Regulation of extra-embryonic endoderm stem cell differentiation by Nodal and Cripto signaling
Open accessAbstract
The signaling pathway for Nodal, a ligand of the TGFβ superfamily, plays a central role in regulating the differentiation and/or maintenance of stem cell types that can be derived from the peri-implantation mouse embryo. Extra-embryonic endoderm stem (XEN) cells resemble the primitive endoderm of the blastocyst, which normally gives rise to the parietal and the visceral endoderm in vivo, but XEN cells do not contribute efficiently to the visceral endoderm in chimeric embryos. We have found that XEN cells treated with Nodal or Cripto (Tdgf1), an EGF-CFC co-receptor for Nodal, display upregulation of markers for visceral endoderm as well as anterior visceral endoderm (AVE), and can contribute to visceral endoderm and AVE in chimeric embryos. In culture, XEN cells do not express Cripto, but do express the related EGF-CFC co-receptor Cryptic (Cfc1), and require Cryptic for Nodal signaling. Notably, the response to Nodal is inhibited by the Alk4/Alk5/Alk7 inhibitor SB431542, but the response to Cripto is unaffected, suggesting that the activity of Cripto is at least partially independent of type I receptor kinase activity. Gene set enrichment analysis of genome-wide expression signatures generated from XEN cells under these treatment conditions confirmed the differing responses of Nodal- and Cripto-treated XEN cells to SB431542. Our findings define distinct pathways for Nodal and Cripto in the differentiation of visceral endoderm and AVE from XEN cells and provide new insights into the specification of these cell types in vivo.
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emVE represents a specialized variant of exVE, perhaps modulating a transcriptional program in response to stimuli such as BMP or Nodal.
“Differential expression between bulk RNA sequenced E7.5 exVE and emVE populations suggested that emVE represents a specialized variant of exVE (Extended Data Fig. 7d), perhaps modulating a transcriptional program in response to stimuli, such as BMP or Nodal38–40.”
From The emergent landscape of the mouse gut endoderm at single-cell resolution (2019) · cites this paper as [39]
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Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482 · see citing works
Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506580102 · Cited by 53,625 · see citing works
Smyth, G. K. (2004) · Statistical Applications in Genetics and Molecular Biology · doi:10.2202/1544-6115.1027 · Cited by 11,829 · see citing works
Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data
Ramakers, C. R. B., Ruijter, J. M., Deprez, R. H. L., & Moorman, A. F. M. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(02)01423-4 · Cited by 3,718 · see citing works
Manipulating the Mouse Embryo: A Laboratory Manual
Behringer, R. R., Gertsenstein, M., Nagy, K. V., & Nagy, A. (2002) · Cited by 2,046 · see citing works
lumi : a pipeline for processing Illumina microarray
Du, P., Kibbe, W. A., & Lin, S. M. (2008) · Bioinformatics · doi:10.1093/bioinformatics/btn224 · Cited by 2,028 · see citing works
Inman, G. J., Nicolás, F. J., Callahan, J. F., Harling, J. D., Gaster, L. M., Reith, A. D., Laping, N. J., & Hill, C. S. (2002) · Molecular Pharmacology · doi:10.1124/mol.62.1.65 · Cited by 1,636 · see citing works
Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells
Vallier, L., Alexander, M., & Pedersen, R. A. (2005) · Journal of Cell Science · doi:10.1242/jcs.02553 · Cited by 948 · see citing works
Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo
Arnold, S. J., & Robertson, E. J. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2618 · Cited by 816 · cited 1× · see citing works
