Astrocytic Piezo1-mediated mechanotransduction determines adult neurogenesis and cognitive functions

Neuron - Tập 110 - Trang 2984-2999.e8 - 2022
Shaopeng Chi1, Yaxiong Cui1, Haiping Wang1, Jinghui Jiang1, Tingxin Zhang1, Suhua Sun2, Zhuan Zhou2, Yi Zhong3, Bailong Xiao1
1State Key Laboratory of Membrane Biology, Tsinghua-Peking Center for Life Sciences, IDG/McGovern Institute for Brain Research, Beijing Frontier Research Center for Biological Structure, Beijing Advanced Innovation Center for Structural Biology, School of Pharmaceutical Sciences, Tsinghua University, Beijing 100084, China
2State Key Laboratory of Membrane Biology, Peking-Tsinghua Center for Life Sciences, PKU-IDG/McGovern Institute for Brain Research, College of Future Technology, Peking University, Beijing 100871, China
3Tsinghua-Peking Center for Life Sciences, IDG/McGovern Institute for Brain Research, School of Life Science, Tsinghua University, Beijing 100084, China

Tài liệu tham khảo

Adamsky, 2018, Astrocytic activation generates de novo neuronal potentiation and memory enhancement, Cell, 174, 10.1016/j.cell.2018.05.002 Araque, 2014, Gliotransmitters travel in time and space, Neuron, 81, 728, 10.1016/j.neuron.2014.02.007 Bae, 2011, The mechanosensitive ion channel Piezo1 is inhibited by the peptide GsMTx4, Biochemistry, 50, 6295, 10.1021/bi200770q Bazargani, 2016, Astrocyte calcium signaling: the third wave, Nat. Neurosci., 19, 182, 10.1038/nn.4201 Bindocci, 2017, Three-dimensional Ca2+ imaging advances understanding of astrocyte biology, Science, 356, 10.1126/science.aai8185 Blumenthal, 2014, Stochastic nanoroughness modulates neuron-astrocyte interactions and function via mechanosensing cation channels, Proc. Natl. Acad. Sci. USA, 111, 16124, 10.1073/pnas.1412740111 Bond, 2015, Adult mammalian neural stem cells and neurogenesis: five decades later, Cell Stem Cell, 17, 385, 10.1016/j.stem.2015.09.003 Bowman, 1992, Mechanotransducing ion channels in astrocytes, Brain Res., 584, 272, 10.1016/0006-8993(92)90906-P Cahalan, 2015, Piezo1 links mechanical forces to red blood cell volume, eLife, 4, e07370, 10.7554/eLife.07370 Cao, 2013, Astrocytic adenosine 5′-triphosphate release regulates the proliferation of neural stem cells in the adult hippocampus, Stem Cells, 31, 1633, 10.1002/stem.1408 Charles, 1991, Intercellular signaling in glial cells: calcium waves and oscillations in response to mechanical stimulation and glutamate, Neuron, 6, 983, 10.1016/0896-6273(91)90238-U Chi, 2010, Baifuzi reduces transient ischemic brain damage through an interaction with the STREX domain of BKCa channels, Cell Death Dis., 1, e13, 10.1038/cddis.2009.10 Chi, 2009, Suppression of neuronal excitability by the secretion of the lamprey (Lampetra japonica) provides a mechanism for its evolutionary stability, Pflugers Arch., 458, 537, 10.1007/s00424-008-0631-1 Coste, 2010, Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels, Science, 330, 55, 10.1126/science.1193270 Coste, 2012, Piezo proteins are pore-forming subunits of mechanically activated channels, Nature, 483, 176, 10.1038/nature10812 Cox, 2016, Removal of the mechanoprotective influence of the cytoskeleton reveals PIEZO1 is gated by bilayer tension, Nat. Commun., 7, 10366, 10.1038/ncomms10366 Douguet, 2019, Mammalian mechanoelectrical transduction: structure and function of force-gated ion channels, Cell, 179, 340, 10.1016/j.cell.2019.08.049 Ellefsen, 2019, Myosin-II mediated traction forces evoke localized