{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,15]],"date-time":"2025-12-15T14:16:15Z","timestamp":1765808175669,"version":"build-2065373602"},"reference-count":143,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2023,5,24]],"date-time":"2023-05-24T00:00:00Z","timestamp":1684886400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["PTDC\/BIA-BID\/28441\/2017","PTDC\/BIA-BID\/1606\/2020","DFA\/BD\/2020\/05582"],"award-info":[{"award-number":["PTDC\/BIA-BID\/28441\/2017","PTDC\/BIA-BID\/1606\/2020","DFA\/BD\/2020\/05582"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JDB"],"abstract":"<jats:p>Primary oocyte determination occurs in many organisms within a germ line cyst, a multicellular structure composed of interconnected germ cells. However, the structure of the cyst is itself highly diverse, which raises intriguing questions about the benefits of this stereotypical multicellular environment for female gametogenesis. Drosophila\u00a0melanogaster is a well-studied model for female gametogenesis, and numerous genes and pathways critical for the determination and differentiation of a viable female gamete have been identified. This review provides an up-to-date overview of Drosophila oocyte determination, with a particular emphasis on the mechanisms that regulate germ line gene expression.<\/jats:p>","DOI":"10.3390\/jdb11020021","type":"journal-article","created":{"date-parts":[[2023,5,25]],"date-time":"2023-05-25T02:00:55Z","timestamp":1684980055000},"page":"21","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Genetic and Epigenetic Regulation of Drosophila Oocyte Determination"],"prefix":"10.3390","volume":"11","author":[{"given":"Brigite","family":"Cabrita","sequence":"first","affiliation":[{"name":"Department of Medical Sciences, Institute of Biomedicine (iBiMED), University of Aveiro, Agra do Crasto, Edif\u00edcio 30, 3810-193 Aveiro, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1641-3403","authenticated-orcid":false,"given":"Rui Gon\u00e7alo","family":"Martinho","sequence":"additional","affiliation":[{"name":"Department of Medical Sciences, Institute of Biomedicine (iBiMED), University of Aveiro, Agra do Crasto, Edif\u00edcio 30, 3810-193 Aveiro, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2023,5,24]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1007\/s10577-021-09664-3","article-title":"Communal living: The role of polyploidy and syncytia in tissue biology","volume":"29","author":"Peterson","year":"2021","journal-title":"Chromosome Res."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"e83230","DOI":"10.7554\/eLife.83230","article-title":"Conservation of oocyte development in germline cysts from Drosophila to mouse","volume":"11","author":"Spradling","year":"2022","journal-title":"eLife"},{"key":"ref_3","unstructured":"Bate, M., and Martinez Arias, A. (1993). The Development of Drosophila Melanogaster, Cold Spring Harbor Laboratory Press."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1006\/dbio.1994.1257","article-title":"Intercellular cytoplasm transport during Drosophila oogenesis","volume":"165","author":"Cooley","year":"1994","journal-title":"Dev. Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"R438","DOI":"10.1016\/j.cub.2004.05.040","article-title":"The origin of asymmetry: Early polarisation of the Drosophila germline cyst and oocyte","volume":"14","author":"Huynh","year":"2004","journal-title":"Curr. Biol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1126\/science.aad2156","article-title":"Mouse oocytes differentiate through organelle enrichment from sister cyst germ cells","volume":"352","author":"Lei","year":"2016","journal-title":"Science"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"2576","DOI":"10.1016\/j.cell.2022.05.001","article-title":"Mouse oocytes develop in cysts with the help of nurse cells","volume":"185","author":"Niu","year":"2022","journal-title":"Cell"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1006\/dbio.2000.0120","article-title":"Comparative aspects of animal oogenesis","volume":"231","author":"Matova","year":"2001","journal-title":"Dev. Biol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/0020-7322(93)90013-Q","article-title":"Germ cell cluster formation in insect ovaries","volume":"22","author":"Buning","year":"1993","journal-title":"Int. J. Insect Morphol. Embryol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"103126","DOI":"10.1016\/j.micron.2021.103126","article-title":"Oogenesis in the tardigrade Hypsibius exemplaris Gasiorek, Stec, Morek & Michalczyk, 2018 (Eutardigrada, Hypsibiidae)","volume":"150","author":"Jezierska","year":"2021","journal-title":"Micron"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.ydbio.2003.10.002","article-title":"Formation, architecture and polarity of female germline cyst in Xenopus","volume":"266","author":"Kloc","year":"2004","journal-title":"Dev. Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"403","DOI":"10.7150\/ijbs.7.403","article-title":"Ovarian germline stem cells in the teleost fish, medaka (Oryzias latipes)","volume":"7","author":"Nakamura","year":"2011","journal-title":"Int. J. Biol. Sci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"dev187773","DOI":"10.1242\/dev.187773","article-title":"Zebrafish dazl regulates cystogenesis and germline stem cell specification during the primordial germ cell to germline stem cell transition","volume":"148","author":"Bertho","year":"2021","journal-title":"Development"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"875","DOI":"10.1534\/genetics.117.300081","article-title":"Female Meiosis: Synapsis, Recombination, and Segregation in Drosophila melanogaster","volume":"208","author":"Hughes","year":"2018","journal-title":"Genetics"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"19","DOI":"10.3389\/fcell.2020.00019","article-title":"Coordinating Proliferation, Polarity, and Cell Fate in the Drosophila Female Germline","volume":"8","author":"Hinnant","year":"2020","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/j.ceb.2019.03.008","article-title":"Regulation of Drosophila germline stem cells","volume":"60","author":"Kahney","year":"2019","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1016\/S0092-8674(00)81424-5","article-title":"Decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary","volume":"94","author":"Xie","year":"1998","journal-title":"Cell"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1353","DOI":"10.1242\/dev.01026","article-title":"Bmp signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary","volume":"131","author":"Song","year":"2004","journal-title":"Development"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1016\/j.devcel.2019.05.020","article-title":"Drosophila Ovarian Germline Stem Cell Cytocensor Projections Dynamically Receive and Attenuate BMP Signaling","volume":"50","author":"Wilcockson","year":"2019","journal-title":"Dev. Cell"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1786","DOI":"10.1016\/j.cub.2003.09.033","article-title":"Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells","volume":"13","author":"Chen","year":"2003","journal-title":"Curr. Biol."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Morris, L.X., and Spradling, A.C. (2012). Steroid signaling within Drosophila ovarian epithelial cells sex-specifically modulates early germ cell development and meiotic entry. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0046109"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Eliazer, S., Palacios, V., Wang, Z., Kollipara, R.K., Kittler, R., and Buszczak, M. (2014). Lsd1 restricts the number of germline stem cells by regulating multiple targets in escort cells. PLoS Genet., 10.","DOI":"10.1371\/journal.pgen.1004200"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1242\/bio.201410553","article-title":"Soma influences GSC progeny differentiation via the cell adhesion-mediated steroid-let-7-Wingless signaling cascade that regulates chromatin dynamics","volume":"4","author":"Konig","year":"2015","journal-title":"Biol. Open"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1083\/jcb.201503033","article-title":"Coordinated niche-associated signals promote germline homeostasis in the Drosophila ovary","volume":"211","author":"Liu","year":"2015","journal-title":"J. Cell Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"4242","DOI":"10.1242\/dev.124768","article-title":"COP9-Hedgehog axis regulates the function of the germline stem cell progeny differentiation niche in the Drosophila ovary","volume":"142","author":"Lu","year":"2015","journal-title":"Development"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.ydbio.2016.06.038","article-title":"The Wnt pathway limits BMP signaling outside of the germline stem cell niche in Drosophila ovaries","volume":"417","author":"Palacios","year":"2016","journal-title":"Dev. Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"dev159186","DOI":"10.1242\/dev.159186","article-title":"Diet regulates membrane extension and survival of niche escort cells for germline homeostasis via insulin signaling","volume":"145","author":"Su","year":"2018","journal-title":"Development"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"dev158527","DOI":"10.1242\/dev.158527","article-title":"Wnt6 maintains anterior escort cells as an integral component of the germline stem cell niche","volume":"145","author":"Wang","year":"2018","journal-title":"Development"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2207","DOI":"10.1242\/dev.065508","article-title":"Long-term live imaging provides new insight into stem cell regulation and germline-soma coordination in the Drosophila ovary","volume":"138","author":"Morris","year":"2011","journal-title":"Development"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"700","DOI":"10.1016\/j.ydbio.2007.11.006","article-title":"Diet controls normal and tumorous germline stem cells via insulin-dependent and -independent mechanisms in Drosophila","volume":"313","author":"Hsu","year":"2008","journal-title":"Dev. Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1242\/dev.088583","article-title":"Cyclin E controls Drosophila female germline stem cell maintenance independently of its role in proliferation by modulating responsiveness to niche signals","volume":"140","author":"Ables","year":"2013","journal-title":"Development"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1016\/j.cub.2005.02.016","article-title":"The division of Drosophila germline stem cells and their precursors requires a specific cyclin","volume":"15","author":"Wang","year":"2005","journal-title":"Curr. Biol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/j.devcel.2005.10.018","article-title":"Bruno inhibits the expression of mitotic cyclins during the prophase I meiotic arrest of Drosophila oocytes","volume":"10","author":"Sugimura","year":"2006","journal-title":"Dev. Cell"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1006\/dbio.1999.9570","article-title":"Cyclin A associates with the fusome during germline cyst formation in the Drosophila ovary","volume":"218","author":"Lilly","year":"2000","journal-title":"Dev. Biol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/j.ydbio.2009.10.018","article-title":"Germline cyst formation and incomplete cytokinesis during Drosophila melanogaster oogenesis","volume":"337","author":"Ong","year":"2010","journal-title":"Dev. Biol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1016\/0962-8924(96)84945-2","article-title":"Stable intercellular bridges in development: The cytoskeleton lining the tunnel","volume":"6","author":"Robinson","year":"1996","journal-title":"Trends Cell Biol."},{"key":"ref_37","first-page":"223","article-title":"Egalitarian and the choice of cell fates in Drosophila melanogaster oogenesis","volume":"182","author":"Carpenter","year":"1994","journal-title":"Ciba Found. Symp."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2785","DOI":"10.1242\/dev.127.13.2785","article-title":"The role of BicD, Egl, Orb and the microtubules in the restriction of meiosis to the Drosophila oocyte","volume":"127","author":"Huynh","year":"2000","journal-title":"Development"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Baluska, F., Volkmann, D., and Barlow, P.W. (2006). Cell-Cell Channels, Springer.","DOI":"10.1007\/978-0-387-46957-7"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"2781","DOI":"10.1242\/dev.125.15.2781","article-title":"Morphogenesis of the Drosophila fusome and its implications for oocyte specification","volume":"125","author":"Spradling","year":"1998","journal-title":"Development"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"947","DOI":"10.1242\/dev.120.4.947","article-title":"The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation","volume":"120","author":"Lin","year":"1994","journal-title":"Development"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1002\/dvg.1020160104","article-title":"Fusome asymmetry and oocyte determination in Drosophila","volume":"16","author":"Lin","year":"1995","journal-title":"Dev. Genet."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"874","DOI":"10.1126\/science.abj3125","article-title":"Symmetry breaking in the female germline cyst","volume":"374","author":"Nashchekin","year":"2021","journal-title":"Science"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.cub.2003.12.056","article-title":"A Spectraplakin Is Enriched on the Fusome and Organizes Microtubules during Oocyte Specification in Drosophila","volume":"14","author":"Brown","year":"2004","journal-title":"Curr. Biol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.1242\/jcs.03407","article-title":"Rtnl1 is enriched in a specialized germline ER that associates with ribonucleoprotein granule components","volume":"120","author":"Roper","year":"2007","journal-title":"J. Cell Sci."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"4512","DOI":"10.1091\/mbc.e04-06-0475","article-title":"The fusome mediates intercellular endoplasmic reticulum connectivity in Drosophila ovarian cysts","volume":"15","author":"Snapp","year":"2004","journal-title":"Mol. Biol. Cell"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.ydbio.2008.02.009","article-title":"New components of the Drosophila fusome suggest it plays novel roles in signaling and transport","volume":"317","author":"Lighthouse","year":"2008","journal-title":"Dev. Biol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1114","DOI":"10.1016\/j.neuron.2011.02.007","article-title":"Hts\/Adducin controls synaptic elaboration and elimination","volume":"69","author":"Pielage","year":"2011","journal-title":"Neuron"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"2443","DOI":"10.1101\/gad.6.12b.2443","article-title":"hu-li tai shao, a gene required for ring canal formation during Drosophila oogenesis, encodes a homolog of adducin","volume":"6","author":"Yue","year":"1992","journal-title":"Genes Dev."