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In situ hybridization study of neuropeptide Y neurons in the rat brain and pelvic paracervical ganglion

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Abstract

The distribution of mRNA encoding neuropeptide Y in cells of the rat pelvic paracervical ganlion was studied by the use of in situ hybridization with a neuropeptide Y oligodeoxynucleotide probe. The specificity of the hybridization signal was assessed on brain sections and the neurons expressing neuropeptide Y mRNA were actually found in several discrete brain regions already described for containing neuropeptide Y neurons. The present study reports the first demonstration of the presence of neuropeptide Y transcripts in nerve cell bodies and small intensively fluorescent (SIF)-like cells of the pelvic paracervical ganglion, thus providing evidence that neuropeptide Y is synthesized in these two cell types. In addition, a quantitative analysis shows a differential pattern of expression of the peptide mRNA in nerve cell bodies throughout the ganglion.

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References

  • Alm P, Lundberg LM (1988) Co-existence and origin of peptidergic and adrenergic nerves in the guinea pig uterus. Cell Tissue Res 254:517–530

    Google Scholar 

  • Alm P, Lundberg LM, Wharton J, Polak JM (1988) Organization of the guinea-pig uterine innervation. Distribution of immunoreactivities for different neuronal markers. Effects of chemical-and pregnancy-induced sympathectomy. J Histochem 20:290–300

    Google Scholar 

  • Bowden JJ, Gibbins IL (1992) Vasoactive intestinal peptide and neuropeptide Y coexist in non-noradrenergic sympathetic neurons to guinea pig trachea. J Auton Nerv Syst 38:1–20

    Google Scholar 

  • Campbell K, Wictorin K, Björklund A (1992) Differential regulation of neuropeptide mRNA expression in intrastriatal striatal transplants by host dopaminergic afferents. Proc Natl Acad Sci USA 89:10489–10493

    Google Scholar 

  • Chan-Palay V, Yassargil G, Hamid Q, Polak JM, Palay SL (1988) Simultaneous demonstrations of neuropeptide Y gene expression and peptide storage in single neurons of the human brain. Proc Natl Acad Sci USA 85:3213–3215

    Google Scholar 

  • Chronwall BM, Di Maggio DA, Massari VJ, Pickel VM, Ruggiero DA, O'Donohue T (1985) The anatomy of neuropeptide Y-containing neurons in rat brain. Neuroscience 15:1159–1181

    Google Scholar 

  • Dail WG, Dziurzynski R (1985) Substance P immunoreactivity in the major pelvic ganglion of the rat. Anat Rec 212:103–109

    Google Scholar 

  • Dail WG, Manzanares K, Moll MA, Minorsky N (1985) The hypogastric nerve innervates a population of penile neurons in the pelvic plexus. Neuroscience 16:1041–1046

    Google Scholar 

  • De Quidt ME, Emson PC (1986) Distribution of neuropeptide Y-like immunoreactivity in the rat central nervous system. II. Immunohistochemical analysis. Neurosci 3:545–618

    Google Scholar 

  • Fried G, Hökfelt T, Terenius L, Goldstein M (1985) Neuropeptide Y (NPY)-like immunoreactivity in guinea pig uterus is reduced during pregnancy in parallel with noradrenergic nerves. Histochem 83:437–442

    Google Scholar 

  • Garcia-Arraras JE, Lugo-Chinchilla AM, Chévere-Colon I (1992) The expression of neuropeptide Y immunoreactivity in the avian sympathoadrenal system conforms with two models of coexpression development for neurons and chromaffin cells. Development 115:617–627

    Google Scholar 

  • Gehlert DR, Chronwall BM, Schafer MP, O'Donohue TL (1987) Localization of neuropeptide Y messenger ribonucleic acid in rat and mouse brain by in situ hybridization. Synapse 1:25–31

    Google Scholar 

  • Gibbins IL (1992) Vasoconstrictor, vasodilator and pilomotor pathways in sympathetic ganglia of guinea-pigs. Neuroscience 47:657–672

    Google Scholar 

  • Goldstein ME, Tank AW, Fossom LH, Hamill RW (1992) Molecular aspects of the regulation of tyrosine hydroxylase by testosterone. Mol Brain Res 14:79–86

    Google Scholar 

  • Håkanson R, Wahlestedt C, Ekblad E, Edvinsson L, Sundler F (1986) Neuropeptide Y: coexistence with noradrenaline. Functional implications. In: Hökfelt T, Fuxe K, Pernow B (eds) Progress in Brain Research, vol 68. Elsevier, Amsterdam New York Oxford, pp 279–287

    Google Scholar 

  • Hamill RW, Schroeder B (1990) Hormonal regulation of adult sympathetic neurons: the effects of castration on neuropeptide Y, norepinephrine, and tyrosine hydroxylase activity. J Neurobiol 21:731–742

    Google Scholar 

  • Higuchi H, Yang HY, Sabol SL (1988) Rat neuropeptide Y precursor gene expression. J Biol Chem 263:6288–6295

