Diverse Regulation of Temperature Sensation by Trimeric G-Protein Signaling in Caenorhabditis elegans

Tomoyo Ujisawa; Akane Ohta; Misato Uda-Yagi; Atsushi Kuhara

doi:10.1371/journal.pone.0165518

Diverse Regulation of Temperature Sensation by Trimeric G-Protein Signaling in Caenorhabditis elegans

PLoS One. 2016 Oct 27;11(10):e0165518. doi: 10.1371/journal.pone.0165518. eCollection 2016.

Authors

Tomoyo Ujisawa^{1

2}, Akane Ohta^{1

3

2}, Misato Uda-Yagi², Atsushi Kuhara^{1

3

2}

Affiliations

¹ Laboratory of Molecular and Cellular Regulation, Graduate school of Natural Sciencey, Konan University, 8-9-1 Okamoto, Higashinada-ku, Kobe 658-8501, Japan.
² Institute for Integrative Neurobiology, Konan University, 8-9-1 Okamoto, Higashinada-ku, Kobe 658-8501, Japan.
³ Laboratory of Molecular and Cellular Regulation, Faculty of Science and Engineering, Konan University, 8-9-1 Okamoto, Higashinada-ku, Kobe 658-8501, Japan.

Abstract

Temperature sensation by the nervous system is essential for life and proliferation of animals. The molecular-physiological mechanisms underlying temperature signaling have not been fully elucidated. We show here that diverse regulatory machinery underlies temperature sensation through trimeric G-protein signaling in the nematode Caenorhabditis elegans. Molecular-genetic studies demonstrated that cold tolerance is regulated by additive functions of three Gα proteins in a temperature-sensing neuron, ASJ, which is also known to be a light-sensing neuron. Optical recording of calcium concentration in ASJ upon temperature-changes demonstrated that three Gα proteins act in different aspects of temperature signaling. Calcium concentration changes in ASJ upon temperature change were unexpectedly decreased in a mutant defective in phosphodiesterase, which is well known as a negative regulator of calcium increase. Together, these data demonstrate commonalities and differences in the molecular components concerned with light and temperature signaling in a single sensory neuron.

MeSH terms

Adaptation, Physiological
Animals
Caenorhabditis elegans / metabolism*
Caenorhabditis elegans / physiology
Calcium / metabolism
Cold Temperature
GTP-Binding Proteins / metabolism*
Germ Cells
Microscopy, Confocal
Signal Transduction*
Temperature*

Substances

GTP-Binding Proteins
Calcium

Grants and funding

AK was supported by the Naito Foundation, the Uehara Memorial Foundation, the Cosmetology Research Foundation, the Hirao Taro Foundation of KONAN GAKUEN for Academic Research, a JSPS KAKENHI Grant-in-Aid for Scientific Research (B) (15H04404) and Grant-in-Aid for Challenging Exploratory Research (26640018), and a Grant-in-Aid for Scientific Research on Innovative Areas, Thermal Biology (15H05928), from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan. AO was supported by the Kato Memorial Bioscience Foundation, the Shiseido Female Researcher Science Grant, the Japan Science Society, JSPS KAKENHI, a Grant-in-Aid for Young Scientists (B) (15K18579), and a Grant-in-Aid for JSPS Fellows PD (16J00123), Japan. TU was supported by a Grant-in-Aid for JSPS Fellows DC (15J04977), Japan. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.