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The Journal of Neuroscience, August 5, 2009, 29(31):9683-9699; doi:10.1523/JNEUROSCI.1145-09.2009

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Development/Plasticity/Repair
5-HT₄ Receptor-Mediated Neuroprotection and Neurogenesis in the Enteric Nervous System of Adult Mice

Min-Tsai Liu,¹ Yung-Hui Kuan,⁴ Jingwen Wang,² René Hen,³ and Michael D. Gershon¹

Departments of ¹Pathology and Cell Biology, ²Biological Sciences, and ³Neuroscience, Columbia University, New York, New York 10032, and ⁴Max Planck Institute for Brain Research, 60528 Frankfurt, Germany

Correspondence should be addressed to Min-Tsai Liu, Department of Pathology and Cell Biology, College of Physicians and Surgeons, Columbia University, 630 West 168th Street, Box 23, New York, NY 10032. Email: ml27{at}columbia.edu

Although the mature enteric nervous system (ENS) has been shown to retain stem cells, enteric neurogenesis has not previously been demonstrated in adults. The relative number of enteric neurons in wild-type (WT) mice and those lacking 5-HT₄ receptors [knock-out (KO)] was found to be similar at birth; however, the abundance of ENS neurons increased during the first 4 months after birth in WT but not KO littermates. Enteric neurons subsequently decreased in both WT and KO but at 12 months were significantly more numerous in WT. We tested the hypothesis that stimulation of the 5-HT₄ receptor promotes enteric neuron survival and/or neurogenesis. In vitro, 5-HT₄ agonists increased enteric neuronal development/survival, decreased apoptosis, and activated CREB (cAMP response element-binding protein). In vivo, in WT but not KO mice, 5-HT₄ agonists induced bromodeoxyuridine incorporation into cells that expressed markers of neurons (HuC/D, doublecortin), neural precursors (Sox10, nestin, Phox2b), or stem cells (Musashi-1). This is the first demonstration of adult enteric neurogenesis; our results suggest that 5-HT₄ receptors are required postnatally for ENS growth and maintenance.

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Received March 9, 2009; revised May 18, 2009; accepted June 19, 2009.

Correspondence should be addressed to Min-Tsai Liu, Department of Pathology and Cell Biology, College of Physicians and Surgeons, Columbia University, 630 West 168th Street, Box 23, New York, NY 10032. Email: ml27{at}columbia.edu

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