{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T23:32:35Z","timestamp":1790811155552,"version":"4.1.0"},"reference-count":79,"publisher":"The Company of Biologists","license":[{"start":{"date-parts":[[2021,5,18]],"date-time":"2021-05-18T00:00:00Z","timestamp":1621296000000},"content-version":"am","delay-in-days":2329,"URL":"http:\/\/creativecommons.org\/licenses\/by\/3.0"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2015,1,1]]},"abstract":"<jats:p>Synaptogenesis requires orchestrated intercellular communication between synaptic partners, with trans-synaptic signals necessarily traversing the extracellular synaptomatrix separating presynaptic and postsynaptic cells. Extracellular matrix metalloproteinases (Mmps) regulated by secreted tissue inhibitors of metalloproteinases (Timps), cleave secreted and membrane-associated targets to sculpt the extracellular environment and modulate intercellular signaling. Here, we test Mmp roles at the neuromuscular junction (NMJ) model synapse in the reductionist Drosophila system, which contains just two Mmps (secreted Mmp1 and GPI-anchored Mmp2) and one secreted Timp. We find all three matrix metalloproteome components co-dependently localize in the synaptomatrix. We find both Mmp1 and Mmp2 independently restrict synapse morphogenesis and functional differentiation. Surprisingly, either dual knockdown or simultaneous inhibition of the two Mmp classes together restores normal synapse development, identifying a novel reciprocal suppression mechanism. We find the two Mmp classes co-regulate a Wnt trans-synaptic signaling pathway modulating structural and functional synaptogenesis, including the GPI-anchored heparan sulfate proteoglycan (HSPG) Wnt co-receptor Dally-like Protein (Dlp), cognate receptor Frizzled-2 and Wingless ligand. Loss of either Mmp1 or Mmp2 reciprocally misregulates Dlp at the synapse, with normal signaling restored by co-removal of both Mmp classes. Correcting Wnt co-receptor Dlp levels in both mmp mutants prevents structural and functional synaptogenic defects. Taken together, these results identify a novel Mmp mechanism that fine-tunes HSPG co-receptor function to modulate Wnt signaling to coordinate synapse structural and functional development.<\/jats:p>","DOI":"10.1242\/dev.124461","type":"journal-article","created":{"date-parts":[[2015,11,25]],"date-time":"2015-11-25T02:59:51Z","timestamp":1448420391000},"source":"Crossref","is-referenced-by-count":34,"title":["Two matrix metalloproteinase classes reciprocally regulate synaptogenesis"],"prefix":"10.1242","author":[{"given":"Mary Lynn","family":"Dear","sequence":"first","affiliation":[{"name":"Department of Biological Sciences, Kennedy Center for Research on Human Development, Vanderbilt University, Nashville, Tennessee, 37235-1634, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Neil","family":"Dani","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, Kennedy Center for Research on Human Development, Vanderbilt University, Nashville, Tennessee, 37235-1634, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William","family":"Parkinson","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, Kennedy Center for Research on Human Development, Vanderbilt University, Nashville, Tennessee, 37235-1634, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Scott","family":"Zhou","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, Kennedy Center for Research on Human Development, Vanderbilt University, Nashville, Tennessee, 37235-1634, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kendal","family":"Broadie","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, Kennedy Center for Research on Human Development, Vanderbilt University, Nashville, Tennessee, 37235-1634, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","reference":[{"key":"2021042608241824600_DEV124461C1","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1016\/j.semcdb.2007.06.003","article-title":"MMPs in the central nervous system: where the good guys go bad","volume":"19","author":"Agrawal","year":"2008","journal-title":"Semin. Cell Dev. Biol."