“In particular, a central role in anterior-posterior (A-P) axis specification is played by the anterior visceral endoderm (AVE), a specialized population of cells within the visceral endoderm that overlies and patterns the adjacent epiblast at pregastrulation and early gastrulation stages (Arnold and Robertson, 2009; R…”
BackgroundThe EGF-CFC Protein One-Eyed Pinhead Is Essential for Nodal Signaling
Gritsman, K., Zhang, J., Cheng, S. K., Heckscher, E. S., Talbot, W. S., & Schier, A. F. (1999) · Cell · doi:10.1016/s0092-8674(00)80720-5 · Cited by 713 · see citing works
A transcriptional partner for MAD proteins in TGF-β signalling
Chen, X., Rubock, M. J., & Whitman, M. (1996) · Nature · doi:10.1038/383691a0 · Cited by 694 · see citing works
Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse
Rossant, J., & Tam, P. (2009) · Development · doi:10.1242/dev.017178 · Cited by 629 · see citing works
Smad4 and FAST-1 in the assembly of activin-responsive factor
Chen, X., Weisberg, E., Fridmacher, V., Watanabe, M., Naco, G., & Whitman, M. (1997) · Nature · doi:10.1038/38008 · Cited by 565 · see citing works
Nodal signalling in the epiblast patterns the early mouse embryo
Brennan, J., Lu, C. C., Norris, D. P., Rodríguez, T. A., Beddington, R. S. P., & Robertson, E. J. (2001) · Nature · doi:10.1038/35082103 · Cited by 551 · see citing works
Nodal signaling: developmental roles and regulation
Shen, M. M. (2007) · Development · doi:10.1242/dev.000166 · Cited by 537 · see citing works
Self-citationThomas, P. Q., Brown, A., & Beddington, R. S. P. (1998) · Development · doi:10.1242/dev.125.1.85 · Cited by 528 · see citing works
Generating green fluorescent mice by germline transmission of green fluorescent ES cells
Hadjantonakis, A., Gertsenstein, M., Ikawa, M., Okabe, M., & Nagy, A. (1998) · Mechanisms of Development · doi:10.1016/s0925-4773(98)00093-8 · Cited by 483 · see citing works
Imprinted X-inactivation in extra-embryonic endoderm cell lines from mouse blastocysts
Kunath, T., Arnaud, D., Uy, G. D., Okamoto, I., Chureau, C., Yamanaka, Y., Heard, É., Gardner, R. L., Avner, P. R., & Rossant, J. (2005) · Development · doi:10.1242/dev.01715 · Cited by 404 · see citing works
Kwon, G. S., Viotti, M., & Hadjantonakis, A.-K. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.07.017 · Cited by 402 · see citing works
Nodal Signals to Smads through Cripto-Dependent and Cripto-Independent Mechanisms
Yeo, C., & Whitman, M. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00249-0 · Cited by 376 · see citing works
Making a firm decision: multifaceted regulation of cell fate in the early mouse embryo
Zernicka‐Goetz, M., Morris, S. A., & Bruce, A. W. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2564 · Cited by 322 · see citing works
Reissmann, E., Jörnvall, H., Blokzijl, A., Andersson, O., Chang, C., Minchiotti, G., Persico, M. G., Ibáñez, C. F., & Brivanlou, A. H. (2001) · Genes & Development · doi:10.1101/gad.201801 · Cited by 307 · see citing works
Conserved requirement for EGF-CFC genes in vertebrate left-right axis formationPreprint
Yan, Y.-T., Gritsman, K., Ding, J., Burdine, R. D., Corrales, J. D., Price, S. M., Talbot, W. S., Schier, A. F., & Shen, M. M. (1999) · Genes & Development · doi:10.1101/gad.13.19.2527 · Cited by 253 · see citing works
Self-citationMesnard, D., Guzman-Ayala, M., & Constam, D. B. (2006) · Development · doi:10.1242/dev.02413 · Cited by 252 · see citing works
Nodal MorphogensPreprint
Schier, A. F. (2009) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a003459 · Cited by 251 · see citing works
The Foxh1-dependent autoregulatory enhancer controls the level of Nodal signals in the mouse embryo
Norris, D. P., Brennan, J., Bikoff, E. K., & Robertson, E. J. (2002) · Development · doi:10.1242/dev.129.14.3455 · Cited by 234 · see citing works
Dual Roles of Cripto as a Ligand and Coreceptor in the Nodal Signaling Pathway
