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Protein & Cell

ISSN 1674-800X

ISSN 1674-8018(Online)

CN 11-5886/Q

邮发代号 80-984

2019 Impact Factor: 10.164

Protein & Cell  2020, Vol. 11 Issue (3): 161-186   https://doi.org/10.1007/s13238-019-0650-z
  本期目录
Long non-coding RNA LncKdm2bregulates cortical neuronal differentiation by cis-activating Kdm2b
Wei Li1, Wenchen Shen1, Bo Zhang1, Kuan Tian1, Yamu Li1, Lili Mu1, Zhiyuan Luo1, Xiaoling Zhong1, Xudong Wu2, Ying Liu1(), Yan Zhou1()
1. College of Life Sciences, Renmin Hospital of Wuhan University, Medical Research Institute at School of Medicine, Wuhan University, Wuhan 430072, China
2. Department of Cell Biology, Tianjin Medical University, Qixiangtai Road 22, Tianjin 300070, China
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Abstract

The mechanisms underlying spatial and temporal control of cortical neurogenesis of the brain are largely elusive. Long non-coding RNAs (lncRNAs) have emerged as essential cell fate regulators. Here we found LncKdm2b(also known as Kancr), a lncRNA divergently transcribed from a bidirectional promoter of Kdm2b,is transiently expressed during early differentiation of cortical projection neurons. Interestingly, Kdm2b’s transcription is positively regulated in cisby LncKdm2b, which has intrinsic-activating function and facilitates a permissive chromatin environment at the Kdm2b’s promoter by associating with hnRNPAB. Lineage tracing experiments and phenotypic analyses indicated LncKdm2band Kdm2bare crucial in proper differentiation and migration of cortical projection neurons. These observations unveiled a lncRNA-dependent machinery in regulating cortical neuronal differentiation.

Key wordslong non-coding RNA    neuronal differentiation    cerebral cortex    KDM2B    divergent lncRNA
收稿日期: 2019-06-11      出版日期: 2020-03-23
Corresponding Author(s): Ying Liu,Yan Zhou   
 引用本文:   
. [J]. Protein & Cell, 2020, 11(3): 161-186.
Wei Li, Wenchen Shen, Bo Zhang, Kuan Tian, Yamu Li, Lili Mu, Zhiyuan Luo, Xiaoling Zhong, Xudong Wu, Ying Liu, Yan Zhou. Long non-coding RNA LncKdm2bregulates cortical neuronal differentiation by cis-activating Kdm2b. Protein Cell, 2020, 11(3): 161-186.
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https://academic.hep.com.cn/pac/CN/10.1007/s13238-019-0650-z
https://academic.hep.com.cn/pac/CN/Y2020/V11/I3/161
1 J Aprea, S Prenninger, M Dori, T Ghosh, LS Monasor, E Wessendorf, S Zocher, S Massalini, D Alexopoulou, M Lescheet al. (2013) Transcriptome sequencing during mouse brain development identifies long non-coding RNAs functionally involved in neurogenic commitment . EMBO J 32:3145–3160
https://doi.org/10.1038/emboj.2013.245
2 JR Arron, MM Winslow, A Polleri, CP Chang, H Wu, X Gao, JR Neilson, L Chen, JJ Heit, SK Kimet al. (2006) NFAT dysregulation by increased dosage of DSCR2 and DYRK1A on chromosome 21 . Nature 441:595–600
https://doi.org/10.1038/nature04678
3 R Ayala, T Shu, LH Tsai (2007) Trekking across the brain: the journey of neuronal migration . Cell 128:29–43
https://doi.org/10.1016/j.cell.2006.12.021
4 AE Ayoub, S Oh, Y Xie, J Leng, J Cotney, MH Dominguez, JP Noonan, P Rakic (2011) Transcriptional programs in transient embryonic zones of the cerebral cortex defined by high-resolution mRNA sequencing . Proc Natl Acad Sci USA 108:14950–14955
https://doi.org/10.1073/pnas.1112213108
