Skip to main content
SpringerLink
Log in

Distribution and colocalization of neuropeptide Y- and tyrosine hydroxylase-like immunoreactivity in the guinea-pig heart

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

Summary

The localization and distribution of neuropeptide Y-like immunoreactivity in the guinea-pig heart were studied by use of immunohistochemical methods. A widespread distribution of immunoreactive processes was observed in all regions of the heart. They occur either singly or together with several other immunoreactive processes and are most often aligned parallel to the myocardial bundles. A dense network of processes is present in the region of both the sinuatrial and atrioventricular nodes and single fibers are occasionally observed to be closely associated with nodal ganglion cells. Positive cell bodies were not seen within the heart. All small, medium and large coronary vessels are surrounded by a dense network of immunoreactive processes. A rich innervation at the media-adventitia junction of the aorta, pulmonary trunk, superior and inferior vena cava was also observed. Comparison of adjacent sections stained with antisera directed to avian pancreatic polypeptide, carboxyl-terminal hexapeptide of pancreatic polypeptide or neuropeptide Y demonstrated a very similar immunoreactive pattern, suggesting that these antisera are reacting with the same or a closely related substance. Likewise, the same immunoreactive patterns were observed in adjacent sections incubated in antiserum to neuropeptide Y or tyrosine hydroxylase, and analysis of elution-restained sections demonstrated that the same processes contain both neuropeptide Y- and tyrosine hydroxylase-like immunoreactivity. Neuropeptide Y- and tyrosine hydroxylase-like immunoreactivity was reduced by the same magnitude after treatment with the sympathetic neurotoxin 6-hydroxydopamine, but it was not affected by the primary sensory neurotoxin capsaicin. Furthermore, the pattern of neuropeptide Y- and tyrosine hydroxylase-like immunoreactivity did not match the staining patterns observed with antisera to vasoactive intestinal polypeptide or substance P or with the acetylcholinesterase staining pattern. In conclusion, neuropeptide Y-like immunoreactivity in the heart and great vessels coexists with that for catecholamines and is likely to originate from sympathetic ganglia.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Allen YS, Adrian TE, Allen JM, Tatemoto K, Crow TJ, Bloom SR, Polak JM (1983a) Neuropeptide Y distribution in the rat brain. Science 221:877–879

    Google Scholar 

  • Allen JM, Bircham PMM, Edwards AV, Tatemoto K, Bloom SR (1983b) Neuropeptide Y (NPY) reduces myocardial perfusion and inhibits the force of contraction of the isolated perfused rabbit heart. Regul Pept 6:247–253

    Google Scholar 

  • Coons AH (1958) Fluorescent antibody methods. In: Danielli JF (ed) General Cytochemical Methods pp 399–422

  • Dahlström A, Fuxe K, Mya-Tu M, Zetterstrom BEM (1965) Observations on adrenergic innervation of dog heart. Am J Physiol 209:689–692

    Google Scholar 

  • Delfs SR, Zhu CH, Dichter MA (1984) Coexistence of acetylcholinesterase and somatostatin-immunoreactivity in neurons cultured from rat cerebrum. Science 223:61–63

    Google Scholar 

  • Della NG, Papka RE, Furness JB, Costa M (1983) Vasoactive intestinal peptide-like immunoreactivity in nerves associated with the cardiovascular system of guinea pigs. Neuroscience 3:605–619

    Google Scholar 

  • Edvinsson L, Emson P, McCulloch J, Tatemoto K, Uddman R (1983) Neuropeptide Y: cerebrovascular innervation and vasoactive effects in the cat. Neurosci Lett 43:79–84

    Google Scholar 

  • Ehinger B, Falck B, Persson H, Sporrong B (1968) Adrenergic and cholinesterase-containing neurons of the heart. Histochemie 16:197–205

