{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,2,21]],"date-time":"2025-02-21T09:29:14Z","timestamp":1740130154840,"version":"3.37.3"},"reference-count":99,"publisher":"Oxford University Press (OUP)","issue":"5","license":[{"start":{"date-parts":[[2020,1,2]],"date-time":"2020-01-02T00:00:00Z","timestamp":1577923200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01MH103716"],"award-info":[{"award-number":["R01MH103716"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,5,14]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Neuregulin\u2013ErbB signaling is essential for numerous functions in the developing, adult, and aging brain, particularly in the prefrontal cortex (PFC). Mouse models with disrupted Nrg and\/or ErbB genes are relevant to psychiatric, developmental, and age-related disorders, displaying a range of abnormalities stemming from cortical circuitry impairment. Many of these models display nonoverlapping phenotypes dependent upon the gene target and timing of perturbation, suggesting that cortical expression of the Nrg\u2013ErbB network undergoes temporal regulation across the lifespan. Here, we report a comprehensive temporal expression mapping study of the Nrg\u2013ErbB signaling network in the mouse PFC across postnatal development through aging. We find that Nrg and ErbB genes display distinct expression profiles; moreover, splice isoforms of these genes are differentially expressed across the murine lifespan. We additionally find a developmental switch in ErbB4 splice isoform expression potentially mediated through coregulation of the lncRNA Miat expression. Our results are the first to comprehensively and quantitatively map the expression patterns of the Nrg\u2013ErbB network in the mouse PFC across the postnatal lifespan and may help disentangle the pathway\u2019s involvement in normal cortical sequences of events across the lifespan, as well as shedding light on the pathophysiological mechanisms of abnormal Nrg\u2013ErbB signaling in neurological disease.<\/jats:p>","DOI":"10.1093\/cercor\/bhz312","type":"journal-article","created":{"date-parts":[[2019,12,2]],"date-time":"2019-12-02T21:04:35Z","timestamp":1575320675000},"page":"3325-3339","source":"Crossref","is-referenced-by-count":5,"title":["Temporal Dynam ics of the Neuregulin\u2013ErbB Network in the Murine Prefrontal Cortex across the Lifespan"],"prefix":"10.1093","volume":"30","author":[{"given":"Clare","family":"Paterson","sequence":"first","affiliation":[{"name":"Department of Psychiatry, University of Colorado, School of Medicine Anschutz Medical Campus, Aurora, CO 80045, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Brooke","family":"Cumming","sequence":"first","affiliation":[{"name":"Department of Psychiatry, University of Colorado, School of Medicine Anschutz Medical Campus, Aurora, CO 80045, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Amanda J","family":"Law","sequence":"first","affiliation":[{"name":"Department of Psychiatry, University of Colorado, School of Medicine Anschutz Medical Campus, Aurora, CO 80045, USA"},{"name":"Department of Cell and Developmental Biology, University of Colorado, School of Medicine Anschutz Medical Campus, Aurora, CO 80045, USA"},{"name":"Department of Medicine, University of Colorado, School of Medicine Anschutz Medical Campus, Aurora, CO 80045, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2020,1,2]]},"reference":[{"key":"2020062010532695300_ref1","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.neuroscience.2009.03.022","article-title":"In situ hybridization reveals developmental regulation of ErbB1-4 mRNA expression in mouse midbrain: implication of ErbB receptors for dopaminergic neurons","volume":"161","author":"Abe","year":"2009","journal-title":"Neuroscience"},{"key":"2020062010532695300_ref2","doi-asserted-by":"crossref","first-page":"1319","DOI":"10.1038\/nn1345","article-title":"Receptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain","volume":"7","author":"Anton","year":"2004","journal-title":"Nat Neurosci"},{"key":"2020062010532695300_ref3","doi-asserted-by":"crossref","first-page":"3145","DOI":"10.1038\/emboj.2013.245","article-title":"Transcriptome sequencing during mouse brain development identifies long non-coding RNAs functionally involved in neurogenic commitment","volume":"32","author":"Aprea","year":"2013","journal-title":"EMBO