{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,19]],"date-time":"2026-05-19T03:51:15Z","timestamp":1779162675860,"version":"3.51.4"},"reference-count":40,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2019,7,1]],"date-time":"2019-07-01T00:00:00Z","timestamp":1561939200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2019,7,1]],"date-time":"2019-07-01T00:00:00Z","timestamp":1561939200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2019,5,12]],"date-time":"2019-05-12T00:00:00Z","timestamp":1557619200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000265","name":"Medical Research Council","doi-asserted-by":"publisher","award":["MR\/L021064\/1"],"award-info":[{"award-number":["MR\/L021064\/1"]}],"id":[{"id":"10.13039\/501100000265","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000288","name":"Royal Society","doi-asserted-by":"publisher","award":["RG130856"],"award-info":[{"award-number":["RG130856"]}],"id":[{"id":"10.13039\/501100000288","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01MH071316"],"award-info":[{"award-number":["R01MH071316"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01MH097216"],"award-info":[{"award-number":["R01MH097216"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009670","name":"National Alliance for Research on Schizophrenia and Depression","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100009670","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009429","name":"Israel National Road Safety Authority","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100009429","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000874","name":"Brain and Behavior Research Foundation","doi-asserted-by":"publisher","award":["25957"],"award-info":[{"award-number":["25957"]}],"id":[{"id":"10.13039\/100000874","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Molecular and Cellular Neuroscience"],"published-print":{"date-parts":[[2019,7]]},"DOI":"10.1016\/j.mcn.2019.05.001","type":"journal-article","created":{"date-parts":[[2019,5,3]],"date-time":"2019-05-03T20:55:04Z","timestamp":1556916904000},"page":"19-31","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":17,"special_numbering":"C","title":["Loss of EPAC2 alters dendritic spine morphology and inhibitory synapse density"],"prefix":"10.1016","volume":"98","author":[{"given":"Kelly A.","family":"Jones","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Michiko","family":"Sumiya","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kevin M.","family":"Woolfrey","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Deepak P.","family":"Srivastava","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Peter","family":"Penzes","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"78","reference":[{"key":"10.1016\/j.mcn.2019.05.001_bb0005","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1038\/sj.mp.4001340","article-title":"Screening of nine candidate genes for autism on chromosome 2q reveals rare nonsynonymous variants in the cAMP-GEFII gene","volume":"8","author":"Bacchelli","year":"2003","journal-title":"Mol. Psychiatry"},{"key":"10.1016\/j.mcn.2019.05.001_bb0010","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1038\/nrm1197","article-title":"Epac: a new cAMP target and new avenues in cAMP research","volume":"4","author":"Bos","year":"2003","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"10.1016\/j.mcn.2019.05.001_bb0015","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1016\/j.bbr.2007.03.010","article-title":"Neurobiology of 50-kHz ultrasonic vocalizations in rats: electrode mapping, lesion, and pharmacology studies","volume":"182","author":"Burgdorf","year":"2007","journal-title":"Behav. Brain Res."},{"key":"10.1016\/j.mcn.2019.05.001_bb0020","doi-asserted-by":"crossref","first-page":"1514","DOI":"10.1086\/320588","article-title":"Evidence for a susceptibility gene for autism on chromosome 2 and for genetic heterogeneity","volume":"68","author":"Buxbaum","year":"2001","journal-title":"Am. J. Hum. Genet."