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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1987 May;84(10):3511–3515. doi: 10.1073/pnas.84.10.3511

Neuropeptide Y-like immunoreactivity in rat cranial parasympathetic neurons: coexistence with vasoactive intestinal peptide and choline acetyltransferase.

G G Leblanc, B A Trimmer, S C Landis
PMCID: PMC304901  PMID: 3554241

Abstract

Neuropeptide Y (NPY) is widely distributed in the sympathetic nervous system, where it is colocalized with norepinephrine. We report here that NPY-immunoreactive neurons are also abundant in three cranial parasympathetic ganglia, the otic, sphenopalatine, and ciliary, in the rat. High-performance liquid chromatographic analysis of the immunoreactive material present in the otic ganglion indicates that this material is very similar to porcine NPY and indistinguishable from the NPY-like immunoreactivity present in rat sympathetic neurons. These findings raise the possibility that NPY acts as a neuromodulator in the parasympathetic as well as the sympathetic nervous system. In contrast to what has been observed for sympathetic neurons, NPY-immunoreactive neurons in cranial parasympathetic ganglia do not contain detectable catecholamines or tyrosine hydroxylase (EC 1.14.16.2) immunoreactivity, and many do contain immunoreactivity for vasoactive intestinal peptide and/or choline acetyltransferase (EC 2.3.1.6). These findings suggest that there is no simple rule governing coexpression of NPY with norepinephrine, acetylcholine, or vasoactive intestinal peptide in autonomic neurons. Further, while functional studies have indicated that NPY exerts actions on the peripheral vasculature which are antagonistic to those of acetylcholine and vasoactive intestinal peptide, the present results raise the possibility that these three substances may have complementary effects on other target tissues.

