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Oxytocin is expressed by both intrinsic sensory and secretomotor neurons in the enteric nervous system of guinea pig

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Abstract

Single- and double-immunostaining techniques were used systematically to study the distribution pattern and neurochemical density of oxytocin-immunoreactive (-ir) neurons in the digestive tract of the guinea pig. Oxytocin immunoreactivity was distributed widely in the guinea pig gastrointestinal tract; 3%, 13%, 17%, 15%, and 10% of ganglion neurons were immunoreactive for oxytocin in the myenteric plexuses of the gastric corpus, jejunum, ileum, proximal colon, and distal colon, respectively, and 36%, 40%, 52%, and 56% of ganglion neurons were immunoreactive for oxytocin in the submucosal plexuses of the jejunum, ileum, proximal colon, and distal colon, respectively. In the myenteric plexus, oxytocin was expressed exclusively in the intrinsic enteric afferent neurons, as identified by calbindin 28 K. In the submucosal plexuses, oxytocin was expressed in non-cholinergic secretomotor neurons, as identified by vasoactive intestinal polypeptide. Oxytocin-ir nerve fibers in the inner circular muscle layer possibly arose from the myenteric oxytocin-ir neurons, and oxytocin-ir nerve fibers in the mucosa possibly arose from both the myenteric and submucosal oxytocin-ir neurons. Thus, oxytocin in the digestive tract might be involved in gastrointestinal tract motility mainly via the regulation of the inner circular muscle and the balance of the absorption and secretion of water and electrolytes.

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References

  • Furness JB (2000) Types of neurons in the enteric nervous system. J Auton Nerv Syst 81:87–96

    Article  PubMed  CAS  Google Scholar 

  • Guo W, Sun J, Xu X, Bunstock G, He C, Xiang Z (2009) P2X receptors are differentially expressed on vasopressin- and oxytocin-containing neurons in the supraoptic and paraventricular nuclei of rat hypothalamus. Histochem Cell Biol 131:29–41

    Article  PubMed  CAS  Google Scholar 

  • Hashmonai M, Torem S, Argov S, Barzilai A, Schramek A (1979) Prolonged post-vagotomy gastric atony treated by oxytocin. Br J Surg 66:550–551

    Article  PubMed  CAS  Google Scholar 

  • Ju G, Hökfelt T, Brodin E, Fahrenkrug J, Fischer JA, Frey P, Elde RP, Brown JC (1987) Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, galanin-, vasoactive intestinal polypeptide- and cholecystokinin-immunoreactive ganglion cells. Cell Tissue Res 247:417–431

    Article  PubMed  CAS  Google Scholar 

  • Laurent FM, Hindelang C, Klein MJ, Stoeckel ME, Felix JM (1989) Expression of the oxytocin and vasopressin genes in the rat hypothalamus during development: an in situ hybridization study. Brain Res Dev Brain Res 46:145–154

    Article  PubMed  CAS  Google Scholar 

  • Louvel D, Delvaux M, Felez A, Fioramonti J, Bueno L, Lazorthes Y, Frexinos J (1996) Oxytocin increases thresholds of colonic visceral perception in patients with irritable bowel syndrome. Gut 39:741–747

    Article  PubMed  CAS  Google Scholar 

  • Mulderry PK, Ghatei MA, Bishop AE, Allen YS, Polak JM, Bloom SR (1985) Distribution and chromatographic characterisation of CGRP-like immunoreactivity in the brain and gut of the rat. Regul Pept 12:133–143

    Article  PubMed  CAS  Google Scholar 

  • Ohlsson B, Truedsson M, Bengtsson M, Torstenson R, Sjolund K, Bjornsson ES, Simren M (2005) Effects of long-term treatment with oxytocin in chronic constipation; a double blind, placebo-controlled pilot trial. Neurogastroenterol Motil 17:697–704

    Article  PubMed  CAS  Google Scholar 

  • Ohlsson B, Bjorgell O, Ekberg O, Darwiche G (2006a) The oxytocin/vasopressin receptor antagonist atosiban delays the gastric emptying of a semisolid meal compared to saline in human. BMC Gastroenterol 6:11

    Article  PubMed  Google Scholar 

  • Ohlsson B, Truedsson M, Djerf P, Sundler F (2006b) Oxytocin is expressed throughout the human gastrointestinal tract. Regul Pept 135:7–11

    Article  PubMed  CAS  Google Scholar 

  • Petring OU (1989) The effect of oxytocin on basal and pethidine-induced delayed gastric emptying. Br J Clin Pharmacol 28:329–332

    PubMed  CAS  Google Scholar 

  • Rhodes CH, Morrell JI, Pfaff DW (1981) Immunohistochemical analysis of magnocellular elements in rat hypothalamus: distribution and numbers of cells containing neurophysin, oxytocin, and vasopressin. J Comp Neurol 198:45–64

    Article  PubMed  CAS  Google Scholar 

  • Van Nassauw L, Brouns I, Adriaensen D, Burnstock G, Timmermans JP (2002) Neurochemical identification of enteric neurons expressing P2X(3) receptors in the guinea-pig ileum.Histochem Cell Biol 118:193–203

    PubMed  Google Scholar 

  • Welch MG, Tamir H, Gross KJ, Chen J, Anwar M, Gershon MD (2009) Expression and developmental regulation of oxytocin (OT) and oxytocin receptors (OTR) in the enteric nervous system (ENS) and intestinal epithelium. J Comp Neurol 512:256–270

    Article  PubMed  CAS  Google Scholar 

  • Wu CL, Hung CR, Chang FY, Pau KY, Wang JL, Wang PS (2002) Involvement of cholecystokinin receptor in the inhibition of gastric emptying by oxytocin in male rats. Pflugers Arch 445:187–193

    Article  PubMed  CAS  Google Scholar 

  • Wu CL, Hung CR, Chang FY, Pau KY, Wang PS (2003) Pharmacological effects of oxytocin on gastric emptying and intestinal transit of a non-nutritive liquid meal in female rats. Naunyn Schmiedebergs Arch Pharmacol 367:406–413

    Article  PubMed  CAS  Google Scholar 

  • Xiang Z, He C, Burnstock G (2006) P2X5 receptors are expressed on neurons containing arginine vasopressin and nitric oxide synthase in the rat hypothalamus. Brain Res 1099:56–63

    Article  PubMed  CAS  Google Scholar 

  • Yu Q, Zhao Z, Sun J, Guo W, Fu J, Burnstock G, He C, Xiang Z (2010) Expression of P2X6 receptors in the enteric nervous system of the rat gastrointestinal tract. Histochem Cell Biol 133:177–188

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank Dr. Gillian E. Knight for her excellent editorial assistance.

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Correspondence to Zhenghua Xiang.

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Qiang Yu and Ruihua Ji contributed equally to this work.

This work was supported by the 973 Program (2011CB504401 to Z. Xiang) and the National Natural Science Foundation of PR China (30970918 to Z. Xiang).

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Yu, Q., Ji, R., Gao, X. et al. Oxytocin is expressed by both intrinsic sensory and secretomotor neurons in the enteric nervous system of guinea pig. Cell Tissue Res 344, 227–237 (2011). https://doi.org/10.1007/s00441-011-1155-0

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