},{"key":"10.1016\/j.mcn.2019.05.001_bb0025","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1111\/j.1601-183X.2010.00610.x","article-title":"Ultrasonic vocalizations in mouse models for speech and socio-cognitive disorders: insights into the evolution of vocal communication","volume":"10","author":"Fischer","year":"2011","journal-title":"Genes Brain Behav."},{"key":"10.1016\/j.mcn.2019.05.001_bb0030","doi-asserted-by":"crossref","first-page":"3527","DOI":"10.2174\/1568026616666160426151306","article-title":"Enhancing cAMP levels as strategy for the treatment of neuropsychiatric disorders","volume":"16","author":"Garcia","year":"2016","journal-title":"Curr. Top. Med. Chem."},{"key":"10.1016\/j.mcn.2019.05.001_bb0035","doi-asserted-by":"crossref","first-page":"1287","DOI":"10.1038\/nprot.2006.220","article-title":"Immunocytochemistry and quantification of protein colocalization in cultured neurons","volume":"1","author":"Glynn","year":"2006","journal-title":"Nat. Protoc."},{"key":"10.1016\/j.mcn.2019.05.001_bb0040","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1007\/7854_2015_369","article-title":"Animal studies on the role of sleep in memory: from behavioral performance to molecular mechanisms","volume":"25","author":"Havekes","year":"2015","journal-title":"Curr. Top. Behav. Neurosci."},{"key":"10.1016\/j.mcn.2019.05.001_bb0045","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.conb.2017.03.005","article-title":"Synaptic adhesion molecules and excitatory synaptic transmission","volume":"45","author":"Jang","year":"2017","journal-title":"Curr. Opin. Neurobiol."},{"key":"10.1016\/j.mcn.2019.05.001_bb0050","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1111\/j.1460-9568.2010.07344.x","article-title":"Learning rules and persistence of dendritic spines","volume":"32","author":"Kasai","year":"2010","journal-title":"Eur. J. Neurosci."},{"key":"10.1016\/j.mcn.2019.05.001_bb0055","doi-asserted-by":"crossref","first-page":"2275","DOI":"10.1126\/science.282.5397.2275","article-title":"A family of cAMP-binding proteins that directly activate Rap1","volume":"282","author":"Kawasaki","year":"1998","journal-title":"Science"},{"key":"10.1016\/j.mcn.2019.05.001_bb0060","doi-asserted-by":"crossref","first-page":"1533","DOI":"10.1016\/j.neubiorev.2008.06.005","article-title":"The cyclic AMP phenotype of fragile X and autism","volume":"32","author":"Kelley","year":"2008","journal-title":"Neurosci. Biobehav. Rev."},{"key":"10.1016\/j.mcn.2019.05.001_bb0065","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1038\/mp.2008.124","article-title":"Developmental etiology for neuroanatomical and cognitive deficits in mice overexpressing Galphas, a G-protein subunit genetically linked to schizophrenia","volume":"14","author":"Kelly","year":"2009","journal-title":"Mol. Psychiatry"},{"key":"10.1016\/j.mcn.2019.05.001_bb0070","doi-asserted-by":"crossref","first-page":"161","DOI":"10.3389\/fphar.2015.00161","article-title":"Global and local missions of cAMP signaling in neural plasticity, learning, and memory","volume":"6","author":"Lee","year":"2015","journal-title":"Front. Pharmacol."},{"key":"10.1016\/j.mcn.2019.05.001_bb0075","doi-asserted-by":"crossref","first-page":"4802","DOI":"10.1523\/JNEUROSCI.3186-15.2016","article-title":"Epac signaling is required for cocaine-induced change in AMPA receptor subunit composition in the ventral tegmental area","volume":"36","author":"Liu","year":"2016","journal-title":"J. Neurosci."},{"key":"10.1016\/j.mcn.2019.05.001_bb0080","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1016\/j.ajhg.2007.12.009","article-title":"Structural variation of chromosomes in autism spectrum disorder","volume":"82","author":"Marshall","year":"2008","journal-title":"Am. J. Hum. Genet."},{"key":"10.1016\/j.mcn.2019.05.001_bb0085","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1083\/jcb.201003007","article-title":"N-cadherin mediates plasticity-induced long-term spine stabilization","volume":"189","author":"Mendez","year":"2010","journal-title":"J. Cell Biol."