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1 Department of Mucosal Inflammation and Physiology & Biophysics, University of Calgary, Calgary, AB, Canada; Gastrointestinal Department and Department of Physiology & Biophysics, University of Calgary, Calgary, AB, USA
2 Gastrointestinal Department and Department of Physiology & Biophysics, University of Calgary, Calgary, AB, USA; Neuroscience Research Groups and Department of Physiology & Biophysics, University of Calgary, Calgary, AB, USA
3 Department of Mucosal Inflammation and Physiology & Biophysics, University of Calgary, Calgary, AB, Canada
4 Departments of Anesthesiology and Physiology & Biophysics, University of Washington, Seattle, WA, USA
5 Department of Mucosal Inflammation and Physiology & Biophysics, University of Calgary, Calgary, AB, Canada; Gastrointestinal Department and Department of Physiology & Biophysics, University of Calgary, Calgary, AB, USA; Neuroscience Research Groups and Department of Physiology & Biophysics, University of Calgary, Calgary, AB, USA
* To whom correspondence should be addressed. E-mail: ksharkey{at}ucalgary.ca.
We investigated the distribution and function of cannabinoid (CB)1 receptors in the submucosal plexus of the guinea pig ileum. CB1 receptors were found on both types of submucosal secretomotor neurons, colocalizing with VIP and NPY, the non-cholinergic and cholinergic secretomotor neurons, respectively. CB1 receptors colocalized with TRPV1 receptors on paravascular nerves and fibers in the submucosal plexus. In the submucosal ganglia, these nerves were preferentially localized at the periphery of the ganglia. In denervated ileal segments, CB1 receptor immunoreactivity in submucosal neurons was not modified, but paravascular and intraganglionic fiber staining was absent. Short circuit current (Isc) was measured as an indicator of net electrogenic ion transport in Ussing chambers. In the ion transport studies, Isc responses to capsaicin, which activates extrinsic primary afferents, and to electrical field stimulation (EFS), were reduced by pretreatment with the muscarinic antagonist, atropine; abolished by tetrodotoxin, but were unaffected by VIP receptor desensitization, hexamethonium, AMPA or NMDA glutamate receptor antagonists. The responses to capsaicin and EFS were reduced by 47±12% and 30±14%, respectively, by the CB1 receptor agonist, WIN 55,212-2. This inhibitory effect was blocked by the CB1 receptor antagonist, SR141716A. Isc responses to forskolin or carbachol, which act directly on the epithelium, were not affected by WIN 55,212-2. The inhibitory effect of WIN 55,212-2 on EFS-evoked secretion was not observed in extrinsically denervated segments of ileum. Taken together, these data show cannabinoids act at CB1 receptors on extrinsic primary afferent nerves, inhibiting the release of transmitters that act on cholinergic secretomotor pathways.
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