    Google Scholar 

  • Huang WM, Gu J, Blank MA, Allen JM, Bloom SR, Polak JM (1984) Peptide immunoreactive nerves in the mammalian female genital tract. J Histochem 16:1297–1310

    Google Scholar 

  • Inyama CO, Hocker GW, Gu J, Dahl D, Bloom SR, Polak JM (1985) Cytochemical relationships in the paracervical ganglion (Frankenhäuser) of rat studied by immunocytochemistry. Neurosci Lett 55:311–316

    Google Scholar 

  • Järvi R (1989) Localization of bombesin-, neuropeptide Y-, enkephalin- and tyrosine hydroxylase-like immunoreactivities in rat coeliac-superior mesenteric ganglion. Histochem 92:231–236

    Google Scholar 

  • Järvi R, Helen P, Pelto-Huikko M, Hervonen A (1986) Neuropeptide Y (NPY)-like immunoreactivity in rat sympathetic neurons and small granule-containing cells. Neurosci Lett 67:223–227

    Google Scholar 

  • Kanerva L (1971) The postnatal development of monoamines and cholinesterases in the paracervical ganglion of the rat uterus. Prog Brain Res 34:433–444

    Google Scholar 

  • Kanerva L (1972) Ultrastructure of sympathetic ganglion cells and granule-containing cells of the paracervical (Frankenhäuser) ganglion of the newborn rat. Z Zellforsch 126:25–40

    Google Scholar 

  • Kanerva L, Teräväinen H (1972) Electron microscopy of the paracervical (Frankenhäuser) ganglion of the adult rat. Z Zellforsch 129:161–177

    Google Scholar 

  • Kanerva L, Hervonen A (1976) SIF cells, short adrenergic neurons and vacuolated nerve cells of the paracervical (Frankenhäuser) ganglion. In: Eränkö O (ed) SIF Cells. Structure and function of the small intensively fluorescent cells. Fogarty, Washington, pp 19–34

    Google Scholar 

  • Kanerva L, Leitzen R, Teräväinen H (1972) Catecholamines and cholinesterases in the paracervical (Frankenhäuser) ganglion of normal and pregnant rats. Acta Physiol Scand 86:271–277

    Google Scholar 

  • Keast JR (1991) Patterns of co-existence of peptides and differences of nerve fibre types associated with noradrenergic and nonnoradrenergic (putative cholinergic) neurons in the major pelvic ganglion of the male rat. Cell Tissue Res 266:405–415

    Google Scholar 

  • Krukoff TL, Zheng Y (1991) Gene expression of tyrosine hydroxylase and neuropeptide Y in prevertebral ganglia of renal hypertensive rats. Am J Physiol 261:R1455-R1460

    Google Scholar 

  • Kummer W, Addicks K, Henkel H, Heym C (1985) Cholecystokinin-like immunoreactivity in cat extra-adrenal paraganglia. Neurosci Lett 55:207–210

    Google Scholar 

  • Larsen PJ, Jessop DS, Chowdrey HS, Lightman SL (1992) Neuropeptide Y messenger ribonucleic acid in the magnocellular hypothalamo-neurohypophysial system of the rat is increased during osmotic stimulation. Neurosci Lett 138:23–26

    Google Scholar 

  • Lascar G, Taxi J (1991) Synaptic contacts between SIF cells immunoreactive to (CCK-8) in the guinea pig inferior mesenteric ganglion. C R Acad Sci Serie III:77–84

    Google Scholar 

  • Lindefors N, Brené S, Herrera-Marschitz M, Persson H (1990) Neuropeptide gene expression in brain is differentially regulated by midbrain dopamine neurons. Exp Brain Res 80:489–500

    Google Scholar 

  • Lindh B, Pelto-Huikko M, Schalling M, Lundberg JM, Hökfelt T (1989) Substance P mRNA is present in a population of CGRP-immunoreactive cholinergic postganglionic sympathetic neurons of the cat: evidence from combined in situ hybridization and immunohistochemistry. Neurosci Lett 107:1–5

    Google Scholar 

  • Lundberg JM, Terenius L, Hökfelt T, Martling CR, Tatemoto K, Mutt V, Polak J, Bloom S, Goldstein M (1982) Neuropeptide Y (NPY)-like immunoreactivity in peripheral noradrenergic neurons and effects of NPY on sympathetic function. Acta Physiol Scand 116:477–480

    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 

  • Macrae IM, Furness JB, Costa M (1986) Distribution of subgroups of noradrenaline neurons in the coeliac ganglion of the guinea pig. Cell Tissue Res 244:173–180

    Google Scholar 

  • Mattiasson A, Ekblad E, Sundler F, Uvelius B (1985) Origin and distribution of neuropeptide Y-vasoactive intestinal polypeptide- and substance P-containing nerve fibers in the urinary bladder of the rat. Cell Tissue Res 239:141–146

