Bend family proteins mark chromatin boundaries and synergistically promote early germ cell differentiation

Guang Shi, Yaofu Bai, Xiya Zhang, Junfeng Su, Junjie Pang, Quanyuan He, Pengguihang Zeng, Junjun Ding, Yuanyan Xiong, Jingran Zhang, Jingwen Wang, Dan Liu, Wenbin Ma, Junjiu Huang, Zhou Songyang

PDF(3114 KB)
PDF(3114 KB)
Protein Cell ›› 2022, Vol. 13 ›› Issue (10) : 721-741. DOI: 10.1007/s13238-021-00884-1
RESEARCH ARTICLE
RESEARCH ARTICLE

Bend family proteins mark chromatin boundaries and synergistically promote early germ cell differentiation

Author information +
History +

Cite this article

Download citation ▾
Guang Shi, Yaofu Bai, Xiya Zhang, Junfeng Su, Junjie Pang, Quanyuan He, Pengguihang Zeng, Junjun Ding, Yuanyan Xiong, Jingran Zhang, Jingwen Wang, Dan Liu, Wenbin Ma, Junjiu Huang, Zhou Songyang. Bend family proteins mark chromatin boundaries and synergistically promote early germ cell differentiation. Protein Cell, 2022, 13(10): 721‒741 https://doi.org/10.1007/s13238-021-00884-1

