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NANOG alone induces germ cells in primed epiblast in vitro by activation of enhancers
Open accessAbstract
Nanog, a core pluripotency factor in the inner cell mass of blastocysts, is also expressed in unipotent primordial germ cells (PGCs) in mice, where its precise role is yet unclear. We investigated this in an in vitro model, in which naive pluripotent embryonic stem (ES) cells cultured in basic fibroblast growth factor (bFGF) and activin A develop as epiblast-like cells (EpiLCs) and gain competence for a PGC-like fate. Consequently, bone morphogenetic protein 4 (BMP4), or ectopic expression of key germline transcription factors Prdm1, Prdm14 and Tfap2c, directly induce PGC-like cells (PGCLCs) in EpiLCs, but not in ES cells. Here we report an unexpected discovery that Nanog alone can induce PGCLCs in EpiLCs, independently of BMP4. We propose that after the dissolution of the naive ES-cell pluripotency network during establishment of EpiLCs, the epigenome is reset for cell fate determination. Indeed, we found genome-wide changes in NANOG-binding patterns between ES cells and EpiLCs, indicating epigenetic resetting of regulatory elements. Accordingly, we show that NANOG can bind and activate enhancers of Prdm1 and Prdm14 in EpiLCs in vitro; BLIMP1 (encoded by Prdm1) then directly induces Tfap2c. Furthermore, while SOX2 and NANOG promote the pluripotent state in ES cells, they show contrasting roles in EpiLCs, as Sox2 specifically represses PGCLC induction by Nanog. This study demonstrates a broadly applicable mechanistic principle for how cells acquire competence for cell fate determination, resulting in the context-dependent roles of key transcription factors during development.
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“For Dex inducible WT or APPA Mettl3 plasmid, GRBD insert from pPyCAG-cGR-IP plasmid (RIKEN, #RDB10440) was subcloned to constitutive PiggyBac plasmid to generate GRBD-FLAG-METTL3WT or GRBD-FLAG-METTL3APPA fusion protein (Murakami et al., 2016).”
From METTL3 uncouples chromatin accessibility from transcription during retinal development (2025) · cites this paper as Murakami et al., 2016
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Cites
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890
Multiplex Genome Engineering Using CRISPR/Cas Systems
Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P. D., Wu, X., Jiang, W., Marraffini, L. A., et al. (2013) · Science · doi:10.1126/science.1231143 · Cited by 15,339
Histone H3K27ac separates active from poised enhancers and predicts developmental state
Creyghton, M. P., Cheng, A. W., Welstead, G. G., Kooistra, T., Carey, B. W., Steine, E. J., Hanna, J., Lodato, M. A., Frampton, G. M., Sharp, P. A., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016071107 · Cited by 4,302
The ground state of embryonic stem cell self-renewal
Ying, Q.-L., Wray, J., Nichols, J., Batlle-Morera, L., Doble, B., Woodgett, J., Cohen, P., & Smith, A. (2008) · Nature · doi:10.1038/nature06968 · Cited by 3,442
Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling
Huang, S.-M. A., Mishina, Y., Liu, S.-M., Cheung, A. K., Stegmeier, F., Michaud, G., Charlat, O., Wiellette, E., Zhang, Y., Wiessner, S., et al. (2009) · Nature · doi:10.1038/nature08356 · Cited by 2,077
Nanog safeguards pluripotency and mediates germline development
