Distinct phosphorylation states of mammalian CaMKIIβ control the induction and maintenance of sleep
The reduced sleep duration previously observed in Camk2b knockout mice revealed a role for Ca2+/calmodulin-dependent protein kinase II (CaMKII)β as a sleep-promoting kinase. However, the underlying mechanism by which CaMKIIβ supports sleep regulation is largely unknown. Here, we demonstrate that act...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2022-10-01
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| Series: | PLoS Biology |
| Online Access: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9531794/?tool=EBI |
| _version_ | 1828107341472464896 |
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| author | Daisuke Tone Koji L. Ode Qianhui Zhang Hiroshi Fujishima Rikuhiro G. Yamada Yoshiki Nagashima Katsuhiko Matsumoto Zhiqing Wen Shota Y. Yoshida Tomoki T. Mitani Yuki Arisato Rei-ichiro Ohno Maki Ukai-Tadenuma Junko Yoshida Garçon Mari Kaneko Shoi Shi Hideki Ukai Kazunari Miyamichi Takashi Okada Kenta Sumiyama Hiroshi Kiyonari Hiroki R. Ueda |
| author_facet | Daisuke Tone Koji L. Ode Qianhui Zhang Hiroshi Fujishima Rikuhiro G. Yamada Yoshiki Nagashima Katsuhiko Matsumoto Zhiqing Wen Shota Y. Yoshida Tomoki T. Mitani Yuki Arisato Rei-ichiro Ohno Maki Ukai-Tadenuma Junko Yoshida Garçon Mari Kaneko Shoi Shi Hideki Ukai Kazunari Miyamichi Takashi Okada Kenta Sumiyama Hiroshi Kiyonari Hiroki R. Ueda |
| author_sort | Daisuke Tone |
| collection | DOAJ |
| description | The reduced sleep duration previously observed in Camk2b knockout mice revealed a role for Ca2+/calmodulin-dependent protein kinase II (CaMKII)β as a sleep-promoting kinase. However, the underlying mechanism by which CaMKIIβ supports sleep regulation is largely unknown. Here, we demonstrate that activation or inhibition of CaMKIIβ can increase or decrease sleep duration in mice by almost 2-fold, supporting the role of CaMKIIβ as a core sleep regulator in mammals. Importantly, we show that this sleep regulation depends on the kinase activity of CaMKIIβ. A CaMKIIβ mutant mimicking the constitutive-active (auto)phosphorylation state promotes the transition from awake state to sleep state, while mutants mimicking subsequent multisite (auto)phosphorylation states suppress the transition from sleep state to awake state. These results suggest that the phosphorylation states of CaMKIIβ differently control sleep induction and maintenance processes, leading us to propose a “phosphorylation hypothesis of sleep” for the molecular control of sleep in mammals. |
| first_indexed | 2024-04-11T10:29:40Z |
| format | Article |
| id | doaj.art-c422f3677b6849ceb5f7d2c1b49d07ab |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-04-11T10:29:40Z |
| publishDate | 2022-10-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-c422f3677b6849ceb5f7d2c1b49d07ab2022-12-22T04:29:28ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852022-10-012010Distinct phosphorylation states of mammalian CaMKIIβ control the induction and maintenance of sleepDaisuke ToneKoji L. OdeQianhui ZhangHiroshi FujishimaRikuhiro G. YamadaYoshiki NagashimaKatsuhiko MatsumotoZhiqing WenShota Y. YoshidaTomoki T. MitaniYuki ArisatoRei-ichiro OhnoMaki Ukai-TadenumaJunko Yoshida GarçonMari KanekoShoi ShiHideki UkaiKazunari MiyamichiTakashi OkadaKenta SumiyamaHiroshi KiyonariHiroki R. UedaThe reduced sleep duration previously observed in Camk2b knockout mice revealed a role for Ca2+/calmodulin-dependent protein kinase II (CaMKII)β as a sleep-promoting kinase. However, the underlying mechanism by which CaMKIIβ supports sleep regulation is largely unknown. Here, we demonstrate that activation or inhibition of CaMKIIβ can increase or decrease sleep duration in mice by almost 2-fold, supporting the role of CaMKIIβ as a core sleep regulator in mammals. Importantly, we show that this sleep regulation depends on the kinase activity of CaMKIIβ. A CaMKIIβ mutant mimicking the constitutive-active (auto)phosphorylation state promotes the transition from awake state to sleep state, while mutants mimicking subsequent multisite (auto)phosphorylation states suppress the transition from sleep state to awake state. These results suggest that the phosphorylation states of CaMKIIβ differently control sleep induction and maintenance processes, leading us to propose a “phosphorylation hypothesis of sleep” for the molecular control of sleep in mammals.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9531794/?tool=EBI |
| spellingShingle | Daisuke Tone Koji L. Ode Qianhui Zhang Hiroshi Fujishima Rikuhiro G. Yamada Yoshiki Nagashima Katsuhiko Matsumoto Zhiqing Wen Shota Y. Yoshida Tomoki T. Mitani Yuki Arisato Rei-ichiro Ohno Maki Ukai-Tadenuma Junko Yoshida Garçon Mari Kaneko Shoi Shi Hideki Ukai Kazunari Miyamichi Takashi Okada Kenta Sumiyama Hiroshi Kiyonari Hiroki R. Ueda Distinct phosphorylation states of mammalian CaMKIIβ control the induction and maintenance of sleep PLoS Biology |
| title | Distinct phosphorylation states of mammalian CaMKIIβ control the induction and maintenance of sleep |
| title_full | Distinct phosphorylation states of mammalian CaMKIIβ control the induction and maintenance of sleep |
| title_fullStr | Distinct phosphorylation states of mammalian CaMKIIβ control the induction and maintenance of sleep |
| title_full_unstemmed | Distinct phosphorylation states of mammalian CaMKIIβ control the induction and maintenance of sleep |
| title_short | Distinct phosphorylation states of mammalian CaMKIIβ control the induction and maintenance of sleep |
| title_sort | distinct phosphorylation states of mammalian camkiiβ control the induction and maintenance of sleep |
| url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9531794/?tool=EBI |
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