References

[1]
Abhiman S, Iyer LM, Aravind L (2008) BEN: a novel domain in chromatin factors and DNA viral proteins. Bioinformatics 24: 458- 461
CrossRef Google scholar
[2]
Afgan E, Baker D, Batut B, van den Beek M, Bouvier D, Cech M, Chilton J, Clements D, Coraor N, Gruning BA et al (2018) The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res 46: W537- W544
CrossRef Google scholar
[3]
Arzate-Mejia R.G., Recillas-Targa F., and Corces V.G. (2018). Developing in 3D: the role of CTCF in cell differentiation. Development 145
CrossRef Google scholar
[4]
Bailey TL (2011) DREME: motif discovery in transcription factor ChIP-seq data. Bioinformatics 27: 1653- 1659
CrossRef Google scholar
[5]
Bailey TL (2012) Inferring direct DNA binding from ChIP-seq. Nucleic Acids Res 40: e128
CrossRef Google scholar
[6]
Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: 823- 837
CrossRef Google scholar
[7]
Beagan JA, Phillips-Cremins JE (2020) On the existence and functionality of topologically associating domains. Nat Genet 52: 8- 16
CrossRef Google scholar
[8]
Beagan JA, Duong MT, Titus KR, Zhou L, Cao Z, Ma J, Lachanski CV, Gillis DR, Phillips-Cremins JE (2017) YY1 and CTCF orchestrate a 3D chromatin looping switch during early neural lineage commitment. Genome Res 27: 1139- 1152
CrossRef Google scholar
[9]
Bortvin A, Goodheart M, Liao M, Page DC (2004) Dppa3/Pgc7/stella is a maternal factor and is not required for germ cell specification in mice. BMC Dev Biol 4: 2
CrossRef Google scholar
[10]
Buecker C, Srinivasan R, Wu Z, Calo E, Acampora D, Faial T, Simeone A, Tan M, Swigut T, Wysocka J (2014) Reorganization of enhancer patterns in transition from naive to primed pluripotency. Cell Stem Cell 14: 838- 853
CrossRef Google scholar
[11]
Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ (2013) Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods 10: 1213- 1218
CrossRef Google scholar
[12]
Cuddapah S, Jothi R, Schones DE, Roh TY, Cui K, Zhao K (2009) Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res 19: 24- 32
CrossRef Google scholar
[13]
Dai Q, Ren A, Westholm JO, Serganov AA, Patel DJ, Lai EC (2013) The BEN domain is a novel sequence-specific DNA-binding domain conserved in neural transcriptional repressors. Genes Dev 27: 602- 614
CrossRef Google scholar
[14]
Dai Q, Ren A, Westholm JO, Duan H, Patel DJ, Lai EC (2015) Common and distinct DNA-binding and regulatory activities of the BEN-solo transcription factor family. Genes Dev 29: 48- 62
CrossRef Google scholar
[15]
de Sousa Lopes SM, Roelen BA, Monteiro RM, Emmens R, Lin HY, Li E, Lawson KA, Mummery CL (2004) BMP signaling mediated by ALK2 in the visceral endoderm is necessary for the generation of primordial germ cells in the mouse embryo. Genes Dev 18: 1838- 1849
CrossRef Google scholar
[16]
Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu JS, Ren B (2012) Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485: 376- 380
CrossRef Google scholar
[17]
Dixon JR, Gorkin DU, Ren B (2016) Chromatin domains: the unit of chromosome organization. Mol Cell 62: 668- 680
CrossRef Google scholar
[18]
Duggal G, Heindryckx B, Warrier S, O’Leary T, Van der Jeught M, Lierman S, Vossaert L, Deroo T, Deforce D, Chuva de Sousa Lopes SM et al (2013) Influence of activin A supplementation during human embryonic stem cell derivation on germ cell differentiation potential. Stem Cells Dev 22: 3141- 3155
CrossRef Google scholar
[19]
Duggal G, Heindryckx B, Warrier S, Taelman J, Van der Jeught M, Deforce D, de Sousa C, Lopes S, De Sutter P (2015) Exogenous supplementation of Activin A enhances germ cell differentiation of human embryonic stem cells. Mol Hum Reprod 21: 410- 423
CrossRef Google scholar
[20]
Fang F, Angulo B, Xia N, Sukhwani M, Wang Z, Carey CC, Mazurie A, Cui J, Wilkinson R, Wiedenheft B et al (2018) A PAX5-OCT4-PRDM1 developmental switch specifies human primordial germ cells. Nat Cell Biol 20: 655- 665
CrossRef Google scholar
[21]
Fedotova A, Clendinen C, Bonchuk A, Mogila V, Aoki T, Georgiev P, Schedl P (2019) Functional dissection of the developmentally restricted BEN domain chromatin boundary factor Insensitive. Epigenet Chromatin 12: 2