Chambers, I., Silva, J. C. R., Colby, D., Nichols, J., Nijmeijer, B., Robertson, M., Vrána, J., Jones, K., Grotewold, L., & Smith, A. G. (2007) · Nature · doi:10.1038/nature06403 · Cited by 1,635
Reconstitution of the Mouse Germ Cell Specification Pathway in Culture by Pluripotent Stem Cells
Hayashi, K., Ohta, H., Kurimoto, K., Aramaki, S., & Saitou, M. (2011) · Cell · doi:10.1016/j.cell.2011.06.052 · Cited by 1,413
Bmp4 is required for the generation of primordial germ cells in the mouse embryo.Preprint
Lawson, K. A., Dunn, N. R., Roelen, B., Zeinstra, L., Davis, A. M., Wright, C., Korving, J., & Hogan, B. (1999) · Genes & Development · doi:10.1101/gad.13.4.424 · Cited by 1,373
Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells
Masui, S., Nakatake, Y., Toyooka, Y., Shimosato, D., Yagi, R., Takahashi, K., Okochi, H., Okuda, A., Matoba, R., Sharov, A., et al. (2007) · Nature Cell Biology · doi:10.1038/ncb1589 · Cited by 1,333
Blimp1 is a critical determinant of the germ cell lineage in mice
Ohinata, Y., Payer, B., O'Carroll, D., Ancelin, K., Ono, Y., Sano, M., Barton, S., Obukhanych, T. V., Nussenzweig, M., Tarakhovsky, A., et al. (2005) · Nature · doi:10.1038/nature03813 · Cited by 1,079
Research works printed but not linked: 1
- Yeom, Y. I. et al. Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Development 122, 881–894 (1996) · DOI
Cited by
Sorted by citations
Items 101–166 of 166
Taheri, M., Saki, G., Nikbakht, R., & Eftekhari, A. (2020) · Cell Biology International · doi:10.1002/cbin.11475 · Cited by 8
“It is also expressed in unipotent PGCs in mammals, where its exact role is still unknown (Murakami et al., 2016).”
BackgroundBhartiya, D., Anand, S., & Patel, H. (2016) · Stem Cell Investigation · doi:10.21037/sci.2016.09.06 · Cited by 8
“We were intrigued to observe that PGCs were recently defined ‘unipotent’ in Nature journal (27) on the assumption that they only give rise to gametes in the body compared to totipotent or pluripotent early stage embryo/ICM which can form the whole body.”
BackgroundMouse Primordial Germ Cell-Like Cells Lack piRNAs
Ramakrishna, N. B., Battistoni, G., Surani, M., Hannon, G., & Miska, E. (2022) · Developmental Cell · doi:10.1016/j.devcel.2022.11.004 · Cited by 7
“…orchestrating this process, as well as histone modification and DNA methylation dynamics in the differentiation of mESCs through to mPGCLCs (Hackett et al., 2018; Kurimoto et al., 2015; Murakami et al., 2016; Nakaki et al., 2013; Saitou and Hayashi, 2021; Tischler et al., 2019; Zhang et al., 2018).”
The Divergent Pluripotent States in Mouse and Human Cells
Wang, X., & Wu, Q. (2022) · Genes · doi:10.3390/genes13081459 · Cited by 7
Artificial Oocyte: Development and Potential Application
Oqani, R. K., So, S., Lee, Y., Ko, J., & Kang, E. (2022) · Cells · doi:10.3390/cells11071135 · Cited by 7
Yang, H., Deng, M.-T., Lv, W.-L., Wei, Z.-Y., Cai, Y., Cheng, P., Wang, F., & Zhang, Y.-L. (2022) · Biology · doi:10.3390/biology11020289 · Cited by 7
“It was also indicated that Nanog alone promoted the differentiation process of PGCLCs, which showed germline-specific epigenetic modification [25].”
BackgroundLee, B., Rengaraj, D., Choi, H.-J., & Han, J. Y. (2020) · The FASEB Journal · doi:10.1096/fj.201901294r · Cited by 7
Fard, S. B., Mazaheri, Z., Ghorbanmehr, N., Movahedin, M., Behzadifard, M., & Gholampour, M. (2019) · International journal of molecular and cellular medicine · doi:10.22088/ijmcm.bums.8.1.14 · Cited by 7
“Nanog is required for maintaining the cells pluripotency (25).”
