Spinal neural tube closure depends on regulation of surface ectoderm identity and biomechanics by Grhl2
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Lack or excess expression of the surface ectoderm-expressed transcription factor Grainyhead-like2 (Grhl2), each prevent spinal neural tube closure. Here we investigate the causative mechanisms and find reciprocal dysregulation of epithelial genes, cell junction components and actomyosin properties in Grhl2 null and over-expressing embryos. Grhl2 null surface ectoderm shows a shift from epithelial to neuroepithelial identity (with ectopic expression of N-cadherin and Sox2), actomyosin disorganisation, cell shape changes and diminished resistance to neural fold recoil upon ablation of the closure point. In contrast, excessive abundance of Grhl2 generates a super-epithelial surface ectoderm, in which up-regulation of cell-cell junction proteins is associated with an actomyosin-dependent increase in local mechanical stress. This is compatible with apposition of the neural folds but not with progression of closure, unless myosin activity is inhibited. Overall, our findings suggest that Grhl2 plays a crucial role in regulating biomechanical properties of the surface ectoderm that are essential for spinal neurulation.
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Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106 · see citing works
Nieto, M. A., Huang, R. Y.-J., Jackson, R. A., & Thiery, J. P. (2016) · Cell · doi:10.1016/j.cell.2016.06.028 · Cited by 4,492 · see citing works
Differential analyses for RNA-seq: transcript-level estimates improve gene-level inferences
Soneson, C., Love, M. I., & Robinson, M. D. (2015) · F1000Research · doi:10.12688/f1000research.7563.1 · Cited by 3,929 · see citing works
New insights into the mechanisms of epithelial–mesenchymal transition and implications for cancer
Dongre, A., & Weinberg, R. A. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0080-4 · Cited by 3,876 · see citing works
Heatmapper: web-enabled heat mapping for all
Babicki, S., Arndt, D., Marcu, A., Liang, Y., Grant, J., Maciejewski, A., & Wishart, D. (2016) · Nucleic Acids Res. · doi:10.1093/nar/gkw419 · Cited by 2,119 · see citing works
Varet, H., Brillet-Guéguen, L., Coppée, J., & Dillies, M. (2016) · PLoS ONE · doi:10.1371/journal.pone.0157022 · Cited by 1,324 · see citing works
Greene, N. D. E., & Copp, A. J. (2014) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062012-170354 · Cited by 656 · see citing works
Self-citationle Duc, Q., Shi, Q., Blonk, I., Sonnenberg, A., Wang, N., Leckband, D., & de Rooij, J. (2010) · Journal of Cell Biology · doi:10.1083/jcb.201001149 · Cited by 652 · see citing works
Force Generation, Transmission, and Integration during Cell and Tissue Morphogenesis
Lecuit, T., Lenne, P.-F., & Munro, E. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100109-104027 · Cited by 621 · see citing works
E-cadherin junctions as active mechanical integrators in tissue dynamics
Lecuit, T., & Yap, A. S. (2015) · Nature Cell Biology · doi:10.1038/ncb3136 · Cited by 550 · see citing works
Neural tube closure: cellular, molecular and biomechanical mechanisms
Nikolopoulou, E., Galea, G. L., Rolo, A., Greene, N. D. E., & Copp, A. J. (2017) · Development · doi:10.1242/dev.145904 · Cited by 529 · see citing works
Self-citationCochard, P., & Paulin, D. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-08-02080.1984 · Cited by 406 · see citing works
Smutny, M., Cox, H. L., Leerberg, J. M., Kovács, É., Conti, M. A., Ferguson, C., Hamilton, N., Parton, R. G., Adelstein, R. S., & Yap, A. S. (2010) · Nature Cell Biology · doi:10.1038/ncb2072 · Cited by 332 · see citing works
Actomyosin networks and tissue morphogenesis
Munjal, A., & Lecuit, T. (2014) · Development · doi:10.1242/dev.091645 · Cited by 249 · see citing works