},{"key":"2021042608241824600_DEV124461C2","doi-asserted-by":"publisher","first-page":"705","DOI":"10.1016\/j.neuron.2008.01.026","article-title":"Rapid activity-dependent modifications in synaptic structure and function require bidirectional Wnt signaling","volume":"57","author":"Ataman","year":"2008","journal-title":"Neuron"},{"key":"2021042608241824600_DEV124461C3","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1242\/dev.128.1.87","article-title":"Heparan sulfate proteoglycans are critical for the organization of the extracellular distribution of Wingless","volume":"128","author":"Baeg","year":"2001","journal-title":"Development"},{"key":"2021042608241824600_DEV124461C4","doi-asserted-by":"publisher","first-page":"954","DOI":"10.1002\/hipo.20872","article-title":"Building and remodeling synapses","volume":"22","author":"Benson","year":"2012","journal-title":"Hippocampus"},{"key":"2021042608241824600_DEV124461C5","doi-asserted-by":"publisher","first-page":"94","DOI":"10.1136\/jmg.2008.061796","article-title":"Minocycline promotes dendritic spine maturation and improves behavioural performance in the fragile X mouse model","volume":"46","author":"Bilousova","year":"2009","journal-title":"J. Med. Genet."},{"key":"2021042608241824600_DEV124461C6","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1741-7007-3-1","article-title":"Discs-large (DLG) is clustered by presynaptic innervation and regulates postsynaptic glutamate receptor subunit composition in Drosophila","volume":"3","author":"Chen","year":"2005","journal-title":"BMC Biol."},{"key":"2021042608241824600_DEV124461C7","doi-asserted-by":"publisher","first-page":"471","DOI":"10.1242\/dmm.004598","article-title":"Fragile X mental retardation protein has a unique, evolutionarily conserved neuronal function not shared with FXR1P or FXR2P","volume":"3","author":"Coffee","year":"2010","journal-title":"Dis. Model. Mech."},{"key":"2021042608241824600_DEV124461C8","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1002\/dneu.20891","article-title":"Glycosylated synaptomatrix regulation of trans-synaptic signaling","volume":"72","author":"Dani","year":"2012","journal-title":"Dev. Neurobiol."},{"key":"2021042608241824600_DEV124461C9","doi-asserted-by":"publisher","first-page":"e1003031","DOI":"10.1371\/journal.pgen.1003031","article-title":"A targeted glycan-related gene screen reveals heparan sulfate proteoglycan sulfation regulates WNT and BMP trans-synaptic signaling","volume":"8","author":"Dani","year":"2012","journal-title":"PLoS Genet."},{"key":"2021042608241824600_DEV124461C10","doi-asserted-by":"publisher","first-page":"13047","DOI":"10.1523\/JNEUROSCI.1484-14.2014","article-title":"Two protein N-acetylgalactosaminyl transferases regulate synaptic plasticity by activity-dependent regulation of integrin signaling","volume":"34","author":"Dani","year":"2014","journal-title":"J. Neurosci."},{"key":"2021042608241824600_DEV124461C11","doi-asserted-by":"publisher","first-page":"956","DOI":"10.1002\/dneu.20963","article-title":"Casting a net on dendritic spines: the extracellular matrix and its receptors","volume":"71","author":"Dansie","year":"2011","journal-title":"Dev. Neurobiol."},{"key":"2021042608241824600_DEV124461C12","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1146\/annurev-physiol-021014-071740","article-title":"Homeostatic control of presynaptic neurotransmitter release","volume":"77","author":"Davis","year":"2015","journal-title":"Annu. Rev. Physiol."},{"key":"2021042608241824600_DEV124461C13","doi-asserted-by":"crossref","first-page":"3023","DOI":"10.1523\/JNEUROSCI.19-08-03023.1999","article-title":"Glutamate receptor expression regulates quantal size and quantal content at the Drosophila neuromuscular junction","volume":"19","author":"Diantonio","year":"1999","journal-title":"J. Neurosci."},{"key":"2021042608241824600_DEV124461C14","doi-asserted-by":"publisher","first-page":"30","DOI":"10.3389\/fncel.2014.00030","article-title":"Impaired activity-dependent neural circuit assembly and refinement in autism spectrum disorder genetic models","volume":"8","author":"Doll","year":"2014","journal-title":"Front. Cell. Neurosci."