},{"key":"10.1016\/j.mcn.2019.05.001_bb0090","doi-asserted-by":"crossref","first-page":"4","DOI":"10.3389\/fninf.2012.00004","article-title":"Neuromantic - from semi-manual to semi-automatic reconstruction of neuron morphology","volume":"6","author":"Myatt","year":"2012","journal-title":"Front Neuroinform."},{"key":"10.1016\/j.mcn.2019.05.001_bb0095","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/S0896-6273(02)00653-0","article-title":"Neurobiology of depression","volume":"34","author":"Nestler","year":"2002","journal-title":"Neuron"},{"key":"10.1016\/j.mcn.2019.05.001_bb0100","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1016\/j.mcn.2010.11.008","article-title":"Epac2-mediated dendritic spine remodeling: implications for disease","volume":"46","author":"Penzes","year":"2011","journal-title":"Mol. Cell. Neurosci."},{"key":"10.1016\/j.mcn.2019.05.001_bb0105","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1038\/nature09146","article-title":"Functional impact of global rare copy number variation in autism spectrum disorders","volume":"466","author":"Pinto","year":"2010","journal-title":"Nature"},{"key":"10.1016\/j.mcn.2019.05.001_bb0110","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1016\/j.tins.2018.02.001","article-title":"cAMP, cGMP and amyloid beta: three ideal partners for memory formation","volume":"41","author":"Ricciarelli","year":"2018","journal-title":"Trends Neurosci."},{"key":"10.1016\/j.mcn.2019.05.001_bb0115","doi-asserted-by":"crossref","first-page":"866","DOI":"10.1038\/nprot.2008.51","article-title":"L-Measure: a web-accessible tool for the analysis, comparison and search of digital reconstructions of neuronal morphologies","volume":"3","author":"Scorcioni","year":"2008","journal-title":"Nat. Protoc."},{"key":"10.1016\/j.mcn.2019.05.001_bb0120","doi-asserted-by":"crossref","first-page":"1058","DOI":"10.1086\/339765","article-title":"Phenotypic homogeneity provides increased support for linkage on chromosome 2 in autistic disorder","volume":"70","author":"Shao","year":"2002","journal-title":"Am. J. Hum. Genet."},{"key":"10.1016\/j.mcn.2019.05.001_bb0125","doi-asserted-by":"crossref","first-page":"19333","DOI":"10.1073\/pnas.0707054104","article-title":"Essential role of Epac2\/Rap1 signaling in regulation of insulin granule dynamics by cAMP","volume":"104","author":"Shibasaki","year":"2007","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.mcn.2019.05.001_bb0130","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1016\/S0361-9230(99)00124-0","article-title":"cAMP and memory: a seminal lesson from Drosophila and Aplysia","volume":"50","author":"Silva","year":"1999","journal-title":"Brain Res. Bull."},{"key":"10.1016\/j.mcn.2019.05.001_bb0135","first-page":"e2794","article-title":"Analysis of dendritic spine morphology in cultured CNS neurons","author":"Srivastava","year":"2011","journal-title":"J. Vis. Exp."},{"key":"10.1016\/j.mcn.2019.05.001_bb0140","doi-asserted-by":"crossref","first-page":"11864","DOI":"10.1523\/JNEUROSCI.1349-12.2012","article-title":"Social, communication, and cortical structural impairments in Epac2-deficient mice","volume":"32","author":"Srivastava","year":"2012","journal-title":"J. Neurosci."},{"key":"10.1016\/j.mcn.2019.05.001_bb0145","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pbio.1001350","article-title":"An autism-associated variant of Epac2 reveals a role for Ras\/Epac2 signaling in controlling basal dendrite maintenance in mice","volume":"10","author":"Srivastava","year":"2012","journal-title":"PLoS Biol."},{"key":"10.1016\/j.mcn.2019.05.001_bb0150","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1113\/jphysiol.2008.157461","article-title":"Epac mediates PACAP-dependent long-term depression in the hippocampus","volume":"587","author":"Ster","year":"2009","journal-title":"J. Physiol."},{"key":"10.1016\/j.mcn.2019.05.001_bb0155","doi-asserted-by":"crossref","first-page":"3030","DOI":"10.1523\/JNEUROSCI.2810-16.2017","article-title":"The Epac-phospholipase Cepsilon pathway regulates endocannabinoid signaling and cocaine-induced disinhibition of ventral tegmental area dopamine neurons","volume":"37","author":"Tong","year":"2017","journal-title":"J. Neurosci. Off. J. Soc. Neurosci."