J"},{"key":"2020062010532695300_ref4","doi-asserted-by":"crossref","first-page":"6399","DOI":"10.1523\/JNEUROSCI.23-16-06399.2003","article-title":"Identification of a Pax6-dependent epidermal growth factor family signaling source at the lateral edge of the embryonic cerebral cortex","volume":"23","author":"Assimacopoulos","year":"2003","journal-title":"J Neurosci"},{"key":"2020062010532695300_ref5","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1093\/cercor\/bhn112","article-title":"Quantification of brain maturation and growth patterns in C57BL\/6J mice via computational neuroanatomy of diffusion tensor images","volume":"19","author":"Baloch","year":"2009","journal-title":"Cereb Cortex"},{"key":"2020062010532695300_ref6","doi-asserted-by":"crossref","first-page":"4507","DOI":"10.1073\/pnas.0900355106","article-title":"Impaired maturation of dendritic spines without disorganization of cortical cell layers in mice lacking NRG1\/ErbB signaling in the central nervous system","volume":"106","author":"Barros","year":"2009","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2020062010532695300_ref7","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1038\/mp.2013.45","article-title":"The long non-coding RNA Gomafu is acutely regulated in response to neuronal activation and involved in schizophrenia-associated alternative splicing","volume":"19","author":"Barry","year":"2014","journal-title":"Mol Psychiatry"},{"key":"2020062010532695300_ref8","doi-asserted-by":"crossref","first-page":"45","DOI":"10.3389\/fneur.2015.00045","article-title":"Long non-coding RNA expression during aging in the human subependymal zone","volume":"6","author":"Barry","year":"2015","journal-title":"Front Neurol"},{"key":"2020062010532695300_ref9","doi-asserted-by":"crossref","first-page":"1157","DOI":"10.1016\/j.celrep.2016.12.089","article-title":"Neuregulin 3 mediates cortical plate invasion and laminar allocation of GABAergic interneurons","volume":"18","author":"Bartolini","year":"2017","journal-title":"Cell Rep"},{"key":"2020062010532695300_ref10","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1186\/s12864-017-3674-x","article-title":"The predictive nature of transcript expression levels on protein expression in adult human brain","volume":"18","author":"Bauernfeind","year":"2017","journal-title":"BMC Genomics."},{"key":"2020062010532695300_ref11","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1016\/S0166-2236(97)01147-8","article-title":"GABAA, NMDA and AMPA receptors: a developmentally regulated \u201cmenage a trois\u201d","volume":"20","author":"Ben-Ari","year":"1997","journal-title":"Trends Neurosci"},{"key":"2020062010532695300_ref12","doi-asserted-by":"crossref","first-page":"611","DOI":"10.1016\/j.yexcr.2008.10.035","article-title":"ErbB receptors and the development of the nervous system","volume":"315","author":"Birchmeier","year":"2009","journal-title":"Exp Cell Res"},{"key":"2020062010532695300_ref13","doi-asserted-by":"crossref","first-page":"758","DOI":"10.1176\/appi.ajp.2014.13111452","article-title":"Prenatal expression patterns of genes associated with neuropsychiatric disorders","volume":"171","author":"Birnbaum","year":"2014","journal-title":"Am J Psychiatry"},{"key":"2020062010532695300_ref14","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1196\/annals.1417.007","article-title":"Neuronal mechanisms underlying attention deficit hyperactivity disorder: the influence of arousal on prefrontal cortical function","volume":"1129","author":"Brennan","year":"2008","journal-title":"Ann N Y Acad Sci"},{"key":"2020062010532695300_ref15","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1016\/j.neuron.2008.06.028","article-title":"Neuregulin-1\/ErbB signaling serves distinct functions in myelination of the peripheral and central nervous system","volume":"59","author":"Brinkmann","year":"2008","journal-title":"Neuron"},{"key":"2020062010532695300_ref16","doi-asserted-by":"crossref","first-page":"8221","DOI":"10.1128\/MCB.24.18.8221-8226.2004","article-title":"Generation and characterization of neuregulin-2-deficient mice","volume":"24","author":"Britto","year":"2004","journal-title":"Mol Cell Biol."