Skip to main content
Log in

NPY-, galanin-, VIP/PHI-, CGRP- and substance P-immunoreactive neuronal subpopulations in cat autonomic and sensory ganglia and their projections

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The neuronal subpopulations in the cat stellate, lower lumbar and sacral sympathetic ganglia were studied with regard to the cellular distribution of immunoreactivity to tyrosine hydroxylase (TH), acetylcholinesterase (AChE) and various neuronal peptides. Coexistence of neuropeptide Y (NPY)- and galanin (GAL)-like immunoreactivity (LI) was found in a high proportion of the neuronal cell bodies; these cells also contained immunoreactivity to TH, confirming their presumably noradrenergic nature. Some TH- and GAL-immunoreactive principal ganglion cells lacked NPY-LI. Two populations (scattered and clustered) of vasoactive intestinal polypeptide (VIP)- and peptide histidine isoleucine (PHI)-positive cell bodies were found in the sympathetic ganglia studied. The scattered VIP/PHI neurons also contained AChE-LI, calcitonin gene-related peptide (CGRP)-and, following culture, substance P (SP)-LI. The clustered type only contained AChE-LI. In the submandibular and sphenopalatine ganglia, neurons were AChE- and VIP/ PHI-immunoreactive but lacked CGRP- and SP-LI. Many GAL- and occasional TH-positive neurons were found in these ganglia. In the spinal ganglia, single NPY-immunoreactive sensory neuronal cells were observed, in addition to CGRP- and SP-positive neurons. The present results show that there are at least two populations of sympathetic cholinergic neurons in the cat. Retrograde tracing experiments indicate that the scattered type of cholinergic neurons contains four vasodilator peptides (VIP, PHI, CGRP, SP) and provides an important input to sweat glands, whereas the clustered type (containing VIP and PHI) mainly innervates blood vessels in muscles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Amara SG, Jonas V, Rosenfeld MG, Ong ES, Evans RM (1982) Alternative processing in calcitonin gene expression generates mRNAs encoding different polypeptide products. Nature 198:240–244

    Google Scholar 

  • Bentivoglio M, Kuypers HGJM, Catsman-Berrevoets CE, Loewe H, Dann O (1980) Two new fluorescent retrograde neuronal tracers which are transported over long distances. Neurosci Lett 18:25–30

    Google Scholar 

  • Bohn MC, Kessler JA, Adler JE, Markey K, Goldstein M, Black IB (1984) Simultaneous expression of the SP-peptidergic and noradrenergic phenotypes in rat sympathetic neurons. Brain Res 298:378–381

    Google Scholar 

  • Brain SD, Williams TJ, Tippins JR, Morris HR, MacIntyre I (1985) Calcitonin gene-related peptide is a potent vasodilator. Nature 313:54–56

    Google Scholar 

  • Chang MM, Leeman SE, Niall HD (1971) Amino acid sequence of substance P. Nature New Biol 232:86–87

    Google Scholar 

  • Coons AH (1958) Fluorescent antibody methods. In: Danielli JF (ed) General cytochemical methods. Academic Press, New York, pp 399–422

    Google Scholar 

  • Cuello AC, Galfre G, Milstein C (1979) Detection of substance P in the central nervous system by a monoclonal antibody. Proc Natl Acad Sci USA 76:3532–3536

    Google Scholar 

  • Darvesh S, Nance DM, Hopkins DA, Armour JA (1987) Distribution of neuropeptide like immunoreactivity in intact and chronically decentralized middle cervical and stellate ganglia of dogs. J Auton Nerv Syst 21:167–180

    Google Scholar 

  • Ekblad E, Håkanson R, Sundler F, Wahlstedt C (1985) Galaninneuromodulatory and direct contractile effects on smooth muscle preparations. Br J Pharmacol 86:241–246

    Google Scholar 

  • Fahrenkrug J, Pedersen JH (1984) Development and validation of a specific radioimmunoassay for PHI in plasma. Clin Chim Acta 143:183–192

    Google Scholar 

  • Fahrenkrug J, Schaffalitzky de Muckadell OB (1977) Radioimmunoassay of vasoactive intestinal polypeptide (VIP) in plasma. J Lab Clin Med 89:1379–1388

    Google Scholar 

  • Fisher LA, Kikkava DO, Rivier JE, Amara SG, Evans RM, Rosenfeld MG, Vale WW, Brown MR (1983) Stimulation of noradrenergic sympathetic outflow by calcitonin gene-related peptide. Nature 305:534–536

