Retinoic acid orchestrates fibroblast growth factor signalling to drive embryonic stem cell differentiation
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Embryonic stem (ES) cells fluctuate between self-renewal and the threshold of differentiation. Signalling via the fibroblast growth factor (Fgf)/Erk pathway is required to progress from this dynamic state and promote mouse ES cell differentiation. Retinoic acid also induces differentiation in many cellular contexts, but its mechanism of action in relation to Fgf/Erk signalling in ES cells is poorly understood. Here, we show for the first time that endogenous retinoid signalling is required for the timely acquisition of somatic cell fate in mouse ES cells and that exposure to retinoic acid advances differentiation by a dual mechanism: first increasing, but in the long-term decreasing, Fgf signalling. Rapid retinoid induction of Fgf8 and downstream Erk activity on day 1 in differentiation conditions may serve to ensure loss of self-renewal. However, more gradual repression of Fgf4 by retinoic acid is accompanied by an overall reduction in Erk activity on day 2, and the acquisition of neural and non-neural fates is now advanced by inhibition of Fgf signalling. So, although blocking Fgf/Erk activity is known to promote ES cell self-renewal, once cells have experienced a period of such signals, subsequent inhibition of Fgf signalling has the opposite effect and drives differentiation. We further show in the embryo that retinoid repression of Fgf signalling promotes neural differentiation onset in an analogous step in the extending embryonic body axis and so identify attenuation of Fgf signalling by retinoic acid as a conserved fundamental mechanism driving differentiation towards somatic cell fates.
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In neuronal cells, Sertoli cells, and embryonic stem cells, RA instead activates p42/p44 Erk or classical MAPKs.
“However, in neuronal cells, Sertoli cells, and embryonic stem cells, RA instead activates the p42/p44 extracellular signal-regulated kinases (Erk) or classical MAPKs ( 116-122 ).”
From Vitamin A and retinoid signaling: genomic and nongenomic effects (2013) · cites this paper as [119]
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“, 1996), early ectodermal formation and patterning (Fgf8) (Stavridis et al., 2010), early mesodermal formation (T) (Herrmann et al.”
BackgroundSpecification of GnRH-1 neurons by antagonistic FGF and retinoic acid signaling
Sabado, V., Barraud, P., Baker, C. V. H., & Streit, A. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.12.016 · Cited by 58 · see citing works
“In the elongating spinal cord and in embryonic stem cells, FGF activity ensures continued proliferation of progenitor cells, while RA initiates neuronal differentiation (Diez del Corral and Storey, 2004; Diez del Corral et al., 2003; Sockanathan et al., 2003; Stavridis et al., 2010).”
BackgroundEpigenetic regulation of Nanog expression by Ezh2 in pluripotent stem cells
Villasante, A., Piazzolla, D., Li, H., Goméz-López, G., Djabali, M., & Serrano, M. (2011) · Cell Cycle · doi:10.4161/cc.10.9.15658 · Cited by 57 · see citing works
Patel, N. S., Rhinn, M., Semprich, C. I., Halley, P. A., Dollé, P., Bickmore, W. A., & Storey, K. G. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003614 · Cited by 56 · see citing works
“Although we assess these changes by detailed investigation around two exemplar neural differentiation genes, FGF signalling in this context represses expression of many such genes, including Sox1 and Sox3 (further regulators of the neural progenitor cell state) and prevents the onset of ventral patterning and neuron p…”
Self-citationLai, Y.-S., Chang, C., Pawlik, K. M., Zhou, D., Renfrow, M. B., & Townes, T. M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1108595109 · Cited by 56 · see citing works
“RA is known to stimulate ESC differentiation through the FGF/ERK pathway (47, 48), and phosphorylation of Parp1 via Erk1/2 is known to induce Parp1 auto-PARylation (49).”
BackgroundMethodGenolet, O., Monaco, A. A., Dunkel, I., Boettcher, M., & Schulz, E. G. (2021) · Genome biology · doi:10.1186/s13059-021-02321-2 · Cited by 54 · see citing works
“The main growth factors that stimulate MAPK signaling at these early developmental stages belong to the fibroblast growth factor (Fgf) family [16, 17].”
