Vet Med - Czech, 2009, 54(12):589-597 | DOI: 10.17221/66/2009-VETMED

Expression of vasoactive intestinal polypeptide, substance P and neuropeptide Y in jejunal enteric nerves is altered in rabbits suffering from long term Trichinella spiralis infection: an immunohistochemical study

M.B. Arciszewski1, Z. Nowakowski1, K. Wasowicz2, J. Calka2
1 Faculty of Veterinary Medicine, University of Life Sciences, Lublin, Poland
2 Faculty of Veterinary Medicine, Warmia and Mazury University, Olsztyn, Poland

In the early intestinal stage of infection with the nematode Trichinella spiralis alterations in gut motility and chemical code of enteric neurons are observed. The present study was designed to characterize the changes in expression pattern of vasoactive intestinal polypeptide (VIP), substance P (SP) and neuropeptide Y (NPY) in enteric nerves of the rabbit jejunum occurring during long-lasting trichinellosis (35 and 42 days). Sections of the jejunum from healthy and T. spiralis-infected rabbits were processed for double immunocytochemistry in which antibodies against protein gene product 9.5 were used as a pan-neuronal marker and mixed with antisera raised against VIP, SP or NPY. At 35 and 42 days post infection a marked decrease of VIP-, SP- and NPY-immunoreactive (IR) jejunal myenteric neurons was found, whereas the expression of these neuropeptides in submucous neurons was unchanged. In the myenteric plexus and the jejunal circular muscle of T. spiralis-infected rabbits a significant reduction of VIP-IR (but not SP-IR) nerve fibres was noted. In the longitudinal muscle of the jejunum from animals with long-lasting trichinellosis the density of SP-IR nerve terminals was decreased, whereas the number of VIP-containing nerve fibres was unchanged. Long-lasting trichinellosis had no influence on NPY-IR nerve fibres in both circular and longitudinal smooth muscles. The number of NPY-positive (but not VIP- and SP-IR) nerve fibres supplying mucosa and blood vessels was decreased in T. spiralis-infected animals. These data indicate that during long-lasting trichinellosis expression of neuropeptides in jejunal enteric neurons is changed. A possible involvement of VIP and SP in persistent intestinal dysmotility and NPY in altered fluid secretion is discussed.

Keywords: neuropeptides; enteric nervous system; neuronal plasticity; trichinellosis; rabbit

Published: December 31, 2009  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Arciszewski MB, Nowakowski Z, Wasowicz K, Calka J. Expression of vasoactive intestinal polypeptide, substance P and neuropeptide Y in jejunal enteric nerves is altered in rabbits suffering from long term Trichinella spiralis infection: an immunohistochemical study. Vet Med - Czech. 2009;54(12):589-597. doi: 10.17221/66/2009-VETMED.
Download citation