CrossRef Google scholar
[22]
Fischer G, Schmidt C, Opitz J, Cully Z, Kuhn K, Poschl E (1993) Identification of a novel sequence element in the common promoter region of human collagen type IV genes, involved in the regulation of divergent transcription. Biochem J 292 (Pt 3): 687- 695
CrossRef Google scholar
[23]
Gaszner M, Felsenfeld G (2006) Insulators: exploiting transcriptional and epigenetic mechanisms. Nat Rev Genet 7: 703- 713
CrossRef Google scholar
[24]
Gkountela S, Zhang KX, Shafiq TA, Liao WW, Hargan-Calvopina J, Chen PY, Clark AT (2015) DNA Demethylation dynamics in the human prenatal germline. Cell 161: 1425- 1436
CrossRef Google scholar
[25]
Guibert S, Forne T, Weber M (2012) Global profiling of DNA methylation erasure in mouse primordial germ cells. Genome Res 22: 633- 641
CrossRef Google scholar
[26]
Hackett JA, Sengupta R, Zylicz JJ, Murakami K, Lee C, Down TA, Surani MA (2013) Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science 339: 448- 452
CrossRef Google scholar
[27]
Hajkova P, Erhardt S, Lane N, Haaf T, El-Maarri O, Reik W, Walter J, Surani MA (2002) Epigenetic reprogramming in mouse primordial germ cells. Mech Dev 117: 15- 23
CrossRef Google scholar
[28]
Han L, Ren C, Li L, Li X, Ge J, Wang H, Miao YL, Guo X, Moley KH, Shu W et al (2018) Publisher correction: embryonic defects induced by maternal obesity in mice derive from Stella insufficiency in oocytes. Nat Genet 50: 768
[29]
Han L, Ren C, Zhang J, Shu W, Wang Q (2019) Differential roles of Stella in the modulation of DNA methylation during oocyte and zygotic development. Cell Discovery 5: 9
CrossRef Google scholar
[30]
Handoko L, Xu H, Li G, Ngan CY, Chew E, Schnapp M, Lee CW, Ye C, Ping JL, Mulawadi F et al (2011) CTCF-mediated functional chromatin interactome in pluripotent cells. Nat Genet 43: 630- 638
CrossRef Google scholar
[31]
Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M (2011) Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 146: 519- 532
CrossRef Google scholar
[32]
Hayashi K, Ogushi S, Kurimoto K, Shimamoto S, Ohta H, Saitou M (2012) Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science 338: 971- 975
CrossRef Google scholar
[33]
Hayashi M, Kawaguchi T, Durcova-Hills G, Imai H (2018) Generation of germ cells from pluripotent stem cells in mammals. Reprod Med Biol 17: 107- 114
CrossRef Google scholar
[34]
Hernandez-Hernandez A, Lilienthal I, Fukuda N, Galjart N, Hoog C (2016) CTCF contributes in a critical way to spermatogenesis and male fertility. Sci Rep 6: 28355
CrossRef Google scholar
[35]
Hikabe O, Hamazaki N, Nagamatsu G, Obata Y, Hirao Y, Hamada N, Shimamoto S, Imamura T, Nakashima K, Saitou M et al (2016) Reconstitution in vitro of the entire cycle of the mouse female germ line. Nature 539: 299- 303
CrossRef Google scholar
[36]
Hill PWS, Leitch HG, Requena CE, Sun Z, Amouroux R, RomanTrufero M, Borkowska M, Terragni J, Vaisvila R, Linnett S et al (2018) Epigenetic reprogramming enables the transition from primordial germ cell to gonocyte. Nature 555: 392- 396
CrossRef Google scholar
[37]
Hu CD, Kerppola TK (2003) Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis. Nat Biotechnol 21: 539- 545
CrossRef Google scholar
[38]
Irie N, Weinberger L, Tang WW, Kobayashi T, Viukov S, Manor YS, Dietmann S, Hanna JH, Surani MA (2015) SOX17 is a critical specifier of human primordial germ cell fate. Cell 160: 253- 268
CrossRef Google scholar
[39]
Ji X, Dadon DB, Powell BE, Fan ZP, Borges-Rivera D, Shachar S, Weintraub AS, Hnisz D, Pegoraro G, Lee TI et al (2016) 3D chromosome regulatory landscape of human pluripotent cells. Cell Stem Cell 18: 262- 275
CrossRef Google scholar
[40]
Kagiwada S, Kurimoto K, Hirota T, Yamaji M, Saitou M (2013) Replication-coupled passive DNA demethylation for the erasure of genome imprints in mice. EMBO J 32: 340- 353
[41]
Kehler J, Tolkunova E, Koschorz B, Pesce M, Gentile L, Boiani M, Lomeli H, Nagy A, McLaughlin KJ, Scholer HR et al (2004) Oct4 is required for primordial germ cell survival. EMBO Rep 5: 1078- 1083