BackgroundTurner, D. A., Trott, J., Hayward, P. C., Rué, P., & Arias, A. M. (2014) · Biology Open · doi:10.1242/bio.20148409 · Cited by 55 · see citing works
Olivera-Martínez, I., Schurch, N., Li, R. A., Song, J., Halley, P. A., Das, R. M., Burt, D. W., Barton, G. J., & Storey, K. G. (2014) · Development · doi:10.1242/dev.112623 · Cited by 53 · see citing works
“…this, the closed caudal neural tube (CNT) is flanked by somites and is an early site of co-expression of all three Sox1B genes, which are characteristic of neural progenitors (Delfino-Machín et al., 2005; Stavridis et al., 2010), and of key ventral patterning genes (Diez del Corral et al., 2003).”
InfluentialSelf-citationRegulation of the ERK signalling pathway in the developing mouse blastocyst
Azami, T., Bassalert, C., Allègre, N., Estrella, L. V., Pouchin, P., Ema, M., & Chazaud, C. (2019) · Development · doi:10.1242/dev.177139 · Cited by 48 · see citing works
“, 2014), express high levels ofFgf4, and theFGFpathway is necessary for their exit of pluripotency and differentiation (Hamilton and Brickman, 2014; Kalkan et al., 2017; Kunath et al., 2007; Molotkov et al., 2017; Schröter et al., 2015; Stavridis et al., 2010).”
BackgroundSantana, M. M., Chung, K.-F., Vukićević, V., Rosmaninho‐Salgado, J., Kanczkowski, W., Cortez, V., Hackmann, K., Bastos, C., Mota, A., Schröck, E., et al. (2012) · Stem Cells Translational Medicine · doi:10.5966/sctm.2012-0022 · Cited by 51 · see citing works
HOX genes in stem cells: Maintaining cellular identity and regulation of differentiation
Steens, J., & Klein, D. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1002909 · Cited by 50 · see citing works
“and thus decisively impact on balancing of stem cell quiescence and activation (Stavridis et al., 2010; Gudas and Wagner, 2011) (Figure 1).”
BackgroundMechanisms of Pluripotency In Vivo and In Vitro
Pósfai, E., Tam, O. H., & Rossant, J. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-416022-4.00001-9 · Cited by 49 · see citing works
Region‐specific regulation of posterior axial elongation during vertebrate embryogenesis
Neijts, R., Simmini, S., Giuliani, F., van Rooijen, C., & Deschamps, J. (2013) · Developmental Dynamics · doi:10.1002/dvdy.24027 · Cited by 44 · see citing works
“The biphasic response of embryonic axial progenitors exhibiting initial compatibility of RA exposure with self-renewal, and later drifting towards differentiation in the presence of RA was reported to be observed as well in murine embryonic stem cells in culture (Stavridis et al., 2010).”
BackgroundNuclear and extranuclear effects of vitamin A
Iskakova, M., Karbyshev, M. S., Piskunov, A., & Rochette‐Egly, C. (2015) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2014-0522 · Cited by 44 · see citing works
WNT/β-CATENIN modulates the axial identity of ES derived human neural crest
Gomez, G. A., Prasad, M. S., Wong, M., Charney, R. M., Shelar, P. B., Sandhu, N., Hackland, J. O. S., Hernández, J. C., Leung, A. W., & García‐Castro, M. I. (2019) · Development · doi:10.1242/dev.175604 · Cited by 43 · see citing works
“Another possibility is that exogenous RA can modulate FGF (Stavridis et al., 2010), and in conditions where RA activity is elevated, FGF inhibition would prevent activation of the NC program.”
Single cell lineage analysis of mouse embryonic stem cells at the exit from pluripotency
Trott, J., & Arias, A. M. (2013) · Biology Open · doi:10.1242/bio.20135934 · Cited by 37 · see citing works
“In the course of our experiments we were surprised to observe cells primed for endoderm and mesoderm in N2B27, which is commonly used as a base medium to generate neural tissue (Ying et al., 2003b; Engberg et al., 2010; Stavridis et al., 2010).”
