TRPA5 encodes a thermosensitive ankyrin ion channel receptor in a triatomine insect

Marjorie A Liénard; David Baez-Nieto; Cheng-Chia Tsai; Wendy A Valencia-Montoya; Balder Werin; Urban Johanson; Jean-Marc Lassance; Jen Q Pan; Nanfang Yu; Naomi E Pierce

doi:10.1016/j.isci.2024.109541

TRPA5 encodes a thermosensitive ankyrin ion channel receptor in a triatomine insect

iScience. 2024 Mar 20;27(4):109541. doi: 10.1016/j.isci.2024.109541. eCollection 2024 Apr 19.

Authors

Marjorie A Liénard^{1

2

3}, David Baez-Nieto⁴, Cheng-Chia Tsai⁵, Wendy A Valencia-Montoya², Balder Werin⁶, Urban Johanson⁶, Jean-Marc Lassance^{2

7}, Jen Q Pan⁴, Nanfang Yu⁵, Naomi E Pierce²

Affiliations

¹ Department of Biology, Lund University, 22362 Lund, Sweden.
² Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA.
³ Broad Institute, Cambridge, MA 02142, USA.
⁴ Stanley Center for Psychiatric Research, Broad Institute, Cambridge, MA 02142, USA.
⁵ Department of Applied Physics and Applied Mathematics, Columbia University, New York, NY 10027, USA.
⁶ Division of Biochemistry and Structural Biology, Department of Chemistry, Lund University, 22362 Lund, Sweden.
⁷ Laboratory of Evolutionary Neuroethology, GIGA Institute, University of Liège, 4000 Liège, Belgium.

Abstract

As ectotherms, insects need heat-sensitive receptors to monitor environmental temperatures and facilitate thermoregulation. We show that TRPA5, a class of ankyrin transient receptor potential (TRP) channels absent in dipteran genomes, may function as insect heat receptors. In the triatomine bug Rhodnius prolixus (order: Hemiptera), a vector of Chagas disease, the channel RpTRPA5B displays a uniquely high thermosensitivity, with biophysical determinants including a large channel activation enthalpy change (72 kcal/mol), a high temperature coefficient (Q₁₀ = 25), and in vitro temperature-induced currents from 53°C to 68°C (T_0.5 = 58.6°C), similar to noxious TRPV receptors in mammals. Monomeric and tetrameric ion channel structure predictions show reliable parallels with fruit fly dTRPA1, with structural uniqueness in ankyrin repeat domains, the channel selectivity filter, and potential TRP functional modulator regions. Overall, the finding of a member of TRPA5 as a temperature-activated receptor illustrates the diversity of insect molecular heat detectors.

Keywords: Biological sciences; Entomology; Molecular biology.