PRC1.6复合体表观遗传调控生殖谱系特异性基因的时空表达

doi:10.16288/j.yczz.18-332

遗传 ›› 2019, Vol. 41 ›› Issue (4): 271-284.doi: 10.16288/j.yczz.18-332

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PRC1.6复合体表观遗传调控生殖谱系特异性基因的时空表达

孙晓伟¹,李宏阳¹,王健¹,程博^1,²()

^1. 兰州大学生命科学学院,兰州 730000
^2. 兰州大学,教育部细胞活动及逆境适应重点实验室,兰州 730000

收稿日期:2019-01-27 修回日期:2019-03-14 出版日期:2019-04-20 发布日期:2019-03-29
通讯作者: 程博 E-mail:bocheng@lzu.edu.cn
作者简介:孙晓伟,在读博士研究生,专业方向：细胞生物学。E-mail: sunxw18@lzu.edu.cn。|李宏阳,在读硕士研究生,专业方向：细胞生物学。E-mail: hyli17@lzu.edu.cn。
基金资助:
国家自然科学基金项目(31471233);国家自然科学基金项目(31771447);中央高校基本科研业务费(lzujbky-2017-it51);中央高校基本科研业务费(lzujbky-2018-k05);教育部细胞活动与逆境适应重点实验室开放基金项目(lzujbky-2017-kb05);教育部细胞活动与逆境适应重点实验室开放基金项目(lzujbky-2018-kb05)

Controlling the spatiotemporal expression of germ line specific genes by PRC1.6 complex

Sun Xiaowei¹,Li Hongyang¹,Wang Jian¹,Cheng Bo^1,²()

^1. School of Life Sciences, Lanzhou University, Lanzhou 730000, China
^2. The Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations, Lanzhou University, Lanzhou 730000, China

Received:2019-01-27 Revised:2019-03-14 Online:2019-04-20 Published:2019-03-29
Contact: Cheng Bo E-mail:bocheng@lzu.edu.cn
Supported by:
the National Natural Science Foundation of China(31471233);the National Natural Science Foundation of China(31771447);the Fundamental Research Funds for the Central Universities(lzujbky-2017-it51);the Fundamental Research Funds for the Central Universities(lzujbky-2018-k05);the Foundation of the Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations(lzujbky-2017-kb05);the Foundation of the Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations(lzujbky-2018-kb05)

摘要/Abstract

摘要：

多梳抑制复合体1 (polycomb repressive complex 1, PRC1)是一类通过催化和识别染色质表观遗传修饰进而调控基因表达的蛋白复合体,主要参与干细胞干性维持、细胞分化以及细胞周期调控等生理过程,该复合体功能异常影响机体发育或导致癌症发生。在哺乳动物细胞内,PRC1根据组成差异被进一步细分为6种不同的亚型PRC1.1~PRC1.6,它们在靶基因群识别、表观调控机制及生物学功能上存在明显特化。近年来研究发现,PRC1.6复合体在胚胎干细胞及体细胞中对于稳定抑制生殖谱系特异性基因的表达至关重要,同时对于生殖干细胞的干性维持以及精子发生过程中生殖谱系特异性基因的精密调控承担着重要作用。本文在介绍PRC1.6复合体的发现、各组分的分子功能及其参与的生化反应途径的基础上,系统阐述了该复合体在胚胎发育、性腺发育、精子发生等过程中对生殖谱系特异性靶基因群的时空表达发挥的重要调控功能,并探讨了PRC1.6与已知表观遗传调控网络的相互作用,以期为进一步探索生殖谱系基因表达、精子发生的表观遗传调控机制以及男性不育的致病机制提供参考。

关键词: 多梳抑制复合体1, PRC1.6, 转录抑制, 生殖谱系特异性基因, 时空表达

Abstract:

Polycomb repressive complex 1 (PRC1) is a class of epigenetic regulatory complexes that normally represses gene expression by catalyzing and/or recognizing chromatin modifications. PRC1 mainly functions in stem cell maintenance, cell differentiation, cell cycle regulation and related processes. PRC1 also have aberrant functions which has been implicated in many types of developmental diseases and cancers. Mammalian PRC1 complexes are divided into six subtypes based on their composition and function; subtypes include PRC1.1 to PRC1.6. Each PRC1 subtype regulates a unique collection of target genes. The PRC1.6 complex subtype plays key roles in specifically repressing transcription of genes controlling germ cell development in embryonic stem cells and other somatic cell types. Recent research demonstrates that the PRC1.6 complex is also crucial for the timely activation of the germ line of specific genes during spermatogenesis, which is essential for proper gonad development. In this review, we summarize the identification of molecular functions of each core component of the PRC1.6 complex including how it recognizes and represses germ line specific genes. We also update the biological roles of this complex in regulating the spatiotemporal expression of germ line specific genes during embryonic development, gonad development, and spermatogenesis. Lastly, the crosstalk between the PRC1.6 complex and the other main epigenetic regulatory mechanisms involved in controlling spermatogenesis is discussed. Our discussion of the PRC1.6 complex in regulating germ line specific genes informs the studies of molecular processes of spermatogenesis and contributes to the understanding of the pathogenic mechanisms of male infertility.

Key words: polycomb repressive complex 1 (PRC1), PRC1.6, transcriptional repression, germ line specific genes, spatiotemporal expression

孙晓伟,李宏阳,王健,程博. PRC1.6复合体表观遗传调控生殖谱系特异性基因的时空表达[J]. 遗传, 2019, 41(4): 271-284.

Sun Xiaowei,Li Hongyang,Wang Jian,Cheng Bo. Controlling the spatiotemporal expression of germ line specific genes by PRC1.6 complex[J]. Hereditas(Beijing), 2019, 41(4): 271-284.