BackgroundThe pluripotency factor NANOG controls primitive hematopoiesis and directly regulates Tal1
de Aja, J. S., Menchero, S., Rollan, I., Barral, A., Tiana, M., Jawaid, W., Cossío, I., Alvarez, A., Carreño-Tarragona, G., Badía-Careaga, C., et al. (2019) · EMBO Journal · doi:10.15252/embj.201899122 · Cited by 7
“Differentiation toward EpiLCs was induced by plating 5 × 10 4 ES cells on a well of a 24-well plate coated with human plasma fibronectin (10 l g/ml, Sigma) in N2B27 medium supplemented with 20 ng/ml Activin A (Prepro-tech),12 ng/ml bFGF (Preprotech), and 1% Knock out serum replacement (Thermo Fisher) for 3 days.”
InfluentialChicken NANOG self‐associates via a novel folding‐upon‐binding mechanism
Choi, H. J., Kim, I., Lee, H. J., Park, Y. H., Suh, J., & Han, J. Y. (2018) · The FASEB Journal · doi:10.1096/fj.201700924rr · Cited by 7
Differential repression of Otx2 underlies the capacity of NANOG and ESRRB to induce germline entry
Vojtek, M., Zhang, J., Sun, J., Zhang, M., & Chambers, I. (2021) · bioRxiv · doi:10.1016/j.stemcr.2021.11.013 · Cited by 6
ALKBH5 regulates somatic cell reprogramming in a phase-specific manner
Khodeer, S., Klungland, A., & Dahl, J. (2021) · bioRxiv · doi:10.1101/2021.05.10.443389 · Cited by 6
“Based on that, we decided to use transgenic MEFs (OG2) with ΔPE-Oct4-GFP reporter as a definitive and the most stringent marker for estimation of the reprograming efficiency, naïve pluripotency and primordial germ cell (PGC) specification [2-4].”
MethodArtificially produced gametes in mice, humans and other species.
Hayashi, K., Galli, C., Diecke, S., & Hildebrandt, T. (2021) · Reproduction, Fertility and Development · doi:10.1071/rd20265 · Cited by 6
“Indeed, details of the transcriptional network and epigenetic landscape were comprehensively revealed using the culture system (Aramaki et al. 2013; Nakaki et al. 2013; Kurimoto et al. 2015;Murakami et al. 2016; Shirane et al. 2016).”
BackgroundWen, L., Jiang, C., Wan, T.-J., Wang, D., Yan, D., Li, G., Su, Y., Liu, X.-Y., Rong, L., Ye, H., et al. (2020) · Evidence-Based Complementary and Alternative Medicine · doi:10.1155/2020/7234893 · Cited by 6
“Firstly, the hierarchical clustering analysis [32] of SDE-miRNAs is shown in Figure 1.”
MethodWang, H. V., & Chekanova, J. A. (2019) · RNA · doi:10.1261/rna.071209.119 · Cited by 6
“The homeobox TF family includes a wide range of well-conserved eukaryotic TFs; specifically, one specific homeobox TF, NANOG, was shown to bind and activate primed enhancers in mice to promote the pluripotent state in mouse embryonic stem cells (Murakami et al. 2016).”
BackgroundSybirna, A., Tang, W. W. C., Dietmann, S., Gruhn, W. H., & Surani, M. (2019) · bioRxiv · doi:10.1101/563072 · Cited by 6
Self-citationResidual pluripotency is required for inductive germ cell segregation
Aramaki, S., Kagiwada, S., Wu, G.-M., Obridge, D., Adachi, K., Kutejova, E., Lickert, H., Hübner, K., & Schöler, H. (2021) · EMBO Reports · doi:10.15252/embr.202152553 · Cited by 5
“The primed pluripotency-specific regulatory mechanism for germ cell fate is also supported by the recent study showing the primed specific NANOG-binding to establish the putative enhancers to induce germ cell fate (Murakami et al , 2016).”
