表观“阅读器”BET蛋白家族对哺乳动物发育和iPSC重编程的调控

doi:10.16288/j.yczz.21-232

[an error occurred while processing this directive]

Hereditas(Beijing) ›› 2022, Vol. 44 ›› Issue (1): 36-45.doi: 10.16288/j.yczz.21-232

• Orginal Articles • Previous Articles Next Articles

Epigenetic “reader” BET proteins regulate mammalian development and iPSC reprogramming

Zhijing Zhang(), Yu Qiao, Yuchen Sun, Lei Lei()

Department of Histology and Embryology, Harbin Medical University, Harbin 150000, China

Received:2021-06-30 Revised:2021-08-23 Online:2022-01-20 Published:2021-10-26
Contact: Lei Lei E-mail:cdzzj1998@163.com;lei086@ems.hrbmu.edu.cn
Supported by:
Supported by the National Natural Science Foundation of China No(31671545)

Abstract

Abstract:

As an epigenetic “reader”, bromodomain and extra-terminal (BET) proteins play a vital role in mammalian development. Each member in the BET family regulates precisely the related genes and promotes the differentiation and development of early embryos specifically through recognizing a variety of epigenetic modifications and recruiting corresponding functional complexes. In addition, with the development of induced pluripotent stem cell (iPSC) technology, accumulating evidence have found that BET family proteins may also play a pivotal role in the iPSC reprogramming. In this review, we summarize the function of the BET family proteins in mammalian development and iPSC reprogramming from recent literatures and speculate new mechanisms of the BET family proteins in regulating reprogramming.

Key words: BET proteins, mammalian development, induced pluripotent stem cell (iPSC)

Zhijing Zhang, Yu Qiao, Yuchen Sun, Lei Lei. Epigenetic “reader” BET proteins regulate mammalian development and iPSC reprogramming[J]. Hereditas(Beijing), 2022, 44(1): 36-45.

