Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
REVIEW

Polycomb in female reproductive health: patterning the present and programming the future

Ellen G. Jarred https://orcid.org/0000-0002-5394-9995 A * and Patrick S. Western https://orcid.org/0000-0002-7587-8227 A *
+ Author Affiliations
- Author Affiliations

A Centre for Reproductive Health, Hudson Institute of Medical Research and Department of Molecular and Translational Science, Monash University, Clayton, Vic, Australia.


Handling Editor: Jennifer Juengel

Reproduction, Fertility and Development 36, RD24152 https://doi.org/10.1071/RD24152
Submitted: 31 August 2024  Accepted: 14 November 2024  Published online: 5 December 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Epigenetic modifications regulate chromatin accessibility, gene expression, cell differentiation and tissue development. As epigenetic modifications can be inherited via mitotic and meiotic cell divisions, they enable a heritable memory of cell identity and function and can alter inherited characteristics in the next generation. Tight regulation of epigenetic information is critical for normal cell function and is often disrupted in diseases including cancer, metabolic, neurological and inherited congenital conditions. The ovary performs critical functions in female reproductive health and fertility, including oocyte and sex-hormone production. Oocytes undergo extensive epigenetic programming including the establishment of maternal genomic imprints, which are critical for offspring health and development. Epigenetic modifiers also regulate ovarian somatic cells, such as granulosa and theca cells which support oocytes and produce hormones. While ovarian dysfunction contributes to serious ovarian conditions such as primary ovarian insufficiency (POI), polycystic ovary syndrome (PCOS) and ovarian cancers, the roles of epigenetic modifications in the ovary and their contribution to ovarian dysfunction are not properly understood. Here we review recent advancements in understanding Polycomb proteins, important epigenetic modifiers that have emerging roles in ovarian development and maternal epigenetic inheritance. Polycomb group proteins (PcGs) contribute to the faithful establishment of epigenetic information in oocytes, a process essential for normal offspring development in mice. Emerging evidence also indicates that PcGs regulate ovarian function and female fertility. Understanding these and similar mechanisms will provide greater insight into the epigenetic regulation of ovarian and oocyte function, and how its disruption can impact reproductive health and maternal inheritance.

Keywords: epigenetics, granulosa, maternal inheritance, oocyte, ovary, Polycomb, polycystic ovary syndrome, PRC1, PRC2, primary ovarian insufficiency.

References

Abir R, Orvieto R, Dicker D, Zukerman Z, Barnett M, Fisch B (2002) Preliminary studies on apoptosis in human fetal ovaries. Fertility and Sterility 78(2), 259-264.
| Crossref | Google Scholar | PubMed |

Azuara V, Perry P, Sauer S, Spivakov M, Jørgensen HF, John RM, Gouti M, Casanova M, Warnes G, Merkenschlager M, Fisher AG (2006) Chromatin signatures of pluripotent cell lines. Nature Cell Biology 8(5), 532-538.
| Crossref | Google Scholar | PubMed |

Barlow DP, Bartolomei MS (2014) Genomic imprinting in mammals. Cold Spring Harbor Perspectives in Biology 6(2), a018382.
| Crossref | Google Scholar |

Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125(2), 315-326.
| Crossref | Google Scholar | PubMed |

Blackledge NP, Klose RJ (2021) The molecular principles of gene regulation by Polycomb repressive complexes. Nature Reviews Molecular Cell Biology 22(12), 815-833.
| Crossref | Google Scholar | PubMed |

Blackledge NP, Farcas AM, Kondo T, King HW, McGouran JF, Hanssen LLP, Ito S, Cooper S, Kondo K, Koseki Y, Ishikura T, Long HK, Sheahan TW, Brockdorff N, Kessler BM, Koseki H, Klose RJ (2014) Variant PRC1 complex-dependent H2A ubiquitylation drives PRC2 recruitment and polycomb domain formation. Cell 157(6), 1445-1459.
| Crossref | Google Scholar | PubMed |

