Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo

Arnold, Sebastian J.; Robertson, Elizabeth J.

doi:10.1038/nrm2618

Cited by 816Developmental Biology and Gene RegulationPluripotent Stem Cells ResearchReproductive Biology and Fertility

Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo

Arnold, Sebastian J., Robertson, Elizabeth J.·2009·Nature Reviews Molecular Cell Biology

DOI 10.1038/nrm2618

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Abstract

Genetic studies have identified the key signalling pathways and developmentally regulated transcription factors that govern cell lineage allocation and axis patterning in the early mammalian embryo. Recent advances have uncovered details of the molecular circuits that tightly control cell growth and differentiation in the mammalian embryo from the blastocyst stage, through the establishment of initial anterior-posterior polarity, to gastrulation, when the germ cells are set aside and the three primary germ layers are specified. Relevant studies in lower vertebrates indicate the conservation and divergence of regulatory mechanisms for cell lineage allocation and axis patterning.

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EPI descendants resembled embryonic VE (emVE) and anterior visceral endoderm (AVE), based on expression of markers including Lefty1, Cer1 and Hhex.
“Expression of markers of embryonic (em)VE, and anterior visceral endoderm (AVE), a specialized cellular cohort of emVE exhibiting an intra-epithelial, distal-to-anterior migratory behavior between E5.5 and E6.0, including Lefty1, Cer1 and Hhex30–32, suggested these EPI descendants resembled emVE and AVE (Fig. 2c, Extended Data Fig. 6e)33.”
From The emergent landscape of the mouse gut endoderm at single-cell resolution (2019) · cites this paper as [33]
The early post-implantation (E5.5) mouse embryo is radially symmetrical, and the VE appears morphologically uniform around its proximal-distal axis.
“The early post-implantation (E5.5, Fig. 1) mouse embryo is radially symmetrical, and the VE appears morphologically uniform around its proximal-distal axis4,33.”
From The emergent landscape of the mouse gut endoderm at single-cell resolution (2019) · cites this paper as [33]

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The amniote primitive streak is defined by epithelial cell intercalation before gastrulation
Voiculescu, O., Bertocchini, F., Wolpert, L., Keller, R. E., & Stern, C. D. (2007) · Nature · doi:10.1038/nature06211 · Cited by 262 · see citing works
Germ Cell Specification in Mice
Hayashi, K., Lopes, S. M. C. D. S., & Surani, M. A. (2007) · Science · doi:10.1126/science.1137545 · Cited by 258 · see citing works
Nodal specifies embryonic visceral endoderm and sustains pluripotent cells in the epiblast before overt axial patterning
Mesnard, D., Guzman-Ayala, M., & Constam, D. B. (2006) · Development · doi:10.1242/dev.02413 · Cited by 252 · see citing works
p38 and a p38-Interacting Protein Are Critical for Downregulation of E-Cadherin during Mouse Gastrulation
Zohn, I. E., Li, Y., Skolnik, E. Y., Anderson, K. V., Han, J., & Niswander, L. A. (2006) · Cell · doi:10.1016/j.cell.2006.03.048 · Cited by 249 · 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 240 · see citing works
Self-citation
From fertilization to gastrulation: axis formation in the mouse embryo
Lu, C. C., Brennan, J., & Robertson, E. J. (2001) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00208-2 · Cited by 238 · see citing works
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Left–Right Asymmetric Expression of lefty2 and nodal Is Induced by a Signaling Pathway that Includes the Transcription Factor FAST2
Saijoh, Y., Adachi, H., Sakuma, R., et al. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)80401-3 · Cited by 236 · see citing works
Establishment of endoderm progenitors by SOX transcription factor expression in human embryonic stem cells.
Séguin, C., Draper, J., Nagy, A., & Rossant, J. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2008.06.018 · Cited by 229 · see citing works
Differential requirements for Smad4 in TGFβ-dependent patterning of the early mouse embryo
Chu, G. C., Dunn, N. R., Anderson, D. C., Oxburgh, L. H., & Robertson, E. J. (2004) · Development · doi:10.1242/dev.01248 · Cited by 226 · see citing works
Self-citation
IFITM/Mil/Fragilis Family Proteins IFITM1 and IFITM3 Play Distinct Roles in Mouse Primordial Germ Cell Homing and Repulsion
Tanaka, S., Yamaguchi, Y. L., Tsoi, B., Lickert, H., & Tam, P. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.10.010 · Cited by 222 · see citing works
The transcription factor FoxH1 (FAST) mediates Nodal signaling during anterior-posterior patterning and node formation in the mousePreprint
Yamamoto, M., Meno, C., Sakai, Y., Shiratori, H., Mochida, K., Ikawa, Y., Saijoh, Y., & Hamada, H. (2001) · Genes & Development · doi:10.1101/gad.883901 · Cited by 219 · see citing works
The type I activin receptor ActRIB is required for egg cylinder organization and gastrulation in the mousePreprint
Gu, Z., Nomura, M., Simpson, B. B., Lei, H., Feijen, A., Raaij, J. V. D. E.-V., Donahoe, P. K., & Li, E. (1998) · Genes & Development · doi:10.1101/gad.12.6.844 · Cited by 219 · see citing works
Loss of the extraembryonic ectoderm in Elf5 mutants leads to defects in embryonic patterning
Donnison, M. J., Beaton, A., Davey, H. W., Broadhurst, R. B., L'Huillier, P. J., & Pfeffer, P. (2005) · Development · doi:10.1242/dev.01819 · Cited by 213 · see citing works
Absence of Nodal signaling promotes precocious neural differentiation in the mouse embryo
Camus, A., Perea-Gómez, A., Moreau, A., & Collignon, J. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.03.047 · Cited by 209 · see citing works
Smad5 is required for mouse primordial germ cell development
Chang, H., & Matzuk, M. M. (2001) · Mechanisms of Development · doi:10.1016/s0925-4773(01)00367-7 · Cited by 207 · see citing works
FoxH1(Fast) functions to specify the anterior primitive streak in the mouse
Hoodless, P. A., Pye, M., Chazaud, C., Labbé, E., Attisano, L., Rossant, J., & Wrana, J. L. (2001) · Genes & Development · doi:10.1101/gad.881501 · Cited by 203 · see citing works
Mesp1 Coordinately Regulates Cardiovascular Fate Restriction and Epithelial-Mesenchymal Transition in Differentiating ESCs
Lindsley, R. C., Gill, J. G., MURPHY, K. M. M., et al. (2008) · Cell stem cell · doi:10.1016/j.stem.2008.04.004 · Cited by 198 · see citing works
Asymmetric and node-specific nodal expression patterns are controlled by two distinct cis-acting regulatory elements.Preprint
