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).
“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
The Methods section on the PiggyBac Tet-on system describes doxycycline-inducible constructs for genes including Nanog, not the claimed dexamethasone-inducible METTL3 constructs. Searches for GRBD, pPyCAG-cGR-IP, METTL3 and APPA found no passage describing the specified insert, subcloning step or fusion proteins in our copy. (LLM, conf=0.75)
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“Recently, PGCs were defined as unipotent stem cells in Nature journal (Murakami et al., 2016) on the assumption that they only give rise to gametes in the body.”
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Enhancer-associated H3K4 methylation safeguards in vitro germline competence
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Choi, K.-J., Quan, M., Qi, C.-Y., Lee, J.-H., Tsoi, P. S., Zahabiyon, M., Bajić, A., Hu, L.-Y., Prasad, B. V. V., Liao, S.-C., et al. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-00896-x · Cited by 37 · see citing works
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Kimura, A. P., Yoneda, R., Kurihara, M., Mayama, S., & Matsubara, S. (2017) · Endocrinology · doi:10.1210/en.2017-00619 · Cited by 43 · see citing works
Modeling human infertility with pluripotent stem cells
Chen, D., Gell, J., Tao, Y., Sosa, E., & Clark, A. (2017) · Stem Cell Research · doi:10.1016/j.scr.2017.04.005 · Cited by 34
“The model proposed from this work follows that NANOG functions upstream of both PRDM14 and PRDM1 by binding to their enhancers in the germline-competent in vitro epiblast-like cells to promote PGC fate (Murakami et al., 2013).”
Induced formation of primordial germ cells from zebrafish blastomeres by germplasm factors
Wang, X.-S., Zhu, J.-W., Wang, H.-P., Deng, W.-Q., Jiao, S.-B., Wang, Y.-Q., He, M.-D., Zhang, F.-H., Liu, T., Hao, Y.-L., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-43587-3 · Cited by 33 · see citing works
Gastruloid Development Competence Discriminates Different States of Pluripotency
Cermola, F., d'Aniello, C., Taté, R., Cesare, D. D., Martinez-Arias, A., Minchiotti, G., & Patriarca, E. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.12.013 · Cited by 33 · see citing works
Sybirna, A., Wong, F. C. K., & Surani, M. (2019) · Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2019.04.004 · Cited by 33 · see citing works
Mammalian Germ Cell Development: From Mechanism to In Vitro Reconstitution
Saitou, M. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.01.008 · Cited by 32 · see citing works
Synthetic organizer cells guide development via spatial and biochemical instructions
Yamada, T., Trentesaux, C., Brunger, J. M., Xiao, Y., Stevens, A. J., Martyn, I., Kašpárek, P., Shroff, N. P., Aguilar, A., Bruneau, B. G., et al. (2024) · Cell · doi:10.1016/j.cell.2024.11.017 · Cited by 38 · see citing works
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“This plasmid was digested with SpeI and XhoI, and the Tesra fragment was inserted into a pPBhCMV∗1-cHA-pA vector which was cut by SpeI and XhoI [51].”
MethodInfluentialIchikawa, K., & Horiuchi, H. (2023) · Genes · doi:10.3390/genes14030612 · Cited by 28
“Additionally, NANOG plays a crucial role in the specification of mammalian PGCs via their epigenetic modification [77,78].”
BackgroundAn, H.-W., Seok, S. H., Kwon, J.-W., Choudhury, A., Oh, J.-S., Voon, D., Kim, D.-Y., & Park, J. W. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111878 · Cited by 27 · see citing works
DNA methylation and the core pluripotency network
Shanak, S., & Helms, V. (2020) · Developmental Biology · doi:10.1016/j.ydbio.2020.06.001 · Cited by 28 · see citing works
STRA8–RB interaction is required for timely entry of meiosis in mouse female germ cells
Shimada, R., Kato, Y., Takeda, N., Fujimura, S., Yasunaga, K.-I., Usuki, S., Niwa, H., Araki, K., & Ishiguro, K.-I. (2023) · Nature Communications · doi:10.1038/s41467-023-42259-6 · Cited by 23 · see citing works
Vijayakumar, S., Sala, R., Kang, G., Chen, A., Pablo, M. A., Adebayo, A., Cipriano, A., Fowler, J. L., Gomes, D., Ang, L., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-41302-w · Cited by 23 · see citing works
“Our demonstration of a functional requirement of NANOG throughout the differentiation process altogether is consistent with a critical role for NANOG in mouse PGC speci fi cation in vivo and in vitro 53,54 .”