},{"key":"2021042608241824600_DEV124461C15","doi-asserted-by":"publisher","first-page":"1346","DOI":"10.1242\/dev.117127","article-title":"Activity-dependent FMRP requirements in development of the neural circuitry of learning and memory","volume":"142","author":"Doll","year":"2015","journal-title":"Development"},{"key":"2021042608241824600_DEV124461C16","doi-asserted-by":"publisher","first-page":"709","DOI":"10.1016\/j.biocel.2012.01.023","article-title":"MMP9: a novel function in synaptic plasticity","volume":"44","author":"Dziembowska","year":"2012","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"2021042608241824600_DEV124461C17","doi-asserted-by":"publisher","first-page":"2813","DOI":"10.1002\/jnr.21273","article-title":"Matrix metalloproteinases in brain development and remodeling: synaptic functions and targets","volume":"85","author":"Ethell","year":"2007","journal-title":"J. Neurosci. Res."},{"key":"2021042608241824600_DEV124461C18","doi-asserted-by":"publisher","first-page":"1400","DOI":"10.1242\/dmm.012229","article-title":"Fragile X mental retardation protein regulates trans-synaptic signaling in Drosophila","volume":"6","author":"Friedman","year":"2013","journal-title":"Dis. Model. Mech."},{"key":"2021042608241824600_DEV124461C19","doi-asserted-by":"publisher","first-page":"789083","DOI":"10.1155\/2012\/789083","article-title":"Neural functions of matrix metalloproteinases: plasticity, neurogenesis, and disease","volume":"2012","author":"Fujioka","year":"2012","journal-title":"Biochem. Res. Int."},{"key":"2021042608241824600_DEV124461C20","doi-asserted-by":"publisher","first-page":"2637","DOI":"10.1242\/dev.022244","article-title":"Temporal requirements of the fragile X mental retardation protein in the regulation of synaptic structure","volume":"135","author":"Gatto","year":"2008","journal-title":"Development"},{"key":"2021042608241824600_DEV124461C21","doi-asserted-by":"publisher","first-page":"834","DOI":"10.1016\/j.conb.2011.04.009","article-title":"Drosophila modeling of heritable neurodevelopmental disorders","volume":"21","author":"Gatto","year":"2011","journal-title":"Curr. Opin. Neurobiol."},{"key":"2021042608241824600_DEV124461C22","doi-asserted-by":"publisher","first-page":"2659","DOI":"10.1073\/pnas.0804171106","article-title":"Distinct functions for the catalytic and hemopexin domains of a Drosophila matrix metalloproteinase","volume":"106","author":"Glasheen","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2021042608241824600_DEV124461C23","doi-asserted-by":"publisher","first-page":"495","DOI":"10.1078\/0171-9335-00072","article-title":"Inflated wings, tissue autolysis and early death in tissue inhibitor of metalloproteinases mutants of Drosophila","volume":"79","author":"Godenschwege","year":"2000","journal-title":"Eur. J. Cell Biol."},{"key":"2021042608241824600_DEV124461C24","doi-asserted-by":"publisher","first-page":"601","DOI":"10.1242\/dev.00958","article-title":"Drosophila glypicans control the cell-to-cell movement of Hedgehog by a dynamin-independent process","volume":"131","author":"Han","year":"2004","journal-title":"Development"},{"key":"2021042608241824600_DEV124461C25","doi-asserted-by":"publisher","first-page":"743","DOI":"10.1038\/nrn3320","article-title":"Synaptic circuit remodelling by matrix metalloproteinases in health and disease","volume":"13","author":"Huntley","year":"2012","journal-title":"Nat. Rev. Neurosci."},{"key":"2021042608241824600_DEV124461C26","doi-asserted-by":"publisher","first-page":"7535","DOI":"10.1038\/srep07535","article-title":"Mmp1 and Mmp2 cooperatively induce Drosophila fat body cell dissociation with distinct roles","volume":"4","author":"Jia","year":"2014","journal-title":"Sci. Rep."},{"key":"2021042608241824600_DEV124461C27","doi-asserted-by":"publisher","first-page":"517","DOI":"10.1016\/j.neuron.2006.01.026","article-title":"The HSPGs syndecan and dallylike bind the receptor phosphatase LAR and exert distinct effects on synaptic development","volume":"49","author":"Johnson","year":"2006","journal-title":"Neuron"},{"key":"2021042608241824600_DEV124461C28","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1083\/jcb.201207036","article-title":"Perlecan regulates bidirectional Wnt signaling at the Drosophila neuromuscular junction","volume":"200","author":"Kamimura","year":"2013","journal-title":"J. Cell Biol."