Categories: NATURE

Postsynaptic competition between calcineurin and PKA regulates mammalian sleep–wake cycles


  • Diering, G. H. et al. Homer1a drives homeostatic scaling-down of excitatory synapses during sleep. Science 355, 511–515 (2017).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wang, Z. et al. Quantitative phosphoproteomic analysis of the molecular substrates of sleep need. Nature 558, 435–439 (2018).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bruning, F. et al. Sleep–wake cycles drive daily dynamics of synaptic phosphorylation. Science 366, eaav3617 (2019).

    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Ode, K. L. & Ueda, H. R. Phosphorylation hypothesis of sleep. Front. Psychol. 11, 575328 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tatsuki, F. et al. Involvement of Ca2+-dependent hyperpolarization in sleep duration in mammals. Neuron 90, 70–85 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Funato, H. et al. Forward-genetics analysis of sleep in randomly mutagenized mice. Nature 539, 378–383 (2016).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mikhail, C., Vaucher, A., Jimenez, S. & Tafti, M. ERK signaling pathway regulates sleep duration through activity-induced gene expression during wakefulness. Sci. Signal. 10, eaai9219 (2017).

    Article 
    PubMed 

    Google Scholar
     

  • Hendricks, J. C. et al. A non-circadian role for cAMP signaling and CREB activity in Drosophila rest homeostasis. Nat. Neurosci. 4, 1108–1115 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Crocker, A., Shahidullah, M., Levitan, I. B. & Sehgal, A. Identification of a neural circuit that underlies the effects of octopamine on sleep:wake behavior. Neuron 65, 670–681 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Crocker, A. & Sehgal, A. Octopamine regulates sleep in Drosophila through protein kinase A-dependent mechanisms. J. Neurosci. 28, 9377–9385 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wu, M. N. et al. The effects of caffeine on sleep in Drosophila require PKA activity, but not the adenosine receptor. J. Neurosci. 29, 11029–11037 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Joiner, W. J., Crocker, A., White, B. H. & Sehgal, A. Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441, 757–760 (2006).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Hellman, K., Hernandez, P., Park, A. & Abel, T. Genetic evidence for a role for protein kinase A in the maintenance of sleep and thalamocortical oscillations. Sleep 33, 19–28 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Park, M. et al. Loss of the conserved PKA sites of SIK1 and SIK2 increases sleep need. Sci. Rep. 10, 8676 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Honda, T. et al. A single phosphorylation site of SIK3 regulates daily sleep amounts and sleep need in mice. Proc. Natl Acad. Sci. USA 115, 10458–10463 (2018).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tomita, J. et al. Pan-neuronal knockdown of calcineurin reduces sleep in the fruit fly, Drosophila melanogaster. J. Neurosci. 31, 13137–13146 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nakai, Y. et al. Calcineurin and its regulator sra/DSCR1 are essential for sleep in Drosophila. J. Neurosci. 31, 12759–12766 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sunagawa, G. A. et al. Mammalian reverse genetics without crossing reveals Nr3a as a short-sleeper gene. Cell Rep. 14, 662–677 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Amieux, P. S. et al. Increased basal cAMP-dependent protein kinase activity inhibits the formation of mesoderm-derived structures in the developing mouse embryo. J. Biol. Chem. 277, 27294–27304 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Skalhegg, B. S. et al. Mutation of the Cα subunit of PKA leads to growth retardation and sperm dysfunction. Mol. Endocrinol. 16, 630–639 (2002).

