Espeleo

LETTER

doi:10.1038/nature10245

Ganglion-specific splicing of TRPV1 underlies
infrared sensation in vampire bats
´
´
´
Elena O. Gracheva1*, Julio F. Cordero-Morales1*, Jose A. Gonzalez-Carcacıa2, Nicholas T. Ingolia3, Carlo Manno4,
Carla I. Aranguren2, Jonathan S. Weissman5,6,7 & David Julius1,5

Initially, transcriptomes from these ganglia appeared to be indistinguishable(Supplementary Fig. 1). However, examination of cDNAs
encoding candidate thermosensors revealed a novel short isoform of
the capsaicin receptor, TRPV1, an excitatory ion channel that is activated by noxious heat (.43 uC) (refs 13–15). This isoform (TRPV1-S)
lacks 62 amino acids from the carboxy terminus (Fig. 2a and Supplementary Fig. 2) and is uniquely expressed in TG from vampire
bat, constitutingbetween 35% and 46% of all TRPV1 transcripts in
TG, but ,3% in DRG, as determined from transcriptome data or direct
cloning and sequencing of RT–PCR (PCR of reverse transcripts) products amplified from sensory ganglia (Fig. 2b). Moreover, TRPV1-S
transcripts were barely detected (,6%) in fruit bat TG or DRG
a

Fruit bat (C. brevicauda)

b

45

TG fruit

Vampire bat (D. rotundus)

50TG vampire

40
Percentage of total neurons

30

30
20

15

10
0

0

DRG vampire

DRG fruit
35

45

25

30

15
15

11
–2
21 0
–3
31 0
–4
41 0
–5
51 0
–6
61 0
–7
0

5
0

0
11
–2
21 0
–3
31 0
–4
41 0
–5
51 0
–6
61 0
–7
0

Vampire bats (Desmodus rotundus) are obligate blood feeders that
have evolved specialized systems to suit theirsanguinary lifestyle1–3.
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’sface5–10. 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-sensitivechannel, 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 6C. This is achieved through alternative
splicing of TRPV1 transcripts to produce a channel with a truncated
carboxy-terminal cytoplasmicdomain. 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. Thesefindings reveal a novel molecular mechanism for physiological tuning of thermosensory nerve fibres.
Vampire bats have three ‘leaf pits’ that surround the nose (Fig. 1a) and
receive input from low-threshold heat-sensitive nerve fibres responding
to stimuli at temperatures .29 uC (refs 1, 7, 11, 12). Closely related fruit
bats (Carollia brevicauda) have a different nasal structure devoid of pitorgans (Fig. 1a) and thus cannot detect infrared stimuli3. Sensory ganglia
of fruit bats showed a typical size distribution of neurons resembling that
seen in other mammals (Fig. 1b). In contrast, trigeminal ganglia (TG)
from vampire bats showed marked skewing towards large diameter
neurons, much like that observed in TG of pit-bearing snakes6, suggesting that anatomical specialization of TG...