Vet Med - Czech, 2011, 56(11):551-560 | DOI: 10.17221/4274-VETMED

Expression of corticotropin releasing factor (CRF) in the enteric nervous system of the jejunum of sheep

A. Czujkowska, M.B. Arciszewski
Department of Animal Anatomy and Histology, Faculty of Veterinary Medicine, University of Life Sciences, Lublin, Poland

Corticotropin releasing factor (CRF), a 41-amino acid neuropeptide widely distributed in the mammalian central nervous system, has been shown to influence several gastrointestinal functions. Recent studies show that CRF released locally from enteric nerves may also underlie alterations in gut function. In this study, immunohistochemisty was applied to demonstrate the presence of CRF in the jejunum of sheep. Using double immunohistochemical staining the co-localization of CRF with vasoactive intestinal peptide (VIP), galanin, tyrosine hydroxylase (TH), neuropeptide Y (NPY) and substance P (SP) was evaluated. The presence of CRF was detected in myenteric neurons (3.6 ± 0.9%) as well as in submucous neurons (10.5 ± 1.2%). In the ovine jejunum different numbers of CRF-expressing nerve fibres were detected in myenteric ganglia, submucous ganglia, circular smooth muscle layer, lamina muscularis mucosae and between mucosal glands. None of the CRF-positive enteric neurons and CRF-positive nerve fibres exhibited the presence of TH. CRF-immunoreactive (IR) myenteric neurons widely co-expressed VIP and/or NPY. A minor population of CRF-IR myenteric neurons additionally co-stored SP. Galanin was not present in CRF-IR myenteric neurons. The presence of VIP was observed in the vast majority of CRF-positive submucous neurons. Moderate numbers of CRF-IR sumbucous neurons co-expressing galanin or NPY were also found. The presence of SP in CRF-positive submucous neurons was noted only incidentally. In the circular smooth muscle layer CRF-IR/VIP-IR, CRF-IR/NPY-IR as well as CRF-IR/SP-IR nerve fibres were present. In the mucosal layer of the ovine jejunum CRF-IR nerve fibres co-stored additionally VIP, galanin, NPY or SP. This present study provides for the first time evidence that CRF present in different subclasses of enteric neurons may influence certain activities of the ovine jejunum. Co-localization studies indicate that VIP, galanin, SP and NPY functionally co-operate with CRF in the jejunum of the sheep.

Keywords: enteric nervous system; myenteric neurons; submucous neurons; corticotropin releasing factor; jejunum; small intestine; sheep

Published: November 30, 2011  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Czujkowska A, Arciszewski MB. Expression of corticotropin releasing factor (CRF) in the enteric nervous system of the jejunum of sheep. Vet Med - Czech. 2011;56(11):551-560. doi: 10.17221/4274-VETMED.
Download citation

