Sustained microglial activation and accelerated elimination of dendritic spines during acute sleep deprivation and restoration

Junru Liu; Yanyi Xu; Yuxin Ji; Kemin Li; Shuang Wang; Bixi Zhao; Jiayi Ruan; Nicholas S. Foulkes; Shengxiang Zhang; Haiyu Zhao

doi:10.59717/j.xinn-life.2023.100037

The Innovation Life > 2023 Vol. 1 > No. 3 > 100037

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Sustained microglial activation and accelerated elimination of dendritic spines during acute sleep deprivation and restoration

1.
School of Life Sciences, Gansu Key Laboratory of Biomonitoring and Bioremediation for Environmental Pollution, Lanzhou University, Lanzhou 730000, China
2.
Institute of Biological and Chemical Systems, Biological Information Processing, Karlsruhe Institute of Technology, Eggenstein-Leopoldshafen 76344, Germany
3.
University of Science and Technology of China, Hefei 230026, China
4.
Lead contact
5.
These authors contributed equally

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Corresponding authors: nicholas.foulkes@kit.edu (N.F.); sxzhang@lzu.edu.cn (S.Z.); zhaohy@lzu.edu.cn (H.Z.)
Received Date: August 30, 2023

Accepted Date: November 21, 2023

Published Online: November 27, 2023

The Innovation Life 1(3), https://doi.org/10.59717/j.xinn-life.2023.100037 | Cite this article

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PUBLIC SUMMARY

PUBLIC SUMMARY
1. Microglial de-ramification occurs during acute sleep deprivation and restoration.
  
  Reduced microglial processes mobility during sleep deprivation and restoration.
  
  Acute sleep deprivation and restoration increase the phagocytosis of microglia.
  
  Acute sleep deprivation and restoration induce elimination of dendritic spines.
  
  A substantial number of metabolites and pathways fail to recover after recovery sleep.

ABSTRACT

ABSTRACT

Sleep is a fundamental physiological condition strongly regulated by a variety of neuroanatomical and neurochemical systems. Recent studies have indicated that catch-up sleep falls short of effectiveness to counteract the negative consequences of sleep debt however, the underlying mechanisms remain poorly understood. In this study, by using various transgenic fluorescent mouse models as well as techniques including intravital two-photon imaging and immunofluorescence staining of brain sections, we have documented morphological and functional changes of microglia during acute sleep deprivation (ASD) and subsequent short-term recovery sleep (RS). In these cerebral resident immune cells, we observed sustained microglial de-ramification, reduction of process motility and enhancement of microglial phagocytosis across brain regions. Given the intimate connections between microglia activity and neuronal plasticity, we also investigated synaptic plasticity and demonstrated an accelerated elimination of dendritic spines during both ASD and subsequent RS. Furthermore, untargeted metabolomic analyses revealed extensive whole-brain metabolic changes during ASD, and that a substantial number of metabolites and pathways failed to recover within a short period of RS. It is tempting to speculate that the disturbed cerebral metabolic homeostasis contributes to the sustained microglial activation and accelerated elimination of dendritic spines during this process. This study reveals the adverse effects of sleep loss on neuroimmunomodulation and neuronal plasticity, and implicates potential mechanisms underlying how irregular sleep schedules lead to neurological disorders.

