactive fibres were totally depleated. Conversely, after capsaicin treatment, an increase of TH-immunoreactive nerves was found in the same tissues, concomitant with a sharp decrease of CGRP-immunoreactive nerves. These changes were particularly evident in iridial stroma and around blood vessels in all tissue, where sensory and sympathetic nerves have a closely overlap** distribution pattern.
The altered proportion of sensory peptide-and catecholamine-containing nerves following sympathetic and sensory denervation suggest that there is a reciprocal trophic influence between the two nerve subsets, possibly with the intervention of neurotrophic substances such as nerve growth factor. These results indicate a close interaction between sensory peptidergic and sympathetic nervous systems in peripheral organs.
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Björklund H, Hökfelt T, Goldstein H, Terenius L, Olson L (1985) Appearance of the noradrenergic markers tyrosine-hydroxylase and neuropeptide Y in cholinergic nerves of the iris following sympathectomy. J Neurosci 5:1633–1643
Bynke G, Brunn A, Håkanson R (1985) Sympathectomy enhances the substance P mediated breakdown of the blood-aqueous barrier in response to infrared irradiation of the rabbit iris. Experientia 41:488–489
Calissano P, Cattaneo A, Biocca S, Aloe L, Mercanti D, Levi-Montalcini R (1984) The nerve growth factor—Established findings and controversial aspects. Exp Cell Res 154:1–9
Carvalho TL, Hodson NP, Blank MA, Natson PF, Mulderry PK, Bishop AE, Gu J, Bloom SR, Polak JM (1986) Occurrence, distribution and origin of peptide-containing nerves of the guinea pig and rat male genitalia, and the effects of denervation on sperm characteristics. J Anat (in press)
Cole DF, Bloom SR, Burnstock G, Butler JM, McGregor GP, Saffrey MJ, Unger WG, Zhang SQ (1983) Increase in SP-like immunoreactivity in nerve fibres of rabbit iris and ciliary body one to four months following sympathetic denervation. Exp Eye Res 37:191–197
Coons AH, Leduc EH, Connolly JM (1955) Studies on antibody production. 1. A method for the histochemical demonstration of specific antibody and its application to a study of the hyperimmune rabbit. J Exp Med 102:49–59
Davies AM, Thoenen H, Barde YA (1986) Different factors from the central nervous system and periphery regulate the survival of sensory neurons. Nature 319:497–499
Goedert M, Stoeckel K, Otten U (1981) Biological importance of the retrograde axonal transport of nerve growth factor in sensory neurons. Proc Natl Acad Sci USA 79:5895–5898
Jänig W, Kollmann W (1984) The involvement of the sympathetic nervous system in pain—Possible neuronal mechanism. Drug Res 34(II):1066–1073
Jonsson G, Halman H (1982) Substance P counteracts neurotoxin damage on norepinephrine neurons in rat brain during ontogeny. Science 215:75–77
Kanakis SJ, Hill CE, Hendry IA, Wattens DJ (1985) Sympathetic neuronal survival factors change after denervation. Dev Brain Res 20:197–202
Kessler JA, Black IB (1980) Nerve growth factor stimulates the development of substance P in sensory ganglia. Proc Natl Acad Sci USA 76:649–652
Kessler JA, Adler JE, Bohn, MC, Black IB (1981) Substance P in principal sympathetic neurons: regulation by impulse activity. Science 214:335–336
Kessler JA, Bell WO, Black IB (1983A) Substance P levels differ in sympathetic target organ terminals and ganglion perikarya. Brain Res 258:144–146
Kessler JA, Bell WO, Black IB (1983B) Interactions between the sympathetic and sensory innervation of the iris. J Neurosci 3:1301–1307
Lee Y, Takami K, Kawai Y, Girgis S, Hillyard CJ, MacIntyre I, Emson PC, Tohyama M (1985) Distribution of calcitonin gene-related peptide in the rat peripheral nervous system with reference to its coexistence with substance P. Neuroscience 15:1227–1237
Levi-Montalcini R (1977) The nerve growth factor: its mode of action on sensory and sympathetic nerve cells. Harvey Lect 60:217–259
Lindner G, Gross G (1981) The effect of substance P on the regeneration of nerve fibres in vitro. Z Mikosk Anat Forsch 95:390–394