},{"key":"2020062010532695300_ref17","doi-asserted-by":"crossref","first-page":"1078","DOI":"10.1093\/cercor\/10.11.1078","article-title":"Physiological dysfunction of the dorsolateral prefrontal cortex in schizophrenia revisited","volume":"10","author":"Callicott","year":"2000","journal-title":"Cereb Cortex"},{"key":"2020062010532695300_ref18","doi-asserted-by":"crossref","first-page":"512","DOI":"10.1038\/387512a0","article-title":"Neuregulin-2, a new ligand of ErbB3\/ErbB4-receptor tyrosine kinases","volume":"387","author":"Carraway","year":"1997","journal-title":"Nature"},{"key":"2020062010532695300_ref19","doi-asserted-by":"crossref","first-page":"898","DOI":"10.1242\/jcs.02799","article-title":"Characterization of a neural-specific splicing form of the human neuregulin 3 gene involved in oligodendrocyte survival","volume":"119","author":"Carteron","year":"2006","journal-title":"J Cell Sci"},{"key":"2020062010532695300_ref20","doi-asserted-by":"crossref","first-page":"6872","DOI":"10.1523\/JNEUROSCI.1815-08.2008","article-title":"Type III neuregulin-1 is required for normal sensorimotor gating, memory-related behaviors, and corticostriatal circuit components","volume":"28","author":"Chen","year":"2008","journal-title":"J Neurosci"},{"key":"2020062010532695300_ref21","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1016\/j.schres.2007.12.474","article-title":"Elevated neuregulin-1 and ErbB4 protein in the prefrontal cortex of schizophrenic patients","volume":"100","author":"Chong","year":"2008","journal-title":"Schizophr Res"},{"key":"2020062010532695300_ref22","doi-asserted-by":"crossref","first-page":"2478","DOI":"10.1038\/s41386-018-0169-7","article-title":"Altered ErbB4 splicing and cortical parvalbumin interneuron dysfunction in schizophrenia and mood disorders","volume":"43","author":"Chung","year":"2018","journal-title":"Neuropsychopharmacology"},{"key":"2020062010532695300_ref23","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1176\/appi.ajp.2015.15020150","article-title":"Dysregulated ErbB4 splicing in schizophrenia: selective effects on Parvalbumin expression","volume":"173","author":"Chung","year":"2016","journal-title":"Am J Psychiatry"},{"key":"2020062010532695300_ref24","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1038\/nature10524","article-title":"Temporal dynamics and genetic control of transcription in the human prefrontal cortex","volume":"478","author":"Colantuoni","year":"2011","journal-title":"Nature"},{"key":"2020062010532695300_ref25","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/0896-6273(95)90244-9","article-title":"Differential expression of ARIA isoforms in the rat brain","volume":"14","author":"Corfas","year":"1995","journal-title":"Neuron"},{"key":"2020062010532695300_ref26","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1038\/s41398-018-0288-2","article-title":"Altered hippocampal gene expression and structure in transgenic mice overexpressing neuregulin 1 (Nrg1) type I","volume":"8","author":"Deakin","year":"2018","journal-title":"Transl Psychiatry"},{"key":"2020062010532695300_ref27","doi-asserted-by":"crossref","first-page":"1523","DOI":"10.1097\/WNR.0b013e328330f6e7","article-title":"Behavioural characterization of neuregulin 1 type I overexpressing transgenic mice","volume":"20","author":"Deakin","year":"2009","journal-title":"Neuroreport"},{"key":"2020062010532695300_ref28","doi-asserted-by":"crossref","first-page":"6169","DOI":"10.1007\/s12035-017-0834-6","article-title":"A novel ultrasensitive in situ hybridization approach to detect short sequences and splice variants with cellular resolution","volume":"55","author":"Erben","year":"2018","journal-title":"Mol Neurobiol"},{"key":"2020062010532695300_ref29","doi-asserted-by":"crossref","first-page":"4999","DOI":"10.1242\/dev.124.24.4999","article-title":"ErbB3 is required for normal cerebellar and cardiac development: a comparison with ErbB2-and heregulin-deficient mice","volume":"124","author":"Erickson","year":"1997","journal-title":"Development"},{"key":"2020062010532695300_ref30","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1016\/S0014-4827(02)00102-7","article-title":"Neuregulins: functions, forms, and signaling strategies","volume":"284","author":"Falls","year":"2003","journal-title":"Exp Cell