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Vasoactive intestinal polypeptide and acetylcholine coexist with neuropeptide Y, dopamine-β-hydroxylase, tyrosine hydroxylase, substance P or calcitonin gene-related peptide in neuronal subpopulations in cranial parasympathetic ganglia of rat

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Summary

Immunohistochemistry has been used to demonstrate that neuropeptide Y, dopamine-β-hydroxylase, calcitonin gene-related peptide or substance P are colocalized with vasoactive intestinal polypeptide and choline acetyltransferase in subpopulations of neurons in cranial parasympathetic ganglia of rat. These comprise the ciliary, sphenopalatine, otic, glossopharyngeal-vagal and internal carotid ganglia. In the ciliary and glossopharyngeal-vagal ganglia tyrosine hydroxylase is also found in such neurons. The findings emphasize that the combined localization of dopamine-β-hydroxylase and neuropeptide Y or the presence of tyrosine hydroxylase is not exclusively a marker for peripheral adrenergic neurons. Further, the co-localization of calcitonin gene-related peptide and substance P is not a decisive indication that a neuron is sensory in nature. It is discussed whether the presence of the enzymes and peptides other than vasoactive intestinal polypeptide is a remnant of a different expresion during ontogenesis or indicates target-specific functions in the adult.

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References

  • Al-Haditi AK, Stauber V, Mitchell J (1988) The co-localization of substance P and VIP in cholinergic-type terminals of the rat parotid gland. J Anat 159:83–92

    Google Scholar 

  • Ayer-Le Lievre C, Seiger Å (1985) Substance P-like immunoreactivity in developing cranial parasympathetic neurons of the rat. Int J Dev Neurosci 3:267–277

    Google Scholar 

  • Björklund H, Hökfelt T, Goldstein M, Terenius L, Olson L (1985) Appearance of the noradrenergic markers tyrosine hydroxylase and neuropeptide Y in cholinergie nerves of the iris following sympathectomy. J Neurosci 5:1633–1643

    Google Scholar 

  • Blessing WW, Howe PRC, Joh TH, Oliver JR, Willoughby JO (1986) Distribution of tyrosine hydroxylase and neuropeptide Y-like immunoreactive neurons in rabbit medulla oblongata, with special attention to colocalization studies, presumptive adrenaline-synthesizing perikarya, and vagal preganglionic cells. J Comp Neurol 248:285–300

    Google Scholar 

  • Chang MM, Leeman SE (1970) Isolation of a sialogogic peptide from bovine hypothalamic tissue and its characterization as substance P. J Biol Chem 245:4784–4790

    Google Scholar 

  • Chorobski J, Penfield W (1932) Cerebral vasodilator nerves and their pathway from the medulla oblongata. With observation on the pial and intracerebral vascular plexus. Arch Neurol Psychiatr 28:1257–1289

    Google Scholar 

  • Coons AH, Leduc EH, Connolly JM (1955) Studies on antibody production. I. A method for the histochemical demonstration of specific antibody and its application to a study of the hyperimmune rabbit. J Exp Med 102:49–60

    Google Scholar 

  • Crawford GD, Correa L, Salvaterra PM (1982) Interaction of monoclonal antibodies with mammalian choline acetyltransferase. Proc Natl Acad Sci USA 79:7031–7035

    Google Scholar 

  • Ekblad E, Håkanson R, Sundler F (1984) VIP and PHI coexist with a NPY-like peptide in intramural neurones of the small intestine. Regul Peptides 10:47–55

    Google Scholar 

  • Ekström J, Håkanson R, Månsson B, Tobin G (1988) Tachykinin involvement in parasympathetic nerve-evoked salivation of the ferret. Br J Pharmacol 94:707–712

    Google Scholar 

  • Forsgren S (1989) Vasoactive intestinal polypeptide-like immunoreactivity in the bovine heart: high degree of coexistence with neuropeptide Y-like immunoreactivity. Cell Tissue Res 256:125–135

    Google Scholar 

  • Gibbins IL (1990) Target-related patterns of co-existence of neuropeptide Y, vasoactive intestinal peptide, enkephalin and substance P in cranial parasympathetic neurons innervating the facial skin and exocrine glands of guinea-pigs. Neuroscience 38:541–560