Brennan J, Capel B (2004) One tissue, two fates: molecular genetic events that underlie testis versus ovary development. Nature Reviews Genetics 5(7), 509-521.
| Crossref | Google Scholar | PubMed |

Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298(5595), 1039-1043.
| Crossref | Google Scholar | PubMed |

Cavalli G, Heard E (2019) Advances in epigenetics link genetics to the environment and disease. Nature 571(7766), 489-499.
| Crossref | Google Scholar | PubMed |

Cohen ASA, Gibson WT (2016) EED-associated overgrowth in a second male patient. Journal of Human Genetics 61(9), 831-834.
| Crossref | Google Scholar | PubMed |

Cohen ASA, Tuysuz B, Shen Y, Bhalla SK, Jones SJM, Gibson WT (2015) A novel mutation in EED associated with overgrowth. Journal of Human Genetics 60(6), 339-342.
| Crossref | Google Scholar | PubMed |

Cooney E, Bi W, Schlesinger AE, Vinson S, Potocki L (2017) Novel EED mutation in patient with Weaver syndrome. American Journal of Medical Genetics Part A 173(2), 541-545.
| Crossref | Google Scholar | PubMed |

Cooper S, Dienstbier M, Hassan R, Schermelleh L, Sharif J, Blackledge NP, De Marco V, Elderkin S, Koseki H, Klose R, Heger A, Brockdorff N (2014) Targeting polycomb to pericentric heterochromatin in embryonic stem cells reveals a role for H2AK119u1 in PRC2 recruitment. Cell Reports 7(5), 1456-1470.
| Crossref | Google Scholar | PubMed |

Cooper S, Grijzenhout A, Underwood E, Ancelin K, Zhang T, Nesterova TB, Anil-Kirmizitas B, Bassett A, Kooistra SM, Agger K, Helin K, Heard E, Brockdorff N (2016) Jarid2 binds mono-ubiquitylated H2A lysine 119 to mediate crosstalk between Polycomb complexes PRC1 and PRC2. Nature Communications 7, 13661.
| Crossref | Google Scholar | PubMed |

Cyrus SS, Cohen ASA, Agbahovbe R, Avela K, Yeung KS, Chung BHY, Luk H-M, Tkachenko N, Choufani S, Weksberg R, Lopez-Rangel E, C.A.U.S.E.S. Study, Brown K, Saenz MS, Svihovec S, McCandless SE, Bird LM, Garcia AG, Gambello MJ, McWalter K, Schnur RE, An J, Jones SJM, Bhalla SK, Pinz H, Braddock SR, Gibson WT (2019) Rare SUZ12 variants commonly cause an overgrowth phenotype. American Journal of Medical Genetics Part C: Seminars in Medical Genetics 181(4), 532-547.
| Crossref | Google Scholar | PubMed |

Dupont S, Capel B (2021) The chromatin state during gonadal sex determination. Sexual Development 15(5–6), 308-316.
| Crossref | Google Scholar | PubMed |

Erhardt S, Su I-H, Schneider R, Barton S, Bannister AJ, Perez-Burgos L, Jenuwein T, Kouzarides T, Tarakhovsky A, Surani MA (2003) Consequences of the depletion of zygotic and embryonic enhancer of zeste 2 during preimplantation mouse development. Development 130(18), 4235-4248.
| Crossref | Google Scholar | PubMed |

Ezhkova E, Lien W-H, Stokes N, Pasolli HA, Silva JM, Fuchs E (2011) EZH1 and EZH2 cogovern histone H3K27 trimethylation and are essential for hair follicle homeostasis and wound repair. Genes & Development 25(5), 485-498.
| Crossref | Google Scholar | PubMed |

Faust C, Schumacher A, Holdener B, Magnuson T (1995) The eed mutation disrupts anterior mesoderm production in mice. Development 121(2), 273-285.
| Crossref | Google Scholar | PubMed |