Werth, M., Walentin, K., Aue, A., Schönheit, J., Wuebken, A., Pode‐Shakked, N., Vilianovich, L., Erdmann, B., Dekel, B., Bäder, M., et al. (2010) · Development · doi:10.1242/dev.055483 · Cited by 215 · see citing works
Suppression of the Epithelial–Mesenchymal Transition by Grainyhead-like-2
Cieply, B. W., Riley, P., Pifer, P. M., Widmeyer, J., Addison, J., Ivanov, A. V., Denvir, J., & Frisch, S. M. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-4038 · Cited by 210 · see citing works
Tension, contraction and tissue morphogenesis
Heer, N. C., & Martin, A. C. (2017) · Development · doi:10.1242/dev.151282 · Cited by 195 · see citing works
Cieply, B. W., Farris, J. C., Denvir, J., Ford, H. L., & Frisch, S. M. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-4082 · Cited by 193 · see citing works
Segmentation and Quantitative Analysis of Epithelial Tissues
Aigouy, B., Umetsu, D., & Eaton, S. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-6371-3_13 · Cited by 184 · see citing works
Pulsation and stabilization: Contractile forces that underlie morphogenesis
Martin, A. C. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.10.031 · Cited by 175 · see citing works
Ting, S. B., Wilanowski, T., Auden, A., Hall, M., Voss, A. K., Thomas, T., Parekh, V., Cunningham, J. M., & Jane, S. M. (2003) · Nature Medicine · doi:10.1038/nm961 · Cited by 174 · see citing works
Yu, Z., Lin, K., Bhandari, A., Spencer, J. A., Xu, X., Wang, N., Lu, Z., Gill, G. N., Roop, D. R., Wertz, P. W., et al. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.07.015 · Cited by 173 · see citing works
Neural plate morphogenesis during mouse neurulation is regulated by antagonism of Bmp signalling
Ybot‐González, P., Gaston‐Massuet, C., Girdler, G. C., Klingensmith, J., Arkell, R. M., Greene, N. D. E., & Copp, A. J. (2007) · Development · doi:10.1242/dev.008177 · Cited by 165 · see citing works
Self-citationArnold, T. R., Stephenson, R. E., & Miller, A. L. (2017) · Experimental Cell Research · doi:10.1016/j.yexcr.2017.03.053 · Cited by 155 · see citing works
Mechanisms of tissue fusion during development
Ray, H. J., & Niswander, L. A. (2012) · Development · doi:10.1242/dev.068338 · Cited by 150 · see citing works
Pyrgaki, C., Liu, A., & Niswander, L. A. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.02.027 · Cited by 149 · see citing works
Dual Roles of the Transcription Factor Grainyhead-like 2 (GRHL2) in Breast Cancer
Werner, S., Frey, S., Riethdorf, S., Schulze, C., Alawi, M., Kling, L., Vafaizadeh, V., Sauter, G., Terracciano, L., Schumacher, U., et al. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.456293 · Cited by 128 · see citing works
Regional neural tube closure defined by the Grainy head-like transcription factors
Rifat, Y., Parekh, V., Wilanowski, T., Hislop, N. R., Auden, A., Ting, S. B., Cunningham, J. M., & Jane, S. M. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.07.017 · Cited by 127 · see citing works
Dynamics of actomyosin contractile activity during epithelial morphogenesis
Gorfinkiel, N., & Blanchard, G. B. (2011) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2011.06.002 · Cited by 121 · see citing works
α-Catenin cytomechanics – role in cadherin-dependent adhesion and mechanotransduction
Barry, A. K., Tabdili, H., Muhamed, I., Wu, J., Shashikanth, N., Gomez, G. A., Yap, A. S., Gottardi, C. J., de Rooij, J., Wang, N., et al. (2014) · Journal of Cell Science · doi:10.1242/jcs.139014 · Cited by 119 · see citing works
RhoGTPases, actomyosin signaling and regulation of the Epithelial Apical Junctional Complex
Quirós, M., & Nusrat, A. (2014) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2014.09.003 · Cited by 119 · see citing works
Stable Force Balance between Epithelial Cells Arises from F-Actin Turnover
Jodoin, J. N., Coravos, J. S., Chanet, S., Vasquez, C. G., Tworoger, M., Kingston, E. R., Perkins, L. A., Perrimon, N., & Martin, A. C. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.11.018 · Cited by 117 · see citing works
