A 90° rotation of the mitotic spindle changes the orientation of mitoses of zebrafish neuroepithelial cells
Abstract
In the neural plate and neural tube in the trunk region of the zebrafish embryo, dividing cells are oriented parallel to the plane of the neuroepithelium, while in neural keel/rod, cells divide perpendicular to it. This change in the orientation of mitosis is brought about by a 90°rotation of the mitotic spindle. As the two halves of the neural primordium in keel/rod stage are in apposition, the perpendicular orientation of mitoses in this stage determines that daughter cells become allocated to both sides of the neural tube. To assess the role played by cell junctions in controlling the orientation of dividing cells, we studied the expression of components of adherens and tight junctions in the neuroepithelial cells. We find that these proteins are distributed irregularly at the neural plate stage and become polarised apically in the cell membrane only during the keel/rod stage. The stereotypic orientation of mitoses is perturbed only weakly upon loss of function of the cell junction components ASIP and aPKCλ, suggesting that mitotic orientation depends in part on the integrity of cell junctions and the polarity of the epithelium as a whole. However, the 90° rotation of the spindle does not require perfectly polarised cell junctions between the neuroepithelial cells.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In zebrafish, most cell divisions are parallel to the epithelial sheet, but during the neural keel/rod phase, mitotic spindles rotate 90° to be perpendicular to it.
“Most cell divisions are parallel to the epithelial sheet, but during the neural keel/rod phase, this changes (Geldmacher-Voss et al., 2003; Žigman et al., 2011). Mitotic spindles set up parallel to the epithelial sheet, but then rotate 90° to be perpendicular to it.”
From Scribble: A master scaffold in polarity, adhesion, synaptogenesis, and proliferation (2019) · cites this paper as Geldmacher-Voss et al., 2003
Cites
Stages of embryonic development of the zebrafish
Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., & Schilling, T. F. (1995) · Developmental Dynamics · doi:10.1002/aja.1002030302 · Cited by 12,037 · see citing works
Circular Statistics in Biology
Watson, G. S., & Batschelet, E. (1982) · Technometrics · doi:10.2307/1267831 · Cited by 4,632 · see citing works
FACS-optimized mutants of the green fluorescent protein (GFP)
Cormack, B. P., Valdivia, R. H., & Falkow, S. (1996) · Gene · doi:10.1016/0378-1119(95)00685-0 · Cited by 2,621 · see citing works
Effective targeted gene ‘knockdown’ in zebrafish
Nasevicius, A., & Ekker, S. C. (2000) · Nature Genetics · doi:10.1038/79951 · Cited by 2,485 · see citing works
Neurons derived from radial glial cells establish radial units in neocortex
Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S., & Kriegstein, A. R. (2001) · Nature · doi:10.1038/35055553 · Cited by 2,016 · see citing works
Defense Strategies Against Hypoxia and Hypothermia
Hochachka, P. W. (1986) · Science · doi:10.1126/science.2417316 · Cited by 1,104 · see citing works
Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate.Preprint
Turner, D. L., & Weintraub, H. (1994) · Genes & Development · doi:10.1101/gad.8.12.1434 · Cited by 1,023 · see citing works
Asymmetric Inheritance of Radial Glial Fibers by Cortical Neurons
Miyata, T., Kawaguchi, A., Okano, H., & Ogawa, M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00420-2 · Cited by 892 · see citing works