Yan, Y., Liu, J.-J., Luo, Y., Chaosu, E., Haltiwanger, R. S., Abate-Shen, C. T., & Shen, M. M. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.13.4439-4449.2002 · Cited by 209 · see citing works
Self-citationTwo Modes by which Lefty Proteins Inhibit Nodal Signaling
Chen, C., & Shen, M. M. (2004) · Current Biology · doi:10.1016/j.cub.2004.02.042 · Cited by 197 · see citing works
Self-citationShani, G., Fischer, W. H., Justice, N. J., Kelber, J. A., Vale, W., & Gray, P. C. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01716-07 · Cited by 186 · see citing works
Active cell migration drives the unilateral movements of the anterior visceral endoderm
Srinivas, S., Rodríguez, T. A., Clements, M., Smith, J. C., & Beddington, R. S. P. (2004) · Development · doi:10.1242/dev.01005 · Cited by 185 · see citing works
Cripto forms a complex with activin and type II activin receptors and can block activin signaling
Gray, P. C., Harrison, C. A., & Vale, W. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0531290100 · Cited by 164 · see citing works
EGF-CFC proteins are essential coreceptors for the TGF-β signals Vg1 and GDF1Preprint
Cheng, S. K., Olale, F., Bennett, J. T., Brivanlou, A. H., & Schier, A. F. (2003) · Genes & Development · doi:10.1101/gad.1041203 · Cited by 160 · see citing works
Antibody blockade of the Cripto CFC domain suppresses tumor cell growth in vivo
Adkins, H. B., Bianco, C., Schiffer, S. G., Rayhorn, P., Zafari, M. R., Cheung, A. E., Orozco, O. E., Olson, D. L., Luca, A. D., Chen, L. L., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17788 · Cited by 157 · see citing works
Chen, C., Ware, S. M., Sato, A., Houston-Hawkins, D. E., Habas, R., Matzuk, M. M., Shen, M. M., & Brown, C. (2005) · Development · doi:10.1242/dev.02210 · Cited by 149 · see citing works
Self-citationBianco, C., Adkins, H. B., Wechselberger, C., Seno, M., Normanno, N., Luca, A. D., Sun, Y., Khan, N. I., Kenney, N. J., Ebert, A. D., et al. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.8.2586-2597.2002 · Cited by 146 · see citing works
Dynamic morphogenetic events characterize the mouse visceral endoderm
Rivera‐Pérez, J. A., Mager, J., & Magnuson, T. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00302-6 · Cited by 131 · see citing works
Artus, J., Panthier, J., & Hadjantonakis, A. (2010) · Development · doi:10.1242/dev.050864 · Cited by 130 · see citing works
The Mouse Embryo Autonomously Acquires Anterior-Posterior Polarity at Implantation
Takaoka, K., Yamamoto, M., Shiratori, H., Meno, C., Rossant, J., Saijoh, Y., & Hamada, H. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.02.017 · Cited by 128 · see citing works
Takaoka, K., Yamamoto, M., & Hamada, H. (2011) · Nature Cell Biology · doi:10.1038/ncb2251 · Cited by 127 · see citing works
Andersson, O., Korach-André, M., Reissmann, E., Ibáñez, C. F., & Bertolino, P. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0800272105 · Cited by 126 · see citing works
Minchiotti, G., Parisi, S., Liguori, G. L., Signore, M., Lania, G., Adamson, E. D., Lago, C. T., & Persico, M. G. (2000) · Mechanisms of Development · doi:10.1016/s0925-4773(99)00235-x · Cited by 118 · see citing works
Long-range action of Nodal requires interaction with GDF1Preprint
Tanaka, C., Sakuma, R., Nakamura, T., Hamada, H., & Saijoh, Y. (2007) · Genes & Development · doi:10.1101/gad.1623907 · Cited by 118 · see citing works
Migeotte, I., Omelchenko, T., Hall, A., & Anderson, K. V. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000442 · Cited by 114 · see citing works
Nodal Signaling Uses Activin and Transforming Growth Factor-β Receptor-regulated Smads
Kumar, A., Novoselov, V. V., Celeste, A. J., Wolfman, N. M., ten Dijke, P., & Kuehn, M. R. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m004649200 · Cited by 111 · see citing works
A Nodal- and ALK4-independent signaling pathway activated by Cripto-1 through Glypican-1 and c-Src.