Figures/Tables 2

References 78

[1]	Rivera RM, Ross JW. Epigenetics in fertilization and preimplantation embryo development. Prog Biophys Mol Biol, 2013, 113(3):423-432. doi: 10.1016/j.pbiomolbio.2013.02.001
[2]	Amdani SN, Yeste M, Jones C, Coward K. Sperm factors and oocyte activation: current controversies and considerations. Biol Reprod, 2015, 93(2): 50,1-8.
[3]	Minami N, Suzuki T, Tsukamoto S. Zygotic gene activation and maternal factors in mammals. J Reprod Dev, 2007, 53(4):707-715. doi: 10.1262/jrd.19029
[4]	Tadros W, Lipshitz HD. The maternal-to-zygotic transition: a play in two acts. Development, 2009, 136(18):3033-3042. doi: 10.1242/dev.033183 pmid: 19700615
[5]	Mihajlović AI, Bruce AW. The first cell-fate decision of mouse preimplantation embryo development: integrating cell position and polarity. Open Biol, 2017, 7(11):170210. doi: 10.1098/rsob.170210
[6]	Yao CM, Zhang WH, Shuai L. The first cell fate decision in pre-implantation mouse embryos. Cell Regen, 2019, 8(2):51-57. doi: 10.1016/j.cr.2019.10.001
[7]	Zaware N, Zhou MM. Chemical modulators for epigenome reader domains as emerging epigenetic therapies for cancer and inflammation. Curr Opin Chem Biol, 2017, 39:116-125. doi: 10.1016/j.cbpa.2017.06.012
[8]	Filippakopoulos P, Knapp S. The bromodomain interaction module. FEBS Lett, 2012, 586(17):2692-2704. doi: 10.1016/j.febslet.2012.04.045 pmid: 22710155
[9]	Filippakopoulos P, Picaud S, Mangos M, Keates T, Lambert JP, Barsyte-Lovejoy D, Felletar I, Volkmer R, Müller S, Pawson T, Gingras AC, Arrowsmith CH, Knapp S. Histone recognition and large-scale structural analysis of the human bromodomain family. Cell, 2012, 149(1):214-231. doi: 10.1016/j.cell.2012.02.013 pmid: 22464331
[10]	Waddington CH. Preliminary notes on the development of the wings in normal and mutant strains of Drosophila. Proc Natl Acad Sci USA, 1939, 25(7):299-307. doi: 10.1073/pnas.25.7.299
[11]	Holliday R. The inheritance of epigenetic defects. Science, 1987, 238(4824):163-170. pmid: 3310230
[12]	Soshnev AA, Josefowicz SZ, Allis CD. Greater than the sum of parts: complexity of the dynamic epigenome. Mol Cell, 2016, 62(5):681-694. doi: 10.1016/j.molcel.2016.05.004 pmid: 27259201
[13]	Jenuwein T, Allis CD. Translating the histone code. Science, 2001, 293(5532):1074-1080. pmid: 11498575
[14]	Lawrence M, Daujat S, Schneider R. Lateral thinking: how histone modifications regulate gene expression. Trends Genet, 2016, 32(1):42-56. doi: S0168-9525(15)00193-6 pmid: 26704082
[15]	Villaseñor R, Baubec T. Regulatory mechanisms governing chromatin organization and function. Curr Opin Cell Biol, 2021, 70:10-17. doi: 10.1016/j.ceb.2020.10.015
[16]	Ura K, Kurumizaka H, Dimitrov S, Almouzni G, Wolffe AP. Histone acetylation: influence on transcription, nucleosome mobility and positioning, and linker histone- dependent transcriptional repression. EMBO J, 1997, 16(8):2096-2107. pmid: 9155035
[17]	Musselman CA, Lalonde ME, Côté J, Kutateladze TG. Perceiving the epigenetic landscape through histone readers. Nat Struct Mol Biol, 2012, 19(12):1218-1227. doi: 10.1038/nsmb.2436
[18]	Patel DJ. A structural perspective on readout of epigenetic histone and DNA methylation marks. Cold Spring Harb Perspect Biol, 2016, 8(3):a018754. doi: 10.1101/cshperspect.a018754
[19]	Villaseñor R, Pfaendler R, Ambrosi C, Butz S, Giuliani S, Bryan E, Sheahan TW, Gable AL, Schmolka N, Manzo M, Wirz J, Feller C, Von Mering C, Aebersold R, Voigt P, Baubec T. ChromID identifies the protein interactome at chromatin marks. Nat Biotechnol, 2020, 38(6):728-736. doi: 10.1038/s41587-020-0434-2 pmid: 32123383