BackgroundMethodStudying Lineage Decision-Making In Vitro: Emerging Concepts and Novel Tools
Semrau, S., & van Oudenaarden, A. (2015) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100814-125300 · Cited by 35 · see citing works
“For example, these screens all identified the repressive factor Tcf3, a terminal component of the Wnt pathway, as a crucial factor, and one study produced several hits in the FGF/ERK signaling pathway (Leeb et al. 2014 ).”
InfluentialZhao, H., Zuo, X., Ren, L., Li, Y., Tai, H., Du, J., Xie, X., Zhang, X., Han, Y., Wu, Y., et al. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.10.002 · Cited by 36 · see citing works
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“This phenomenon could be linked to the conservation of progenitor cell populations during lung morphogenesis (50).”
Nuclear and Extra-Nuclear Effects of Retinoid Acid Receptors: How They Are Interconnected
Piskunov, A., Tanoury, Z. A., & Rochette‐Egly, C. (2014) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-94-017-9050-5_6 · Cited by 34 · see citing works
“RA activates the p42/p44 MAPKs (also called Erks) in neurons, Sertoli cells, and embryonic stem cells [30, 33, 59, 87, 123].”
BackgroundChen, Y., Liu, Y., Miao, Z., Yin, M., Lu, W., Lv, Y., Ding, M., & Deng, H. (2010) · Blood · doi:10.1182/blood-2010-01-263335 · Cited by 33 · see citing works
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“The spatially positioned and locally high concentration of RA in NSCs over time significantly enhanced RA transportation into the nucleus to bind with transcription factors in initiating stem cell differentiation.(37)”
Liu, Q., Lyu, Z., You, Y., Zhao, Z., Hu, S., Yuan, L., Chen, G., & Chen, H. (2017) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.7b01397 · Cited by 32 · see citing works
“differentiation of mESCs into neural cells.(22,23) Nevertheless, the use of native GAGs is limited due to problems such as variation in structure and contamination.”
BackgroundZhu, X., Wang, W., Zhang, X., Bai, J., Chen, G., Li, L., & Li, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0143255 · Cited by 31 · see citing works
Arber, C., & Li, M. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00010 · Cited by 32 · see citing works
“Although the use of RA is contentious, the RA signaling pathway has been shown to be relevant for early forebrain development (Schneider et al., 2001; Stavridis et al., 2010; Chatzi et al., 2011).”
BackgroundModeling Mammalian Commitment to the Neural Lineage Using Embryos and Embryonic Stem Cells
Shparberg, R. A., Glover, H. J., & Morris, M. B. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00705 · Cited by 35 · see citing works
“Following a short burst of Fgf4 -mediated ERK activity, RA gradually downregulates the expression of Fgf4 and p-ERK, which is accompanied by an increase in Sox1 + neurectoderm cells (Stavridis et al., 2010; Rizvi et al., 2017).”
Annenkov, A. E. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8532-5 · Cited by 29 · see citing works
“ling on neural differentiation of ES cells has also been reported [185, 186].”
BackgroundA gene regulatory network for neural induction
Trevers, K. E., Lu, H., Yang, Y., Thiery, A. P., Strobl, A., Anderson, C., Pálinkášová, B., Oliveira, N. M. M., Almeida, I. D., Khan, M. A. F., et al. (2023) · eLife · doi:10.7554/elife.73189 · Cited by 29 · see citing works
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“…decade, this scenario became more complicated with the discovery that RA also has non-genomic effects and induces the rapid activation of the MAPK pathway (Piskunov and Rochette-Egly, 2012; Stavridis et al., 2010), and that RARs are phosphoproteins (Al Tanoury et al., 2013b; Rochette-Egly, 2003).”
BackgroundResultBarceinas, R. S. Q., García-Regalado, A., Aréchaga-Ocampo, E., Villegas‐Sepúlveda, N., & la Rosa, C. H. G.-D. (2015) · BioMed Research International · doi:10.1155/2015/404368 · Cited by 28 · see citing works
“ATRA may also directly regulate the activation of some kinase signaling pathways by so-called nongenomic mechanisms, which do not involve a transcriptional response [9], such as retinoylation [10].”