},{"key":"2021042608241824600_DEV124461C29","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1016\/j.cell.2010.03.015","article-title":"Matrix metalloproteinases: regulators of the tumor microenvironment","volume":"141","author":"Kessenbrock","year":"2010","journal-title":"Cell"},{"key":"2021042608241824600_DEV124461C30","doi-asserted-by":"publisher","first-page":"300","DOI":"10.1016\/j.stem.2013.06.005","article-title":"A role for matrix metalloproteinases in regulating mammary stem cell function via the Wnt signaling pathway","volume":"13","author":"Kessenbrock","year":"2013","journal-title":"Cell Stem Cell"},{"key":"2021042608241824600_DEV124461C31","doi-asserted-by":"publisher","first-page":"15230","DOI":"10.1073\/pnas.0507393102","article-title":"Dendrite-specific remodeling of Drosophila sensory neurons requires matrix metalloproteases, ubiquitin-proteasome, and ecdysone signaling","volume":"102","author":"Kuo","year":"2005","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2021042608241824600_DEV124461C32","doi-asserted-by":"publisher","first-page":"35978","DOI":"10.1074\/jbc.M006045200","article-title":"Dm1-MMP, a matrix metalloproteinase from Drosophila with a potential role in extracellular matrix remodeling during neural development","volume":"275","author":"Llano","year":"2000","journal-title":"J. Biol. Chem."},{"key":"2021042608241824600_DEV124461C33","doi-asserted-by":"publisher","first-page":"23321","DOI":"10.1074\/jbc.M200121200","article-title":"Structural and enzymatic characterization of Drosophila Dm2-MMP, a membrane-bound matrix metalloproteinase with tissue-specific expression","volume":"277","author":"Llano","year":"2002","journal-title":"J. Biol. Chem."},{"key":"2021042608241824600_DEV124461C34","doi-asserted-by":"publisher","first-page":"3303","DOI":"10.1242\/jcs.069468","article-title":"The nonsense-mediated decay pathway maintains synapse architecture and synaptic vesicle cycle efficacy","volume":"123","author":"Long","year":"2010","journal-title":"J. Cell Sci."},{"key":"2021042608241824600_DEV124461C35","doi-asserted-by":"publisher","first-page":"924","DOI":"10.1016\/j.cub.2004.05.047","article-title":"Preferential localization of glutamate receptors opposite sites of high presynaptic release","volume":"14","author":"Marrus","year":"2004","journal-title":"Curr. Biol."},{"key":"2021042608241824600_DEV124461C36","doi-asserted-by":"publisher","first-page":"1344","DOI":"10.1126\/science.1117051","article-title":"Wingless signaling at synapses is through cleavage and nuclear import of receptor DFrizzled2","volume":"310","author":"Mathew","year":"2005","journal-title":"Science"},{"key":"2021042608241824600_DEV124461C37","doi-asserted-by":"publisher","first-page":"647","DOI":"10.1002\/wdev.108","article-title":"Development and plasticity of the Drosophila larval neuromuscular junction","volume":"2","author":"Menon","year":"2013","journal-title":"Wiley Interdiscip. Rev. Dev. Biol."},{"key":"2021042608241824600_DEV124461C38","doi-asserted-by":"publisher","first-page":"6007","DOI":"10.1523\/JNEUROSCI.5346-08.2009","article-title":"Matrix metalloproteinase-9 controls NMDA receptor surface diffusion through integrin beta1 signaling","volume":"29","author":"Michaluk","year":"2009","journal-title":"J. Neurosci."},{"key":"2021042608241824600_DEV124461C39","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1242\/dev.011072","article-title":"Matrix metalloproteinases promote motor axon fasciculation in the Drosophila embryo","volume":"135","author":"Miller","year":"2008","journal-title":"Development"},{"key":"2021042608241824600_DEV124461C40","doi-asserted-by":"publisher","first-page":"5335","DOI":"10.1523\/JNEUROSCI.4811-10.2011","article-title":"Drosophila MMP2 regulates the matrix molecule faulty attraction (Frac) to promote motor axon targeting in Drosophila","volume":"31","author":"Miller","year":"2011","journal-title":"J. Neurosci."},{"key":"2021042608241824600_DEV124461C41","doi-asserted-by":"publisher","first-page":"1048","DOI":"10.1016\/j.neuroscience.2008.02.060","article-title":"Stoned B mediates sorting of integral synaptic vesicle proteins","volume":"153","author":"Mohrmann","year":"2008","journal-title":"Neuroscience"},{"key":"2021042608241824600_DEV124461C42","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1016\/j.ajpath.2011.09.008","article-title":"An alternate perspective on the roles of TIMPs and MMPs in pathology","volume":"180","author":"Moore","year":"2012","journal-title":"Am. J. Pathol."