TY - JOUR
T1 - cGMP dynamics that underlies thermosensation in temperature-sensing neuron regulates thermotaxis behavior in C. elegans
AU - Aok, Ichiro
AU - Shiota, Makoto
AU - Tsukada, Yuki
AU - Nakano, Shunji
AU - Mori, Ikue
N1 - Funding Information:
This study was funded by following grants to I.M.: Ministry of Education, Culture, Sports, Science and Technology (MEXT) KAKENHI JP16H01272 and JP18H04693 (https://www.mext.go.jp/en/policy/science_technology/researchpromotion/title01/detail01/1374077.htm), and Japan Society for the Promotion of Science (JSPS) Grants-in-Aid for Scientific Research JP 16H01272, JP 16H02516 and JP 18H04693 (https://www.jsps.go.jp/english/e-grants/index. html). Some strains were provided by the Caenorhabditis Genetics Center (CGC), which is funded by NIH Office of Research Infrastructure Programs (P40 OD010440). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank H. Matsuyama for critical reading; and K. Ikegami, Y. Murakami, for technical assistance. Some strains were provided by the Caenorhabditis Genetics Center (CGC), which is funded by NIH Office of Research Infrastructure Programs (P40 OD010440).
Publisher Copyright:
© 2022 Aok et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
PY - 2022/12
Y1 - 2022/12
N2 - Living organisms including bacteria, plants and animals sense ambient temperature so that they can avoid noxious temperature or adapt to new environmental temperature. A nematode C. elegans can sense innocuous temperature, and navigate themselves towards memorize past cultivation temperature (Tc) of their preference. For this thermotaxis, AFD thermosensory neuron is pivotal, which stereotypically responds to warming by increasing intracellular Ca2+ level in a manner dependent on the remembered past Tc. We aimed to reveal how AFD encodes the information of temperature into neural activities. cGMP synthesis in AFD is crucial for thermosensation in AFD and thermotaxis behavior. Here we characterized the dynamic change of cGMP level in AFD by imaging animals expressing a fluorescence resonance energy transfer (FRET)-based cGMP probe specifically in AFD and found that cGMP dynamically responded to both warming and cooling in a manner dependent on past Tc. Moreover, we characterized mutant animals that lack guanylyl cyclases (GCYs) or phosphodiesterases (PDEs), which synthesize and hydrolyze cGMP, respectively, and uncovered how GCYs and PDEs contribute to cGMP and Ca2+ dynamics in AFD and to thermotaxis behavior.
AB - Living organisms including bacteria, plants and animals sense ambient temperature so that they can avoid noxious temperature or adapt to new environmental temperature. A nematode C. elegans can sense innocuous temperature, and navigate themselves towards memorize past cultivation temperature (Tc) of their preference. For this thermotaxis, AFD thermosensory neuron is pivotal, which stereotypically responds to warming by increasing intracellular Ca2+ level in a manner dependent on the remembered past Tc. We aimed to reveal how AFD encodes the information of temperature into neural activities. cGMP synthesis in AFD is crucial for thermosensation in AFD and thermotaxis behavior. Here we characterized the dynamic change of cGMP level in AFD by imaging animals expressing a fluorescence resonance energy transfer (FRET)-based cGMP probe specifically in AFD and found that cGMP dynamically responded to both warming and cooling in a manner dependent on past Tc. Moreover, we characterized mutant animals that lack guanylyl cyclases (GCYs) or phosphodiesterases (PDEs), which synthesize and hydrolyze cGMP, respectively, and uncovered how GCYs and PDEs contribute to cGMP and Ca2+ dynamics in AFD and to thermotaxis behavior.
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U2 - 10.1371/journal.pone.0278343
DO - 10.1371/journal.pone.0278343
M3 - Article
C2 - 36472979
AN - SCOPUS:85143644985
SN - 1932-6203
VL - 17
JO - PLoS One
JF - PLoS One
IS - 12 December
M1 - e0278343
ER -