{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,27]],"date-time":"2026-09-27T23:16:12Z","timestamp":1790550972141,"version":"4.1.0"},"reference-count":57,"publisher":"Public Library of Science (PLoS)","issue":"8","license":[{"start":{"date-parts":[[2019,8,13]],"date-time":"2019-08-13T00:00:00Z","timestamp":1565654400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0220125","type":"journal-article","created":{"date-parts":[[2019,8,13]],"date-time":"2019-08-13T17:34:15Z","timestamp":1565717655000},"page":"e0220125","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":26,"title":["Cell-autonomous and non-cell autonomous effects of neuronal BIN1 loss in vivo"],"prefix":"10.1371","volume":"14","author":[{"given":"Kathleen M.","family":"McAvoy","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hameetha","family":"Rajamohamed Sait","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Galina","family":"Marsh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Peterson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Taylor L.","family":"Reynolds","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jake","family":"Gagnon","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah","family":"Geisler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Prescott","family":"Leach","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chris","family":"Roberts","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ellen","family":"Cahir-McFarland","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard M.","family":"Ransohoff","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9421-4370","authenticated-orcid":true,"given":"Andrea","family":"Crotti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2019,8,13]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1007\/BF00308809","article-title":"Neuropathological stageing of Alzheimer-related changes","volume":"82","author":"H Braak","year":"1991","journal-title":"Acta Neuropathol"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1016\/0197-4580(95)00021-6","article-title":"Staging of Alzheimer&apos;s disease-related neurofibrillary changes","volume":"16","author":"H Braak","year":"1995","journal-title":"Neurobiol Aging"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"1237","DOI":"10.1126\/science.7058341","article-title":"Alzheimer&apos;s disease and senile dementia: loss of neurons in the basal forebrain","volume":"215","author":"PJ Whitehouse","year":"1982","journal-title":"Science"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"1832","DOI":"10.1001\/jama.2010.574","article-title":"Genome-wide analysis of genetic loci associated with Alzheimer disease","volume":"303","author":"S Seshadri","year":"2010","journal-title":"JAMA"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"1452","DOI":"10.1038\/ng.2802","article-title":"Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer&apos;s disease","volume":"45","author":"JC Lambert","year":"2013","journal-title":"Nat Genet"},{"key":"ref6","first-page":"25","article-title":"BAR the door: cancer suppression by amphiphysin-like genes","volume":"1795","author":"GC Prendergast","year":"2009","journal-title":"Biochim Biophys Acta"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1128\/MMBR.70.1.37-120.2006","article-title":"The BAR domain proteins: molding membranes in fission, fusion, and phagy","volume":"70","author":"G Ren","year":"2006","journal-title":"Microbiol Mol Biol Rev"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"15101","DOI":"10.1074\/jbc.272.24.15101","article-title":"A new member of the amphiphysin family connecting endocytosis and signal transduction pathways","volume":"272","author":"C Leprince","year":"1997","journal-title":"J Biol Chem"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"720","DOI":"10.1038\/nm.2374","article-title":"Misregulated alternative splicing of BIN1 is associated with T tubule alterations and muscle weakness in myotonic dystrophy","volume":"17","author":"C Fugier","year":"2011","journal-title":"Nat Med"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"31453","DOI":"10.1074\/jbc.272.50.31453","article-title":"Structural analysis of the human BIN1 gene. Evidence for tissue-specific transcriptional regulation and alternate RNA splicing","volume":"272","author":"R Wechsler-Reya","year":"1997","journal-title":"J Biol Chem"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"789","DOI":"10.1016\/S0896-6273(02)00601-3","article-title":"Decreased