Loss of Resf1 reduces the efficiency of embryonic stem cell self-renewal and germline entry
Vojtek, M., & Chambers, I. (2021) · Life Science Alliance · doi:10.26508/lsa.202101190 · Cited by 5
“Nanog overexpression can also induce speci fi cation of germline competent epiblast-like cells (EpiLCs) into PGC-like cells (PGCLCs) in vitro without the otherwise requisite cytokines (Murakami et al, 2016).”
Ando, Y., Okeyo, K., & Adachi, T. (2019) · APL Bioengineering · doi:10.1063/1.5072761 · Cited by 5
Nanog suppresses the expression of vasa by directly regulating nlk1 in the early zebrafish embryo.
Liu, Y., Xue, W.-W., Zhu, L., Ye, D., Zhu, X., Wang, H.-N., Sun, Y.-H., & Deng, F.-J. (2017) · Biochimie · doi:10.1016/j.biochi.2017.07.014 · Cited by 5
“Nanog alone can induce PGC-like cells from primed epiblasts in vitro, independently of BMP4 (Murakami et al., 2016).”
BackgroundPenfold, C. A., Sybirna, A., Reid, J. E., Venzor, A. C., Drousioti, E., Huang, Y., Grant, M., Wernisch, L., Ghahramani, Z., & Surani, M. (2017) · bioRxiv · doi:10.1101/167684 · Cited by 5
“In mouse in vitro models NANOG is sufficient to directly induce PGC-like cell fate by binding and activating enhancers of Prdm1 and Prdm14 (Murakami et al. 2016), although loss of function studies have yielded equivocal results as to its requirement for mouse PGC fate (Chambers et al. 2007; Yamaguchi et al. 2009; Cart…”
ResultInfluentialYang, N., Seol, D.-W., Jo, J., Jang, H., Yoon, S.-Y., Lee, W. S., & Lee, D. R. (2016) · Reproductive Sciences · doi:10.1177/1933719116643594 · Cited by 5
“Among them, cellpenetrating peptides (CPPs, also known as protein transduction domains or membrane transduction peptides) are useful tools that easily translocate across cellular membranes23 and even into the nucleus.24,25 We previously showed that a CPPconjugated ESRRB recombinant protein (CPP-ESRRB) could significan…”
BackgroundInduction of germline-like cells (PGCLCs)
Tkemaladze, J. (2025) · Longevity Horizon · doi:10.65649/faca1a76 · Cited by 4
“Remarkably, forced coordinated expression of these transcription factors has proven sufficient to directly reprogram somatic cell lineages into PGCLCs, bypassing the pluripotent intermediate state entirely (Murakami et al., 2016).”
Budreika, A., Phoenix, J. T., Kostlan, R. J., Deegan, C. D., Ferrari, M. G., Young, K., Fanning, S., & Kregel, S. (2025) · Cancers · doi:10.3390/cancers17020306 · Cited by 4
Integrated analysis of the role of PR/SET domain 14 in gastric cancer
Li, X., Wang, C., Wang, Y., Chen, X.-B., Li, Z., Wang, J., & Liu, Y.-J. (2024) · BMC Cancer · doi:10.1186/s12885-024-12424-1 · Cited by 4
Ruthig, V. A., Hatkevich, T., Hardy, J., Friedersdorf, M. B., Mayère, C., Nef, S., Keene, J. D., & Capel, B. (2023) · PLoS Genetics · doi:10.1371/journal.pgen.1010656 · Cited by 8
“Are DND1 levels in MGCs regulated by surrounding somatic cells or are levels of DND1 intrinsically regulated? TFAP2c (which is highly upregulated in DND1-GFP-hi cells) was reported to regulate DND1 levels in induced primordial germ cells (PGCs) [69].”
BackgroundDucos, B., Bensimon, D., & Scerbo, P. (2022) · Cells · doi:10.3390/cells11152299 · Cited by 10
Lu, Y., Wang, H., Cao, H., Chen, X., Li, D.-F., Yu, D.-B., & Yu, M.-L. (2022) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/s11626-022-00659-w · Cited by 4
“The previous findings indicated that NANOG is important in mouse PGC development (Murakami et al. 2016).”