参考文献

[1]	Schuettengruber B, Bourbon HM, Di Croce L, Cavalli G . Genome regulation by polycomb and trithorax: 70 years and counting. Cell, 2017,171(1):34-57.
[2]	Pasini D, Bracken AP, Helin K . Polycomb group proteins in cell cycle progression and cancer. Cell Cycle, 2004,3(4):396-400.
[3]	Lewis EB . A gene complex controlling segmentation in Drosophila. Nature, 1978,276(5688):565-570.
[4]	Struhl G . A homoeotic mutation transforming leg to antenna in Drosophila. Nature, 1981,292(5824):635-638.
[5]	Geisler SJ, Paro R . Trithorax and polycomb group- dependent regulation: a tale of opposing activities. Development, 2015,142(17):2876-2887.
[6]	Ingham PW . Differential expression of bithorax complex genes in the absence of the extra sex combs and trithorax genes. Nature, 1983,306(5943):591-593.
[7]	Creppe C, Palau A, Malinverni R, Valero V, Buschbeck M . A Cbx8-containing polycomb complex facilitates the transition to gene activation during ES cell differentiation. PLoS Genet, 2014,10(12):e1004851.
[8]	Gao Z, Lee P , Stafford JM, von Schimmelmann M, Schaefer A, Reinberg D. An AUTS2-polycomb complex activates gene expression in the CNS. Nature, 2014,516(7531):349-354.
[9]	Morey L, Santanach A, Blanco E, Aloia L, Nora EP, Bruneau BG, Di Croce L . Polycomb regulates mesoderm cell fate-specification in embryonic stem cells through activation and repression mechanisms. Cell Stem Cell, 2015,17(3):300-315.
[10]	Margueron R, Li GH, Sarma K, Blais A, Zavadil J, Woodcock CL, Dynlacht BD, Reinberg D . Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol Cell, 2008,32(4):503-518.
[11]	Margueron R, Justin N, Ohno K, Sharpe ML, Son J, Drury WJ, Voigt P, Martin SR, Taylor WR, De Marco V, Pirrotta V, Reinberg D, Gamblin SJ . Role of the polycomb protein EED in the propagation of repressive histone marks. Nature, 2009,461(7265):762-767.
[12]	Buchwald G, van der Stoop P, Weichenrieder O, Perrakis A, van Lohuizen M, Sixma TK . Structure and E3-ligase activity of the Ring-Ring complex of polycomb proteins Bmi1 and Ring1B. Embo J, 2006,25(11):2465-2474.
[13]	Li ZZ, Cao R, Wang M, Myers MP, Zhang Y, Xu RM . Structure of a Bmi1-Ring1b polycomb group ubiquitin ligase complex. J Biol Chem, 2006,281(29):20643-20649.
[14]	de Napoles M, Mermoud JE, Wakao R, Tang YA, Endoh M, Appanah R, Nesterova TB, Silva J, Otte AP, Vidal M, Koseki H, Brockdorff N . Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev Cell, 2004,7(5):663-676.
[15]	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 . Targeting polycomb to pericentric heterochromatin in embryonic stem cells reveals a role for H2AK119u1 in PRC2 recruitment. Cell Rep, 2014,7(5):1456-1470.
[16]	Ma RG, Zhang Y, Sun TT, Cheng B . Epigenetic regulation by polycomb group complexes: focus on roles of CBX proteins. J Zhejiang Univ-Sc B, 2014,15(5):412-428.
[17]	Gil J, O'Loghlen A . PRC1 complex diversity: Where is it taking us? Trends Cell Biol, 2014,24(11):632-641.
[18]	Connelly KE, Dykhuizen EC . Compositional and functional diversity of canonical PRC1 complexes in mammals. BBA-Gene Regul Mech, 2016,1860(2):233-245.
[19]	Ogawa H, Ishiguro K, Gaubatz S, Livingston DM, Nakatani Y . A complex with chromatin modifiers that occupies E2F- and Myc-responsive genes in G0 cells. Science, 2002,296(5570):1132-1136.
[20]	Trojer P, Cao AR, Gao ZH, Li Y, Zhang J, Xu X, Li G, Losson R, Erdjument-Bromage H, Tempst P, Farnham PJ, Reinberg D . L3mbtl2 protein acts in concert with PcG protein-mediated monoubiquitination of H2A to establish a repressive chromatin structure. Mol Cell, 2011,42(4):438-450.
