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

• Published in: Nature (London) Vol. 476; no. 7358; pp. 88 - 91
• Main Authors: Gracheva, Elena O., Cordero-Morales, Julio F., González-Carcacía, José A., Ingolia, Nicholas T., Manno, Carlo, Aranguren, Carla I., Weissman, Jonathan S., Julius, David
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 03.08.2011; Nature Publishing Group
• Subjects: 631/181/757; 631/337/1645/1946; 631/378/2620; 631/45/269/1153; Alternative Splicing - genetics; Amino Acid Sequence; Animals; Biological and medical sciences; Cattle; Chiroptera - anatomy & histology; Chiroptera - classification; Chiroptera - genetics; Chiroptera - physiology; Desmodus rotundus; Face - anatomy & histology; Face - innervation; Feeding Behavior - physiology; Fundamental and applied biological sciences. Psychology; HEK293 Cells; Hot Temperature; Humanities and Social Sciences; Humans; Infrared Rays; letter; Molecular Sequence Data; multidisciplinary; Organ Specificity - genetics; Phylogeny; Predatory Behavior - physiology; Protein Isoforms - chemistry; Protein Isoforms - genetics; Protein Isoforms - metabolism; Protein Structure, Tertiary; Science; Science (multidisciplinary); Sensation - physiology; Trigeminal Ganglion - metabolism; TRPV Cation Channels - chemistry; TRPV Cation Channels - genetics; TRPV Cation Channels - metabolism; Vertebrates: nervous system and sense organs; Fissipedia; Alternative splicing; Carnivora; Spinal cord; Temperature; Central nervous system; Environmental factor; Ox; Thermoreceptor; Vertebrata; Heat; TRPV1 vanilloid receptor; Mammalia; Trigeminal nerve; Development; Spinal ganglion; Artiodactyla; Dog; Ungulata; Adaptation; Biological receptor
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature10245

The vampire bat's unique infrared detectors Blood-feeding vampire bats have evolved the ability to detect infrared (IR) radiation as a means of locating hot spots on warm-blooded prey. Only three other vertebrate lineages have this 'sixth' sense: three distantly related groups of snakes (pit vipers, pythons and boas). In all cases, the IR sensor is a highly specialized facial structure called the pit organ. In the snakes, a non-heat-sensitive ion channel (vertebrate TRPA1) has become an infrared detector. As reported in this issue, vampire bats use a slightly different molecular mechanism whereby RNA splicing generates a variant of the ubiquitous TRPV1 heat-sensitive channel that is tuned to lower temperatures. Comparison of this channel's gene sequence with the equivalent in other mammals lends support to the hypothesis based on molecular data that these bats are evolutionarily grouped with horses, dogs, cows, moles and dolphins (in the Laurasiatheria superorder), rather than with humans, monkeys and rodents (in the Euarchontoglires) as originally proposed on anatomical criteria. Vampire bats ( Desmodus rotundus ) are obligate blood feeders that have evolved specialized systems to suit their sanguinary lifestyle 1 , 2 , 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 , 6 , 7 , 8 , 9 , 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.