Ferguson-Smith AC (2011) Genomic imprinting: the emergence of an epigenetic paradigm. Nature Reviews Genetics 12, 565-575.
| Crossref | Google Scholar | PubMed |

Ferguson-Smith AC, Bourc’his D (2018) 2018 gairdner awards: the discovery and importance of genomic imprinting. eLife 7, e42368.
| Crossref | Google Scholar | PubMed |

Fulton N, Martins da Silva SJ, Bayne RAL, Anderson RA (2005) Germ cell proliferation and apoptosis in the developing human ovary. The Journal of Clinical Endocrinology & Metabolism 90(8), 4664-4670.
| Crossref | Google Scholar | PubMed |

Gao Z, Zhang J, Bonasio R, Strino F, Sawai A, Parisi F, Kluger Y, Reinberg D (2012) PCGF homologs, CBX proteins, and RYBP define functionally distinct PRC1 family complexes. Molecular Cell 45(3), 344-356.
| Crossref | Google Scholar | PubMed |

Gao M, Zhang T, Chen T, Chen Z, Zhu Z, Wen Y, Qin S, Bao Y, Zhao T, Li H, Liu L, Hao M, Wang J, Wang F, Wang H, Zhou B, Zhang H, Xia G, Wang C (2024) Polycomb repressive complex 1 modulates granulosa cell proliferation in early folliculogenesis to support female reproduction. Theranostics 14(4), 1371-1389.
| Crossref | Google Scholar | PubMed |

Garcia-Moreno SA, Lin Y-T, Futtner CR, Salamone IM, Capel B, Maatouk DM (2019) CBX2 is required to stabilize the testis pathway by repressing Wnt signaling. PLoS Genetics 15(5), e1007895.
| Crossref | Google Scholar | PubMed |

Hanna CW, Kelsey G (2021) Features and mechanisms of canonical and noncanonical genomic imprinting. Genes & Development 35(11-12), 821-834.
| Crossref | Google Scholar | PubMed |

Harris C, Cloutier M, Trotter M, Hinten M, Gayen S, Du Z, Xie W, Kalantry S (2019) Conversion of random X-inactivation to imprinted X-inactivation by maternal PRC2. eLife 8, e44258.
| Crossref | Google Scholar | PubMed |

Heard E, Martienssen RA (2014) Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157(1), 95-109.
| Crossref | Google Scholar | PubMed |

Hogg K, Western PS (2015) Refurbishing the germline epigenome: out with the old, in with the new. Seminars in Cell & Developmental Biology 45, 104-113.
| Crossref | Google Scholar | PubMed |

Ilango S, Paital B, Jayachandran P, Padma PR, Nirmaladevi R (2020) Epigenetic alterations in cancer. Frontiers in Bioscience (Landmark Edition) 25(6), 1058-1109.
| Crossref | Google Scholar | PubMed |

Imagawa E, Higashimoto K, Sakai Y, Numakura C, Okamoto N, Matsunaga S, Ryo A, Sato Y, Sanefuji M, Ihara K, Takada Y, Nishimura G, Saitsu H, Mizuguchi T, Miyatake S, Nakashima M, Miyake N, Soejima H, Matsumoto N (2017) Mutations in genes encoding polycomb repressive complex 2 subunits cause Weaver syndrome. Human Mutation 38(6), 637-648.
| Crossref | Google Scholar | PubMed |

Imagawa E, Albuquerque EVA, Isidor B, Mitsuhashi S, Mizuguchi T, Miyatake S, Takata A, Miyake N, Boguszewski MCS, Boguszewski CL, Lerario AM, Funari MA, Jorge AAL, Matsumoto N (2018) Novel SUZ12 mutations in Weaver-like syndrome. Clinical Genetics 94(5), 461-466.
| Crossref | Google Scholar | PubMed |