},{"key":"2021042608241824600_DEV124461C43","doi-asserted-by":"publisher","first-page":"562","DOI":"10.1016\/j.cardiores.2005.12.002","article-title":"Structure and function of matrix metalloproteinases and TIMPs","volume":"69","author":"Nagase","year":"2006","journal-title":"Cardiovasc. Res."},{"key":"2021042608241824600_DEV124461C44","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1016\/S0092-8674(02)01047-4","article-title":"The Drosophila Wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation","volume":"111","author":"Packard","year":"2002","journal-title":"Cell"},{"key":"2021042608241824600_DEV124461C45","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1016\/S1534-5807(02)00400-8","article-title":"Drosophila matrix metalloproteinases are required for tissue remodeling, but not embryonic development","volume":"4","author":"Page-McCaw","year":"2003","journal-title":"Dev. Cell"},{"key":"2021042608241824600_DEV124461C46","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1038\/nrm2125","article-title":"Matrix metalloproteinases and the regulation of tissue remodelling","volume":"8","author":"Page-McCaw","year":"2007","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2021042608241824600_DEV124461C47","doi-asserted-by":"publisher","first-page":"4970","DOI":"10.1242\/dev.099192","article-title":"N-glycosylation requirements in neuromuscular synaptogenesis","volume":"140","author":"Parkinson","year":"2013","journal-title":"Development"},{"key":"2021042608241824600_DEV124461C48","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1016\/j.nbd.2014.06.003","article-title":"Metalloproteinase inhibition prevents inhibitory synapse reorganization and seizure genesis","volume":"70","author":"Pollock","year":"2014","journal-title":"Neurobiol. Dis."},{"key":"2021042608241824600_DEV124461C49","doi-asserted-by":"publisher","first-page":"3209","DOI":"10.1523\/JNEUROSCI.4194-04.2005","article-title":"Four different subunits are essential for expressing the synaptic glutamate receptor at neuromuscular junctions of Drosophila","volume":"25","author":"Qin","year":"2005","journal-title":"J. Neurosci."},{"key":"2021042608241824600_DEV124461C50","doi-asserted-by":"publisher","first-page":"819","DOI":"10.1083\/jcb.135.3.819","article-title":"Glycosaminoglycans can modulate extracellular localization of the wingless protein and promote signal transduction","volume":"135","author":"Reichsman","year":"1996","journal-title":"J. Cell Biol."},{"key":"2021042608241824600_DEV124461C51","doi-asserted-by":"publisher","first-page":"280","DOI":"10.3389\/fncel.2015.00280","article-title":"A delicate balance: role of MMP-9 in brain development and pathophysiology of neurodevelopmental disorders","volume":"9","author":"Reinhard","year":"2015","journal-title":"Front. Cell. Neurosci."},{"key":"2021042608241824600_DEV124461C52","doi-asserted-by":"publisher","first-page":"8539","DOI":"10.1523\/JNEUROSCI.5587-08.2009","article-title":"Cell type-specific requirements for heparan sulfate biosynthesis at the Drosophila neuromuscular junction: effects on synapse function, membrane trafficking, and mitochondrial localization","volume":"29","author":"Ren","year":"2009","journal-title":"J. Neurosci."},{"key":"2021042608241824600_DEV124461C53","doi-asserted-by":"publisher","first-page":"2607","DOI":"10.1101\/gad.1574107","article-title":"Presynaptic establishment of the synaptic cleft extracellular matrix is required for post-synaptic differentiation","volume":"21","author":"Rohrbough","year":"2007","journal-title":"Genes Dev."},{"key":"2021042608241824600_DEV124461C54","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1159\/000334862","article-title":"Serum levels of matrix metalloproteinases: implications in clinical neurology","volume":"67","author":"Romi","year":"2012","journal-title":"Eur. Neurol."},{"key":"2021042608241824600_DEV124461C55","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1016\/j.conb.2015.08.005","article-title":"Tuning synapses by proteolytic remodeling of the adhesive surface","volume":"35","author":"Shinoe","year":"2015","journal-title":"Curr. Opin. Neurobiol."