Keeping the blood flowing—plasminogen activator genes and feeding behavior in vampire bats

Tellgren-Roth, Åsa; Dittmar, Katharina; Massey, Steven E.; Kemi, Cecilia; Tellgren-Roth, Christian; Savolainen, Peter; Lyons, Leslie A.; Liberles, David A.

doi:10.1007/s00114-008-0446-0

Cited by 26 publications

(23 citation statements)

References 37 publications

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“… Vampire bats ( Desmodus rotundus ) are obligate blood feeders that have evolved specialized systems to suit their unique sanguinary lifestyle 1–3 . Chief among such adaptations is the ability to detect infrared radiation as a means of locating hot spots on warm-blooded prey.…”

mentioning

confidence: 99%

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

Gracheva

Cordero-Morales

González-Carcacía

et al. 2011

Nature

216

126

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Vampire bats (Desmodus rotundus) are obligate blood feeders that have evolved specialized systems to suit their unique sanguinary lifestyle 1–3. Chief among such adaptations is the ability to detect infrared radiation as a means of locating hot spots 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 heat is detected by trigeminal nerve fibers 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 or cell type specific manner. Previously, we have shown that snakes co-opt a non-heat sensitive channel (vertebrate TRPA1) to produce an infrared detector 6. Here we show that vampire bats tune an already heat sensitive channel (TRPV1) by lowering its thermal activation threshold to ~30°C. This is achieved through alternative splicing of TRPV1 transcripts to produce a channel with a truncated C-terminal cytoplasmic domain. Remarkably, these splicing events occur exclusively in trigeminal ganglia (TG), and not dorsal root ganglia (DRG), 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 unique molecular mechanism for physiological tuning of thermosensory nerve fibers.

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mentioning

confidence: 99%

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

Gracheva

Cordero-Morales

González-Carcacía

et al. 2011

Nature

216

126

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“…Plasminogen activators have been purified from the venomous snake, Trimeresurus stejnegeri [44] and from the saliva of common vampire bat, Desmodus rotundus [10], [45]. In vampire bats, plasminogen activator is thought to be a key enzyme that plays a crucial role in the maintenance of the flow of blood during the feeding process [46] and snake-venom plasminogen activator is associated with the pathogenesis of envenomation rendering the blood incoagulable [44]. Maintenance of hosts' blood fluidity at the site of biting is also very critical for the development of blood pool and subsequent blood feeding, and eventually for the survival of ixodid ticks.…”

Section: Discussionmentioning

confidence: 99%

Longistatin, a Plasminogen Activator, Is Key to the Availability of Blood-Meals for Ixodid Ticks

et al. 2011

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Ixodid ticks are notorious blood-sucking ectoparasites and are completely dependent on blood-meals from hosts. In addition to the direct severe effects on health and productivity, ixodid ticks transmit various deadly diseases to humans and animals. Unlike rapidly feeding vessel-feeder hematophagous insects, the hard ticks feed on hosts for a long time (5−10 days or more), making a large blood pool beneath the skin. Tick's salivary glands produce a vast array of bio-molecules that modulate their complex and persistent feeding processes. However, the specific molecule that functions in the development and maintenance of a blood pool is yet to be identified. Recently, we have reported on longistatin, a 17.8-kDa protein with two functional EF-hand Ca++-binding domains, from the salivary glands of the disease vector, Haemaphysalis longicornis, that has been shown to be linked to blood-feeding processes. Here, we show that longistatin plays vital roles in the formation of a blood pool and in the acquisition of blood-meals. Data clearly revealed that post-transcriptional silencing of the longistatin-specific gene disrupted ticks' unique ability to create a blood pool, and they consequently failed to feed and replete on blood-meals from hosts. Longistatin completely hydrolyzed α, β and γ chains of fibrinogen and delayed fibrin clot formation. Longistatin was able to bind with fibrin meshwork, and activated fibrin clot-bound plasminogen into its active form plasmin, as comparable to that of tissue-type plasminogen activator (t-PA), and induced lysis of fibrin clot and platelet-rich thrombi. Plasminogen activation potentiality of longistatin was increased up to 4 times by soluble fibrin. Taken together, our results suggest that longistatin may exert potent functions both as a plasminogen activator and as an anticoagulant in the complex scenario of blood pool formation; the latter is critical to the feeding success and survival of ixodid ticks.

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“…Upon analysis, both fecal samples showed that pig and chicken blood had been ingested, indicating feeding flexibility in D. youngi. Like D. rotundus, D. youngi saliva also has a protease that greatly slows mammalian blood coagulation (Tellgren-Roth et al 2009). However, it is known that D. youngi has difficulty digesting high amounts of dry matter from mammal's blood (Coen 2002).…”

Section: Discussionmentioning

confidence: 99%

Prey preference of the common vampire bat (Desmodus rotundus, Chiroptera) using molecular analysis

Bobrowiec¹

2015

Journal of Mammalogy

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Morphological identification of prey fragments in vampire bat feces is impossible because of an exclusively blood-based diet. Therefore, studies of their foraging ecology require innovative approaches. We investigated the diet of Desmodus rotundus using a PCR-restriction fragment length polymorphism (RFLP) molecular method by amplifying the cytochrome b mitochondrial gene (380 bp) from DNA fecal samples collected from captive bats fed with blood from chickens, cattle, pigs, dogs, and humans-the 5 most frequently attacked prey species in rural areas of the Brazilian Amazonia. The prey preference of the vampire bat was investigated in 18 riverine villages, where the availability of domestic animals to bats was quantified. Prey DNA amplified from fecal samples exhibited no visible signals of vampire bat DNA. A PCR-RFLP flowchart and a combination of 2 DNA restriction enzymes allowed the direct identification of prey to species level. The enzymes' restriction profile did not overlap with those of vampire bats or wild mammal and avian species. Chickens were the most attacked prey species (61.4% of the identifications, n = 27), but pigs were highly preferred in relation to prey availability. This suggests a preference for mammalian blood in D. rotundus diet, with chickens exploited as a secondary food source. No wild vertebrate species was identified in the fecal samples, indicating that vampire bats are selectively feeding on the blood of domesticated animals, probably because they are more predictable and easily accessed resources.

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Keeping the blood flowing—plasminogen activator genes and feeding behavior in vampire bats

Cited by 26 publications

References 37 publications

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

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

Longistatin, a Plasminogen Activator, Is Key to the Availability of Blood-Meals for Ixodid Ticks

Prey preference of the common vampire bat (Desmodus rotundus, Chiroptera) using molecular analysis

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