{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,15]],"date-time":"2026-04-15T05:56:58Z","timestamp":1776232618351,"version":"3.50.1"},"reference-count":67,"publisher":"Public Library of Science (PLoS)","issue":"12","license":[{"start":{"date-parts":[[2013,12,12]],"date-time":"2013-12-12T00:00:00Z","timestamp":1386806400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosgenetics.org"],"crossmark-restriction":false},"short-container-title":["PLoS Genet"],"DOI":"10.1371\/journal.pgen.1004017","type":"journal-article","created":{"date-parts":[[2013,12,12]],"date-time":"2013-12-12T21:32:51Z","timestamp":1386883971000},"page":"e1004017","update-policy":"https:\/\/doi.org\/10.1371\/journal.pgen.corrections_policy","source":"Crossref","is-referenced-by-count":31,"title":["Histone Methylation Restrains the Expression of Subtype-Specific Genes during Terminal Neuronal Differentiation in Caenorhabditis elegans"],"prefix":"10.1371","volume":"9","author":[{"given":"Chaogu","family":"Zheng","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Siavash","family":"Karimzadegan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Victor","family":"Chiang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Martin","family":"Chalfie","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2013,12,12]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1016\/j.gde.2004.07.006","article-title":"Epigenetic control of neural stem cell fate","volume":"14","author":"J Hsieh","year":"2004","journal-title":"Curr Opin Genet Dev"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1038\/nature04733","article-title":"Polycomb complexes repress developmental regulators in murine embryonic stem cells","volume":"441","author":"LA Boyer","year":"2006","journal-title":"Nature"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1016\/j.cell.2006.02.043","article-title":"Control of developmental regulators by Polycomb in human embryonic stem cells","volume":"125","author":"TI Lee","year":"2006","journal-title":"Cell"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"1559","DOI":"10.1002\/stem.82","article-title":"Maintenance of undifferentiated state and self-renewal of embryonic neural stem cells by Polycomb protein Ring1B","volume":"27","author":"M Roman-Trufero","year":"2009","journal-title":"Stem Cells"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"1445","DOI":"10.1016\/j.cub.2008.08.047","article-title":"A self-regulating feed-forward circuit controlling C. elegans egg-laying behavior","volume":"18","author":"M Zhang","year":"2008","journal-title":"Curr Biol"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"8060","DOI":"10.1523\/JNEUROSCI.23-22-08060.2003","article-title":"Genetic and cellular basis for acetylcholine inhibition of Caenorhabditis elegans egg-laying behavior","volume":"23","author":"IA Bany","year":"2003","journal-title":"J Neurosci"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1101\/gad.1502107","article-title":"UNC-4 represses CEH-12\/HB9 to specify synaptic inputs to VA motor neurons in C. elegans","volume":"21","author":"SE Von Stetina","year":"2007","journal-title":"Genes Dev"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"875","DOI":"10.1016\/S1097-2765(03)00400-3","article-title":"Nucleotide binding by the Mdm2 RING domain facilitates Arf-independent Mdm2 nucleolar localization","volume":"12","author":"MV Poyurovsky","year":"2003","journal-title":"Mol Cell"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"17131","DOI":"10.1073\/pnas.262544899","article-title":"Glutamine\/proline-rich PQE-1 proteins protect Caenorhabditis elegans neurons from huntingtin polyglutamine neurotoxicity","volume":"99","author":"PW Faber","year":"2002","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1002\/1096-9861(20000101)429:1<127::AID-CNE10>3.0.CO;2-H","article-title":"IDA-1, a Caenorhabditis elegans homolog of the diabetic autoantigens IA-2 and phogrin, is expressed in peptidergic neurons in the worm","volume":"429","author":"TR Zahn","year":"2001","journal-title":"J Comp Neurol"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1098\/rstb.1986.0056","article-title":"The structure of the nervous system of the nematode Caenorhabditis elegans","volume":"314","author":"JG White","year":"1986","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.gene.2012.01.003","article-title":"Structural biology of the chromodomain: form and function","volume":"496","author":"JC Eissenberg","year":"2012","journal-title":"Gene"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"2991","DOI":"10.1242\/dev.009373","article-title":"Two C. elegans histone methyltransferases repress lin-3 EGF transcription to inhibit vulval development","volume":"134","author":"EC Andersen","year":"2007","journal-title":"Development"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"e1003089","DOI":"10.1371\/journal.pgen.1003089","article-title":"Histone methyltransferases MES-4 and MET-1 promote meiotic checkpoint activation in Caenorhabditis elegans","volume":"8","author":"P