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5-Hydroxytryptophan activates colonic myenteric neurons and propulsive motor function through 5-HT₄ receptors in conscious mice

¹Center for Ulcer Research and Education: Digestive Diseases Research Center and Center for Neurovisceral Sciences and Woman's Health, Division of Digestive Diseases, Department of Medicine, David Geffen School of Medicine, University of California Los Angeles, and ²Veterans Affairs Greater Los Angeles Healthcare System, Los Angeles, California; ³Molecular Neuroscience Research Center, Shiga University Medical Science, Otsu, Japan

Submitted 30 June 2006 ; accepted in final form 16 September 2006

ABSTRACT

Serotonin [5-hydroxytryptamine (5-HT)] acts as a modulator of colonic motility and secretion. We characterized the action of the 5-HT precursor 5-hydroxytryptophan (5-HTP) on colonic myenteric neurons and propulsive motor activity in conscious mice. Fos immunoreactivity (IR), used as a marker of neuronal activation, was monitored in longitudinal muscle/myenteric plexus whole mount preparations of the distal colon 90 min after an intraperitoneal injection of 5-HTP. Double staining of Fos IR with peripheral choline acetyltransferase (pChAT) IR or NADPH-diaphorase activity was performed. The injection of 5-HTP (0.5, 1, 5, or 10 mg/kg ip) increased fecal pellet output and fluid content in a dose-related manner, with a peak response observed within the first 15 min postinjection. 5-HTP (0.5–10 mg/kg) dose dependently increased Fos expression in myenteric neurons, with a maximal response of 9.9 ± 1.0 cells/ganglion [P < 0.05 vs. vehicle-treated mice (2.3 ± 0.6 cells/ganglion)]. There was a positive correlation between Fos expression and fecal output. Of Fos-positive ganglionic cells, 40 ± 4% were also pChAT positive and 21 ± 5% were NADPH-diaphorase positive in response to 5-HTP, respectively. 5-HTP-induced defecation and Fos expression were completely prevented by pretreatment with the selective 5-HT₄ antagonist RS-39604. These results show that 5-HTP injected peripherally increases Fos expression in different populations of cholinergic and nitrergic myenteric neurons in the distal colon and stimulates propulsive colonic motor function through 5-HT₄ receptors in conscious mice. These findings suggest an important role of activation of colonic myenteric neurons in the 5-HT₄ receptor-mediated colonic propulsive motor response.

cholinergic neurons; NADPH-diaphorase; peripheral choline acetyltransferase; serotonin; serotonin receptors

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