synaptic vesicle recycling efficiency and cognitive deficits in amphiphysin 1 knockout mice","volume":"33","author":"G Di Paolo","year":"2002","journal-title":"Neuron"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1042\/BJ20121373","article-title":"Interaction of amphiphysins with AP-1 clathrin adaptors at the membrane","volume":"450","author":"S Huser","year":"2013","journal-title":"Biochem J"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1038\/nm1196","article-title":"Inhibition of indoleamine 2,3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy","volume":"11","author":"AJ Muller","year":"2005","journal-title":"Nat Med"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"1399","DOI":"10.1038\/ncb1986","article-title":"AMPH-1\/Amphiphysin\/Bin1 functions with RME-1\/Ehd1 in endocytic recycling","volume":"11","author":"S Pant","year":"2009","journal-title":"Nat Cell Biol"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"2369","DOI":"10.1046\/j.1471-4159.1998.70062369.x","article-title":"Multiple amphiphysin II splice variants display differential clathrin binding: identification of two distinct clathrin-binding sites","volume":"70","author":"AR Ramjaun","year":"1998","journal-title":"J Neurochem"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"2051","DOI":"10.15252\/embr.201744137","article-title":"Bin1 directly remodels actin dynamics through its BAR domain","volume":"18","author":"NM Drager","year":"2017","journal-title":"EMBO Rep"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"1355","DOI":"10.1083\/jcb.137.6.1355","article-title":"Amphiphysin II (SH3P9; BIN1), a member of the amphiphysin\/Rvs family, is concentrated in the cortical cytomatrix of axon initial segments and nodes of ranvier in brain and around T tubules in skeletal muscle","volume":"137","author":"MH Butler","year":"1997","journal-title":"J Cell Biol"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"16700","DOI":"10.1074\/jbc.272.26.16700","article-title":"Identification and Characterization of a Nerve Terminal-enriched Amphiphysin Isoform","volume":"272","author":"AR Ramjaun","year":"1997","journal-title":"Journal of Biological Chemistry"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"1914","DOI":"10.4161\/cc.6.15.4514","article-title":"Bin1 interacts with and restrains the DNA end-binding protein complex Ku","volume":"6","author":"A Ramalingam","year":"2007","journal-title":"Cell Cycle"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"1225","DOI":"10.1038\/mp.2013.1","article-title":"Increased expression of BIN1 mediates Alzheimer genetic risk by modulating tau pathology","volume":"18","author":"J Chapuis","year":"2013","journal-title":"Mol Psychiatry"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"179","DOI":"10.3233\/JAD-150972","article-title":"Bridging Integrator 1 (BIN1) Genotypes Mediate Alzheimer&apos;s Disease Risk by Altering Neuronal Degeneration","volume":"52","author":"HF Wang","year":"2016","journal-title":"J Alzheimers Dis"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1186\/s40478-015-0237-8","article-title":"Tau phosphorylation regulates the interaction between BIN1&apos;s SH3 domain and Tau&apos;s proline-rich domain","volume":"3","author":"Y Sottejeau","year":"2015","journal-title":"Acta Neuropathol Commun"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"e103187","DOI":"10.1371\/journal.pone.0103187","article-title":"Intracellular clusterin interacts with brain isoforms of the bridging integrator 1 and with the microtubule-associated protein Tau in Alzheimer&apos;s disease","volume":"9","author":"Y Zhou","year":"2014","journal-title":"PLoS One"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1001\/archneurol.2010.108","article-title":"Genetic variation and neuroimaging measures in Alzheimer disease","volume":"67","author":"A Biffi","year":"2010","journal-title":"Arch Neurol"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"1794","DOI":"10.1038\/npp.2015.30","article-title":"Bridging Integrator 1 (BIN1) Genotype Effects on Working Memory, Hippocampal Volume, and Functional Connectivity in Young Healthy Individuals","volume":"40","author":"X Zhang","year":"2015","journal-title":"Neuropsychopharmacology"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.nbd.2015.11.011","article-title":"Gene expression variance in hippocampal tissue of temporal lobe epilepsy patients corresponds to differential memory performance","volume":"86","author":"J