Identification of genes required for cytoplasmic localization in early C. elegans embryos
Kemphues, K. J., Priess, J. R., Morton, D. G., & Cheng, N. N. (1988) · Cell · doi:10.1016/s0092-8674(88)80024-2 · Cited by 859 · see citing works
Chenn, A., & McConnell, S. K. (1995) · Cell · doi:10.1016/0092-8674(95)90035-7 · Cited by 766 · see citing works
Origin and organization of the zebrafish fate map
Kimmel, C. B., Warga, R. M., & Schilling, T. F. (1990) · Development · doi:10.1242/dev.108.4.581 · Cited by 698 · see citing works
Mutations affecting the formation and function of the cardiovascular system in the zebrafish embryo
Stainier, D. Y. R., Fouquet, B., Chen, J., Warren, K. S., Weinstein, B. M., Meiler, S. E. L., Mohideen, M.-A. P. K., Neuhauss, S. C. F., Solnica-Krezel, L., Schier, A. F., et al. (1996) · Development · doi:10.1242/dev.123.1.285 · Cited by 625 · see citing works
Itoh, M., Nagafuchi, A., Yonemura, S., Kitani-Yasuda, T., Tsukita, S., & Tsukita, S. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.121.3.491 · Cited by 576 · see citing works
β-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos
Schneider, S., Steinbeißer, H., Warga, R. M., & Hausen, P. (1996) · Mechanisms of Development · doi:10.1016/0925-4773(96)00546-1 · Cited by 515 · see citing works
Izumi, Y., Hirose, T., Tamai, Y., Hirai, S.-I., Nagashima, Y., Fujimoto, T., Tabuse, Y., Kemphues, K. J., & Ohno, S. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.143.1.95 · Cited by 505 · see citing works
Wodarz, A., Ramrath, A., Grimm, A., & Knust, E. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.150.6.1361 · Cited by 472 · see citing works
Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts
Wodarz, A., Ramrath, A., Kuchinke, U., & Knust, E. (1999) · Nature · doi:10.1038/990128 · Cited by 451 · see citing works
Suzuki, A., Yamanaka, T., Hirose, T., Manabe, N., Mizuno, K., Shimizu, M., Akimoto, K., Izumi, Y., Ohnishi, T., & Ohno, S. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.152.6.1183 · Cited by 441 · see citing works
DmPAR-6 directs epithelial polarity and asymmetric cell division of neuroblasts in Drosophila
Petronczki, M. P., & Knoblich, J. A. (2000) · Nature Cell Biology · doi:10.1038/35050550 · Cited by 419 · see citing works
Ohno, S. (2001) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(00)00264-7 · Cited by 418 · see citing works
Role of inscuteable in orienting asymmetric cell divisions in Drosophila
Kraut, R. S., Chia, W. N., Jan, L. Y., Jan, Y. N., & Knoblich, J. A. (1996) · Nature · doi:10.1038/383050a0 · Cited by 394 · see citing works
Müller, H. A., & Wieschaus, E. (1996) · The Journal of cell biology · doi:10.1083/jcb.134.1.149 · Cited by 384 · see citing works
Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts
Schöber, M., Schaefer, M., & Knoblich, J. A. (1999) · Nature · doi:10.1038/990135 · Cited by 383 · see citing works
Mutations affecting the development of the embryonic zebrafish brain
Schier, A. F., Neuhauss, S. C. F., Harvey, M., Malicki, J. J., Solnica‐Krezel, L., Stainier, D. Y. R., Zwartkruis, F. J. T., Abdelilah, S., Stemple, D. L., Rangini, Z., et al. (1996) · Development · doi:10.1242/dev.123.1.165 · Cited by 372 · see citing works
Yu, F., Morin, X., Cai, Y., Yang, X., & Chia, W. N. (2000) · Cell · doi:10.1016/s0092-8674(00)80676-5 · Cited by 370 · see citing works
Mutations affecting development of the zebrafish retina