    Google Scholar 

  • Ekblad E, Edvinsson L, Wahlestedt C, Uddman R, Håkanson R, Sundler F (1984) Neuropeptide Y co-exists and co-operates with noradrenaline in perivascular nerve fibers. Regul Pept 8:225–235

    Google Scholar 

  • Everitt BJ, Hökfelt T, Terenius L, Tatemoto K, Mutt V, Goldstein M (1984) Differential co-existence of neuropeptide Y (NPY)-like immunoreactivity with catecholamines in the central nervous system of the rat. Neuroscience 11:443–462

    Google Scholar 

  • Furness JB, Costa M, Walsh JH (1981) Evidence for and significance of the projection of VIP neurons from the myenteric plexus to the taenia coli in the guinea pig. Gastroenterology 80:1557–1561

    Google Scholar 

  • Furness JB, Costa M, Emson PC, Håkanson R, Moghimzadeh E, Sundler F, Taylor IL, Chance RE (1983) Distribution, pathways and reactions to drug treatment of nerves with neuropeptide Y- and pancreatic polypeptide-like immunoreactivity in the guinea-pig digestive tract. Cell Tissue Res 234:71–92

    Google Scholar 

  • Fuxe K, Agnati LF, Harfstrand A, Zini I, Tatemoto K, Pich EM, Hökfelt T, Mutt V, Terenius L (1983) Central administration of neuropeptide Y induces hypotension, bradypnea and EEG synchronization in the rat. Acta Physiol Scand 118:189–192

    Google Scholar 

  • Gu J, Adrian TE, Tatemoto K, Polak JM, Alien JM, Bloom SR (1983) Neuropeptide tyrosine (NPY) — a major cardiac neuropeptide. Lancet 1:1008–1010

    Google Scholar 

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

    Google Scholar 

  • Hökfelt T, Elfvin LG, Elde R, Schultzberg M, Goldstein M, Luft R (1977b) Occurrence of somatostatin-like immunoreactivity in some peripheral sympathetic noradrenergic neurons. Proc Natl Acad Sci USA 74:3587–3591

    Google Scholar 

  • Hökfelt T, Lundberg JM, Schultzberg M, Johansson O, Ljungdhal Å, Rehfeld J (1980a) Coexistence of peptides and putative transmitters in neurons. In: Costa E, Trabuechi M (eds) Neural peptides and neuronal communication, Raven Press, New York, pp 1–23

    Google Scholar 

  • Hökfelt T, Johansson O, Ljungdahl Å, Lundberg MJ, Schultzberg M (1980b) Peptidergic neurons. Nature (Lond) 284:515–521

    Google Scholar 

  • Hökfelt T, Lundberg JM, Terenius L, Jancso G, Kimmel J (1981) Avian pancreatic polypeptide (APP) immunoreactive neurons in the spinal cord and spinal trigeminal nucleus. Peptides 2:81–87

    Google Scholar 

  • Hökfelt T, Lundberg M, Vincent SR (1982) Coexistence of classical transmitters and peptides in neurons. In: Cuello AC (ed) Cotransmission. MacMillan, London, pp 77–125

    Google Scholar 

  • Hökfelt T, Lundberg JM, Tatemoto K, Mutt V, Terenius L, Polak JM, Bloom SR, Sasek C, Elde R, Goldstein M (1983a) Neuropeptide Y (NPY) and FMRF amide neuropeptide-like immunoreactivities in catecholamine neurons of the rat medulla oblongata. Acta Physiol Scand 117:315–318

    Google Scholar 

  • Hökfelt T, Lundberg JM, Lagercrantz H, Tatemoto K, Mutt V, Lundberg J, Terenius L, Everett BJ, Fuxe K, Agnati L and Goldstein M (1983b) Occurrence of neuropeptide Y (NPY)-like immunoreactivity in catecholamine neurons in the human medulla oblongata. Neurosci Lett 36:217–222