[20]	Tchasovnikarova IA, Timms RT, Matheson NJ, Wals K, Antrobus R, Göttgens B, Dougan G, Dawson MA, Lehner PJ. GENE SILENCING. Epigenetic silencing by the HUSH complex mediates position-effect variegation in human cells. Science, 2015, 348(6242):1481-1485. doi: 10.1126/science.aaa7227 pmid: 26022416
[21]	Taverna SD, Li HT, Ruthenburg AJ, Allis CD, Patel DJ. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol, 2007, 14(11):1025-1040. doi: 10.1038/nsmb1338 pmid: 17984965
[22]	Zeng L, Zhou MM. Bromodomain: an acetyl-lysine binding domain. FEBS Lett, 2002, 513(1):124-128. pmid: 11911891
[23]	Matzuk MM, Mckeown MR, Filippakopoulos P, Li QL, Ma L, Agno JE, Lemieux ME, Picaud S, Yu RN, Qi J, Knapp S, Bradner JE. Small-molecule inhibition of BRDT for male contraception. Cell, 2012, 150(4):673-684. doi: 10.1016/j.cell.2012.06.045
[24]	Berkovits BD, Wolgemuth DJ. The first bromodomain of the testis-specific double bromodomain protein Brdt is required for chromocenter organization that is modulated by genetic background. Dev Biol, 2011, 360(2):358-368. doi: 10.1016/j.ydbio.2011.10.005 pmid: 22020252
[25]	Bisgrove DA, Mahmoudi T, Henklein P, Verdin E. Conserved P-TEFb-interacting domain of BRD4 inhibits HIV transcription. Proc Natl Acad Sci USA, 2007, 104(34):13690-13695. doi: 10.1073/pnas.0705053104
[26]	Zhao R, Nakamura T, Fu Y, Lazar Z, Spector DL. Gene bookmarking accelerates the kinetics of post-mitotic transcriptional re-activation. Nat Cell Biol, 2011, 13(11):1295-1304. doi: 10.1038/ncb2341 pmid: 21983563
[27]	Gaucher J, Boussouar F, Montellier E, Curtet S, Buchou T, Bertrand S, Hery P, Jounier S, Depaux A, Vitte AL, Guardiola P, Pernet K, Debernardi A, Lopez F, Holota H, Imbert J, Wolgemuth DJ, Gérard M, Rousseaux S, Khochbin S. Bromodomain-dependent stage-specific male genome programming by Brdt. EMBO J, 2012, 31(19):3809-3820. doi: 10.1038/emboj.2012.233
[28]	Wang L, Wolgemuth DJ. BET protein BRDT complexes with HDAC1, PRMT5, and TRIM28 and functions in transcriptional repression during spermatogenesis. J Cell Biochem, 2016, 117(6):1429-1438. doi: 10.1002/jcb.25433 pmid: 26565999
[29]	Manterola M, Brown TM, Oh MY, Garyn C, Gonzalez BJ, Wolgemuth DJ. BRDT is an essential epigenetic regulator for proper chromatin organization, silencing of sex chromosomes and crossover formation in male meiosis. PLoS Genet, 2018, 14(3):e1007209. doi: 10.1371/journal.pgen.1007209
[30]	Yanagimachi R. Male gamete contributions to the embryo. Ann N Y Acad Sci, 2005, 1061:203-207. doi: 10.1196/annals.1336.022
[31]	Devaiah BN, Gegonne A, Singer DS. Bromodomain 4: a cellular Swiss army knife. J Leukoc Biol, 2016, 100(4):679-686. doi: 10.1189/jlb.2RI0616-250R
[32]	Floyd SR, Pacold ME, Huang QY, Clarke SM, Lam FC, Cannell IG, Bryson BD, Rameseder J, Lee MJ, Blake EJ, Fydrych A, Ho R, Greenberger BA, Chen GC, Maffa A, Del Rosario AM, Root DE, Carpenter AE, Hahn WC, Sabatini DM, Chen CC, White FM, Bradner JE, Yaffe MB. The bromodomain protein Brd4 insulates chromatin from DNA damage signalling. Nature, 2013, 498(7453):246-250. doi: 10.1038/nature12147
[33]	Liu W, Stein P, Cheng X, Yang W, Shao NY, Morrisey EE, Schultz RM, You J. BRD4 regulates Nanog expression in mouse embryonic stem cells and preimplantation embryos. Cell Death Differ, 2014, 21(12):1950-1960. doi: 10.1038/cdd.2014.124 pmid: 25146928
[34]	Houzelstein D, Bullock SL, Lynch DE, Grigorieva EF, Wilson VA, Beddington RS. Growth and early postimplantation defects in mice deficient for the bromodomain- containing protein Brd4. Mol Cell Biol, 2002, 22(11):3794-3802. doi: 10.1128/MCB.22.11.3794-3802.2002 pmid: 11997514