Norris, D. P., & Robertson, E. J. (1999) · Genes & Development · doi:10.1101/gad.13.12.1575 · Cited by 196 · see citing works
Self-citation
Canonical Wnt Signaling and Its Antagonist Regulate Anterior-Posterior Axis Polarization by Guiding Cell Migration in Mouse Visceral Endoderm
Kimura-Yoshida, C., Nakano, H., Okamura, D., Nakao, K., Yonemura, S., Belo, J. A., Aizawa, S., Matsui, Y., & Matsuo, I. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.09.011 · Cited by 193 · see citing works
BMP signaling mediated by ALK2 in the visceral endoderm is necessary for the generation of primordial germ cells in the mouse embryoPreprint
Lopes, S. M. C. D. S., Roelen, B. A. J., Monteiro, R. M., Emmens, R., Lin, H. Y.-F., Li, E., Lawson, K. A., & Mummery, C. L. (2004) · Genes & Development · doi:10.1101/gad.294004 · Cited by 189 · 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
Combinatorial activities of Smad2 and Smad3 regulate mesoderm formation and patterning in the mouse embryo
Dunn, N. R., Vincent, S. D., Oxburgh, L. H., et al. (2004) · Development · doi:10.1242/dev.01072 · Cited by 184 · see citing works
Self-citation
Sdf1/Cxcr4 signaling controls the dorsal migration of endodermal cells during zebrafish gastrulation
Mizoguchi, T., Verkade, H. M., Heath, J. K., Kuroiwa, A., & Kikuchi, Y. (2008) · Development · doi:10.1242/dev.020107 · Cited by 182 · see citing works
Live Imaging and Genetic Analysis of Mouse Notochord Formation Reveals Regional Morphogenetic Mechanisms
Yamanaka, Y., Tamplin, O. J., Beckers, A., Gossler, A., & Rossant, J. (2007) · Developmental Cell · doi:10.1016/j.devcel.2007.10.016 · Cited by 182 · see citing works
Formation of the definitive endoderm in mouse is a Smad2-dependent process
Tremblay, K. D., Hoodless, P. A., Bikoff, E. K., & Robertson, E. J. (2000) · Development · doi:10.1242/dev.127.14.3079 · Cited by 178 · see citing works
Self-citation
Clonal Analysis of Cell Fate During Gastrulation and Early Neurulation in the Mouse
Lawson, K. A., & Pedersen, R. A. (2007) · Novartis Foundation symposium · doi:10.1002/9780470514221.ch2 · Cited by 177 · see citing works
Sox17 is essential for the specification of cardiac mesoderm in embryonic stem cells
Liu, Y., Asakura, M., Inoue, H., Nakamura, T., Sano, M., Niu, Z., Chen, M. M., Schwartz, R. J., & Schneider, M. D. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609100104 · Cited by 170 · see citing works
Dose-dependent Smad1, Smad5 and Smad8 signaling in the early mouse embryo
Arnold, S. J., Maretto, S., Islam, A., Bikoff, E. K., & Robertson, E. J. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.04.442 · Cited by 163 · see citing works
Self-citation
BMP signalling inhibits premature neural differentiation in the mouse embryo
Gregorio, A. D., Sancho, M., Stuckey, D. W., Crompton, L., Godwin, J., Mishina, Y. M., & Rodríguez, T. A. (2007) · Development · doi:10.1242/dev.005967 · Cited by 159 · see citing works
Nodal protein processing and fibroblast growth factor 4 synergize to maintain a trophoblast stem cell microenvironment
Guzman-Ayala, M., Ben-Haim, N., Beck, S., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405429101 · Cited by 156 · see citing works
Induction and migration of the anterior visceral endoderm is regulated by the extra-embryonic ectoderm
Rodríguez, T. A., Srinivas, S., Clements, M., Smith, J. C., & Beddington, R. S. P. (2005) · Development · doi:10.1242/dev.01847 · Cited by 154 · see citing works
Epidermal terminal differentiation depends on B lymphocyte-induced maturation protein-1
Magnúsdóttir, E., Kalachikov, S., Mizukoshi, K., Savitsky, D., Ishida-Yamamoto, A., Panteleyev, A. A., & Calame, K. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707323104 · Cited by 152 · see citing works
Misexpression of Cwnt8C in the mouse induces an ectopic embryonic axis and causes a truncation of the anterior neuroectoderm
Pöpperl, H., Schmidt, C., Wilson, V. A., Hume, R. C., Dodd, J., Krumlauf, R. K., & Beddington, R. S. P. (1997) · Development · doi:10.1242/dev.124.15.2997 · Cited by 148 · see citing works
Dppa3 / Pgc7 / stella is a maternal factor and is not required for germ cell specification in mice
Bortvin, A. L., Goodheart, M. L., Liao, M., & Page, D. C. (2004) · BMC Developmental Biology · doi:10.1186/1471-213x-4-2 · Cited by 145 · see citing works
Otx2 is required for visceral endoderm movement and for the restriction of posterior signals in the epiblast of the mouse embryo
Perea-Gómez, A., Lawson, K. A., Rhinn, M., Zakin, L., Brûlet, P., Mazan, S., & Ang, S. (2001) · Development · doi:10.1242/dev.128.5.753 · Cited by 145 · see citing works
HNF3β and Lim1 interact in the visceral endoderm to regulate primitive streak formation and anterior-posterior polarity in the mouse embryo
Perea-Gómez, A., Shawlot, W., Sasaki, H., Behringer, R. R., & Ang, S. (1999) · Development · doi:10.1242/dev.126.20.4499 · Cited by 135 · see citing works
Immune and nervous system CXCL12 and CXCR4: parallel roles in patterning and plasticity
Klein, R. S., & Rubin, J. B. (2004) · Trends in Immunology · doi:10.1016/j.it.2004.04.002 · Cited by 132 · see citing works
Blimp1 regulates development of the posterior forelimb, caudal pharyngeal arches, heart and sensory vibrissae in mice
Robertson, E. J., Charatsi, I., Joyner, C. J., Koonce, C. H., Morgan, M., Islam, A., Paterson, C. A., Lejsek, E., Arnold, S. J., Kallies, A., et al. (2007) · Development · doi:10.1242/dev.012047 · Cited by 129 · see citing works
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Normal Germ Line Establishment in Mice Carrying a Deletion of the Ifitm/Fragilis Gene Family Cluster
Lange, U. C., Adams, D. J., Lee, C. Y., et al. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.00272-08 · Cited by 128 · see citing works
Inactivation of the FGF-4 Gene in Embryonic Stem Cells Alters the Growth and/or the Survival of Their Early Differentiated Progeny
Wilder, P. J., Kelly, D., Brigman, K., Peterson, C. L., Nowling, T. K., Gao, Q.-S., McComb, R. D., Capecchi, M. R., & Rizzino, A. (1997) · Developmental Biology · doi:10.1006/dbio.1997.8777 · Cited by 128 · see citing works
TGF-β signaling-mediated morphogenesis: modulation of cell adhesion via cadherin endocytosisPreprint
Ogata, S., Morokuma, J., Hayata, T., Kolle, G., Niehrs, C., Ueno, N., & Cho, K. W. Y. (2007) · Genes & Development · doi:10.1101/gad.1541807 · Cited by 125 · see citing works
Induction of the mammalian node requires Arkadia function in the extraembryonic lineages
Episkopou, V., Arkell, R. M., Timmons, P. M., Walsh, J. J., Andrew, R. L., & Swan, D. (2001) · Nature · doi:10.1038/35071095 · Cited by 110 · see citing works