CrossRef Google scholar
[42]
Kumar V, Muratani M, Rayan NA, Kraus P, Lufkin T, Ng HH, Prabhakar S (2013) Uniform, optimal signal processing of mapped deep-sequencing data. Nat Biotechnol 31: 615- 622
CrossRef Google scholar
[43]
Kurimoto K, Yabuta Y, Ohinata Y, Shigeta M, Yamanaka K, Saitou M (2008a) Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice. Genes Dev 22: 1617- 1635
CrossRef Google scholar
[44]
Kurimoto K, Yamaji M, Seki Y, Saitou M (2008b) Specification of the germ cell lineage in mice: a process orchestrated by the PRdomain proteins, Blimp1 and Prdm14. Cell Cycle 7: 3514- 3518
CrossRef Google scholar
[45]
Kurimoto K, Yabuta Y, Hayashi K, Ohta H, Kiyonari H, Mitani T, Moritoki Y, Kohri K, Kimura H, Yamamoto T et al (2015) Quantitative dynamics of chromatin remodeling during germ cell specification from mouse embryonic stem cells. Cell Stem Cell 16: 517- 532
CrossRef Google scholar
[46]
Lee J, Inoue K, Ono R, Ogonuki N, Kohda T, Kaneko-Ishino T, Ogura A, Ishino F (2002) Erasing genomic imprinting memory in mouse clone embryos produced from day 11. 5 primordial germ cells. Development 129: 1807- 1817
[47]
Lee OH, Kim H, He Q, Baek HJ, Yang D, Chen LY, Liang J, Chae HK, Safari A, Liu D et al (2011) Genome-wide YFP fluorescence complementation screen identifies new regulators for telomere signaling in human cells. Mol Cell Proteom: MCP 10: M110001628
CrossRef Google scholar
[48]
Li Y, Zhang Z, Chen J, Liu W, Lai W, Liu B, Li X, Liu L, Xu S, Dong Q et al (2018) Stella safeguards the oocyte methylome by preventing de novo methylation mediated by DNMT1. Nature 564: 136- 140
CrossRef Google scholar
[49]
Liu L, Mao SQ, Ray C, Zhang Y, Bell FT, Ng SF, Xu GL, Li X (2015) Differential regulation of genomic imprinting by TET proteins in embryonic stem cells. Stem Cell Res 15: 435- 443
CrossRef Google scholar
[50]
Liu X, Wang C, Liu W, Li J, Li C, Kou X, Chen J, Zhao Y, Gao H, Wang H et al (2016) Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos. Nature 537: 558- 562
CrossRef Google scholar
[51]
Lobanenkov VV, Nicolas RH, Adler VV, Paterson H, Klenova EM, Polotskaja AV, Goodwin GH (1990) A novel sequence-specific DNA binding protein which interacts with three regularly spaced direct repeats of the CCCTC-motif in the 5’-flanking sequence of the chicken c-myc gene. Oncogene 5: 1743- 1753
[52]
Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, Bourque G, George J, Leong B, Liu J et al (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38: 431- 440
CrossRef Google scholar
[53]
Lucifero D, Mertineit C, Clarke HJ, Bestor TH, Trasler JM (2002) Methylation dynamics of imprinted genes in mouse germ cells. Genomics 79: 530- 538
CrossRef Google scholar
[54]
Magaraki A, van der Heijden G, Sleddens-Linkels E, Magarakis L, van Cappellen WA, Peters A, Gribnau J, Baarends WM, Eijpe M (2017) Silencing markers are retained on pericentric heterochromatin during murine primordial germ cell development. Epigenet Chromatin 10: 11
CrossRef Google scholar
[55]
Miyoshi N, Stel JM, Shioda K, Qu N, Odajima J, Mitsunaga S, Zhang X, Nagano M, Hochedlinger K, Isselbacher KJ et al (2016) Erasure of DNA methylation, genomic imprints, and epimutations in a primordial germ-cell model derived from mouse pluripotent stem cells. Proc Natl Acad Sci USA 113: 9545- 9550
CrossRef Google scholar
[56]
Moore JM, Rabaia NA, Smith LE, Fagerlie S, Gurley K, Loukinov D, Disteche CM, Collins SJ, Kemp CJ, Lobanenkov VV et al (2012) Loss of maternal CTCF is associated with peri-implantation lethality of Ctcf null embryos. PLoS ONE 7: e34915
CrossRef Google scholar
[57]
Mulholland CB, Nishiyama A, Ryan J, Nakamura R, Yigit M, Gluck IM, Trummer C, Qin W, Bartoschek MD, Traube FR et al (2020) Recent evolution of a TET-controlled and DPPA3/STELLA-driven pathway of passive DNA demethylation in mammals. Nat Commun 11: 5972
CrossRef Google scholar
[58]
Murakami K, Gunesdogan U, Zylicz JJ, Tang WWC, Sengupta R, Kobayashi T, Kim S, Butler R, Dietmann S, Surani MA (2016) NANOG alone induces germ cells in primed epiblast in vitro by activation of enhancers. Nature 529: 403- 407