BackgroundThe BLIMP1—EZH2 nexus in a non-Hodgkin lymphoma
Anderson, K. J., Ósvaldsdóttir, Á. B., Atzinger, B., Traustadóttir, G. Á., Jensen, K. N., Lárusdóttir, A. E., Bergþorsson, J. Þ., Harðardóttir, I., & Magnúsdóttir, E. (2020) · Oncogene · doi:10.1038/s41388-020-1347-8 · Cited by 5
“The miRNA sequences (Table S20) were cloned into the tetracycline-inducible pPB-hCMV*1-miR plasmid [76, 77].”
MethodTerada, M., Kawamata, M., Kimura, R., Sekiya, S., Nagamatsu, G., Hayashi, K., Horisawa, K., & Suzuki, A. (2019) · Genesis · doi:10.1002/dvg.23334 · Cited by 3
“Forced expression of Nanog endows ESCs and epiblast-like cells with cytokine-independent self- renewal capacity (Chambers et al., 2003) and germline competency (Murakami et al., 2016), respectively.”
BackgroundModern Technologies Deriving Human Primordial Germ Cells in vitro
Abdyyev, V., Dashinimayev, E. B., Neklyudova, I., Vorotelyak, E., & Vasiliev, A. (2019) · Biochemistry (Moscow) · doi:10.1134/s0006297919030040 · Cited by 3
Reprogramming p53-Deficient Germline Stem Cells Into Pluripotent State by Nanog
Feng, Y., Ning, Y., Lin, X., Zhang, D., Liao, S., Zheng, C., Chen, J., Wang, Y., Ma, L., Xie, D., et al. (2018) · Stem Cells and Development · doi:10.1089/scd.2018.0047 · Cited by 3
“Recently, Murakami et al. [34] reported that Nanog alone induced primed epiblasts into PGCLCs, which were further converted back to EG-like cells in vitro.”
A primordial germ cell-like-cell platform enables CRISPRi screen for epigenetic fertility modifiers
Li, L., Gao, J., Yi, D., Sheft, A. P., Schimenti, J., & Ding, X.-B. (2025) · EMBO Reports · doi:10.1038/s44319-025-00633-z · Cited by 2
“Studies using Ck-, 3TF-and Nanog-induction systems have demonstrated that a formative state is essential for robust induction of a PGC-like state (Nakaki et al, 2013; Hayashi et al, 2011; Murakami et al, 2016).”
InfluentialLi, L., Gao, J., Yi, D., Sheft, A. P., Schimenti, J., & Ding, X.-B. (2024) · bioRxiv · doi:10.1101/2024.02.15.580543 · Cited by 2
“The overexpression of Nanog can promote efficient PGCLC differentiation by binding endogenous enhancers of Prdm1 and Prdm14 , even without BMP4 and associated cytokines (12).”
InfluentialSato, J., Satoh, Y., Yamamoto, T., Watanabe, T., Matsubara, S., Satake, H., & Kimura, A. P. (2023) · Gene · doi:10.1016/j.gene.2023.147907 · Cited by 2
Li, X., Chen, P., Ji, J.-X., Duan, Q., Cao, J., Huang, R., & Ye, S.-D. (2023) · Cell & Bioscience · doi:10.1186/s13578-023-01096-2 · Cited by 2
“Many important candidate genes, such as Nanog [8], Esrrb [9], Otx2 [10], SETDB1 [11], Sox17 [12] and Tfcp2l1 [13], have been identified by using this system.”