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REFERENCES

[1]	Karmanova, I.G. and Lazarev, S.G. (1979). Stages of sleep evolution (facts and hypotheses). Waking Sleeping 3 : 137−147. View in Article Google Scholar
[2]	Cappuccio, F.P., D’Elia, L., Strazzullo, P., et al. (2010). Quantity and quality of sleep and incidence of type 2 diabetes: A systematic review and meta-analysis. Diabetes Care 33 : 414−420. DOI: 10.2337/dc09-1124. View in Article Google Scholar
[3]	Huang, W., Ramsey, K.M., Marcheva, B., and Bass, J. (2011). Circadian rhythms, sleep, and metabolism. J. Clin. Invest. 121 : 2133−2141. DOI: 10.1172/JCI46043. View in Article Google Scholar
[4]	Romero-Corral, A., Caples, S.M., Lopez-Jimenez, F., and Somers, V.K. (2010). Interactions between obesity and obstructive sleep apnea: Implications for treatment. Chest 137 : 711−719. DOI: 10.1378/chest.09-0360. View in Article Google Scholar
[5]	Nagai, M., Hoshide, S., and Kario, K. (2010). Sleep duration as a risk factor for cardiovascular disease- a review of the recent literature. Curr. Cardiol. Rev. 6 : 54−61. DOI: 10.2174/157340310790231635. View in Article Google Scholar
[6]	Miller, M.A. (2015). The role of sleep and sleep disorders in the development, diagnosis, and management of neurocognitive disorders. Front. Neurol. 6 : 224. DOI: 10.3389/fneur.2015.00224. View in Article Google Scholar
[7]	Raven, F., Van der Zee, E.A., Meerlo, P., and Havekes, R. (2018). The role of sleep in regulating structural plasticity and synaptic strength: Implications for memory and cognitive function. Sleep Med. Rev. 39 : 3−11. DOI: 10.1016/j.smrv.2017.05.002. View in Article Google Scholar
[8]	Bolin, D.J. (2019). Sleep deprivation and its contribution to mood and performance deterioration in college athletes. Curr. Sports Med. Rep. 18 : 305−310. DOI: 10.1249/JSR.0000000000000621. View in Article Google Scholar
[9]	Lewis, K.S., Gordon-Smith, K., Forty, L., et al. (2017). Sleep loss as a trigger of mood episodes in bipolar disorder: Individual differences based on diagnostic subtype and gender. Br. J. Psychiatry 211 : 169−174. DOI: 10.1192/bjp.bp.117.202259. View in Article Google Scholar
[10]	Musiek, E.S., and Holtzman, D.M. (2016). Mechanisms linking circadian clocks, sleep, and neurodegeneration. Science 354 : 1004−1008. DOI: 10.1126/science.aah4968. View in Article Google Scholar
[11]	Puentes-Mestril, C., and Aton, S.J. (2017). Linking network activity to synaptic plasticity during sleep: Hypotheses and recent data. Front. Neural Circuits 11 : 61. DOI: 10.3389/fncir.2017.00061. View in Article Google Scholar
[12]	Puentes-Mestril, C., Roach, J., Niethard, N., et al. (2019). How rhythms of the sleeping brain tune memory and synaptic plasticity. Sleep 42 : zsz095. DOI: 10.1093/sleep/zsz095. View in Article Google Scholar
[13]	Thomas, C.W., Guillaumin, M.C.C., McKillop, L.E., et al. (2020). Global sleep homeostasis reflects temporally and spatially integrated local cortical neuronal activity. eLife 9 : 1−25. DOI: 10.7554/eLife.54148. View in Article Google Scholar
[14]	Delorme, J., Wang, L., Kuhn, F.R., et al. (2021). Sleep loss drives acetylcholine- And somatostatin interneuron-mediated gating of hippocampal activity to inhibit memory consolidation. Proc. Natl. Acad. Sci. USA 118 : e2019318118. DOI: 10.1073/pnas.2019318118. View in Article Google Scholar
[15]	Lyons, L.C., Chatterjee, S., Vanrobaeys, Y., et al. (2020). Translational changes induced by acute sleep deprivation uncovered by TRAP-Seq. Mol. Brain. 13 : 165. DOI: 10.1186/s13041-020-00702-5. View in Article Google Scholar
[16]	Noya, S.B., Colameo, D., Brüning, F., et al. (2019). The forebrain synaptic transcriptome is organized by clocks but its proteome is driven by sleep. Science 366 : eaav2642. DOI: 10.1126/science.aav2642. View in Article Google Scholar