Bianco, C., Strizzi, L., Rehman, A. O., Normanno, N., Wechselberger, C., Sun, Y., Khan, N. I., Hirota, M., Adkins, H. B., Williams, K. P., et al. (2003) · PubMed · Cited by 104 · see citing works
Synergistic interaction between Gdf1 and Nodal during anterior axis development
Andersson, O., Reissmann, E., Jörnvall, H., & Ibáñez, C. F. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.02.002 · Cited by 98 · see citing works
Andersson, O., Bertolino, P., & Ibáñez, C. F. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.08.060 · Cited by 94 · see citing works
Cripto Binds Transforming Growth Factor β (TGF-β) and Inhibits TGF-β Signaling
Gray, P. C., Shani, G., Aung, K., Kelber, J. A., & Vale, W. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.01168-06 · Cited by 93 · see citing works
Master regulators used as breast cancer metastasis classifier.
Lim, W. K., Lyashenko, E., & Califano, A. (2009) · PubMed · Cited by 78 · see citing works
Self-citationCripto Binds Transforming Growth Factor β (TGF-β) and Inhibits TGF-β Signaling
Gray, P. C., Shani, G., Aung, K., Kelber, J. A., & Vale, W. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.01609-08 · Cited by 68 · see citing works
Kelber, J. A., Shani, G., Booker, E. C., Vale, W., & Gray, P. C. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m704960200 · Cited by 68 · see citing works
Non-cell-autonomous role forCriptoin axial midline formation during vertebrate embryogenesis
Chu, J., Ding, J., Jeays-Ward, K., Price, S. M., Placzek, M., & Shen, M. M. (2005) · Development · doi:10.1242/dev.02157 · Cited by 63 · see citing works
Self-citationA Comparative Analysis of Extra-Embryonic Endoderm Cell Lines
Brown, K., Legros, S., Artus, J., Doss, M. X., Khanin, R., Hadjantonakis, A., & Foley, A. C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012016 · Cited by 59 · see citing works
Trichas, G., Joyce, B. W., Crompton, L., Wilkins, V., Clements, M., Tada, M., Rodríguez, T. A., & Srinivas, S. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001019 · Cited by 57 · see citing works
Ebert, A. D., Wechselberger, C., Frank, S., Wallace‐Jones, B., Seno, M., Martínez-Lacaci, I., Bianco, C., Santis, M. D., Weitzel, H. K., & Salomon, D. S. (1999) · PubMed · Cited by 57 · see citing works
Torres‐Padilla, M., Richardson, L., Kolasinska-Zwierz, P., Meilhac, S. M., Luetke-Eversloh, M. V., & Zernicka‐Goetz, M. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.06.020 · Cited by 56 · see citing works
MASTER REGULATORS USED AS BREAST CANCER METASTASIS CLASSIFIER
Lim, W. K., Lyashenko, E., & Califano, A. (2008) · Pacific Symposium on Biocomputing (PSB) · doi:10.1142/9789812836939_0048 · Cited by 55 · see citing works
Self-citationEnhancement of Notch receptor maturation and signaling sensitivity by Cripto-1
Watanabe, K., Nagaoka, T., Lee, J. M., Bianco, C., Gonzales, M., de Castro, N. P., Rangel, M. C., Sakamoto, K., Sun, Y., Callahan, R., et al. (2009) · The Journal of Cell Biology · doi:10.1083/jcb.200905105 · Cited by 54 · see citing works
Isolation of Oct4-Expressing Extraembryonic Endoderm Precursor Cell Lines
Debeb, B. G., Galat, V., Epple-Farmer, J., Iannaccone, S., Woodward, W. A., Bäder, M., Iannaccone, P. M., & Binas, B. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007216 · Cited by 53 · see citing works
Coordination of cell proliferation and anterior-posterior axis establishment in the mouse embryo
Stuckey, D. W., Clements, M., Gregorio, A. D., Senner, C. E., Tissier, P. L., Srinivas, S., & Rodríguez, T. A. (2011) · Development · doi:10.1242/dev.063537 · Cited by 52 · see citing works