    Google Scholar 

  • Gibbins IL, Morris JL (1987) Co-existence of neuropeptides in sympathetic, cranial autonomic and sensory neurons innervating the iris of the guinea-pig. JAuton Nerv Sys 21:67–82

    Google Scholar 

  • Gibbins IL, Morris JL (1988) Co-existence of immunoreactivity to neuropeptide Y and vasoactive intestinal peptide in nonnoradrenergic axons innervating guinea pig cerebral arteries after sympathectomy. Brain Res 444:402–406

    Google Scholar 

  • Grunditz T, Ekman R, Håkanson R, Sundler F, Uddman R (1988) Neuropeptide Y and vasoactive intestinal peptide coexist in rat thyroid nerve fibers emanating from the thyroid ganglion. Regul Peptides 23:193–208

    Google Scholar 

  • Hardebo JE, Arbab MAR, Suzuki N, Svendgaard NA (1991) Origins and pathways of cerebrovascular parasympathetic and sensory nerves in the monkey. Stroke 22:331–342

    Google Scholar 

  • Helke CJ, Niederer AJ (1990) Studies on the coexistence of substance P with other putative transmitters in the nodose and petrosal ganglia. Synapse 5:144–151

    Google Scholar 

  • Ju G, Hökfelt T, Brodin E, Fahrenkrug J, Fischer JA, Frey P, Elde RP, Brown JC (1987) Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, galanin-, vasoactive intestinal polypeptide- and cholecystokinin-immunoreactive ganglion cells. Cell Tissue Res 247:417–431

    Google Scholar 

  • Katz DM, Markey KA, Goldstein M, Black IB (1983) Expression of catecholaminergic characteristics by primary sensory neurons in the normal adult rat in vivo. Proc Natl Acad Sci USA 80:3526–3530

    Google Scholar 

  • Keen P, Nielsch U, Watts PA (1989) An investigation into the mechanism of induction of vasoactive intestinal peptide gene expression in rat sensory neurones following nerve injury. J Physiol (Lond) 410:62P

    Google Scholar 

  • Lacroix JS, Änggård A, Hökfelt T, O'Hare MMT, Fahrenkrug J, Lundberg JM (1990) Neuropeptide Y: presence in sympathetic and parasympathetic innervation of the nasal mucosa. Cell Tissue Res 259:119–128

    Google Scholar 

  • Landis SC, Keefe D (1983) Evidence for neurotransmitter plasticity in vivo: Developmental changes in properties of cholinergic sympathetic neurons. Dev Biol 98:349–372

    Google Scholar 

  • Leblanc GG, Landis SC (1988) Target specificity of neuropeptide Y-immunoreactive cranial parasympathetic neurons. J Neurosci 8:146–155

    Google Scholar 

  • Leblanc GG, Landis SC (1989) Differentiation of noradrenergic traits in the principal neurons and small intensely fluorescent cells of the parasympathetic sphenopalatine ganglion of the rat. Dev Biol 131:44–59

    Google Scholar 

  • Leblanc GG, Trimmer BA, Landis SC (1987) Neuropeptide Y-like immunoreactivity in rat cranial parasympathetic neurons: coexistence with vasoactive intestinal peptide and choline acetyltransferase. Proc Natl Acad Sci USA 84:3511–3515

    Google Scholar 

  • Lee Y, Takami K, 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

    Google Scholar 

  • Lindh B, Haegerstrand A, Lundberg JM, Hökfelt T, Fahrenkrug J, Cuello AC, Grassi J, Massoulié J (1988) Substance P-, VIP-and CGRP-like immunoreactivities coexist in a population of cholinergic postganglionic sympathetic nerves innervating sweat glands in the cat. Acta Physiol Scand 134:569–570

    Google Scholar 

  • Lindh B, Lundberg JM, Hökfelt T (1989) NPY-, galanin-, VIP/PHI-, CGRP- and substance P-immunoreactive neuronal subpopulations in cat autonomic and sensory ganglia and their projections. Cell Tissue Res 256:259–273

    Google Scholar 

  • Lundberg JM, Terenius L, Hökfelt T, Goldstein M (1983) High levels of neuropeptide Y in peripheral noradrenergic neurons in various mammals including man. Neurosci Lett 42:167–172