CrossRef Google scholar
[59]
Nakaki F, Hayashi K, Ohta H, Kurimoto K, Yabuta Y, Saitou M (2013) Induction of mouse germ-cell fate by transcription factors in vitro. Nature 501: 222- 226
CrossRef Google scholar
[60]
Nakamura T, Arai Y, Umehara H, Masuhara M, Kimura T, Taniguchi H, Sekimoto T, Ikawa M, Yoneda Y, Okabe M et al (2007) PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat Cell Biol 9: 64- 71
CrossRef Google scholar
[61]
Ohinata Y, Payer B, O’Carroll D, Ancelin K, Ono Y, Sano M, Barton SC, Obukhanych T, Nussenzweig M, Tarakhovsky A et al (2005) Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436: 207- 213
CrossRef Google scholar
[62]
Okamura D, Tokitake Y, Niwa H, Matsui Y (2008) Requirement of Oct3/4 function for germ cell specification. Dev Biol 317: 576- 584
CrossRef Google scholar
[63]
Okashita N, Kumaki Y, Ebi K, Nishi M, Okamoto Y, Nakayama M, Hashimoto S, Nakamura T, Sugasawa K, Kojima N et al (2014) PRDM14 promotes active DNA demethylation through the teneleven translocation (TET)-mediated base excision repair pathway in embryonic stem cells. Development 141: 269- 280
CrossRef Google scholar
[64]
Pastor WA, Aravind L, Rao A (2013) TETonic shift: biological roles of TET proteins in DNA demethylation and transcription. Nat Rev Mol Cell Biol 14: 341- 356
CrossRef Google scholar
[65]
Payer B, Saitou M, Barton SC, Thresher R, Dixon JP, Zahn D, Colledge WH, Carlton MB, Nakano T, Surani MA (2003) Stella is a maternal effect gene required for normal early development in mice. Curr Biol: CB 13: 2110- 2117
CrossRef Google scholar
[66]
Payer B, de Sousa C, Lopes SM, Barton SC, Lee C, Saitou M, Surani MA (2006) Generation of stella-GFP transgenic mice: a novel tool to study germ cell development. Genesis 44: 75- 83
CrossRef Google scholar
[67]
Plasschaert RN, Vigneau S, Tempera I, Gupta R, Maksimoska J, Everett L, Davuluri R, Mamorstein R, Lieberman PM, Schultz D et al (2014) CTCF binding site sequence differences are associated with unique regulatory and functional trends during embryonic stem cell differentiation. Nucleic Acids Res 42: 774- 789
CrossRef Google scholar
[68]
Pope BD, Ryba T, Dileep V, Yue F, Wu W, Denas O, Vera DL, Wang Y, Hansen RS, Canfield TK et al (2014) Topologically associating domains are stable units of replication-timing regulation. Nature 515: 402- 405
CrossRef Google scholar
[69]
Radzisheuskaya A, Chia Gle B, dos Santos RL, Theunissen TW, Castro LF, Nichols J, Silva JC (2013) A defined Oct4 level governs cell state transitions of pluripotency entry and differentiation into all embryonic lineages. Nat Cell Biol 15: 579- 590
CrossRef Google scholar
[70]
Saitou M, Yamaji M (2010) Germ cell specification in mice: signaling, transcription regulation, and epigenetic consequences. Reproduction 139: 931- 942
CrossRef Google scholar
[71]
Saitou M, Kagiwada S, Kurimoto K (2012) Epigenetic reprogramming in mouse pre-implantation development and primordial germ cells. Development 139: 15- 31
CrossRef Google scholar
[72]
Senft AD, Bikoff EK, Robertson EJ, Costello I (2019) Genetic dissection of Nodal and Bmp signalling requirements during primordial germ cell development in mouse. Nat Commun 10: 1089
CrossRef Google scholar
[73]
Smith ZD, Meissner A (2013) DNA methylation: roles in mammalian development. Nat Rev Genet 14: 204- 220
CrossRef Google scholar
[74]
Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663- 676
CrossRef Google scholar
[75]
Tang WW, Kobayashi T, Irie N, Dietmann S, Surani MA (2016) Specification and epigenetic programming of the human germ line. Nat Rev Genet 17: 585- 600
CrossRef Google scholar
[76]
van den Berg DL, Zhang W, Yates A, Engelen E, Takacs K, Bezstarosti K, Demmers J, Chambers I, Poot RA (2008) Estrogen-related receptor beta interacts with Oct4 to positively regulate Nanog gene expression. Mol Cell Biol 28: 5986- 5995
CrossRef Google scholar
[77]