Piezo1-dependent Ca2+ flickers, Commun. Biol., 2, 298, 10.1038/s42003-019-0514-3 Fiacco, 2007, Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity, Neuron, 54, 611, 10.1016/j.neuron.2007.04.032 Ge, 2015, Architecture of the mammalian mechanosensitive Piezo1 channel, Nature, 527, 64, 10.1038/nature15247 Geng, 2020, A plug-and-latch mechanism for gating the mechanosensitive piezo channel, Neuron, 106, 10.1016/j.neuron.2020.02.010 Gonçalves, 2016, Adult neurogenesis in the hippocampus: from stem cells to behavior, Cell, 167, 897, 10.1016/j.cell.2016.10.021 Guo, 2012, Isolation of multipotent neural stem or progenitor cells from both the dentate gyrus and subventricular zone of a single adult mouse, Nat. Protoc., 7, 2005, 10.1038/nprot.2012.123 Guo, 2017, Structure-based membrane dome mechanism for Piezo mechanosensitivity, eLife, 6, e33660, 10.7554/eLife.33660 Guthrie, 1999, ATP released from astrocytes mediates glial calcium waves, J. Neurosci., 19, 520, 10.1523/JNEUROSCI.19-02-00520.1999 Haselwandter, 2018, Piezo’s membrane footprint and its contribution to mechanosensitivity, eLife, 7, e41968, 10.7554/eLife.41968 Hayashi, 2004, Detecting ATP release by a biosensor method, Sci. STKE, 2004, pl14, 10.1126/stke.2582004pl14 Holt, 2021, Spatiotemporal dynamics of PIEZO1 localization controls keratinocyte migration during wound healing, eLife, 10, e65415, 10.7554/eLife.65415 Jiang, 2021, Structural designs and mechanogating mechanisms of the mechanosensitive piezo channels, Trends Biochem. Sci., 46, 472, 10.1016/j.tibs.2021.01.008 Koizumi, 2003, Dynamic inhibition of excitatory synaptic transmission by astrocyte-derived ATP in hippocampal cultures, Proc. Natl. Acad. Sci. USA, 100, 11023, 10.1073/pnas.1834448100 Lewis, 2015, Mechanical sensitivity of Piezo1 ion channels can be tuned by cellular membrane tension, eLife, 4, 10.7554/eLife.12088 Lin, 2019, Force-induced conformational changes in PIEZO1, Nature, 573, 230, 10.1038/s41586-019-1499-2 López, 2021, A physiologic rise in cytoplasmic calcium ion signal increases pannexin1 channel activity via a C-terminus phosphorylation by CaMKII, Proc. Natl. Acad. Sci. USA, 118, 10.1073/pnas.2108967118 Ma, 2021, A role of PIEZO1 in iron metabolism in mice and humans, Cell, 184, 10.1016/j.cell.2021.01.024 Newman, 2001, Propagation of intercellular calcium waves in retinal astrocytes and Muller cells, J. Neurosci., 21, 2215, 10.1523/JNEUROSCI.21-07-02215.2001 Pryazhnikov, 2008, Sub-micromolar increase in [Ca(2+)](i) triggers delayed exocytosis of ATP in cultured astrocytes, Glia, 56, 38, 10.1002/glia.20590 Ranade, 2014, Piezo1, a mechanically activated ion channel, is required for vascular development in mice, Proc. Natl. Acad. Sci. USA, 111, 10347, 10.1073/pnas.1409233111 Ranade, 2014, Piezo2 is the major transducer of mechanical forces for touch sensation in mice, Nature, 516, 121, 10.1038/nature13980 Rungta, 2016, Ca2+ transients in astrocyte fine processes occur via Ca2+ influx in the adult mouse hippocampus, Glia, 64, 2093, 10.1002/glia.23042 Saotome, 2018, Structure of the mechanically activated ion channel Piezo1, Nature, 554, 481, 10.1038/nature25453 Schildge, 2013, Isolation and culture of mouse cortical astrocytes, J. Vis. Exp., 50079 Servin-Vences, 2017, Direct measurement of TRPV4 and PIEZO1 activity reveals multiple mechanotransduction pathways in chondrocytes, eLife, 6, e21074, 10.7554/eLife.21074 Shigetomi, 2013, Imaging calcium microdomains within entire astrocyte territories