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1242\/dev.02766","article-title":"The Ovhts polyprotein is cleaved to produce fusome and ring canal proteins required for Drosophila oogenesis","volume":"134","author":"Petrella","year":"2007","journal-title":"Development"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1201","DOI":"10.1242\/dev.128.7.1201","article-title":"PAR-1 is required for the maintenance of oocyte fate in Drosophila","volume":"128","author":"Huynh","year":"2001","journal-title":"Development"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1889","DOI":"10.1242\/dev.128.10.1889","article-title":"Centrosome migration into the Drosophila oocyte is independent of BicD and egl, and of the organisation of the microtubule cytoskeleton","volume":"128","author":"Bolivar","year":"2001","journal-title":"Development"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1579","DOI":"10.1242\/dev.00365","article-title":"A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis","volume":"130","author":"Cox","year":"2003","journal-title":"Development"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1016\/0092-8674(89)90611-9","article-title":"Structure of the Drosophila BicaudalD protein and its role in localizing the posterior determinant nanos","volume":"59","author":"Wharton","year":"1989","journal-title":"Cell"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1957","DOI":"10.1101\/gad.3.12a.1957","article-title":"Bicaudal-D, a Drosophila gene involved in developmental asymmetry: Localized transcript accumulation in ovaries and sequence similarity to myosin heavy chain tail domains","volume":"3","author":"Suter","year":"1989","journal-title":"Genes Dev."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1101\/gad.11.4.423","article-title":"An Egalitarian-BicaudalD complex is essential for oocyte specification and axis determination in Drosophila","volume":"11","author":"Mach","year":"1997","journal-title":"Genes Dev."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1038\/ncb1122","article-title":"Egalitarian binds dynein light chain to establish oocyte polarity and maintain oocyte fate","volume":"6","author":"Navarro","year":"2004","journal-title":"Nat. Cell Biol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/0092-8674(91)90137-N","article-title":"Oskar organizes the germ plasm and directs localization of the posterior determinant nanos","volume":"66","author":"Ephrussi","year":"1991","journal-title":"Cell"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"598","DOI":"10.1101\/gad.8.5.598","article-title":"The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity","volume":"8","author":"Lantz","year":"1994","journal-title":"Genes Dev."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Wong, L.C., and Schedl, P. (2011). Cup blocks the precocious activation of the orb autoregulatory loop. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0028261"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"614","DOI":"10.1101\/gad.8.5.614","article-title":"orb is required for anteroposterior and dorsoventral patterning during Drosophila oogenesis","volume":"8","author":"Christerson","year":"1994","journal-title":"Genes Dev."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1006\/dbio.1999.9444","article-title":"The Drosophila CPEB homolog, orb, is required for oskar protein expression in oocytes","volume":"215","author":"Chang","year":"1999","journal-title":"Dev. Biol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"3169","DOI":"10.1242\/dev.128.16.3169","article-title":"Functioning of the Drosophila orb gene in gurken mRNA localization and translation","volume":"128","author":"Chang","year":"2001","journal-title":"Development"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"835","DOI":"10.1242\/dev.00309","article-title":"Orb and a long poly(A) tail are required for efficient oskar translation at the posterior pole of the Drosophila oocyte","volume":"130","author":"Castagnetti","year":"2003","journal-title":"Development"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1159","DOI":"10.1242\/dev.128.7.1159","article-title":"An autoregulatory feedback loop directs the localized expression of the Drosophila CPEB protein Orb in the developing oocyte","volume":"128","author":"Tan","year":"2001","journal-title":"Development"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1431","DOI":"10.1534\/genetics.119.302687","article-title":"The Drosophila CPEB Protein Orb Specifies Oocyte Fate by a 3\u2019UTR-Dependent Autoregulatory Loop","volume":"213","author":"Barr","year":"2019","journal-title":"Genetics"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1080\/15384101.2015.1131524","article-title":"How to pre-pair chromosomes for meiosis","volume":"15","author":"Rubin","year":"2016","journal-title":"Cell Cycle"},{"key":"ref_68","doi-asserted-by":"crossref","unstructured":"Christophorou, N., Rubin, T., and Huynh, J.R. (2013). Synaptonemal complex components promote centromere pairing in pre-meiotic germ cells. PLoS Genet., 9.","DOI":"10.1371\/journal.pgen.1004012"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"5628","DOI":"10.1038\/s41467-020-19361-0","article-title":"A single-cell atlas and lineage analysis of the adult Drosophila ovary","volume":"11","author":"Rust","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1083\/jcb.201407102","article-title":"Translational control in germline stem cell development","volume":"207","author":"Slaidina","year":"2014","journal-title":"J. Cell