Biomechanical coupling facilitates spinal neural tube closure in mouse embryos
Galea, G. L., Cho, Y.-J., Galea, G., Molè, M. A., Rolo, A., Savery, D., MOULDING, D. A., Culshaw, L. H., Nikolopoulou, E., Greene, N. D. E., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1700934114 · Cited by 113 · see citing works
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Xiang, X., Deng, Z., Zhuang, X., Ju, S., Mu, J., Jiang, H., Zhang, L., Yan, J., Miller, D., & Zhang, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050781 · Cited by 111 · see citing works
Kohn, K. W., Zeeberg, B. M., Reinhold, W. C., & Pommier, Y. G. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099269 · Cited by 109 · see citing works
Senga, K., Mostov, K. E., Mitaka, T., Miyajima, A., & Tanimizu, N. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e12-02-0097 · Cited by 109 · see citing works
Harris, A. R., Daeden, A., & Charras, G. (2014) · Journal of Cell Science · doi:10.1242/jcs.142349 · Cited by 104 · see citing works
Aue, A., Hinze, C., Walentin, K., Ruffert, J., Yurtdas, Z. Y., Werth, M., Chen, W., Rabien, A., Kilic, E., Schulzke, J., et al. (2015) · Journal of the American Society of Nephrology · doi:10.1681/asn.2014080759 · Cited by 93 · see citing works
Gao, X., Vockley, C. M., Pauli, F., Newberry, K. M., Xue, Y., Randell, S. H., Reddy, T. E., & Hogan, B. L. M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1307589110 · Cited by 86 · see citing works
Escuin, S., Vernay, B., Savery, D., Gurniak, C. B., Witke, W., Greene, N. D. E., & Copp, A. J. (2015) · Journal of Cell Science · doi:10.1242/jcs.164574 · Cited by 83 · see citing works
Self-citationIncreased expression of Grainyhead-like-3 rescues spina bifida in a folate-resistant mouse model
Gustavsson, P., Greene, N. D. E., Lad, D., Pauws, E., de Castro, S. C., Stanier, P., & Copp, A. J. (2007) · Human Molecular Genetics · doi:10.1093/hmg/ddm221 · Cited by 81 · see citing works
Self-citationRoles of Grainyhead-like transcription factors in cancer
Frisch, S. M., Farris, J. C., & Pifer, P. M. (2017) · Oncogene · doi:10.1038/onc.2017.178 · Cited by 81 · see citing works
Regulation of cell protrusions by small GTPases during fusion of the neural folds
Rolo, A., Savery, D., Escuin, S., de Castro, S. C., Armer, H. E. J., Munro, P., Molè, M. A., Greene, N. D. E., & Copp, A. J. (2016) · eLife · doi:10.7554/elife.13273 · Cited by 80 · see citing works
Self-citationGrhl2 reduces invasion and migration through inhibition of TGFβ-induced EMT in gastric cancer
Xiang, J., Fu, X., Ran, W., & Wang, Z. (2017) · Oncogenesis · doi:10.1038/oncsis.2016.83 · Cited by 77 · see citing works
Gorfinkiel, N., & Arias, A. M. (2007) · Journal of Cell Science · doi:10.1242/jcs.010850 · Cited by 76 · see citing works
Luo, Y., Xiao, W., Zhu, X., Mao, Y., Liu, X., Chen, X., Huang, J., Tang, S., & Rizzolo, L. J. (2011) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.11-7185 · Cited by 74 · see citing works
Claudin 7 expression and localization in the normal murine mammary gland and murine mammary tumors
Blackman, B. E., Russell, T. D., Nordeen, S. K., Medina, D., & Neville, M. C. (2005) · Breast Cancer Research · doi:10.1186/bcr988 · Cited by 71 · see citing works
Mashburn, D. N., Lynch, H. E., Ma, X., & Hutson, M. S. (2012) · Cytometry Part A · doi:10.1002/cyto.a.22034 · Cited by 62 · see citing works
Abnormal Placental Development and Early Embryonic Lethality in EpCAM-Null Mice
Nagao, K., Zhu, J., Heneghan, M. B., Hanson, J. C., Morasso, M. I., Tessarollo, L., Mackem, S., & Udey, M. C. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008543 · Cited by 59 · see citing works
Over-expression of Grhl2 causes spina bifida in the Axial defects mutant mouse