5 ST Baek, G Kerjan, SL Bielas, JE Lee, AG Fenstermaker, G Novarino, JG Gleeson (2014) Off-target effect of doublecortin family shRNA on neuronal migration associated with endogenous microRNA dysregulation . Neuron 82:1255–1262
https://doi.org/10.1016/j.neuron.2014.04.036
6 AR Bassett, A Akhtar, DP Barlow, AP Bird, N Brockdorff, D Duboule, A Ephrussi, AC Ferguson-Smith, TR Gingeras, W Haertyet al. (2014) Considerations when investigating lncRNA function in vivo . Elife 3:e03058
https://doi.org/10.7554/eLife.03058
7 M Bauer, N Kinkl, A Meixner, E Kremmer, M Riemenschneider, H Forstl, T Gasser, M Ueffing (2009) Prevention of interferonstimulated gene expression using microRNA-designed hairpins . Gene Ther 16:142–147
https://doi.org/10.1038/gt.2008.123
8 TG Belgard, AC Marques, PL Oliver, HO Abaan, TM Sirey, A HoerderSuabedissen, F Garcia-Moreno, Z Molnar, EH Margulies, CP Ponting (2011) A transcriptomic atlas of mouse neocortical layers. Neuron 71:605–616
https://doi.org/10.1016/j.neuron.2011.06.039
9 R Benavides-Piccione, M Dierssen, I Ballesteros-Yanez, M Martinez de Lagran, ML Arbones, V Fotaki, J DeFelipe, GN Elston (2005) Alterations in the phenotype of neocortical pyramidal cells in the Dyrk1A+/mouse . Neurobiol Dis 20:115–122
https://doi.org/10.1016/j.nbd.2005.02.004
10 EG Berghoff, MF Clark, S Chen, I Cajigas, DE Leib, JD Kohtz (2013) Evf2 (Dlx6as) lncRNA regulates ultraconserved enhancer methylation and the differential transcriptional control of adjacent genes . Development 140:4407–4416
https://doi.org/10.1242/dev.099390
11 DS Cabianca, V Casa, B Bodega, A Xynos, E Ginelli, Y Tanaka, D Gabellini (2012) A long ncRNA links copy number variation to a polycomb/trithorax epigenetic switch in FSHD muscular dystrophy . Cell 149:819–831
https://doi.org/10.1016/j.cell.2012.03.035
12 M Cheng, X Jin, L Mu, F Wang, W Li, X Zhong, X Liu, W Shen, Y Liu, Y Zhou (2016) Combination of the clustered regularly interspaced short palindromic repeats (CRISPR)-associated 9 technique with the piggybac transposon system for mouse in utero electroporation to study cortical development . J Neurosci Res 94:814–824
https://doi.org/10.1002/jnr.23776
13 P Corish, C Tyler-Smith (1999) Attenuation of green fluorescent protein half-life in mammalian cells . Protein Eng 12:1035–1040
https://doi.org/10.1093/protein/12.12.1035
14 W da Huang, BT Sherman, RA Lempicki (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources . Nat Protoc 4:44–57
https://doi.org/10.1038/nprot.2008.211
15 G Diez-Roux, S Banfi, M Sultan, L Geffers, S Anand, D Rozado, A Magen, E Canidio, M Pagani, I Pelusoet al. (2011) A highresolution anatomical atlas of the transcriptome in the mouse embryo . PLoS Biol 9:e1000582
https://doi.org/10.1371/journal.pbio.1000582
16 AA Dillman, DN Hauser, JR Gibbs, MA Nalls, MK McCoy, IN Rudenko, D Galter, MR Cookson (2013) mRNA expression, splicing and editing in the embryonic and adult mouse cerebral cortex . Nat Neurosci 16:499–506
https://doi.org/10.1038/nn.3332
17 JM Engreitz, JE Haines, EM Perez, G Munson, J Chen, M Kane, PE McDonel, M Guttman, ES Lander (2016) Local regulation of gene expression by lncRNA promoters, transcription and splicing . Nature 539:452–455
https://doi.org/10.1038/nature20149
18 SA Fietz, WB Huttner (2011) Cortical progenitor expansion, selfrenewal and neurogenesis-a polarized perspective . Curr Opin Neurobiol 21:23–35
https://doi.org/10.1016/j.conb.2010.10.002