Malicki, J. J., Neuhauss, S. C. F., Schier, A. F., Solnica‐Krezel, L., Stemple, D. L., Stainier, D. Y. R., Abdelilah, S., Zwartkruis, F. J. T., Rangini, Z., & Driever, W. (1996) · Development · doi:10.1242/dev.123.1.263 · Cited by 369 · see citing works
Schaefer, M., Shevchenko, A., Shevchenko, A., & Knoblich, J. A. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00401-2 · Cited by 337 · see citing works
Holley, S. A., Geisler, R., & Nüsslein‐Volhard, C. (2000) · Genes & Development · doi:10.1101/gad.14.13.1678 · Cited by 321 · see citing works
Asymmetric cell division during animal development
Knoblich, J. A. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35048085 · Cited by 311 · see citing works
Kaltschmidt, J. A., Davidson, C. M., Brown, N. H., & Brand, A. H. (1999) · Nature Cell Biology · doi:10.1038/71323 · Cited by 288 · see citing works
Positional cloning of heart and soul reveals multiple roles for PKCλ in zebrafish organogenesis
Horne‐Badovinac, S., Lin, D., Waldron, S., Schwarz, M., Mbamalu, G., Pawson, T. J., Jan, Y. N., Stainier, D. Y. R., & Abdelilah‐Seyfried, S. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00458-4 · Cited by 283 · see citing works
Drosophila Stardust is a partner of Crumbs in the control of epithelial cell polarity
Bachmann, A., Schneider, M., Theilenberg, E., Grawe, F., & Knust, E. (2001) · Nature · doi:10.1038/414638a · Cited by 279 · see citing works
Adherens junctions inhibit asymmetric division in the Drosophila epithelium
Lu, B., Roegiers, F., Jan, L. Y., & Jan, Y. N. (2001) · Nature · doi:10.1038/35054077 · Cited by 237 · see citing works
Concha, M. L., & Adams, R. J. (1998) · Development · doi:10.1242/dev.125.6.983 · Cited by 237 · see citing works
Control of spindle orientation in Drosophila by the Par-3-related PDZ-domain protein Bazooka
Kuchinke, U., Grawe, F., & Knust, E. (1998) · Current Biology · doi:10.1016/s0960-9822(98)00016-5 · Cited by 234 · see citing works
Hinds, J. W., & Ruffett, T. L. (1971) · Cell and Tissue Research · doi:10.1007/bf00391127 · Cited by 231 · see citing works
Gho, M., & Schweisguth, F. (1998) · Nature · doi:10.1038/30265 · Cited by 230 · see citing works
Cell cycles and clonal strings during formation of the zebrafish central nervous system
Kimmel, C. B., Warga, R. M., & Kane, D. A. (1994) · Development · doi:10.1242/dev.120.2.265 · Cited by 224 · see citing works
Establishing cell polarity in development
Wodarz, A. (2002) · Nature Cell Biology · doi:10.1038/ncb0202-e39 · Cited by 218 · see citing works
Reinsch, S. S., & Karsenti, E. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.126.6.1509 · Cited by 215 · see citing works
Hartenstein, V. (1989) · Neuron · doi:10.1016/0896-6273(89)90200-6 · Cited by 207 · see citing works
Kraut, R. S., & Campos‐Ortega, J. A. (1996) · Developmental Biology · doi:10.1006/dbio.1996.0052 · Cited by 176 · see citing works
Self-citationMigratory paths of neurons and glia in the embryonic chick spinal cord
Leber, S., & Sanes, J. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-02-01236.1995 · Cited by 166 · see citing works
Pauls, S., Geldmacher-Voss, B., & Campos‐Ortega, J. A. (2001) · Development Genes and Evolution · doi:10.1007/s00427-001-0196-x · Cited by 163 · see citing works
Self-citationAsymmetric Segregation of Numb in Retinal Development and the Influence of the Pigmented Epithelium
Cayouette, M., Whitmore, A. V., Jeffery, G., & RAFF, M. C. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-15-05643.2001 · Cited by 152 · see citing works
Molecular genetics of asymmetric cleavage in the early Caenorhabditis elegans embryo