Lamelza","year":"2012","journal-title":"PLoS Genet"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1242\/dev.02698","article-title":"Histone methylation is required for oogenesis in Drosophila","volume":"134","author":"E Clough","year":"2007","journal-title":"Development"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1101\/gad.973302","article-title":"SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins","volume":"16","author":"DC Schultz","year":"2002","journal-title":"Genes Dev"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"934","DOI":"10.1016\/j.cell.2012.06.051","article-title":"Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery","volume":"150","author":"BD Towbin","year":"2012","journal-title":"Cell"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.gde.2007.02.006","article-title":"Global patterns of histone modifications","volume":"17","author":"OJ Rando","year":"2007","journal-title":"Curr Opin Genet Dev"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"e1001091","DOI":"10.1371\/journal.pgen.1001091","article-title":"The histone H3K36 methyltransferase MES-4 acts epigenetically to transmit the memory of germline gene expression to progeny","volume":"6","author":"A Rechtsteiner","year":"2010","journal-title":"PLoS Genet"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1016\/j.ydbio.2006.06.039","article-title":"Unique and redundant functions of C. elegans HP1 proteins in post-embryonic development","volume":"298","author":"S Schott","year":"2006","journal-title":"Dev Biol"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"e1002940","DOI":"10.1371\/journal.pgen.1002940","article-title":"Transcriptional repression of Hox genes by C. elegans HP1\/HPL and H1\/HIS-24","volume":"8","author":"M Studencka","year":"2012","journal-title":"PLoS Genet"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1128\/MCB.05229-11","article-title":"Novel roles of Caenorhabditis elegans heterochromatin protein HP1 and linker histone in the regulation of innate immune gene expression","volume":"32","author":"M Studencka","year":"2012","journal-title":"Mol Cell Biol"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1534\/g3.112.002832","article-title":"Mutations in the pqe-1 gene enhance transgene expression in Caenorhabditis elegans","volume":"2","author":"K Yamada","year":"2012","journal-title":"G3 (Bethesda)"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"877","DOI":"10.1038\/nmeth.1253","article-title":"Imaging individual mRNA molecules using multiple singly labeled probes","volume":"5","author":"A Raj","year":"2008","journal-title":"Nat Methods"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1093\/embo-reports\/kvf051","article-title":"A heterochromatin protein 1 homologue in Caenorhabditis elegans acts in germline and vulval development","volume":"3","author":"F Couteau","year":"2002","journal-title":"EMBO Rep"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1016\/j.devcel.2006.04.001","article-title":"SynMuv genes redundantly inhibit lin-3\/EGF expression to prevent inappropriate vulval induction in C. elegans","volume":"10","author":"M Cui","year":"2006","journal-title":"Dev Cell"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1016\/S1097-2765(01)00194-0","article-title":"dpl-1 DP and efl-1 E2F act with lin-35 Rb to antagonize Ras signaling in C. elegans vulval development","volume":"7","author":"CJ Ceol","year":"2001","journal-title":"Mol Cell"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1016\/j.ydbio.2006.04.474","article-title":"The C. elegans HP1 homologue HPL-2 and the LIN-13 zinc finger protein form a complex implicated in vulval development","volume":"297","author":"V Coustham","year":"2006","journal-title":"Dev Biol"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1534\/genetics.106.069633","article-title":"LIN-61, one of two Caenorhabditis elegans malignant-brain-tumor-repeat-containing proteins, acts with the DRM and NuRD-like protein complexes in vulval development but not in certain other biological processes","volume":"176","author":"MM Harrison","year":"2007","journal-title":"Genetics"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"e1002017","DOI":"10.1371\/journal.pgen.1002017","article-title":"H3K9me2\/3 binding of the MBT domain protein LIN-61 is essential for Caenorhabditis elegans vulva development","volume":"7","author":"N Koester-Eiserfunke","year":"2011","journal-title":"PLoS Genet"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1534\/genetics.106.056465","article-title":"Identification and classification of genes that act antagonistically to let-60 Ras signaling in Caenorhabditis elegans vulval development","volume":"173","author":"CJ Ceol","year":"2006","journal-title":"Genetics"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"2830","DOI":"10.1523\/JNEUROSCI.3344-05.2006","article-title":"Differential contributions of Caenorhabditis elegans histone deacetylases to huntingtin polyglutamine toxicity","volume":"26","author":"EA Bates","year":"2006","journal-title":"J