Inoue A (2023) Noncanonical imprinting: intergenerational epigenetic inheritance mediated by Polycomb complexes. Current Opinion in Genetics & Development 78, 102015.
| Crossref | Google Scholar | PubMed |

Inoue A, Jiang L, Lu F, Suzuki T, Zhang Y (2017) Maternal H3K27me3 controls DNA methylation-independent imprinting. Nature 547, 419-424.
| Crossref | Google Scholar | PubMed |

Inoue A, Chen Z, Yin Q, Zhang Y (2018) Maternal Eed knockout causes loss of H3K27me3 imprinting and random X inactivation in the extraembryonic cells. Genes & Development 32(23–24), 1525-1536.
| Crossref | Google Scholar | PubMed |

Ito S, Umehara T, Koseki H (2024) Polycomb-mediated histone modifications and gene regulation. Biochemical Society Transactions 52(1), 151-161.
| Crossref | Google Scholar | PubMed |

Jameson SA, Lin Y-T, Capel B (2012) Testis development requires the repression of Wnt4 by Fgf signaling. Developmental Biology 370(1), 24-32.
| Crossref | Google Scholar | PubMed |

Jarred EG, Bildsoe H, Western PS (2018) Out of sight, out of mind? Germ cells and the potential impacts of epigenomic drugs. F1000Research 7, 1967.
| Crossref | Google Scholar |

Jarred EG, Qu Z, Tsai T, Oberin R, Petautschnig S, Bildsoe H, Pederson S, Zhang Q-H, Stringer JM, Carroll J, Gardner DK, Van den Buuse M, Sims NA, Gibson WT, Adelson DL, Western PS (2022) Transient Polycomb activity represses developmental genes in growing oocytes. Clinical Epigenetics 14(1), 183.
| Crossref | Google Scholar | PubMed |

John RM (2017) Imprinted genes and the regulation of placental endocrine function: pregnancy and beyond. Placenta 56, 86-90.
| Crossref | Google Scholar | PubMed |

Kalb R, Latwiel S, Baymaz HI, Jansen PWTC, Müller CW, Vermeulen M, Müller J (2014) Histone H2A monoubiquitination promotes histone H3 methylation in Polycomb repression. Nature Structural & Molecular Biology 21(6), 569-571.
| Crossref | Google Scholar | PubMed |

Kim Y, Kobayashi A, Sekido R, DiNapoli L, Brennan J, Chaboissier M-C, Poulat F, Behringer RR, Lovell-Badge R, Capel B (2006) Fgf9 and Wnt4 act as antagonistic signals to regulate mammalian sex determination. PLoS Biology 4(6), e187.
| Crossref | Google Scholar | PubMed |

Kowluru RA, Mohammad G (2022) Epigenetic modifications in diabetes. Metabolism 126, 154920.
| Crossref | Google Scholar | PubMed |

Lewis PH, Mislove RF (1947) New mutants report. Drosophila Information Service 21, 69.
| Google Scholar |

Li Y, Mo Y, Chen C, He J, Guo Z (2024) Research advances of polycomb group proteins in regulating mammalian development. Frontiers in Cell and Developmental Biology 12, 1383200.
| Crossref | Google Scholar |

Liu X, Wang C, Liu W, Li J, Li C, Kou X, Chen J, Zhao Y, Gao H, Wang H, Zhang Y, Gao Y, Gao S (2016) Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos. Nature 537(7621), 558-562.
| Crossref | Google Scholar | PubMed |

Maheshwari A, Fowler PA (2008) Primordial follicular assembly in humans – revisited. Zygote 16(4), 285-296.
| Crossref | Google Scholar | PubMed |

Mann JR, Lovell-Badge RH (1984) Inviability of parthenogenones is determined by pronuclei, not egg cytoplasm. Nature 310(5972), 66-67.
| Crossref | Google Scholar | PubMed |

Marsit CJ (2015) Influence of environmental exposure on human epigenetic regulation. Journal of Experimental Biology 218(1), 71-79.
| Crossref | Google Scholar |