Guo, S., & Kemphues, K. J. (1996) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(96)80061-x · Cited by 150 · see citing works
On the formation of the neural keel and neural tube in the zebrafishDanio (Brachydanio) rerio
Papan, C., & Campos-Ortega, J. A. (1994) · Development Genes and Evolution · doi:10.1007/bf00636333 · Cited by 147 · see citing works
Self-citationPeterson, R. T., Mably, J. D., Chen, J., & Fishman, M. C. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00482-1 · Cited by 146 · see citing works
Cheng, N. N., Kirby, C., & Kemphues, K. J. (1995) · Genetics · doi:10.1093/genetics/139.2.549 · Cited by 138 · see citing works
Neurulation in the anterior trunk region of the zebrafish Brachydanio rerio
Schmitz, B., Papan, C., & Campos-Ortega, J. A. (1993) · Development Genes and Evolution · doi:10.1007/bf00363214 · Cited by 128 · see citing works
Self-citationBorgne, R. L., Bellaı̈che, Y., & Schweisguth, F. (2002) · Current Biology · doi:10.1016/s0960-9822(01)00648-0 · Cited by 121 · see citing works
Two types of asymmetric divisions in the Drosophila sensory organ precursor cell lineage
Roegiers, F., Younger, S. H., Jan, L. Y., & Jan, Y. N. (2000) · Nature Cell Biology · doi:10.1038/35050568 · Cited by 113 · see citing works
Early pattern of neuronal differentiation in the Xenopus embryonic brainstem and spinal cord
Hartenstein, V. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903280205 · Cited by 107 · see citing works
Association of ASIP/mPAR‐3 with adherens junctions of mouse neuroepithelial cells
Manabe, N., Hirai, S.-I., Imai, F., Nakanishi, H., Takai, Y., & Ohno, S. (2002) · Developmental Dynamics · doi:10.1002/dvdy.10139 · Cited by 104 · see citing works
Chapter 11 Confocal Microscopic Analysis of Morphogenetic Movements
Cooper, M. S., D’Amico, L., & Henry, C. A. (1998) · Methods in cell biology · doi:10.1016/s0091-679x(08)61826-9 · Cited by 86 · see citing works
Metaphase Spindles Rotate in the Neuroepithelium of Rat Cerebral Cortex
Adams, R. J. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-23-07610.1996 · Cited by 71 · see citing works
Cell lineages generating axial muscle in the zebrafish embryo
Kimmel, C. B., & Warga, R. M. (1987) · Nature · doi:10.1038/327234a0 · Cited by 69 · see citing works
Lumsden, A., Clarke, J. D. W., Keynes, R. J., & Fraser, S. E. (1994) · Development · doi:10.1242/dev.120.6.1581 · Cited by 66 · see citing works
Region-specific cell clones in the developing spinal cord of the zebrafish
Papan, C., & Campos‐Ortega, J. A. (1999) · Development Genes and Evolution · doi:10.1007/s004270050237 · Cited by 32 · see citing works
Self-citationDorsal and Ventral Cell Types Can Arise from Common Neural Tube Progenitors
Artinger, K., Fraser, S. E., & Bronner-Fraser, M. E. (1995) · Developmental Biology · doi:10.1006/dbio.1995.8038 · Cited by 32 · see citing works
Soula, C., Foulquier, F., Duprat, A. M., & Cochard, P. (1993) · Developmental Biology · doi:10.1006/dbio.1993.1233 · Cited by 16 · see citing works
A clonal analysis of spinal cord development in the zebrafish
Papan, C., & Campos‐Ortega, J. A. (1997) · Development Genes and Evolution · doi:10.1007/s004270050093 · Cited by 15 · see citing works
Self-citation
Flagged first, then by citations
1 of the 64 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Kosodo, Y., Röper, K., Haubensak, W. E., Marzesco, A., Corbeil, D., & Huttner, W. Β. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600223 · Cited by 435 · see citing works