References

  1. Anton PM, Gay J, Mykoniatis A, Pan A, O'Brien M, Brown D, Karalis K, Pothoulakis C (2004): Corticotropin-releasing hormone (CRH) requirement in Clostridium difficile toxin A-mediated intestinal inflammation. Proceedings of the National Academy of Sciences, USA 101, 8503-8598. Go to original source... Go to PubMed...
  2. Bisschops R, Vanden Berghe P, Sarnelli G, Janssens J, Tack J (2006): CRF-induced calcium signaling in guinea pig small intestine myenteric neurons involves CRF-1 receptors and activation of voltage-sensitive calcium channels. American Journal Physiology, 290, G1252-G1260. Go to original source... Go to PubMed...
  3. Brookes SJH (2001): Classes of enteric nerve cells in the guinea-pig small intestine. Anatomical Record 262, 58-70. Go to original source...
  4. Castagliuolo I, Lamont JT, Qiu B, Fleming SM, Bhaskar KR, Nikulasson ST, Kornetsky C, Pothoulakis C (1996): Acute stress causes mucin release from rat colon: role of corticotropin releasing factor and mast cells. American Journal of Physiology 271, G884-G892. Go to original source... Go to PubMed...
  5. Chatzaki E, Crowe PD, Wang L, Million M, Tache Y, Grigoriadis DE (2004): CRF receptor type 1 and 2 expression and anatomical distribution in the rat colon. Journal of Neurochemistry 90, 309-316. Go to original source... Go to PubMed...
  6. Costa M, Brookes SJ, Steele PA, Gibbins I, Burcher E, Kandiah CJ (1996): Neurochemical classification of myenteric neurons in the guinea-pig ileum. Neuroscience 75, 949-967. Go to original source... Go to PubMed...
  7. Cox HM, Cuthbert AW (1990): The effects of neuropeptide Y and its fragments upon basal and electrically stimulated ion secretion in rat jejunum mucosa. British Journal of Pharmacology 101, 247-252. Go to original source... Go to PubMed...
  8. Druge G, Raedler A, Greten H, Lenz HJ (1989): Pathways mediating CRF-induced inhibition of gastric acid secretion in rats. American Journal of Physiology 256, G214-G219. Go to original source... Go to PubMed...
  9. Ekblad E, Hakanson R, Sundler F, Wahlestedt C (1985): Galanin: neuromodulatory and direct contractile effects on smooth muscle preparations. British Journal of Pharmacology 86, 241-246. Go to original source... Go to PubMed...
  10. Furness JB (2000): Types of neurons in the enteric nervous system. Journal of Autonomic Nervous System 81, 87-96. Go to original source... Go to PubMed...
  11. Grigoriadis DE, Lovenberg TW, Chalmers DT, Liaw C, De Souze EB (1996): Characterization of corticotropin-releasing factor receptor subtypes. Annals of the New York Academy of Sciences 780, 60-80. Go to original source... Go to PubMed...
  12. Jingami H, Mizuno N, Takahashi H, Shibahara S, Furutani Y, Imura H, Numa S (1985): Cloning and sequence analysis of cDNA for rat corticotropin-releasing factor precursor. FEBS Letters 191, 63-66. Go to original source... Go to PubMed...
  13. Kawai K, Hotate K, Chiba Y, Munekata E, Ohashi S, Wakabayashi I, Yamashita K (1985): The distribution of corticotrophin-releasing factor immunoreactivity in various ovine tissues. Acta Endocrinologica 108, 433-439. Go to original source... Go to PubMed...
  14. la Fleur SE, Wick EC, Idumalla PS, Grady EF, Bhargava A (2005): Role of peripheral corticotropin-releasing factor and urocortin II in intestinal inflammation and motility in terminal ileum. Proceedings of the National Academy of Sciences, USA 102, 7647-7652. Go to original source... Go to PubMed...
  15. Larauche M, Kiank C, Tache Y (2009): Corticotropin releasing factor signaling in colon and ileum: regulation by stress and pathophysiological implications. Journal of Physiology and Pharmacology 60 (Suppl. 7), 33-46.
  16. Lazar Z, Benko R, Bolcskei K, Rumbus Z, Wolf M, Holzer P, Maggi CA, Bartho L (2003): Actions of endothelin and corticotropin releasing factor in the guinea-pig ileum: no evidence for an interaction with capsaicinsensitive neurons. Neuropeptides 37, 220-232. Go to original source... Go to PubMed...
  17. Lenz HJ, Raedler A, Greten H, Vale WW, Rivier JE (1988): Stress-induced gastrointestinal secretory and motor responses in rats are mediated by endogenous corticotropin-releasing factor. Gastroenterology 95, 1510-1517. Go to original source... Go to PubMed...