    Google Scholar 

  • Lundberg JM, Martling CR, 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. Vol 6: The peripheral nervous system. Elsevier, Amsterdam, pp 391–444

    Google Scholar 

  • Marek KL, Mains RE (1989) Biosynthesis, development, and regulation of neuropeptide Y in superior cervical ganglion culture. J Neurochem 52:1807–1816

    Google Scholar 

  • Mitchell GAG (1953) The cranial extremities of the sympathetic trunks. Acta Anat 18:195–201

    Google Scholar 

  • Morris JL, Gibbins IL (1987) Neuronal colocalization of peptides, catecholamines, and catecholamine-synthesizing enzymes in guinea pig paracervical ganglia. J Neurosci 7:3117–3130

    Google Scholar 

  • Morris JL, Gibbins IL, Furness JB, Costa M, Murphy R (1985) Co-localization of neuropeptide Y, vasoactive intestinal polypeptide and dynorphin in non-noradrenergic axons of the guinea pig uterine artery. Neurosci Lett 62:31–37

    Google Scholar 

  • Morris JL, Gibbins IL, Furness JB (1987) Increased dopamine-β-hydroxylase-like immunoreactivity in non-noradrenergic axons supplying the guinea-pig uterine artery after 6-hydroxydopamine treatment. J Auton Nerv Syst 21:15–27

    Google Scholar 

  • Potter DD, Landis SC, Matsumoto SG, Furshpan EJ (1986) Synaptic functions in rat sympathetic neurons in microculture. II. Adrenergic/cholinergic dual status and plasticity. J Neurosci 6:1080–1098

    Google Scholar 

  • Silverman JD, Kruger L (1989) Calcitonin-gene-related-peptide-immunoreactive innervation of the rat head with emphasis on specialized sensory structures. J Comp Neurol 280:303–330

    Google Scholar 

  • Stjärne P, Lundblad L, Änggård A, Hökfelt T, Lundberg JM (1989) Tachykinins and calcitonin gene-related peptide: coexistence in sensory nerves of the nasal mucosa and effects on blood flow. Cell Tissue Res 256:439–446

    Google Scholar 

  • Stone RA, McGlinn AM, Kuwayama Y, Grimes PA (1988) Peptide immunoreactivity of the ciliary ganglion and its accessory cells in the rat. Brain Res 475:389–392

    Google Scholar 

  • Suzuki N, Hardebo JE (1990) The anatomical basis for a parasympathetic and sensory innervation of the intracranial segment of the internal carotid artery in man. Possible implication for vascular headache. J Neurol Sci 104:19–31

    Google Scholar 

  • Suzuki N, Hardebo JE, Owman C (1988) Origins and pathways of cerebrovascular vasoactive intestinal polypeptide-positive nerves in rat. J Cereb Blood Flow Metab 8:697–712

    Google Scholar 

  • Suzuki N, Hardebo JE, Kåhrström J, Owman C (1990) Neuropeptide Y coexists with vasoactive intestinal polypeptide and acetylcholine in parasympathetic cerebrovascular nerves originating in the sphenopalatine, otic, and internal carotid ganglia of the rat. Neuroscience 36:507–519

    Google Scholar 

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Authors and Affiliations

  1. Department of Medical Cell Research, University of Lund, S-223 62, Lund, Sweden

    J. E. Hardebo, N. Suzuki, E. Ekblad & C. Owman

  2. Department of Neurology, University of Lund, S-223 62, Lund, Sweden

    J. E. Hardebo

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  1. J. E. Hardebo
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  2. N. Suzuki
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  3. E. Ekblad
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  4. C. Owman
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Hardebo, J.E., Suzuki, N., Ekblad, E. et al. Vasoactive intestinal polypeptide and acetylcholine coexist with neuropeptide Y, dopamine-β-hydroxylase, tyrosine hydroxylase, substance P or calcitonin gene-related peptide in neuronal subpopulations in cranial parasympathetic ganglia of rat. Cell Tissue Res 267, 291–300 (1992). https://doi.org/10.1007/BF00302967

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  • DOI: https://doi.org/10.1007/BF00302967

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