Biol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"2463","DOI":"10.1242\/dev.124.12.2463","article-title":"A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary","volume":"124","author":"Lin","year":"1997","journal-title":"Development"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1242\/dev.125.4.679","article-title":"Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells","volume":"125","author":"Forbes","year":"1998","journal-title":"Development"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"981","DOI":"10.1016\/j.cub.2004.05.049","article-title":"Repression of primordial germ cell differentiation parallels germ line stem cell maintenance","volume":"14","author":"Gilboa","year":"2004","journal-title":"Curr. Biol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1016\/j.stemcr.2013.09.007","article-title":"The CCR4 deadenylase acts with Nanos and Pumilio in the fine-tuning of Mei-P26 expression to promote germline stem cell self-renewal","volume":"1","author":"Joly","year":"2013","journal-title":"Stem Cell Rep."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1038\/nature07014","article-title":"Mei-P26 regulates microRNAs and cell growth in the Drosophila ovarian stem cell lineage","volume":"454","author":"Neumuller","year":"2008","journal-title":"Nature"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1016\/j.devcel.2010.11.019","article-title":"Brat promotes stem cell differentiation via control of a bistable switch that restricts BMP signaling","volume":"20","author":"Harris","year":"2011","journal-title":"Dev. Cell"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"9304","DOI":"10.1073\/pnas.0901452106","article-title":"Bam and Bgcn antagonize Nanos-dependent germ-line stem cell maintenance","volume":"106","author":"Li","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"9465","DOI":"10.1073\/pnas.1120473109","article-title":"Sex-lethal enables germline stem cell differentiation by down-regulating Nanos protein levels during Drosophila oogenesis","volume":"109","author":"Chau","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_79","doi-asserted-by":"crossref","unstructured":"Li, Y., Zhang, Q., Carreira-Rosario, A., Maines, J.Z., McKearin, D.M., and Buszczak, M. (2013). Mei-p26 cooperates with Bam, Bgcn and Sxl to promote early germline development in the Drosophila ovary. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0058301"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1016\/j.devcel.2016.02.010","article-title":"Repression of Pumilio Protein Expression by Rbfox1 Promotes Germ Cell Differentiation","volume":"36","author":"Bhargava","year":"2016","journal-title":"Dev. Cell"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"12331","DOI":"10.1038\/ncomms12331","article-title":"Early programming of the oocyte epigenome temporally controls late prophase I transcription and chromatin remodelling","volume":"7","author":"McCarthy","year":"2016","journal-title":"Nat. Commun."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1016\/j.ydbio.2021.02.003","article-title":"Epigenetic regulation of Drosophila germline stem cell maintenance and differentiation","volume":"473","author":"Vidaurre","year":"2021","journal-title":"Dev. Biol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.cell.2017.08.002","article-title":"Genome Regulation by Polycomb and Trithorax: 70 Years and Counting","volume":"171","author":"Schuettengruber","year":"2017","journal-title":"Cell"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"1699","DOI":"10.1534\/genetics.115.185116","article-title":"Polycomb and Trithorax Group Genes in Drosophila","volume":"206","author":"Kassis","year":"2017","journal-title":"Genetics"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1038\/s41580-021-00398-y","article-title":"The molecular principles of gene regulation by Polycomb repressive complexes","volume":"22","author":"Blackledge","year":"2021","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"e03737","DOI":"10.7554\/eLife.03737","article-title":"Establishment of regions of genomic activity during the Drosophila maternal to zygotic transition","volume":"3","author":"Li","year":"2014","journal-title":"eLife"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1038\/nature19362","article-title":"Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos","volume":"537","author":"Liu","year":"2016","journal-title":"Nature"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"e56922","DOI":"10.7554\/eLife.56922","article-title":"Differentiating Drosophila female germ cells initiate Polycomb silencing by regulating PRC2-interacting proteins","volume":"9","author":"DeLuca","year":"2020","journal-title":"eLife"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"1110","DOI":"10.1101\/gad.377406","article-title":"A Polycomb group protein complex with sequence-specific DNA-binding and selective methyl-lysine-binding activities","volume":"20","author":"Klymenko","year":"2006","journal-title":"Genes Dev."