Chu, J., & Shen, M. M. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.03.009 · Cited by 35 · see citing works
Self-citationDevelopmental Potential of Rat Extraembryonic Stem Cells
Galat, V., Binas, B., Iannaccone, S., Postovit, L.-M. M., Debeb, B. G., & Iannaccone, P. M. (2009) · Stem Cells and Development · doi:10.1089/scd.2009.0115 · Cited by 33 · see citing works
Flagged first, then by citations
1 of the 63 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
The emergent landscape of the mouse gut endoderm at single-cell resolution
Nowotschin, S., Setty, M., Kuo, Y.-Y., Liu, V., Garg, V., Sharma, R., Simon, C. S., Saiz, N., Gardner, R., Boutet, S. C., et al. (2019) · Nature · doi:10.1038/s41586-019-1127-1 · Cited by 383 · see citing works
Oct4 Cell-Autonomously Promotes Primitive Endoderm Development in the Mouse Blastocyst
Frum, T., Halbisen, M. A., Wang, C., Amiri, H., Robson, P., & Ralston, A. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.05.004 · Cited by 194 · see citing works
Semrau, S., Goldmann, J. E., Soumillon, M., Mikkelsen, T. S., Jaenisch, R., & van Oudenaarden, A. (2017) · Nature Communications · doi:10.1038/s41467-017-01076-4 · Cited by 182 · see citing works
Derivation of extraembryonic endoderm stem (XEN) cells from mouse embryos and embryonic stem cells
Niakan, K. K., Schrode, N., Cho, L. T. Y., & Hadjantonakis, A. (2013) · Nature Protocols · doi:10.1038/nprot.2013.049 · Cited by 132 · see citing works
Walsh, L. A., Alvarez, M. J., Sabio, E. Y., Reyngold, M., Makarov, V., Mukherjee, S., Lee, K.-W., Desrichard, A., Turcan, Ş., Dalin, M. G., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.07.052 · Cited by 118 · see citing works
Self-citationRole of Cripto-1 during Epithelial-to-Mesenchymal Transition in Development and Cancer
Rangel, M. C., Karasawa, H., de Castro, N. P., Nagaoka, T., Salomon, D. S., & Bianco, C. (2012) · American Journal Of Pathology · doi:10.1016/j.ajpath.2012.02.031 · Cited by 101 · see citing works
Insulin fine-tunes self-renewal pathways governing naive pluripotency and extra-embryonic endoderm
Anderson, K. G. V., Hamilton, W. B., Roske, F. V., Azad, A., Knudsen, T. E., Canham, M. A., Forrester, L. M., & Brickman, J. M. (2017) · Nature Cell Biology · doi:10.1038/ncb3617 · Cited by 93 · see citing works
Opportunities and challenges with stem cell-based embryo models
Rossant, J., & Tam, P. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.02.002 · Cited by 91 · see citing works
BMP signaling induces visceral endoderm differentiation of XEN cells and parietal endoderm
Paca, A., Séguin, C. A., Clements, M., Ryczko, M., Rossant, J., Rodriguez, T. A., & Kunath, T. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2011.10.013 · Cited by 87 · see citing works
Artus, J., Douvaras, P., Piliszek, A., Isern, J., Baron, M. H., & Hadjantonakis, A.-K. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2011.10.015 · Cited by 83 · see citing works
Strizzi, L., Hardy, K. M., Margaryan, N. V., Hillman, D. W., Seftor, E. A., Chen, B., Geiger, X. J., Thompson, E. A., Lingle, W. L., Andorfer, C. A., et al. (2012) · Breast Cancer Research · doi:10.1186/bcr3185 · Cited by 66 · see citing works
A close look at the mammalian blastocyst: epiblast and primitive endoderm formation
Artus, J., & Chazaud, C. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1630-3 · Cited by 60 · see citing works
Deonovic, B., Wang, Y., Weirather, J. L., Wang, X., & Au, K. F. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw1076 · Cited by 54 · see citing works