Dynamic expression of Lrp2 pathway members reveals progressive epithelial differentiation of primitive endoderm in mouse blastocyst
Gerbe, F., Cox, B., Rossant, J., & Chazaud, C. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.10.048 · Cited by 109 · see citing works
Multiple roles for Nodal in the epiblast of the mouse embryo in the establishment of anterior-posterior patterning
Lu, C. C., & Robertson, E. J. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.06.004 · Cited by 107 · see citing works
Self-citation
Axis specification and morphogenesis in the mouse embryo requireNap1, a regulator of WAVE-mediated actin branching
Rakeman, A. S., & Anderson, K. V. (2006) · Development · doi:10.1242/dev.02473 · Cited by 107 · see citing works
Dkk1andWnt3interact to control head morphogenesis in the mouse
Lewis, S. L., Khoo, P., Young, R. A. D., Steiner, K. A., Wilcock, C. C., Mukhopadhyay, M., Westphal, H., Jamieson, R. V., Robb, L., & Tam, P. (2008) · Development · doi:10.1242/dev.018853 · Cited by 105 · see citing works
Complete dissipation of coherent clonal growth occurs before gastrulation in mouse epiblast
Gardner, R. L., & Cockroft, D. L. (1998) · Development · doi:10.1242/dev.125.13.2397 · Cited by 98 · see citing works
Disruption of early proximodistal patterning and AVE formation in Apc mutants
Chazaud, C., & Rossant, J. (2006) · Development · doi:10.1242/dev.02523 · Cited by 97 · see citing works
Arkadia Enhances Nodal/TGF-β Signaling by Coupling Phospho-Smad2/3 Activity and Turnover
Mavrakis, K. J., Andrew, R. L., Lee, K. L., Petropoulou, C., Dixon, J. E., Navaratnam, N., Norris, D. P., & Episkopou, V. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050067 · Cited by 94 · see citing works
Mesodermal patterning defect in mice lacking the Ste20 NCK interacting kinase (NIK)
Xue, Y., Wang, X., Li, Z., Gotoh, N., Chapman, D. L., & Skolnik, E. Y. (2001) · Development · doi:10.1242/dev.128.9.1559 · Cited by 93 · see citing works
Evolution of the mechanisms and molecular control of endoderm formation
Grapin‐Botton, A., & Constam, D. B. (2007) · Mechanisms of Development · doi:10.1016/j.mod.2007.01.001 · Cited by 89 · see citing works
Inner cell allocation in the mouse morula: The role of oriented division during fourth cleavage
Sutherland, A. E., Speed, T. P., & Calarco, P. G. (1990) · Developmental Biology · doi:10.1016/0012-1606(90)90003-2 · Cited by 84 · see citing works
Ets2 is necessary in trophoblast for normal embryonic anteroposterior axis development
Georgiades, P., & Rossant, J. (2006) · Development · doi:10.1242/dev.02277 · Cited by 80 · see citing works
Arkadia enhances nodal-related signalling to induce mesendoderm
Niederländer, C., Walsh, J. J., Episkopou, V., et al. (2001) · Nature · doi:10.1038/35071103 · Cited by 75 · see citing works
Fate mapping the mouse embryo
Lawson, K. A. (1999) · The International Journal of Developmental Biology · doi:10.1387/ijdb.10668985 · Cited by 66 · see citing works
Ventral closure, headfold fusion and definitive endoderm migration defects in mouse embryos lacking the fibronectin leucine-rich transmembrane protein FLRT3
Maretto, S., Müller, P.-S., Aricescu, A. R., Cho, K. W. Y., Bikoff, E. K., & Robertson, E. J. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.03.021 · Cited by 61 · see citing works
Self-citation
A mechanism for the sharp transition of morphogen gradient interpretation in Xenopus
Saka, Y., & Smith, J. C. (2007) · BMC Developmental Biology · doi:10.1186/1471-213x-7-47 · Cited by 54 · see citing works
Genome-Wide Identification of Smad/Foxh1 Targets Reveals a Role for Foxh1 in Retinoic Acid Regulation and Forebrain Development
Silvestri, C., Narimatsu, M., von Both, I., Liu, Y., Tan, N. B. J., Izzi, L., McCaffery, P. J. A., Wrana, J. L., & Attisano, L. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.01.004 · Cited by 54 · see citing works
Crucial roles of Foxa2 in mouse anterior–posterior axis polarization via regulation of anterior visceral endoderm-specific genes
Kimura-Yoshida, C., Tian, E., Nakano, H., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607779104 · Cited by 53 · see citing works
Proximal visceral endoderm and extraembryonic ectoderm regulate the formation of primordial germ cell precursors
Lopes, S. M. C. D. S., Hayashi, K., & Surani, M. A. (2007) · BMC Developmental Biology · doi:10.1186/1471-213x-7-140 · Cited by 52 · see citing works
One-eyed pinhead regulates cell motility independent of Squint/Cyclops signaling
Warga, R. M., & Kane, D. A. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00328-2 · Cited by 49 · see citing works
Origin of body axes in the mouse embryo
Takaoka, K., Yamamoto, M., & Hamada, H. (2007) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2007.06.001 · Cited by 46 · see citing works
SDF-1α regulates mesendodermal cell migration during frog gastrulation
Fukui, A., Goto, T., Kitamoto, J., et al. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.01.007 · Cited by 40 · see citing works
Regulation of the Xenopus Xsox17α1 promoter by co-operating VegT and Sox17 sites
Howard, L., Rex, M., Clements, D., et al. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.07.028 · Cited by 22 · see citing works

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Building Muscle: Molecular Regulation of MyogenesisPreprint
Bentzinger, C. F., Wang, Y. X., & Rudnicki, M. A. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a008342 · Cited by 1,198 · see citing works
A method to recapitulate early embryonic spatial patterning in human embryonic stem cells
Warmflash, A., Sorre, B., Etoc, F., Siggia, E. D., & Brivanlou, A. H. (2014) · Nature Methods · doi:10.1038/nmeth.3016 · Cited by 885 · see citing works
Molecular Signals of Epigenetic States
Bonasio, R., Tu, S., & Reinberg, D. (2010) · Science · doi:10.1126/science.1191078 · Cited by 912 · see citing works
The Crumbs Complex Couples Cell Density Sensing to Hippo-Dependent Control of the TGF-β-SMAD Pathway
Varelas, X., Samavarchi‐Tehrani, P., Narimatsu, M., Weiss, A., Cockburn, K., Larsen, B. G., Rossant, J., & Wrana, J. L. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.11.012 · Cited by 683 · see citing works
Production of de novo cardiomyocytes: human pluripotent stem cell differentiation and direct reprogramming
Burridge, P. W., Keller, G., Gold, J. D., & Wu, J. C. (2012) · Cell Stem Cell · doi:10.1016/j.stem.2011.12.013 · Cited by 670 · see citing works
“Cardiomyogenesis begins with the generation of mesoderm via the process of gastrulation, which has been best studied in the mouse (Arnold and Robertson, 2009; Buckingham et al., 2005; Tam and Loebel, 2007) (Figure 1).”
