Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-26T15:58:44.592Z Has data issue: false hasContentIssue false
  • English
  • Français

Nippostrongylus brasiliensis infection evokes neuronal abnormalities and alterations in neurally regulated electrolyte transport in rat jejunum

Published online by Cambridge University Press:  06 April 2009

S. D. Masson ,
D. M. McKay ,
R. H. Stead ,
A. Agro ,
A. Stanisz  and
M. H. Perdue
S. D. Masson
Affiliation:
Intestinal Disease Research Programme, Department of Pathology, McMaster University, Hamilton, Ontario, CanadaL8N 3Z5
D. M. McKay*
Affiliation:
Intestinal Disease Research Programme, Department of Pathology, McMaster University, Hamilton, Ontario, CanadaL8N 3Z5
R. H. Stead
Affiliation:
Intestinal Disease Research Programme, Department of Pathology, McMaster University, Hamilton, Ontario, CanadaL8N 3Z5
A. Agro
Affiliation:
Intestinal Disease Research Programme, Department of Pathology, McMaster University, Hamilton, Ontario, CanadaL8N 3Z5
A. Stanisz
Affiliation:
Intestinal Disease Research Programme, Department of Pathology, McMaster University, Hamilton, Ontario, CanadaL8N 3Z5
M. H. Perdue
Affiliation:
Intestinal Disease Research Programme, Department of Pathology, McMaster University, Hamilton, Ontario, CanadaL8N 3Z5
*
*Corresponding author. Intestinal Disease Research Programme, HSC-3N5, McMaster University, 1200 Main Street West, Hamilton, Ontario, Canada, L8N 3Z5. Tel: 905 525 9140 (ext. 22585). Fax: 905 522 3454. Email: [email protected].
Get access Rights & Permissions [Opens in a new window]

Summary

Neuronal abnormalities have been described in the intestine of helminth-infected rats. However, the physiological ramifications of these changes have not been determined. Here, we examined epithelial ion secretion, indicated by increases in short-circuit current (Isc), evoked by electrical transmural stimulation (TS) of enteric nerves in Ussing-chambered jejunal tissues from Nippostrongylus brasiliensis-infected rats. Rats were examined at 10 and 35 days post-infection (p.i.); non-infected rats served as controls. TS resulted in significantly reduced ion secretion in jejunum from 10 day p.i. rats compared to controls or jejunum from 35 day p.i. rats. The TS response in tissue from infected rats had, unlike controls, no cholinergic component. Tissues from both non-infected and infected rats were equally responsive to the muscarinic agonist bethanechol, suggesting that the cholinergic defect was neuronal and not an inability of the epithelium to respond to cholinergic stimulation. However, increases in Isc evoked by exogenous substance P (SP) in tissue from rats 10 day p.i. were reduced in magnitude to approximately 25% of control values. Concomitant with these physiological changes, tissue from infected rats contained increased amounts of substance P immunoreactivity and intestinal sections displayed increased numbers of substance P-immunoreactive nerve fibre profiles at both 10 and 35 days p.i. Thus, following N. brasiliensis infection there is a shift in the enteric nervous system away from cholinergic to non-cholinergic regulation, associated with increased amounts of the pro-inflammatory neuropeptide, substance P. We speculate that changes in neuronal structure and function are intimately involved in the co-ordinated multicellular response to intestinal parasitic infection and subsequent gut recovery.