Semprich, C. I., Davidson, L., Torres, A. A., Patel, H., Briscoe, J., Metzis, V., & Storey, K. G. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3000221 · Cited by 26 · see citing works
Self-citationGamm, D. M., Clark, E., Capowski, E. E., & Singh, R. (2019) · American Journal of Ophthalmology · doi:10.1016/j.ajo.2019.04.033 · Cited by 26 · see citing works
Ectodermal progenitors derived from epiblast stem cells by inhibition of Nodal signaling
Li, L., Song, L., Liu, C. X., Chen, J., Peng, G., Wang, R., Liu, P., Tang, K., Rossant, J., & Jing, N. (2015) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjv030 · Cited by 26 · see citing works
“…BMP4 and PD17 increases the proportion of K8/K18-positive Downloaded from https://academic.oup.com/jmcb/article-abstract/7/5/455/966093 by guest on 27 July 2018 populations during ESC differentiation (Stavridis et al., 2010), indicating that epidermis development is enhanced by these two factors.”
BackgroundWesterman, B. A., Braat, A. K., Taub, N., Potman, M., Vissers, J. H. A., Blom, M., Verhoeven, E., Stoop, H., Gillis, A., Velds, A., et al. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20102037 · Cited by 26 · see citing works
“This is consistent with a recent study showing that lowering FGF signaling in mouse ES cells after initial FGF-mediated differentiation leads to enhanced differentiation (Stavridis et al., 2010).”
ResultInhibition of Cell Division and DNA Replication Impair Mouse-Naïve Pluripotency Exit
Waisman, A., Echegaray, C. V., Solari, C., Cosentino, M. S., Martyn, I., Deglincerti, A., Ozair, M. Z., Ruzo, A., Barañao, L., Miriuka, S., et al. (2017) · Journal of Molecular Biology · doi:10.1016/j.jmb.2017.06.020 · Cited by 25 · see citing works
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“26 This could have been the reason why this study showed a decrease in proliferation in the cocultures that had growth factors.”
N-cadherin stabilises neural identity by dampening anti-neural signals
Punovuori, K., Migueles, R. P., Malaguti, M., Blin, G., Macleod, K. G., Carragher, N. O., Pieters, T., Roy, F. M. V., Stemmler, M., & Lowell, S. (2019) · Development · doi:10.1242/dev.183269 · Cited by 22 · see citing works
“It has previously been reported that FGF signalling promotes the acquisition and maintenance of primed pluripotency, but must then be downregulated in order for primed cells to progress to a neural fate (Greber et al., 2010; Jaeger et al., 2011; Stavridis et al., 2010; Sterneckert et al., 2010).”
Resveratrol Enhances Self‐Renewal of Mouse Embryonic Stem Cells
Li, N., Du, Z., Shen, Q., Lei, Q., Zhang, Y., Zhang, M., & Hua, J. (2017) · Journal of Cellular Biochemistry · doi:10.1002/jcb.25942 · Cited by 23 · see citing works
“The method for RA treatment was adapted from several earlier reports [Aubert et al., 2002; Ying et al., 2003; Ying and Smith, 2003; Stavridis et al., 2010; Li et al., 2014].”
MethodManku, G., Wang, Y., Merkbaoui, V., Boisvert, A., Ye, X., Blonder, J., & Culty, M. (2014) · Endocrinology · doi:10.1210/en.2014-1524 · Cited by 22 · see citing works
“Such a process has been observed in the cross talk between fibroblast growth factor (FGF) and RA, where there is an initial rapid RA-induced induction of FGF8 (which contains RAREs), followed by a long-term FGF4 repression, which results in ESC neuronal differentiation (14, 59).”
BackgroundBouffant, R. L., Wang, J., Futel, M., Buisson, I., Umbhauer, M., & Riou, J. (2012) · Biology of the Cell · doi:10.1111/boc.201200005 · Cited by 21 · see citing works
“Nonetheless, they essentially involve mkp3, as observed in the tailbud (Moreno and Kintner, 2004; Stavridis et al., 2010).”