Neurosci"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1016\/0896-6273(90)90195-L","article-title":"Organogenesis in C. elegans: positioning of neurons and muscles in the egg-laying system","volume":"4","author":"C Li","year":"1990","journal-title":"Neuron"},{"key":"ref34","first-page":"1","article-title":"RTK\/Ras\/MAPK signaling","author":"MV Sundaram","year":"2006","journal-title":"WormBook"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"340","DOI":"10.1038\/356340a0","article-title":"C. elegans cell-signalling gene sem-5 encodes a protein with SH2 and SH3 domains","volume":"356","author":"SG Clark","year":"1992","journal-title":"Nature"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"742","DOI":"10.1101\/gad.9.6.742","article-title":"MEK-2, a Caenorhabditis elegans MAP kinase kinase, functions in Ras-mediated vulval induction and other developmental events","volume":"9","author":"Y Wu","year":"1995","journal-title":"Genes Dev"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1016\/0092-8674(95)90317-8","article-title":"Different levels of the C. elegans growth factor LIN-3 promote distinct vulval precursor fates","volume":"82","author":"WS Katz","year":"1995","journal-title":"Cell"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/S0960-9822(99)80112-2","article-title":"Reciprocal EGF signaling back to the uterus from the induced C. elegans vulva coordinates morphogenesis of epithelia","volume":"9","author":"C Chang","year":"1999","journal-title":"Curr Biol"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1016\/0092-8674(83)90377-X","article-title":"The lin-12 locus specifies cell fates in Caenorhabditis elegans","volume":"34","author":"IS Greenwald","year":"1983","journal-title":"Cell"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"3149","DOI":"10.1101\/gad.9.24.3149","article-title":"The Caenorhabditis elegans gene lin-1 encodes an ETS-domain protein and defines a branch of the vulval induction pathway","volume":"9","author":"GJ Beitel","year":"1995","journal-title":"Genes Dev"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"876","DOI":"10.1038\/344876a0","article-title":"Novel cysteine-rich motif and homeodomain in the product of the Caenorhabditis elegans cell lineage gene lin-11","volume":"344","author":"G Freyd","year":"1990","journal-title":"Nature"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"2589","DOI":"10.1242\/dev.00500","article-title":"The C. elegans LIM homeobox gene lin-11 specifies multiple cell fates during vulval development","volume":"130","author":"BP Gupta","year":"2003","journal-title":"Development"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"941","DOI":"10.1016\/j.cell.2004.12.012","article-title":"Histone demethylation mediated by the nuclear amine oxidase homolog LSD1","volume":"119","author":"Y Shi","year":"2004","journal-title":"Cell"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1038\/nature04020","article-title":"LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription","volume":"437","author":"E Metzger","year":"2005","journal-title":"Nature"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1016\/j.cell.2009.02.015","article-title":"A C. elegans LSD1 demethylase contributes to germline immortality by reprogramming epigenetic memory","volume":"137","author":"DJ Katz","year":"2009","journal-title":"Cell"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1016\/j.cell.2006.04.024","article-title":"Structural insights into histone demethylation by JMJD2 family members","volume":"125","author":"Z Chen","year":"2006","journal-title":"Cell"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1016\/j.cell.2006.03.028","article-title":"Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases","volume":"125","author":"JR Whetstine","year":"2006","journal-title":"Cell"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"2101","DOI":"10.4161\/cc.8.13.8927","article-title":"Lung cancer-associated JmjC domain protein mdig suppresses formation of tri-methyl lysine 9 of histone H3","volume":"8","author":"Y Lu","year":"2009","journal-title":"Cell Cycle"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"2001","DOI":"10.1523\/JNEUROSCI.21-06-02001.2001","article-title":"Regulation of neurotransmitter vesicles by the homeodomain protein UNC-4 and its transcriptional corepressor UNC-37\/groucho in Caenorhabditis elegans cholinergic motor neurons","volume":"21","author":"KM Lickteig","year":"2001","journal-title":"J Neurosci"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"560","DOI":"10.1038\/35000609","article-title":"Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant","volume":"403","author":"JY Sze","year":"2000","journal-title":"Nature"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"1168","DOI":"10.1038\/nn.2186","article-title":"FMRFamide neuropeptides and acetylcholine synergistically inhibit egg-laying by C. elegans","volume":"11","author":"N Ringstad","year":"2008","journal-title":"Nat Neurosci"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"36143","DOI":"10.1074\/jbc.M705811200","article-title":"A