    CAS 
    PubMed 

    Google Scholar
     

  • Franken, P., Chollet, D. & Tafti, M. The homeostatic regulation of sleep need is under genetic control. J. Neurosci. 21, 2610–2621 (2001).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Manschwetus, J. T. et al. A stapled peptide mimic of the pseudosubstrate inhibitor PKI inhibits protein kinase A. Molecules 24, 1567 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tone, D. et al. Distinct phosphorylation states of mammalian CaMKIIβ control the induction and maintenance of sleep. PLoS Biol. 20, e3001813 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nathanson, J. L., Yanagawa, Y., Obata, K. & Callaway, E. M. Preferential labeling of inhibitory and excitatory cortical neurons by endogenous tropism of adeno-associated virus and lentivirus vectors. Neuroscience 161, 441–450 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Scott, J. D., Glaccum, M. B., Fischer, E. H. & Krebs, E. G. Primary-structure requirements for inhibition by the heat-stable inhibitor of the cAMP-dependent protein kinase. Proc. Natl Acad. Sci. USA 83, 1613–1616 (1986).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Willis, B. S., Niswender, C. M., Su, T., Amieux, P. S. & McKnight, G. S. Cell-type specific expression of a dominant negative PKA mutation in mice. PLoS ONE 6, e18772 (2011).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Clegg, C. H., Correll, L. A., Cadd, G. G. & McKnight, G. S. Inhibition of intracellular cAMP-dependent protein kinase using mutant genes of the regulatory type I subunit. J. Biol. Chem. 262, 13111–13119 (1987).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Orellana, S. A. & McKnight, G. S. Mutations in the catalytic subunit of cAMP-dependent protein kinase result in unregulated biological activity. Proc. Natl Acad. Sci. USA 89, 4726–4730 (1992).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Esteban, J. A. et al. PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat. Neurosci. 6, 136–143 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gross, G. G. et al. Recombinant probes for visualizing endogenous synaptic proteins in living neurons. Neuron 78, 971–985 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, H. et al. In vivo selection of kinase-responsive RNA elements controlling alternative splicing. J. Biol. Chem. 284, 16191–16201 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Goebbels, S. et al. Genetic targeting of principal neurons in neocortex and hippocampus of NEX-Cre mice. Genesis 44, 611–621 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mansuy, I. M. & Shenolikar, S. Protein serine/threonine phosphatases in neuronal plasticity and disorders of learning and memory. Trends Neurosci. 29, 679–686 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sents, W. et al. PP2A inactivation mediated by PPP2R4 haploinsufficiency promotes cancer development. Cancer Res. 77, 6825–6837 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Blake, J. A. et al. Mouse Genome Database (MGD): knowledgebase for mouse–human comparative biology. Nucleic Acids Res. 49, D981–D987 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Allen, P. B., Ouimet, C. C. & Greengard, P. Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc. Natl Acad. Sci. USA 94, 9956–9961 (1997).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, J., Zhang, Z., Brew, K. & Lee, E. Y. Mutational analysis of the catalytic subunit of muscle protein phosphatase-1. Biochemistry 35, 6276–6282 (1996).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Berndt, N., Dohadwala, M. & Liu, C. W. Constitutively active protein phosphatase 1α causes Rb-dependent G1 arrest in human cancer cells. Curr. Biol. 7, 375–386 (1997).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Cohen, P. T. Protein phosphatase 1—targeted in many directions. J. Cell Sci. 115, 241–256 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Huang, H. B. et al. Characterization of the inhibition of protein phosphatase-1 by DARPP-32 and inhibitor-2. J. Biol. Chem. 274, 7870–7878 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Eto, M., Karginov, A. & Brautigan, D. L. A novel phosphoprotein inhibitor of protein type-1 phosphatase holoenzymes. Biochemistry 38, 16952–16957 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang, G. et al. Somatic genetics analysis of sleep in adult mice. J. Neurosci. 42, 5617–5640 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • O’Keefe, S. J., Tamura, J., Kincaid, R. L., Tocci, M. J. & O’Neill, E. A. FK-506- and CsA-sensitive activation of the interleukin-2 promoter by calcineurin. Nature 357, 692–694 (1992).