},{"key":"10.1016\/j.mcn.2019.05.001_bb0160","doi-asserted-by":"crossref","first-page":"H1662","DOI":"10.1152\/ajpheart.00159.2007","article-title":"Developmental changes in gene expression of Epac and its upregulation in myocardial hypertrophy","volume":"293","author":"Ulucan","year":"2007","journal-title":"Am. J. Physiol. Heart Circ. Physiol."},{"key":"10.1016\/j.mcn.2019.05.001_bb0165","doi-asserted-by":"crossref","DOI":"10.1038\/srep14622","article-title":"Quantifying barcodes of dendritic spines using entropy-based metrics","volume":"5","author":"Viggiano","year":"2015","journal-title":"Sci. Rep."},{"key":"10.1016\/j.mcn.2019.05.001_bb0170","article-title":"Ultrasonic vocalizations induced by sex and amphetamine in M2, M4, M5 muscarinic and D2 dopamine receptor knockout mice","volume":"3","author":"Wang","year":"2008","journal-title":"PLoS One"},{"key":"10.1016\/j.mcn.2019.05.001_bb0175","doi-asserted-by":"crossref","first-page":"5272","DOI":"10.1038\/s41598-017-05588-3","article-title":"Synaptic GAP and GEF complexes cluster proteins essential for GTP signaling","volume":"7","author":"Wilkinson","year":"2017","journal-title":"Sci. Rep."},{"key":"10.1016\/j.mcn.2019.05.001_bb0180","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1038\/ejhg.2009.199","article-title":"Haploinsufficiency of MBD5 associated with a syndrome involving microcephaly, intellectual disabilities, severe speech impairment, and seizures","volume":"18","author":"Williams","year":"2010","journal-title":"Eur. J. Hum. Genet."},{"key":"10.1016\/j.mcn.2019.05.001_bb0185","doi-asserted-by":"crossref","first-page":"1275","DOI":"10.1038\/nn.2386","article-title":"Epac2 induces synapse remodeling and depression and its disease-associated forms alter spines","volume":"12","author":"Woolfrey","year":"2009","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.mcn.2019.05.001_bb0190","doi-asserted-by":"crossref","first-page":"6079","DOI":"10.1523\/JNEUROSCI.1170-08.2008","article-title":"Coordination of synaptic adhesion with dendritic spine remodeling by AF-6 and kalirin-7","volume":"28","author":"Xie","year":"2008","journal-title":"J. Neurosci."},{"key":"10.1016\/j.mcn.2019.05.001_bb0195","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1016\/j.neuron.2012.02.003","article-title":"EPAC null mutation impairs learning and social interactions via aberrant regulation of miR-124 and Zif268 translation","volume":"73","author":"Yang","year":"2012","journal-title":"Neuron"},{"key":"10.1016\/j.mcn.2019.05.001_bb0200","doi-asserted-by":"crossref","first-page":"e881","DOI":"10.1038\/tp.2016.129","article-title":"Anxiety and depression with neurogenesis defects in exchange protein directly activated by cAMP 2-deficient mice are ameliorated by a selective serotonin reuptake inhibitor, Prozac","volume":"6","author":"Zhou","year":"2016","journal-title":"Transl. Psychiatry"}],"container-title":["Molecular and Cellular Neuroscience"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S104474311930017X?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S104474311930017X?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2026,5,12]],"date-time":"2026-05-12T10:50:02Z","timestamp":1778583002000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S104474311930017X"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,7]]},"references-count":40,"alternative-id":["S104474311930017X"],"URL":"https:\/\/doi.org\/10.1016\/j.mcn.2019.05.001","relation":{},"ISSN":["1044-7431"],"issn-type":[{"value":"1044-7431","type":"print"}],"subject":[],"published":{"date-parts":[[2019,7]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Loss of EPAC2 alters dendritic spine morphology and inhibitory synapse density","name":"articletitle","label":"Article Title"},{"value":"Molecular and Cellular Neuroscience","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.mcn.2019.05.001","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2019 The Authors. Published by Elsevier Inc.","name":"copyright","label":"Copyright"}]}}