Activity-Dependent Exocytosis of Lysosomes Regulates the Structural Plasticity of Dendritic Spines

Neuron - Tập 93 - Trang 132-146 - 2017
Zahid Padamsey1, Lindsay McGuinness1, Scott J. Bardo1, Marcia Reinhart1, Rudi Tong1, Anne Hedegaard1, Michael L. Hart1, Nigel J. Emptage1
1Department of Pharmacology, University of Oxford, Mansfield Road, Oxford OX1 3QT, UK

Tài liệu tham khảo

Arantes, 2006, A role for synaptotagmin VII-regulated exocytosis of lysosomes in neurite outgrowth from primary sympathetic neurons, J. Neurosci., 26, 4630, 10.1523/JNEUROSCI.0009-06.2006 Bak, 1999, Nicotinic acid adenine dinucleotide phosphate triggers Ca2+ release from brain microsomes, Curr. Biol., 9, 751, 10.1016/S0960-9822(99)80335-2 Berg, 2000, Nicotinic acid adenine dinucleotide phosphate (NAADP(+)) is an essential regulator of T-lymphocyte Ca(2+)-signaling, J. Cell Biol., 150, 581, 10.1083/jcb.150.3.581 Blott, 2002, Secretory lysosomes, Nat. Rev. Mol. Cell Biol., 3, 122, 10.1038/nrm732 Brailoiu, 2003, Modulation of spontaneous transmitter release from the frog neuromuscular junction by interacting intracellular Ca(2+) stores: critical role for nicotinic acid-adenine dinucleotide phosphate (NAADP), Biochem. J., 373, 313, 10.1042/bj20030472 Brailoiu, 2005, Nicotinic acid adenine dinucleotide phosphate potentiates neurite outgrowth, J. Biol. Chem., 280, 5646, 10.1074/jbc.M408746200 Brailoiu, 2006, Messenger-specific role for nicotinic acid adenine dinucleotide phosphate in neuronal differentiation, J. Biol. Chem., 281, 15923, 10.1074/jbc.M602249200 Brailoiu, 2009, NAADP-mediated channel ‘chatter’ in neurons of the rat medulla oblongata, Biochem J., 419, 91, 10.1042/BJ20081138 Calcraft, 2009, NAADP mobilizes calcium from acidic organelles through two-pore channels, Nature, 459, 596, 10.1038/nature08030 Cang, 2014, The voltage-gated sodium channel TPC1 confers endolysosomal excitability, Nat. Chem. Biol., 10, 463, 10.1038/nchembio.1522 Chazotte, 2011, Labeling lysosomes in live cells with LysoTracker, Cold Spring Harb. Protoc., 2011 Christie, 1995, Different Ca2+ channels in soma and dendrites of hippocampal pyramidal neurons mediate spike-induced Ca2+ influx, J. Neurophysiol., 73, 2553, 10.1152/jn.1995.73.6.2553 Davis, 2012, NAADP activates two-pore channels on T cell cytolytic granules to stimulate exocytosis and killing, Curr. Biol., 22, 2331, 10.1016/j.cub.2012.10.035 Dziembowska, 2012, MMP9: a novel function in synaptic plasticity, Int. J. Biochem. Cell Biol., 44, 709, 10.1016/j.biocel.2012.01.023 Dziembowska, 2012, Activity-dependent local translation of matrix metalloproteinase-9, J. Neurosci., 32, 14538, 10.1523/JNEUROSCI.6028-11.2012 Emptage, 1999, Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines, Neuron, 22, 115, 10.1016/S0896-6273(00)80683-2 Erecińska, 1991, Relations between intracellular ions and energy metabolism: a study with monensin in synaptosomes, neurons, and C6 glioma cells, J. Neurosci., 11, 2410, 10.1523/JNEUROSCI.11-08-02410.1991 Galione, 2015, A primer of NAADP-mediated Ca(2+) signalling: From sea urchin eggs to mammalian cells, Cell Calcium, 58, 27, 10.1016/j.ceca.2014.09.010 Galione, 2010, NAADP as an intracellular messenger regulating lysosomal calcium-release channels, Biochem. Soc. Trans., 38, 1424, 10.1042/BST0381424 Gan, 2004, Identification of cathepsin B as a mediator of neuronal death induced by Abeta-activated microglial cells using a functional genomics approach, J. Biol. Chem., 279, 5565, 10.1074/jbc.M306183200 Grubb, 2009 Guse, 