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

Summary: 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...

Full description

Bibliographic Details
Main Authors: 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
Format: Article
Language:English
Published: Elsevier 2024-04-01
Series:iScience
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2589004224007636
_version_ 1797226608909615104
author 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
author_facet 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
author_sort Marjorie A. Liénard
collection DOAJ
description Summary: 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 (T0.5 = 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.
first_indexed 2024-04-24T14:27:37Z
format Article
id doaj.art-2267e094972541aea03611109c7abb4d
institution Directory Open Access Journal
issn 2589-0042
language English
last_indexed 2024-04-24T14:27:37Z
publishDate 2024-04-01
publisher Elsevier
record_format Article
series iScience
spelling doaj.art-2267e094972541aea03611109c7abb4d2024-04-03T04:27:14ZengElsevieriScience2589-00422024-04-01274109541TRPA5 encodes a thermosensitive ankyrin ion channel receptor in a triatomine insectMarjorie A. Liénard0David Baez-Nieto1Cheng-Chia Tsai2Wendy A. Valencia-Montoya3Balder Werin4Urban Johanson5Jean-Marc Lassance6Jen Q. Pan7Nanfang Yu8Naomi E. Pierce9Department of Biology, Lund University, 22362 Lund, Sweden; Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA; Broad Institute, Cambridge, MA 02142, USA; Corresponding authorStanley Center for Psychiatric Research, Broad Institute, Cambridge, MA 02142, USA; Corresponding authorDepartment of Applied Physics and Applied Mathematics, Columbia University, New York, NY 10027, USADepartment of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USADivision of Biochemistry and Structural Biology, Department of Chemistry, Lund University, 22362 Lund, SwedenDivision of Biochemistry and Structural Biology, Department of Chemistry, Lund University, 22362 Lund, SwedenDepartment of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA; Laboratory of Evolutionary Neuroethology, GIGA Institute, University of Liège, 4000 Liège, BelgiumStanley Center for Psychiatric Research, Broad Institute, Cambridge, MA 02142, USADepartment of Applied Physics and Applied Mathematics, Columbia University, New York, NY 10027, USADepartment of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USASummary: 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 (T0.5 = 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.http://www.sciencedirect.com/science/article/pii/S2589004224007636Biological sciencesEntomologyMolecular biology
spellingShingle 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
TRPA5 encodes a thermosensitive ankyrin ion channel receptor in a triatomine insect
iScience
Biological sciences
Entomology
Molecular biology
title TRPA5 encodes a thermosensitive ankyrin ion channel receptor in a triatomine insect
title_full TRPA5 encodes a thermosensitive ankyrin ion channel receptor in a triatomine insect
title_fullStr TRPA5 encodes a thermosensitive ankyrin ion channel receptor in a triatomine insect
title_full_unstemmed TRPA5 encodes a thermosensitive ankyrin ion channel receptor in a triatomine insect
title_short TRPA5 encodes a thermosensitive ankyrin ion channel receptor in a triatomine insect
title_sort trpa5 encodes a thermosensitive ankyrin ion channel receptor in a triatomine insect
topic Biological sciences
Entomology
Molecular biology
url http://www.sciencedirect.com/science/article/pii/S2589004224007636
work_keys_str_mv AT marjoriealienard trpa5encodesathermosensitiveankyrinionchannelreceptorinatriatomineinsect
AT davidbaeznieto trpa5encodesathermosensitiveankyrinionchannelreceptorinatriatomineinsect
AT chengchiatsai trpa5encodesathermosensitiveankyrinionchannelreceptorinatriatomineinsect
AT wendyavalenciamontoya trpa5encodesathermosensitiveankyrinionchannelreceptorinatriatomineinsect
AT balderwerin trpa5encodesathermosensitiveankyrinionchannelreceptorinatriatomineinsect
AT urbanjohanson trpa5encodesathermosensitiveankyrinionchannelreceptorinatriatomineinsect
AT jeanmarclassance trpa5encodesathermosensitiveankyrinionchannelreceptorinatriatomineinsect
AT jenqpan trpa5encodesathermosensitiveankyrinionchannelreceptorinatriatomineinsect
AT nanfangyu trpa5encodesathermosensitiveankyrinionchannelreceptorinatriatomineinsect
AT naomiepierce trpa5encodesathermosensitiveankyrinionchannelreceptorinatriatomineinsect