    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Shibasaki, F., Price, E. R., Milan, D. & McKeon, F. Role of kinases and the phosphatase calcineurin in the nuclear shuttling of transcription factor NF-AT4. Nature 382, 370–373 (1996).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Miyakawa, T. et al. Conditional calcineurin knockout mice exhibit multiple abnormal behaviors related to schizophrenia. Proc. Natl Acad. Sci. USA 100, 8987–8992 (2003).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Saper, C. B. & Fuller, P. M. Wake–sleep circuitry: an overview. Curr. Opin. Neurobiol. 44, 186–192 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Diekelmann, S. & Born, J. The memory function of sleep. Nat. Rev. Neurosci. 11, 114–126 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Foley, K., McKee, C., Nairn, A. C. & Xia, H. Regulation of synaptic transmission and plasticity by protein phosphatase 1. J. Neurosci. 41, 3040–3050 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cho, J. et al. Fear memory consolidation in sleep requires protein kinase A. Learn. Mem. 25, 241–246 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Thiel, G., Greengard, P. & Sudhof, T. C. Characterization of tissue-specific transcription by the human synapsin I gene promoter. Proc. Natl Acad. Sci. USA 88, 3431–3435 (1991).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Villa, K. L. et al. Inhibitory synapses are repeatedly assembled and removed at persistent sites in vivo. Neuron 89, 756–769 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nishiyama, J., Mikuni, T. & Yasuda, R. Virus-mediated genome editing via homology-directed repair in mitotic and postmitotic cells in mammalian brain. Neuron 96, 755–768.e5 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Niwa, Y. et al. Muscarinic acetylcholine receptors Chrm1 and Chrm3 are essential for REM sleep. Cell Rep. 24, 2231–2247.e7 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yoshida, K. et al. Leak potassium channels regulate sleep duration. Proc. Natl Acad. Sci. USA 115, E9459–E9468 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Naito, Y., Hino, K., Bono, H. & Ui-Tei, K. CRISPRdirect: software for designing CRISPR/Cas guide RNA with reduced off-target sites. Bioinformatics 31, 1120–1123 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Cho, S. W., Kim, S., Kim, J. M. & Kim, J. S. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31, 230–232 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sumiyama, K., Kawakami, K. & Yagita, K. A simple and highly efficient transgenesis method in mice with the Tol2 transposon system and cytoplasmic microinjection. Genomics 95, 306–311 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tsujino, K. et al. Establishment of TSH β real-time monitoring system in mammalian photoperiodism. Genes Cells 18, 575–588 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Challis, R. C. et al. Systemic AAV vectors for widespread and targeted gene delivery in rodents. Nat. Protoc. 14, 379–414 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chan, K. Y. et al. Engineered AAVs for efficient noninvasive gene delivery to the central and peripheral nervous systems. Nat. Neurosci. 20, 1172–1179 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yamada, R. G., Matsuzawa, K., Ode, K. L. & Ueda, H. R. An automated sleep staging tool based on simple statistical features of mice electroencephalography (EEG) and electromyography (EMG) data. Eur. J. Neurosci. 60, 5467–5486 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Virtanen, P. et al. SciPy 1.0: fundamental algorithms for scientific computing in Python. Nat. Methods 17, 261–272 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ukai, H., Kiyonari, H. & Ueda, H. R. Production of knock-in mice in a single generation from embryonic stem cells. Nat. Protoc. 12, 2513–2530 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ode, K. L. et al. Knockout–rescue embryonic stem cell-derived mouse reveals circadian-period control by quality and quantity of CRY1. Mol. Cell 65, 176–190 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kiyonari, H., Kaneko, M., Abe, S. & Aizawa, S. Three inhibitors of FGF receptor, ERK, and GSK3 establishes germline-competent embryonic stem cells of C57BL/6N mouse strain with high efficiency and stability. Genesis 48, 317–327 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sato, H., Amagai, K., Shimizukawa, R. & Tamai, Y. Stable generation of serum- and feeder-free embryonic stem cell-derived mice with full germline-competency by using a GSK3 specific inhibitor. Genesis 47, 414–422 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     



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