novel CpG-free vertebrate insulator silences the testis-specific SP-10 gene in somatic tissues: role for TDP-43 in insulator function","volume":"282","author":"MM Abhyankar","year":"2007","journal-title":"J Biol Chem"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"26304","DOI":"10.1074\/jbc.M110.125039","article-title":"Interaction with polyglutamine aggregates reveals a Q\/N-rich domain in TDP-43","volume":"285","author":"RA Fuentealba","year":"2010","journal-title":"J Biol Chem"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1016\/j.cell.2005.03.013","article-title":"REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis","volume":"121","author":"N Ballas","year":"2005","journal-title":"Cell"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1038\/nature06863","article-title":"REST maintains self-renewal and pluripotency of embryonic stem cells","volume":"453","author":"SK Singh","year":"2008","journal-title":"Nature"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"16659","DOI":"10.1073\/pnas.0407643101","article-title":"Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells","volume":"101","author":"J Hsieh","year":"2004","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"2484","DOI":"10.1101\/gad.1837309","article-title":"SetDB1 contributes to repression of genes encoding developmental regulators and maintenance of ES cell state","volume":"23","author":"S Bilodeau","year":"2009","journal-title":"Genes Dev"},{"key":"ref58","doi-asserted-by":"crossref","first-page":"11341","DOI":"10.1158\/0008-5472.CAN-06-1570","article-title":"Androgen receptor coactivators lysine-specific histone demethylase 1 and four and a half LIM domain protein 2 predict risk of prostate cancer recurrence","volume":"66","author":"P Kahl","year":"2006","journal-title":"Cancer Res"},{"key":"ref59","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1093\/emboj\/19.3.359","article-title":"FHL2, a novel tissue-specific coactivator of the androgen receptor","volume":"19","author":"JM Muller","year":"2000","journal-title":"EMBO J"},{"key":"ref60","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1242\/dev.117.3.1071","article-title":"Cell interactions control the direction of outgrowth, branching and fasciculation of the HSN axons of Caenorhabditis elegans","volume":"117","author":"G Garriga","year":"1993","journal-title":"Development"},{"key":"ref61","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1073\/pnas.1111628109","article-title":"Lysine methyltransferase G9a methylates the transcription factor MyoD and regulates skeletal muscle differentiation","volume":"109","author":"BM Ling","year":"2012","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref62","doi-asserted-by":"crossref","first-page":"7219","DOI":"10.1093\/nar\/gks399","article-title":"The histone demethylase Kdm3a is essential to progression through differentiation","volume":"40","author":"M Herzog","year":"2012","journal-title":"Nucleic Acids Res"},{"key":"ref63","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1093\/genetics\/77.1.71","article-title":"The genetics of Caenorhabditis elegans","volume":"77","author":"S Brenner","year":"1974","journal-title":"Genetics"},{"key":"ref64","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1038\/nmeth.1249","article-title":"Caenorhabditis elegans mutant allele identification by whole-genome sequencing","volume":"5","author":"S Sarin","year":"2008","journal-title":"Nat Methods"},{"key":"ref65","doi-asserted-by":"crossref","first-page":"549","DOI":"10.1038\/nmeth.f.260","article-title":"MAQGene: software to facilitate C. elegans mutant genome sequence analysis","volume":"6","author":"H Bigelow","year":"2009","journal-title":"Nat Methods"},{"key":"ref66","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/S0091-679X(08)61390-4","article-title":"Laser killing of cells in Caenorhabditis elegans","volume":"48","author":"CI Bargmann","year":"1995","journal-title":"Methods Cell Biol"},{"key":"ref67","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/S0092-8674(00)80998-8","article-title":"EGL-10 regulates G protein signaling in the C. elegans nervous system and shares a conserved domain with many mammalian proteins","volume":"84","author":"MR Koelle","year":"1996","journal-title":"Cell"}],"container-title":["PLoS Genetics"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pgen.1004017","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,3,19]],"date-time":"2022-03-19T16:40:05Z","timestamp":1647708005000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pgen.1004017"}},"subtitle":[],"editor":[{"given":"Julie","family":"Ahringer","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2013,12,12]]},"references-count":67,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2013,12,12]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pgen.1004017","relation":{},"ISSN":["1553-7404"],"issn-type":[{"value":"1553-7404","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013,12,12]]}}}