Res"},{"key":"2020062010532695300_ref31","doi-asserted-by":"crossref","first-page":"1376","DOI":"10.1038\/nature08928","article-title":"Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling","volume":"464","author":"Fazzari","year":"2010","journal-title":"Nature"},{"key":"2020062010532695300_ref32","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1016\/j.neuron.2004.09.028","article-title":"Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1","volume":"44","author":"Flames","year":"2004","journal-title":"Neuron"},{"key":"2020062010532695300_ref33","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.mcn.2016.10.008","article-title":"Neuregulin1 alpha activates migration of neuronal progenitors expressing ErbB4","volume":"77","author":"Fornasari","year":"2016","journal-title":"Mol Cell Neurosci"},{"key":"2020062010532695300_ref34","doi-asserted-by":"crossref","first-page":"584","DOI":"10.1002\/jnr.20381","article-title":"Developmental profile of ErbB receptors in murine central nervous system: implications for functional interactions","volume":"79","author":"Fox","year":"2005","journal-title":"J Neurosci Res"},{"key":"2020062010532695300_ref35","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1097\/WNR.0000000000000073","article-title":"The four isoforms of the tyrosine kinase receptor ErbB4 provide neural progenitor cells with an adhesion preference for the transmembrane type III isoform of the ligand neuregulin 1","volume":"25","author":"Fregnan","year":"2014","journal-title":"Neuroreport"},{"key":"2020062010532695300_ref36","doi-asserted-by":"crossref","first-page":"48808","DOI":"10.1074\/jbc.M408374200","article-title":"ErbB4 expression in neural progenitor cells (ST14A) is necessary to mediate neuregulin-1beta1-induced migration","volume":"279","author":"Gambarotta","year":"2004","journal-title":"J Biol Chem"},{"key":"2020062010532695300_ref37","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1016\/S0166-4328(99)00175-8","article-title":"Heregulin, but not ErbB2 or ErbB3, heterozygous mutant mice exhibit hyperactivity in multiple behavioral tasks","volume":"109","author":"Gerlai","year":"2000","journal-title":"Behav Brain Res"},{"key":"2020062010532695300_ref38","doi-asserted-by":"crossref","first-page":"8174","DOI":"10.1073\/pnas.0402680101","article-title":"Dynamic mapping of human cortical development during childhood through early adulthood","volume":"101","author":"Gogtay","year":"2004","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2020062010532695300_ref39","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1016\/0165-3806(82)90146-8","article-title":"Postnatal development of monoamine content and synthesis in the cerebral cortex of rhesus monkeys","volume":"256","author":"Goldman-Rakic","year":"1982","journal-title":"Brain Res"},{"key":"2020062010532695300_ref40","doi-asserted-by":"crossref","first-page":"2681","DOI":"10.1038\/sj.onc.1202631","article-title":"Neuregulin-4: a novel growth factor that acts through the ErbB-4 receptor tyrosine kinase","volume":"18","author":"Harari","year":"1999","journal-title":"Oncogene"},{"key":"2020062010532695300_ref41","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1038\/sj.mp.4001434","article-title":"Expression analysis of neuregulin-1 in the dorsolateral prefrontal cortex in schizophrenia","volume":"9","author":"Hashimoto","year":"2004","journal-title":"Mol Psychiatry"},{"key":"2020062010532695300_ref42","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1101\/gad.338505","article-title":"Identification of the scaramanga gene implicates Neuregulin3 in mammary gland specification","volume":"19","author":"Howard","year":"2005","journal-title":"Genes Dev."},{"key":"2020062010532695300_ref43","doi-asserted-by":"crossref","first-page":"704","DOI":"10.1111\/gtc.12169","article-title":"Formation of nuclear bodies by the lncRNA Gomafu-associating proteins Celf3 and SF1","volume":"19","author":"Ishizuka","year":"2014","journal-title":"Genes Cells."},{"key":"2020062010532695300_ref44","doi-asserted-by":"crossref","first-page":"2614","DOI":"10.3892\/mmr.2016.5542","article-title":"Neuregulin-1 (Nrg1) signaling has a preventive role and is altered in the frontal cortex under the pathological conditions of Alzheimer's disease","volume":"14","author":"Jiang","year":"2016","journal-title":"Mol Med Rep"},{"key":"2020062010532695300_ref45","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/S0169-328X(00)00257-6","article-title":"Expression of TMEFF1 mRNA in the mouse central nervous system: precise examination and comparative studies of TMEFF1 and TMEFF2","volume":"86","author":"Kanemoto","year":"2001","journal-title":"Brain Res Mol Brain Res"},{"key":"2020062010532695300_ref46","doi-asserted-by":"crossref","first-page":"15619","DOI":"10.1073\/pnas.1005410107","article-title":"Common genetic variation in Neuregulin 3 (NRG3) influences risk for schizophrenia and impacts NRG3 expression in human brain","volume":"107","author":"Kao","year":"2010","journal-title":"Proc Natl Acad Sci U S A."