Actl6a Protects Embryonic Stem Cells From Differentiating Into Primitive Endoderm
Lu, W., Fang, L., Ouyang, B., Zhang, X., Zhan, S., Feng, X., Bai, Y., Han, X., Kim, H., He, Q., et al. (2015) · Stem Cells · doi:10.1002/stem.2000 · Cited by 48 · see citing works
Primitive endoderm differentiation: from specification to epithelium formation
Hermitte, S., & Chazaud, C. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0537 · Cited by 47 · see citing works
Primitive Endoderm Differentiation: From Specification to Epithelialization
Bassalert, C., Estrella, L. V., & Chazaud, C. (2018) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2017.12.001 · Cited by 38 · see citing works
Karkampouna, S., van der Helm, D., Gray, P. C., Chen, L., Klima, I., Grosjean, J., Burgmans, M. C., Sarasqueta, A. F., Snaar-Jagalska, E. B., Stroka, D., et al. (2018) · The Journal of Pathology · doi:10.1002/path.5083 · Cited by 34 · see citing works
Self-citationVrij, E., Reimer, Y. S. O., Fuentes, L. R., Guerreiro, I. M., Holzmann, V., Frias-Aldeguer, J., Sestini, G., Koo, B., Kind, J., van Blitterswijk, C., et al. (2022) · Development · doi:10.1242/dev.192310 · Cited by 33 · see citing works
Zhang, P., Zhai, X., Huang, B., Sun, S., Wang, W., & Zhang, M. (2023) · Science China Life Sciences · doi:10.1007/s11427-022-2209-3 · Cited by 30 · see citing works
Roles of MicroRNAs in Establishing and Modulating Stem Cell Potential
Zhang, Z., Zhuang, L., & Lin, C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20153643 · Cited by 28 · see citing works
Soszyńska, A., Klimczewska, K., & Suwińska, A. (2019) · The International Journal of Developmental Biology · doi:10.1387/ijdb.180408as · Cited by 26 · see citing works
Hardy, K. M., Strizzi, L., Margaryan, N. V., Gupta, K., Murphy, G. F., Scolyer, R. A., & Hendrix, M. J. C. (2015) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-14-0077 · Cited by 24 · see citing works
Extraembryonic Endoderm cells as a model of endoderm development
Moerkamp, A. T., Paca, A., Goumans, M., Kunath, T., Kruithof, B. P. T., & Julio, M. K. (2013) · Development Growth & Differentiation · doi:10.1111/dgd.12036 · Cited by 22 · see citing works
Self-citationLaise, P., Turunen, M. M., Garcia, A. C., Tomassoni, L., Maurer, H. C., Elyada, E., Schmierer, B., Worley, J., Kesner, J. S., Tan, X., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.27.357269 · Cited by 21 · see citing works
Self-citationChuykin, I. A., Schulz, H., Guan, K., & Bäder, M. (2012) · Journal of Cell Science · doi:10.1242/jcs.110239 · Cited by 17 · see citing works
In vitro modeling of early mammalian embryogenesis
Hadjantonakis, A., Siggia, E. D., & Simunovic, M. (2020) · Current Opinion in Biomedical Engineering · doi:10.1016/j.cobme.2020.02.003 · Cited by 16 · see citing works
Meharwade, T., Joumier, L., Parisotto, M., Huynh, V., da Rocha, E. L., & Malleshaiah, M. K. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112438 · Cited by 14 · see citing works
Sousa, E. R., Zoni, E., Karkampouna, S., Manna, F. L., Gray, P. C., Menna, M. D., & Julio, M. K. (2020) · Cancers · doi:10.3390/cancers12061480 · Cited by 14 · see citing works
Self-citationIntrauterine hyperglycemia impairs endometrial receptivity via up-regulating SGK1 in diabetes
Xu, H., Li, J., Jin, L., Zhang, D., Chen, B., Liu, X., Lin, X.-H., Huang, Y., Ke, Z.-H., Liu, J., et al. (2022) · Science China Life Sciences · doi:10.1007/s11427-021-2035-2 · Cited by 12 · see citing works