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Selected References

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  1. Allen J. M., Adrian T. E., Tatemoto K., Polak J. M., Hughes J., Bloom S. R. Two novel related peptides, neuropeptide Y (NPY) and peptide YY (PYY) inhibit the contraction of the electrically stimulated mouse vas deferens. Neuropeptides. 1982 Dec;3(2):71–77. doi: 10.1016/0143-4179(82)90001-4. [DOI] [PubMed] [Google Scholar]
  2. Bloom S. R., Edwards A. V. Vasoactive intestinal peptide in relation to atropine resistant vasodilatation in the submaxillary gland of the cat. J Physiol. 1980 Mar;300:41–53. doi: 10.1113/jphysiol.1980.sp013150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. De la Torre J. C. An improved approach to histofluorescence using the SPG method for tissue monoamines. J Neurosci Methods. 1980 Oct;3(1):1–5. doi: 10.1016/0165-0270(80)90029-1. [DOI] [PubMed] [Google Scholar]
  4. Eckenstein F., Barde Y. A., Thoenen H. Production of specific antibodies to choline acetyltransferase purified from pig brain. Neuroscience. 1981;6(6):993–1000. doi: 10.1016/0306-4522(81)90065-8. [DOI] [PubMed] [Google Scholar]
  5. Edvinsson L., Emson P., McCulloch J., Tatemoto K., Uddman R. Neuropeptide Y: cerebrovascular innervation and vasomotor effects in the cat. Neurosci Lett. 1983 Dec 23;43(1):79–84. doi: 10.1016/0304-3940(83)90132-5. [DOI] [PubMed] [Google Scholar]
  6. Furness J. B., Costa M., Keast J. R. Choline acetyltransferase- and peptide immunoreactivity of submucous neurons in the small intestine of the guinea-pig. Cell Tissue Res. 1984;237(2):329–336. doi: 10.1007/BF00217152. [DOI] [PubMed] [Google Scholar]
  7. Gu J., Polak J. M., Adrian T. E., Allen J. M., Tatemoto K., Bloom S. R. Neuropeptide tyrosine (NPY)--a major cardiac neuropeptide. Lancet. 1983 May 7;1(8332):1008–1010. doi: 10.1016/s0140-6736(83)92642-9. [DOI] [PubMed] [Google Scholar]
  8. Gu J., Polak J. M., Allen J. M., Huang W. M., Sheppard M. N., Tatemoto K., Bloom S. R. High concentrations of a novel peptide, neuropeptide Y, in the innervation of mouse and rat heart. J Histochem Cytochem. 1984 May;32(5):467–472. doi: 10.1177/32.5.6546942. [DOI] [PubMed] [Google Scholar]
  9. Hassall C. J., Burnstock G. Neuropeptide Y-like immunoreactivity in cultured intrinsic neurones of the heart. Neurosci Lett. 1984 Nov 23;52(1-2):111–115. doi: 10.1016/0304-3940(84)90359-8. [DOI] [PubMed] [Google Scholar]
  10. Jacobowitz D. M., Olschowka J. A. Bovine pancreatic polypeptide-like immunoreactivity in brain and peripheral nervous system: coexistence with catecholaminergic nerves. Peptides. 1982 May-Jun;3(3):569–590. doi: 10.1016/0196-9781(82)90128-0. [DOI] [PubMed] [Google Scholar]
  11. Leblanc G., Landis S. Development of choline acetyltransferase (CAT) in the sympathetic innervation of rat sweat glands. J Neurosci. 1986 Jan;6(1):260–265. doi: 10.1523/JNEUROSCI.06-01-00260.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lundberg J. M., Anggård A., Pernow J., Hökfelt T. Neuropeptide Y-, substance P- and VIP-immunoreactive nerves in cat spleen in relation to autonomic vascular and volume control. Cell Tissue Res. 1985;239(1):9–18. doi: 10.1007/BF00214896. [DOI] [PubMed] [Google Scholar]
  13. Lundberg J. M., Fahrenkrug J., Hökfelt T., Martling C. R., Larsson O., Tatemoto K., Anggård A. Co-existence of peptide HI (PHI) and VIP in nerves regulating blood flow and bronchial smooth muscle tone in various mammals including man. Peptides. 1984 May-Jun;5(3):593–606. doi: 10.1016/0196-9781(84)90090-1. [DOI] [PubMed] [Google Scholar]
  14. Lundberg J. M., Hua X. Y., Franco-Cereceda A. Effects of neuropeptide Y (NPY) on mechanical activity and neurotransmission in the heart, vas deferens and urinary bladder of the guinea-pig. Acta Physiol Scand. 1984 Aug;121(4):325–332. doi: 10.1111/j.1748-1716.1984.tb07463.x. [DOI] [PubMed] [Google Scholar]
  15. Lundberg J. M., Hökfelt T., Anggård A., Terenius L., Elde R., Markey K., Goldstein M., Kimmel J. Organizational principles in the peripheral sympathetic nervous system: subdivision by coexisting peptides (somatostatin-, avian pancreatic polypeptide-, and vasoactive intestinal polypeptide-like immunoreactive materials). Proc Natl Acad Sci U S A. 1982 Feb;79(4):1303–1307. doi: 10.1073/pnas.79.4.1303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lundberg J. M., Hökfelt T., Schultzberg M., Uvnäs-Wallensten K., Köhler C., Said S. I. Occurrence of vasoactive intestinal polypeptide (VIP)-like immunoreactivity in certain cholinergic neurons of the cat: evidence from combined immunohistochemistry and acetylcholinesterase staining. Neuroscience. 1979;4(11):1539–1559. doi: 10.1016/0306-4522(79)90018-6. [DOI] [PubMed] [Google Scholar]
  17. Lundberg J. M., Tatemoto K. Pancreatic polypeptide family (APP, BPP, NPY and PYY) in relation to sympathetic vasoconstriction resistant to alpha-adrenoceptor blockade. Acta Physiol Scand. 1982 Dec;116(4):393–402. doi: 10.1111/j.1748-1716.1982.tb07157.x. [DOI] [PubMed] [Google Scholar]
  18. Lundberg J. M., Terenius L., Hökfelt T., Martling C. R., Tatemoto K., Mutt V., Polak J., Bloom S., Goldstein M. Neuropeptide Y (NPY)-like immunoreactivity in peripheral noradrenergic neurons and effects of NPY on sympathetic function. Acta Physiol Scand. 1982 Dec;116(4):477–480. doi: 10.1111/j.1748-1716.1982.tb07171.x. [DOI] [PubMed] [Google Scholar]
  19. Lundberg J. M., Terenius L., Hökfelt T., Tatemoto K. 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. 1984 Sep;4(9):2376–2386. doi: 10.1523/JNEUROSCI.04-09-02376.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Said S. I., Mutt V. Polypeptide with broad biological activity: isolation from small intestine. Science. 1970 Sep 18;169(3951):1217–1218. doi: 10.1126/science.169.3951.1217. [DOI] [PubMed] [Google Scholar]
  21. Stjernquist M., Emson P., Owman C., Sjöberg N. O., Sundler F., Tatemoto K. Neuropeptide Y in the female reproductive tract of the rat. Distribution of nerve fibres and motor effects. Neurosci Lett. 1983 Sep 9;39(3):279–284. doi: 10.1016/0304-3940(83)90313-0. [DOI] [PubMed] [Google Scholar]
  22. Tatemoto K. Neuropeptide Y: complete amino acid sequence of the brain peptide. Proc Natl Acad Sci U S A. 1982 Sep;79(18):5485–5489. doi: 10.1073/pnas.79.18.5485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Teitelman G., Joh T. H., Grayson L., Park D. H., Reis D. J., Iacovitti L. Cholinergic neurons of the chick ciliary ganglia express adrenergic traits in vivo and in vitro. J Neurosci. 1985 Jan;5(1):29–39. doi: 10.1523/JNEUROSCI.05-01-00029.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Terenghi G., Polak J. M., Allen J. M., Zhang S. Q., Unger W. G., Bloom S. R. Neuropeptide Y-immunoreactive nerves in the uvea of guinea pig and rat. Neurosci Lett. 1983 Nov 21;42(1):33–38. doi: 10.1016/0304-3940(83)90417-2. [DOI] [PubMed] [Google Scholar]
  25. Thibault J., Vidal D., Gros F. In vitro translation of mRNA from rat pheochromocytoma tumors, characterization of tyrosine hydroxylase. Biochem Biophys Res Commun. 1981 Apr 15;99(3):960–968. doi: 10.1016/0006-291x(81)91256-0. [DOI] [PubMed] [Google Scholar]
  26. Uddman R., Fahrenkrug J., Malm L., Alumets J., Håkanson R., Sundler F. Neuronal VIP in salivary glands: distribution and release. Acta Physiol Scand. 1980 Sep;110(1):31–38. doi: 10.1111/j.1748-1716.1980.tb06626.x. [DOI] [PubMed] [Google Scholar]
  27. Uddman R., Malm L., Sundler F. The origin of vasoactive intestinal polypeptide (VIP) nerves in the feline nasal mucosa. Acta Otolaryngol. 1980 Jan-Feb;89(1-2):152–156. doi: 10.3109/00016488009127121. [DOI] [PubMed] [Google Scholar]

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