Brouns, M. R., de Castro, S. C., Terwindt‐Rouwenhorst, E., Massa, V., Hekking, J. W. M., Hirst, C. S., Savery, D., Munts, C., Partridge, D. D., Lamers, W., et al. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr031 · Cited by 56 · see citing works
Self-citationGalea, G. L., Nychyk, O., Molè, M. A., MOULDING, D. A., Savery, D., Nikolopoulou, E., Henderson, D. J., Greene, N. D. E., & Copp, A. J. (2018) · Disease Models & Mechanisms · doi:10.1242/dmm.032219 · Cited by 56 · see citing works
Self-citationGolgi apparatus self-organizes into the characteristic shape via postmitotic reassembly dynamics
Tachikawa, M., & Mochizuki, A. (2017) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1619264114 · Cited by 47 · see citing works
Grainyhead genes and mammalian neural tube closure
Gustavsson, P., Copp, A. J., & Greene, N. D. E. (2008) · Birth Defects Research Part A Clinical and Molecular Teratology · doi:10.1002/bdra.20494 · Cited by 44 · see citing works
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Ybot‐González, P., Copp, A. J., & Greene, N. D. E. (2005) · Developmental Dynamics · doi:10.1002/dvdy.20383 · Cited by 41 · see citing works
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Pryor, S. E., Massa, V., Savery, D., Greene, N. D. E., & Copp, A. J. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-510-7_11 · Cited by 34 · see citing works
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Benko, R., & Brodland, G. W. (2007) · Annals of Biomedical Engineering · doi:10.1007/s10439-006-9250-1 · Cited by 33 · see citing works
Dynamic behaviors of the non-neural ectoderm during mammalian cranial neural tube closure
Ray, H. J., & Niswander, L. A. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.06.030 · Cited by 29 · see citing works
Neural tube closure depends on expression of Grainyhead-like 3 in multiple tissues
de Castro, S. C., Hirst, C. S., Savery, D., Rolo, A., Lickert, H., D, B. A. M., Copp, A. J., & Greene, N. D. E. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2018.01.016 · Cited by 29 · see citing works
Self-citationde Castro, S. C., Gustavsson, P., Marshall, A. R., Gordon, W. M., Galea, G. L., Nikolopoulou, E., Savery, D., Rolo, A., Stanier, P., D, B. A. M., et al. (2018) · Human Molecular Genetics · doi:10.1093/hmg/ddy313 · Cited by 21 · see citing works
Self-citationYates, B. P., Zetterberg, C., Rajeev, V., Reiß, M., & Rittling, S. R. (2007) · Experimental Cell Research · doi:10.1016/j.yexcr.2007.07.026 · Cited by 17 · see citing works
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Yang, F., Wang, W., Wang, F., Fang, Y., Tang, D., Huang, J., Lu, H., & Yao, J. (2021) · doi:10.1101/2021.12.05.471261 · Cited by 617 · see citing works
Verstappe, J., & Berx, G. (2023) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2023.02.001 · Cited by 63 · see citing works
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Molè, M. A., Galea, G. L., Rolo, A., Weberling, A., Nychyk, O., de Castro, S. C., Savery, D., Fässler, R., Ybot‐González, P., Greene, N. D. E., et al. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.01.012 · Cited by 62 · see citing works
Self-citationChandler, M. R., Jain, S., Halman, J. R., Hong, E., Dobrovolskaia, M. A., Zakharov, A. V., & Afonin, K. A. (2022) · Small · doi:10.1002/smll.202204941 · Cited by 61 · see citing works
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Galea, G. L., Maniou, E., Edwards, T. J. C., Marshall, A. R., Ampartzidis, I., Greene, N. D. E., & Copp, A. J. (2021) · Nature Communications · doi:10.1038/s41467-021-21372-4 · Cited by 45 · see citing works
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Maniou, E., Todros, S., Urciuolo, A., MOULDING, D. A., Magnussen, M., Ampartzidis, I., Brandolino, L., Bellet, P., Giomo, M., Pavan, P. G., et al. (2024) · Nature Materials · doi:10.1038/s41563-024-01942-9 · Cited by 42 · see citing works