Planar cell polarity signalling couples cell division and morphogenesis during neurulation
Ciruna, B. G., Jenny, A., Lee, D. W., Mlodzik, M., & Schier, A. F. (2006) · Nature · doi:10.1038/nature04375 · Cited by 400 · see citing works
Asymmetric cell divisions promote Notch-dependent epidermal differentiation
Williams, S. E., Beronja, S., Pasolli, H. A., & Fuchs, E. (2011) · Nature · doi:10.1038/nature09793 · Cited by 406 · see citing works
Vangl2 directs the posterior tilting and asymmetric localization of motile primary cilia
Borovina, A., Superina, S., Voskas, D., & Ciruna, B. G. (2010) · Nature Cell Biology · doi:10.1038/ncb2042 · Cited by 345 · see citing works
Regulation of Neurogenesis by Interkinetic Nuclear Migration through an Apical-Basal Notch Gradient
Bene, F. D., Wehman, A. M., Link, B. A., & Baier, H. (2008) · Cell · doi:10.1016/j.cell.2008.07.017 · Cited by 339 · see citing works
Théry, M., & Bornens, M. (2006) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2006.10.001 · Cited by 296 · see citing works
Huttner, W. Β., & Kosodo, Y. (2005) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2005.10.005 · Cited by 295 · see citing works
Campinho, P., Behrndt, M., Ranft, J., Risler, T., Minc, N., & Heisenberg, C. (2013) · Nature Cell Biology · doi:10.1038/ncb2869 · Cited by 271 · see citing works
Polarization and orientation of retinal ganglion cells in vivo
Zolessi, F. R., Poggi, L., Wilkinson, C. J., Chien, C.-B., & Harris, W. A. (2006) · Neural Development · doi:10.1186/1749-8104-1-2 · Cited by 236 · see citing works
Strategies of vertebrate neurulation and a re-evaluation of teleost neural tube formation
Lowery, L. A., & Sive, H. L. (2004) · Mechanisms of Development · doi:10.1016/j.mod.2004.04.022 · Cited by 232 · see citing works
A mirror-symmetric cell division that orchestrates neuroepithelial morphogenesis
Tawk, M., Araya, C., Lyons, D. A., Reugels, A. M., Girdler, G. C., Bayley, P. R., Hyde, D. R., Tada, M., & Clarke, J. D. W. (2007) · Nature · doi:10.1038/nature05722 · Cited by 217 · see citing works
Self-citationAsymmetric cell division during neurogenesis in Drosophila and vertebrates
Wodarz, A., & Huttner, W. Β. (2003) · Mechanisms of Development · doi:10.1016/j.mod.2003.06.003 · Cited by 198 · see citing works
Campinho, P., Behrndt, M., Ranft, J., Risler, T., Minc, N., & Heisenberg, C. (2013) · MPG.PuRe (Max Planck Society) · Cited by 194 · see citing works
Ben-Yair, R., & Kalcheim, C. (2005) · Development · doi:10.1242/dev.01617 · Cited by 187 · see citing works
Influences on neural lineage and mode of division in the zebrafish retina in vivo
Poggi, L., Vitorino, M., Masai, I., & Harris, W. A. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200509098 · Cited by 181 · see citing works
EphA4 Is Required for Cell Adhesion and Rhombomere-Boundary Formation in the Zebrafish
Cooke, J. E., Kemp, H. A., & Moens, C. B. (2005) · Current Biology · doi:10.1016/j.cub.2005.02.019 · Cited by 174 · see citing works
Cell Division Orientation in Animals
Gillies, T. E., & Cabernard, C. (2011) · Current Biology · doi:10.1016/j.cub.2011.06.055 · Cited by 173 · see citing works
Scribble: A master scaffold in polarity, adhesion, synaptogenesis, and proliferation
Bonello, T. T., & Peifer, M. (2019) · Journal of Cell Biology · doi:10.1083/jcb.201810103 · Cited by 127 · see citing works
“Most cell divisions are parallel to the epithelial sheet, but during the neural keel/rod phase, this changes (Geldmacher-Voss et al., 2003; Žigman et al., 2011).”
