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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: mckayd@fhs.mcmaster.ca.
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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

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