2012, Linking NAADP to ion channel activity: a unifying hypothesis, Sci. Signal., 5, pe18, 10.1126/scisignal.2002890 Helmchen, 1996, Ca2+ buffering and action potential-evoked Ca2+ signaling in dendrites of pyramidal neurons, Biophys. J., 70, 1069, 10.1016/S0006-3495(96)79653-4 Hook, 2015, Cathepsin B is a New Drug Target for Traumatic Brain Injury Therapeutics: Evidence for E64d as a Promising Lead Drug Candidate, Front. Neurol., 6, 178, 10.3389/fneur.2015.00178 Hui, 2015, Release of calcium from endolysosomes increases calcium influx through N-type calcium channels: Evidence for acidic store-operated calcium entry in neurons, Cell Calcium, 58, 617, 10.1016/j.ceca.2015.10.001 Jaffe, 1992, The spread of Na+ spikes determines the pattern of dendritic Ca2+ entry into hippocampal neurons, Nature, 357, 244, 10.1038/357244a0 Kingham, 2001, Microglial secreted cathepsin B induces neuronal apoptosis, J. Neurochem., 76, 1475, 10.1046/j.1471-4159.2001.00146.x Kostoulas, 1999, Stimulation of angiogenesis through cathepsin B inactivation of the tissue inhibitors of matrix metalloproteinases, FEBS Lett., 455, 286, 10.1016/S0014-5793(99)00897-2 Kovalchuk, 2000, NMDA receptor-mediated subthreshold Ca(2+) signals in spines of hippocampal neurons, J. Neurosci., 20, 1791, 10.1523/JNEUROSCI.20-05-01791.2000 Linebaugh, 1999, Exocytosis of active cathepsin B enzyme activity at pH 7.0, inhibition and molecular mass, Eur. J. Biochem., 264, 100, 10.1046/j.1432-1327.1999.00582.x Luzio, 2007, The role of calcium and other ions in sorting and delivery in the late endocytic pathway, Biochem. Soc. Trans., 35, 1088, 10.1042/BST0351088 Luzio, 2007, Lysosomes: fusion and function, Nat. Rev. Mol. Cell Biol., 8, 622, 10.1038/nrm2217 Markram, 1995, Dendritic calcium transients evoked by single back-propagating action potentials in rat neocortical pyramidal neurons, J. Physiol., 485, 1, 10.1113/jphysiol.1995.sp020708 Martinez, 2000, Synaptotagmin VII regulates Ca(2+)-dependent exocytosis of lysosomes in fibroblasts, J. Cell Biol., 148, 1141, 10.1083/jcb.148.6.1141 Masgrau, 2003, NAADP: a new second messenger for glucose-induced Ca2+ responses in clonal pancreatic beta cells, Curr. Biol., 13, 247, 10.1016/S0960-9822(03)00041-1 McGuinness, 2007, The lysosome or lysosome-related organelle may serve as a Ca2+ store in the boutons of hippocampal pyramidal cells, Neuropharmacology, 52, 126, 10.1016/j.neuropharm.2006.07.029 Miller, 2011, Proteolytic Activity Matrix Analysis (PrAMA) for simultaneous determination of multiple protease activities, Integr. Biol. (Camb.), 3, 422, 10.1039/C0IB00083C Mitrović, 2016, Inhibition of endopeptidase and exopeptidase activity of cathepsin B impairs extracellular matrix degradation and tumour invasion, Biol. Chem., 397, 165, 10.1515/hsz-2015-0236 Morgan, 2014, Two-pore channels (TPCs): current controversies, BioEssays, 36, 173, 10.1002/bies.201300118 Morgan, 2011, Molecular mechanisms of endolysosomal Ca2+ signalling in health and disease, Biochem. J., 439, 349, 10.1042/BJ20110949 Morgan, 2013, Bidirectional Ca2+ signaling occurs between the endoplasmic reticulum and acidic organelles, J. Cell Biol., 200, 789, 10.1083/jcb.201204078 Morgan, 2015, Imaging approaches to measuring lysosomal calcium, Methods Cell Biol., 126, 159, 10.1016/bs.mcb.2014.10.031 Morgan, 2015, TPC: the NAADP discovery channel?, Biochem. Soc. Trans., 43, 384, 10.1042/BST20140300 Mort, 1984, Extracellular presence of the lysosomal proteinase cathepsin B in rheumatoid synovium and its activity