Mathieu M, Drelon C, Rodriguez S, Tabbal H, Septier A, Damon-Soubeyrand C, Dumontet T, Berthon A, Sahut-Barnola I, Djari C, Batisse-Lignier M, Pointud J-C, Richard D, Kerdivel G, Calméjane M-A, Boeva V, Tauveron I, Lefrançois-Martinez A-M, Martinez A, Val P (2018) Steroidogenic differentiation and PKA signaling are programmed by histone methyltransferase EZH2 in the adrenal cortex. Proceedings of the National Academy of Sciences 115(52), E12265-E12274.
| Crossref | Google Scholar | PubMed |

Matoba S, Kozuka C, Miura K, Inoue K, Kumon M, Hayashi R, Ohhata T, Ogura A, Inoue A (2022) Noncanonical imprinting sustains embryonic development and restrains placental overgrowth. Genes & Development 36(7–8), 483-494.
| Crossref | Google Scholar | PubMed |

Matson CK, Murphy MW, Sarver AL, Griswold MD, Bardwell VJ, Zarkower D (2011) DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 476(7358), 101-104.
| Crossref | Google Scholar | PubMed |

McGrath J, Solter D (1984) Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37(1), 179-183.
| Crossref | Google Scholar | PubMed |

Mei H, Kozuka C, Hayashi R, Kumon M, Koseki H, Inoue A (2021) H2AK119ub1 guides maternal inheritance and zygotic deposition of H3K27me3 in mouse embryos. Nature Genetics 53(4), 539-550.
| Crossref | Google Scholar | PubMed |

Min J, Zhang Y, Xu R-M (2003) Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes & Development 17(15), 1823-1828.
| Crossref | Google Scholar | PubMed |

Oberin R, Petautschnig S, Jarred EG, Qu Z, Tsai T, Youngson NA, Pulsoni G, Truong TT, Fernando D, Bildsoe H, Blücher RO, van den Buuse M, Gardner DK, Sims NA, Adelson DL, Western PS (2024) Fetal growth delay caused by loss of non-canonical imprinting is resolved late in pregnancy and culminates in offspring overgrowth. eLife 13, e81875.
| Crossref | Google Scholar |

O’Carroll D, Erhardt S, Pagani M, Barton SC, Surani MA, Jenuwein T (2001) The polycomb-group geneEzh2 is required for early mouse development. Molecular and Cellular Biology 21(13), 4330-4336.
| Crossref | Google Scholar | PubMed |

Pasini D, Bracken AP, Jensen MR, Denchi EL, Helin K (2004) Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. The EMBO Journal 23(20), 4061-4071.
| Crossref | Google Scholar | PubMed |

Pepling ME, Spradling AC (2001) Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Developmental Biology 234(2), 339-351.
| Crossref | Google Scholar | PubMed |

Peters H (1969) The development of the mouse ovary from birth to maturity. Acta Endocrinologica 62(1), 98-116.
| Crossref | Google Scholar | PubMed |

Prokopuk L, Western PS, Stringer JM (2015) Transgenerational epigenetic inheritance: adaptation through the germline epigenome? Epigenomics 7(5), 829-846.
| Crossref | Google Scholar | PubMed |

Prokopuk L, Stringer JM, White CR, Vossen RHAM, White SJ, Cohen ASA, Gibson WT, Western PS (2018) Loss of maternal EED results in postnatal overgrowth. Clinical Epigenetics 10(1), 95.
| Crossref | Google Scholar | PubMed |

Prokopuk L, Jarred EG, Blücher RO, McLaughlin EA, Stringer JM, Western PS (2022) An essential role for Polycomb Repressive Complex 2 in the mouse ovary. Reproduction 163(3), 167-182.
| Crossref | Google Scholar | PubMed |

Radford EJ (2018) Exploring the extent and scope of epigenetic inheritance. Nature Reviews Endocrinology 14(6), 345-355.
| Crossref | Google Scholar | PubMed |