Bungenberg","year":"2016","journal-title":"Neurobiol Dis"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"e78806","DOI":"10.1371\/journal.pone.0078806","article-title":"BIN1 is decreased in sporadic but not familial Alzheimer&apos;s disease or in aging","volume":"8","author":"EB Glennon","year":"2013","journal-title":"PLoS One"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"1221","DOI":"10.3233\/JAD-132450","article-title":"Bridging integrator 1 (BIN1) protein expression increases in the Alzheimer&apos;s disease brain and correlates with neurofibrillary tangle pathology","volume":"42","author":"CJ Holler","year":"2014","journal-title":"J Alzheimers Dis"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1093\/jnen\/nlw056","article-title":"Subcellular Changes in Bridging Integrator 1 Protein Expression in the Cerebral Cortex During the Progression of Alzheimer Disease Pathology","volume":"75","author":"SL Adams","year":"2016","journal-title":"J Neuropathol Exp Neurol"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1186\/s13024-016-0124-1","article-title":"Predominant expression of Alzheimer&apos;s disease-associated BIN1 in mature oligodendrocytes and localization to white matter tracts","volume":"11","author":"P De Rossi","year":"2016","journal-title":"Mol Neurodegener"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/j.neuron.2007.01.010","article-title":"Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model","volume":"53","author":"Y Yoshiyama","year":"2007","journal-title":"Neuron"},{"key":"ref32","article-title":"BIN1 recovers tauopathy-induced long-term memory deficits in mice and interacts with Tau through Thr(348) phosphorylation","author":"M Sartori","year":"2019","journal-title":"Acta Neuropathol"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"1464","DOI":"10.1001\/jamaneurol.2017.2822","article-title":"Kinetics of Human Mutant Tau Prion Formation in the Brains of 2 Transgenic Mouse Lines","volume":"74","author":"AL Woerman","year":"2017","journal-title":"JAMA Neurol"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"2304","DOI":"10.1016\/j.celrep.2014.11.042","article-title":"Channelrhodopsin-assisted patching: in vivo recording of genetically and morphologically identified neurons throughout the brain","volume":"9","author":"W Munoz","year":"2014","journal-title":"Cell Rep"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"3445","DOI":"10.1523\/JNEUROSCI.22-09-03445.2002","article-title":"Neuronal deficiency of presenilin 1 inhibits amyloid plaque formation and corrects hippocampal long-term potentiation but not a cognitive defect of amyloid precursor protein [V717I] transgenic mice","volume":"22","author":"I Dewachter","year":"2002","journal-title":"J Neurosci"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"13149","DOI":"10.1038\/ncomms13149","article-title":"Molecular characterization of Thy1 expressing fear-inhibiting neurons within the basolateral amygdala","volume":"7","author":"KM McCullough","year":"2016","journal-title":"Nat Commun"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"10396","DOI":"10.1523\/JNEUROSCI.5539-12.2013","article-title":"Thy1-expressing neurons in the basolateral amygdala may mediate fear inhibition","volume":"33","author":"AM Jasnow","year":"2013","journal-title":"J Neurosci"},{"key":"ref38","article-title":"Methods of Behavior Analysis in Neuroscience","author":"P Curzon","year":"2009"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"636","DOI":"10.1016\/j.seizure.2007.05.005","article-title":"Timed pentylenetetrazol infusion test: a comparative analysis with s.c.PTZ and MES models of anticonvulsant screening in mice","volume":"16","author":"SN Mandhane","year":"2007","journal-title":"Seizure"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1016\/0896-6273(90)90106-P","article-title":"The regulation and function of c-fos and other immediate early genes in the nervous system","volume":"4","author":"M Sheng","year":"1990","journal-title":"Neuron"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/j.brainres.2014.11.005","article-title":"Using c-fos to study neuronal ensembles in corticostriatal circuitry of addiction","volume":"1628","author":"FC Cruz","year":"2015","journal-title":"Brain Res"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1038\/nn.4170","article-title":"Stimulus-specific combinatorial functionality of neuronal c-fos enhancers","volume":"19","author":"JY Joo","year":"2016","journal-title":"Nat