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OLA-1, an Obg-like ATPase, integrates hunger with temperature information in sensory neurons in C. elegans

Animals detect changes in both their environment and their internal state and modify their behavior accordingly. Yet, it remains largely to be clarified how information of environment and internal state is integrated and how such integrated information modifies behavior. Well-fed C. elegans migrates...

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Autores principales: Aoki, Ichiro, Jurado, Paola, Nawa, Kanji, Kondo, Rumi, Yamashiro, Riku, Matsuyama, Hironori J., Ferrer, Isidre, Nakano, Shunji, Mori, Ikue
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9176836/
https://www.ncbi.nlm.nih.gov/pubmed/35675262
http://dx.doi.org/10.1371/journal.pgen.1010219
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author Aoki, Ichiro
Jurado, Paola
Nawa, Kanji
Kondo, Rumi
Yamashiro, Riku
Matsuyama, Hironori J.
Ferrer, Isidre
Nakano, Shunji
Mori, Ikue
author_facet Aoki, Ichiro
Jurado, Paola
Nawa, Kanji
Kondo, Rumi
Yamashiro, Riku
Matsuyama, Hironori J.
Ferrer, Isidre
Nakano, Shunji
Mori, Ikue
author_sort Aoki, Ichiro
collection PubMed
description Animals detect changes in both their environment and their internal state and modify their behavior accordingly. Yet, it remains largely to be clarified how information of environment and internal state is integrated and how such integrated information modifies behavior. Well-fed C. elegans migrates to past cultivation temperature on a thermal gradient, which is disrupted when animals are starved. We recently reported that the neuronal activities synchronize between a thermosensory neuron AFD and an interneuron AIY, which is directly downstream of AFD, in well-fed animals, while this synchrony is disrupted in starved animals. However, it remained to be determined whether the disruption of the synchrony is derived from modulation of the transmitter release from AFD or from the modification of reception or signal transduction in AIY. By performing forward genetics on a transition of thermotaxis behavior along starvation, we revealed that OLA-1, an Obg-like ATPase, functions in AFD to promote disruption of AFD-AIY synchrony and behavioral transition. Our results suggest that the information of hunger is delivered to the AFD thermosensory neuron and gates transmitter release from AFD to disrupt thermotaxis, thereby shedding light onto a mechanism for the integration of environmental and internal state to modulate behavior.
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spelling pubmed-91768362022-06-09 OLA-1, an Obg-like ATPase, integrates hunger with temperature information in sensory neurons in C. elegans Aoki, Ichiro Jurado, Paola Nawa, Kanji Kondo, Rumi Yamashiro, Riku Matsuyama, Hironori J. Ferrer, Isidre Nakano, Shunji Mori, Ikue PLoS Genet Research Article Animals detect changes in both their environment and their internal state and modify their behavior accordingly. Yet, it remains largely to be clarified how information of environment and internal state is integrated and how such integrated information modifies behavior. Well-fed C. elegans migrates to past cultivation temperature on a thermal gradient, which is disrupted when animals are starved. We recently reported that the neuronal activities synchronize between a thermosensory neuron AFD and an interneuron AIY, which is directly downstream of AFD, in well-fed animals, while this synchrony is disrupted in starved animals. However, it remained to be determined whether the disruption of the synchrony is derived from modulation of the transmitter release from AFD or from the modification of reception or signal transduction in AIY. By performing forward genetics on a transition of thermotaxis behavior along starvation, we revealed that OLA-1, an Obg-like ATPase, functions in AFD to promote disruption of AFD-AIY synchrony and behavioral transition. Our results suggest that the information of hunger is delivered to the AFD thermosensory neuron and gates transmitter release from AFD to disrupt thermotaxis, thereby shedding light onto a mechanism for the integration of environmental and internal state to modulate behavior. Public Library of Science 2022-06-08 /pmc/articles/PMC9176836/ /pubmed/35675262 http://dx.doi.org/10.1371/journal.pgen.1010219 Text en © 2022 Aoki et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Aoki, Ichiro
Jurado, Paola
Nawa, Kanji
Kondo, Rumi
Yamashiro, Riku
Matsuyama, Hironori J.
Ferrer, Isidre
Nakano, Shunji
Mori, Ikue
OLA-1, an Obg-like ATPase, integrates hunger with temperature information in sensory neurons in C. elegans
title OLA-1, an Obg-like ATPase, integrates hunger with temperature information in sensory neurons in C. elegans
title_full OLA-1, an Obg-like ATPase, integrates hunger with temperature information in sensory neurons in C. elegans
title_fullStr OLA-1, an Obg-like ATPase, integrates hunger with temperature information in sensory neurons in C. elegans
title_full_unstemmed OLA-1, an Obg-like ATPase, integrates hunger with temperature information in sensory neurons in C. elegans
title_short OLA-1, an Obg-like ATPase, integrates hunger with temperature information in sensory neurons in C. elegans
title_sort ola-1, an obg-like atpase, integrates hunger with temperature information in sensory neurons in c. elegans
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9176836/
https://www.ncbi.nlm.nih.gov/pubmed/35675262
http://dx.doi.org/10.1371/journal.pgen.1010219
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