ResultEpigenome regulation during germ cell specification and development from pluripotent stem cells.
Kurimoto, K., & Saitou, M. (2018) · Current Opinion in Genetics and Development · doi:10.1016/j.gde.2018.06.004 · Cited by 23
What Can Stem Cell Models Tell Us About Human Germ Cell Biology?
Irie, N., Sybirna, A., & Surani, M. A. (2018) · Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2018.02.010 · Cited by 22 · see citing works
Protein phosphatase 1 acts as a RIF1 effector to suppress DSB resection prior to Shieldin action
Isobe, S.-Y., Hiraga, S., Nagao, K., Sasanuma, H., Donaldson, A. D., & Obuse, C. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109383 · Cited by 28 · see citing works
Zuo, Q.-S., Jin, K., Wang, M., Zhang, Y.-N., Chen, G.-H., & Li, B.-C. (2020) · Journal of Cell Science · doi:10.1242/jcs.249375 · Cited by 21 · see citing works
PRDM14 and BLIMP1 control the development of chicken primordial germ cells.
Okuzaki, Y., Kaneoka, H., Suzuki, T., Hagihara, Y., Nakayama, Y., Murakami, S., Murase, Y., Kuroiwa, A., Iijima, S., & Nishijima, K. (2019) · Developmental Biology · doi:10.1016/j.ydbio.2019.06.018 · Cited by 21
Committing the primordial germ cell: An updated molecular perspective
Tan, H., & Tee, W.-W. (2018) · Wiley Interdisciplinary Reviews: Systems Biology and Medicine · doi:10.1002/wsbm.1436 · Cited by 21
“…the overexpression of Nanog in mEpiLCs also led to mPGCLC differentiation, and Nanog was found to bind and activate Prdm1 and Prdm14 expression (Murakami et al., 2016); conversely, differentiation of Nanog-null cells revealed a reduction in mPGCLC yield which could be rescued by ectopic Nanog…”
BackgroundInfluentialLincU Preserves Naïve Pluripotency by Restricting ERK Activity in Embryonic Stem Cells
Jiapaer, Z., Li, G.-P., Ye, D., Bai, M.-L., Li, J., Guo, X.-D., Du, Y.-H., Su, D., Jia, W.-W., Chen, W., et al. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.06.010 · Cited by 21 · see citing works
“, 2003) we found that Nanog can bind the promoter region of LincU, which is located on chromosome 16 (9,133,405–9,138,147) (mm9) (Murakami et al., 2016).”
BackgroundBMP4 drives primed to naïve transition through PGC-like state
Yu, S.-Y., Zhou, C.-H., He, J.-P., Yao, Z., Huang, X.-N., Rong, B.-W., Zhu, H., Wang, S.-J., Chen, S.-Y., Wang, X., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-30325-4 · Cited by 20 · see citing works
Wang, X., Veerapandian, V., Yang, X., Song, K., Xu, X., Cui, M., Yuan, W.-Y., Huang, Y., Xia, X., Yao, Z., et al. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.03.032 · Cited by 20 · see citing works
“Moreover, SOX15 peaks were detected at the proximal regulatory elements of several pluripotency-related genes, such as PRDM14, NANOG, ETV4, and ETV5 (Figures 6G and S7D) (Kalkan et al., 2019; Murakami et al., 2016; Sybirna et al., 2020).”
BackgroundFunctional characterization of NANOG in goat pre-implantation embryonic development.
Habibi, R., Hosseini, S., Zadegan, F. G., Hajian, M., Ostadhosseini, S., Vash, N. T., Naddafpour, A., & Esfahani, M. N. N. (2018) · Theriogenology · doi:10.1016/j.theriogenology.2018.07.023 · Cited by 20 · see citing works
Transcriptional control of human gametogenesis
Fang, F., Iaquinta, P. J., Xia, N., Liu, L., Diao, L., & Pera, R. A. R. (2022) · Human Reproduction Update · doi:10.1093/humupd/dmac002 · Cited by 22 · see citing works
“Pluripotency genes OCT4 and NANOG are re-expressed in both mPGCs (Murakami et al., 2016) and hPGCs (Guo et al., 2015; Tang et al., 2015), and SOX2 is absent in hPGCs (Lin et al., 2014) although .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. ..it is required for mouse PGC survival…”
Deb, S., Felix, D. A., Koch, P., Deb, M. K., Szafranski, K., Buder, K., Sannai, M., Groth, M., Kirkpatrick, J. M., Pietsch, S., et al. (2020) · EMBO Reports · doi:10.15252/embr.201949328 · Cited by 19 · see citing works
“Immunofluorescence staining was performed as previously described (Murakami et al , 2016).”