BackgroundN-cadherinis required for the polarized cell behaviors that drive neurulation in the zebrafish
Hong, E., & Brewster, R. M. (2006) · Development · doi:10.1242/dev.02560 · Cited by 127 · see citing works
Totally tubular: the mystery behind function and origin of the brain ventricular system
Lowery, L. A., & Sive, H. L. (2009) · BioEssays · doi:10.1002/bies.200800207 · Cited by 116 · see citing works
Hernandez, R. E., Rikhof, H. A., Bachmann‐Gagescu, R., & Moens, C. B. (2004) · Development · doi:10.1242/dev.01297 · Cited by 112 · see citing works
Takle, H., Bæverfjord, G., Lunde, M., Kolstad, K., & Andersen, Ø. (2005) · Aquaculture · doi:10.1016/j.aquaculture.2005.04.043 · Cited by 112 · see citing works
Reversible Optogenetic Control of Subcellular Protein Localization in a Live Vertebrate Embryo
Buckley, C. E., Moore, R. E., Reade, A., Goldberg, A. R., Weiner, O. D., & Clarke, J. D. W. (2016) · Developmental Cell · doi:10.1016/j.devcel.2015.12.011 · Cited by 109 · see citing works
Protocadherin-19 and N-cadherin interact to control cell movements during anterior neurulation
Biswas, S., Emond, M. R., & Jontes, J. D. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201007008 · Cited by 109 · see citing works
Stereotypical Cell Division Orientation Controls Neural Rod Midline Formation in Zebrafish
Quesada-Hernández, E., Caneparo, L., Kaufmann, S., Winkler, S., Liebling, M., Fraser, S. E., & Heisenberg, C. (2010) · Current Biology · doi:10.1016/j.cub.2010.10.009 · Cited by 97 · see citing works
Mechanical Forces Program the Orientation of Cell Division during Airway Tube Morphogenesis
Tang, Z., Hu, Y., Wang, Z., Jiang, K., Zhan, C., Marshall, W. F., & Tang, N. (2018) · Developmental Cell · doi:10.1016/j.devcel.2017.12.013 · Cited by 86 · see citing works
Mitotic cell rounding and epithelial thinning regulate lumen growth and shape
Hoijman, E., Rubbini, D., Colombelli, J., & Alsina, B. (2015) · Nature Communications · doi:10.1038/ncomms8355 · Cited by 85 · see citing works
Ivanovitch, K., Cavodeassi, F., & Wilson, S. W. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.09.023 · Cited by 84 · see citing works
PAR3 acts as a molecular organizer to define the apical domain of chick neuroepithelial cells
Afonso, C., & Henrique, D. (2006) · Journal of Cell Science · doi:10.1242/jcs.03170 · Cited by 84 · see citing works
Mechanics and Regulation of Cell Shape During the Cell Cycle
Clark, A. G., & Paluch, E. K. (2011) · Results and problems in cell differentiation · doi:10.1007/978-3-642-19065-0_3 · Cited by 81 · see citing works
Lee, J. D., Silva-Gagliardi, N. F., Tepaß, U., McGlade, C. J., & Anderson, K. V. (2007) · Development · doi:10.1242/dev.000885 · Cited by 82 · see citing works
Zic1 and Zic4 regulate zebrafish roof plate specification and hindbrain ventricle morphogenesis
Elsen, G. E., Choi, L. Y., Millen, K. J., Grinblat, Y., & Prince, V. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2007.12.006 · Cited by 78 · see citing works
Zebrafish neural tube morphogenesis requires Scribble-dependent oriented cell divisions
Žigman, M., Trinh, L. A., Fraser, S. E., & Moens, C. B. (2011) · Current Biology · doi:10.1016/j.cub.2010.12.005 · Cited by 71 · see citing works
Gil, C., Landeira, B. S., Ramos, C., Costa, M. R., & Müller, U. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1793-14.2014 · Cited by 66 · see citing works
Tanabe, K., Kani, S., Shimizu, T., Bae, Y., Abe, T., & Hibi, M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3352-10.2010 · Cited by 71 · see citing works