    Google Scholar 

  • Fisone G, Wu CF, Consolo S, Nordström Ö, Brynne N, Bartfai T, Melander T, Hökfelt T (1987) Galanin inhibits acetylcholine release in the ventral hippocampus of the rat, in vivo and in vitro studies. Proc Natl Acad Sci USA 84:7339–7343

    Google Scholar 

  • Fredricsson B, Sjöqvist F (1962) A cytomorphological study of cholinesterase in sympathetic ganglia of the cat. Acta Morphol Neerl Scand 47:284–296

    Google Scholar 

  • Hamberger B, Norberg K-A, Sjöqvist F (1965) Correlated studies on monoamines and acetylcholinesterase in sympathetic ganglia, illustrating the distribution of adrenergic and cholinergic neurons. In: Koelle GB, Douglas WW, Carlsson A (eds) Pharmacology of cholinergic and adrenergic transmission. Pergamon Press, Oxford, pp 41–54

    Google Scholar 

  • Hartman BK, Zide D, Udenfriend S (1972) The use of dopamine β-hydroxylase as a marker for the noradrenergic pathways of the central nervous system in the rat. Proc Natl Acad Sci USA 69:2722–2726

    Google Scholar 

  • Heym C, Reinecke M, Weihe E, Forssmann WG (1984) Dopamineβ-hiydroxylase-, neurotensin-, substance P-, vasoactive intestinal polypeptide-, and enkephalin-immunohistochemistry of paravertebral and prevertebral ganglia in the cat. Cell Tissue Res 235:411–418

    Google Scholar 

  • Holets VR, Hökfelt T, Rökaeus Å, Terenius L, Goldstein M (1988) Locus coeruleus neurons in the rat containing neuropeptide Y, tyrosine hydroxylase or galanin and their efferent projections to the spinal cord, cerebral cortex and hypothalamus. Neuroscience 24:893–906

    Google Scholar 

  • Holmstedt B, Sjöqvist F (1957) Distribution of acetocholinesterase in various sympathetic ganglia. Acta Physiol Scand 42 [Suppl] 145:72–73

    Google Scholar 

  • Holmstedt B, Sjöqvist F (1959) Distribution of acetocholinesterase in the ganglion cells of various sympathetic ganglia. Acta Physiol Scand 47:284–296

    Google Scholar 

  • Hökfelt T, Kellerth J-O, Nilsson G, Pernow B (1975) Experimental immunohistochemical studies on the localization and distribution of substance P in cat primary sensory neurons. Brain Res 100:235–250

    Google Scholar 

  • Hökfelt T, Elfvin L-G, Schultzberg M, Goldstein M, Nilsson G (1977) On the occurrence of substance P-containing fibers in sympathetic ganglia: immunohistochemical evidence. Brain Res 132:29–41

    Google Scholar 

  • Itoh N, Obata K, Yanaihara N, Okamoto H (1983) Human preprovasoactive intestinal polypeptide contains a novel PHI-27-like peptide, PHM-27. Nature 304:547–549

    Google Scholar 

  • Järhult J, Hellstrand P, Sundler F (1980) Immunohistochemical localization and vascular effects of vasoactive intestinal polypeptide in skeletal muscle of the cat. Cell Tissue Res 207:55–64

    Google Scholar 

  • Kessler JA, Adler J, Bohn M, Black IB (1981) Substance P in sympathetic neurons: regulation by impulse activity. Science 214:335–336

    Google Scholar 

  • Kessler JA, Adler JE, Bell WO, Black IB (1983) Substance P and somatostatin metabolism in sympathetic and special sensory ganglia in vitro. Neuroscience 9:309–318

    Google Scholar 

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

    Google Scholar 

  • Koelle GB (1955) The histochemical identification of acetylcholinesterase in cholinergic, adrenergic and sensory neurons. J Pharmacol Exp Ther 114:167–184

    Google Scholar 

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

    Google Scholar 

  • Kummer W (1987) Galanin- and neuropeptide Y-like immunoreac-tivities coexist in paravertebral sympathetic neurons of the cat. Neurosci Lett 78:127–131

    Google Scholar 

  • Kummer W, Heym C (1988) Neuropeptide distribution in the cervico-thoracic paravertebral ganglia of the cat with particular reference to calcitonin gene-related peptide immunoreactivity. Cell Tissue Res 252:463–471