Skeletal muscle: A review of molecular structure and function, in health and disease
Mukund, K., & Subramaniam, S. (2019) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1462 · Cited by 680 · see citing works
“The positions and identities of cells that will form the three germ layers (ectoderm, mesoderm, and endoderm) are determined early in gestation (S. J. Arnold & Robertson, 2009).”
Background
The TGFbeta Superfamily Signaling Pathway
Weiss, A., & Attisano, L. (2012) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.86 · Cited by 563 · see citing works
TGF-β orchestrates fibrogenic and developmental EMTs via the RAS effector RREB1
Su, J., Morgani, S. M., David, C. J., Wang, Q., Er, E. E., Huang, Y.-H., Basnet, H., Zou, Y., Shu, W., Soni, R. K., et al. (2020) · Nature · doi:10.1038/s41586-019-1897-5 · Cited by 498 · see citing works
Mechanisms of early placental development in mouse and humans
Hemberger, M., Hanna, C. W., & Dean, W. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-019-0169-4 · Cited by 492 · see citing works
Single-cell transcriptomic characterization of a gastrulating human embryo
Tyser, R. C. V., Mahammadov, E., Nakanoh, S., Vallier, L., Scialdone, A., & Srinivas, S. (2021) · Nature · doi:10.1038/s41586-021-04158-y · Cited by 467 · see citing works
Symmetry breaking, germ layer specification and axial organisation in aggregates of mouse embryonic stem cells
van den Brink, S., Baillie‐Johnson, P., Balayo, T., Hadjantonakis, A., Nowotschin, S., Turner, D. A., & Arias, A. M. (2014) · Development · doi:10.1242/dev.113001 · Cited by 461 · see citing works
“Signalling and pattern formation during aggregate differentiation In the early postimplantation epiblast, cell fate assignments are triggered by interactions between BMP, Nodal, Wnt signalling and their antagonists, and lead to the partitioning of the embryo into anterior neuroectodermal and posterior mesendodermal po…”
Influential
Assembly of embryonic and extraembryonic stem cells to mimic embryogenesis in vitro
Harrison, S., Sözen, B., Christodoulou, N., Kyprianou, C., & Zernicka‐Goetz, M. (2017) · Science · doi:10.1126/science.aal1810 · Cited by 393 · see citing works
Developmental barcoding of whole mouse via homing CRISPR
Kalhor, R., Kalhor, K., Mejia, L., Leeper, K., Graveline, A., Mali, P., & Church, G. M. (2018) · Science · doi:10.1126/science.aat9804 · Cited by 363 · see citing works
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
Beyond TGFβ: roles of other TGFβ superfamily members in cancer
Wakefield, L. M., & Hill, C. S. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3500 · Cited by 373 · see citing works
Integration of spatial and single-cell transcriptomic data elucidates mouse organogenesis
Lohoff, T., Ghazanfar, S., Missarova, A. M., Koulena, N., Pierson, N. G., Griffiths, J. A., Bardot, E., Eng, C.-H. L., Tyser, R. C. V., Argelaguet, R., et al. (2021) · Nature Biotechnology · doi:10.1038/s41587-021-01006-2 · Cited by 349 · see citing works
A Balance between Secreted Inhibitors and Edge Sensing Controls Gastruloid Self-Organization
Etoc, F., Metzger, J. J., Ruzo, A., Kirst, C., Yoney, A., Ozair, M. Z., Brivanlou, A. H., & Siggia, E. D. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.09.016 · Cited by 343 · see citing works
“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript NOGGIN as a direct BMP target; CHX cyclohexamide, SB and IWP2 respectively inhibit Activin/Nodal and Wnt signaling.”
BackgroundInfluential
Pluripotency factors regulate definitive endoderm specification through eomesoderminPreprint
Teo, A. K. K., Arnold, S. J., Trotter, M. W. B., Brown, S. E., Ang, L. T., Chng, Z., Robertson, E. J., Dunn, N. R., & Vallier, L. (2011) · Genes & Development · doi:10.1101/gad.607311 · Cited by 338 · see citing works
Self-citation
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McCauley, H. A., & Wells, J. M. (2017) · Development · doi:10.1242/dev.140731 · Cited by 322 · see citing works
The Germ Cell Fate of Cynomolgus Monkeys Is Specified in the Nascent Amnion
Sasaki, K., Nakamura, T., Okamoto, I., Yabuta, Y., Iwatani, C., Tsuchiya, H., Seita, Y., Nakamura, S., Shiraki, N., Takakuwa, T., et al. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.09.007 · Cited by 311 · see citing works
Germ cell specification in mice
Saitou, M. (2009) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2009.06.003 · Cited by 301 · see citing works
Transposable elements shape the evolution of mammalian development
Senft, A. D., & Macfarlan, T. S. (2021) · Nature Reviews Genetics · doi:10.1038/s41576-021-00385-1 · Cited by 276 · see citing works
Maintaining embryonic stem cell pluripotency with Wnt signaling
Sokol, S. Y. (2011) · Development · doi:10.1242/dev.066209 · Cited by 257 · see citing works
“This is achieved primarily by cell-cell interactions mediated by the bone morphogenetic protein (BMP), fibroblast growth factor (FGF), Nodal and Wnt pathways, which constitute the major embryonic signaling pathways, the precise functions of which are still under investigation (Arnold and Robertson, 2009; Conlon et al.…”
BackgroundInfluential
Early patterning and specification of cardiac progenitors in gastrulating mesoderm
Devine, W. P., Wythe, J. D., George, M., Koshiba‐Takeuchi, K., & Bruneau, B. G. (2014) · eLife · doi:10.7554/elife.03848 · Cited by 247 · see citing works
“At least two sets of molecularly and morphologically distinct cardiac precursors have been identified in the mammalian embryo, referred to as the first and second heart fields; these populations contribute to distinct anatomical structures within the heart (Evans et al., 2010; Buckingham et al.,…”
Background
Nodal MorphogensPreprint
Schier, A. F. (2009) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a003459 · Cited by 251 · see citing works
New Insights into Early Human Development: Lessons for Stem Cell Derivation and Differentiation
Rossant, J., & Tam, P. (2017) · Cell stem cell · doi:10.1016/j.stem.2016.12.004 · Cited by 251 · see citing works
“In both embryos, the EPI is remodeled by cavitation and polarization, accompanied by rosette formation (Bedzhov and Zernicka-Goetz, 2014; Shahbazi et al., 2016), to an epithelial layer with a central lumen.”
“You Shall Not Pass”—tight junctions of the blood brain barrier
Bauer, H., Krizbai, I. A., Bauer, H., & Traweger, A. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00392 · Cited by 240 · see citing works
“…on embryonic axis establishment and blastocyst lineage formation is beyond the scope of this review and the reader is referred to a series of excellent reviews (Larue et al., 1994; Arnold and Robertson, 2009; Rossant and Tam, 2009; Morris and Zernicka-Goetz, 2012; Takaoka and Hamada, 2012).”