Jung, H., Hwang, Y., Park, Y. H., Ho, Y.-O.-C., Rengaraj, D., & Han, J. (2018) · Stem Cells and Development · doi:10.1089/scd.2018.0059 · Cited by 19
“The recent report showed that NANOG solely activated enhancers upstream of germ cell specifiers to generate PGC-like cells from epiblast-like cells, but not in ESCs in mouse [22], indicating that its function differs according to cell type.”
Dynamics of male canine germ cell development
de Souza, A. F., Pieri, N. C. G., Roballo, K., Bressan, F., Casals, J. B., Ambrósio, C., Perecin, F., & Martins, D. S. (2018) · PLoS ONE · doi:10.1371/journal.pone.0193026 · Cited by 19
Shirazi, R., Zarnani, A., Soleimani, M., Nayernia, K., & Kashani, I. R. (2017) · Microscopy research and technique (Print) · doi:10.1002/jemt.22812 · Cited by 19
Molecular versatility during pluripotency progression
Furlan, G., Huyghe, A., Combémorel, N., & Lavial, F. (2023) · Nature Communications · doi:10.1038/s41467-022-35775-4 · Cited by 18 · see citing works
Zhou, J.-L., He, H., Zhang, J.-J., Liu, X., Yao, W., Li, C., Xu, T., Yin, S.-Y., Wu, D., Dou, C.-L., et al. (2022) · Autophagy · doi:10.1080/15548627.2022.2055285 · Cited by 18 · see citing works
“Indeed, overexpression of NANOG in EpiLCs cannot maintain primed pluripotency, but promotes germline specification through binding active enhancers proximate to the Prdm14 and Prdm1 loci [57], suggesting the epigenetic resetting of NANOG binding profiles in EpiLCs was associated with germline specification.”
BackgroundEnhanced cultivation of chicken primordial germ cells
Dehdilani, N., Taemeh, S. Y., Rival-Gervier, S., Montillet, G., Kress, C., Jean, C., Goshayeshi, L., Dehghani, H., & Pain, B. (2023) · Scientific Reports · doi:10.1038/s41598-023-39536-1 · Cited by 17
Jung, K., Seo, M.-J., Kim, Y. M., Kim, J. L., & Han, J. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.791335 · Cited by 17
“Avian PGCs follow a preformation mode that is formed autonomously by maternally-inherited germ plasm, unlike mouse PGCs that are induced by signals received from surrounding tissues during development (Murakami et al., 2016; Jung et al., 2018).”
BackgroundZhang, M., Ji, J., Wang, X.-X., Zhang, X.-B., Zhang, Y., Li, Y.-T., Wang, X., Li, X.-F., Ban, Q., & Ye, S.-D. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.101217 · Cited by 17 · see citing works
“However, induced expression of estrogen related receptor beta (Esrrb) can restore PGCLC numbers in Nanog-null mouse ESCs (34).”
BackgroundInfluentialZhao, R.-F., Zuo, Q.-S., Yuan, X.-Y., Jin, K., Jin, J., Ding, Y., Zhang, C., Li, T.-T., Jiang, J.-Y., Li, J., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23242-5 · Cited by 17
RetractedAgrawal, P., Blinka, S., Pulakanti, K., Reimer, M. H., Stelloh, C. T., Meyer, A. E., & Rao, S. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra120.015152 · Cited by 17 · see citing works
“Of importance, this DNA element may function as an alternative promoter in other contexts, such as alternative pluripotent states or in primordial germ cells, where Nanog is also expressed (37).”
BackgroundChoi, H.-J., Jin, S., Rengaraj, D., Kim, J. H., Pain, B., & Han, J. (2020) · Journal of Animal Science and Biotechnology · doi:10.1186/s40104-021-00563-5 · Cited by 17
Evolving Role of RING1 and YY1 Binding Protein in the Regulation of Germ-Cell-Specific Transcription
Bajusz, I., Henry, S., Sutus, E., Kovács, G., & Pirity, M. (2019) · Genes · doi:10.3390/genes10110941 · Cited by 17 · see citing works
“Ectopic induction of Nanog expression alone can trigger the differentiation of PGCLCs from ES cells and the activation of Prdm1 and Prdm14 transcription independently of the activation of BMP4 and RA signaling [61].”
BackgroundHu, B., Wang, R.-J., Wu, D., Long, R., Ruan, J., Jin, L., Ma, D., Sun, C.-Y., & Liao, S.-J. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1177443 · Cited by 16 · see citing works
“NANOG is upstream of PRDM14 and BLIMP1, and NANOG binds to their enhancers (Murakami et al., 2016).”
