P.M. Masliukov a, J.P. Timmermans b, A.A. Zverev c, T.L. Zefirov c
a Yaroslavl State Medical University, Yaroslavl, 150000 Russia
b University of Antwerp, Antwerp, 2000 Belgium
c Kazan Federal University, Kazan, 420008 Russia
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Abstract
Neuropeptide Y (NPY) acts as a neurotransmitter in the autonomic nervous system, including in the metasympathetic intramural ganglia of the intestine. In this study, NPY-positive neurons were detected using immunohistochemical methods in intramural ganglia of the duodenum in the following age groups of rats: newborn pups; 10-, 20-, 30-, and 60-day-old; 1- and 2-year-old rats.
As a result of the immunohistochemical analysis, the NPY-containing neurons were found in small number in the intramural ganglia of the myenteric plexus from the moment of birth and during other periods of life. In ganglia of the submucosal plexus, NPY-immunoreactive neurons were detected in large numbers only starting from day 10 of life. Their proportion did not change until the age of one year and then decreased in the two-year-old rats. The density of Y1R and Y2R receptors increased, while the proportion of Y5R receptors decreased. These changes can be associated with the trophic action of the NPY.
It was concluded that neuropeptide Y is a fairly common neuropeptide in various parts of the autonomic nervous system, including sympathetic, parasympathetic, and metasympathetic, and plays an important role in the processes of age-related neuronal development.
Keywords: neuropeptide Y, receptors, autonomic nervous system, rats, ontogenesis
References
- Nozdrachev A.D., Masliukov P.M. Neuropeptide Y and autonomic nervous system. J. Evol. Biochem. Physiol., 2011, vol. 47, no. 2, pp. 121–130. doi: 10.1134/S0022093011020010.
- Hansel D.E., Eipper B.A., Ronnett G.V. Neuropeptide Y functions as a neuroproliferative factor. Nature, 2001, vol. 410, pp. 940–944. doi: 10.1038/35073601.
- Balasubramaniam A.A. Neuropeptide Y family of hormones: Receptor subtypes and antagonists. Peptides, 1997, vol. 18, no. 3, pp. 445–457. doi: 10.1016/S0196-9781(96)00347-6.
- Michel M.C., Beck-Sickinger A., Cox H., Doods H.N., Herzog H., Larhammar D., Quirion R., Schwartz T., Westfall T. XVI. International Union of Pharmacology recommendations for the nomenclature of neuropeptide Y, peptide YY, and pancreatic polypeptide receptors. Pharmacol. Rev., 1998, vol. 50, no. 1, pp. 143–150.
- Kuo L.E., Kitlinska J.B., Tilan J.U., Li L., Baker S.B., Johnson M.D., Lee E.W., Burnett M.S., Fricke S.T., Kvetnansky R., Herzog H., Zukowska Z. Neuropeptide Y acts directly in the periphery on fat tissue and mediates stress-induced obesity and metabolic syndrome. Nat. Med., 2007, vol. 13, pp. 803–811. doi: 10.1038/nm1611.
- Parker S.L., Balasubramaniam A. Neuropeptide Y Y2 receptor in health and disease. Br. J. Pharmacol., 2008, vol. 153, no. 3, pp. 420–431. doi: 10.1038/sj.bjp.0707445.
- Zhang P., Qi Y.X., Yao Q.P., Chen X.H., Wang G.L., Shen B.R., Han Y., Gao L.Z., Jiang Z.L. Neuropeptide Y stimulates proliferation and migration of vascular smooth muscle cells from pregnancy hypertensive rats via Y1 and Y5 receptors. PLoS One, 2015, vol. 10, no. 7, art. e0131124, pp. 1–13. doi: 10.1371/journal.pone.0131124.