and endfeet with GCaMPs expressed using adeno-associated viruses, J. Gen. Physiol., 141, 633, 10.1085/jgp.201210949 Shigetomi, 2013, TRPA1 channels are regulators of astrocyte basal calcium levels and long-term potentiation via constitutive D-serine release, J. Neurosci., 33, 10143, 10.1523/JNEUROSCI.5779-12.2013 Shigetomi, 2010, A genetically targeted optical sensor to monitor calcium signals in astrocyte processes, Nat. Neurosci., 13, 759, 10.1038/nn.2557 Song, 2002, Astroglia induce neurogenesis from adult neural stem cells, Nature, 417, 39, 10.1038/417039a Srinivasan, 2015, Ca2+ signaling in astrocytes from Ip3r2(−/−) mice in brain slices and during startle responses in vivo, Nat. Neurosci., 18, 708, 10.1038/nn.4001 Suyama, 2012, Purinergic signaling promotes proliferation of adult mouse subventricular zone cells, J. Neurosci., 32, 9238, 10.1523/JNEUROSCI.4001-11.2012 Swain, 2022, Piezo1-mediated stellate cell activation causes pressure-induced pancreatic fibrosis in mice, JCI Insight, 7, e158288, 10.1172/jci.insight.158288 Syeda, 2016, Piezo1 channels are inherently mechanosensitive, Cell Rep., 17, 1739, 10.1016/j.celrep.2016.10.033 Syeda, 2015, Chemical activation of the mechanotransduction channel Piezo1, eLife, 4, e0736, 10.7554/eLife.07369 Toth, 2019, CRAC channels regulate astrocyte Ca2+ signaling and gliotransmitter release to modulate hippocampal GABAergic transmission, Sci. Signal., 12, eaaw5450, 10.1126/scisignal.aaw5450 Turovsky, 2020, Mechanosensory signaling in astrocytes, J. Neurosci., 40, 9364, 10.1523/JNEUROSCI.1249-20.2020 Velasco-Estevez, 2020, Piezo1 regulates calcium oscillations and cytokine release from astrocytes, Glia, 68, 145, 10.1002/glia.23709 Vicidomini, 2020, Communication, cross talk, and signal integration in the adult hippocampal neurogenic niche, Neuron, 105, 220, 10.1016/j.neuron.2019.11.029 Wang, 2019, Brain endothelial cells maintain lactate homeostasis and control adult hippocampal neurogenesis, Cell Stem Cell, 25, 10.1016/j.stem.2019.09.009 Wang, 2019, Structure and mechanogating of the mammalian tactile channel PIEZO2, Nature, 573, 225, 10.1038/s41586-019-1505-8 Wu, 2022, A sensitive GRAB sensor for detecting extracellular ATP in vitro and in vivo, Neuron, 110, 10.1016/j.neuron.2021.11.027 Xiao, 2020, Levering mechanically activated Piezo channels for potential pharmacological intervention, Annu. Rev. Pharmacol. Toxicol., 60, 195, 10.1146/annurev-pharmtox-010919-023703 Xiong, 2018, Stretch-induced Ca2+ independent ATP release in hippocampal astrocytes, J. Physiol., 596, 1931, 10.1113/JP275805 Yang, 2022, Structure deformation and curvature sensing of PIEZO1 in lipid membranes, Nature, 604, 377, 10.1038/s41586-022-04574-8 Zeisel, 2018, Molecular architecture of the mouse nervous system, Cell, 174, 10.1016/j.cell.2018.06.021 Zhang, 2019, Mechanically activated piezo channels mediate touch and suppress acute mechanical pain response in mice, Cell Rep., 26, 10.1016/j.celrep.2019.01.056 Zhang, 2017, A protein interaction mechanism for suppressing the mechanosensitive Piezo channels, Nat. Commun., 8, 1797, 10.1038/s41467-017-01712-z Zhao, 2016, Ion permeation and mechanotransduction mechanisms of mechanosensitive Piezo channels, Neuron, 89, 1248, 10.1016/j.neuron.2016.01.046 Zhao, 2018, Structure and mechanogating mechanism of the Piezo1 channel, Nature, 554, 487, 10.1038/nature25743 Zhuo, 2001, hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo, Genesis, 31, 85, 10.1002/gene.10008