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NEUROREGULATION AND MOTILITY

Interleukin-1 activates specific populations of enteric neurons and enteric glia in the guinea pig ileum and colon

¹Gastrointestinal and Neuroscience Research Groups, Department of Physiology and Biophysics, University of Calgary, Calgary, Alberta T2N 4N1, Canada; ²Departments of Medical Physiology and Surgery, University Medical Centre, Utrecht, The Netherlands; and ³Department of Gastroenterology, University Medical Centre, Nijmegen, The Netherlands

Submitted 14 February 2003 ; accepted in final form 22 July 2003

Fos expression was used to assess whether the proinflammatory cytokine interleukin-1 (IL-1) activated specific, chemically coded neuronal populations in isolated preparations of guinea pig ileum and colon. Whether the effects of IL-1 were mediated through a prostaglandin pathway and whether IL-1 induced the expression of cyclooxygenase (COX)-2 was also examined. Single- and double-labeling immunohistochemistry was used after treatment of isolated tissues with IL-1 (0.1-10 ng/ml). IL-1 induced Fos expression in enteric neurons and also in enteric glia in the ileum and colon. For enteric neurons, activation was concentration-dependent and sensitive to indomethacin, in both the myenteric and submucosal plexuses in both regions of the gut. The maximum proportion of activated neurons differed between the ileal (15%) and colonic (42%) myenteric and ileal (60%) and colonic (75%) submucosal plexuses. The majority of neurons activated in the myenteric plexus of the ileum expressed nitric oxide synthase (NOS) or enkephalin immunoreactivity. In the colon, activated myenteric neurons expressed NOS. In the submucosal plexus of both regions of the gut, the majority of activated neurons were vasoactive intestinal polypeptide (VIP) immunoreactive. After treatment with IL-1, COX-2 immunoreactivity was detected in the wall of the gut in both neurons and nonneuronal cells. In conclusion, we have found that the proinflammatory cytokine IL-1 specifically activates certain neurochemically defined neural pathways and that these changes may lead to disturbances in motility observed in the inflamed bowel.

myenteric plexus; submucosal plexus; cyclooxygenase-2; vasoactive intestinal polypeptide; nitric oxide synthase

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