    Google Scholar 

  • McLachlan EM, Llewllyn-Smith IJ (1986) The immunohistochemical distribution of neuropeptide Y in lumbar pre- and paravertebral sympathetic ganglia of the guinea pig. J Auton Nerv Syst 17:313–324

    Google Scholar 

  • Melvin JE, Hamill RW (1986) Gonadal hormone regulation of neurotransmitter synthesizing enzymes in the developing hypogastric ganglion. Brain Res 383:38–46

    Google Scholar 

  • Melvin JE, Hamill RW (1987) The major pelvic ganglion: androgen control of postnatal development. J Neurosci 7:1607–1612

    Google Scholar 

  • Morris BJ (1989) Neuronal localisation of neuropeptide Y gene expression in rat brain. J Comp Neurol 290:358–368

    Google Scholar 

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

    Google Scholar 

  • Normand E, Bloch B (1992) Protocoles pour la détection d'ARNm par hybridation in situ avec les sondes radioactives et biotinylées. In: Calas A, Bloch B, Fournier JG, Trembleau A (eds) Hybridation in situ. Méthodes pratiques. Société Française de Microscopie Electronique, Ivry, pp 21–32

    Google Scholar 

  • Ottesen B, Wagner G, Fahrenkrug J (1988) Peptidergic innervation of the sexual organs. In: Sitsen JMA (ed) Handbook of sexology, vol 6, Elsevier, Amsterdam New York Oxford, pp 66–97

    Google Scholar 

  • Owman C, Stjernquist M (1988) Origin, distribution, and functional aspects of aminergic and peptidergic nerves in the male and female reproductive tracts. In: Björklund A, Hökfelt T, Owman C (eds) Handbook of Chemical Neuroanatomy, vol 6. The Peripheral Nervous System, Elsevier, Amsterdam New York Oxford, pp 445–544

    Google Scholar 

  • Papka RE, Traurig HH, Klenn P (1987) Paracervical ganglia of the female rat: histochemistry and immunochemistry of neurons, SIF cells and nerve terminals. Am J Anat 179:243–257

    Google Scholar 

  • Pieribone VA, Brodin L, Friberg K, Dahlstrand J, Söderberg C, Larhammar D, Hökfelt T (1992) Differential expression of mRNA for neuropeptide Y-related peptides in rat nervous tissues: possible evolutionnary conservation. J Neurosci 12:3361–3371

    Google Scholar 

  • Schalling M, Franco-Cereceda A, Hökfelt T, Persson H, Lundberg JM (1988) Increased neuropeptide Y messenger RNA and peptide in sympathetic ganglia after reserpine pretreatment. Eur J Pharmacol 156:419–420

    Google Scholar 

  • Schalling M, Stieg PE, Lindquist C, Goldstein M, Hökfelt T (1989) Rapid increase in enzyme and peptide mRNA in sympathetic ganglia after electrical stimulation in humans. Proc Natl Acad Sci USA 86:4302–4305

    Google Scholar 

  • Tatemoto K (1982) Neuropeptide Y: complete amino acid sequence of the brain peptide. Proc Natl Acad Sci USA 79:5485–5489

    Google Scholar 

  • Taxi J, Derer M, Domich A (1983) Morphology and histophysiology of SIF cells in the autonomic ganglia. In: Elfvin LG (ed) Autonomic Ganglia. Wiley, New York, pp 67–95

    Google Scholar 

  • Terenghi G, Polak JM, Hamid Q, O'Brien E, Denny P, Legon S, Dixon J, Minth CD, Palay SL, Yasargil G, Chan-Palay V (1987) Localization of neuropeptide Y mRNA in neurons of human cerebral cortex by means of in situ hybridization with a complementary RNA probe. Proc Natl Acad Sci USA 84:7315–7318

    Google Scholar 

  • Williams TH, Jew J (1983) Monoamine connection in sympathetic ganglia. In: Elfvin LG (ed) Autonomic Ganglia. Wiley, New York, pp 235–264

    Google Scholar 

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Authors and Affiliations

  1. Laboratoire de Physiologie de la Reproduction, Groupe Neurophysiologie, CNRS (URA 1449), Université Pierre et Marie Curie, 7 Quai St. Bernard, F-75252, Paris Cedex 05, France

    Eric Houdeau

  2. Institut des Neurosciences CNRS (URA 1488), Dpt. Neurobiologie des Signaux Intercellulaires, Université Pierre et Marie Curie, 7 Quai St. Bernard, F-75252, Paris Cedex 05, France

    Pierre-Alain Boyer

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  1. Eric Houdeau
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Houdeau, E., Boyer, PA. In situ hybridization study of neuropeptide Y neurons in the rat brain and pelvic paracervical ganglion. Cell Tissue Res 277, 579–586 (1994). https://doi.org/10.1007/BF00300232

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  • DOI: https://doi.org/10.1007/BF00300232

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