Richards JS, Pangas SA (2010) The ovary: basic biology and clinical implications. Journal of Clinical Investigation 120(4), 963-972.
| Crossref | Google Scholar | PubMed |

Rimon-Dahari N, Yerushalmi-Heinemann L, Alyagor L, Dekel N (2016) Ovarian folliculogenesis. In ‘Molecular mechanisms of cell differentiation in gonad development’. (Ed. RP Piprek) pp. 167–190. (Springer International Publishing: Cham) 10.1007/978-3-319-31973-5_7

Rosen ED, Kaestner KH, Natarajan R, Patti M-E, Sallari R, Sander M, Susztak K (2018) Epigenetics and epigenomics: implications for diabetes and obesity. Diabetes 67(10), 1923-1931.
| Crossref | Google Scholar | PubMed |

Rossitto M, Déjardin S, Rands CM, Le Gras S, Migale R, Rafiee M-R, Neirijnck Y, Pruvost A, Nguyen AL, Bossis G, Cammas F, Le Gallic L, Wilhelm D, Lovell-Badge R, Boizet-Bonhoure B, Nef S, Poulat F (2022) TRIM28-dependent SUMOylation protects the adult ovary from activation of the testicular pathway. Nature Communications 13(1), 4412.
| Crossref | Google Scholar | PubMed |

Schuettengruber B, Bourbon H-M, Di Croce L, Cavalli G (2017) Genome regulation by Polycomb and Trithorax: 70 years and counting. Cell 171(1), 34-57.
| Crossref | Google Scholar | PubMed |

Schumacher A, Faust C, Magnuson T (1996) Erratum: positional cloning of a global regulator of anterior–posterior patterning in mice. Nature 384(6610), 648.
| Crossref | Google Scholar | PubMed |

Sforza C, Vizzotto L, Ferrario VF, Forabosco A (2003) Position of follicles in normal human ovary during definitive histogenesis. Early Human Development 74(1), 27-35.
| Crossref | Google Scholar | PubMed |

Shen X, Liu Y, Hsu Y-J, Fujiwara Y, Kim J, Mao X, Yuan G-C, Orkin SH (2008) EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Molecular Cell 32(4), 491-502.
| Crossref | Google Scholar | PubMed |

Shi TH, Sugishita H, Gotoh Y (2024) Crosstalk within and beyond the Polycomb repressive system. Journal of Cell Biology 223(5), e202311021.
| Crossref | Google Scholar |

Stévant I, Kühne F, Greenfield A, Chaboissier M-C, Dermitzakis ET, Nef S (2019) Dissecting cell lineage specification and sex fate determination in gonadal somatic cells using single-cell transcriptomics. Cell Reports 26(12), 3272-3283.E3.
| Crossref | Google Scholar | PubMed |

Stewart KR, Veselovska L, Kelsey G (2016) Establishment and functions of DNA methylation in the germline. Epigenomics 8(10), 1399-1413.
| Crossref | Google Scholar | PubMed |

Surani MAH, Barton SC, Norris ML (1984) Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308, 548-550.
| Crossref | Google Scholar | PubMed |

Tatton-Brown K, Hanks S, Ruark E, Zachariou A, Duarte SDV, Ramsay E, Snape K, Murray A, Perdeaux ER, Seal S, Loveday C, Banka S, Clericuzio C, Flinter F, Magee A, McConnell V, Patton M, Raith W, Rankin J, Splitt M, Strenger V, Taylor C, Wheeler P, Temple IK, Cole T, The Childhood Overgrowth Collaboration, Douglas J, Rahman N (2011) Germline mutations in the oncogene EZH2 cause Weaver syndrome and increased human height. Oncotarget 2(12), 1127-1133.
| Crossref | Google Scholar | PubMed |