},{"key":"2021042608241824600_DEV124461C56","doi-asserted-by":"publisher","first-page":"9867","DOI":"10.1523\/JNEUROSCI.1162-14.2014","article-title":"Genetic removal of matrix metalloproteinase 9 rescues the symptoms of fragile X syndrome in a mouse model","volume":"34","author":"Sidhu","year":"2014","journal-title":"J. Neurosci."},{"key":"2021042608241824600_DEV124461C57","doi-asserted-by":"publisher","first-page":"673","DOI":"10.1242\/dmm.008045","article-title":"Neural circuit architecture defects in a Drosophila model of Fragile X syndrome are alleviated by minocycline treatment and genetic removal of matrix metalloproteinase","volume":"4","author":"Siller","year":"2011","journal-title":"Dis. Model. Mech."},{"key":"2021042608241824600_DEV124461C58","doi-asserted-by":"publisher","first-page":"124548","DOI":"10.1155\/2012\/124548","article-title":"Matrix metalloproteinases and minocycline: therapeutic avenues for fragile X syndrome","volume":"2012","author":"Siller","year":"2012","journal-title":"Neural Plast."},{"key":"2021042608241824600_DEV124461C59","doi-asserted-by":"publisher","first-page":"832","DOI":"10.1016\/j.cell.2012.03.032","article-title":"Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling","volume":"149","author":"Speese","year":"2012","journal-title":"Cell"},{"key":"2021042608241824600_DEV124461C60","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1146\/annurev.cellbio.17.1.463","article-title":"How matrix metalloproteinases regulate cell behavior","volume":"17","author":"Sternlicht","year":"2001","journal-title":"Annu. Rev. Cell Biol."},{"key":"2021042608241824600_DEV124461C61","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1016\/j.neuroscience.2007.07.032","article-title":"Matrix metalloproteinase-7 modulates synaptic vesicle recycling and induces atrophy of neuronal synapses","volume":"149","author":"Szklarczyk","year":"2007","journal-title":"Neuroscience"},{"key":"2021042608241824600_DEV124461C62","doi-asserted-by":"publisher","first-page":"3757","DOI":"10.1096\/fj.07-101402","article-title":"MMP-7 cleaves the NR1 NMDA receptor subunit and modifies NMDA receptor function","volume":"22","author":"Szklarczyk","year":"2008","journal-title":"FASEB J."},{"key":"2021042608241824600_DEV124461C63","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1007\/978-3-642-21649-7_7","article-title":"Molecular and Genetic Analysis of the Drosophila Model of Fragile X Syndrome. In","volume-title":"Modeling Fragile X Syndrome","author":"Tessier","year":"2012"},{"key":"2021042608241824600_DEV124461C64","doi-asserted-by":"publisher","first-page":"687","DOI":"10.1083\/jcb.200612097","article-title":"Activation of NMDA receptors promotes dendritic spine development through MMP-mediated ICAM-5 cleavage","volume":"178","author":"Tian","year":"2007","journal-title":"J. Cell Biol."},{"key":"2021042608241824600_DEV124461C65","doi-asserted-by":"publisher","first-page":"2332","DOI":"10.1111\/febs.12198","article-title":"Functional interactions between matrix metalloproteinases and glycosaminoglycans","volume":"280","author":"Tocchi","year":"2013","journal-title":"FEBS J."},{"key":"2021042608241824600_DEV124461C66","doi-asserted-by":"publisher","first-page":"5294","DOI":"10.1038\/sj.emboj.7601401","article-title":"JNK- and Fos-regulated Mmp1 expression cooperates with Ras to induce invasive tumors in Drosophila","volume":"25","author":"Uhlirova","year":"2006","journal-title":"EMBO J."},{"key":"2021042608241824600_DEV124461C67","doi-asserted-by":"publisher","first-page":"a007914","DOI":"10.1101\/cshperspect.a007914","article-title":"Alternative Wnt pathways and receptors","volume":"4","author":"van Amerongen","year":"2012","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"2021042608241824600_DEV124461C68","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1016\/j.neuint.2010.05.004","article-title":"The synaptomatrix: a solid though dynamic contact disconnecting transmissions from exocytotic events","volume":"57","author":"Vautrin","year":"2010","journal-title":"Neurochem. Int."