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Gaucher              J, Boussouar              F, Montellier              E, Curtet              S, Buchou              T, Bertrand              S, Hery              P, Jounier              S, Depaux              A, Vitte              AL, Guardiola              P, Pernet              K, Debernardi              A, Lopez              F, Holota              H, Imbert              J, Wolgemuth              DJ, G\u00e9rard              M, Rousseaux              S, Khochbin              S. Bromodomain-dependent stage-specific male genome programming            by Brdt. <i>EMBO J<\/i>          2012; 31: 3809\u20133820.","DOI":"10.1038\/emboj.2012.233"},{"key":"2","doi-asserted-by":"crossref","unstructured":"2.  Manterola              M, Brown              TM, Oh              MY, Garyn              C, Gonzalez              BJ, Wolgemuth              DJ. BRDT is an essential epigenetic regulator for proper            chromatin organization, silencing of sex chromosomes and crossover formation in male meiosis. <i>PLoS              Genet<\/i>          2018; 14: e1007209.","DOI":"10.1371\/journal.pgen.1007209"},{"key":"3","doi-asserted-by":"crossref","unstructured":"3.  Hu              J, Donahue              G, Dorsey              J, Govin              J, Yuan              Z, Garcia              BA, Shah              PP, Berger              SL. H4K44 acetylation facilitates chromatin accessibility during            meiosis. <i>Cell Rep<\/i>          2015; 13: 1772\u20131780.","DOI":"10.1016\/j.celrep.2015.10.070"},{"key":"4","doi-asserted-by":"crossref","unstructured":"4.  Rathke              C, Baarends              WM, Awe              S, Renkawitz-Pohl              R. Chromatin dynamics during spermiogenesis.              <i>Biochim Biophys Acta<\/i>          2014; 1839: 155\u2013168.","DOI":"10.1016\/j.bbagrm.2013.08.004"},{"key":"5","doi-asserted-by":"crossref","unstructured":"5.  Wang              T, Gao              H, Li              W, Liu              C. Essential role of histone replacement and modifications in            male fertility. <i>Front Genet<\/i>          2019; 10: 962.","DOI":"10.3389\/fgene.2019.00962"},{"key":"6","doi-asserted-by":"crossref","unstructured":"6.  Hazzouri              M, Pivot-Pajot              C, Faure              AK, Usson              Y, Pelletier              R, S\u00e8le              B, Khochbin              S, Rousseaux              S. Regulated hyperacetylation of core histones during mouse            spermatogenesis: involvement of histone deacetylases. <i>Eur J Cell Biol<\/i>          2000; 79: 950\u2013960.","DOI":"10.1078\/0171-9335-00123"},{"key":"7","doi-asserted-by":"crossref","unstructured":"7.  Ketchum              CC, Larsen              CD, McNeil              A, Meyer-Ficca              ML, Meyer              RG. Early histone H4 acetylation during chromatin remodeling in            equine spermatogenesis. <i>Biol Reprod<\/i>          2018; 98: 115\u2013129.","DOI":"10.1093\/biolre\/iox159"},{"key":"8","doi-asserted-by":"crossref","unstructured":"8.  Goudarzi              A, Shiota              H, Rousseaux              S, Khochbin              S. Genome-scale acetylation-dependent histone eviction during            spermatogenesis. <i>J Mol Biol<\/i>          2014; 426: 3342\u20133349.","DOI":"10.1016\/j.jmb.2014.02.023"},{"key":"9","doi-asserted-by":"crossref","unstructured":"9.  Shiota              H, Barral              S, Buchou              T, Tan              M, Cout\u00e9              Y, Charbonnier              G, Reynoird              N, Boussouar              F, G\u00e9rard              M, Zhu              M, Bargier              L, Puthier              D, Chuffart              F, Bourova-Flin              E, Picaud              S, Filippakopoulos              P, Goudarzi              A, Ibrahim              Z, Panne              D, Rousseaux              S, Zhao              Y, Khochbin              S. Nut directs p300-dependent, genome-wide H4 hyperacetylation in            male germ cells. <i>Cell Rep<\/i>          2018; 24: 3477\u20133487.e6.","DOI":"10.1016\/j.celrep.2018.08.069"},{"key":"10","doi-asserted-by":"crossref","unstructured":"10.  Luense              LJ, Donahue              G, Lin-Shiao              E, Rangel              R, Weller              AH, Bartolomei              MS, Berger              SL. Gcn5-mediated histone acetylation governs nucleosome dynamics            in spermiogenesis. <i>Dev Cell<\/i>          2019; 51: 745\u2013758.e6.","DOI":"10.1016\/j.devcel.2019.10.024"},{"key":"11","doi-asserted-by":"crossref","unstructured":"11.  Dong              Y, Isono              KI, Ohbo              K, Endo              TA, Ohara              O, Maekawa              M, Toyama              Y, Ito              C, Toshimori              K, Helin              K, Ogonuki              N, Inoue              K, Ogura              A, Yamagata              K, Kitabayashi              I, Koseki              H. EPC1\/TIP60-mediated histone acetylation facilitates            spermiogenesis in mice. <i>Mol Cell Biol<\/i>          2017; 37: e00082\u2013e17.","DOI":"10.1128\/MCB.00082-17"},{"key":"12","doi-asserted-by":"crossref","unstructured":"12.  Shang              E, Salazar              G, Crowley              TE, Wang              X, Lopez              RA, Wang              X, Wolgemuth              DJ. Identification of unique, differentiation stage-specific            patterns of expression of the bromodomain-containing genes Brd2, Brd3, Brd4, and Brdt in the mouse testis.              <i>Gene Expr Patterns<\/i>          2004; 4: 513\u2013519.","DOI":"10.1016\/j.modgep.2004.03.002"},{"key":"13","doi-asserted-by":"crossref","unstructured":"13.  Shang              E, Nickerson              HD, Wen              D, Wang              X, Wolgemuth              DJ. The first bromodomain of Brdt, a testis-specific member of            the BET sub-family of double-bromodomain-containing proteins, is essential for male germ cell differentiation.              <i>Development<\/i>          2007; 134: 3507\u20133515.","DOI":"10.1242\/dev.004481"},{"key":"14","doi-asserted-by":"crossref","unstructured":"14.  Berkovits              BD, Wolgemuth              DJ. The first bromodomain of the testis-specific double            bromodomain protein Brdt is required for chromocenter organization that is modulated by genetic background.              <i>Dev Biol<\/i>          2011; 360: 358\u2013368.","DOI":"10.1016\/j.ydbio.2011.10.005"},{"key":"15","doi-asserted-by":"crossref","unstructured":"15.  Fu              J, Zhang              J, Chen              X, Liu              Z, Yang              X, He              Z, Hao              Y, Liu              B, Yao              D. ATPase family AAA domain-containing protein 2 (ATAD2): From an            epigenetic modulator to cancer therapeutic target. <i>Theranostics<\/i>          2023; 13: 787\u2013809.","DOI":"10.7150\/thno.78840"},{"key":"16","doi-asserted-by":"crossref","unstructured":"16.  Morozumi              Y, Boussouar              F, Tan              M, Chaikuad              A, Jamshidikia              M, Colak              G, He              H, Nie              L, Petosa              C, de Dieuleveult              M, Curtet              S, Vitte              AL, Rabatel              C, Debernardi              A, Cosset              FL, Verhoeyen              E, Emadali              A, Schweifer              N, Gianni              D, Gut              M, Guardiola              P, Rousseaux              S, G\u00e9rard              M, Knapp              S, Zhao              Y, Khochbin              S. Atad2 is a generalist facilitator of chromatin dynamics in            embryonic stem cells. <i>J Mol Cell Biol<\/i>          2016; 8: 349\u2013362.","DOI":"10.1093\/jmcb\/mjv060"},{"key":"17","doi-asserted-by":"crossref","unstructured":"17.  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SYMPK Is required for meiosis and involved in alternative            splicing in male germ cells. <i>Front Cell Dev Biol<\/i>          2021; 9: 715733.","DOI":"10.3389\/fcell.2021.715733"},{"key":"19","doi-asserted-by":"crossref","unstructured":"19.  Crespo              M, Damont              A, Blanco              M, Lastrucci              E, Kennani              SE, Ialy-Radio              C, Khattabi              LE, Terrier              S, Louwagie              M, Kieffer-Jaquinod              S, Hesse              AM, Bruley              C, Chantalat              S, Govin              J, Fenaille              F, Battail              C, Cocquet              J, Pflieger              D. Multi-omic analysis of gametogenesis reveals a novel signature            at the promoters and distal enhancers of active genes. <i>Nucleic Acids Res<\/i>          2020; 48: 4115\u20134138.","DOI":"10.1093\/nar\/gkaa163"},{"key":"20","doi-asserted-by":"crossref","unstructured":"20.  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Mutual balance of histone deacetylases 1 and 2 and the acetyl            reader ATAD2 regulates the level of acetylation of histone H4 on nascent chromatin of human cells. <i>Mol              Cell Biol<\/i>          2020; 40: 40.","DOI":"10.1128\/MCB.00421-19"},{"key":"23","doi-asserted-by":"crossref","unstructured":"23.  Tropberger              P, Pott              S, Keller              C, Kamieniarz-Gdula              K, Caron              M, Richter              F, Li              G, Mittler              G, Liu              ET, B\u00fchler              M, Margueron              R, Schneider              R. Regulation of transcription through acetylation of H3K122 on            the lateral surface of the histone octamer. <i>Cell<\/i>          2013; 152: 859\u2013872.","DOI":"10.1016\/j.cell.2013.01.032"},{"key":"24","doi-asserted-by":"crossref","unstructured":"24.  Nitahara              K, Kawamura              A, Kitamura              Y, Kato              K, Namekawa              SH, Nishiyama              M. Chromatin remodeler CHD8 is required for spermatogonial            proliferation and early meiotic progression. <i>Nucleic Acids Res<\/i>          2024; 52: 2995\u20133010.","DOI":"10.1093\/nar\/gkad1256"},{"key":"25","doi-asserted-by":"crossref","unstructured":"25.  Tang              P, Argentaro              A, Pask              AJ, O\u2019Donnell              L, Marshall-Graves              J, Familari              M, Harley              VR. Localization of the chromatin remodelling protein, ATRX in            the adult testis. <i>J Reprod Dev<\/i>          2011; 57: 317\u2013321.","DOI":"10.1262\/jrd.20221"},{"key":"26","doi-asserted-by":"crossref","unstructured":"26.  Guarnera              L, D\u2019addona              M, Bravo-Perez              C, Visconte              V. 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