[35]	Nagashima T, Maruyama T, Furuya M, Kajitani T, Uchida H, Masuda H, Ono M, Arase T, Ozato K, Yoshimura Y. Histone acetylation and subcellular localization of chromosomal protein BRD4 during mouse oocyte meiosis and mitosis. Mol Hum Reprod, 2007, 13(3):141-148. pmid: 17267518
[36]	Beck S, Hanson I, Kelly A, Pappin DJ, Trowsdale J. A homologue of theDrosophila female sterile homeotic (fsh) gene in the class II region of the human MHC. DNA Seq, 1992, 2(4):203-210.
[37]	Florence B, Faller DV. You bet-cha: a novel family of transcriptional regulators. Front Biosci, 2001, 6:D1008-D1018.
[38]	Denis GV, Green MR. A novel, mitogen-activated nuclear kinase is related to a Drosophila developmental regulator. Genes Dev, 1996, 10(3):261-271. doi: 10.1101/gad.10.3.261
[39]	Shang EY, Wang XY, Wen DC, Greenberg DA, Wolgemuth DJ. Double bromodomain-containing gene Brd2 is essential for embryonic development in mouse. Dev Dyn, 2009, 238(4):908-917. doi: 10.1002/dvdy.21911
[40]	Gyuris A, Donovan DJ, Seymour KA, Lovasco LA, Smilowitz NR, Halperin AL, Klysik JE, Freiman RN. The chromatin-targeting protein Brd2 is required for neural tube closure and embryogenesis. Biochim Biophys Acta, 2009, 1789(5):413-421. doi: 10.1016/j.bbagrm.2009.03.005 pmid: 19362612
[41]	Denis GV, Mccomb ME, Faller DV, Sinha A, Romesser PB, Costello CE. Identification of transcription complexes that contain the double bromodomain protein Brd2 and chromatin remodeling machines. J Proteome Res, 2006, 5(3):502-511. doi: 10.1021/pr050430u
[42]	Leroy G, Rickards B, Flint SJ. The double bromodomain proteins Brd2 and Brd3 couple histone acetylation to transcription. Mol Cell, 2008, 30(1):51-60. doi: 10.1016/j.molcel.2008.01.018
[43]	Lambert JP, Picaud S, Fujisawa T, Hou HY, Savitsky P, Uuskula-Reimand L, Gupta GD, Abdouni H, Lin ZY, Tucholska M, Knight JDR, Gonzalez-Badillo B, St-Denis N, Newman JA, Stucki M, Pelletier L, Bandeira N, Wilson MD, Filippakopoulos P, Gingras AC. Interactome rewiring following pharmacological targeting of BET bromodomains. Mol Cell, 2019, 73(3):621-638 e617. doi: 10.1016/j.molcel.2018.11.006
[44]	Lamonica JM, Deng WL, Kadauke S, Campbell AE, Gamsjaeger R, Wang HX, Cheng Y, Billin AN, Hardison RC, Mackay JP, Blobel GA. Bromodomain protein Brd3 associates with acetylated GATA1 to promote its chromatin occupancy at erythroid target genes. Proc Natl Acad Sci USA, 2011, 108(22):E159-168. doi: 10.1073/pnas.1102140108
[45]	Kulikowski E, Rakai BD, Wong NCW. Inhibitors of bromodomain and extra-terminal proteins for treating multiple human diseases. Med Res Rev, 2021, 41(1):223-245. doi: 10.1002/med.v41.1
[46]	Wu T, Kamikawa YF, Donohoe ME. Brd4's bromodomains mediate histone H3 acetylation and chromatin remodeling in pluripotent cells through P300 and Brg1. Cell Rep, 2018, 25(7):1756-1771. doi: 10.1016/j.celrep.2018.10.003
[47]	Greer CB, Tanaka Y, Kim YJ, Xie P, Zhang MQ, Park IH, Kim TH. Histone deacetylases positively regulate transcription through the elongation machinery. Cell Rep, 2015, 13(7):1444-1455. doi: 10.1016/j.celrep.2015.10.013
[48]	Jang MK, Mochizuki K, Zhou MS, Jeong HS, Brady JN, Ozato K. The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase II-dependent transcription. Mol Cell, 2005, 19(4):523-534. doi: 10.1016/j.molcel.2005.06.027
[49]	Yang ZY, Yik JHN, Chen RC, He NH, Jang MK, Ozato K, Zhou Q. Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Mol Cell, 2005, 19(4):535-545. doi: 10.1016/j.molcel.2005.06.029
[50]	Zhang WS, Prakash C, Sum C, Gong Y, Li YH, Kwok JJ, Thiessen N, Pettersson S, Jones SJM, Knapp S, Yang H, Chin KC. Bromodomain-containing protein 4 (BRD4) regulates RNA polymerase II serine 2 phosphorylation in human CD4+ T cells. J Biol Chem, 2012, 287(51):43137-43155. doi: 10.1074/jbc.M112.413047