},{"key":"2021042608241824600_DEV124461C69","doi-asserted-by":"publisher","first-page":"833","DOI":"10.1016\/j.neuron.2006.02.008","article-title":"Bruchpilot, a protein with homology to ELKS\/CAST, is required for structural integrity and function of synaptic active zones in Drosophila","volume":"49","author":"Wagh","year":"2006","journal-title":"Neuron"},{"key":"2021042608241824600_DEV124461C70","doi-asserted-by":"publisher","first-page":"923","DOI":"10.1083\/jcb.201403084","article-title":"A matrix metalloproteinase mediates long-distance attenuation of stem cell proliferation","volume":"206","author":"Wang","year":"2014","journal-title":"J. Cell Biol."},{"key":"2021042608241824600_DEV124461C71","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/j.devcel.2009.11.004","article-title":"Spatial restriction of FGF signaling by a matrix metalloprotease controls branching morphogenesis","volume":"18","author":"Wang","year":"2010","journal-title":"Dev. Cell"},{"key":"2021042608241824600_DEV124461C72","doi-asserted-by":"publisher","first-page":"12200","DOI":"10.1021\/bi035358x","article-title":"Drosophila TIMP is a potent inhibitor of MMPs and TACE: similarities in structure and function to TIMP-3","volume":"42","author":"Wei","year":"2003","journal-title":"Biochemistry"},{"key":"2021042608241824600_DEV124461C73","doi-asserted-by":"publisher","first-page":"1021","DOI":"10.1083\/jcb.200708213","article-title":"Important role of matrix metalloproteinase 9 in epileptogenesis","volume":"180","author":"Wilczynski","year":"2008","journal-title":"J. Cell Biol."},{"key":"2021042608241824600_DEV124461C74","doi-asserted-by":"publisher","first-page":"313","DOI":"10.3389\/fncel.2015.00313","article-title":"Diverse impact of acute and long-term extracellular proteolytic activity on plasticity of neuronal excitability","volume":"9","author":"W\u00f3jtowicz","year":"2015","journal-title":"Front. Cell. Neurosci."},{"key":"2021042608241824600_DEV124461C75","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1016\/S0076-6879(10)80002-3","article-title":"Dual roles of Drosophila glypican Dally-like in Wingless\/Wnt signaling and distribution","volume":"480","author":"Wu","year":"2010","journal-title":"Methods Enzymol."},{"key":"2021042608241824600_DEV124461C76","doi-asserted-by":"publisher","first-page":"470","DOI":"10.1016\/j.devcel.2009.09.001","article-title":"The core protein of glypican Dally-like determines its biphasic activity in wingless morphogen signaling","volume":"17","author":"Yan","year":"2009","journal-title":"Dev. Cell"},{"key":"2021042608241824600_DEV124461C77","doi-asserted-by":"publisher","first-page":"621","DOI":"10.1016\/j.devcel.2010.02.010","article-title":"Dendrite reshaping of adult Drosophila sensory neurons requires matrix metalloproteinase-mediated modification of the basement membranes","volume":"18","author":"Yasunaga","year":"2010","journal-title":"Dev. Cell"},{"key":"2021042608241824600_DEV124461C78","doi-asserted-by":"publisher","first-page":"e5181","DOI":"10.1371\/journal.pone.0005181","article-title":"Newly generated heparanase knock-out mice unravel co-regulation of heparanase and matrix metalloproteinases","volume":"4","author":"Zcharia","year":"2009","journal-title":"PLoS ONE"},{"key":"2021042608241824600_DEV124461C79","doi-asserted-by":"publisher","first-page":"7296","DOI":"10.1073\/pnas.1322264111","article-title":"O-glycosylation regulates polarized secretion by modulating Tango1 stability","volume":"111","author":"Zhang","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"}],"container-title":["Development"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/journals.biologists.com\/dev\/article-pdf\/143\/1\/75\/1840936\/dev124461.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/dev\/article-pdf\/doi\/10.1242\/dev.124461\/2033983\/dev_124461v1.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/dev\/article-pdf\/doi\/10.1242\/dev.124461\/2033983\/dev_124461v1.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,5,18]],"date-time":"2021-05-18T20:49:31Z","timestamp":1621370971000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/dev\/article\/doi\/10.1242\/dev.124461\/256941\/Two-matrix-metalloproteinase-classes-reciprocally"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,1,1]]},"references-count":79,"URL":"https:\/\/doi.org\/10.1242\/dev.124461","relation":{},"ISSN":["1477-9129","0950-1991"],"issn-type":[{"value":"1477-9129","type":"electronic"},{"value":"0950-1991","type":"print"}],"subject":[],"published":{"date-parts":[[2015,1,1]]},"article-number":"dev.124461"}}