Keywords

Nippostrongylus brasiliensiselectrophysiologycholinergicsubstance Penteric nervous system
Type
Research Article
Information
Parasitology , Volume 113 , Issue 2 , August 1996 , pp. 173 - 182
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alizadeh, H., Castro, G. A. & Weems, W. A. (1987). Intrinsic jejunal propulsion in the guinea pig during parasitism with Trichinella spiralis. Gastroenterology 93, 784–790.CrossRefGoogle ScholarPubMed
Castro, G. A. (1989). Immunophysiology of enteric parasitism. Parasitology Today 5, 11–19.CrossRefGoogle ScholarPubMed
Catterall, W. A. (1980). Neurotoxins that act on voltage-sensitive sodium channels in excitable membranes. Annual Review of Pharmacology and Toxicology 20, 15–43.Google Scholar
Collins, S. M., Blennerhassett, P. A., Blennerhassett, M. G. & Vermellion, D. L. (1989). Impaired acetylcholine release from the myenteric plexus of Trichinella-infected rats. American Journal of Physiology 257, G898–G903.Google ScholarPubMed
Cooke, H. J. (1994). Neuroimmune signalling in regulation of intestinal ion transport. American Journal of Physiology 266, G167–G178.Google Scholar
cox, F. E. G. & Liew, F. Y. (1992). T cell subsets and cytokines in parasitic infections. Parasitology Today 8, 371–374.CrossRefGoogle ScholarPubMed
Crosthwaite, A. I. P., Huizinga, J. D. & Fox, J-A. E. T. (1990). Jejunal circular muscle motility is decreased in nematode-infected rat. Gastroenterology 98, 59–65.CrossRefGoogle ScholarPubMed
Diaz, A., Ferreira, A. M. & Nieto, A. (1995). Echinococcus granulosus: interactions with host complement in secondary infection in mice. Experimental Parasitology 80, 473–482.Google Scholar
Dusser, D. J., Umeno, E., Graf, P. D., Djokic, T., Borson, D. B. & Nadel, J. A. (1988). Airway neutral endopeptidase-like enzyme modulates tachykinin-induced bronchoconstriction in vivo. Journal of Applied Physiology 65, 2585–2591.CrossRefGoogle ScholarPubMed
Frieling, T., Palmer, J. M., Cooke, H. J. & Wood, J. D. (1994). Neuorimmune communication in the submucous plexus of guinea pig colon after infection with Trichinella spiralis. Gastroenterology 107, 1602–1609.Google Scholar
Goetzl, E. D. & Sreedharan, S. P. (1992). Mediators of communication and adaptation in the neuroendocrine and immune systems. FASEB Journal 6, 2646–2652.Google Scholar
Jodal, M., Wingren, U., Jansson, M., Heidemann, M. & Lundgren, O. (1993). Nerve involvement in fluid transport in the inflamed rat jejunum. Gut 34, 1526–1530.Google Scholar
Kataeva, G., Agro, A. & Stanisz, A. M. (1994). Substance- P-mediated intestinal inflammation: inhibitory effects of CP96.345 and SMS201–995. Neuroimmunomodulation 1, 350–356.CrossRefGoogle Scholar
Lotz, M., Vaughan, J. H. & Carson, D. A. (1988). Effect of neuropeptides on production of inflammatory cytokines by human monocytes. Science 241, 1218–1221.CrossRefGoogle ScholarPubMed
Masella, P. S., Davis, K. A. & Blennerhassett, M. G. (1995). Decreased cholinesterase activity with increased acetylcholine synthesis in inflamed rat intestine: potential for increased cholinergic influence. Gastroenterology 108, A872 (abstract).Google Scholar
Mckay, D. M., Benjamin, M., Baca-Estrada, M., D'inca, R., Croitoru, K. & Perdue, M. H. (1995). Role of T lymphocytes in secretory response to an enteric nematode parasite: studies in athymic rats. Digestive Diseases and Sciences 40, 331–337.CrossRefGoogle Scholar
Mckay, D. M. & Bienenstock, J. (1994). The interaction between mast cells and nerves in the gastrointestinal tract. Immunology Today 15, 533–538.Google Scholar
Mckay, D. M., Bienenstock, J. & Perdue, M. H. (1993). Inhibition of antigen-induced secretion in the rat jejunum by interferon α/β. Regional Immunology 5, 53–59.Google ScholarPubMed
Mckay, D. M., Halton, D. W., Johnston, C. F., Shaw, C., Fairweather, I. & Buchanan, K. D. (1991). Hymenolepis diminuta: changes in the levels of certain intestinal regulatory peptides in infected C57 mice. Experimental Parasitology 73, 15–26.CrossRefGoogle ScholarPubMed
Mckay, D. M., Halton, D. W., Mccaigue, M. D., Johnston, C. F., Fairweather, I. & Shaw, C. (1990). Hymenolepis diminuta: intestinal goblet cell response to infection in C57 mice. Experimental Parasitology 71, 9–20.Google Scholar
Miller, H. R. P., Woodbury, R. G., Huntley, J. F. & Newlands, G. (1983). Systemic release of mucosal mast cell protease in primed rats challenged with Nippostrongylus brasiliensis. Immunology 49, 271–279.Google Scholar