[51]	Sims RJ 3rd, Belotserkovskaya R, Reinberg D. Elongation by RNA polymerase II: the short and long of it. Genes Dev, 2004, 18(20):2437-2468. doi: 10.1101/gad.1235904
[52]	Itzen F, Greifenberg AK, Bösken CA, Geyer M. Brd4 activates P-TEFb for RNA polymerase II CTD phosphorylation. Nucleic Acids Res, 2014, 42(12):7577-7590. doi: 10.1093/nar/gku449
[53]	Rasmussen EB, Lis JT. In vivo transcriptional pausing and cap formation on three Drosophila heat shock genes. Proc Natl Acad Sci USA, 1993, 90(17):7923-7927. doi: 10.1073/pnas.90.17.7923
[54]	Hnisz D, Abraham BJ, Lee TI, Lau A, Saint-André V, Sigova AA, Hoke HA, Young RA. Super-enhancers in the control of cell identity and disease. Cell, 2013, 155(4):934-947. doi: 10.1016/j.cell.2013.09.053
[55]	Pott S, Lieb JD. What are super-enhancers? Nat Genet, 2015, 47(1):8-12. doi: 10.1038/ng.3167
[56]	Whyte WA, Orlando DA, Hnisz D, Abraham BJ, Lin CY, Kagey MH, Rahl PB, Lee TI, Young RA. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell, 2013, 153(2):307-319. doi: 10.1016/j.cell.2013.03.035
[57]	Di Micco R, Fontanals-Cirera B, Low V, Ntziachristos P, Yuen SK, Lovell CD, Dolgalev I, Yonekubo Y, Zhang GT, Rusinova E, Gerona-Navarro G, Cañamero M, Ohlmeyer M, Aifantis I, Zhou MM, Tsirigos A, Hernando E. Control of embryonic stem cell identity by BRD4-dependent transcriptional elongation of super-enhancer-associated pluripotency genes. Cell Rep, 2014, 9(1):234-247. doi: 10.1016/j.celrep.2014.08.055
[58]	Lovén J, Hoke HA, Lin CY, Lau A, Orlando DA, Vakoc CR, Bradner JE, Lee TI, Young RA. Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell, 2013, 153(2):320-334. doi: 10.1016/j.cell.2013.03.036
[59]	Dey A, Nishiyama A, Karpova T, Mcnally J, Ozato K. Brd4 marks select genes on mitotic chromatin and directs postmitotic transcription. Mol Biol Cell, 2009, 20(23):4899-4909. doi: 10.1091/mbc.e09-05-0380
[60]	Mochizuki K, Nishiyama A, Jang MK, Dey A, Ghosh A, Tamura T, Natsume H, Yao HJ, Ozato K. The bromodomain protein Brd4 stimulates G1 gene transcription and promotes progression to S phase. J Biol Chem, 2008, 283(14):9040-9048. doi: 10.1074/jbc.M707603200 pmid: 18223296
[61]	Devaiah BN, Case-Borden C, Gegonne A, Hsu CH, Chen QR, Meerzaman D, Dey A, Ozato K, Singer DS. BRD4 is a histone acetyltransferase that evicts nucleosomes from chromatin. Nat Struct Mol Biol, 2016, 23(6):540-548. doi: 10.1038/nsmb.3228
[62]	You JX, Li Q, Wu C, Kim J, Ottinger M, Howley PM. Regulation of aurora B expression by the bromodomain protein Brd4. Mol Cell Biol, 2009, 29(18):5094-5103. doi: 10.1128/MCB.00299-09
[63]	Farina A, Hattori M, Qin J, Nakatani Y, Minato N, Ozato K. Bromodomain protein Brd4 binds to GTPase-activating SPA-1, modulating its activity and subcellular localization. Mol Cell Biol, 2004, 24(20):9059-9069. doi: 10.1128/MCB.24.20.9059-9069.2004
[64]	Maruyama T, Farina A, Dey A, Cheong J, Bermudez VP, Tamura T, Sciortino S, Shuman J, Hurwitz J, Ozato K. A mammalian bromodomain protein, brd4, interacts with replication factor C and inhibits progression to S phase. Mol Cell Biol, 2002, 22(18):6509-6520. doi: 10.1128/MCB.22.18.6509-6520.2002 pmid: 12192049
[65]	Tasdemir N, Banito A, Roe JS, Alonso-Curbelo D, Camiolo M, Tschaharganeh DF, Huang CH, Aksoy O, Bolden JE, Chen CC, Fennell M, Thapar V, Chicas A, Vakoc CR, Lowe SW. BRD4 connects enhancer remodeling to senescence immune surveillance. Cancer Discov, 2016, 6(6):612-629. doi: 10.1158/2159-8290.CD-16-0217 pmid: 27099234