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"2367","DOI":"10.1101\/gad.226621.113","article-title":"Structural basis for targeting the chromatin repressor Sfmbt to Polycomb response elements","volume":"27","author":"Alfieri","year":"2013","journal-title":"Genes Dev."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1101\/gad.260562.115","article-title":"Sex comb on midleg (Scm) is a functional link between PcG-repressive complexes in Drosophila","volume":"29","author":"Kang","year":"2015","journal-title":"Genes Dev."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"1116","DOI":"10.1101\/gad.279141.116","article-title":"Molecular basis of PRC1 targeting to Polycomb response elements by PhoRC","volume":"30","author":"Frey","year":"2016","journal-title":"Genes Dev."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"3371","DOI":"10.1242\/dev.128.17.3371","article-title":"Su(z)12, a novel Drosophila Polycomb group gene that is conserved in vertebrates and plants","volume":"128","author":"Birve","year":"2001","journal-title":"Development"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1016\/j.devcel.2013.06.021","article-title":"PRC2 controls Drosophila oocyte cell fate by repressing cell cycle genes","volume":"26","author":"Iovino","year":"2013","journal-title":"Dev. Cell"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"e2204701119","DOI":"10.1073\/pnas.2204701119","article-title":"Polycomb group (PcG) proteins prevent the assembly of abnormal synaptonemal complex structures during meiosis","volume":"119","author":"Feijao","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_96","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":"Clough","year":"2007","journal-title":"Development"},{"key":"ref_97","doi-asserted-by":"crossref","unstructured":"Yoon, J., Lee, K.S., Park, J.S., Yu, K., Paik, S.G., and Kang, Y.K. (2008). dSETDB1 and SU(VAR)3-9 sequentially function during germline-stem cell differentiation in Drosophila melanogaster. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0002234"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"1373","DOI":"10.1016\/j.cub.2011.06.057","article-title":"piRNA production requires heterochromatin formation in Drosophila","volume":"21","author":"Rangan","year":"2011","journal-title":"Curr. Biol."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"955","DOI":"10.1016\/j.celrep.2019.03.071","article-title":"A Comprehensive Drosophila melanogaster Transcription Factor Interactome","volume":"27","author":"Shokri","year":"2019","journal-title":"Cell Rep."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"983","DOI":"10.1091\/mbc.e08-06-0639","article-title":"Stwl modifies chromatin compaction and is required to maintain DNA integrity in the presence of perturbed DNA replication","volume":"20","author":"Yi","year":"2009","journal-title":"Mol. Biol. Cell"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"1471","DOI":"10.1242\/dev.02810","article-title":"Stonewalling Drosophila stem cell differentiation by epigenetic controls","volume":"134","author":"Maines","year":"2007","journal-title":"Development"},{"key":"ref_102","doi-asserted-by":"crossref","unstructured":"Zinshteyn, D., and Barbash, D.A. (2022). Stonewall prevents expression of ectopic genes in the ovary and accumulates at insulator elements in D. melanogaster. PLoS Genet., 18.","DOI":"10.1371\/journal.pgen.1010110"},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/S1097-2765(02)00802-X","article-title":"Bre1, an E3 ubiquitin ligase required for recruitment and substrate selection of Rad6 at a promoter","volume":"11","author":"Wood","year":"2003","journal-title":"Mol. Cell"},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1016\/j.devcel.2004.11.020","article-title":"Bre1 is required for Notch signaling and histone modification","volume":"8","author":"Bray","year":"2005","journal-title":"Dev. Cell"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"4310","DOI":"10.1128\/MCB.06092-11","article-title":"The COMPASS family of H3K4 methylases in Drosophila","volume":"31","author":"Mohan","year":"2011","journal-title":"Mol. Cell. Biol."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/j.ydbio.2013.04.015","article-title":"dBre1\/dSet1-dependent pathway for histone H3K4 trimethylation has essential roles in controlling germline stem cell maintenance and germ cell differentiation in the Drosophila ovary","volume":"379","author":"Xuan","year":"2013","journal-title":"Dev. Biol."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"e45728","DOI":"10.15252\/embr.201845728","article-title":"The Trithorax group protein dMLL3\/4 instructs the assembly of the zygotic genome at fertilization","volume":"19","author":"Prudencio","year":"2018","journal-title":"EMBO Rep."