},{"key":"2020062010532695300_ref47","doi-asserted-by":"crossref","first-page":"1045","DOI":"10.1016\/j.bbrc.2004.07.066","article-title":"Neuroglycan C, a novel member of the neuregulin family","volume":"321","author":"Kinugasa","year":"2004","journal-title":"Biochem Biophys Res Commun"},{"key":"2020062010532695300_ref48","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1093\/hmg\/ddl449","article-title":"Disease-associated intronic variants in the ErbB4 gene are related to altered ErbB4 splice-variant expression in the brain in schizophrenia","volume":"16","author":"Law","year":"2007","journal-title":"Hum Mol Genet"},{"key":"2020062010532695300_ref49","doi-asserted-by":"crossref","first-page":"6747","DOI":"10.1073\/pnas.0602002103","article-title":"Neuregulin 1 transcripts are differentially expressed in schizophrenia and regulated by 5' SNPs associated with the disease","volume":"103","author":"Law","year":"2006","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2020062010532695300_ref50","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1016\/j.neuron.2007.03.028","article-title":"The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity","volume":"54","author":"Li","year":"2007","journal-title":"Neuron"},{"key":"2020062010532695300_ref51","doi-asserted-by":"crossref","first-page":"8491","DOI":"10.1523\/JNEUROSCI.5317-10.2011","article-title":"Specific regulation of NRG1 isoform expression by neuronal activity","volume":"31","author":"Liu","year":"2011","journal-title":"J Neurosci"},{"key":"2020062010532695300_ref52","doi-asserted-by":"crossref","first-page":"8885","DOI":"10.1523\/JNEUROSCI.2476-04.2004","article-title":"Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development","volume":"24","author":"Liu","year":"2004","journal-title":"J Neurosci"},{"key":"2020062010532695300_ref53","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1002\/cne.20016","article-title":"Neuregulin-2 is developmentally regulated and targeted to dendrites of central neurons","volume":"472","author":"Longart","year":"2004","journal-title":"J Comp Neurol"},{"key":"2020062010532695300_ref54","doi-asserted-by":"crossref","first-page":"648","DOI":"10.1016\/j.biopsych.2014.02.011","article-title":"Neuregulin-3 in the mouse medial prefrontal cortex regulates impulsive action","volume":"76","author":"Loos","year":"2014","journal-title":"Biol Psychiatry"},{"key":"2020062010532695300_ref55","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/j.ejphar.2016.04.015","article-title":"Prefrontal cortical neuregulin-ErbB modulation of inhibitory control in rats","volume":"781","author":"Loos","year":"2016","journal-title":"Eur J Pharmacol"},{"key":"2020062010532695300_ref56","doi-asserted-by":"crossref","first-page":"1828","DOI":"10.1002\/cne.23262","article-title":"Periadolescent maturation of the prefrontal cortex is sex-specific and is disrupted by prenatal stress","volume":"521","author":"Markham","year":"2013","journal-title":"J Comp Neurol"},{"key":"2020062010532695300_ref57","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.neuroscience.2007.04.066","article-title":"Developmental profile of neuregulin receptor ErbB4 in postnatal rat cerebral cortex and hippocampus","volume":"148","author":"Mechawar","year":"2007","journal-title":"Neuroscience"},{"key":"2020062010532695300_ref58","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/j.neuron.2014.06.007","article-title":"Neuregulin-ERBB signaling in the nervous system and neuropsychiatric diseases","volume":"83","author":"Mei","year":"2014","journal-title":"Neuron"},{"key":"2020062010532695300_ref59","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1038\/nrn2392","article-title":"Neuregulin 1 in neural development, synaptic plasticity and schizophrenia","volume":"9","author":"Mei","year":"2008","journal-title":"Nat Rev