    Google Scholar 

  • Hökfelt T, Everitt BJ, Theodorsson-Norheim E, Goldstein M (1984) Occurrence of neurotensin-like immunoreactivity in subpopulations of hypothalamic, mesencephalic, and medullary catecholamine neurons. J Comp Neurol 222:543–559

    Google Scholar 

  • Hougland MW, Hoover DB (1983) Detection of substance P-like immunoreactivity in nerve fibers in the heart of guinea-pigs but not rats. J Auton Nerv Syst 8:295–301

    Google Scholar 

  • Hunt SP, Emson PC, Gilbert R, Goldstein M, Kimmel JR (1981) Presence of avian pancreatic polypeptide-like immunoreactivity in catecholamine and methionine enkephaline containing neurons within the central nervous system. Neurosci Lett 21:125–130

    Google Scholar 

  • Jacobowitz DM, Olschowka JA (1982) Coexistence of bovine pancreatic polypeptide-like immunoreactivity and catecholamine in neurons of the ventral aminergic pathway of the rat brain. Brain Res Bull 9:391–406

    Google Scholar 

  • Jacobowitz DM, Cooper T, Barner HB (1967) Histochemical and chemical studies of the localization of adrenergic and cholinergic nerves in normal and denervated cat hearts. Circ Res 20:289–298

    Google Scholar 

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

    Google Scholar 

  • Kimmel JR, Hayden LJ, Pollock HG (1975) Isolation and characterization of a new pancreatic polypeptide hormone. J Biol Chem 250:9369–9376

    Google Scholar 

  • Kobayashi S, Kyoshima K, Olschowka JA, Jacobowitz DM (1983a) Vasoactive intestinal polypeptide immunoreactive and cholinergic nerves in the whole mount preparation of the major cerebral arteries of the rat. Histochemistry 79:377–381

    Google Scholar 

  • Kobayashi S, Olschowka JA, Jacobowitz DM (1983b) Bovine pancreatic polypeptide-like immunoreactive nerves in the rat major cerebral arteries. Brain Res Bull 10:373–376

    Google Scholar 

  • Loren I, Alumets J, Hakanson R, Sundler F (1979) Immunoreactive pancreatic polypeptide (PP) occurs in the central and peripheral nervous system: preliminary immunocytochemical observations. Cell Tissue Res 200:179–186

    Google Scholar 

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

    Google Scholar 

  • Lundberg JM, Hökfelt T, Schultzberg M, Uvnas-Wallesten K, Kohler G, 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

    Article  CAS  PubMed  Google Scholar 

  • Lundberg JM, Hökfelt T, Änggard Å, Kimmel J, Goldstein M, Markey K (1980a) Coexistence of an avian pancreatic polypeptide (APP) immunoreactive substance and catecholamines in some peripheral and central neurons. Acta Physiol Scand 110:107–109

    Google Scholar 

  • Lundberg JM, Hökfelt T, Änggard Å, Uvnas-Wallensten K, Brimijoin S, Brodin E, Fahrenkrug J (1980b) Peripheral peptide neurons: distribution, axonal transport and some aspects on possible function. In: Costa E, Trabuechi N (eds) Neural peptides and neuronal communication, Raven Press, New York pp 25–36

    Google Scholar 

  • Lundberg JM, Hedlund B, Änggard Å, Fahrenkrug J, Hökfelt T, Tatemoto K, Bartfai T (1982a) In: Bloom SR, Polak JM, Lindenlaub E (eds) Systemic role of regulatory peptides. Schattauer, Stuttgart, pp 145–168

    Google Scholar 

  • Lundberg JM, Hökfelt T, Änggard Å, Terenius L, Elde R, Markey K, Goldstein M, Kimmel J (1982b) Organizational principles in the peripheral sympathetic nervous system: subdivisions by coexisting peptides (somatostatin-, avian pancreatic polypeptide- and vasoactive intestinal polypeptide-like immunoreactive materials). Proc Natl Acad Sci, USA 79:1303–1307