19 V Fotaki, M Dierssen, S Alcantara, S Martinez, E Marti, C Casas, J Visa, E Soriano, X Estivill, ML Arbones (2002) Dyrk1A haploinsufficiency affects viability and causes developmental delay and abnormal brain morphology in mice . Mol Cell Biol 22:6636–6647
https://doi.org/10.1128/MCB.22.18.6636-6647.2002
20 XD Fu (2014) Non-coding RNA: a new frontier in regulatory biology . Natl Sci Rev 1:190–204
https://doi.org/10.1093/nsr/nwu008
21 N Gaspard, T Bouschet, R Hourez, J Dimidschstein, G Naeije, J van den Ameele, I Espuny-Camacho, A Herpoel, L Passante, SN Schiffmannet al. (2008) An intrinsic mechanism of corticogenesis from embryonic stem cells . Nature 455:351–357
https://doi.org/10.1038/nature07287
22 A Ghosh, ME Greenberg (1995) Distinct roles for bFGF and NT-3 in the regulation of cortical neurogenesis . Neuron 15:89–103
https://doi.org/10.1016/0896-6273(95)90067-5
23 J Goecks, A Nekrutenko, J Taylor, T Galaxy (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences . Genome Biol 11:R86
https://doi.org/10.1186/gb-2010-11-8-r86
24 LC Greig, MB Woodworth, MJ Galazo, H Padmanabhan, JD Macklis (2013) Molecular logic of neocortical projection neuron specification, development and diversity . Nat Rev Neurosci 14:755–769
https://doi.org/10.1038/nrn3586
25 P Grote, L Wittler, D Hendrix, F Koch, S Wahrisch, A Beisaw, K Macura, G Blass, M Kellis, M Werberet al. (2013) The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse . Dev Cell 24:206–214
https://doi.org/10.1016/j.devcel.2012.12.012
26 C Guo, MJ Eckler, WL McKenna, GL McKinsey, JL Rubenstein, B Chen (2013) Fezf2 expression identifies a multipotent progenitor for neocortical projection neurons, astrocytes, and oligodendrocytes . Neuron 80:1167–1174
https://doi.org/10.1016/j.neuron.2013.09.037
27 M Guttman, M Garber, JZ Levin, J Donaghey, J Robinson, X Adiconis, L Fan, MJ Koziol, A Gnirke, C Nusbaumet al. (2010) Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs . Nat Biotechnol 28:503–510
https://doi.org/10.1038/nbt.1633
28 H Hagege, P Klous, C Braem, E Splinter, J Dekker, G Cathala, W de Laat, T Forne (2007) Quantitative analysis of chromosome conformation capture assays (3C-qPCR) . Nat Protoc 2:1722–1733
https://doi.org/10.1038/nprot.2007.243
29 ND Heintzman, GC Hon, RD Hawkins, P Kheradpour, A Stark, LF Harp, Z Ye, LK Lee, RK Stuart, CW Chinget al. (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression . Nature 459:108–112
https://doi.org/10.1038/nature07829
30 CC Homem, M Repic, JA Knoblich (2015) Proliferation control in neural stem and progenitor cells . Nat Rev Neurosci 16:647–659
https://doi.org/10.1038/nrn4021
31 I Imayoshi, R Kageyama (2014) bHLH factors in self-renewal, multipotency, and fate choice of neural progenitor cells . Neuron 82:9–23
https://doi.org/10.1016/j.neuron.2014.03.018
32 CA Klattenhoff, JC Scheuermann, LE Surface, RK Bradley, PA Fields, ML Steinhauser, H Ding, VL Butty, L Torrey, S Haaset al. (2013) Braveheart, a long noncoding RNA required for cardiovascular lineage commitment . Cell 152:570–583
https://doi.org/10.1016/j.cell.2013.01.003
33 F Kottakis, C Polytarchou, P Foltopoulou, I Sanidas, SC Kampranis, PN Tsichlis (2011) FGF-2 regulates cell proliferation, migration, and angiogenesis through an NDY1/KDM2B-miR-101-EZH2 pathway . Mol Cell 43:285–298
https://doi.org/10.1016/j.molcel.2011.06.020
34 KY Kwan, N Sestan, ES Anton (2012) Transcriptional co-regulation of neuronal migration and laminar identity in the neocortex . Development 139:1535–1546
https://doi.org/10.1242/dev.069963