- Zukowska-Grojec Z., Karwatowska-Prokopczuk E., Rose W., Rone J., Movafagh S., Ji H., Yeh Y., Chen W.T., Kleinman H.K., Grouzmann E., Grant D.S. Neuropeptide Y: A novel angiogenic factor from the sympathetic nerves and endothelium. Circ. Res., 1998, vol. 83, no. 2, pp. 187–195. doi: 10.1161/01.res.83.2.187.
- Masliukov P.M., Shilkin V.V., Nozdrachev A.D., Timmermans J.-P. Histochemical features of neurons in the cat stellate ganglion during postnatal ontogenesis. Auton. Neurosci., 2003, vol. 106, no 2, pp. 84–90. doi: 10.1016/S1566-0702(03)00051-1.
- Masliukov P.M., Shilkin V.V., Timmermans J.-P. Immunocytochemical characteristic of neurons of the mouse truncus sympaticus stellate ganglion in postnatal ontogenesis. Morfologiya, 2005, vol. 128, no 5, pp. 41–44. (In Russian)
- Maslyukov P.M., Korzina M.B., Emanuilov A.I., Shilkin V.V. Neurotransmitter composition of neurons in the cranial cervical and celiac sympathetic ganglia in postnatal ontogenesis. Neurosci. Behav. Physiol., 2010, vol. 40, no. 2, pp. 143–147. doi: 10.1007/s11055-009-9247-y.
- Masliukov P.M., Konovalov V.V., Emanuilov A.I., Nozdrachev A.D. Development of neuropeptide Y-containing neurons in sympathetic ganglia of rats. Neuropeptides, 2012, vol. 46, no. 6, pp. 345–352. doi: 10.1016/j.npep.2012.08.003.
- Masliukov P.M., Emanuilov A.I., Moiseev K., Nozdrachev A.D., Dobrotvorskaya S., Timmermans J.P. Development of non-catecholaminergic sympathetic neurons in para- and prevertebral ganglia of cats. Int. J. Dev. Neurosci., 2015, vol. 40, pp. 76–84. doi: 10.1016/j.ijdevneu.2014.12.004.
- Masliukov P.M., Moiseev K., Emanuilov A.I., Anikina T.A., Zverev A.A., Nozdrachev A.D. Development of neuropeptide Y-mediated heart innervation in rats. Neuropeptides, 2016, vol. 55, pp. 47–54. doi: 10.1016/j.npep.2015.10.007.
- Sang Q., Young H.M. Chemical coding of neurons in the myenteric plexus and external muscle of the small and large intestine of the mouse. Cell Tissue Res., 1996, vol. 284, no. 1, pp. 39–53. doi: 10.1007/s004410050565.
- Furness J.B. Types of neurons in the enteric nervous system. J. Auton. Nerv. Syst., 2000, vol. 81, nos. 1–2, pp. 87–96. doi: 10.1016/S0165-1838(00)00127-2.
- Mann P.T., Furness J.B., Southwell B.R. Choline acetyltransferase immunoreactivity of putative intrinsic primary afferent neurons in the rat ileum. Cell Tissue Res., 1999, vol. 297, no. 2, pp. 241–248. doi: 10.1007/s004410051352.
- Kapur R., Yost C., Palmiter R. A transgenic model for studying development of the enteric nervous system in normal and aganglionic mice. Development, 1992, vol. 116, no. 1, pp. 167–175.
- Masliukov P.M., Budnik A.F., Nozdrachev A.D. Neurochemical features of metasympathetic system ganglia in the course of ontogenesis. Adv. Gerontol., 2017, vol. 7, no. 4, pp. 281–289. doi: 10.1134/S2079057017040087.
- Masliukov P.M., Emanuilov A.I., Nozdrachev A.D. Developmental changes of neurotransmitter properties in sympathetic neurons. Adv. Gerontol., 2016, vol. 29, no 3, pp. 442–453.