at neutral pH, Arthritis Rheum., 27, 509, 10.1002/art.1780270505 Murphy, 2012, Activation of the P2X7 receptor induces migration of glial cells by inducing cathepsin B degradation of tissue inhibitor of metalloproteinase 1, J. Neurochem., 123, 761, 10.1111/jnc.12031 Nagy, 2006, Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory, J. Neurosci., 26, 1923, 10.1523/JNEUROSCI.4359-05.2006 Ogata, 1995, Steps involved in activation of the pro-matrix metalloproteinase 9 (progelatinase B)-tissue inhibitor of metalloproteinases-1 complex by 4-aminophenylmercuric acetate and proteinases, J. Biol. Chem., 270, 18506, 10.1074/jbc.270.31.18506 Pandey, 2009, Recruitment of NAADP-sensitive acidic Ca2+ stores by glutamate, Biochem. J., 422, 503, 10.1042/BJ20090194 Patel, 2000, Widespread distribution of binding sites for the novel Ca2+-mobilizing messenger, nicotinic acid adenine dinucleotide phosphate, in the brain, J. Biol. Chem., 275, 36495, 10.1074/jbc.C000458200 Patel, 2001, Coordination of Ca2+ signalling by NAADP, Trends Biochem. Sci., 26, 482, 10.1016/S0968-0004(01)01896-5 Penny, 2014, A computational model of lysosome-ER Ca2+ microdomains, J. Cell Sci., 127, 2934, 10.1242/jcs.149047 Pišlar, 2014, Cysteine cathepsins in neurological disorders, Mol. Neurobiol., 49, 1017, 10.1007/s12035-013-8576-6 Pitt, 2010, TPC2 is a novel NAADP-sensitive Ca2+ release channel, operating as a dual sensor of luminal pH and Ca2+, J. Biol. Chem., 285, 35039, 10.1074/jbc.M110.156927 Pitt, 2014, Reconstituted human TPC1 is a proton-permeable ion channel and is activated by NAADP or Ca2+, Sci. Signal., 7, ra46, 10.1126/scisignal.2004854 Pryor, 2000, The role of intraorganellar Ca(2+) in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles, J. Cell Biol., 149, 1053, 10.1083/jcb.149.5.1053 Reddy, 2001, Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes, Cell, 106, 157, 10.1016/S0092-8674(01)00421-4 Ryan, 1995, Microglial cathepsin B: an immunological examination of cellular and secreted species, J. Neurochem., 65, 1035, 10.1046/j.1471-4159.1995.65031035.x Rybalchenko, 2012, Membrane potential regulates nicotinic acid adenine dinucleotide phosphate (NAADP) dependence of the pH- and Ca2+-sensitive organellar two-pore channel TPC1, J. Biol. Chem., 287, 20407, 10.1074/jbc.M112.359612 Sandow, 1952, Excitation-contraction coupling in muscular response, Yale J. Biol. Med., 25, 176 Sbai, 2008, Vesicular trafficking and secretion of matrix metalloproteinases-2, -9 and tissue inhibitor of metalloproteinases-1 in neuronal cells, Mol. Cell. Neurosci., 39, 549, 10.1016/j.mcn.2008.08.004 Spruston, 1995, Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites, Science, 268, 297, 10.1126/science.7716524 Wang, 2008, Extracellular proteolysis by matrix metalloproteinase-9 drives dendritic spine enlargement and long-term potentiation coordinately, Proc. Natl. Acad. Sci. USA, 105, 19520, 10.1073/pnas.0807248105 Wlodarczyk, 2011, Extracellular matrix molecules, their receptors, and secreted proteases in synaptic plasticity, Dev. Neurobiol., 71, 1040, 10.1002/dneu.20958 Wu, 2001, Activity-dependent CREB phosphorylation: convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen-activated protein kinase pathway, Proc. Natl. Acad. Sci. USA, 98, 2808, 10.1073/pnas.051634198 Wu, 2001, Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology, Nat. Neurosci., 4, 151, 10.1038/83976 Zhang, 2007, Regulated ATP release from astrocytes through lysosome exocytosis, Nat. Cell Biol., 9, 945, 10.1038/ncb1620