    Google Scholar 

  • Landis SC, Fredieu JR (1986) Coexistence of calcitonin gene-related peptide and vasoactive intestinal peptide in cholinergic sympathetic innervation of rat sweat glands. Brain Res 377:177–181

    Google Scholar 

  • Lindh B, Lundberg JM, Hökfelt T, Elfvin L-G, Fahrenkrug J, Fischer J (1987) Coexistence of CGRP- and VIP-like immunoreactivities in a population of neurons in the cat stellate ganglia. Acta Physiol Scand 131:475–476

    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 

  • Lundberg JM, Hökfelt T (1986) Multiple co-existence of peptides and classical transmitters in peripheral autonomic and sensory neurones-functional and pharmacological implications. In: Hökfelt T, Fuxe K, Pernow B (eds) Progress in brain research, Vol 68. Elsevier, Amsterdam, pp 241–262

    Google Scholar 

  • Lundberg JM, Tatemoto K (1982) Pancreatic polypeptide family (APP, BPP, NPY and PYY) in relation to α-adrenoceptor-resistant sympathetic vasoconstriction. Acta Physiol Scand 116:393–402

    Google Scholar 

  • Lundberg JM, Hökfelt T, Schultzberg M, Uvnäs-Wallensten K, Köhler C, Said SI (1979) Occurrence of vasoactive intestinal polypeptide (VIP)-like immunoreactivity in certain cholinergic neurons of the cat. Evidence from combined immunohistochemistry and acetylcholinesterase staining. Neuroscience 4:1539–1559

    Google Scholar 

  • Lundberg JM, Änggård A, Fahrenkrug J, Hökfelt T, Mutt V (1980) Vasoactive intestinal polypeptide in cholinergic neurons of exocrine glands: Functional significance of coexisting transmitters for vasodilation and secretion. Proc Natl Acad Sci USA 77:1651–1655

    Google Scholar 

  • Lundberg JM, Änggård A, Fahrenkrug J (1981) Complementary roles of vasoactive intestinal peptide (VIP) and acetylcholine for cat submandibular gland blood flow and secretion. II Effects of cholinergic antagonists and VIP antiserum. Acta Physiol Scand 113:329–336

    Google Scholar 

  • Lundberg JM, Änggård A, Fahrenkrug J (1982a) Complementary role of vasoactive intestinal polypeptide (VIP) and acetylcholine for cat submandibular blood flow and secretion. III Effects of local infusions. Acta Physiol Scand 114:329–338

    Google Scholar 

  • Lundberg JM, Änggård A, Fahrenkrug J, Lundgren C, Holmstedt B (1982b) Co-release of VIP and acetylcholine in relation to blood flow and salivary secretion in cat submandibular salivary gland. Acta Physiol Scand 115:525–528

    Google Scholar 

  • Lundberg JM, Hedlund B, Bartfai T (1982c) Vasoactive intestinal polypeptide (VIP) enhances muscarinic ligand binding in cat submandibular salivary gland. Nature 295:147–149

    Google Scholar 

  • Lundberg JM, Tcrenius L, Hökfelt T, Martling CR, Tatemoto K, Mutt V, Polak J, Bloom SR, Goldstein M (1982d) Neuropcptidc 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 

  • Lundberg JM, Terenius L, Hökfelt T, Tatemoto K (1984) Comparative immunohistochemical and biochemical analysis of pancreatic polypeptide-like peptides with special reference to presence of neuropeptide Y in central and peripheral neurons. J Neurosci 4:2376–2386

    Google Scholar 

  • Markey KA, Kondo S, Shenkman L, Goldstein M (1980) Purification and characterization of tyrosine hydroxylase from a clonal pheochromocytoma cell line. Mol Pharmacol 17:79–85

    Google Scholar 

  • Marsh D, Grassi J, Vigny M, Massoulié J (1984) An immunological study of rat acetylcholinesterase: comparison with acetylcholinesterases from other vertebrates. J Neurochem 43:204–213

    Google Scholar 

  • Melander T, Hökfelt T, Rökaeus Å (1986) Distribution of galaninlike immunoreactivity in the rat central nervous system. J Comp Neurol 248:475–517

    Google Scholar 

  • Melander T, Hökfelt T, Rökaeus Å, Cuello AC, Oertel W, Verhofstad A, Goldstein M (1987) Coexistence of galanin-like immu-noreactivity with catecholamines, 5-hydroxytryptamine, GAB and neuropeptides in the rat CNS. J Neurosci 6:3640–3654