Self-citationManiou, E., Staddon, M. F., Marshall, A. R., Greene, N. D. E., Copp, A. J., Banerjee, S., & Galea, G. L. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2023163118 · Cited by 38 · see citing works
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Moon, L. D., & Xiong, F. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.09.009 · Cited by 33 · see citing works
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Sundararajan, V., Pang, Q. Y., Choolani, M. A., & Huang, R. Y. (2020) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2020.00213 · Cited by 29 · see citing works
Christodoulou, N., & Skourides, P. A. (2022) · Development · doi:10.1242/dev.200358 · Cited by 29 · see citing works
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He, J., Feng, C., Zhu, H., Wu, S., Jin, P., & Xu, T. (2020) · PubMed Central · Cited by 27 · see citing works
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Li, C., Hsu, T., Chang, Y., Chan, M., Lu, P., & Hsiao, M. (2021) · Biomedicines · doi:10.3390/biomedicines9091265 · Cited by 19 · see citing works
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Self-citationHuang, H., Liu, J., Li, M., Guo, H., Zhu, J., Zhu, L., Wu, S., Mo, K., Huang, Y., Tan, J., et al. (2022) · Science Advances · doi:10.1126/sciadv.abo5668 · Cited by 17 · see citing works
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Kruse, K., Berthoz, R., Barberi, L., Reymann, A.-C., & Riveline, D. (2024) · Current Biology · doi:10.1016/j.cub.2024.08.043 · Cited by 16 · see citing works
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Andrews, T. G. R., & Priya, R. (2024) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a041520 · Cited by 15 · see citing works
Goering, J. P., Wenger, L. W., Stetsiv, M., Moedritzer, M., Hall, E. G., Isai, D. G., Jack, B., Umar, Z., Rickabaugh, M. K., Czirók, A., et al. (2021) · Human Molecular Genetics · doi:10.1093/hmg/ddab211 · Cited by 14 · see citing works
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Marshall, A. R., Galea, G. L., Copp, A. J., & Greene, N. D. E. (2023) · Cells and Development · doi:10.1016/j.cdev.2023.203840 · Cited by 11 · see citing works
Self-citationJAFFE, E. A., & Niswander, L. A. (2020) · Developmental Dynamics · doi:10.1002/dvdy.292 · Cited by 11 · see citing works
Filo, M., Kumar, S., Anastassov, S., & Khammash, M. (2022) · IEEE Conference on Decision and Control (CDC) · doi:10.1109/cdc51059.2022.9993268 · Cited by 10 · see citing works
Crane‐Smith, Z., de Castro, S. C., Nikolopoulou, E., Wolujewicz, P., Smedley, D. P., Lei, Y., Mather, E., Santos, C., Hopkinson, M., Pitsillides, A. A., et al. (2023) · Human Molecular Genetics · doi:10.1093/hmg/ddad094 · Cited by 10 · see citing works
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Mirdass, C., Catala, M., Bocel, M., Nedelec, S., & Ribes, V. (2023) · Emerging Topics in Life Sciences · doi:10.1042/etls20230087 · Cited by 12 · see citing works
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Tidei, J. J., Oakes, P. W., & Beach, J. R. (2025) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2025.102522 · Cited by 7 · see citing works
Gene expression dynamics of human and mouse craniofacial development at the single-cell level
Khouri‐Farah, N., Manchel, A., Winchester, E. W., Schilder, B. M., Robinson, K. R., Curtis, S. W., Skene, N., Leslie, E. J., & Cotney, J. L. (2026) · Nature Communications · doi:10.1038/s41467-026-70232-6 · Cited by 8 · see citing works
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Legere, E.-A., Baumholtz, A. I., Lachance, J.-F. B., Archer, M., Piontek, J., & Ryan, A. K. (2023) · Developmental Biology · doi:10.1016/j.ydbio.2023.12.009 · Cited by 7 · see citing works
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Copp, A. J., Clark, M., & Greene, N. D. E. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1223849 · Cited by 7 · see citing works