BackgroundGlycans in Diseases and Therapeutics
Pavão, M. S. G. (2011) · Springer eBooks · doi:10.1007/978-3-642-16833-8 · Cited by 22 · see citing works
Effects of all-trans and 9-cis retinoic acid on differentiating human neural stem cells in vitro
Kubíčková, B., Martinkova, S., Bohačiaková, D., Nezvedová, M., Liu, R., Brózman, O., Spáčil, Z., & Hilscherová, K. (2023) · Toxicology · doi:10.1016/j.tox.2023.153461 · Cited by 18 · see citing works
Velkey, J. M., & O’Shea, K. S. (2013) · Developmental Dynamics · doi:10.1002/dvdy.23920 · Cited by 18 · see citing works
“Fgf signaling can maintain self-renewal of ESC (Sterneckert et al., 2010; Staviridis et al., 2010), and is required for cell cycle exit and the transition to lineage differentiation (Kunath et al., 2007).”
BackgroundSnai1 Promotes ESC Exit from the Pluripotency by Direct Repression of Self-Renewal Genes
Galvagni, F., Lentucci, C., Neri, F., Dettori, D., Clemente, C. D., Orlandini, M., Anselmi, F., Rapelli, S., Grillo, M., Borghi, S., et al. (2014) · Stem Cells · doi:10.1002/stem.1898 · Cited by 17 · see citing works
Retinoic Acid Signaling during Early Spinal Cord Development
del Corral, R. D., & Morales, A. V. (2014) · Journal of Developmental Biology · doi:10.3390/jdb2030174 · Cited by 17 · see citing works
“Although Sox2 is expressed in RA-deficient conditions [49], the expression of Sox1 and Sox3 is greatly downregulated in VAD quails, and this may also contribute to the downregulation of many of the ventral patterning genes, although this has not been examined yet [75].”
BackgroundThe molecular circuitry underlying pluripotency in embryonic stem cells
Warmflash, A., Arduini, B. L., & Brivanlou, A. H. (2012) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1182 · Cited by 16 · see citing works
Neural Differentiation of Mouse Embryonic Stem Cells in Serum-free Monolayer Culture
Wongpaiboonwattana, W., & Stavridis, M. P. (2015) · Journal of Visualized Experiments · doi:10.3791/52823 · Cited by 17 · see citing works
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Zfhx1b Induces a Definitive Neural Stem Cell Fate in Mouse Embryonic Stem Cells
Dang, L. T. H., Wong, L., & Tropepe, V. (2012) · Stem Cells and Development · doi:10.1089/scd.2011.0593 · Cited by 15 · see citing works
“A recent report suggests that RA signaling controls the switch from the pluripotent state to differentiation by first suppressing Oct4 expression as well as mediating Erk signaling to induce Fgf8 expression [44].”
Promoting neural differentiation of embryonic stem cells using β-cyclodextrin sulfonate
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“Retinoic acid has also been shown to coordinate FGF signaling during stem cell differentiation [54].”
BackgroundRetinoic acid-stimulated ERK1/2 pathway regulates meiotic initiation in cultured fetal germ cells
Kim, S. M., YOKOYAMA, T., Ng, D., Ulu, F., & Yamazaki, Y. (2019) · PLoS ONE · doi:10.1371/journal.pone.0224628 · Cited by 13 · see citing works
Patel, N. S., Rhinn, M., Semprich, C. I., Halley, P. A., Dollé, P., Bickmore, W. A., & Storey, K. G. (2013) · PLoS Genetics · doi:10.1371/annotation/c066bb84-13ea-4b36-a481-f149df8ce929 · Cited by 13 · see citing works
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“…for the repair of traumatic nerve injury and neurological diseases with application of the optimal combination of RA and OECs for neuronal differentiation of hBMSCs. Keywords Human bone marrow stromal stem cells Retinoic acid Neural differentiation Human olfactory ensheathing cells Co-culture”
BackgroundNovel Function of Sprouty4 as a Regulator of Stemness and Differentiation of Embryonic Stem Cells
Lee, J., Park, S., Kim, K., Ko, J., Lee, S., Kim, K. P., & Park, K. (2016) · Development & Reproduction · doi:10.12717/dr.2016.20.2.171 · Cited by 10 · see citing works
“…response to external differentiation-inducing stimuli as well as inducing the expression of inhibitors of FGF signaling to generate a negative-feedback loop that would facilitate reversion back to the original unprimed state (Kunath et al., 2007; Stavridis et al., 2007; Stavridis et al., 2010).”
