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The Journal of Neuroscience, July 30, 2008, 28(31):7863-7875; doi:10.1523/JNEUROSCI.1696-08.2008
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Development/Plasticity/Repair
TRPA1 Channels Mediate Cold Temperature Sensing in Mammalian Vagal Sensory Neurons: Pharmacological and Genetic Evidence
Otto Fajardo, Victor Meseguer, Carlos Belmonte, andFélix Viana Instituto de Neurociencias de Alicante, Universidad Miguel Hernández–Consejo Superior de Investigaciones Científicas, 03550 San Juan de Alicante, Spain
Correspondence should be addressed to Dr. Félix Viana, Instituto de Neurociencias de Alicante, Universidad Miguel Hernández-Spanish Consejo Superior de Investigaciones Científicas, Avenida S. Ramón y Cajal s.n., Apartado 18, 03550 San Juan de Alicante, Spain. Email: felix.viana{at}umh.es
Cold thermoreceptors have been described in different territories of the vagus nerve. Application of cold temperature to these visceral afferents can evoke major protective reflexes and thermoregulatory responses. However, virtually nothing is known about the transduction mechanisms underlying cold sensitivity in vagal afferents. Here, we investigated the effects of cold stimulation on intracellular calcium responses and excitability of cultured vagal sensory neurons in the rat nodose ganglion. A large fraction of vagal neurons were activated by cold, with a mean threshold of
24°C. Cooling was accompanied by development of a small inward current and the firing of action potentials. Most cold-sensitive neurons were also activated by heat and capsaicin, suggesting a nociceptive function. The pharmacological response to TRPM8 and TRPA1 agonists and antagonists suggested that, unlike results observed in somatic tissues, TRPA1 is the major mediator of cold-evoked responses in vagal visceral neurons. Thus, most cold-evoked responses were potentiated by cinnamaldehyde, menthol, icilin, and BCTC [4-(3-chloro-pyridin-2-yl)-piperazine-1-carboxylic acid (4-tert-butyl-phenyl)-amide], agonists of TRPA1, and were inhibited by ruthenium red, camphor, and HC03001 [2-(1,3-dimethyl-2,6-dioxo-1,2,3,6-tetrahydro-7H-purin-7-yl)-N-(4-isopropylphenyl)acetamide]. Results in mouse nodose neurons revealed a similar pharmacological profile of cold-evoked responses. Furthermore, experiments in TRPA1 knock-out mice showed a large reduction in the percentage of cold-sensitive neurons compared with wild-type animals. Together, these results support an important role of TRPA1 channels in visceral thermosensation and indicate major differences in the transduction of temperature signals between somatic and visceral sensory neurons.
Key words: thermotransduction; nodose ganglion; laryngeal afferents; TRP channel; nociceptor; noxious cold
Received April 18, 2008; revised June 6, 2008; accepted June 25, 2008.
Correspondence should be addressed to Dr. Félix Viana, Instituto de Neurociencias de Alicante, Universidad Miguel Hernández-Spanish Consejo Superior de Investigaciones Científicas, Avenida S. Ramón y Cajal s.n., Apartado 18, 03550 San Juan de Alicante, Spain. Email: felix.viana{at}umh.es
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