BackgroundBai, X.-M., Li, J.-N., Zhang, Z., Qu, X.-M., Tao, W., Zhou, L.-Y., Wang, D.-S., & Wei, J. (2022) · Comparative Biochemistry and Physiology Part B Comparative Biochemistry · doi:10.1016/j.cbpb.2022.110812 · Cited by 2
Juliá, M. G., & Medrano, J. V. (2020) · EMJ Reproductive Health · doi:10.33590/emjreprohealth/20-00096 · Cited by 2
Voronina, A. S., & Pshennikova, E. S. (2020) · Molecular Biology · doi:10.1134/s002689332002017x · Cited by 2
METTL3 uncouples chromatin accessibility from transcription during retinal development
Xu, J., Huang, Y., Han, Z., Li, Q., Liu, J., & Rao, R. C. (2025) · Stem Cell Reports · doi:10.1016/j.stemcr.2025.102690 · Cited by 1
Zhi, M., Yao, Y., Liang, C., Wang, Y., Wang, S., Pang, J. K. S., Soh, B.-S., & Han, J. (2026) · Engineering · doi:10.1016/j.eng.2026.07.032 · Cited by 1
NELFA supports naïve pluripotency and drives 8C-like state in human embryonic stem cells
Su, X., Yang, F., Neupane, J., Lu, Z., Wu, H., Gu, M., Zhang, Y., Bao, S.-Q., Li, X.-H., Surani, M., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-72714-z · Cited by 1
WDR5 remodels NANOG condensates to drive transcriptional programs and sustain stem cell identity
Wang, D., Shi, X., Xie, J., Zhao, L., Wu, B., Dong, Q., Huang, Y.-G., Suo, J., Wang, X., He, B.-X., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-68623-w · Cited by 1
“…increased expression of somatic lineage markers relative to WT cells, whereas the expression of primordial germ cell (PGC) markers was reduced, consistent with previous fi ndings that NANOG is required not only to maintain pluripotency but also to promote PGC speci fi cation 44 (Supplementary Fig.”
OTX2 controls chromatin accessibility to direct somatic versus germline differentiation
Barbieri, E., & Chambers, I. (2025) · bioRxiv · doi:10.1038/s44319-025-00622-2 · Cited by 1
“In addition, Nanog overexpression is suf fi cient to induce PGCLC formation from EpiLCs (Murakami et al, 2016), with induction of NANOG repressing Otx2 expression in the absence of cytokines (Vojtek et al, 2022).”
Li, L., Ding, X.-B., Sheft, A. P., & Schimenti, J. (2024) · bioRxiv · doi:10.1101/2024.02.26.582097 · Cited by 1
The pluripotency factor Tex10 finetunes Wnt signaling for PGC and male germline developmentPreprint
Li, D., Yang, J.-H., Ma, F.-L., Malik, V., Zang, R., Shi, X., Huang, X., Zhou, H.-W., & Wang, J.-L. (2023) · bioRxiv · doi:10.1101/2023.02.23.529824 · Cited by 1
“Interestingly, many pluripotency factors play an important role in the specification of PGCs, exemplified by the requirement of the key pluripotency factors Nanog (Murakami et al. 2016), Oct4 (Kehler et al. 2004), and Sox2 (Campolo et al. 2013) for PGC specification and development.”
BackgroundInfluentialThe vulnerable primed cancer stem cells in disguise: demystifying the role of Maspin
Sheng, S., Bernardo, M., Dzinic, S. H., Chen, K., & Sakr, W. (2022) · Cancer metastasis reviews · doi:10.1007/s10555-022-10070-2 · Cited by 1
Gallic acid ameliorates thymic involution via activating Sox2 and Nanog
Guo, L., Cao, J.-H., Cheng, D., Dong, H., You, L., Sun, Y., Ding, Y., & Chai, Y.-R. (2022) · Scandinavian Journal of Immunology · doi:10.1111/sji.13202 · Cited by 1
Wang, P.-B., Hu, H.-H., Li, X., Zhang, R., Cheng, H.-B., Qin, H., Ji, G.-J., Feng, H.-G., Liu, Y.-L., & Lin, J.-T. (2021) · Ginekologia Polska · doi:10.5603/gp.a2021.0144 · Cited by 1
Generation of Miniaturized Ovaries by In Vitro Culture from Mouse Gonads
Jang, S. W., & Choi, H. W. (2021) · Development & Reproduction · doi:10.12717/dr.2020.25.3.173 · Cited by 1
Investigation into germ cell fate determination of rat embryonic stem cells
Taylor, R. (2020) · doi:10.7488/era/281 · Cited by 1
“NANOG is reported to bind to enhancer regions of Blimp1 and Prdm14 in differentiating cells, activing their expression independently of BMP4 and WNT signalling (Murakami et al. 2016).”