35 JD Labonne, KH Lee, S Iwase, IK Kong, MP Diamond, LC Layman, CH Kim, HG Kim (2016) An atypical 12q24.31 microdeletion implicates six genes including a histone demethylase KDM2B and a histone methyltransferase SETD1B in syndromic intellectual disability . Hum Genet 135:757–771
https://doi.org/10.1007/s00439-016-1668-4
36 C Lepoivre, M Belhocine, A Bergon, A Griffon, M Yammine, L Vanhille, J Zacarias-Cabeza, MA Garibal, F Koch, MA Maqboolet al. (2013) Divergent transcription is associated with promoters of transcriptional regulators . BMC Genomics 14:914
https://doi.org/10.1186/1471-2164-14-914
37 W Li, D Notani, Q Ma, B Tanasa, E Nunez, AY Chen, D Merkurjev, J Zhang, K Ohgi, X Songet al. (2013) Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation . Nature 498:516–520
https://doi.org/10.1038/nature12210
38 Y Li, W Wang, F Wang, Q Wu, W Li, X Zhong, K Tian, T Zeng, L Gao, Y Liuet al. (2017) Paired related homeobox 1 transactivates dopamine D2 receptor to maintain propagation and tumorigenicity of glioma-initiating cells . J Mol Cell Biol 9:302–314
https://doi.org/10.1093/jmcb/mjx017
39 N Lin, KY Chang, Z Li, K Gates, ZA Rana, J Dang, D Zhang, T Han, CS Yang, TJ Cunninghamet al. (2014) An evolutionarily conserved long noncoding RNA TUNA controls pluripotency and neural lineage commitment . Mol Cell 53:1005–1019
https://doi.org/10.1016/j.molcel.2014.01.021
40 B Liu, B Ye, L Yang, X Zhu, G Huang, P Zhu, Y Du, J Wu, X Qin, R Chenet al. (2017) Long noncoding RNA lncKdm2b is required for ILC3 maintenance by initiation of Zfp292 expression . Nat Immunol 18:499–508
https://doi.org/10.1038/ni.3712
41 J Lu, V Sheen (2005) Periventricular heterotopia . Epilepsy Behav 7:143–149
https://doi.org/10.1016/j.yebeh.2005.05.001
42 S Luo, JY Lu, L Liu, Y Yin, C Chen, X Han, B Wu, R Xu, W Liu, P Yanet al. (2016) Divergent lncRNAs regulate gene expression and lineage differentiation in pluripotent cells . Cell Stem Cell 18:637–652
https://doi.org/10.1016/j.stem.2016.01.024
43 TR Mercer, IA Qureshi, S Gokhan, ME Dinger, G Li, JS Mattick, MF Mehler (2010) Long noncoding RNAs in neuronal-glial fate specification and oligodendrocyte lineage maturation . BMC Neurosci 11:14
https://doi.org/10.1186/1471-2202-11-14
44 BJ Molyneaux, LA Goff, AC Brettler, HH Chen, S Hrvatin, JL Rinn, P Arlotta (2015) DeCoN: genome-wide analysis of in vivo transcriptional dynamics during pyramidal neuron fate selection in neocortex . Neuron 85:275–288
https://doi.org/10.1016/j.neuron.2014.12.024
45 SY Ng, GK Bogu, BS Soh, LW Stanton (2013) The long noncoding RNA RMST interacts with SOX2 to regulate neurogenesis . Mol Cell 51:349–359
https://doi.org/10.1016/j.molcel.2013.07.017
46 FC Noonan, PJ Goodfellow, LJ Staloch, DG Mutch, TC Simon (2003) Antisense transcripts at the EMX2 locus in human and mouse . Genomics 81:58–66
https://doi.org/10.1016/S0888-7543(02)00023-X
47 UA Orom, T Derrien, M Beringer, K Gumireddy, A Gardini, G Bussotti, F Lai, M Zytnicki, C Notredame, Q Huanget al. (2010) Long noncoding RNAs with enhancer-like function in human cells . Cell 143:46–58
https://doi.org/10.1016/j.cell.2010.09.001
48 M Perino, GJ Veenstra (2016) Chromatin control of developmental dynamics and plasticity . Dev Cell 38:610–620
https://doi.org/10.1016/j.devcel.2016.08.004
49 J Ponjavic, PL Oliver, G Lunter, CP Ponting (2009) Genomic and transcriptional co-localization of protein-coding and long noncoding RNA pairs in the developing brain . PLoS Genet 5: e1000617
https://doi.org/10.1371/journal.pgen.1000617