[21]	Gao Z, Zhang J, Bonasio R, Strino F, Sawai A, Parisi F, Kluger Y, Reinberg D . PCGF homologs, CBX proteins, and RYBP define functionally distinct PRC1 family complexes. Mol Cell, 2012,45(3):344-356.
[22]	Endoh M, Endo TA, Shinga J, Hayashi K, Farcas A, Ma KW, Ito S, Sharif J, Endoh T, Onaga N, Nakayama M, Ishikura T, Masui O, Kessler BM, Suda T, Ohara O, Okuda A, Klose R, Koseki H . PCGF6-PRC1 suppresses premature differentiation of mouse embryonic stem cells by regulating germ cell-related genes. eLife, 2017,6:e21064.
[23]	Arrigoni R, Alam SL, Wamstad JA, Bardwell VJ, Sundquist WI, Schreiber-Agus N . The polycomb- associated protein RYBP is a ubiquitin binding protein. Febs Lett, 2006,580(26):6233-6241.
[24]	Zhao W, Tong H, Huang Y, Yan Y, Teng H, Xia Y, Jiang Q, Qin J . Essential role for polycomb group protein PCGF6 in embryonic stem cell maintenance and a noncanonical polycomb repressive complex 1 (PRC1) integrity. J Biol Chem, 2017,292(7):2773-2784.
[25]	Stielow B, Finkernagel F, Stiewe T, Nist A, Suske G . MGA, L3MBTL2 and E2F6 determine genomic binding of the non-canonical Polycomb repressive complex PRC1.6. PLoS Genet, 2018,14(1):e1007193.
[26]	Hurlin PJ, Steingrìmsson E, Copeland NG, Jenkins NA, Eisenman RN . Mga, a dual-specificity transcription factor that interacts with Max and contains a T-domain DNA-binding motif. Embo J, 1999,18(24):7019-7028.
[27]	Cartwright P, Müller H, Wagener C, Holm K, Helin K . E2f-6: a novel member of the E2F family is an inhibitor of E2F-dependent transcription. Oncogene, 1998,17(5):611-623.
[28]	Stielow C, Stielow B, Finkernagel F, Scharfe M, Jarek M, Suske G . SUMOylation of the polycomb group protein L3MBTL2 facilitates repression of its target genes. Nucleic Acids Res, 2013,42(5):3044-3058.
[29]	Guo Y, Nady N, Qi C, Allali-Hassani A, Zhu H, Pan P, Adams-Cioaba MA, Amaya MF, Dong A, Vedadi M, Schapira M, Read RJ, Arrowsmith CH, Min J . Methylation-state-specific recognition of histones by the MBT repeat protein L3MBTL2. Nucleic Acids Res, 2009,37(7):2204-2210.
[30]	Rose NR, King HW, Blackledge NP, Fursova NA, Ember KJI, Fischer R, Kessler BM, Klose RJ . RYBP stimulates PRC1 to shape chromatin-based communication between Polycomb repressive complexes. eLife, 2016,5:e18591.
[31]	Zimberlin CD, Lancini C, Sno R, Rosekrans SL, McLean CM, Vlaming H, van den Brink GR, Bots M, Medema JP, Dannenberg JH . HDAC1 and HDAC2 collectively regulate intestinal stem cell homeostasis. Faseb J, 2015,29(5):2070-2080.
[32]	Vakoc CR, Mandat SA, Olenchock BA, Blobel GA . Histone H3 lysine 9 methylation and HP1gamma are associated with transcription elongation through mammalian chromatin. Mol Cell, 2005,19(3):381-391.
[33]	Yang CS, Chang KY, Dang J, Rana TM . Polycomb group protein PCGF6 acts as a master regulator to maintain embryonic stem cell identity. Sci Rep, 2016,6:26899.
[34]	Zdzieblo D, Li X, Lin Q, Zenke M, Illich DJ, Becker M, Müller AM . Pcgf6, a polycomb group protein, regulates mesodermal lineage differentiation in murine ESCs and functions in iPS reprogramming. Stem Cells, 2014,32(12):3112-3125.
[35]	Huang Y, Zhao W, Wang C, Zhu Y, Liu M, Tong H, Xia Y, Jiang Q, Qin J . Combinatorial control of recruitment of a variant PRC1.6 complex in embryonic stem cells. Cell Rep, 2018,22(11):3032-3043.
[36]	Bandara LR, Buck VM, Zamanian M, Johnston LH, La Thangue NB . Functional synergy between DP-1 and E2F-1 in the cell cycle-regulating transcription factor DRTF1/E2F. Embo J, 1993,12(11):4317-4324.
[37]	Rowland BD, Bernards R . Re-evaluating cell-cycle regulation by E2Fs. Cell, 2006,127(5):871-874.