    Google Scholar 

  • Lundberg JM, Terenius L, Hökfelt T, Martling CR, Tatemoto K, Mutt V, Polak J, Bloom S, Goldstein M (1982c) 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 

  • 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 

  • Olschowka JA, Jacobowitz DM (1983) The coexistence and release of bovine pancreatic polypeptide-like immunoreactivity from noradrenergic superior cervical ganglia neurons. Peptides 4:231–238

    Google Scholar 

  • Olschowka JA, O'Donohue TC, Jacobowitz DM (1981) The distribution of bovine pancreatic polypeptide-like immunoreactive neurons in rat brain. Peptides 2:309–331

    Google Scholar 

  • Papka RE, Furness JB, Della NG, Costa M (1981) Depletion by capsaicin of substance-P immunoreactivity and acetylcholinesterase activity from nerve fibres in the guinea pig heart. Neurosci Lett 27:47–53

    Google Scholar 

  • Reinecke M, Weihe E, Forssmann WG (1980) Substance P-immunoreactive nerve fibers in the heart. Neurosci Lett 20:265–269

    Google Scholar 

  • Stephens JK, Masserano JM, Vulliet PR, Weiner N, Nakane PK (1981) Immunocytochemical localization of tyrosine hydroxylase in rat adrenal medulla by the peroxidase labeled antibody method: effects of enzyme activation on ultrastructural distribution of the enzyme. Brain Res 209:339–354

    Google Scholar 

  • Sternberger LA (1974) Immunocytochemistry. Prentice-Hall, Englewood Cliffs, N.J.

    Google Scholar 

  • Sternini C, Brecha N (1984) Localization and distribution of neuropeptide Y (NPY)-like immunoreactivity in the guinea pig heart. Soc Neurosci Abs 10:430

    Google Scholar 

  • Sundler F, Moghimzadeh E, Hakanson R, Ekelund M, Emson P (1983) Nerve fibers in the gut and pancreas of the rat displaying neuropeptide-Y immunoreactivity. Cell Tissue Res 230:487–493

    Google Scholar 

  • Tatemoto K (1982) Neuropeptide Y: complete amino acid sequence of the brain peptide. Proc Natl Acad Sci, USA 79:5485–5689

    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 

  • Taylor IL, Vaillant CR (1983) Pancreatic polypeptide-like material in nerves and endocrine cells of the rat. Peptides 4:245–253

    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 

  • Vaillant C, Taylor I (1981) Demonstration of carboxyl-terminal PP-like peptides in endocrine cells and nerves. Peptides 2 (suppl. 2):31–35

    Google Scholar 

  • Weihe E, Reinecke M (1981) Peptidergic innervation of the mammalian sinus nodes: vasoactive intestinal polypeptide, neurotensin, substance P. Neurosci Lett 26:283–288

    Google Scholar 

  • Wharton J, Polak JM, McGregor GP, Bishop AE, Bloom SR (1981) The distribution of substance P-like immunoreactive nerves in the guinea pig heart. Neuroscience 6:2193–2204

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Medicine I, University of Bologna, S. Orsola Hospital, Bologna, Italy

    C. Sternini M.D.

  2. Center for Ulcer Research and Education, VA Medical Center, Wadsworth, Los Angeles, California, USA

    C. Sternini M.D. & N. Brecha

  3. Department of Medicine, Brain Research Institute and Jules Stein Eye Institute, UCLA School of Medicine, Los Angeles, California, USA

    N. Brecha

Authors
  1. C. Sternini M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. Brecha
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sternini, C., Brecha, N. Distribution and colocalization of neuropeptide Y- and tyrosine hydroxylase-like immunoreactivity in the guinea-pig heart. Cell Tissue Res. 241, 93–102 (1985). https://doi.org/10.1007/BF00214630

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00214630

Key words

Search

Navigation