- Newgreen D.F., Hartley L. Extracellular matrix and adhesive molecules in the early development of the gut and its innervation in normal and spotting lethal rat embryos. Acta Anat. (Basel), 1995, vol. 154, no. 4, pp. 243–260. doi: 10.1159/000147776.
- Young H.M. Functional development of the enteric nervous system-from migration to motility. Neurogastroenterol. Motil., 2008, vol. 20, suppl. 1, pp. 20–31. doi: 10.1111/j.1365-2982.2008.01098.x.
- Ho M.W.Y., Beck-Sickinger A.G., Colmers W.F. Neuropeptide Y5 receptors reduce synaptic excitation in proximal subiculum, but not epileptiform activity in rat hippocampal slices. J. Neurophysiol., 2000, vol. 83, no. 2, pp. 723–734. doi: 10.1152/jn.2000.83.2.723.
- Protas L., Qu J., Robinson R.B. Neuropeptide Y: Neurotransmitter or trophic factor in the heart? News Physiol. Sci., 2003, vol. 18, no. 5, pp. 181–185. doi: 10.1152/nips.01437.2003.
- Movafagh S., Hobson J.P., Spiegel S., Kleinman H.K., Zukowska Z., Neuropeptide Y induces migration, proliferation, and tube formation of endothelial cells bimodally via Y1, Y2, and Y5 receptors. FASEB J., 2006, vol. 20, no. 11, pp. 1924–1926. doi: 10.1096/fj.05-4770fje.
- Pellieux C., Sauthier T., Domenighetti A., Marsh D.J., Palmiter R.D., Brunner H.R., Pedrazzini, T. Neuropeptide Y (NPY) potentiates phenylephrine-induced mitogen-activated protein kinase activation in primary cardiomyocytes via NPY Y5 receptors. Proc. Natl. Acad. Sci. USA, 2000, vol. 97, no. 4, pp. 1595–1600. doi: 10.1073/pnas.030533197.
- Sheriff S., Ali M., Yahya A., Haider K.H., Balasubramaniam A., Amlal H., Neuropeptide Y Y5 receptor promotes cell growth through extracellular signal-regulated kinase signaling and cyclic AMP inhibition in a human breast cancer cell line. Mol. Cancer Res., 2010, vol. 8, no. 4, pp. 604–614. doi: 10.1158/1541-7786.MCR-09-0301.
Received
July 11, 2018
Masliukov Petr Mikhailovich, Doctor of Medical Sciences, Professor, Department of Normal Physiology with Biophysics
Yaroslavl State Medical University
ul. Revolyutsionnaya, 5, Yaroslavl, 150000 Russia
E-mail: mpm@ysmu.ru
Timmermans Jean Pierre, PhD, Professor, Department of Veterinary Sciences
University of Antwerp
St-Jacobsmarkt 9-13, Antwerp, 2000, Belgium
Zverev Aleksei Anatol’evich, Candidate of Biological Sciences, Associate Professor, Department of Human Health Protection
Kazan Federal University
ul. Kremlevskaya, 18, Kazan, 420008 Russia
E-mail: Alekcei5@rambler.ru
Zefirov Timur L’vovich, Doctor of Medical Sciences, Professor, Department of Human Health Protection
Kazan Federal University
ul. Kremlevskaya, 18, Kazan, 420008 Russia
E-mail: zefirovtl@mail.ru
For citation: Masliukov P.M., Timmermans J.P., Zverev A.A., Zefirov T.L. Development of neuropeptide Y-ergic innervation of the small intestine in rats. Uchenye Zapiski Kazanskogo Universiteta. Seriya Estestvennye Nauki, 2018, vol. 160, no. 4, pp. 621–629.
Для цитирования: Masliukov P.M., Timmermans J.P., Zverev A.A., Zefirov T.L. Development of neuropeptide Y-ergic innervation of the small intestine in rats // Учен. зап. Казан. ун-та. Сер. Естеств. науки. – 2018. – Т. 160, кн. 4. – С. 621–629.
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