[38]	Hisada K, Sánchez C, Endo TA, Endoh M, Román- Trufero M, Sharif J, Koseki H, Vidal M . Rybp represses endogenous retroviruses and preimplantation- and germ line-specific genes in mouse embryonic stem cells. Mol Cell Biol, 2012,32(6):1139-1149.
[39]	Maeda I, Okamura D, Tokitake Y, Ikeda M, Kawaguchi H, Mise N, Abe K, Noce T, Okuda A, Matsui Y . Max is a repressor of germ cell-related gene expression in mouse embryonic stem cells. Nat Commun, 2013,4:1754.
[40]	Suzuki A, Hirasaki M, Hishida T, Wu J, Okamura D, Ueda A, Nishimoto M, Nakachi Y, Mizuno Y, Okazaki Y, Matsui Y, Izpisua Belmonte JC, Okuda A . Loss of Max results in meiotic entry in mouse embryonic and germline stem cells. Nat Commun, 2016,7:11056.
[41]	Qin JZ, Whyte WA, Anderssen E, Apostolou E, Chen HH, Akbarian S, Bronson RT, Hochedlinger K, Ramaswamy S, Young RA, Hock H . The polycomb group protein L3mbtl2 assembles an atypical PRC1- family complex that is essential in pluripotent stem cells and early development. Cell Stem Cell, 2012,11(3):319-332.
[42]	Pohlers M, Truss M, Frede U, Scholz A, Strehle M, Kuban RJ, Hoffmann B, Morkel M, Birchmeier C, Hagemeier C . A role for E2F6 in the restriction of male-germ-cell-specific gene expression. Curr Biol: CB, 2005,15(11):1051-1057.
[43]	Storre J, Schäfer A, Reichert N, Barbero JL, Hauser S, Eilers M, Gaubatz S . Silencing of the meiotic genes Smc1beta and Stag3 in somatic cells by E2F6. J Biol Chem, 2005,280(50):41380-41386.
[44]	Shen-Li H, O'Hagan RC, Hou H Jr, Horner JW, Lee HW, DePinho RA . Essential role for Max in early embryonic growth and development. Gene Dev, 2000,14(1):17-22.
[45]	Washkowitz AJ, Schall C, Zhang K, Wurst W, Floss T, Mager J, Papaioannou VE . Mga is essential for the survival of pluripotent cells during peri-implantation development. Development, 2015,142(1):31-40.
[46]	Burn SF, Washkowitz AJ, Gavrilov S, Papaioannou VE . Postimplantation Mga expression and embryonic lethality of two gene-trap alleles. Gene Expr Patterns: GEP, 2018,27:31-35.
[47]	Jørgensen HF, Giadrossi S, Casanova M, Endoh M, Koseki H, Brockdorff N, Fisher AG . Stem cells primed for action: polycomb repressive complexes restrain the expression of lineage-specific regulators in embryonic stem cells. Cell Cycle, 2006,5(13):1411-1414.
[48]	Terranova R, Yokobayashi S, Stadler MB, Otte AP, van Lohuizen M, Orkin SH, Peters AH . Polycomb group proteins EZH2 and RNF2 direct genomic contraction and imprinted repression in early mouse embryos. Dev Cell, 2008,15(5):668-679.
[49]	Endoh M, Endo TA, Endoh T, Fujimura Y, Ohara O, Toyoda T, Otte AP, Okano M, Brockdorff N, Vidal M, Koseki H . Polycomb group proteins Ring1A/B are functionally linked to the core transcriptional regulatory circuitry to maintain ES cell identity. Development, 2008,135(8):1513-1524.
[50]	Stock JK, Giadrossi S, Casanova M, Brookes E, Vidal M, Koseki H, Brockdorff N, Fisher AG, Pombo A . Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase ii at bivalent genes in mouse ES cells. Nat Cell Biol, 2007,9(12):1428-1435.
[51]	Voncken JW, Roelen BA, Roefs M, de Vries S, Verhoeven E, Marino S, Deschamps J, van Lohuizen M . Rnf2 (Ring1B) deficiency causes gastrulation arrest and cell cycle inhibition. Proc Natl Acad Sci USA, 2003,100(5):2468-2473.
[52]	Suzuki M, Mizutani-Koseki Y, Fujimura Y, Miyagishima H, Kaneko T, Takada Y, Akasaka T, Tanzawa H, Takihara Y, Nakano M, Masumoto H, Vidal M, Isono K, Koseki H . Involvement of the polycomb- group gene Ring1B in the specification of the anterior- posterior axis in mice. Development, 2002,129(18):4171-4183.