[66]	Maherali N, Sridharan R, Xie W, Utikal J, Eminli S, Arnold K, Stadtfeld M, Yachechko R, Tchieu J, Jaenisch R, Plath K, Hochedlinger K. Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell, 2007, 1(1):55-70. doi: 10.1016/j.stem.2007.05.014 pmid: 18371336
[67]	Mikkelsen TS, Hanna J, Zhang XL, Ku MC, Wernig M, Schorderet P, Bernstein BE, Jaenisch R, Lander ES, Meissner A. Dissecting direct reprogramming through integrative genomic analysis. Nature, 2008, 454(7200):49-55. doi: 10.1038/nature07056
[68]	Liu LQ, Xu Y, He MH, Zhang M, Cui FG, Lu LN, Yao MZ, Tian WH, Benda C, Zhuang Q, Huang ZJ, Li WJ, Li XC, Zhao P, Fan WX, Luo ZW, Li Y, Wu YS, Hutchins AP, Wang DY, Tse HF, Schambach A, Frampton J, Qin BM, Bao XC, Yao HJ, Zhang BL, Sun H, Pei DQ, Wang HT, Wang J, Esteban MA. Transcriptional pause release is a rate-limiting step for somatic cell reprogramming. Cell Stem Cell, 2014, 15(5):574-588. doi: 10.1016/j.stem.2014.09.018
[69]	Di Stefano B, Collombet S, Jakobsen JS, Wierer M, Sardina JL, Lackner A, Stadhouders R, Segura-Morales C, Francesconi M, Limone F, Mann M, Porse B, Thieffry D, Graf T. C/EBPalpha creates elite cells for iPSC reprogramming by upregulating Klf4 and increasing the levels of Lsd1 and Brd4. Nat Cell Biol, 2016, 18(4):371-381. doi: 10.1038/ncb3326 pmid: 26974661
[70]	Wang Z, Oron E, Nelson B, Razis S, Ivanova N. Distinct lineage specification roles for NANOG, OCT4, and SOX2 in human embryonic stem cells. Cell Stem Cell, 2012, 10(4):440-454. doi: 10.1016/j.stem.2012.02.016
[71]	Shao ZC, Yao CP, Khodadadi-Jamayran A, Xu WH, Townes TM, Crowley MR, Hu KJ. Reprogramming by de-bookmarking the somatic transcriptional program through targeting of BET bromodomains. Cell Rep, 2016, 16(12):3138-3145. doi: 10.1016/j.celrep.2016.08.060
[72]	Yamanaka S. Elite and stochastic models for induced pluripotent stem cell generation. Nature, 2009, 460(7251):49-52. doi: 10.1038/nature08180
[73]	Shao ZC, Zhang RW, Khodadadi-Jamayran A, Chen B, Crowley MR, Festok MA, Crossman DK, Townes TM, Hu KJ. The acetyllysine reader BRD3R promotes human nuclear reprogramming and regulates mitosis. Nat Commun, 2016, 7:10869. doi: 10.1038/ncomms10869
[74]	Lorthongpanich C, Solter D, Lim CY. Nuclear reprogramming in zygotes. Int J Dev Biol, 2010, 54(11-12):1631-1640. doi: 10.1387/ijdb.103201cl pmid: 21404184
[75]	Egli D, Birkhoff G, Eggan K. Mediators of reprogramming: transcription factors and transitions through mitosis. Nat Rev Mol Cell Biol, 2008, 9(7):505-516.
[76]	Izumikawa K, Ishikawa H, Yoshikawa H, Fujiyama S, Watanabe A, Aburatani H, Tachikawa H, Hayano T, Miura Y, Isobe T, Simpson RJ, Li L, Min JR, Takahashi N. LYAR potentiates rRNA synthesis by recruiting BRD2/4 and the MYST-type acetyltransferase KAT7 to rDNA. Nucleic Acids Res, 2019, 47(19):10357-10372. doi: 10.1093/nar/gkz747 pmid: 31504794
[77]	Zhao QS, Wu YS, Shan ZY, Bai GY, Wang ZD, Hu J, Liu L, Li T, Shen JL, Lei L. Serum starvation-induced cell cycle synchronization stimulated mouse rDNA transcription reactivation during somatic cell reprogramming into iPSCs. Stem Cell Res Ther, 2016, 7(1):112. doi: 10.1186/s13287-016-0369-1
[78]	Zheng Z, Jia JL, Bou G, Hu LL, Wang ZD, Shen XH, Shan ZY, Shen JL, Liu ZH, Lei L. rRNA genes are not fully activated in mouse somatic cell nuclear transfer embryos. J Biol Chem, 2012, 287(24):19949-19960. doi: 10.1074/jbc.M112.355099

Metrics

Comments

www.chinagene.cn
备案号：京ICP备09063187号

Epigenetic “reader” BET proteins regulate mammalian development and iPSC reprogramming

RichHTML

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

Figures/Tables 2

References 78

Related Articles 0

Recommended Articles

Metrics

Comments