Alvarez, M. J., Yan, P., Alpaugh, M. L., Bowden, M., Sicińska, E., Zhou, C. W., Karan, C., Realubit, R. B., Mundi, P. S., Grunn, A., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/677435 · Cited by 12 · see citing works
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Kelly, G. M., & Drysdale, T. A. (2015) · Journal of Developmental Biology · doi:10.3390/jdb3020025 · Cited by 12 · see citing works
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Binas, B., & Verfaillie, C. M. (2012) · Stem Cells · doi:10.1002/stem.1287 · Cited by 11 · see citing works
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Garg, V., Morgani, S. M., & Hadjantonakis, A. (2016) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2016.04.007 · Cited by 10 · see citing works
Liu, W., Brown, K., Legros, S., & Foley, A. C. (2012) · Biology Open · doi:10.1242/bio.2012038 · Cited by 11 · see citing works
Holzner, M., Sonicki, T., Hunn, H., Uliana, F., Jiang, W., Gade, V. R., Weis, K., Wutz, A., & Minin, G. D. (2024) · Cell Death and Differentiation · doi:10.1038/s41418-024-01435-x · Cited by 9 · see citing works
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Filimonow, K., & de la Fuente, R. (2021) · Theriogenology · doi:10.1016/j.theriogenology.2021.12.021 · Cited by 9 · see citing works
Laise, P., Stanifer, M. L., Bosker, G., Sun, X., Triana, S., Doldan, P., Manna, F. L., Menna, M. D., Realubit, R. B., Pampou, S., et al. (2022) · Communications Biology · doi:10.1038/s42003-022-03663-8 · Cited by 8 · see citing works
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Perera, M., & Brickman, J. M. (2023) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2023.102115 · Cited by 7 · see citing works
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Nowotschin, S., Setty, M. N., Kuo, Y.-Y., Lui, V. C. H., Garg, V., Sharma, R., Simon, C. S., Saiz, N., Gardner, R., Boutet, S. C., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/471078 · Cited by 7 · see citing works
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Perea-Gómez, A., & Meilhac, S. M. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-405945-0.00010-7 · Cited by 6 · see citing works
Garg, V., Yang, Y., Nowotschin, S., Setty, M. N., Kuo, Y.-Y., Sharma, R., Polyzos, A., Salataj, E., Murphy, D., Jang, A., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.03.28.534648 · Cited by 6 · see citing works
Zhong, Y., & Binas, B. (2019) · Genes to Cells · doi:10.1111/gtc.12678 · Cited by 5 · see citing works
Garg, V., Yang, Y., Nowotschin, S., Setty, M. N., Salataj, E., Kuo, Y.-Y., Murphy, D., Sharma, R., Jang, A., Polyzos, A., et al. (2024) · Developmental Cell · doi:10.1016/j.devcel.2024.11.022 · Cited by 9 · see citing works
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Arboretto, P., Cillo, M., & Leonardi, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22157838 · Cited by 4 · see citing works
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Tang, P. W., Miri, K., & Varmuza, S. (2019) · Biology Open · doi:10.1242/bio.043638 · Cited by 4 · see citing works
Mitotic bookmarking by transcription factors and the preservation of pluripotency
Owens, N. D. L., González, I., Artus, J., & Navarro, P. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814085-7.00006-4 · Cited by 3 · see citing works
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Julio, M. K., Alvarez, M. J., Galli, A., Chu, J., Price, S. M., Califano, A., & Shen, M. M. (2011) · Journal of Cell Science · doi:10.1242/jcs.098848 · Cited by 3 · see citing works
Self-citationZhang, P., Zhai, X., Huang, B., Sun, S., Wang, W., & Zhang, M. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.03.01.481880 · Cited by 3 · see citing works