[53]	Maezawa S, Hasegawa K, Yukawa M, Sakashita A, Alavattam KG, Andreassen PR, Vidal M, Koseki H, Barski A, Namekawa SH . Polycomb directs timely activation of germline genes in spermatogenesis. Gene Dev, 2017,31(16):1693-1703.
[54]	Yokobayashi S, Liang CY, Kohler H, Nestorov P, Liu Z, Vidal M, van Lohuizen M, Roloff TC, Peters AH . PRC1 coordinates timing of sexual differentiation of female primordial germ cells. Nature, 2013,495(7440):236-240.
[55]	Ujhelly O, Szabo V, Kovacs G, Vajda F, Mallok S, Prorok J, Acsai K, Hegedus Z, Krebs S, Dinnyes A, Pirity MK . Lack of RYBP in mouse embryonic stem cells impairs cardiac differentiation. Stem Cells Dev, 2015,24(18):2193-2205.
[56]	Pirity MK, Locker J, Schreiber-Agus N . RYBP/DEDAF is required for early postimplantation and for central nervous system development. Mol Cell Biol, 2005,25(16):7193-7202.
[57]	Jamaladdin S, Kelly RD, O'Regan L, Dovey OM, Hodson GE, Millard CJ, Portolano N, Fry AM, Schwabe JW, Cowley SM . Histone deacetylase (HDAC) 1 and 2 are essential for accurate cell division and the pluripotency of embryonic stem cells. Proc Natl Acad Sci USA, 2014,111(27):9840-9845.
[58]	Lagger G, O'Carroll D, Rembold M, Khier H, Tischler J, Weitzer G, Schuettengruber B, Hauser C, Brunmeir R, Jenuwein T, Seiser C . Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. Embo J, 2002,21(11):2672-2681.
[59]	Wang Y, Tian Y, Morley MP, Lu MM, Demayo FJ, Olson EN, Morrisey EE . Development and regeneration of Sox2+ endoderm progenitors are regulated by a Hdac1/2-Bmp4/Rb1 regulatory pathway. Dev Cell, 2013,24(4):345-358.
[60]	Caillier M, Thénot S, Tribollet V, Birot AM, Samarut J, Mey A . Role of the epigenetic regulator HP1γ in the control of embryonic stem cell properties. PLoS One, 2010,5(11):e15507.
[61]	Brown JP, Bullwinkel J, Baron-Lühr B, Billur M, Schneider P, Winking H, Singh PB . Hp1gamma function is required for male germ cell survival and spermatogenesis. Epigenet Chromat, 2012,5(1):18.
[62]	Takada Y, Naruse C, Costa Y, Shirakawa T, Tachibana M, Sharif J, Kezuka-Shiotani F, Kakiuchi D, Masumoto H, Shinkai Y, Ohbo K, Peters AHFM, Turner JMA, Asano M, Koseki H . Hp1γ links histone methylation marks to meiotic synapsis in mice. Development, 2011,138(19):4207-4217.
[63]	Leseva M, Santostefano KE, Rosenbluth AL, Hamazaki T, Terada N . E2f6-mediated repression of the meiotic Stag3 and Smc1β genes during early embryonic development requires Ezh2 and not the de novo methyltransferase Dnmt3b. Epigenetics, 2013,8(8):873-884.
[64]	Storre J, Elsässer HP, Fuchs M, Ullmann D, Livingston DM, Gaubatz S . Homeotic transformations of the axial skeleton that accompany a targeted deletion of E2f6. Embo Rep, 2002,3(7):695-700.
[65]	Courel M, Friesenhahn L, Lees JA . E2f6 and Bmi1 cooperate in axial skeletal development. Dev Dynam, 2008,237(5):1232-1242.
[66]	Kohn MJ, Leung SW, Criniti V, Agromayor M, Yamasaki L . Dp1 is largely dispensable for embryonic development. Mol Cell Biol, 2004,24(16):7197-7205.
[67]	Kohn MJ, Bronson RT, Harlow E, Dyson NJ, Yamasaki L . Dp1 is required for extra-embryonic development. Development, 2003,130(7):1295-1305.
[68]	Hu G, Kim J, Xu QK, Leng YM, Orkin SH, Elledge SJ . A genome-wide RNAi screen identifies a new transcriptional module required for self-renewal. Gene Dev, 2009,23(7):837-848.
[69]	Meng C, Liao J, Zhao D, Huang H, Qin J, Lee TL, Chen D, Chan WY, Xia Y . L3mbtl2 regulates chromatin remodeling during spermatogenesis. Cell Death Differ, 2019. doi: 10.1038/s41418-019-0283-z.[Epub ahead of print]
[70]	Uysal F, Akkoyunlu G, Ozturk S . DNA methyltransferases exhibit dynamic expression during spermatogenesis. Reprod Biomed Online, 2016,33(6):690-702.