Self-citationSupracellular actomyosin assemblies: master coordinators of development
Röper, K. (2025) · Development · doi:10.1242/dev.204896 · Cited by 10 · see citing works
Dong, Y., Huang, L., & Liu, L. (2024) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2024.114562 · Cited by 6 · see citing works
Ventral body wall closure: Mechanistic insights from mouse models and translation to human pathology
Formstone, C. J., Aldeiri, B., Davenport, M., & Francis‐West, P. H. (2024) · Developmental Dynamics · doi:10.1002/dvdy.735 · Cited by 7 · see citing works
Downregulation of Extraembryonic Tension Controls Body Axis Formation in Avian EmbryosPreprint
Kunz, D., Wang, A., Chan, C. U., Pritchard, R. H., Wang, W., Gallo, F., Bradshaw, C. R., Terenzani, E., Müller, K. H., Huang, Y. Y. S., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.24.432525 · Cited by 6 · see citing works
Anisotropic Cell Shape and Motion Coordinate Hindbrain Neuropore MorphogenesisPreprint
Pérez-Verdugo, F., Maniou, E., Galea, G. L., & Banerjee, S. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.21.624679 · Cited by 6 · see citing works
Self-citationScrib organizes cortical actomyosin clusters to maintain adherens junctions and angiogenic sprouting
Mayo, L. N., Duong, F. H. T., Mompeón, A., Jacobs, K. A., Iruela‐Arispe, M. L., & Kutys, M. L. (2026) · The Journal of Cell Biology · doi:10.1083/jcb.202503146 · Cited by 5 · see citing works
Epithelial fusion is mediated by a partial epithelial–mesenchymal transition
Tamilkumar, V. N., Purushothama, H., & Ladher, R. K. (2025) · Biology Open · doi:10.1242/bio.062213 · Cited by 4 · see citing works
Cell and Tissue Nanomechanics: From Early Development to Carcinogenesis
Shmelev, M. E., Titov, S., Belousov, A. S., Farniev, V. M., Zhmenia, V., Lanskikh, D., Penkova, A. O., & Kumeiko, V. V. (2022) · Biomedicines · doi:10.3390/biomedicines10020345 · Cited by 4 · see citing works
Neurulation and Neural Tube Defects
ten Donkelaar, H. J., Copp, A. J., Bekker, M. N., Renier, W. O., Hori, A., & Shiota, K. (2023) · Springer eBooks · doi:10.1007/978-3-031-26098-8_4 · Cited by 4 · see citing works
Self-citationMoran, C. M., & Zohn, I. E. (2025) · Developmental Biology · doi:10.1016/j.ydbio.2025.11.002 · Cited by 2 · see citing works
Association Analysis of SNPs in GRHL2 and RORA Genes with Lambing Number in Small-Tailed Han Sheep
Pu, X., Liu, K., Wang, X., Di, R., He, X., Liu, Y., & Chu, M. (2025) · Animals · doi:10.3390/ani15101432 · Cited by 2 · see citing works
Brooks, E., Hwang, S.-H., White, K. A., & Mukhopadhyay, S. (2025) · Development · doi:10.1242/dev.205171 · Cited by 2 · see citing works
Quantifying mechanical forces during vertebrate morphogenesisPreprint
Maniou, E., Todros, S., Urciuolo, A., MOULDING, D. A., Magnussen, M., Giomo, M., Pavan, P. G., Galea, G. L., & Elvassore, N. (2022) · Research Square · doi:10.21203/rs.3.rs-1095730/v1 · Cited by 2 · see citing works
Self-citationMonitoring the Mechanical Evolution of Tissue During Neural Tube Closure of Chick Embryo
Shi, C., Handler, C., Florn, H., & Zhang, J. (2023) · Journal of Visualized Experiments · doi:10.3791/66117 · Cited by 1 · see citing works
Kimura-Yoshida, C., Mochida, K., Matsuno, C., Kano, K., Mishiro‐Sato, E., & Matsuo, I. (2025) · Development · doi:10.1242/dev.204700 · Cited by 1 · see citing works
Legere, E.-A., Dumont, M., Dias, J., Yamanaka, Y., Galea, G. L., & Ryan, A. K. (2026) · Journal of Cell Science · doi:10.1242/jcs.264758 · Cited by 1 · see citing works
Self-citationDelgado, C. Z., Ambekar, Y. S., Mekonnen, T. T., Zvietcovich, F., Nijem, N., Singh, M., Lekven, A. C., Aglyamov, S. R., & Larin, K. V. (2023) · Optical Coherence Tomography and Coherence Domain Optical Methods in Biomedicine · doi:10.1117/12.2650904 · Cited by 1 · see citing works
The protective effect of niamid on hearing in patients treated with large doses of streptomycin.