Murray, M., Miller, H. R. P., Sanford, J. & Jarrett, W. F. H. (1971). 5-hydroxytryptamine in intestinal immunological reactions. Its relationship to mast cell activity and worm expulsion in rats infected with Nippostrongylus brasiliensis. International Archives of Allergy 40, 236–247.CrossRefGoogle ScholarPubMed
Nakazawa, M., Yamada, M., Uchikawa, R. & Arizono, N. (1995). Immunocytochemical localization of secretory acetylcholinesterase of the parasitic nematode Nippostrongylus brasiliensis. Cell and Tissue Research 280, 59–64.Google Scholar
Ottawa, C. A. & Stanisz, A. M. (1995). Neural-immune interactions in the intestine: implications for inflammatory bowel disease. In Inflammatory Bowel Disease, 4th Edn, (ed. Kirsner, J. B. & Shorter, R. G.), pp. 281–300, Williams & Wilkins, London.Google Scholar
Perdue, M. H. & Davison, J. S. (1986). Response of jejunal mucosa to electrical transmural stimulation and two neurotoxins. American Journal of Physiology 251, G642–G648.Google ScholarPubMed
Perdue, M. H., Ramage, J. K., Budget, D., Marshall, J. & Masson, S. (1989). Intestinal mucosal injury is associated with mast cell activation and leukotriene generation during Nippostrongylus-induced inflammation in the rat. Digestive Diseases and Sciences 34, 724–731.Google Scholar
Perdue, M. H., Marshall, J. S. & Masson, S. (1990). Ion transport abnormalities in inflamed rat jejunum: involvement of mast cells and nerves. Gastroenterology 98, 561–567.CrossRefGoogle ScholarPubMed
Perdue, M. H. & Mckay, D. M. (1994). Integrative immunophysiology in the intestinal mucosa. American Journal of Physiology 267, G151–G165.Google Scholar
Phillips, T. E. (1992). Both crypt and villus intestinal goblet cells secrete mucin in response to cholinergic stimulation. American Journal of Physiology 262, G327–G331.Google ScholarPubMed
Phillips, T. E., Phillips, T. L. & Neutra, M. R. (1987). Macromolecules can pass through occluding junctions of rat ileal epithelia during cholinergic stimulation. Cell and Tissue Research 247, 547–554.Google Scholar
Satoh, Y., Ishikawa, K., Oomori, Y., Takeda, S. & Ono, K. (1992). Bethanechol and the G-protein activator, NaF/AICl3, induce secretory response in Paneth cells of mouse intestine. Cell and Tissue Research 269, 213–220.CrossRefGoogle Scholar
Scicchitano, R., Bienenstock, J. & Stanisz, A. M. (1988). In vivo immunomodulation by the neuropeptide substance P. Immunology 63, 733–735.Google ScholarPubMed
Shanahan, F., Denburg, J. A., Fox, J., Bienenstock, J. & Befus, D. (1985). Mast cell heterogeneity: effects of neuroenteric peptides on histamine release. Journal of Immunology 135, 1331–1337.CrossRefGoogle ScholarPubMed
Stead, R. H., Kosecka-Janiszewska, U., Oestreicher, A. B., Dixon, M. F. & Bienenstock, J. (1991). Remodelling of B-50 (GAP-43)- and NSE-immunoreactive mucosal nerves in the intestine of rats infected with Nippostrongylus brasiliensis. Journal of Neuroscience 11, 3809–3821.CrossRefGoogle ScholarPubMed
Stead, R. H., Tomioka, M., Quinonez, G., Simon, G. T., Felton, S. Y. & Bienenstock, J. (1987). Intestinal mucosal mast cells in normal and nematode-infected rat intestines are in intimate contact with peptidergic nerves. Proceedings of the National Academy of Sciences, USA 84, 2975–2979.CrossRefGoogle ScholarPubMed
Swain, M. G., Agro, A., Blennerhassett, P., Stanisz, A. M. & Collins, S. M. (1992). Increased levels of substance P in the myenteric plexus of Trichinella-infected rats. Gastroenterology 102, 1913–1919.Google Scholar
Swain, M. G., Blennerhassett, P. & Collins, S. M. (1991). Impaired sympathetic nerve function in the inflamed rat intestine. Gastroenterology 100, 675–682.CrossRefGoogle ScholarPubMed
Walling, M. W., Brasitus, T. A. & Kimberg, D. V. (1977). Effects of calcitonin and substance P on the transport of Ca2+, Na+ and Cl− across rat ileum in vitro. Gastroenterology 73, 89–94.Google Scholar
Wang, Y. -Z., Palmer, J. M. & Cooke, H. (1991). Neuroimmune regulation of colonic secretion in guinea pigs. American Journal of Physiology 260, G307–G314.Google Scholar
Watanabe, N., Katakura, K., Kobayashi, A., Okumura, K. & Ovary, Z. (1988). Protective immunity and eosinophilia in IgE-deficient SJA/9 mice infected with Nippostrongylus brasiliensis and Trichinella spiralis. Proceedings of the National Academy of Sciences, USA 85, 4460–4462.Google Scholar
Wood, J. D. (1993). Neuro-immunophysiology of colon function. Pharmacology (Suppl. 1) 47, 7–13.CrossRefGoogle ScholarPubMed