[71]	Ge SQ, Lin SL, Zhao ZH, Sun QY . Epigenetic dynamics and interplay during spermatogenesis and embryogenesis: Implications for male fertility and offspring health. Oncotarget, 2017,8(32):53804-53818.
[72]	Xiong J, Wang H, Guo G, Wang S, He L, Chen H, Wu J . Male germ cell apoptosis and epigenetic histone modification induced by Tripterygium wilfordii Hook F. PLoS One, 2011,6(6):e20751.
[73]	Sheng K, Liang X, Huang S, Xu W . The role of histone ubiquitination during spermatogenesis. Biomed Res Int, 2014,2014:870695.
[74]	Liu S, Yu H, Liu Y, Liu X, Zhang Y, Bu C, Yuan S, Chen Z, Xie G, Li W, Xu B, Yang J, He L, Jin T, Xiong Y, Sun L, Liu X, Han C, Cheng Z, Liang J, Shang Y . Chromodomain protein CDYl acts as a crotonyl-CoA hydratase to regulate histone crotonylation and spermatogenesis. Mol Cell, 2017, 67(5): 853- 866.e5.
[75]	Maze I, Noh KM, Soshnev AA, Allis CD . Every amino acid matters: essential contributions of histone variants to mammalian development and disease. Nat Rev Genet, 2014,15(4):259-271.
[76]	Bao J, Bedford MT . Epigenetic regulation of the histone-to-protamine transition during spermiogenesis. Reproduction, 2016,151(5):R55-70.
[77]	Russell SJ, Stalker L, LaMarre J . Piwis, piRNAs and retrotransposons: complex battles during reprogramming in gametes and early embryos. Reprod Domest Anim, 2017,52(Suppl. 4):28-38.
[78]	Hong SH, Kwon JT, Kim J, Jeong J, Kim J, Lee S, Cho C . Profiling of testis-specific long noncoding RNAs in mice. BMC Genomics, 2018,19(1):539.
[79]	Bie B, Wang Y, Li L, Fang H, Liu L, Sun J . Noncoding RNAs: potential players in the self-renewal of mammalian spermatogonial stem cells. Mol Reprod Dev, 2018,85(8-9):720-728.
[80]	Chen X, Li X, Guo J, Zhang P, Zeng W . The roles of microRNAs in regulation of mammalian spermatogenesis. J Anim Sci Biotechno, 2017,8:35.
[81]	Wichman L, Somasundaram S, Breindel C, Valerio DM, McCarrey JR, Hodges CA, Khalil AM . Dynamic expression of long noncoding RNAs reveals their potential roles in spermatogenesis and fertility. Biol Reprod, 2017,97(2):313-323.
[82]	Yang Y, Chen YS, Sun BF, Yang YG . RNA methylation: regulations and mechanisms. Hereditas(Beijing), 2018,40(11):964-976.
[82]	杨莹, 陈宇晟, 孙宝发, 杨运桂 . RNA甲基化修饰调控和规律. 遗传, 2018,40(11):964-976.
[83]	Peer E, Rechavi G, Dominissini D . Epitranscriptomics: regulation of mRNA metabolism through modifications. Curr Opin Chem Biol, 2017,41:93-98.
[84]	Oakes CC, La Salle S, Smiraglia DJ, Robaire B, Trasler JM . A unique configuration of genome-wide DNA methylation patterns in the testis. Proc Natl Acad Sci USA, 2006,104(1):228-233.
[85]	Hata K, Kusumi M, Yokomine T, Li E, Sasaki H . Meiotic and epigenetic aberrations in Dnmt3l-deficient male germ cells. Mol Reprod Dev, 2006,73(1):116-122.
[86]	de Vries M, Ramos L, Housein Z, de Boer P . Chromatin remodelling initiation during human spermiogenesis. Biol Open, 2012,1(5):446-457.
[87]	Hazzouri M, Pivot-Pajot C, Faure AK, Usson Y, Pelletier R, Sèle B, Khochbin S, Rousseaux S . Regulated hyperacetylation of core histones during mouse spermatogenesis: involvement of histone deacetylases. Eur J Cell Biol, 2000,79(12):950-960.
[88]	Hirota T, Lipp JJ, Toh BH, Peters JM . Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature, 2005,438(7071):1176-1180.
[89]	Lu LY, Wu JX, Ye L, Gavrilina GB, Saunders TL, Yu XC . RNF8-dependent histone modifications regulate nucleosome removal during spermatogenesis. Dev Cell, 2010,18(3):371-384.
[90]	Sin HS, Barski A, Zhang F, Kartashov AV, Nussenzweig A, Chen JJ, Andreassen PR, Namekawa SH . RNF8 regulates active epigenetic modifications and escape gene activation from inactive sex chromosomes in post-meiotic spermatids. Gene Dev, 2012,26(24):2737-2748.