50 AD Ramos, A Diaz, A Nellore, RN Delgado, KY Park, G GonzalesRoybal, MC Oldham, JS Song, DA Lim (2013) Integration of genome-wide approaches identifies lncRNAs of adult neural stem cells and their progeny in vivo . Cell Stem Cell 12:616–628
https://doi.org/10.1016/j.stem.2013.03.003
51 JL Rinn, HY Chang (2012) Genome regulation by long noncoding RNAs . Annu Rev Biochem 81:145–166
https://doi.org/10.1146/annurev-biochem-051410-092902
52 TC Roberts, JR Hart, MU Kaikkonen, MS Weinberg, PK Vogt, KV Morris (2015) Quantification of nascent transcription by bromouridine immunocapture nuclear run-on RT-qPCR . Nat Protoc 10:1198–1211
https://doi.org/10.1038/nprot.2015.076
53 LM Saba, SC Flink, LA Vanderlinden, Y Israel, L Tampier, G Colombo, K Kiianmaa, RL Bell, MP Printz, P Flodmanet al. (2015) The sequenced rat brain transcriptome—its use in identifying networks predisposing alcohol consumption . FEBS J 282:3556–3578
https://doi.org/10.1111/febs.13358
54 MR Sarkisian, CM Bartley, P Rakic (2008) Trouble making the first move: interpreting arrested neuronal migration in the cerebral cortex . Trends Neurosci 31:54–61
https://doi.org/10.1016/j.tins.2007.11.009
55 BS Scruggs, K Adelman (2015) The importance of controlling transcription elongation at coding and noncoding RNA loci . Cold Spring Harb Symp Quant Biol 80:33–44
https://doi.org/10.1101/sqb.2015.80.027235
56 BS Scruggs, DA Gilchrist, S Nechaev, GW Muse, A Burkholder, DC Fargo, K Adelman (2015) Bidirectional transcription arises from two distinct hubs of transcription factor binding and active chromatin . Mol Cell 58:1101–1112
https://doi.org/10.1016/j.molcel.2015.04.006
57 Q Shen, Y Wang, JT Dimos, CA Fasano, TN Phoenix, IR Lemischka, NB Ivanova, S Stifani, EE Morrisey, S Temple (2006) The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells . Nat Neurosci 9:743–751
https://doi.org/10.1038/nn1694
58 AA Sigova, AC Mullen, B Molinie, S Gupta, DA Orlando, MG Guenther, AE Almada, C Lin, PA Sharp, CC Giallourakiset al. (2013) Divergent transcription of long noncoding RNA/mRNA gene pairs in embryonic stem cells . Proc Natl Acad Sci USA 110:2876–2881
https://doi.org/10.1073/pnas.1221904110
59 JR Sinnamon, CB Waddell, S Nik, EI Chen, K Czaplinski (2012) Hnrpab regulates neural development and neuron cell survival after glutamate stimulation . RNA 18:704–719
https://doi.org/10.1261/rna.030742.111
60 G Spigoni, C Gedressi, A Mallamaci (2010) Regulation of Emx2 expression by antisense transcripts in murine cortico-cerebral precursors . PLoS ONE 5:e8658
https://doi.org/10.1371/journal.pone.0008658
61 C Trapnell, L Pachter, SL Salzberg (2009) TopHat: discovering splice junctions with RNA-Seq . Bioinformatics 25:1105–1111
https://doi.org/10.1093/bioinformatics/btp120
62 C Trapnell, A Roberts, L Goff, G Pertea, D Kim, DR Kelley, H Pimentel, SL Salzberg, JL Rinn, L Pachter (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks . Nat Protoc 7:562–578
https://doi.org/10.1038/nprot.2012.016
63 T Trimarchi, E Bilal, P Ntziachristos, G Fabbri, R Dalla-Favera, A Tsirigos, I Aifantis (2014) Genome-wide mapping and characterization of Notch-regulated long noncoding RNAs in acute leukemia . Cell 158:593–606
https://doi.org/10.1016/j.cell.2014.05.049
64 MC Tsai, O Manor, Y Wan, N Mosammaparast, JK Wang, F Lan, Y Shi, E Segal, HY Chang (2010) Long noncoding RNA as modular scaffold of histone modification complexes . Science 329:689–693
https://doi.org/10.1126/science.1192002
