Cargando…

Characterization of TRPA channels in the starfish Patiria pectinifera: involvement of thermally activated TRPA1 in thermotaxis in marine planktonic larvae

The vast majority of marine invertebrates spend their larval period as pelagic plankton and are exposed to various environmental cues. Here we investigated the thermotaxis behaviors of the bipinnaria larvae of the starfish, Patiria pectinifera, in association with TRPA ion channels that serve as the...

Descripción completa

Detalles Bibliográficos
Autores principales: Saito, Shigeru, Hamanaka, Gen, Kawai, Narudo, Furukawa, Ryohei, Gojobori, Jun, Tominaga, Makoto, Kaneko, Hiroyuki, Satta, Yoko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5438368/
https://www.ncbi.nlm.nih.gov/pubmed/28526851
http://dx.doi.org/10.1038/s41598-017-02171-8
_version_ 1783237743808086016
author Saito, Shigeru
Hamanaka, Gen
Kawai, Narudo
Furukawa, Ryohei
Gojobori, Jun
Tominaga, Makoto
Kaneko, Hiroyuki
Satta, Yoko
author_facet Saito, Shigeru
Hamanaka, Gen
Kawai, Narudo
Furukawa, Ryohei
Gojobori, Jun
Tominaga, Makoto
Kaneko, Hiroyuki
Satta, Yoko
author_sort Saito, Shigeru
collection PubMed
description The vast majority of marine invertebrates spend their larval period as pelagic plankton and are exposed to various environmental cues. Here we investigated the thermotaxis behaviors of the bipinnaria larvae of the starfish, Patiria pectinifera, in association with TRPA ion channels that serve as thermal receptors in various animal species. Using a newly developed thermotaxis assay system, we observed that P. pectinifera larvae displayed positive thermotaxis toward high temperatures, including toward temperatures high enough to cause death. In parallel, we identified two TRPA genes, termed PpTRPA1 and PpTRPA basal, from this species. We examined the phylogenetic position, spatial expression, and channel properties of each PpTRPA. Our results revealed the following: (1) The two genes diverged early in animal evolution; (2) PpTRPA1 and PpTRPA basal are expressed in the ciliary band and posterior digestive tract of the larval body, respectively; and (3) PpTRPA1 is activated by heat stimulation as well as by known TRPA1 agonists. Moreover, knockdown and rescue experiments demonstrated that PpTRPA1 is involved in positive thermotaxis in P. pectinifera larvae. This is the first report to reveal that TRPA1 channels regulate the behavioral response of a marine invertebrate to temperature changes during its planktonic larval period.
format Online
Article
Text
id pubmed-5438368
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-54383682017-05-22 Characterization of TRPA channels in the starfish Patiria pectinifera: involvement of thermally activated TRPA1 in thermotaxis in marine planktonic larvae Saito, Shigeru Hamanaka, Gen Kawai, Narudo Furukawa, Ryohei Gojobori, Jun Tominaga, Makoto Kaneko, Hiroyuki Satta, Yoko Sci Rep Article The vast majority of marine invertebrates spend their larval period as pelagic plankton and are exposed to various environmental cues. Here we investigated the thermotaxis behaviors of the bipinnaria larvae of the starfish, Patiria pectinifera, in association with TRPA ion channels that serve as thermal receptors in various animal species. Using a newly developed thermotaxis assay system, we observed that P. pectinifera larvae displayed positive thermotaxis toward high temperatures, including toward temperatures high enough to cause death. In parallel, we identified two TRPA genes, termed PpTRPA1 and PpTRPA basal, from this species. We examined the phylogenetic position, spatial expression, and channel properties of each PpTRPA. Our results revealed the following: (1) The two genes diverged early in animal evolution; (2) PpTRPA1 and PpTRPA basal are expressed in the ciliary band and posterior digestive tract of the larval body, respectively; and (3) PpTRPA1 is activated by heat stimulation as well as by known TRPA1 agonists. Moreover, knockdown and rescue experiments demonstrated that PpTRPA1 is involved in positive thermotaxis in P. pectinifera larvae. This is the first report to reveal that TRPA1 channels regulate the behavioral response of a marine invertebrate to temperature changes during its planktonic larval period. Nature Publishing Group UK 2017-05-19 /pmc/articles/PMC5438368/ /pubmed/28526851 http://dx.doi.org/10.1038/s41598-017-02171-8 Text en © The Author(s) 2017 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Saito, Shigeru
Hamanaka, Gen
Kawai, Narudo
Furukawa, Ryohei
Gojobori, Jun
Tominaga, Makoto
Kaneko, Hiroyuki
Satta, Yoko
Characterization of TRPA channels in the starfish Patiria pectinifera: involvement of thermally activated TRPA1 in thermotaxis in marine planktonic larvae
title Characterization of TRPA channels in the starfish Patiria pectinifera: involvement of thermally activated TRPA1 in thermotaxis in marine planktonic larvae
title_full Characterization of TRPA channels in the starfish Patiria pectinifera: involvement of thermally activated TRPA1 in thermotaxis in marine planktonic larvae
title_fullStr Characterization of TRPA channels in the starfish Patiria pectinifera: involvement of thermally activated TRPA1 in thermotaxis in marine planktonic larvae
title_full_unstemmed Characterization of TRPA channels in the starfish Patiria pectinifera: involvement of thermally activated TRPA1 in thermotaxis in marine planktonic larvae
title_short Characterization of TRPA channels in the starfish Patiria pectinifera: involvement of thermally activated TRPA1 in thermotaxis in marine planktonic larvae
title_sort characterization of trpa channels in the starfish patiria pectinifera: involvement of thermally activated trpa1 in thermotaxis in marine planktonic larvae
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5438368/
https://www.ncbi.nlm.nih.gov/pubmed/28526851
http://dx.doi.org/10.1038/s41598-017-02171-8
work_keys_str_mv AT saitoshigeru characterizationoftrpachannelsinthestarfishpatiriapectiniferainvolvementofthermallyactivatedtrpa1inthermotaxisinmarineplanktoniclarvae
AT hamanakagen characterizationoftrpachannelsinthestarfishpatiriapectiniferainvolvementofthermallyactivatedtrpa1inthermotaxisinmarineplanktoniclarvae
AT kawainarudo characterizationoftrpachannelsinthestarfishpatiriapectiniferainvolvementofthermallyactivatedtrpa1inthermotaxisinmarineplanktoniclarvae
AT furukawaryohei characterizationoftrpachannelsinthestarfishpatiriapectiniferainvolvementofthermallyactivatedtrpa1inthermotaxisinmarineplanktoniclarvae
AT gojoborijun characterizationoftrpachannelsinthestarfishpatiriapectiniferainvolvementofthermallyactivatedtrpa1inthermotaxisinmarineplanktoniclarvae
AT tominagamakoto characterizationoftrpachannelsinthestarfishpatiriapectiniferainvolvementofthermallyactivatedtrpa1inthermotaxisinmarineplanktoniclarvae
AT kanekohiroyuki characterizationoftrpachannelsinthestarfishpatiriapectiniferainvolvementofthermallyactivatedtrpa1inthermotaxisinmarineplanktoniclarvae
AT sattayoko characterizationoftrpachannelsinthestarfishpatiriapectiniferainvolvementofthermallyactivatedtrpa1inthermotaxisinmarineplanktoniclarvae