[91]	Tanaka H, Iguchi N, Isotani A, Kitamura K, Toyama Y, Matsuoka Y, Onishi M, Masai K, Maekawa M, Toshimori K, Okabe M, Nishimune Y . HANP1/H1T2, a novel histone H1-like protein involved in nuclear formation and sperm fertility. Mol Cell Biol, 2005,25(16):7107-7119.
[92]	Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, Chien M, Russo JJ, Ju J, Sheridan R, Sander C, Zavolan M, Tuschl T . A novel class of small RNAs bind toMILI protein in mouse testes. Nature, 2006,442(7099):203-207.
[93]	Manakov SA, Pezic D, Marinov GK, Pastor WA, Sachidanandam R, Aravin AA . MIWI2 and MILI have differential effects on piRNA biogenesis and DNA methylation. Cell Rep, 2015,12(8):1234-1243.
[94]	Moritoki Y, Hayashi Y, Mizuno K, Kamisawa H, Nishio H, Kurokawa S, Ugawa S, Kojima Y, Kohri K . Expression profiling of microRNA in cryptorchid testes: MiR-135a contributes to the maintenance of spermatogonial stem cells by regulating FoxO1. J Urology, 2013,191(4):1174-1180.
[95]	Niu Z, Goodyear SM, Rao S, Wu X, Tobias JW, Avarbock MR, Brinster RL . MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells. Proc Natl Acad Sci USA, 2011,108(31):12740-12745.
[96]	Li L, Wang M, Wang M, Wu X, Geng L, Xue Y, Wei X, Jia Y, Wu X . A long non-coding rna interacts with gfra1 and maintains survival of mouse spermatogonial stem cells. Cell Death Dis, 2016,7:e2140.
[97]	Lin Z, Hsu PJ, Xing X, Fang J, Lu Z, Zou Q, Zhang KJ, Zhang X, Zhou Y, Zhang T, Zhang Y, Song W, Jia G, Yang X, He C, Tong MH . Mettl3-/Mettl14-mediated mRNA N(6)-methyladenosine modulates murine spermatogenesis. Cell Res, 2017,27(10):1216-1230.
[98]	Leseva M, Santostefano KE, Rosenbluth AL, Hamazaki T, Terada N . E2f6-mediated repression of the meiotic stag3 and Smc1β genes during early embryonic development requires Ezh2 and not the de novo methyltransferase Dnmt3b. Epigenetics, 2013,8(8):873-884.
[99]	Velasco G, Hubé F, Rollin J, Neuillet D, Philippe C, Bouzinba-Segard H, Galvani A, Viegas-Péquignot E, Francastel C . Dnmt3b recruitment through E2F6 transcriptional repressor mediates germ-line gene silencing in murine somatic tissues. Proc Natl Acad Sci USA, 2010,107(20):9281-9286.
[100]	Tatsumi D, Hayashi Y, Endo M, Kobayashi H, Yoshioka T, Kiso K, Kanno S, Nakai Y, Maeda I, Mochizuki K, Tachibana M, Koseki H, Okuda A, Yasui A, Kono T, Matsui Y . DNMTs and SETDB1 function as co-repressors in Max-mediated repression of germ cell-related genes in mouse embryonic stem cells. PLoS One, 2018,13(11):e0205969.
[101]	Li HH, Lai P, Jia JP, Song YW, Xia Q, Huang KM, He N, Ping WF, Chen JY, Yang ZZ, Li J, Yao MZ, Dong XT, Zhao JC, Hou CH, Esteban MA, Gao SR, Pei DQ, Hutchins AP, Yao HJ . RNA helicase DDX5 inhibits reprogramming to pluripotency by miRNA-based repression of RYBP and its PRC1-dependent and -independent functions. Cell Stem Cell, 2017,20(4):462-477.
[102]	Cheng FHC, Lin HY, Hwang TW, Chen YC, Huang RL, Chang CB, Yang W, Lin RI, Lin CW, Chen GCW, Mai SY, Lin JMJ, Chuang YM, Chou JL, Kuo LW, Li C, Cheng ASL, Lai HC, Wu SF, Tsai JC, Chan MWY . E2f6 functions as a competing endogenous RNA, and transcriptional repressor, to promote ovarian cancer stemness. Cancer Sci, 2019,110(3):1085-1095.

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PRC1.6复合体表观遗传调控生殖谱系特异性基因的时空表达

Controlling the spatiotemporal expression of germ line specific genes by PRC1.6 complex

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[2]	黄骥，张红生. TFⅢA型锌指蛋白及在提高植物耐逆性中的作用[J]. 遗传, 2007, 29(8): 915-922.
[3]	田春艳，张令强，贺福初. KRAB型锌指蛋白(KZNF)的研究进展[J]. 遗传, 2006, 28(11): 1451-1456.