    Google Scholar 

  • Mutt V, Said SI (1974) Structure of the porcine vasoactive intestinal octacosapeptide: The amino-acid sequence. Use of kallikrein in its determination. Eur J Biochem 42:581–589

    Google Scholar 

  • Nordström Ö, Melander T, Hökfelt T, Bartfai T, Goldstein M (1987) Evidence for an inhibitory effect of the peptide galanin on dopamine release from the rat median eminence. Neurosci Lett 73:21–26

    Google Scholar 

  • Ohhashi T, Jacobowitz M (1985) Galanin potentiates electrical stimulation and exogenous norepinephrine-induced contractions in the rat vas deferens. Regul Pept 12:163–171

    Google Scholar 

  • Pernow B(1983) Substance P. Pharmacol Rev 35:85–141

    Google Scholar 

  • Rökaeus Å (1987) Galanin — a newly isolated biologically active neuropeptide. TINS 10:158–164

    Google Scholar 

  • Rosenfeld MG, Mermod JJ, Amara SG, Swanson LW, Sawchenko PE, Rivier J, Vale WW, Evans RM (1983) Production of a novel neuropeptide by the calcitonin gene via tissue-specific RNA processing. Nature 304:129–132

    Google Scholar 

  • Said SI, Mutt V (1970) Polypeptide with broad biological activity. Isolation from small intestine. Science 169:1217–1218

    Google Scholar 

  • Scheibner T, Read DJC, Sullivan CE (1988) Distribution of substance P-immunoreactive structures in the developing cat carotid body. Brain Res 453:72–78

    Google Scholar 

  • Schmitt M, Kummer W, Heym C (1988) Calcitonin gene-related peptide (CGRP)-immunoreactive neurons in the human cervico-thoracic paravertebral ganglia. J Chem Neuroanat 1:287–292

    Google Scholar 

  • Schmued LC, Fallon JH (1986) Fluoro-Gold: a new fluorescent retrograde axonal tracer with numerous unique properties. Brain Res 377:147–154

    Google Scholar 

  • Semenenko FM, Cuello AC, Goldstein M, Lee KY, Sidebottom E (1986) A monoclonal antibody against tyrosine hydroxylase: Application in light and electron microscopy. J Histochem Cytochem 34:817–821

    Google Scholar 

  • Sjöqvist F (1962) Cholinergic sympathetic ganglion cells. M.D. Thesis, Karolinska Institutet, Stockholm

    Google Scholar 

  • Skofitsch G, Jacobowitz DM (1985) Immunohistochemical mapping of galanin-like neurons in the rat central nervous system. Peptides 6:509–546

    Google Scholar 

  • Strömberg I, Björklund H, Melander T, Rökaeus Å, Hökfelt T, Olson L (1987) Galanin-immunoreactive nerves in the rat iris: alterations induced by denervations. Cell Tissue Res 250:267–275

    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 

  • Tatemoto K, Mutt V (1981) Isolation and characterization of the intestinal peptide porcine PHI (PHI-27), a new member of the glucagon-secretin family. Proc Natl Acad Sci USA 78:6603–6607

    Google Scholar 

  • Tatemoto K, Carlquist M, Mutt V (1982) Neuropeptide Y: a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature 296:659–660

    Google Scholar 

  • Tatemoto K, Rökaeus Å, Jörnvall H, McDonald MJ, Mutt V (1983) Galanin — a novel biologically active peptide from porcine intestine. FEBS Lett 164:124–128

    Google Scholar 

  • Tramu G, Pillez A, Leonardelli J (1978) An efficient method of antibody elution for the successive or simultaneous localization of two antigens by immunocytochemistry. J Histochem Cytochem 26:322–324

    Google Scholar 

  • Tschopp FA, Tobler FH, Fischer JA (1984) Calcitonin gene-related peptide in the human thyroid, pituitary and brain. Mol Cell Endocrinol 36:53–57

    Google Scholar 

  • von Euler US, Gaddum JH (1931) An unidentified depressor substance in certain tissue extracts. J Physiol (Lond) 72:74–87

    Google Scholar 

  • Zamboni L, de Martino C (1967) Buffered picric acid formaldehyde: A new rapid fixative for electron microscopy. J Cell Biol 35:148A

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lindh, B., Lundberg, J.M. & Hökfelt, T. 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 (1989). https://doi.org/10.1007/BF00218883

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00218883

Key words

Navigation