Semczuk, B., Klonowski, S., & Gołabek, W. (1974) · PubMed
Federici, A., Bernardi, G., Senna, I., Fantoni, M., Ernst, M. O., Ricciardi, E., & Bottari, D. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.05.17.492319
Das, S., & Srivastava, D. (2022) · bioRxiv · doi:10.1101/2022.08.01.502395
CFL1-dependency of discrete cell behaviours driving mouse spinal zipperingPreprint
Marshall, A. R., Krstevski, A., Croswell, H., Shah, R., Maniou, E., Greene, N. D. E., Copp, A. J., & Galea, G. L. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.07.565942
Self-citationMolecular and morphogenetic features of neurulation
Nevmerzhytska, N. M., Grabovyi, O. M., Yaremenko, L. M., Dzevulska, І. V., Synytska, A. M., & Kozak, H. I. (2024) · Zaporozhye Medical Journal · doi:10.14739/2310-1210.2024.1.288912
Legere, E.-A., Dumont, M., Yamanaka, Y., Galea, G. L., & Ryan, A. K. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.14.682463
Self-citationMechanosensitive feedback organizes cell shape and motion during hindbrain neuropore morphogenesis
Pérez-Verdugo, F., Maniou, E., Galea, G. L., & Banerjee, S. (2026) · Current Biology · doi:10.1016/j.cub.2026.02.068
Self-citation
- Authors
- Nikolopoulou, E., Hirst, C. S., Galea, G., Venturini, C., Moulding, D., Marshall, A. R., Rolo, A., De Castro, S. C. P., Copp, A. J., & Greene, N. D. E.
- Affiliations
- University College London (GB)
- Horizon Discovery (United Kingdom) (GB)
- University of Lisbon (PT)
- Corresponding author
- Greene, Nicholas D. E.
- Venue
- Nature Communications
- Published
- 2019-06-06
- Volume
- 10
- Issue
- 1
- Pages
- 2487-2487
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC6554357
- OpenAlex
- W2948595072
- Cited by
- 62
- References
- 60
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 7 · 2023: 19 · 2022: 11 · 2021: 7 · 2020: 4
- FWCI
- 1.82
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Wellcome Trust (211112/Z/18/Z, 107474, 087525, /Z/15/Z, 107474/Z/15/Z)
- NIHR Biomedical Research Centre, Royal Marsden NHS Foundation Trust/Institute of Cancer Research
- National Institute for Health and Care Research
- University College London (087525)
- Great Ormond Street Hospital for Children
- Medical Research Council (G0802163)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Spinal Dysraphism and Malformations
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- GRHL2, neural tube closure, neurulation, surface ectoderm, epithelial-mesenchymal transition, N-cadherin, SOX2, actomyosin, cell-cell contact, tissue mechanics, mechanical stress, myosin, transcription factors
- MeSH terms
- Actomyosin, Animals, Biomechanical Phenomena, Ectoderm, Embryo, Mammalian, Epithelial Cells, Intercellular Junctions, Stress, Mechanical, Transcription Factors, Cadherins, Gene Expression Regulation, Developmental, Neuroepithelial Cells, Mice, Neural Tube, Neurulation, SOXB1 Transcription Factors
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