},{"key":"ref_108","doi-asserted-by":"crossref","unstructured":"Navarro-Costa, P., and Martinho, R.G. (2020). The emerging role of transcriptional regulation in the oocyte-to-zygote transition. PLoS Genet., 16.","DOI":"10.1371\/journal.pgen.1008602"},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1242\/bio.201410850","article-title":"H3K36 Trimethylation-Mediated Epigenetic Regulation is Activated by Bam and Promotes Germ Cell Differentiation During Early Oogenesis in Drosophila","volume":"4","author":"Mukai","year":"2015","journal-title":"Biol. Open"},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"dev199625","DOI":"10.1242\/dev.199625","article-title":"Msl3 promotes germline stem cell differentiation in female Drosophila","volume":"149","author":"McCarthy","year":"2022","journal-title":"Development"},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"784","DOI":"10.1016\/j.bbrc.2007.05.189","article-title":"Drosophila dSet2 functions in H3-K36 methylation and is required for development","volume":"359","author":"Stabell","year":"2007","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.molcel.2007.08.011","article-title":"MSL complex is attracted to genes marked by H3K36 trimethylation using a sequence-independent mechanism","volume":"28","author":"Larschan","year":"2007","journal-title":"Mol. Cell"},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"773","DOI":"10.1534\/genetics.118.301004","article-title":"The Histone Demethylase KDM5 Is Essential for Larval Growth in Drosophila","volume":"209","author":"Drelon","year":"2018","journal-title":"Genetics"},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"dev182568","DOI":"10.1242\/dev.182568","article-title":"The histone demethylase KDM5 controls developmental timing in Drosophila by promoting prothoracic gland endocycles","volume":"146","author":"Drelon","year":"2019","journal-title":"Development"},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"9493","DOI":"10.1093\/nar\/gks773","article-title":"dKDM5\/LID regulates H3K4me3 dynamics at the transcription-start site (TSS) of actively transcribed developmental genes","volume":"40","author":"Rossell","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"ref_116","doi-asserted-by":"crossref","unstructured":"Zhaunova, L., Ohkura, H., and Breuer, M. (2016). Kdm5\/Lid Regulates Chromosome Architecture in Meiotic Prophase I Independently of Its Histone Demethylase Activity. PLoS Genet., 12.","DOI":"10.1371\/journal.pgen.1006241"},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"2219","DOI":"10.1016\/j.celrep.2015.11.007","article-title":"The Histone Demethylase KDM5 Activates Gene Expression by Recognizing Chromatin Context through Its PHD Reader Motif","volume":"13","author":"Liu","year":"2015","journal-title":"Cell Rep."},{"key":"ref_118","doi-asserted-by":"crossref","unstructured":"Liu, X., Greer, C., and Secombe, J. (2014). KDM5 interacts with Foxo to modulate cellular levels of oxidative stress. PLoS Genet., 10.","DOI":"10.1371\/journal.pgen.1004676"},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1186\/s13072-016-0053-9","article-title":"The histone demethylase dKDM5\/LID interacts with the SIN3 histone deacetylase complex and shares functional similarities with SIN3","volume":"9","author":"Gajan","year":"2016","journal-title":"Epigenet. Chromatin"},{"key":"ref_120","doi-asserted-by":"crossref","unstructured":"Torres-Campana, D., Kimura, S., Orsi, G.A., Horard, B., Benoit, G., and Loppin, B. (2020). The Lid\/KDM5 histone demethylase complex activates a critical effector of the oocyte-to-zygote transition. PLoS Genet., 16.","DOI":"10.1371\/journal.pgen.1008543"},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00412-023-00784-9","article-title":"A large-scale RNAi screen reveals that mitochondrial function is important for meiotic chromosome organization in oocytes","volume":"132","author":"Nieken","year":"2023","journal-title":"Chromosoma"},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"1487","DOI":"10.1126\/science.1120140","article-title":"Stem cell self-renewal controlled by chromatin remodeling factors","volume":"310","author":"Xi","year":"2005","journal-title":"Science"},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1126\/science.1165678","article-title":"Drosophila stem cells share a common requirement for the histone H2B ubiquitin protease scrawny","volume":"323","author":"Buszczak","year":"2009","journal-title":"Science"},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"1572","DOI":"10.1101\/gr.176487.114","article-title":"Cotranscriptional histone H2B monoubiquitylation is tightly coupled with RNA polymerase II elongation rate","volume":"24","author":"Fuchs","year":"2014","journal-title":"Genome Res."},{"key":"ref_125","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1534\/genetics.111.136465","article-title":"Stringent analysis of gene function and protein-protein interactions using fluorescently tagged genes","volume":"190","author":"Neumuller","year":"2012","journal-title":"Genetics"},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"1067","DOI":"10.1038\/emboj.2009.56","article-title":"Spt6 enhances the elongation rate of RNA polymerase II in vivo","volume":"28","author":"Ardehali","year":"2009","journal-title":"EMBO J."},{"key":"ref_127","doi-asserted-by":"crossref","unstructured":"He, J., Xuan, T., Xin, T., An, H., Wang, J., Zhao, G., and Li, M. (2014). Evidence for chromatin-remodeling complex PBAP-controlled maintenance of the Drosophila ovarian germline stem cells. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0103473"},{"key":"ref_128","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.celrep.2019.03.034","article-title":"Lysosomal Machinery Drives Extracellular Acidification to Direct Non-apoptotic Cell Death","volume":"27","author":"Mondragon","year":"2019","journal-title":"Cell Rep."},{"key":"ref_129","doi-asserted-by":"crossref","first-page":"2627","DOI":"10.1242\/dev.005611","article-title":"Cellular dynamics associated with the genome-wide epigenetic reprogramming in migrating primordial germ cells in mice","volume":"134","author":"Seki","year":"2007","journal-title":"Development"},{"key":"ref_130","doi-asserted-by":"crossref","first-page":"849","DOI":"10.1016\/j.molcel.2012.11.001","article-title":"The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells","volume":"48","author":"Seisenberger","year":"2012","journal-title":"Mol. Cell"},{"key":"ref_131","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1016\/j.ydbio.2004.11.025","article-title":"Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice","volume":"278","author":"Seki","year":"2005","journal-title":"Dev. Biol."},{"key":"ref_132","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/j.gde.2021.01.008","article-title":"Mechanisms of maternal intergenerational epigenetic inheritance","volume":"67","author":"Staubli","year":"2021","journal-title":"Curr. Opin. Genet. Dev."},{"key":"ref_133","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1038\/nature23262","article-title":"Maternal H3K27me3 controls DNA methylation-independent imprinting","volume":"547","author":"Inoue","year":"2017","journal-title":"Nature"},{"key":"ref_134","doi-asserted-by":"crossref","first-page":"eaay7246","DOI":"10.1126\/sciadv.aay7246","article-title":"Allelic H3K27me3 to allelic DNA methylation switch maintains noncanonical imprinting in extraembryonic cells","volume":"5","author":"Chen","year":"2019","journal-title":"Sci. Adv."},{"key":"ref_135","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1038\/s41588-021-00820-3","article-title":"H2AK119ub1 guides maternal inheritance and zygotic deposition of H3K27me3 in mouse embryos","volume":"53","author":"Mei","year":"2021","journal-title":"Nat. Genet."},{"key":"ref_136","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1126\/science.aam5339","article-title":"Germ line-inherited H3K27me3 restricts enhancer function during maternal-to-zygotic transition","volume":"357","author":"Zenk","year":"2017","journal-title":"Science"},{"key":"ref_137","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/j.cell.2020.05.026","article-title":"Intergenerationally Maintained Histone H4 Lysine 16 Acetylation Is Instructive for Future Gene Activation","volume":"182","author":"Samata","year":"2020","journal-title":"Cell"},{"key":"ref_138","doi-asserted-by":"crossref","first-page":"538","DOI":"10.1038\/35046205","article-title":"DNA methylation in Drosophila melanogaster","volume":"408","author":"Lyko","year":"2000","journal-title":"Nature"},{"key":"ref_139","doi-asserted-by":"crossref","first-page":"20210150","DOI":"10.1098\/rspb.2021.0150","article-title":"Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution","volume":"288","author":"Church","year":"2021","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"ref_140","doi-asserted-by":"crossref","first-page":"eadd2873","DOI":"10.1126\/sciadv.add2873","article-title":"Conserved meiotic mechanisms in the cnidarian Clytia hemisphaerica revealed by Spo11 knockout","volume":"9","author":"Munro","year":"2023","journal-title":"Sci. Adv."},{"key":"ref_141","doi-asserted-by":"crossref","unstructured":"Miramon-Puertolas, P., and Steinmetz, P.R.H. (2023). An adult stem-like cell population generates germline and neurons in the sea anemone Nematostella vectensis. bioRxiv.","DOI":"10.1101\/2023.01.27.525880"},{"key":"ref_142","doi-asserted-by":"crossref","first-page":"eaaz6830","DOI":"10.1126\/science.aaz6830","article-title":"Mammalian in vitro gametogenesis","volume":"374","author":"Saitou","year":"2021","journal-title":"Science"},{"key":"ref_143","doi-asserted-by":"crossref","unstructured":"Aizawa, E., Ozonov, E.A., Kawamura, Y.K., Dumeau, C.-E., Nagaoka, S., Saitou, M., Peters, A.H.F.M., and Wutz, A. (2023). Comprehensive comparison of female germ cell development in vitro and in vivo identifies epigenetic gene regulation crucial for oocyte development and embryonic competence. bioRxiv.","DOI":"10.1101\/2023.02.15.528760"}],"container-title":["Journal of Developmental Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2221-3759\/11\/2\/21\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:40:57Z","timestamp":1760125257000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2221-3759\/11\/2\/21"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5,24]]},"references-count":143,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,6]]}},"alternative-id":["jdb11020021"],"URL":"https:\/\/doi.org\/10.3390\/jdb11020021","relation":{},"ISSN":["2221-3759"],"issn-type":[{"type":"electronic","value":"2221-3759"}],"subject":[],"published":{"date-parts":[[2023,5,24]]}}}