Meharwade, T., Joumier, L., Parisotto, M., Huynh, V., da Rocha, E. L., & Malleshaiah, M. K. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.04.15.488509 · Cited by 3 · see citing works
Heterotaxy polysplenia syndrome with cholangiopancreatic cancer: a case report and literature review
Chen, Z., Chen, Y.-A., Wang, X., Song, W., Geng, Y., Wang, P., Kong, S., Dong, J., Bai, H., & Wang, Y. (2025) · Frontiers in Medicine · doi:10.3389/fmed.2025.1537227 · Cited by 2 · see citing works
Generation of Mouse Primitive Endoderm Stem Cells
Ohinata, Y., Saraya, A., & Koseki, H. (2023) · BIO-PROTOCOL · doi:10.21769/bioprotoc.4878 · Cited by 1 · see citing works
First Cell Fate Decisions in Early Development
Hemberger, M., & Dean, W. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-394445-0.00008-4 · Cited by 1 · see citing works
Tirado, G. P. (2002) · Dialnet (Universidad de la Rioja) · Cited by 1 · see citing works
Stem Cells from Early Mammalian Embryos
Hadjantonakis, A., Gavrilov, S., Xenopoulos, P., & Papaioannou, V. E. (2013) · Springer eBooks · doi:10.1007/978-1-4614-7696-2_3
Laise, P., Stanifer, M. L., Bosker, G., Sun, X., Triana, S., Doldan, P., Manna, F. L., Menna, M. D., Realubit, R. B., Pampou, S., et al. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3904344
Self-citationLaise, P., Stanifer, M. L., Bosker, G., Sun, X., Triana, S., Doldan, P., Manna, F. L., Menna, M. D., Realubit, R. B., Pampou, S., et al. (2022) · Research Square · doi:10.21203/rs.3.rs-1287631/v1
Self-citationIn vitro models of human blastocysts and early embryogenesis
Tan, J. P., Liu, X., & Polo, J. M. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-91380-5.00001-0
The vertebrate yolk sac: evolutionary origins and current advances in in vitro models
Blagrove, J. R., Orsi, A. E. R., Cindrová‐Davies, T., & Niakan, K. K. (2026) · Development · doi:10.1242/dev.205384
A primitive endoderm-centric view of mammalian development
Kim, R., Faerberg, D. F., & Pósfai, E. (2026) · Development · doi:10.1242/dev.205485
- Authors
- Julio, M. K.-D., Alvarez, M. J., Galli, A., Chu, J., Price, S. M., Califano, A., & Shen, M. M.
- Affiliations
- Columbia University Irving Medical Center (US)
- University of Medicine and Dentistry of New Jersey (US)
- Corresponding author
- Shen, Michael M.
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2011-09-15
- Volume
- 138
- Issue
- 18
- Pages
- 3885-3895
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- PMC
- PMC3160087
- OpenAlex
- W2141775956
- Cited by
- 62
- References
- 63
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 3 · 2023: 6 · 2022: 6 · 2021: 4 · 2020: 4 · 2019: 6 · 2018: 4 · 2017: 4 · 2016: 2 · 2015: 3 · 2014: 3 · 2013: 5 · 2012: 5
- FWCI
- 2.08
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Development (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD42837, R01HD042837)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
- Keywords
- Nodal signaling, Cripto, TDGF1, visceral endoderm, anterior visceral endoderm, primitive endoderm, peri-implantation embryo, chimeric embryos, SB431542, TGF-beta superfamily, cell fate specification
- MeSH terms
- Animals, Cell Differentiation, Cell Line, Embryo, Mammalian, Endoderm, Epidermal Growth Factor, Female, Extraembryonic Membranes, Membrane Glycoproteins, Mice, Inbred ICR, Mice, Transgenic, Neoplasm Proteins, Pregnancy, Signal Transduction, Gene Expression Profiling, Microarray Analysis, Mice, Embryonic Stem Cells, Nodal Protein
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