[17]	Delorme, J., Wang, L., Kodoth, V., et al. (2021). Hippocampal neurons’ cytosolic and membrane-bound ribosomal transcript profiles are differentially regulated by learning and subsequent sleep. Proc. Natl. Acad. Sci. USA 118 : e2108534118. DOI: 10.1073/pnas.2108534118. View in Article Google Scholar
[18]	Li, Q., and Barres, B.A. (2018). Microglia and macrophages in brain homeostasis and disease. Nat. Rev. Immunol. 18 : 225−242. DOI: 10.1038/nri.2017.125. View in Article Google Scholar
[19]	Butovsky, O. and Weiner, H.L. (2018). Microglial signatures and their role in health and disease. Nat. Rev. Neurosci. 19 : 622−635. DOI: 10.1038/s41583-018-0057-5. View in Article Google Scholar
[20]	Corsi, G., Picard, K., di Castro, M.A., et al. (2022). Microglia modulate hippocampal synaptic transmission and sleep duration along the light/dark cycle. Glia 70 : 89−105. DOI: 10.1002/glia.24090. View in Article Google Scholar
[21]	Deurveilher, S., Golovin, T., Hall, S., and Semba, K. (2021). Microglia dynamics in sleep/wake states and in response to sleep loss. Neurochem. Int. 143 : 104944. DOI: 10.1016/j.neuint.2020.104944. View in Article Google Scholar
[22]	Wadhwa, M., Kumari, P., Chauhan, G., et al. (2017). Sleep deprivation induces spatial memory impairment by altered hippocampus neuroinflammatory responses and glial cells activation in rats. J. Neuroimmunol. 312 : 38−48. DOI: 10.1016/j.jneuroim.2017.09.003. View in Article Google Scholar
[23]	Bellesi, M., Vivo, L. De., Chini, M., et al. (2017). Sleep loss promotes astrocytic phagocytosis and microglial activation in mouse cerebral cortex. J. Neurosci. 37 : 5263−5273. DOI: 10.1523/JNEUROSCI.3981-16.2017. View in Article Google Scholar
[24]	Wadhwa, M., Prabhakar, A., Ray, K., et al. (2017). Inhibiting the microglia activation improves the spatial memory and adult neurogenesis in rat hippocampus during 48 h of sleep deprivation. J. Neuroinflammation. 14 : 222. DOI: 10.1186/s12974-017-0998-z. View in Article Google Scholar
[25]	Wisor, J.P., Schmidt, M.A., and Clegern, W.C. (2011). Evidence for neuroinflammatory and microglial changes in the cerebral response to sleep loss. Sleep. 34, 261−272. DOI: 10.1093/sleep/34.3.261. View in Article CrossRef Google Scholar
[26]	Manchanda, S., Singh, H., Kaur, T., and Kaur, G. (2018). Low-grade neuroinflammation due to chronic sleep deprivation results in anxiety and learning and memory impairments. Mol. Cell Biochem. 449 : 63−72. DOI: 10.1007/s11010-018-3343-7. View in Article Google Scholar
[27]	Zielinski, M.R., Kim, Y., Karpova, S.A., et al. (2014). Chronic sleep restriction elevates brain interleukin-1 beta and tumor necrosis factor-alpha and attenuates brain-derived neurotrophic factor expression. Neurosci. Lett. 580 : 27−31. DOI: 10.1016/j.neulet.2014.07.043. View in Article Google Scholar
[28]	Hsu, J.C., Lee, Y.S., Chang, C.N., et al. (2003). Sleep deprivation inhibits expression of NADPH-d and NOS while activating microglia and astroglia in the rat hippocampus. Cells Tissues Organs 173 : 242−254. DOI: 10.1159/000070380. View in Article Google Scholar
[29]	Neniskyte, U., and Gross, C.T. (2017). Errant gardeners: Glial-cell-dependent synaptic pruning and neurodevelopmental disorders. Nat. Rev. Neurosci. 18 : 658−670. DOI: 10.1038/nrn.2017.110. View in Article Google Scholar
[30]	Mallya, A.P., Wang, H.D., Lee, H.NR., and Deutch, A.Y. (2019). Microglial Pruning of Synapses in the Prefrontal Cortex during Adolescence Cereb. Cortex 29 : 1634−1643. DOI: 10.1093/cercor/bhy061. View in Article Google Scholar
[31]	Kopec, A.M., Smith, C.J., Ayre, N.R., et al. (2018). Microglial dopamine receptor elimination defines sex-specific nucleus accumbens development and social behavior in adolescent rats. Nat. Commun. 9 : 3769. DOI: 10.1038/s41467-018-06118-z. View in Article Google Scholar