Neurosci"},{"key":"2020062010532695300_ref60","doi-asserted-by":"crossref","first-page":"716","DOI":"10.1073\/pnas.0706729105","article-title":"Specific expression of long noncoding RNAs in the mouse brain","volume":"105","author":"Mercer","year":"2008","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2020062010532695300_ref61","doi-asserted-by":"crossref","first-page":"1064","DOI":"10.1073\/pnas.91.3.1064","article-title":"Distinct isoforms of neuregulin are expressed in mesenchymal and neuronal cells during mouse development","volume":"91","author":"Meyer","year":"1994","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2020062010532695300_ref62","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1038\/378386a0","article-title":"Multiple essential functions of neuregulin in development","volume":"378","author":"Meyer","year":"1995","journal-title":"Nature"},{"key":"2020062010532695300_ref63","doi-asserted-by":"crossref","first-page":"3575","DOI":"10.1242\/dev.124.18.3575","article-title":"Isoform-specific expression and function of neuregulin","volume":"124","author":"Meyer","year":"1997","journal-title":"Development"},{"key":"2020062010532695300_ref64","doi-asserted-by":"crossref","first-page":"700","DOI":"10.1126\/science.1095862","article-title":"Axonal neuregulin-1 regulates myelin sheath thickness","volume":"304","author":"Michailov","year":"2004","journal-title":"Science"},{"key":"2020062010532695300_ref65","doi-asserted-by":"crossref","first-page":"582","DOI":"10.1111\/jnc.14664","article-title":"Poor transcript-protein correlation in the brain: negatively correlating gene products reveal neuronal polarity as a potential cause","volume":"149","author":"Moritz","year":"2019","journal-title":"J Neurochem."},{"key":"2020062010532695300_ref66","doi-asserted-by":"crossref","first-page":"636","DOI":"10.1016\/j.biopsych.2011.04.016","article-title":"Conserved interneuron-specific ErbB4 expression in frontal cortex of rodents, monkeys, and humans: implications for schizophrenia","volume":"70","author":"Neddens","year":"2011","journal-title":"Biol Psychiatry"},{"key":"2020062010532695300_ref67","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1038\/mp.2008.150","article-title":"A 5\u2032 promoter region SNP in NRG1 is associated with schizophrenia risk and type III isoform expression","volume":"14","author":"Nicodemus","year":"2009","journal-title":"Mol Psychiatry"},{"key":"2020062010532695300_ref68","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1093\/schbul\/sbx122","article-title":"Overexpression of Neuregulin 1 type III confers hippocampal mRNA alterations and schizophrenia-like behaviors in mice","volume":"44","author":"Olaya","year":"2018","journal-title":"Schizophr Bull"},{"key":"2020062010532695300_ref69","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1016\/S0168-0102(98)00013-3","article-title":"Expression of receptors for neuregulins, ErbB2, ErbB3 and ErbB4, in developing mouse cerebellum","volume":"30","author":"Ozaki","year":"1998","journal-title":"Neurosci Res"},{"key":"2020062010532695300_ref70","doi-asserted-by":"crossref","first-page":"4859","DOI":"10.1523\/JNEUROSCI.4632-15.2016","article-title":"Behavioral, neurophysiological, and synaptic impairment in a transgenic Neuregulin1 (NRG1-IV) murine schizophrenia model","volume":"36","author":"Papaleo","year":"2016","journal-title":"J Neurosci"},{"key":"2020062010532695300_ref71","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0104172","article-title":"Transient overexposure of neuregulin 3 during early postnatal development impacts selective behaviors in adulthood","volume":"9","author":"Paterson","year":"2014","journal-title":"PLoS One"},{"key":"2020062010532695300_ref72","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1176\/appi.ajp.2016.16060721","article-title":"Temporal, diagnostic, and tissue-specific regulation of NRG3 isoform expression in human brain development and affective disorders","volume":"174","author":"Paterson","year":"2017","journal-title":"Am J Psychiatry"},{"key":"2020062010532695300_ref73","doi-asserted-by":"crossref","first-page":"979","DOI":"10.1176\/appi.ajp.2014.13111518","article-title":"Effects of schizophrenia risk variation in the NRG1 gene on NRG1-IV splicing during fetal and early postnatal human neocortical development","volume":"171","author":"Paterson","year":"2014","journal-title":"Am J