MacMahon SB, Gibson S, Polak JMP (1986) Peptide expression is altered when afferent nerves reinnervate inappropriate tissue. Neurosci Lett (in press)
Magnusson T, Carlsson A, Fisher GH, Chang D, Folkers K (1976) Effect of synthetic substance P on monoaminergic mechanism in brain. J Neurol Transm 38:89–93
Nishimoto T, Ichikawa Hm Wakisaka S, Matsuo S, Yamamoto K, Nakata T, Akai M (1985) Immunohistochemical observation on substance P in regenerating taste buds of the rat. Anat Rec 212:430–436
Otten NV, Goedert M, Mayer N, Lembeck F (1980) Requirement of nerve growth factor for development of substance P containing sensory neurones. Nature 287:158–159
Paravicini U, Stoeckel K, Thoenen H (1975) Biological importance of retrograde axonal transport of nerve growth factor in adrenergic neurons. Brain Res 84:279–291
Rawdon BB, Dockray GJ (1982) Effects of conditional media on extension of substance P-immunoreactive neurites from cultured mouse sensory ganglia. Neurosci Lett 34:159–164
Rodrigo J, Polak JM, Terenghi G, Carvantes C, Ghatei MA, Mulderry PK, Bloom SR (1985) Calcitonin gene-related peptide (CGRP)-immunoreactive sensory and motor nerves of the mammalian palate. Histochemistry 82:67–74
Rush RA (1984) Immunohistochemical localisation of endogenous nerve growth factor. Nature 312:364–367
Schon F, Ghatei M, Allen JM, Mulderry PK, Kelly JS, Bloom SR (1985) The effect of sympathectomy on calcitonin generelated peptide levels in the rat trigeminovascular system. Brain Res 348:197–200
Stone RA, Kuwayama Y, Terenghi G, Polak JM (1986) Calcitonin generelated peptide: occurence in corneal sensory nerves. Exp Eye Res (in press)
Taylor WT, Weber RJ (1951) Functional mammalian anatomy. D Van Nostrand, Toronto
Terenghi G, Polak JM, Probert L, McGregor GP, Ferri GL, Blank MA, Butler JM, Unger WG, Zhang SQ, Cole DF, Bloom SR (1982) Map**, quantitative distribution and origin of substance P and VIP-containing nerves in the uvea of guinea pig eye. Histochemistry 75:399–417
Terenghi G, Polak JM, Ghatei MA, Mulderry PK, Butler JM, Unger WG, Bloom SR (1985) Distribution and origin of calcitonin gene-related peptide (CGRP) immunoreactivity in the sensory innervation of the mammalian eye. J Comp Neurol 233:506–516
Terenghi G, Polak JM, Rodrigo J, Mulderry PK, Bloom SR (1986) Calcitonin gene-related peptide immunoreactive nerves in the tongue, epiglottis and pharynx of the rat: occurence, distribution and origin. Brain Res 365:1–14
Tervo K, Tervo T, Eränko L, Eränko O, Valtonen S, Cuello AC (1982) Effect of sensory and sympathetic denervation on substance P immunoreactivity in nerve fibres of the rabbit eye. Exp Eye Res 34:577–585
Thibault J, Vidal D, Cross F (1981) In vitro translation of mRNA from rat phacochromocytoma tumours, characterisation of tyrosin hydroxylase. Biochem Biophys Res Commun 99:960–968
Tracy GP, Cockett FB (1957) Pain in the lower limb after sympathectomy. Lancet 272:12–14
Trendelenberg U (1966) Mechanisms in supersensitivity and subsensitivity to sympathomimetic amines. Pharmacol Rev 18:629–640
Unger WG (1977) The effect of unilateral sympathectomy on the ocular response of the rabbit eye to laser irradiation of the iris. Trans Ophthalmol Soc UK 97:674–678
Unger WG, Butler JM, Cole DF (1981) Prostaglandin and an increased sensitivity of the sympathectomised rabbit eye to laser irradiation of the iris. Exp Eye Res 32:699–707
Unger WG, Terenghi G, Ghatei MA, Ermis KW, Butler JM, Zhang S-Q, Too HP, Polak JM, Bloom SR (1985) Calcitonin gene-related polypeptide as a mediator of the neurogenic ocular injury response. J Ocular Pharmacol 1:189–199
Zhang SQ, Terenghi G, Unger WG, Ermis KW, Polak JM (1984) Changes in substance P- and neuropeptide Y-immunoreactive fibres in rat and guinea pig irides following unilateral sympathectomy. Exp Eye Res 39:365–372
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Terenghi, G., Zhang, S.Q., Unger, W.G. et al. Morphological changes of sensory CGRP-immunoreactive and sympathetic nerves in peripheral tissues following chronic denervation. Histochemistry 86, 89–95 (1986). https://doi.org/10.1007/BF00492350
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DOI: https://doi.org/10.1007/BF00492350