[32]	Stowell, R.D., Sipe, G.O., Dawes, R.P., et al. (2019). Noradrenergic signaling in the wakeful state inhibits microglial surveillance and synaptic plasticity in the mouse visual cortex. Nat. Neurosci. 22 : 1782−1792. DOI: 10.1038/s41593-019-0514-0. View in Article Google Scholar
[33]	Liu, Y.U., Ying, Y., Li, Y., et al. (2019). Neuronal network activity controls microglial process surveillance in awake mice via norepinephrine signaling. Nat. Neurosci. 22 : 1771−1781. DOI: 10.1038/s41593-019-0511-3. View in Article Google Scholar
[34]	Hristovska, I., Robert, M., Combet, K., et al. (2022). Sleep decreases neuronal activity control of microglial dynamics in mice. Nat. Commun. 13 : 1−15. DOI: 10.1038/s41467-022-34035-9. View in Article Google Scholar
[35]	Nadjar, A., Wigren, H.K.M., and Tremblay, M.E. (2017). Roles of microglial phagocytosis and inflammatory mediators in the pathophysiology of sleep disorders. Front. Cell Neurosci. 11 : 1−11. DOI: 10.3389/fncel.2017.00250. View in Article Google Scholar
[36]	Brüning, F., Noya, S.B., Bange, T., et al. (2019). Sleep-wake cycles drive daily dynamics of synaptic phosphorylation. Science 366 : eaav3617. DOI: 10.1126/science.aav3617. View in Article Google Scholar
[37]	Datta, S. (2010). Cellular and chemical neuroscience of mammalian sleep. Sleep Med. 11 : 431−440. DOI: 10.1016/j.sleep.2010.02.002. View in Article Google Scholar
[38]	Bellesi, M., Bushey, D., Chini, M., et al. (2016). Contribution of sleep to the repair of neuronal DNA double-strand breaks: Evidence from flies and mice. Sci. Rep. 6 : 36804. DOI: 10.1038/srep36804. View in Article Google Scholar
[39]	Vaccaro, A., Kaplan, Dor. Y., Nambara, K., et al. (2020). Sleep loss can cause death through accumulation of reactive oxygen species in the gut. Cell 181 : 1307−1328.e15. DOI: 10.1016/j.cell.2020.04.049. View in Article Google Scholar
[40]	Hines, D.J., Schmitt, L.I., Hines, R.M., et al. (2013). Antidepressant effects of sleep deprivation require astrocyte-dependent adenosine mediated signaling. Transl. Psychiatry 3 : e212−9. DOI: 10.1038/tp.2012.136. View in Article Google Scholar
[41]	Naidoo, N., Davis, J.G., Zhu, J., et al. (2014). Aging and sleep deprivation induce the unfolded protein response in the pancreas: Implications for metabolism. Aging Cell 13 : 131−141. DOI: 10.1111/acel.12158. View in Article Google Scholar
[42]	Dunn, W.B., Broad hurst, D., Begley, P., et al. (2011). Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry. Nat. Protoc. 6: 1060−1083. DOI: 10.1038/nprot.2011.335. View in Article CrossRef Google Scholar
[43]	Want, E.J., Wilson, I.D., Gika, H., et al. (2010). Global metabolic profiling procedures for urine using UPLC-MS. Nat. Protoc. 5: 1005−1018. DOI: 10.1038/nprot.2010.50. View in Article CrossRef Google Scholar
[44]	Wang, J., Zhang, T., Shen, X., et al. (2016). Serum metabolomics for early diagnosis of esophageal squamous cell carcinoma by UHPLC-QTOF/MS. Metabolomics 12: 116. DOI: 10.1007/s11306-016-1050-5. View in Article CrossRef Google Scholar
[45]	Smith, C.A., Want, E.J., O’Maille, G., et al. XCMS: Processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal. Chem. 78: 779−787. DOI: 10.1021/ac051437y. View in Article CrossRef Google Scholar
[46]	Kuhl, C., Tautenhahn, R., Böttcher, C., et al. (). CAMERA: An integrated strategy for compound spectra extraction and annotation of liquid chromatography/mass spectrometry data sets. Anal. Chem. 84(): 283−289. View in Article Google Scholar
[47]	Chong, J., Wishart, D.S., and Xia, J. (2019). Using MetaboAnalyst 4.0 for comprehensive and integrative metabolomics data analysis. Curr. Protoc. Bioinforma. 68: e86. DOI: 10.1002/cpbi.86. View in Article CrossRef Google Scholar
[48]	Zhu, L., Wang, L., Ju, F., et al. (2017). Transient global cerebral ischemia induces rapid and sustained reorganization of synaptic structures. J. Cereb. Blood Flow Metab. 37: 2756−2767. DOI: 10.1177/0271678X16674736. View in Article CrossRef Google Scholar