Psychiatry"},{"year":"2012","author":"Paxinos","key":"2020062010532695300_ref74a"},{"key":"2020062010532695300_ref74","doi-asserted-by":"crossref","first-page":"2803","DOI":"10.1038\/sj.onc.1201466","article-title":"Differential expression of NDF\/neuregulin receptors ErbB-3 and ErbB-4 and involvement in inhibition of neuronal differentiation","volume":"15","author":"Pinkas-Kramarski","year":"1997","journal-title":"Oncogene"},{"key":"2020062010532695300_ref75","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1002\/cne.24559","article-title":"Developmental expression of Neuregulin-3 in the rat central nervous system","volume":"527","author":"Rahman","year":"2019","journal-title":"J Comp Neurol"},{"issue":"Suppl 3","key":"2020062010532695300_ref76","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1289\/ehp.00108s3511","article-title":"Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models","volume":"108","author":"Rice","year":"2000","journal-title":"Environ Health Perspect"},{"key":"2020062010532695300_ref77","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1016\/j.gde.2010.12.010","article-title":"Neuregulin signaling, cortical circuitry development and schizophrenia","volume":"21","author":"Rico","year":"2011","journal-title":"Curr Opin Genet Dev"},{"key":"2020062010532695300_ref78","doi-asserted-by":"crossref","first-page":"8131","DOI":"10.1073\/pnas.0702157104","article-title":"Loss of erbB signaling in oligodendrocytes alters myelin and dopaminergic function, a potential mechanism for neuropsychiatric disorders","volume":"104","author":"Roy","year":"2007","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2020062010532695300_ref79","doi-asserted-by":"crossref","first-page":"1403","DOI":"10.1001\/archneur.58.9.1403","article-title":"Selective preservation and degeneration within the prefrontal cortex in aging and Alzheimer disease","volume":"58","author":"Salat","year":"2001","journal-title":"Arch Neurol"},{"key":"2020062010532695300_ref80","doi-asserted-by":"crossref","first-page":"4419","DOI":"10.1523\/JNEUROSCI.5714-09.2010","article-title":"Longitudinal magnetic resonance imaging study of cortical development through early childhood in autism","volume":"30","author":"Schumann","year":"2010","journal-title":"J Neurosci"},{"key":"2020062010532695300_ref81","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1038\/nn1008","article-title":"Mapping cortical change across the human life span","volume":"6","author":"Sowell","year":"2003","journal-title":"Nat Neurosci"},{"key":"2020062010532695300_ref82","doi-asserted-by":"crossref","first-page":"494","DOI":"10.1006\/exnr.1999.7163","article-title":"Differential expression of ErbB3 and ErbB4 neuregulin receptors in dopamine neurons and forebrain areas of the adult rat","volume":"159","author":"Steiner","year":"1999","journal-title":"Exp Neurol"},{"key":"2020062010532695300_ref83","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.gene.2004.07.029","article-title":"Multiple novel transcription initiation sites for NRG1","volume":"342","author":"Steinthorsdottir","year":"2004","journal-title":"Gene"},{"key":"2020062010532695300_ref84","doi-asserted-by":"crossref","first-page":"373","DOI":"10.3389\/fncel.2014.00373","article-title":"De-regulation of gene expression and alternative splicing affects distinct cellular pathways in the aging hippocampus","volume":"8","author":"Stilling","year":"2014","journal-title":"Front Cell Neurosci"},{"key":"2020062010532695300_ref85","doi-asserted-by":"crossref","first-page":"4275","DOI":"10.1091\/mbc.e10-04-0332","article-title":"Cell death or survival promoted by alternative isoforms of ErbB4","volume":"21","author":"Sundvall","year":"2010","journal-title":"Mol Biol Cell"},{"key":"2020062010532695300_ref86","doi-asserted-by":"crossref","first-page":"24343","DOI":"10.1074\/jbc.M702953200","article-title":"Molecular cloning of a brain-specific, developmentally regulated neuregulin 1 (NRG1) isoform and identification of a functional promoter variant associated with schizophrenia","volume":"282","author":"Tan","year":"2007","journal-title":"J Biol Chem"},{"key":"2020062010532695300_ref87","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1038\/npp.2009.115","article-title":"Normal development of brain circuits","volume":"35","author":"Tau","year":"2010","journal-title":"Neuropsychopharmacology"},{"key":"2020062010532695300_ref88","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.brainres.2006.11.047","article-title":"Widespread expression of ErbB2, ErbB3 and ErbB4 in non-human primate brain","volume":"1139","author":"Thompson","year":"2007","journal-title":"Brain Res"},{"key":"2020062010532695300_ref89","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1111\/j.1365-2443.2011.01502.x","article-title":"Competition between a noncoding exon and introns: Gomafu contains tandem UACUAAC repeats and associates with splicing factor-1","volume":"16","author":"Tsuiji","year":"2011","journal-title":"Genes Cells."