BackgroundResultInfluentialVoronina, A. S., & Pshennikova, E. S. (2020) · Молекулярная биология · doi:10.31857/s0026898420020172 · Cited by 1
The BLIMP1 – EZH2 nexus in a non-Hodgkin lymphoma
Anderson, K., Ósvaldsdóttir, Á. B., Atzinger, B., Traustadottir, G. A., Jensen, K. N., Lárusdóttir, A. E., Bergþorsson, J. Þ., Harðardóttir, I., & Magnúsdóttir, E. (2019) · bioRxiv · doi:10.1101/606749 · Cited by 1
Reconstitution of Germ Cell Development In Vitro
Yokobayashi, S., & Saitou, M. (2018) · Springer eBooks · doi:10.1007/978-981-10-7941-2_1 · Cited by 1
He, P.-C., Zhong, L., Chen, T.-Z., Yan, Y.-X., Chen, X.-Z., Li, R.-B., Wang, Y.-J., Teng, Y.-D., Zhi, M.-L., Wang, M., et al. (2026) · Advancement of science · doi:10.1002/advs.78213
“In mEpiLCs, PRDM14 alone initiates the network, while co-activation with BLIMP1 and TFAP2C enables cytokine-free induction [ 13, 66 ].”
Human-Mouse Chimerism for Organogenesis Without Neural or Germline Contributions
Ye, S., Kadier, K., Yi, Y., Qin, G.-H., Huang, B.-R., Fu, S.-Y., Alev, C., & Xu, R.-H. (2026) · International Journal on Biological Sciences · doi:10.7150/ijbs.119609
“KO of BLIMP1 in hESCs has been described to lead to failure of hPGCLC specification and increase the expression of somatic markers during the PGC differentiation [17].”
TET knockout cells transit between pluripotent states and exhibit precocious germline entry
Gutkowski, J., Barbieri, E., Brito, S. G., Thomson, E., Tatar, T., Colby, D., Zhang, M., & Chambers, I. (2025) · The EMBO Journal · doi:10.1038/s44318-025-00597-9 · Cited by 4
“EpiLCs can also differentiate to PGCLCs without cytokines upon induced expression of NANOG (Murakami et al, 2016; Zhang et al, 2018b).”
InfluentialSelective GSK3α Inhibition Promotes Self-Renewal Across Different Stem Cell StatesPreprint
Wang, D., Wang, X.-K., Wang, S.-L., Shi, K.-X., Malki, S., Chan, Y.-P., Feng, J., Tang, J., Chen, X., Mckim, D., et al. (2025) · bioRxiv · doi:10.1101/2025.05.16.653860
HELQ deficiency impairs the induction of primordial germ cell‐like cells
Wan, C., Huang, Y., Xue, X., Chang, G., Wang, M., Zhao, X., Luo, F., & Tang, Z. (2024) · FEBS Open Bio · doi:10.1002/2211-5463.13810
“…human PSCs, have provided a platform and robust experimental materials for studying the physiology and pathology of germ cell development [12,22 – 24,35 Previous studies have demonstrated that disruption of the DNA damage repair mechanisms promote genomic instability, and lead to increased risks…”
BackgroundMethodSingle Cell Sequencing Reveals Early PGC-like Intermediates During Mouse Primed to Naïve TransitionPreprint
Liu, J., Yu, S.-Y., Zhou, C.-H., He, J.-P., Huang, X.-N., Yao, Z., Zhu, H., Cai, B.-M., Xiao, L., Liu, H., et al. (2021) · Research Square · doi:10.21203/rs.3.rs-151340/v1
Agrawal, P., Blinka, S., Pulakanti, K., Reimer, M. H., & Rao, S. (2020) · bioRxiv · doi:10.1101/2020.05.27.118612
“Importantly, 280 this DNA element may function as an alternative promoter in other context, such as alternative 281 pluripotent states or primordial germ cells, both of which express Nanog [35].”