BackgroundGermline specification from pluripotent stem cells
Yao, C., Yao, R., Luo, H., & Shuai, L. (2022) · Stem cell research & therapeutics · doi:10.1186/s13287-022-02750-1 · Cited by 16
“T cells directly activate Blimp1 and Prdm14.”
BackgroundInfluentialWang, X., Liao, T.-T., Wan, C., Yang, X.-Y., Zhao, J., Fu, R., Yao, Z., Huang, Y., Shi, Y., Chang, G., et al. (2019) · PeerJ · doi:10.7717/peerj.6143 · Cited by 16
Tischler, J., Swank, Z., Hsiung, H.-A., Vianello, S., Lutolf, M., & Maerkl, S. J. (2022) · Cell Reports Methods · doi:10.1016/j.crmeth.2022.100244 · Cited by 15 · see citing works
Shono, M., Kishimoto, K., Hikabe, O., Hayashi, M., Semi, K., Takashima, Y., Sasaki, E., Kato, K., & Hayashi, K. (2023) · Scientific Reports · doi:10.1038/s41598-023-29850-z · Cited by 14
Nanog regulates Pou3f1 expression at the exit from pluripotency during gastrulation
Barral, A., Rollan, I., Sánchez-Iranzo, H., Jawaid, W., Badía-Careaga, C., Menchero, S., Gómez, M., Torroja, C., Sánchez-Cabo, F., Göttgens, B., et al. (2019) · Biology Open · doi:10.1242/bio.046367 · Cited by 14 · see citing works
“Sequence (right) of the genomic regions (A, -9kb; B, -11.5kb; C, +9kb) from the Pou3f1 locus showing NANOG binding as determined by ChIP-seq by from Murakami et al. (2016), and PCR genotyping of single embryos (left) showing the wild type and the corresponding deleted bands by gel electrophoresis.”
BackgroundMethodInfluentialOf mice and men: in vivo and in vitro studies of primordial germ cell specification
Kumar, D. L., & DeFalco, T. (2017) · Seminars in Reproductive Medicine · doi:10.1055/s-0037-1599085 · Cited by 14
Capturing Pluripotency and Beyond
Yeh, C.-Y., Huang, W.-H., Chen, H.-C., & Meir, Y. (2021) · Cells · doi:10.3390/cells10123558 · Cited by 13 · see citing works
Chimeric NANOG repressors inhibit glioblastoma growth in vivo in a context-dependent manner
Kuciak, M., Mas, C., Borges, I., Sánchez-Gómez, P., & Altaba, A. R. I. (2019) · Scientific Reports · doi:10.1038/s41598-019-39473-y · Cited by 13 · see citing works
Yu, S. E., Kim, M. S., Park, S. H., Yoo, B., Kim, K.-H., & Jang, Y. (2017) · Cell Biochemistry and Function · doi:10.1002/cbf.3269 · Cited by 13 · see citing works
Yuan, F., Yang, J.-H., Ma, F., Hu, Z., Malik, V., Zang, R., Li, D., Shi, X., Huang, X., Zhou, H.-W., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-57165-2 · Cited by 12 · see citing works
“Given that Tex10 interacts with and regulates Nanog in mouse ESCs 20 and that Nanog acts as a potent inducer of PGC speci fi cation from ESC-derived EpiLCs 7 , we next asked if Tex10 overexpression (OE) would promote PGC development.”
Tissue and cell interactions in mammalian PGC development.
Cooke, C. B., & Moris, N. (2021) · Development · doi:10.1242/dev.200093 · Cited by 12
Shi, G., Bai, Y., Zhang, X.-Y., Su, J., Pang, J., He, Q., Zeng, P., Ding, J.-J., Xiong, Y.-Y., Zhang, J., et al. (2021) · Protein & Cell · doi:10.1007/s13238-021-00884-1 · Cited by 12 · see citing works
“, Stella, BlIMP1, NANOS2) and is essential for germ cell lineage determination (Kehler et al., 2004; van den Berg et al., 2008; Murakami et al., 2016; Fang et al., 2018).”