Tatton-Brown K, Loveday C, Yost S, Clarke M, Ramsay E, Zachariou A, Elliott A, Wylie H, Ardissone A, Rittinger O, Stewart F, Temple IK, Cole T, Childhood Overgrowth Collaboration, Mahamdallie S, Seal S, Ruark E, Rahman N (2017) Mutations in epigenetic regulation genes are a major cause of overgrowth with intellectual disability. The American Journal of Human Genetics 100(5), 725-736.
| Crossref | Google Scholar | PubMed |

Tran NQV, Miyake K (2017) Neurodevelopmental disorders and environmental toxicants: epigenetics as an underlying mechanism. International Journal of Genomics 2017, 7526592.
| Crossref | Google Scholar |

Tran N, Broun A, Ge K (2020) Lysine demethylase KDM6A in differentiation, development, and cancer. Molecular and Cellular Biology 40(20), e00341-20.
| Crossref | Google Scholar | PubMed |

Uckelmann M, Davidovich C (2024) Chromatin compaction by Polycomb group proteins revisited. Current Opinion in Structural Biology 86, 102806.
| Crossref | Google Scholar | PubMed |

Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R, Kress J, Treier A-C, Klugmann C, Klasen C, Holter NI, Riethmacher D, Schütz G, Cooney AJ, Lovell-Badge R, Treier M (2009) Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 139(6), 1130-1142.
| Crossref | Google Scholar | PubMed |

Vijayanathan M, Trejo-Arellano MG, Mozgová I (2022) Polycomb repressive complex 2 in eukaryotes – an evolutionary perspective. Epigenomes 6(1), 3.
| Crossref | Google Scholar |

Wang L, Brown JL, Cao R, Zhang Y, Kassis JA, Jones RS (2004) Hierarchical recruitment of polycomb group silencing complexes. Molecular Cell 14(5), 637-646.
| Crossref | Google Scholar | PubMed |

Wang Y, Wang W, Cheng K, Geng K, Liang J, Wang P, Zhang J, Niu S, Jia L, Zhang S, Li L, Feng X, Wang C, Wang H, Zhang H, Zhang Y (2022) Polycomb subunit Pcgf2 mediates ovulation and fertility through transcriptional regulation progesterone receptor. Frontiers in Cell and Developmental Biology 10, 101061.
| Crossref | Google Scholar |

Xia W, Xu J, Yu G, Yao G, Xu K, Ma X, Zhang N, Liu B, Li T, Lin Z, Chen X, Li L, Wang Q, Shi D, Shi S, Zhang Y, Song W, Jin H, Hu L, Bu Z, Wang Y, Na J, Xie W, Sun Y-P (2019) Resetting histone modifications during human parental-to-zygotic transition. Science 365(6451), 353-360.
| Crossref | Google Scholar | PubMed |

Zepeda-Martinez JA, Pribitzer C, Wang J, Bsteh D, Golumbeanu S, Zhao Q, Burkard TR, Reichholf B, Rhie SK, Jude J, Moussa HF, Zuber J, Bell O (2020) Parallel PRC2/cPRC1 and vPRC1 pathways silence lineage-specific genes and maintain self-renewal in mouse embryonic stem cells. Science Advances 6(14), eaax5692.
| Crossref | Google Scholar |

Zhao Y, Bai D, Wu Y, Zhang D, Liu M, Tian Y, Lu J, Wang H, Gao S, Lu Z (2022) Maternal Ezh1/2 deficiency in oocyte delays H3K27me2/3 restoration and impairs epiblast development responsible for embryonic sub-lethality in mouse. Development 149(15), dev200316.
| Crossref | Google Scholar |

Zheng H, Huang B, Zhang B, Xiang Y, Du Z, Xu Q, Li Y, Wang Q, Ma J, Peng X, Xu F, Xie W (2016) Resetting epigenetic memory by reprogramming of histone modifications in mammals. Molecular Cell 63(6), 1066-1079.
| Crossref | Google Scholar | PubMed |