Wang, Z., Li, S., Lin-Chen, G. U. O., Yin, M., & Sun, Y. (2011) · YAKUGAKU ZASSHI · doi:10.1248/yakushi.131.993 · Cited by 10 · see citing works
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A cross-disciplinary approach to understanding neural stem cells in development and disease
Henrique, D., & Bally‐Cuif, L. (2010) · Development · doi:10.1242/dev.052621 · Cited by 6 · see citing works
“We focus here on some of the key issues and perspectives that emerged during the meeting.”
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“According to previous investigations on RA-induced neural differentiation (Kunath et al., 2007; Li et al., 2006; Lu et al., 2009; Stavridis et al., 2007; Stavridis et al., 2010), fibroblast growth factor (Fgf)/extracellular signal-regulated kinase (Erk) signaling may cooperate with RA signaling and play an important r…”
Glover, H. J., Holliday, H., Shparberg, R. A., Winkler, D. A., Day, M. L., & Morris, M. B. (2023) · Development · doi:10.1242/dev.201704 · Cited by 5 · see citing works
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Inhibition of MUC1-C Increases ROS and Cell Death in Mouse Embryonic Stem Cells
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“The protein level of MUC1-C was decreased during differentiation of mES cells To investigate the expression patterns of MUC1 in undifferentiated mES cells and differentiated cells, we determined the mRNA and protein levels of MUC1 during RA-induced differentiation (19) of mES cells.”
BackgroundDNA-Dependent Protein Kinase Is a Context Dependent Regulator of Lmx1a and Midbrain Specification
Hunt, C. P. J., Fabb, S. A., Pouton, C. W., & Haynes, J. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078759 · Cited by 4 · see citing works
“The MAPK pathway is critical in maintaining ESC pluripotency [39] and is an important contributor to the dopaminergic specification of neuroectoderm [40,41].”
BackgroundNeural Differentiation of Mouse Embryonic Stem Cells in Serum-free Monolayer Culture
Wongpaiboonwattana, W., & Stavridis, M. P. (2015) · Journal of Visualized Experiments · doi:10.3791/52823-v · Cited by 4 · see citing works
Self-citationSemprich, C. I., Metzis, V., Patel, H., Briscoe, J., & Storey, K. G. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/586719 · Cited by 4 · see citing works
“Importantly, however, only a short critical period of ERK1/2 signalling is required in 73 mES cells for subsequent expression of neural genes [27], after which FGF inhibition then accelerates 74 neural differentiation [27, 30, 31].”
BackgroundSelf-citationGenolet, O., Monaco, A. A., Dunkel, I., Boettcher, M., & Schulz, E. G. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.03.09.983544 · Cited by 4 · see citing works
“The main growth factors that stimulate MAPK signalling at these early developmental stages belong to the fibroblast growth factor (Fgf) family (Kunath et al. 2007; Stavridis et al. 2010).”
- Authors
- Stavridis, M. P., Collins, B. J., & Storey, K. G.
- Affiliations
- University of Dundee (GB)
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2010-03-15
- Volume
- 137
- Issue
- 6
- Pages
- 881-890
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- PMC
- PMC2834455
- OpenAlex
- W2115463333
- Cited by
- 124
- References
- 60
- Citations by year
- 2026: 2 · 2023: 6 · 2022: 3 · 2021: 4 · 2020: 5 · 2019: 10 · 2018: 4 · 2017: 7 · 2016: 4 · 2015: 15 · 2014: 13 · 2013: 15 · 2012: 12
- FWCI
- 6.52
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Development (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Discovery Research Portal (University of Dundee) (publishedVersion)
- Funders
- Biotechnology and Biological Sciences Research Council
- 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 › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- retinoic acid, FGF signaling, embryonic stem cell differentiation, self-renewal, FGF8, FGF4, neuronal differentiation, retinoic acid signaling, mouse embryo
- MeSH terms
- Animals, Cell Differentiation, Cells, Cultured, Chick Embryo, Fibroblast Growth Factors, Neurons, Pyrimidines, Tretinoin, Signal Transduction, Receptors, Fibroblast Growth Factor, Body Patterning, Protein Kinase Inhibitors, Extracellular Signal-Regulated MAP Kinases, Mice, Embryonic Stem Cells, Neurogenesis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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