BackgroundInfluentialRore, H., Owen, N., Piña-Aguilar, R., Docherty, K., & Sekido, R. (2021) · Communications Biology · doi:10.1038/s42003-021-02322-8 · Cited by 12
The transcription factor GABPA is a master regulator of naive pluripotency
Zhou, C.-J., Wang, M., Zhang, C., & Zhang, Y. (2025) · Nature Cell Biology · doi:10.1038/s41556-024-01554-0 · Cited by 11 · see citing works
Giovannantonio, L. D. D., Acampora, D., Omodei, D., Nigro, V., Barba, P., Barbieri, E., Chambers, I., & Simeone, A. (2021) · Development · doi:10.1242/dev.199166 · Cited by 11 · see citing works
YAP establishes epiblast responsiveness to inductive signals for germ cell fate
Kagiwada, S., Aramaki, S., Wu, G.-M., Shin, B., Kutejova, E., Obridge, D., Adachi, K., Wrana, J., Hübner, K., & Schöler, H. (2021) · Development · doi:10.1242/dev.199732 · Cited by 10
“We would like the reviewer to note that the previous study clearly indicates that integrinb3/ SSEA1 double-positive cells are equivalent to the cell fraction of functional PGCLCs with further differentiation competence, and the methodology is a reliable method for identifying specified PGCLCs in the relevant field (Ha…”
MethodTranscriptional and epigenetic control of germline competence and specification.
Bleckwehl, T., & Rada-Iglesias, Á. (2019) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2019.05.006 · Cited by 10 · see citing works
LIN28A activates the transcription of NANOG in dairy goat male germline stem cells
Ma, F.-L., Du, X., Wei, Y., Zhou, Z., Clotaire, D. Z. J., Li, N., Peng, S., Li, G.-P., & Hua, J. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27593 · Cited by 10 · see citing works
“Furthermore, NANOG promoted the proliferation of the embryonic stem cells (ESCs) (Camp et al., 2009; Schuff et al., 2012) and alone induced germ cells to primed epiblast (Murakami et al., 2016).”
BackgroundDong, G.-Y., Shang, Z.-C., Liu, L.-Q., Liu, C.-Y., Ge, Y., Wang, Q.-L., Wu, L., Chen, F., Li, B.-L., Liu, X., et al. (2017) · Bioscience Reports · doi:10.1042/bsr20170637 · Cited by 10
Li, Z.-L., Fang, F., Long, Y., Zhao, Q., Wang, X.-T., Ye, Z., Meng, T.-Q., Gu, X.-L., Xiang, W.-P., Xiong, C.-L., et al. (2022) · Cell & Bioscience · doi:10.1186/s13578-022-00917-0 · Cited by 9 · see citing works
“Conversely, SOX17 is not critical for mPGC differentiation, and overexpression of Nanog along can induce PGCLCs in mouse EpiLCs (epiblast-like cells) [49], which illustrates that NANOG plays different roles in human and mouse PGC specification (Fig.”
BackgroundAdvances in Female Germ Cell Induction from Pluripotent Stem Cells
Gulimiheranmu, M., Wang, X., & Zhou, J.-M. (2021) · Stem Cells International · doi:10.1155/2021/8849230 · Cited by 9 · see citing works
“Migrating human PGCs mainly express early GCs markers BLIMP1, TFAP2C, and SSEA1 as well as pluripotency markers OCT4 and NANOG.”
BackgroundMethodInfluentialEnhancer priming by H3K4 methylation safeguards germline competence
Bleckwehl, T., Schaaf, K., Crispatzu, G., Respuela, P., Bartusel, M., Benson, L., Clark, S. J., Dorighi, K. M., Barral, A., Laugsch, M., et al. (2020) · bioRxiv · doi:10.1101/2020.07.07.192427 · Cited by 9
Segregation of the mouse germline and soma
Zhang, M., & Chambers, I. (2019) · Cell Cycle · doi:10.1080/15384101.2019.1672466 · Cited by 9
“In addition, regulatory interactions by pluripotency TFs on genes encoding the PGC TFs have been reported [35].”
BackgroundDNMT1 can induce primary germ layer differentiation through de novo DNA methylation
Ito, T., Kubiura-Ichimaru, M., Miura, F., Tajima, S., Surani, M., Ito, T., Yamaguchi, S., & Tada, M. (2024) · Genes to Cells · doi:10.1111/gtc.13130 · Cited by 8 · see citing works
“Furthermore, NANOG can induce the expression of PGC-related genes without BMP4 signaling (Murakami et al., 2016).”
BackgroundResultLi, Q., Huang, Y.-H., Xu, J., Mao, F.-B., Zhou, B., Sun, L.-C., Basinski, B. W., Aksu, M., Liu, J., Dou, Y., et al. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.10.002 · Cited by 8 · see citing works
“Growth advantage of mESCs by p53 deletion and upregulation of p53 target gene Nanog may account for enriched PGCLC differentiation (Lin et al., 2005; Murakami et al., 2016).”
Background
- 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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