Background
The T-box transcription factor Eomesodermin acts upstream of Mesp1 to specify cardiac mesoderm during mouse gastrulation
Costello, I., Pimeisl, I., Dräger, S., Bikoff, E. K., Robertson, E. J., & Arnold, S. J. (2011) · Nature Cell Biology · doi:10.1038/ncb2304 · Cited by 241 · see citing works
“Much has been learned about the coordinated activities of key regulatory networks of transcription factors and growth-factor signalling pathways governing cell-fate decisions during gastrulatio”
BackgroundSelf-citation
The Many Faces of Neuroendocrine Differentiation in Prostate Cancer Progression
Terry, S., & Beltran, H. (2014) · Frontiers in Oncology · doi:10.3389/fonc.2014.00060 · Cited by 238 · see citing works
Distinct Wnt-driven primitive streak-like populations reflect in vivo lineage precursors
Tsakiridis, A., Huang, Y., Blin, G., Skylaki, S., Wymeersch, F. J., Osorno, R., Economou, C. N., Karagianni, E., Zhao, S., Lowell, S., et al. (2014) · Development · doi:10.1242/dev.101014 · Cited by 230 · see citing works
“, 1991) by localised signalling cues and is reflected by the regionalised expression of lineage-specific markers (Pfister et al., 2007; Arnold and Robertson, 2009; Teo et al., 2011).”
BackgroundInfluential
Spatial Transcriptome for the Molecular Annotation of Lineage Fates and Cell Identity in Mid-gastrula Mouse Embryo
Peng, G., Suo, S., Chen, J., Chen, W., Liu, C. X., Fang, Y., Wang, R., Chen, S., Sun, N., Cui, G., et al. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.02.020 · Cited by 235 · see citing works
“…and the choreography of switches in genetic and signaling activity that may drive lineage specification and tissue modeling in the embryo (Arnold and Robertson, 2009; Kojima et al., 2014b; Pfister et al., 2007; Solnica-Krezel and Sepich, 2012; Tam and Behringer, 1997; Tam and Loebel,…”
BackgroundInfluential
Molecular architecture of lineage allocation and tissue organization in early mouse embryo
Peng, G., Suo, S., Cui, G., Yu, F., Wang, R., Chen, J., Chen, S., Liu, Z., Chen, G., Qian, Y., et al. (2019) · Nature · doi:10.1038/s41586-019-1469-8 · Cited by 230 · see citing works
Complete human day 14 post-implantation embryo models from naive ES cells
Oldak, B., Wildschutz, E., Bondarenko, V., Comar, M.-Y., Zhao, C., Aguilera-Castrejon, A., Tarazi, S., Viukov, S. V., Pham, T. X. A., Ashouokhi, S., et al. (2023) · Nature · doi:10.1038/s41586-023-06604-5 · Cited by 232 · see citing works
Bioengineering Approaches for the Advanced Organoid Research
Yi, S. A., Zhang, Y., Rathnam, C., Pongkulapa, T., & Lee, K. (2021) · Advanced Materials · doi:10.1002/adma.202007949 · Cited by 218 · see citing works
TET-mediated DNA demethylation controls gastrulation by regulating Lefty-Nodal signalling
Dai, H.-Q., Wang, B.-A., Yang, L., Chen, J.-J., Zhu, G.-C., Sun, M.-L., Ge, H., Wang, R., Chapman, D. L., Tang, F., et al. (2016) · Nature · doi:10.1038/nature20095 · Cited by 206 · see citing works
Single cell transcriptome analysis of human, marmoset and mouse embryos reveals common and divergent features of preimplantation development
Boroviak, T., Stirparo, G. G., Dietmann, S., Hernando-Herraez, I., Mohammed, H., Reik, W., Smith, A. G., Sasaki, E., Nichols, J., & Bertone, P. (2018) · Development · doi:10.1242/dev.167833 · Cited by 216 · see citing works
“The amnion is specified via the amniochorionic fold during gastrulation (Arnold and Robertson, 2009; Rossant and Tam, 2009; Pereira et al., 2011).”
Background
A single-embryo, single-cell time-resolved model for mouse gastrulation
Mittnenzweig, M., Mayshar, Y., Cheng, S., Ben-Yair, R., Hadas, R., Rais, Y., Chomsky, E., Reines, N., Uzonyi, A., Lumerman, L., et al. (2021) · Cell · doi:10.1016/j.cell.2021.04.004 · Cited by 214 · see citing works
Dynamic epigenomic landscapes during early lineage specification in mouse embryos
Zhang, Y., Xiang, Y., Yin, Q., Du, Z., Xu, P., Wang, Q., Fidalgo, M., Xia, W., Li, Y., Zhao, Z., et al. (2017) · Nature Genetics · doi:10.1038/s41588-017-0003-x · Cited by 210 · see citing works
Sequence-specific regulator Prdm14 safeguards mouse ESCs from entering extraembryonic endoderm fates
Ma, Z., Swigut, T., Valouev, A., Rada-Iglesias, Á., & Wysocka, J. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2000 · Cited by 199 · see citing works
“2000" language="eng" relation="no"> In the mammalian embryo, each cell of the inner cell mass (ICM) of the blastocyst is destined to choose between two prospective fates: that of the epiblast, which gives rise to all tissues of the embryo proper, and that of the primitive endoderm, which develops into the visceral and…”
Background
Epigenetic restriction of extraembryonic lineages mirrors the somatic transition to cancer
Smith, Z. D., Shi, J., Gu, H., Donaghey, J., Clement, K., Cacchiarelli, D., Gnirke, A., Michor, F., & Meissner, A. (2017) · Nature · doi:10.1038/nature23891 · Cited by 201 · see citing works
In vitro culture of cynomolgus monkey embryos beyond early gastrulation
Ma, H., Zhai, J., Wan, H., Jiang, X., Wang, X., Wang, L., Xiang, Y., He, X., Zhao, Z., Zhao, B., et al. (2019) · Science · doi:10.1126/science.aax7890 · Cited by 203 · see citing works
Dissecting the dynamics of signaling events in the BMP, WNT, and NODAL cascade during self-organized fate patterning in human gastruloids
Chhabra, S., Liu, L., Goh, R., Kong, X., & Warmflash, A. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000498 · Cited by 203 · see citing works
“Prior studies have shown that a signaling cascade in which BMP activates WNT, which subsequently activates NODAL (BMP!WNT!NODAL), is integral to initiating gastrulation in the mouse embryo and is also active during in vitro human gastrulation in a different protocol [1,33].”