},{"key":"2020062010532695300_ref90","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1159\/000430095","article-title":"Sequence of molecular events during the maturation of the developing mouse prefrontal cortex","volume":"1","author":"Ueda","year":"2015","journal-title":"Mol Neuropsychiatry"},{"key":"2020062010532695300_ref91","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1038\/nrg3185","article-title":"Insights into the regulation of protein abundance from proteomic and transcriptomic analyses","volume":"13","author":"Vogel","year":"2012","journal-title":"Nat Rev Genet."},{"key":"2020062010532695300_ref92","doi-asserted-by":"crossref","first-page":"7222","DOI":"10.1038\/ncomms8222","article-title":"A negative feedback loop controls NMDA receptor function in cortical interneurons via neuregulin 2\/ErbB4 signalling","volume":"6","author":"Vullhorst","year":"2015","journal-title":"Nat Commun"},{"key":"2020062010532695300_ref93","doi-asserted-by":"crossref","first-page":"13105","DOI":"10.1073\/pnas.1811287115","article-title":"Genetic recovery of ErbB4 in adulthood partially restores brain functions in null mice","volume":"115","author":"Wang","year":"2018","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2020062010532695300_ref94","doi-asserted-by":"crossref","first-page":"2028","DOI":"10.1038\/npp.2009.20","article-title":"Cell type-specific development of NMDA receptors in the interneurons of rat prefrontal cortex","volume":"34","author":"Wang","year":"2009","journal-title":"Neuropsychopharmacology"},{"key":"2020062010532695300_ref95","doi-asserted-by":"crossref","first-page":"31692","DOI":"10.1038\/srep31692","article-title":"Neuregulin 1 improves cognitive deficits and neuropathology in an Alzheimer's disease model","volume":"6","author":"Xu","year":"2016","journal-title":"Sci Rep"},{"key":"2020062010532695300_ref96","doi-asserted-by":"crossref","first-page":"1233","DOI":"10.1038\/mp.2017.22","article-title":"Neuregulin-2 ablation results in dopamine dysregulation and severe behavioral phenotypes relevant to psychiatric disorders","volume":"23","author":"Yan","year":"2018","journal-title":"Mol Psychiatry"},{"key":"2020062010532695300_ref97","doi-asserted-by":"crossref","first-page":"19724","DOI":"10.1523\/JNEUROSCI.1584-13.2013","article-title":"Development of GABA circuitry of fast-spiking basket interneurons in the medial prefrontal cortex of erbb4-mutant mice","volume":"33","author":"Yang","year":"2013","journal-title":"J Neurosci"},{"key":"2020062010532695300_ref98","doi-asserted-by":"crossref","first-page":"9562","DOI":"10.1073\/pnas.94.18.9562","article-title":"Neuregulin-3 (NRG3): a novel neural tissue-enriched protein that binds and activates ErbB4","volume":"94","author":"Zhang","year":"1997","journal-title":"Proc Natl Acad Sci U S A"}],"container-title":["Cerebral Cortex"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/cercor\/article-pdf\/30\/5\/3325\/33411388\/bhz312.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/cercor\/article-pdf\/30\/5\/3325\/33411388\/bhz312.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,10,7]],"date-time":"2022-10-07T12:23:05Z","timestamp":1665145385000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/cercor\/article\/30\/5\/3325\/5688725"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,1,2]]},"references-count":99,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2020,1,2]]},"published-print":{"date-parts":[[2020,5,14]]}},"URL":"https:\/\/doi.org\/10.1093\/cercor\/bhz312","relation":{},"ISSN":["1047-3211","1460-2199"],"issn-type":[{"type":"print","value":"1047-3211"},{"type":"electronic","value":"1460-2199"}],"subject":[],"published-other":{"date-parts":[[2020,5]]},"published":{"date-parts":[[2020,1,2]]}}}