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

Abstract

Vampire bats (Desmodus rotundus) are obligate blood feeders that have evolved specialized systems to suit their sanguinary lifestyle1,2,3. 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 radiation1,4. In each case, infrared signals are detected by trigeminal nerve fibres that innervate specialized pit organs on the animal’s face5,6,7,8,9,10. 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 detector6. 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.

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Figure 1: Anatomy of fruit bat and vampire bat sensory ganglia.
Figure 2: Sequence and distribution of vampire bat TRPV1.
Figure 3: Functional analyses of vampire bat TRPV1 isoforms.
Figure 4: Genomic organization of mammalian Trpv1 locus.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Gene Expression Omnibus

Data deposits

Deep sequencing data are archived under GEO accession number GSE28243. GenBank accession numbers are JN006855 (D. rotundus TRPV1-S), JN006856 (D. rotundus TRPV1-L), JN006857 (D. rotundus TRPA1), JN006858 (C. brevicauda TRPA1), JN006859 (C. brevicauda TRPV1-L), JN006860 (C. brevicauda TRPV1-S), JN006861 (Scapanus orarius TRPV1-L), JN006862 (S. orarius TRPV1-S), JN006863 (Pteropus rodricensis intron), JN006864 (D. rotundus intron), JN006865 (C. brevicauda intron), JN006866 (P. vampyrus intron), JN006867 (Rousettus aegyptiacus intron) and JN006868 (S. orarius intron).

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Acknowledgements

We thank Y. Kelly and J. Poblete for technical assistance, C. Sehnert for help with bovine tissue collection, M. Suzawa and H. Ingraham for providing zebrafish mRNA, A. Walsh for providing megabat blood samples, the Centro Técnico de Producción Socialista Florentino for providing access to Hato Piñero (Cojedes, Venezuela) for animal collection and J. Nassar for providing access to laboratory material required for specimen collection. This work was supported by a Ruth L. Kirschstein National Research Service Award (GM080853; N.T.I.), a Pathway to Independence Fellowship from the UCSF CVRI (E.O.G.), the Howard Hughes Medical Institute (J.S.W.), and grants from NIH, including P01 AG010770 (J.S.W.) and NS047723 and NS055299 (D.J.).

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E.O.G., J.F.C.-M. and N.T.I. designed and performed experiments and analysed data. N.T.I. and J.S.W. developed analytical tools and analysed data. J.A.G.-C., C.I.A. and C.M. collected bat species and obtained tissues for analysis. E.O.G., J.F.C.-M. and D.J. wrote the manuscript with discussion and contributions from all authors. J.S.W. and D.J. provided advice and guidance throughout.

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Correspondence to Nicholas T. Ingolia or David Julius.

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The authors declare no competing financial interests.

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Gracheva, E., Cordero-Morales, J., González-Carcacía, J. et al. Ganglion-specific splicing of TRPV1 underlies infrared sensation in vampire bats. Nature 476, 88–91 (2011). https://doi.org/10.1038/nature10245

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