[49]	Yang, G., Pan, F., Parkhurst, C.N., et al. (2010). Thinned-skull cranial window technique for long-term imaging of the cortex in live mice. Nat. Protoc. 5: 213−220. View in Article Google Scholar
[50]	Zuo, Y., Yang, G., Kwon, E., et al. (2005). Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature 436: 261−265. DOI: 10.1038/nature03715. View in Article CrossRef Google Scholar
[51]	Ju, F., Ran, Y., Zhu, L., et al. (2018). Increased BBB permeability enhances activation of microglia and exacerbates loss of dendritic spines after transient global cerebral ischemia. Front. Cell Neurosci. 12: 1−14. DOI: 10.3389/fncel.2018.00236. View in Article CrossRef Google Scholar
[52]	Sipe, G.O., Lowery, R.L., Tremblay, M., et al. (2016). Microglial P2Y12 is necessary for synaptic plasticity in mouse visual cortex. Nat. Commun. 7: 10905. DOI: 10.1038/ncomms10905. View in Article CrossRef Google Scholar
[53]	Liu, Y.U., Ying, Y., Li, Y., et al. (2019). Neuronal network activity controls microglial process surveillance in awake mice via norepinephrine signaling. Nat. Neurosci. 22: 1771−1781. DOI: 1038/s41593-019-0511-3. View in Article CrossRef Google Scholar
[54]	Morrison, H.W. and Filosa, J.A. (2013). A quantitative spatiotemporal analysis of microglia morphology during ischemic stroke and reperfusion. J. Neuroinflammation 10: 1−20. DOI: 10.1186/ 1742-2094-10-4. View in Article CrossRef Google Scholar
[55]	York, E.M., Bernier, L.P., and MacVicar, B.A. (2018). Microglial modulation of neuronal activity in the healthy brain. Dev Neurobiol. 78 : 593−603. DOI: 10.1002/dneu.22571. View in Article Google Scholar
[56]	Wake, H., Horiuchi, H., Kato, D., et al. (2019). Physiological implications of microglia–synapse interactions. Methods Mol. Biol. 2034 : 69−80. DOI: 10.1007/978-1-4939-9658-2_6. View in Article Google Scholar
[57]	Socodato, R., Portugal, C.C., Domith, I., et al. (2015). c-Src function is necessary and sufficient for triggering microglial cell activation. Glia 63 : 497−511. DOI: 10.1002/glia.22767. View in Article Google Scholar
[58]	Li, T., Pang, S., Yu, Y., et al. (2013). Proliferation of parenchymal microglia is the main source of microgliosis after ischaemic stroke. Brain 136 : 3578−3588. DOI: 10.1093/brain/awt287. View in Article Google Scholar
[59]	Kyrargyri, V., Madry, C., Rifat, A., et al. (2020). P2Y(13) receptors regulate microglial morphology, surveillance, and resting levels of interleukin 1β release. Glia 68 : 328−344. DOI: 10.1002/glia.23719. View in Article Google Scholar
[60]	Kettenmann, H., Kirchhoff, F., and Verkhratsky, A. (2013). Microglia: new roles for the synaptic stripper. Neuron 77 : 10−18. DOI: 10.1016/j.neuron.2012.12.023. View in Article Google Scholar
[61]	Illouz, T., Madar, R., Biragyn, A., and Okun, E. (2019). Restoring microglial and astroglial homeostasis using DNA immunization in a Down Syndrome mouse model. Brain Behav. Immun. 75 : 163−180. DOI: 10.1016/j.bbi.2018.10.004. View in Article Google Scholar
[62]	Korzhevskii, D.E., and Kirik, O.V. (2016). Brain microglia and microglial markers. Neurosci. Behav. Physiol. 46 : 284−290. DOI: 10.1007/s11055-016-0231-z. View in Article Google Scholar
[63]	Liu, Y.J., Spangenberg, E.E., Tang, B., et al. (2021). Microglia elimination increases neural circuit connectivity and activity in adult mouse cortex. J. Neurosci. 41 : 1274−1287. DOI: 10.1523/JNEUROSCI.2140-20.2020. View in Article Google Scholar
[64]	Hong, S., Beja-Glasser, V.F., Nfonoyim, B.M., et al. (2016). Complement and microglia mediate early synapse loss in Alzheimer mouse models. Science 352 : 712−716. DOI: 10.1126/science.aad8373. View in Article Google Scholar
[65]	Wake, H., Moorhouse, A.J., Jinno, S., et al. (2009). Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J Neurosci. 29 : 3974−3980. DOI: 10.1523/JNEUROSCI.4363-08.2009. View in Article Google Scholar