65 CD Venkov, AJ Link, JL Jennings, D Plieth, T Inoue, K Nagai, C Xu, YN Dimitrova, FJ Rauscher, EG Neilson (2007) A proximal activator of transcription in epithelial-mesenchymal transition . J Clin Invest 117:482–491
https://doi.org/10.1172/JCI29544
66 AL Vescovi, BA Reynolds, DD Fraser, S Weiss (1993) bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells . Neuron 11:951–966
https://doi.org/10.1016/0896-6273(93)90124-A
67 TA Vickers, S Koo, CF Bennett, ST Crooke, NM Dean, BF Baker (2003) Efficient reduction of target RNAs by small interfering RNA and RNase H-dependent antisense agents. A comparative analysis . J Biol Chem 278:7108–7118
https://doi.org/10.1074/jbc.M210326200
68 J Vierstra, E Rynes, R Sandstrom, M Zhang, T Canfield, RS Hansen, S Stehling-Sun, PJ Sabo, R Byron, R Humbertet al. (2014) Mouse regulatory DNA landscapes reveal global principles of cisregulatory evolution . Science 346:1007–1012
https://doi.org/10.1126/science.1246426
69 RY Walder, JA Walder (1988) Role of RNase H in hybrid-arrested translation by antisense oligonucleotides . Proc Natl Acad Sci USA 85:5011–5015
https://doi.org/10.1073/pnas.85.14.5011
70 A Wang, J Wang, Y Liu, Y Zhou (2017) Mechanisms of long noncoding RNAs in the assembly and plasticity of neural circuitry . Front Neural Circuits 11:76
https://doi.org/10.3389/fncir.2017.00076
71 KC Wang, YW Yang, B Liu, A Sanyal, R Corces-Zimmerman, Y Chen, BR Lajoie, A Protacio, RA Flynn, RA Guptaet al. (2011) A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression . Nature 472:120–124
https://doi.org/10.1038/nature09819
72 Y Wang, L He, Y Du, P Zhu, G Huang, J Luo, X Yan, B Ye, C Li, P Xiaet al. (2015) The long noncoding RNA lncTCF7 promotes selfrenewal of human liver cancer stem cells through activation of Wnt signaling . Cell Stem Cell 16:413–425
https://doi.org/10.1016/j.stem.2015.03.003
73 M Wu, PF Wang, JS Lee, S Martin-Brown, L Florens, M Washburn, A Shilatifard (2008) Molecular regulation of H3K4 trimethylation by Wdr82, a component of human Set1/COMPASS . Mol Cell Biol 28:7337–7344
https://doi.org/10.1128/MCB.00976-08
74 YH Xing, RW Yao, Y Zhang, CJ Guo, S Jiang, G Xu, R Dong, L Yang, LL Chen (2017) SLERT Regulates DDX21 Rings Associated with Pol I Transcription . Cell 169:664–678.e616
https://doi.org/10.1016/j.cell.2017.04.011
75 B Ye, B Liu, L Yang, X Zhu, D Zhang, W Wu, P Zhu, Y Wang, S Wang, P Xiaet al. (2018) LncKdm2b controls self-renewal of embryonic stem cells via activating expression of transcription factor Zbtb3 . EMBO J 37:e97174
https://doi.org/10.15252/embj.201797174
76 Y Yin, P Yan, J Lu, G Song, Y Zhu, Z Li, Y Zhao, B Shen, X Huang, H Zhuet al. (2015) Opposing roles for the lncRNA haunt and its genomic locus in regulating HOXA gene activation during embryonic stem cell differentiation . Cell Stem Cell 16:504–516
https://doi.org/10.1016/j.stem.2015.03.007
77 F Yue, Y Cheng, A Breschi, J Vierstra, W Wu, T Ryba, R Sandstrom, Z Ma, C Davis, BD Popeet al. (2014) A comparative encyclopedia of DNA elements in the mouse genome . Nature 515:355–364
https://doi.org/10.1038/nature13992
78 ZJ Zhou, Z Dai, SL Zhou, ZQ Hu, Q Chen, YM Zhao, YH Shi, Q Gao, WZ Wu, SJ Qiuet al. (2014) HNRNPAB induces epithelialmesenchymal transition and promotes metastasis of hepatocellular carcinoma by transcriptionally activating SNAIL . Cancer Res 74:2750
https://doi.org/10.1158/0008-5472.CAN-13-2509
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