Diverse sensitivities of TRPA1 from different mosquito species to thermal and chemical stimuli

Tianbang Li,Shigeru Saito,Makoto Tominaga,Tomoyuki Hikitsuchi,Yoshihiro Inoguchi,Honami Mitsuishi,Claire T Saito

doi:10.1038/s41598-019-56639-w

Abstract

Temperature and odors profoundly affect the behavior of animals. Transient receptor potential channel, subfamily A, member 1 (TRPA1) functions as a polymodal nociceptor for sensing both vital environmental cues in insects. Mosquitoes are recognized as disease vectors, and many efforts have been devoted to investigations of their host-seeking behaviors and repellents. However, the physiological characteristics of mosquito TRPA1 have not been systematically studied. We identified multiple alternative splice variants of the TrpA1 gene from Anopheles gambiae, Anopheles stephensi, Aedes aegypti and Culex pipiens pallens mosquitoes. And we performed comparative analyses of the responses of mosquito TRPA1s to heat or chemical stimuli with calcium-imaging and whole-cell patch-clamp methods. Comparison of TRPA1 among four mosquito species from different thermal niches revealed that TRPA1 of Culex pipiens pallens inhabiting the temperate zone had a lower temperature threshold for heat-evoked activation, which was supported by the in vivo heat-avoidance test. Notably, the chemosensitivity of mosquito TRPA1 channels revealed differences not only between variants but also among species. Moreover, we discovered three novel mosquito TRPA1 agonists. Thermal niches selection and evolutionary trajectories significantly affect the functional properties of mosquito TRPA1, which represents a hallmark of the behaviors that may permit the design of improved mosquito control methods.

Highlights

Temperature and odors profoundly affect the behavior of animals
We discovered that temperature thresholds for heat-evoked activation of TRPA1 of mosquitoes could be indicative of their respective thermotaxis behaviors in vivo
TrpA1 was newly cloned from Anopheles stephensi (As), Aedes aegypti (Aa) and Culex pipiens pallens (Cp) in the present study

Summary

Introduction

Temperature and odors profoundly affect the behavior of animals. Transient receptor potential channel, subfamily A, member 1 (TRPA1) functions as a polymodal nociceptor for sensing both vital environmental cues in insects. TRP ankyrin 1 (TRPA1) is a calcium-permeable non-selective cation channel with multiple ankyrin repeats in the amino-terminus[4,5] It functions as a polymodal receptor for detecting noxious temperature and adverse chemicals, suggesting that it is involved in nociception[6,7,8]. Genus Anopheles and Aedes/Culex diverged approximately 150 million years ago These mosquitoe species inhabit different areas of the world, suggesting that mosquito TRPA1 channels might exhibit species-specific differences in sensitivity to both thermal and chemical stimuli. Different N-termini of TRPA1 variants of Anopheles gambiae were investigated and the studies revealed that those different structures are involved in distinct www.nature.com/scientificreports thermosensitivities and chemosensitivities[10,15,20] Whether this phenomenon is consistent in other disease vector mosquitoes remains unanswered. Understanding of the physiological functions of disease vector mosquito TRPA1 could be extended to shed light upon the mechanism by which TRPA1 functions in the regulation of mosquito host-seeking and avoidance behaviors

Methods

Results

Conclusion