Ganglion-specific splicing of TRPV1 underlies infrared sensation in vampire bats

• Published in: Nature (London) 2011-08, Vol.476 (7358), p.88
• Main Authors: Gracheva, Elena O, Cordero-Morales, Julio F, Gonzalez-Carcacia, Jose A, Ingolia, Nicholas T, Manno, Carlo, Aranguren, Carla I, Weissman, Jonathan S, Julius, David
• Format: Article
• Language: English
• Subjects: Chemical properties; Infrared radiation; Ion channels; Physiological aspects; Thermal properties; Vampire bats
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/naturel0245

Vampire bats (Desmodus rotundus) are obligate blood feeders that have evolved specialized systems to suit their sanguinary lifestyle (1-3). Chief among such adaptations is the ability to detect infrared radiation as a means of locating hotspots on warm-blooded prey. Among vertebrates, only vampire bats, boas, pythons and pit vipers are capable of detecting infrared radiation (1,4). In each case, infrared signals are detected by trigeminal nerve fibres that innervate specialized pit organs on the animal's face (5-10). Thus, vampire bats and snakes have taken thermosensation to the extreme by developing specialized systems for detecting infrared radiation. As such, these creatures provide a window into the molecular and genetic mechanisms underlying evolutionary tuning of thermoreceptors in a species-specific or cell-type-specific manner. Previously, we have shown that snakes co-opt a non-heat-sensitive channel, vertebrate TRPA1 (transient receptor potential cation channel A1), to produce an infrared detector (6). Here we show that vampire bats tune a channel that is already heat-sensitive, TRPV1, by lowering its thermal activation threshold to about 30 °C. This is achieved through alternative splicing of TRPV1 transcripts to produce a channel with a truncated carboxy-terminal cytoplasmic domain. These splicing events occur exclusively in trigeminal ganglia, and not in dorsal root ganglia, thereby maintaining a role for TRPV1 as a detector of noxious heat in somatic afferents. This reflects a unique organization of the bat Trpv1 gene that we show to be characteristic of Laurasiatheria mammals (cows, dogs and moles), supporting a close phylogenetic relationship with bats. These findings reveal a novel molecular mechanism for physiological tuning of thermosensory nerve fibres.