[66]	Tremblay, M.Ě., Lowery, R.L., and Majewska, A.K. (2010). Microglial interactions with synapses are modulated by visual experience. PLoS Biol. 8 : e1000527. DOI: 10.1371/journal.pbio.1000527. View in Article Google Scholar
[67]	Schafer, D.P., Lehrman, E.K., Kautzman, A.G., et al. (2012). Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74 : 691−705. DOI: 10.1016/j.neuron.2012.03.026. View in Article Google Scholar
[68]	Irwin, M.R. (2019). Sleep and inflammation: partners in sickness and in health. Nat. Rev. Immunol. 19 : 702−715. DOI: 10.1038/s41577-019-0190-z. View in Article Google Scholar
[69]	Irwin, M.R. and Opp, M.R. (2017). Sleep health: Reciprocal regulation of sleep and innate immunity. Neuropsychopharmacology 42 : 129−155. DOI: 10.1038/npp.2016.148. View in Article Google Scholar
[70]	Garbarino, S., Lanteri, P., Bragazzi, N.L., et al. (2021). Role of sleep deprivation in immune-related disease risk and outcomes. Commun. Biol. 4 : 1304. DOI: 10.1038/s42003-021-02825-4. View in Article Google Scholar
[71]	Besedovsky, L., Lange, T., and Haack, M. (2019). The sleep-immune crosstalk in health and disease. Physiol. Rev. 99, 1325−1380. DOI: 10.1152/physrev.00010.2018. View in Article Google Scholar
[72]	Bellesi, M., de Vivo, L., Chini, M., et al. (2017). Sleep loss promotes astrocytic phagocytosis and microglial activation in mouse cerebral cortex. J. Neurosci. 37 : 5263−5273. DOI: 10.1523/JNEUROSCI.3981-16.2017. View in Article Google Scholar
[73]	Tuan, L.H. and Lee, L.J. (2019). Microglia-mediated synaptic pruning is impaired in sleep-deprived adolescent mice. Neurobiol. Dis. 130 : 104517. DOI: 10.1016/j.nbd.2019.104517. View in Article Google Scholar
[74]	Xie, Y., Ba, L., Wang, M., et al. (2020). Chronic sleep fragmentation shares similar pathogenesis with neurodegenerative diseases: Endosome-autophagosome-lysosome pathway dysfunction and microglia-mediated neuroinflammation. CNS Neurosci. Ther. 26 : 215−227. DOI: 10.1111/cns.13218. View in Article Google Scholar
[75]	Hall, S., Deurveilher, S., Robertson, G.S., and Semba, K. (2020). Homeostatic state of microglia in a rat model of chronic sleep restriction. Sleep 43 : zsaa108. DOI: 10.1093/sleep/zsaa108. View in Article Google Scholar
[76]	Parhizkar, S., Gent, G., Chen, Y., et al. (2023). Sleep deprivation exacerbates microglial reactivity and Aβ deposition in a TREM2-dependent manner in mice. Sci. Transl. Med. 15 : eade6285. DOI: 10.1126/scitranslmed.ade6285. View in Article Google Scholar
[77]	Zhu, B., Dong, Y., Xu, Z., et al. (2012). Sleep disturbance induces neuroinflammation and impairment of learning and memory. Neurobiol. Dis. 48 : 348−355. DOI: 10.1016/j.nbd.2012.06.022. View in Article Google Scholar
[78]	Yin, M., Chen, Y., Zheng, H., et al. (2017). Assessment of mouse cognitive and anxiety-like behaviors and hippocampal inflammation following a repeated and intermittent paradoxical sleep deprivation procedure. Behav. Brain Res. 321 : 69−78. DOI: 10.1016/j.bbr.2016.12.034. View in Article Google Scholar
[79]	Mishra, I., Pullum, K.B., Eads, K.N., et al. (2022). Peripheral sympathectomy alters neuroinflammatory and microglial responses to sleep fragmentation in female mice. Neuroscience 505 : 111−124. DOI: 10.1016/j.neuroscience.2022.09.022. View in Article Google Scholar
[80]	Faraut, B., Boudjeltia, K.Z., Vanhamme, L., and Kerkhofs, M. (2012). Immune, inflammatory and cardiovascular consequences of sleep restriction and recovery. Sleep Med. Rev. 16 : 137−149. DOI: 10.1016/j.smrv.2011.05.001. View in Article Google Scholar
[81]	Faraut, B., Boudjeltia, K.Z., Dyzma, M., et al. (2011). Benefits of napping and an extended duration of recovery sleep on alertness and immune cells after acute sleep restriction. Brain Behav. Immun. 25 : 16−24. DOI: 10.1016/j.bbi.2010.08.001. View in Article Google Scholar