Neurosci"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/S0896-6273(03)00627-5","article-title":"Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles","volume":"40","author":"JC Cruz","year":"2003","journal-title":"Neuron"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1016\/j.celrep.2017.09.039","article-title":"Temporal Tracking of Microglia Activation in Neurodegeneration at Single-Cell Resolution","volume":"21","author":"H Mathys","year":"2017","journal-title":"Cell Rep"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"10536","DOI":"10.1523\/JNEUROSCI.3133-06.2006","article-title":"p25\/cyclin-dependent kinase 5 induces production and intraneuronal accumulation of amyloid beta in vivo","volume":"26","author":"JC Cruz","year":"2006","journal-title":"J Neurosci"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1016\/j.bbr.2016.05.007","article-title":"Transcriptional signatures of brain aging and Alzheimer&apos;s disease: What are our rodent models telling us?","volume":"322","author":"KE Hargis","year":"2017","journal-title":"Behav Brain Res"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"1276","DOI":"10.1016\/j.cell.2017.05.018","article-title":"A Unique Microglia Type Associated with Restricting Development of Alzheimer&apos;s Disease","volume":"169","author":"H Keren-Shaul","year":"2017","journal-title":"Cell"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1186\/s12929-017-0399-8","article-title":"Inhibitory or excitatory? Optogenetic interrogation of the functional roles of GABAergic interneurons in epileptogenesis","volume":"24","author":"H Ye","year":"2017","journal-title":"J Biomed Sci"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1002\/neu.480260313","article-title":"Cell death, gliosis, and synaptic remodeling in the hippocampus of epileptic rats","volume":"26","author":"A Represa","year":"1995","journal-title":"J Neurobiol"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1038\/nn1707","article-title":"Potential role for adult neurogenesis in the encoding of time in new memories","volume":"9","author":"JB Aimone","year":"2006","journal-title":"Nat Neurosci"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1152\/physrev.00037.2015","article-title":"Cardiac T-Tubule Microanatomy and Function","volume":"97","author":"T Hong","year":"2017","journal-title":"Physiol Rev"},{"key":"ref52","article-title":"A novel role for the late-onset Alzheimer&apos;s disease (LOAD)-associated protein Bin1 in regulating postsynaptic trafficking and glutamatergic signaling","author":"B Schurmann","year":"2019","journal-title":"Mol Psychiatry"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"1553","DOI":"10.1038\/nn.4418","article-title":"Functional and structural underpinnings of neuronal assembly formation in learning","volume":"19","author":"A Holtmaat","year":"2016","journal-title":"Nat Neurosci"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"5484","DOI":"10.1523\/JNEUROSCI.2685-05.2006","article-title":"Context fear learning in the absence of the hippocampus","volume":"26","author":"BJ Wiltgen","year":"2006","journal-title":"J Neurosci"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1016\/S1474-4422(17)30044-3","article-title":"Epileptic activity in Alzheimer&apos;s disease: causes and clinical relevance","volume":"16","author":"KA Vossel","year":"2017","journal-title":"Lancet Neurol"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"177","DOI":"10.2217\/fnl.12.8","article-title":"Alzheimer&apos;s disease and epilepsy: insight from animal models","volume":"7","author":"HE Scharfman","year":"2012","journal-title":"Future Neurol"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1038\/nrn.2016.141","article-title":"Network abnormalities and interneuron dysfunction in Alzheimer disease","volume":"17","author":"JJ Palop","year":"2016","journal-title":"Nat Rev Neurosci"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0220125","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,5,8]],"date-time":"2020-05-08T19:17:42Z","timestamp":1588965462000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0220125"}},"subtitle":[],"editor":[{"given":"Giuseppe","family":"Biagini","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2019,8,13]]},"references-count":57,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2019,8,13]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0220125","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,8,13]]}}}