BackgroundResultInfluential
Role of the transcription factor T (brachyury) in the pathogenesis of sporadic chordoma: a genetic and functional‐based study
Presneau, N., Shalaby, A. A., Ye, H., et al. (2010) · The Journal of Pathology · doi:10.1002/path.2816 · Cited by 201 · see citing works
Mapping the route from naive pluripotency to lineage specification
Kalkan, T., & Smith, A. G. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0540 · Cited by 197 · see citing works
The embryonic origins of erythropoiesis in mammals
Baron, M. H., Isern, J., & Fraser, S. T. (2012) · Blood · doi:10.1182/blood-2012-01-153486 · Cited by 192 · see citing works
Origin and function of the yolk sac in primate embryogenesis
Ross, C., & Boroviak, T. (2020) · Nature Communications · doi:10.1038/s41467-020-17575-w · Cited by 193 · see citing works
The Harmonies Played by TGF-β in Stem Cell Biology
Oshimori, N., & Fuchs, E. V. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.11.001 · Cited by 189 · see citing works
Dynamics of lineage commitment revealed by single-cell transcriptomics of differentiating embryonic stem cells
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
Micropattern differentiation of mouse pluripotent stem cells recapitulates embryo regionalized cell fate patterning
Morgani, S. M., Metzger, J. J., Nichols, J., Siggia, E. D., & Hadjantonakis, A. (2018) · eLife · doi:10.7554/elife.32839 · Cited by 177 · see citing works
Endogenous Wnt signalling in human embryonic stem cells generates an equilibrium of distinct lineage-specified progenitors
Blauwkamp, T. A., Nigam, S., Ardehali, R., Weissman, I. L., & Nusse, R. (2012) · Nature Communications · doi:10.1038/ncomms2064 · Cited by 185 · see citing works
Mesp1 Patterns Mesoderm into Cardiac, Hematopoietic, or Skeletal Myogenic Progenitors in a Context-Dependent Manner
Chan, S. S.-K., Shi, X., Toyama, A., Arpke, R. W., Dandapat, A., Iacovino, M., Kang, J., Le, G., Hagen, H. R., Garry, D. J., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.03.004 · Cited by 183 · see citing works
“The impact of signaling on mesodermal patterning has been extensively studied (Arnold and Robertson, 2009; Tam and Loebel, 2007).”
Background
Activin/nodal signalling in stem cells
Pauklin, S., & Vallier, L. (2015) · Development · doi:10.1242/dev.091769 · Cited by 183 · see citing works
“Following implantation, a gradient of Nodal signalling defines the proximal-distal axis, which in turn establishes the anterior-posterior axis of the developing embryo (Arnold and Robertson, 2009).”
Background
A 3D model of a human epiblast reveals BMP4-driven symmetry breaking
Simunovic, M., Metzger, J. J., Etoc, F., et al. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0349-7 · Cited by 178 · see citing works
The many faces of Pluripotency: in vitro adaptations of a continuum of in vivo states
Morgani, S. M., Nichols, J., & Hadjantonakis, A. (2017) · BMC Developmental Biology · doi:10.1186/s12861-017-0150-4 · Cited by 167 · see citing works
“As development progresses, a combination of Fibroblast Growth Factor (FGF), Bone Morphogenetic Protein (BMP), Wnt and Nodal signaling triggers the loss of pluripotency by driving differentiation of the Epi into specialized, developmentally-restricted fates [1].”
Background
Development of a scalable suspension culture for cardiac differentiation from human pluripotent stem cells
Chen, V. C., Ye, J., Shukla, P., Hua, G., Chen, D., Lin, Z., Liu, J., Chai, J., Gold, J., Wu, J. C., et al. (2015) · Stem Cell Research · doi:10.1016/j.scr.2015.08.002 · Cited by 174 · see citing works
Activin/Nodal Signaling Controls Divergent Transcriptional Networks in Human Embryonic Stem Cells and in Endoderm Progenitors
Brown, S. E., Teo, A. K. K., Pauklin, S., Hannan, N. R. F., Cho, C. H.-H., Lim, B., Vardy, L. A., Dunn, N. R., Trotter, M. W. B., Pedersen, R. A., et al. (2011) · Stem Cells · doi:10.1002/stem.666 · Cited by 174 · see citing works
NANOG and CDX2 Pattern Distinct Subtypes of Human Mesoderm during Exit from Pluripotency
Mendjan, S., Mascetti, V. L., Ortmann, D., Ortiz, M., Karjosukarso, D. W., Ng, Y., Moreau, T., & Pedersen, R. A. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.06.006 · Cited by 171 · see citing works
Control of embryonic stem cell lineage commitment by core promoter factor, TAF3
Liu, Z., Scannell, D. R., Eisen, M. B., & Tjian, R. (2011) · Cell · doi:10.1016/j.cell.2011.08.005 · Cited by 167 · see citing works
“During early embryogenesis, the correct execution of patterning gene expression programs is essential for proper cell migration and fate allocation (Arnold and Robertson, 2009).”
Distinct levels of Notch activity for commitment and terminal differentiation of stem cells in the adult fly intestine
Perdigoto, C. N., Schweisguth, F., & Bardin, A. J. (2011) · Development · doi:10.1242/dev.065292 · Cited by 168 · see citing works
“During embryogenesis, an orchestrated commitment of stem cells underlies the formation of the germ layers and adult structures (Arnold and Robertson, 2009; Hemberger et al., 2009).”
Background
Wnt/β-catenin and FGF signalling direct the specification and maintenance of a neuromesodermal axial progenitor in ensembles of mouse embryonic stem cells
Turner, D. A., Hayward, P. C., Baillie‐Johnson, P., Rué, P., Broome, R., Faunes, F., & Arias, A. M. (2014) · Development · doi:10.1242/dev.112979 · Cited by 158 · see citing works
“…to one of two prospective fates: anterior neuroectoderm (aNECT) that will give rise to the anterior nervous system; or, posteriorly, to a rapidly expanding population that gives rise to the mesoderm and the endoderm through the primitive streak (Arnold and Robertson, 2009; Rossant and Tam, 2009).”
Engineered signaling centers for the spatially controlled patterning of human pluripotent stem cells
Manfrin, A., Tabata, Y., Paquet, É. R., Vuaridel, A. R., Rivest, F. R., Naef, F., & Lütolf, M. P. (2019) · Nature Methods · doi:10.1038/s41592-019-0455-2 · Cited by 160 · see citing works
Self-organization of human embryonic stem cells on micropatterns
Deglincerti, A., Etoc, F., Guerra, M. C., Martyn, I., Metzger, J. J., Ruzo, A., Simunovic, M., Yoney, A., Brivanlou, A. H., Siggia, E. D., et al. (2016) · Nature Protocols · doi:10.1038/nprot.2016.131 · Cited by 163 · see citing works
The lateral plate mesoderm
Prummel, K. D., Nieuwenhuize, S., & Mosimann, C. (2020) · Development · doi:10.1242/dev.175059 · Cited by 162 · see citing works
Stem-cell-based embryo models for fundamental research and translation
Fu, J., Warmflash, A., & Lütolf, M. P. (2020) · Nature Materials · doi:10.1038/s41563-020-00829-9 · Cited by 160 · see citing works
Lineage tracing of human development through somatic mutations
Spencer-Chapman, M., Ranzoni, A. M., Myers, B., Williams, N., Coorens, T., Mitchell, E., Butler, T., Dawson, K., Hooks, Y., Moore, L., et al. (2021) · Nature · doi:10.1038/s41586-021-03548-6 · Cited by 138 · see citing works
Specific gene-regulation networks during the pre-implantation development of the pig embryo as revealed by deep sequencing
Cao, S., Han, J., Wu, J., Li, Q., Liu, S., Zhang, W., Pei, Y., Ruan, X., Liu, Z., Wang, X., et al. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-4 · Cited by 157 · see citing works
“The second event is regulated by Nanog and Gata6, resulting in the segregation of the primitive endoderm and epiblast lineages from the ICM at the blastocyst stage [32].”