BackgroundZuo, Q.-S., Zhang, Y.-N., Chen, G.-H., & Li, B.-C. (2020) · doi:10.21203/rs.3.rs-26853/v1
Nanog regulates Pou3f1 expression and represses anterior fate at the exit from pluripotency
Barral, A., Rollan, I., Sánchez-Iranzo, H., Jawaid, W., Badía-Careaga, C., Menchero, S., Gomez-Rodriguez, M., Torroja, C., Sánchez-Cabo, F., Göttgens, B., et al. (2019) · doi:10.1101/598656
“The EpiLC (primed) state represents a pregastrulating epiblast in vitro (Murakami et al., 2016; Nichols and Smith, 2009b; Tesar et al., 2007).”
BackgroundMethodInfluentialUtilising embryonic and extra-embryonic stem cells to model early mammalian embryogenesis in vitro
Harrison, S. (2018) · doi:10.17863/cam.22635
“This transcriptional programme is then followed by the re-expression of pluripotency factors associated with the pre-implantation EPI, such as Nanog and Sox2 (Günesdogan, Magnúsdóttir and Surani, 2014; Murakami et al., 2016).”
BackgroundRespuela, P., & Rada-Iglesias, Á. (2016) · Current Stem Cell Reports · doi:10.1007/s40778-016-0050-8
Male germ cell derivation from PSCs
Liang, D.-L., & Wang, Y. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-822230-0.00007-7
Metadata
- Authors
- Murakami, K., Günesdogan, U., Zylicz, J. J., Tang, W. W. C., Sengupta, R., Kobayashi, T., Kim, S., Butler, R., Dietmann, S., & Azim Surani, M.
- Affiliations
- Hokkaido University (JP)
- Wellcome/MRC Cambridge Stem Cell Institute (GB)
- University of Cambridge (GB)
- ORCID
- Venue
- Nature
- Published
- 2016-01
- Volume
- 529
- Issue
- 7586
- Pages
- 403-407
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4724940
- OpenAlex
- W2238949050
- Cited by
- 180
- References
- 40
- Citations by year
- 2026: 4 · 2025: 11 · 2024: 12 · 2023: 15 · 2022: 19 · 2021: 28 · 2020: 15 · 2019: 26 · 2018: 22 · 2017: 17 · 2016: 11
- FWCI
- 13.17
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Apollo (University of Cambridge) (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Funders
- Wellcome Trust (RG44593, 096738, 092096)
- Cancer Research UK (C6946 /A14492)
- Medical Research Council (MC_PC_12009)
- Japan Society for the Promotion of Science (15K18539)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- Nanog, epiblast-like cells, enhancer activation, chromatin accessibility, Blimp-1, PRDM14, TFAP2C, SOX2, pluripotency, naïve-to-primed transition, transcription factor binding sites
- MeSH terms
- Mouse Embryonic Stem Cells, Nanog Homeobox Protein, Positive Regulatory Domain I-Binding Factor 1, Animals, Cell Differentiation, Chromatin, DNA-Binding Proteins, Enhancer Elements, Genetic, Female, Germ Cells, Germ Layers, Male, Protein Binding, Transcription Factors, Fibroblast Growth Factor 2, RNA-Binding Proteins, Genome, Homeodomain Proteins, Gene Expression Regulation, Developmental, Activins, Pluripotent Stem Cells, Epigenesis, Genetic, Transcription Factor AP-2, Mice, Bone Morphogenetic Protein 4, SOXB1 Transcription Factors
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