[82]	Combs, C.K., Karlo, J.C., Kao, S.C., and Landreth, G.E. (2001). beta-Amyloid stimulation of microglia and monocytes results in TNFalpha-dependent expression of inducible nitric oxide synthase and neuronal apoptosis. J. Neurosci. 21 : 1179−1188. DOI: 10.1523/JNEUROSCI.21-04-01179.2001. View in Article Google Scholar
[83]	Perry, V.H., and Holmes, C. (2014). Microglial priming in neurodegenerative disease. Nat. Rev. Neurol. 10 : 217−224. DOI: 10.1038/nrneurol.2014.38. View in Article Google Scholar
[84]	Hu, Y., Cao, K., Wang, F., et al. (2022). Dual roles of hexokinase 2 in shaping microglial function by gating glycolytic flux and mitochondrial activity. Nat. Metab. 4 : 1756−1774. DOI: 10.1038/s42255-022-00707-5. View in Article Google Scholar
[85]	Miyamoto, A., Wake, H., Ishikawa, A.W., et al. (2016). Microglia contact induces synapse formation in developing somatosensory cortex. Nat. Commun. 7 : 12540. DOI: 10.1038/ncomms12540. View in Article Google Scholar
[86]	Akiyoshi, R., Wake, H., Kato, D., et al. (2018). Microglia enhance synapse activity to promote local network synchronization. eNeuro. 5 : ENEURO.0088−18.2018. DOI: 10.1523/ENEURO.0088-18.2018. View in Article Google Scholar
[87]	Eyo, U.B., Peng, J., Swiatkowski, P., et al. (2014). Neuronal hyperactivity recruits microglial processes via neuronal NMDA receptors and microglial P2Y12 receptors after status epilepticus. J. Neurosci. 34 : 10528−10540. DOI: 10.1523/JNEUROSCI.0416-14.2014. View in Article Google Scholar
[88]	Lou, N., Takano, T., Pei, Y., et al. (2016). Purinergic receptor P2RY12-dependent microglial closure of the injured blood-brain barrier. Proc. Natl. Acad. Sci. USA. 113 : 1074−1079. DOI: 10.1073/pnas.1520398113. View in Article Google Scholar
[89]	Paolicelli, R.C., Bolasco, G., Pagani, F., et al. (2011). Synaptic pruning by microglia is necessary for normal brain development. Science 333 : 1456−1458. DOI: 10.1126/science.1202529. View in Article Google Scholar
[90]	Filipello, F., Morini, R., Corradini, I., et al. (2018). The microglial innate immune receptor trem2 is required for synapse elimination and normal brain connectivity. Immunity 48 : 979−991. DOI: 10.1016/j.immuni.2018.04.016. View in Article Google Scholar
[91]	Wang, C., Yue, H., Hu, Z., et al. (2020). Microglia mediate forgetting via complement-dependent synaptic elimination. Science 367 : 688−694. DOI: 10.1126/science.aaz2288. View in Article Google Scholar
[92]	Damisah, E.C., Hill, R.A., Rai, A., et al. (2020). Astrocytes and microglia play orchestrated roles and respect phagocytic territories during neuronal corpse removal in vivo. Sci. Adv. 6 : eaba3239. DOI: 10.1126/sciadv.aba3239. View in Article Google Scholar
[93]	Salvany, S., Casanovas, A., Piedrafita, L., et al. (2021). Microglial recruitment and mechanisms involved in the disruption of afferent synaptic terminals on spinal cord motor neurons after acute peripheral nerve injury. Glia 69 : 1216−1240. DOI: 10.1002/glia.23959. View in Article Google Scholar
[94]	Zhu, M., Xiao, B., Xue, T., et al. (2023). Cdc42GAP deficiency contributes to the Alzheimer’s disease phenotype. Brain 146 : 4350−4365. DOI: 10.1093/brain/awad184. View in Article Google Scholar
[95]	Raamsdonk, L.M., Teusink, B., Broadhurst, D., et al. (2001). A functional genomics strategy that uses metabolome data to reveal the phenotype of silent mutations. Nat. Biotechnol. 19 : 45−50. DOI: 10.1038/83496. View in Article Google Scholar
[96]	Giskeødegård, G.F., Davies, S.K., Revell, V.L., et al. (2015). Diurnal rhythms in the human urine metabolome during sleep and total sleep deprivation. Sci. Rep. 5 : 14843. DOI: 10.1038/srep14843. View in Article Google Scholar
[97]	Davies, S.K., Ang, J.E., Revell, V.L., et al. (2014). Effect of sleep deprivation on the human metabolome. Proc. Natl. Acad. Sci. USA. 111 : 10761−10766. DOI: 10.1073/pnas.1402663111. View in Article Google Scholar