Background
TGF-β Family Signaling in Early Vertebrate DevelopmentPreprint
Zinski, J. M., Tajer, B. J., & Mullins, M. C. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a033274 · Cited by 153 · see citing works
Genetically engineering self-organization of human pluripotent stem cells into a liver bud-like tissue using Gata6
Guye, P., Ebrahimkhani, M. R., Kipniss, N. H., Velazquez, J. J., Schoenfeld, E., Kiani, S., Griffith, L. G., & Weiss, R. (2016) · Nature Communications · doi:10.1038/ncomms10243 · Cited by 157 · see citing works
Brachyury and SMAD signalling collaboratively orchestrate distinct mesoderm and endoderm gene regulatory networks in differentiating human embryonic stem cells
Faial, T., Bernardo, A. S., Mendjan, S., Diamanti, E., Ortmann, D., Gentsch, G. E., Mascetti, V. L., Trotter, M. W. B., Smith, J. C., & Pedersen, R. A. (2015) · Development · doi:10.1242/dev.117838 · Cited by 155 · see citing works
“The three primary germ layers (ectoderm, mesoderm and endoderm) arise from the pluripotent epiblast during gastrulation in the amniote embryo (Arnold and Robertson, 2009; Tam and Loebel, 2007); this can be modelled in vitro using pluripotent stem cells (Murry and Keller, 2008).”
Influential
In Vivo Human Somitogenesis Guides Somite Development from hPSCs
Xi, H., Fujiwara, W., Gonzalez, K. M., Jan, M., Liebscher, S., Handel, B. V., Schenke‐Layland, K., & Pyle, A. D. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.01.040 · Cited by 156 · see citing works
“…followed by WNT/β-catenin activation specifies hPSCs to a somite fate Our human profiling data reveal enriched WNT signaling in PSM, consistent with its pivotal role in paraxial mesoderm development in model organisms (Arnold and Robertson, 2009; Hubaud and Pourquie, 2014; Tam and Loebel, 2007).”
Background
Mouse gastrulation: Coordination of tissue patterning, specification and diversification of cell fate
Bardot, E., & Hadjantonakis, A. (2020) · Mechanisms of Development · doi:10.1016/j.mod.2020.103617 · Cited by 144 · see citing works
“DVE cells are specified from a subset of emVE based on exposure to low levels of Nodal signaling (Arnold and Robertson, 2009; Lu and Robertson, 2004; Takaoka et al., 2017).”
Background
A Role for the Long Noncoding RNA SENCR in Commitment and Function of Endothelial Cells
Boulberdaa, M., Scott, E., Ballantyne, M. D., García, R., Descamps, B., Angelini, G. D., Brittan, M., Hunter, A., McBride, M., McClure, J., et al. (2016) · Molecular Therapy · doi:10.1038/mt.2016.41 · Cited by 153 · see citing works
Spatial profiling of early primate gastrulation in utero
Bergmann, S., Penfold, C. A., Slatery, E. M., Siriwardena, D., Drummer, C., Clark, S. J., Strawbridge, S. E., Kishimoto, K., Vickers, A., Tewary, M., et al. (2022) · Nature · doi:10.1038/s41586-022-04953-1 · Cited by 152 · see citing works
SOX17 links gut endoderm morphogenesis and germ layer segregation
Viotti, M., Nowotschin, S., & Hadjantonakis, A.-K. (2014) · Nature Cell Biology · doi:10.1038/ncb3070 · Cited by 150 · see citing works
“As a paradigm for tissue growth and remodeling, gastrulation in amniotes transforms the embryo comprising the epiblast and adjacent VE, into a three-layered configuration comprising epiblast/ectoderm, mesoderm and gut endoderm 2, 3 .”
Timing of developmental events in the early mouse embryo
Kojima, Y., Tam, O. H., & Tam, P. (2014) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2014.06.010 · Cited by 144 · see citing works
Modeling post-implantation stages of human development into early organogenesis with stem-cell-derived peri-gastruloids
Liu, L., Oura, S., Markham, Z., Hamilton, J. N., Skory, R. M., Li, L., Sakurai, M., Wang, L., Pinzón-Arteaga, C. A., Plachta, N., et al. (2023) · Cell · doi:10.1016/j.cell.2023.07.018 · Cited by 149 · see citing works
Signalling pathways that control vertebrate haematopoietic stem cell specification
Clements, W. K., & Traver, D. J. (2013) · Nature reviews. Immunology · doi:10.1038/nri3443 · Cited by 145 · see citing works
Establishment of trophectoderm and inner cell mass lineages in the mouse embryo
Marikawa, Y., & Alarcón, V. B. (2009) · Molecular Reproduction and Development · doi:10.1002/mrd.21057 · Cited by 144 · see citing works
“Lastly, for those readers who are interested in mouse embryo development beyond the blastocyst stage, particularly regarding the molecular regulations of germ layer formation, we recommend several recent review articles (Tam and Loebel, 2007; Arnold and Robertson, 2009; Rossant and Tam, 2009).”
Background
External Mechanical Cues Trigger the Establishment of the Anterior-Posterior Axis in Early Mouse Embryos
Hiramatsu, R., Matsuoka, T., Kimura-Yoshida, C., Han, S.-W., Mochida, K., ADACHI, T., Takayama, S., & Matsuo, I. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.09.026 · Cited by 143 · see citing works
Epigenetic regulator function through mouse gastrulation
Grosswendt, S., Kretzmer, H., Smith, Z. D., Kumar, A. S., Hetzel, S., Wittler, L., Klages, S., Timmermann, B., Mukherji, S., & Meissner, A. (2020) · Nature · doi:10.1038/s41586-020-2552-x · Cited by 132 · see citing works
Germ cell specification in mice: signaling, transcription regulation, and epigenetic consequences
Saitou, M., & Yamaji, M. (2010) · Reproduction · doi:10.1530/rep-10-0043 · Cited by 140 · see citing works
“…signaling center emitting the anteriorization/anti-posteriorization signals (e.g. LEFTY1 against NODAL, DKK1 against WNT, Cerberus-like against BMP, etc.; Arnold & Robertson 2009), Prdm1 expression expands into all the epiblast cells contacting the ExE, as well as those locating much more distally.”