van den Berg DL, Snoek T, Mullin NP, Yates A, Bezstarosti K, Demmers J, Chambers I, Poot RA (2010) An Oct4-centered protein interaction network in embryonic stem cells. Cell Stem Cell 6: 369- 381
CrossRef Google scholar
[78]
Verma N, Pan H, Dore LC, Shukla A, Li QV, Pelham-Webb B, Teijeiro V, Gonzalez F, Krivtsov A, Chang CJ et al (2018) TET proteins safeguard bivalent promoters from de novo methylation in human embryonic stem cells. Nat Genet 50: 83- 95
CrossRef Google scholar
[79]
Vincent SD, Dunn NR, Sciammas R, Shapiro-Shalef M, Davis MM, Calame K, Bikoff EK, Robertson EJ (2005) The zinc finger transcriptional repressor Blimp1/Prdm1 is dispensable for early axis formation but is required for specification of primordial germ cells in the mouse. Development 132: 1315- 1325
CrossRef Google scholar
[80]
Vincent JJ, Huang Y, Chen PY, Feng S, Calvopina JH, Nee K, Lee SA, Le T, Yoon AJ, Faull K et al (2013) Stage-specific roles for tet1 and tet2 in DNA demethylation in primordial germ cells. Cell Stem Cell 12: 470- 478
CrossRef Google scholar
[81]
von Meyenn F, Berrens RV, Andrews S, Santos F, Collier AJ, Krueger F, Osorno R, Dean W, Rugg-Gunn PJ, Reik W (2016) Comparative principles of DNA methylation reprogramming during human and mouse in vitro primordial germ cell specification. Dev Cell 39: 104- 115
CrossRef Google scholar
[82]
Wan LB, Pan H, Hannenhalli S, Cheng Y, Ma J, Fedoriw A, Lobanenkov V, Latham KE, Schultz RM, Bartolomei MS (2008) Maternal depletion of CTCF reveals multiple functions during oocyte and preimplantation embryo development. Development 135: 2729- 2738
CrossRef Google scholar
[83]
Wei W, Qing T, Ye X, Liu H, Zhang D, Yang W, Deng H (2008) Primordial germ cell specification from embryonic stem cells. PLoS ONE 3: e4013
CrossRef Google scholar
[84]
Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, Schirghuber E, Tsutsumi S, Nagae G, Ishihara K, Mishiro T et al (2008) Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451: 796- 801
CrossRef Google scholar
[85]
Williams K, Christensen J, Pedersen MT, Johansen JV, Cloos PA, Rappsilber J, Helin K (2011) TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 473: 343- 348
CrossRef Google scholar
[86]
Wongtrakoongate P, Jones M, Gokhale PJ, Andrews PW (2013) STELLA facilitates differentiation of germ cell and endodermal lineages of human embryonic stem cells. PLoS ONE 8: e56893
CrossRef Google scholar
[87]
Wu X, Zhang Y (2017) TET-mediated active DNA demethylation:mechanism, function and beyond. Nat Rev Genet 18: 517- 534
CrossRef Google scholar
[88]
Yakhkeshi S, Rahimi S, Sharafi M, Hassani SN, Taleahmad S, Shahverdi A, Baharvand H (2018) In vitro improvement of quail primordial germ cell expansion through activation of TGF-beta signaling pathway. J Cell Biochem 119: 4309- 4319
CrossRef Google scholar
[89]
Yamaguchi S, Shen L, Liu Y, Sendler D, Zhang Y (2013) Role of Tet1 in erasure of genomic imprinting. Nature 504: 460- 464
CrossRef Google scholar
[90]
Yamaji M, Seki Y, Kurimoto K, Yabuta Y, Yuasa M, Shigeta M, Yamanaka K, Ohinata Y, Saitou M (2008) Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat Genet 40: 1016- 1022
CrossRef Google scholar
[91]
Yao M, Zhou X, Zhou J, Gong S, Hu G, Li J, Huang K, Lai P, Shi G, Hutchins AP et al (2018) PCGF5 is required for neural differentiation of embryonic stem cells. Nat Commun 9: 1463
CrossRef Google scholar
[92]
Zhang Y, Feng XH, Derynck R (1998) Smad3 and Smad4 cooperate with c-Jun/c-Fos to mediate TGF-beta-induced transcription. Nature 394: 909- 913
CrossRef Google scholar
[93]
Zhang H, Zhang X, Clark E, Mulcahey M, Huang S, Shi YG (2010) TET1 is a DNA-binding protein that modulates DNA methylation and gene transcription via hydroxylation of 5-methylcytosine. Cell Res 20: 1390- 1393
CrossRef Google scholar
[94]
Zhang W, Xia W, Wang Q, Towers AJ, Chen J, Gao R, Zhang Y, Yen CA, Lee AY, Li Y et al (2016) Isoform switch of TET1 regulates DNA demethylation and mouse development. Mol Cell 64: 1062- 1073
CrossRef Google scholar

RIGHTS & PERMISSIONS

2021 The Author(s)
AI Summary AI Mindmap
PDF(3114 KB)

Accesses

Citations

Detail

Sections
Recommended

/