References

  1. Auli M., Nasser Y., Ho W., Burgueno J.F., Keenan C.M., Romero C., Sharkey K.A., Fernandez E. (2008): Neuromuscular changes in a rat model of colitis. Autonomic Neuroscience: Basic and Clinical, 141, 10-21. Go to original source... Go to PubMed...
  2. Barbara G., Vallance B.A., Collins S.M. (1997): Persistent intestinal neuromuscular dysfunction after acute nematode infection in mice. Gastroenterololgy, 113, 1224-1232. Go to original source... Go to PubMed...
  3. Bercik P., Wang L., Verdu E.F., Mao Y.K., Blennerhassett P., Khan W.I., Kean I., Tougas G., Collins S.M. (2004): Visceral hyperalgesia and intestinal dysmotility in a mouse model of postinfective gut dysfunction. Gastroenterology, 127, 179-187. Go to original source... Go to PubMed...
  4. Collins S.M., Blennerhassett P.A., Blennerhassett M.G., Vermillion D.L. (1989): Impaired acetylcholine release from the myenteric plexus of Trichinella-infected rats. American Journal of Physiology - Gastrointestinal and Liver Physiology, 257, 20-26. Go to original source... Go to PubMed...
  5. Costa M., Furness J.B. (1983): The origins, pathways and terminations of neurons with VIP-like immunoreactivity in the guinea-pig small intestine. Neuroscience, 8, 665-676. Go to original source... Go to PubMed...
  6. Davis K.A.M., Masella J., Blennerhassett M.G. (1998): Acetylcholine metabolism in the inflamed rat intestine. Experimental Neurology, 152, 251-258. Go to original source... Go to PubMed...
  7. De Giorgio R., Barbara G., Blennerhassett P., Wang L., Stanghellini V., Corinaldesi R., Collins S.M., Tougas G. (2001): Intestinal inflammation and activation of sensory nerve pathways: A functional and morphological study in the nematode infected rat. Gut, 49, 822-827. Go to original source... Go to PubMed...
  8. Eckert J. (1996): Workshop summary: Food safety: Meatand fish-borne zoonoses. Veterinary Parasitology, 64, 143-147. Go to original source... Go to PubMed...
  9. Ekblad E., Bauer A.J. (2004): Role of vasoactive intestinal peptide and inflammatory mediators in enteric neuronal plasticity. Neurogastroenterology and Motility, 16 (Suppl. 1), 123-128. Go to original source... Go to PubMed...
  10. Farmer S.G. (1981): Propulsive activity of the rat small intestine during infection with the nematode Nippostrongylus brasiliensis. Parasite Immunology, 3, 227-234. Go to original source... Go to PubMed...
  11. Frieling T., Palmer J.M., Cooke H.J., Wood J.D. (1994): Neuroimmune communications in the submucous plexus of guinea pig colon after infection with Trichinella spiralis. Gastroenterology, 107, 1602-1609. Go to original source... Go to PubMed...
  12. Furness J.B. (2000): Types of neurons in the enteric nervous system. Journal of Autonomic Nervous System, 81, 87-96. Go to original source... Go to PubMed...
  13. Goldin E., Karmeli F., Selinger Z., Rachmilewitz D. (1989): Colonic substance P levels are increased in ulcerative colitis and decreased in chronic severe constipation. Digestive Diseases and Sciences, 34, 754-757. Go to original source... Go to PubMed...
  14. Holzer P., Holzer-Petsche U. (1997): Tachykinins in the gut. Part I. Expression, release and motor function. Pharmacology and Therapeutics, 73, 173-217. Go to original source... Go to PubMed...
  15. Hubel K.A., Renquist K.S. (1986): Effect of neuropeptide Y on ion transport by the rabbit ileum. Journal of Pharmacology and Experimental Therapeutics, 238, 167-169.
  16. Jonsson M., Norrgard O., Forsgren S. (2005): Substance P and the neurokinin-1 receptor in relation to eosinophilia in ulcerative colitis. Peptides, 26, 799-814. Go to original source... Go to PubMed...
  17. Keast J.R., Furness J.B., Costa M. (1987): Distribution of peptide-containing neurons and endocrine cells in the rabbit gastrointestinal tract, with particular reference to the mucosa. Cell and Tissue Research, 248, 565-577. Go to original source... Go to PubMed...
  18. Maggi C.A. (1997): The effects of tachykinins on inflammatory and immune cells. Regulatory Peptides, 70, 75-90. Go to original source... Go to PubMed...
  19. Meneghelli U.G. (1985): Chagas' disease: a model of denervation in the study of digestive tract motility. Brazilian Journal of Medical and Biological Research, 18, 155-164.
  20. Palmer J.M., Greenwood B. (1993): Regional content of enteric substance P and vasoactive intestinal peptide during intestinal inflammation in parasitized ferret. Neuropeptides, 25, 95-103. Go to original source... Go to PubMed...
  21. Palmer J.M., Koch T.R. (1995): Altered neuropeptide content and cholinergic enzymatic activity in the inflamed guinea pig jejunum during parasitism. Neuropeptides, 28, 287-297. Go to original source... Go to PubMed...
  22. Palmer J.M., Wong-Riley M., Sharkey K.A. (1998): Functional alterations in jejunal myenteric neurons during inflammation in nematode-infected guinea pigs. American Journal of Physiology - Gastrointestinal and Liver Physiology, 275, G922-G935. Go to original source... Go to PubMed...
  23. Pozo D., Delgado M. (2004): The many faces of VIP in neuroimmunology: a cytokine rather a neuropeptide? The Federation of American Societies for Experimental Biology Journal, 18, 1325-1334. Go to original source... Go to PubMed...
  24. Renzi D., Mantellini P., Calabro A., Panerai C., Amorosi A., Salvador G., Garcea M.R., Surrenti C. (1998): Substance P and vasoactive intestinal polypeptide but not calcitonin gene-related peptide concentrations are reduced in patients with moderate arid severe ulcerative colitis. Italian Journal of Gastroenterology and Hepatology, 30, 62-70.
  25. Serna H., Porras M., Vergara P. (2006): Mast cell stabilizer ketotifen [4-(1-methyl-4-piperidylidene)-4H-benzo[4,5] cyclohepta[1,2-b]thiophen-10(9H)-one fumarate] prevents mucosal mast cell hyperplasia and intestinal dysmotility in experimental Trichinella spiralis inflammation in the rat. Journal of Pharmacology and Experimental Therapeutics, 319, 1104-1111. Go to original source... Go to PubMed...
  26. Sundler F., Moghimzadeh E., Hakanson R. (1983): Nerve fibers in the gut and pancreas of the rat displaying neuropeptide-Y immunoreactivity. Intrinsic and extrinsic origin. Cell and Tissue Research, 230, 487-493. Go to original source... Go to PubMed...
  27. Swain M.G., Blennerhassett P.A., Vermillion D.L. (1991): Impaired sympathetic nerve function in the inflamed rat intestine. Gastroenterology, 100, 675-682. Go to original source... Go to PubMed...
  28. Swain M.G., Agro A., Blennerhassett P., Stanisz A., Collins S.M. (1992): Increased levels of substance P in the myenteric plexus of Trichinella-infected rats. Gastroenterology, 102, 1913-1919. 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.