[98]	Akazawa, N., Kobayashi, N., Nakamura, Y., et al. (2019). Effect of sleep efficiency on salivary metabolite profile and cognitive function during exercise in volleyball athletes. Eur. J. Appl. Physiol. 119 : 2215−2223. DOI: 10.1007/s00421-019-04205-7. View in Article Google Scholar
[99]	Liu, D., Wang, Q., Li, Y., et al. (2023). Fructus gardeniae ameliorates anxiety-like behaviors induced by sleep deprivation via regulating hippocampal metabolomics and gut microbiota. Front. Cell Infect. Microbiol. 13 : 1167312. DOI: 10.3389/fcimb.2023.1167312. View in Article Google Scholar
[100]	An, Y., Varma, V.R., Varma, S., et al. (2018). Evidence for brain glucose dysregulation in Alzheimer’s disease. Alzheimers Dement. 14 : 318−329. DOI: 10.1016/j.jalz.2017.09.011. View in Article Google Scholar
[101]	Alam, Z.I., Jenner, A., Daniel, S.E., et al. (1997). Oxidative DNA damage in the parkinsonian brain: an apparent selective increase in 8-hydroxyguanine levels in substantia nigra. J. Neurochem. 69 : 1196−1203. DOI: 10.1046/j.1471-4159.1997.69031196.x. View in Article Google Scholar
[102]	Markesbery, W.R., and Lovell, M.A. (2006). DNA oxidation in Alzheimer’s disease. Antioxid Redox Signal 8 : 2039−2045. DOI: 10.1089/ars.2006.8.2039. View in Article Google Scholar
[103]	Barbieri, I., and Kouzarides, T. (2020). Role of RNA modifications in cancer. Nat. Rev. Cancer 20 : 303−322. DOI: 10.1038/s41568-020-0253-2. View in Article Google Scholar
[104]	Sheng, Z., Oka, S., Tsuchimoto, D., et al. (2012). 8-Oxoguanine causes neurodegeneration during MUTYH-mediated DNA base excision repair. J. Clin. Invest. 122 : 4344−4361. DOI: 10.1172/JCI65053. View in Article Google Scholar
[105]	Takahashi, T. and Suzuki, T. (2012). Role of sulfatide in normal and pathological cells and tissues. J. Lipid Res. 53 : 1437−1450. DOI: 10.1194/jlr.R026682. View in Article Google Scholar
[106]	Tsukahara, T., Matsuda, Y., and Haniu, H. (2017). Lysophospholipid-related diseases and pparγ signaling pathway. Int. J. Mol. Sci. 18 : 2730. DOI: 10.3390/ijms18122730. View in Article Google Scholar
[107]	Schilcher, I., Ledinski, G., Radulović, S., et al. (2019). Endothelial lipase increases antioxidative capacity of high-density lipoprotein. Biochim. Biophys. acta Mol. cell Biol. lipids 1864 : 1363−1374. DOI: 10.1016/j.bbalip.2019.06.011. View in Article Google Scholar
[108]	Radu, C.G., Yang, L.V., Riedinger, M., et al. (2004). T cell chemotaxis to lysophosphatidylcholine through the G2A receptor. Proc. Natl. Acad. Sci. USA 101 : 245−250. DOI: 10.1073/pnas.2536801100. View in Article Google Scholar
[109]	Ngwenya, B.Z. and Yamamoto, N. (1985). Activation of peritoneal macrophages by lysophosphatidylcholine. Biochim. Biophys. Acta 839 : 9−15. DOI: 10.1016/0304-4165(85)90175-8. View in Article Google Scholar
[110]	Qin, X., Qiu, C., and Zhao, L. (2014). Lysophosphatidylcholine perpetuates macrophage polarization toward classically activated phenotype in inflammation. Cell Immunol. 289 : 185−190. DOI: 10.1016/j.cellimm.2014.04.010. View in Article Google Scholar

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Liu J., Xu Y., Ji Y., et al., (2023). Sustained microglial activation and accelerated elimination of dendritic spines during acute sleep deprivation and restoration. The Innovation Life 1(3), 100037. https://doi.org/10.59717/j.xinn-life.2023.100037

Liu J., Xu Y., Ji Y., et al., (2023). Sustained microglial activation and accelerated elimination of dendritic spines during acute sleep deprivation and restoration. The Innovation Life 1(3), 100037. https://doi.org/10.59717/j.xinn-life.2023.100037

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Sustained microglial activation and accelerated elimination of dendritic spines during acute sleep deprivation and restoration

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Sustained microglial activation and accelerated elimination of dendritic spines during acute sleep deprivation and restoration

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