Background
Primate embryogenesis predicts the hallmarks of human naïve pluripotency
Boroviak, T., & Nichols, J. (2017) · Development · doi:10.1242/dev.145177 · Cited by 134 · see citing works
Cardiac Regeneration
Galdos, F. X., Guo, Y., Paige, S. L., VanDusen, N. J., Wu, S. M., & Pu, W. T. (2017) · Circulation Research · doi:10.1161/circresaha.116.309040 · Cited by 131 · see citing works
“High concentrations of NODAL at the anterior PS specify definitive endoderm precursors, whereas lower levels of NODAL in concert with BMP and WNT signaling specify mesodermal precursors in the intermediate and posterior PS.1,13 Cardiac mesoderm precursors form anterior and lateral to the PS as a result of this morphog…”
Influential
Comparative analysis of human and mouse development: From zygote to pre-gastrulation
Molè, M. A., Weberling, A., & Zernicka‐Goetz, M. (2019) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2019.10.002 · Cited by 132 · see citing works
Inducible Stem-Cell-Derived Embryos Capture Mouse Morphogenetic Events In Vitro
Amadei, G., Lau, K. Y. C., Jonghe, J. D., Gantner, C. W., Sözen, B., Chan, C., Zhu, M., Kyprianou, C., Hollfelder, F., & Zernicka‐Goetz, M. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.12.004 · Cited by 128 · see citing works
“Between 13 and 16 h, the layer formed by the egressing cells had almost extended to the distal tip, similar to PS formation in embryos (Arnold and Robertson, 2009).”
Background
The Dynamics of Morphogenesis in the Early Mouse EmbryoPreprint
Rivera‐Pérez, J. A., & Hadjantonakis, A. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a015867 · Cited by 132 · see citing works
A single cell characterisation of human embryogenesis identifies pluripotency transitions and putative anterior hypoblast centre
Molè, M. A., Coorens, T. H. H., Shahbazi, M. N., Weberling, A., Weatherbee, B. A. T., Gantner, C. W., Sancho‐Serra, C., Richardson, L., Drinkwater, A., Syed, N., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23758-w · Cited by 131 · see citing works
A role for PDGF signaling in expansion of the extra-embryonic endoderm lineage of the mouse blastocyst
Artus, J., Panthier, J., & Hadjantonakis, A. (2010) · Development · doi:10.1242/dev.050864 · Cited by 130 · see citing works
“Lineage choice is governed by the expression of key lineage-specific transcription factors that regulate downstream signaling pathways (reviewed by Arnold and Robertson, 2009; Niwa, 2007; Rossant and Tam, 2009), such that ES cells can be converted into TS-like (Niwa et al., 2005) or XENlike…”
Background
Integrating developmental signals: a Hippo in the (path)way
Mauviel, A., Nallet-Staub, F., & Varelas, X. (2011) · Oncogene · doi:10.1038/onc.2011.363 · Cited by 129 · see citing works
SIP1 Mediates Cell-Fate Decisions between Neuroectoderm and Mesendoderm in Human Pluripotent Stem Cells
Chng, Z., Teo, A. K. K., Pedersen, R. A., & Vallier, L. (2010) · Cell stem cell · doi:10.1016/j.stem.2009.11.015 · Cited by 129 · see citing works
A wave of WNT signaling balanced by secreted inhibitors controls primitive streak formation in micropattern colonies of human embryonic stem cells
Martyn, I., Brivanlou, A. H., & Siggia, E. D. (2019) · Development · doi:10.1242/dev.172791 · Cited by 129 · see citing works
Epigenomic analysis of gastrulation identifies a unique chromatin state for primed pluripotency
Xiang, Y.-L., Zhang, Y., Xu, Q.-H., Zhou, C., Liu, B.-F., Du, Z., Zhang, K., Zhang, B., Wang, X.-X., Gayen, S., et al. (2019) · Nature Genetics · doi:10.1038/s41588-019-0545-1 · Cited by 105 · see citing works
Dose-dependent Nodal/Smad signals pattern the early mouse embryo
Robertson, E. J. (2014) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2014.03.028 · Cited by 126 · see citing works
Self-citation
Patterned Differentiation of Individual Embryoid Bodies in Spatially Organized 3D Hybrid Microgels
Qi, H., Du, Y., Wang, L., Kaji, H., Bae, H., & Khademhosseini, A. (2010) · Advanced Materials · doi:10.1002/adma.201002873 · Cited by 124 · see citing works
Multi-Cellular Rosettes in the Mouse Visceral Endoderm Facilitate the Ordered Migration of Anterior Visceral Endoderm Cells
Trichas, G., Smith, A. M., White, N., et al. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001256 · Cited by 122 · see citing works
“From this position, the AVE induces anterior pattern in the underlying epiblast by restricting expression of posterior markers to the opposite side of the epiblast cup [6,14].”
Amnion signals are essential for mesoderm formation in primates
Yang, R., Goedel, A., Kang, Y., Si, C., Chu, C., Zheng, Y., Chen, Z., Gruber, P. J., Xiao, Y., Zhou, C., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25186-2 · Cited by 123 · see citing works
Rapid changes in morphogen concentration control self-organized patterning in human embryonic stem cells
Heemskerk, I., Burt, K., Miller, M., Chhabra, S., Guerra, M. C., Liu, L., & Warmflash, A. (2019) · eLife · doi:10.7554/elife.40526 · Cited by 121 · see citing works
Eomes and Brachyury control pluripotency exit and germ-layer segregation by changing the chromatin state
Tošić, J., Kim, G.-J., Pavlovic, M., Schröder, C. M., Mersiowsky, S., Barg, M., Hofherr, A., Probst, S., Köttgen, M., Hein, L., et al. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0423-1 · Cited by 121 · see citing works
Self-citation
Cardiopoietic Factors
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Self-citation

Authors: Arnold, S. J., & Robertson, E. J.
Affiliations: University of Oxford (GB)
Corresponding author: Robertson, Elizabeth J.
ORCID: Arnold, Sebastian J.
Robertson, Elizabeth J.
Venue: Nature Reviews Molecular Cell Biology
Publisher: Springer Science and Business Media LLC
Published: 2009-01-08
Volume: 10
Issue: 2
Pages: 91-103
ISSN: 1471-0072 (ISSN-L)
1471-0080
DOI: 10.1038/nrm2618
OpenAlex: W2070700342
Cited by: 816
References: 147
Citations by year: 2026: 39 · 2025: 52 · 2024: 46 · 2023: 45 · 2022: 55 · 2021: 66 · 2020: 49 · 2019: 56 · 2018: 60 · 2017: 48 · 2016: 46 · 2015: 35 · 2014: 56 · 2013: 41 · 2012: 39
FWCI: 3.14
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Reviews Molecular Cell Biology (publishedVersion)
PubMed (publishedVersion)
Funders: Wellcome Trust (059312)
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
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
Keywords: early mouse embryo, anterior-posterior polarity, gastrulation, germ layer specification, germ cell specification, signaling pathways, transcription factors, blastocyst, in vivo imaging, developmental conservation, lower vertebrates
MeSH terms: Positive Regulatory Domain I-Binding Factor 1, Animals, DNA-Binding Proteins, Embryo, Mammalian, Morphogenesis, Transcription Factors, Signal Transduction, RNA-Binding Proteins, Cell Lineage, Bone Morphogenetic Proteins, Body Patterning, Mice, Smad Proteins, Gastrulation

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Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo

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