  18. Liu S, Gao N, Hu H-Z, Wang X, Wang G-D, Fang X, Gao X, Xia Y, Wood JD (2006): Distribution and chemical coding of corticotropin-releasing factor-immunoreactive neurons in the guinea pig enteric nervous system. Journal of Comparative Neurology 494, 63-74. Go to original source... Go to PubMed...
  19. Martinez V, Tache Y (2001): Role of CRF receptor 1 in central CRF-induced stimulation of colonic propulsion in rats. Brain Research 893, 29-35. Go to original source... Go to PubMed...
  20. Martinez V, Barquist E, Rivier J, Tache Y (1998): Central CRF inhibits gastric emptying of a nutrient solid meal in rats: the role of CRF2 receptors. American Journal of Physiology 274, G965-G970. Go to original source... Go to PubMed...
  21. Martinez V, Rivier J, Tache Y (1999): Peripheral injection of a new corticotropin-releasing factor (CRF) antagonist, astressin, blocks peripheral CRF- and abdominal surgery-induced delayed gastric emptying in rats. Journal of Pharmacology and Experimental Therapeutics 290, 629-634. Go to PubMed...
  22. Mayer EA, Sytnik B, Reddy SN, van Deventer GM, Tache Y (1992): Corticotropin releasing factor (CRF) increases post-prandial duodenal motor activity in humans. Neurogastroenterology and Motility 4, 53-60. Go to original source...
  23. Moga MM, Gray TS (1985): Evidence for corticotropinreleasing factor, neurotensin, and somatostatin in the neural pathway from the central nucleus of the amygdala to the parabrachial nucleus. Journal of Comparative Neurology 241, 275-284. Go to original source... Go to PubMed...
  24. Pammer C, Fodor M, Palkovits M (1988): Localization of corticotropin-releasing factor, somatostatin, and vasoactive intestinal polypeptide in the parabrachial nuclei of the human brain. Journal of Neuroscience Research 20, 109-114. Go to original source... Go to PubMed...
  25. Porcher C, Juhem A, Peinnequin A, Sinniger V, Bonaz B (2005): Expression and effects of metabotropic CRF1 and CRF2 receptors in rat small intestine. American Journal of Physiology 288, G1091-G1103. Go to original source... Go to PubMed...
  26. Sand E, Themner-Persson A, Ekblad E (2011): Corticotropin releasing factor-distribution in rat intestine and role in neuroprotection. Regulatory Peptides 166, 68-75. Go to original source... Go to PubMed...
  27. Sarnyai Z, Shaham Y, Heinrichs SC (2001): The role of corticotropin-releasing factor in drug addiction. Pharmacological Reviews 53, 209-243. Go to PubMed...
  28. Sawchenko PE, Swanson LW, Vale WW (1984): Co-expression of corticotropin-releasing factor and vasopressin immunoreactivity in parvocellular neurosecretory neurons of the adrenalectomized rat. Proceedings of the National Academy of Sciences, USA 81, 1883-1887. Go to original source... Go to PubMed...
  29. Tsukamoto K, Nakade Y, Mantyh C, Ludwig K, Pappas TN, Takahashi T (2006): Peripherally administered CRF stimulates colonic motility via central CRF receptors and vagal pathways in conscious rats. American Journal of Physiology 290, R1537-R1541. Go to original source... Go to PubMed...
  30. Vale W, Spiess J, Rivier C, Rivier J (1981): Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and β-endorphin. Science 213, 1394-1397. Go to original source... Go to PubMed...
  31. Wlk M, Wang C, Venichaki M, Kuhnt-Moore S, Zhao D, Zacks J, Liu J, Karalis K, Pothoulakis C (2001): Corticotropin releasing hormone (CRH) is a proinflammatory peptide in mouse ileum. Gastroenterology 120 (Suppl. 1), A38-A39. Go to original source...
  32. Wolter HJ (1984): Corticotropin-releasing factor is contained within perikarya and nerve fibres of rat duodenum. Biochemical and Biophysical Research Communications 122, 381-387. Go to original source... Go to PubMed...
  33. Wolter HJ (1985): Corticotropin-releasing factor: Immunohistochemical co-localization with adrenocorticotropin and β-endorphin, but not with Met-enkephalin, in subpopulations of duodenal perikarya of rat. Biochemical and Biophysical Research Communications 128, 402-410. Go to original source... Go to PubMed...
  34. Yuan PQ, Million M, Wu SV, Rivier J, Tache Y (2007): Peripheral corticotropin releasing factor (CRF) and a novel CRF1 receptor agonist, stressin1-A activate CRF1 receptor expressing cholinergic and nitrergic myenteric neurons selectively in the colon of conscious rats. Neurogastroenterology and Motility 19, 923-936. Go to original source... Go to PubMed...

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.