Kemp, H. A., Cooke, J. E., & Moens, C. B. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.12.010 · Cited by 68 · see citing works
PAR-1 Phosphorylates Mind Bomb to Promote Vertebrate Neurogenesis
Ossipova, O., Ezan, J., & Sokol, S. Y. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.06.010 · Cited by 67 · see citing works
Azuma, M., Embree, L. J., Sabaawy, H. E., & Hickstein, D. D. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000979 · Cited by 68 · see citing works
The zebrafish Pard3 ortholog is required for separation of the eye fields and retinal lamination
Wei, X., Cheng, Y., Luo, Y., Shi, X., Nelson, S., & Hyde, D. R. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.01.017 · Cited by 67 · see citing works
Hudish, L. I., Blasky, A. J., & Appel, B. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.10.015 · Cited by 60 · see citing works
The polarity protein Pard3 is required for centrosome positioning during neurulation
Hong, E., Jayachandran, P., & Brewster, R. M. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.01.034 · Cited by 61 · see citing works
Recher, G., Jouralet, J., Brombin, A., Heuzé, A., Dambroise, E., Hermel, J., Salomé‐Desnoulez, S., Savy, T., Herbomel, P., Bourrat, F., et al. (2013) · Development · doi:10.1242/dev.099010 · Cited by 58 · see citing works
Regulation of neurocoel morphogenesis by Pard6γb
Munson, C., Huisken, J., Bit‐Avragim, N., Kuo, T., Dong, P. D. S., Ober, E. A., Verkade, H. M., Abdelilah‐Seyfried, S., & Stainier, D. Y. R. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.08.033 · Cited by 58 · see citing works
Borovina, A., & Ciruna, B. G. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.08.043 · Cited by 53 · see citing works
Strauss, B., Adams, R. J., & Papalopulu, N. (2006) · Development · doi:10.1242/dev.02578 · Cited by 53 · see citing works
Comparative analysis of neurulation: First impressions do not count
Harrington, M., Hong, E., & Brewster, R. M. (2009) · Molecular Reproduction and Development · doi:10.1002/mrd.21085 · Cited by 51 · see citing works
Kee, N., Wilson, N. H., Vries, M. D., Bradford, D., Key, B., & Cooper, H. M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4265-08.2008 · Cited by 49 · see citing works
Asymmetric Cell Divisions in the Epidermis
Poulson, N. D., & Lechler, T. (2012) · International review of cytology · doi:10.1016/b978-0-12-394306-4.00012-5 · Cited by 48 · see citing works
Spindle orientation in animal cell mitosis: Roles of integrin in the control of spindle axis
Toyoshima, F., & Nishida, E. (2007) · Journal of Cellular Physiology · doi:10.1002/jcp.21227 · Cited by 49 · see citing works
Role of polarized cell divisions in zebrafish neural tube formation
Clarke, J. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.04.010 · Cited by 49 · see citing works
Chapter 6 Cellular and Molecular Mechanisms Underlying the Formation of Biological Tubes
Baer, M. M., Chanut-Delalande, H., & Affolter, M. (2009) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(09)89006-6 · Cited by 48 · see citing works
Microtubules, polarity and vertebrate neural tube morphogenesis
Cearns, M. D., Escuin, S., Alexandre, P., Greene, N. D. E., & Copp, A. J. (2016) · Journal of Anatomy · doi:10.1111/joa.12468 · Cited by 46 · see citing works
Cellular and molecular mechanisms of convergence and extension in zebrafish
Williams, M. K., & Solnica‐Krezel, L. (2020) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2019.08.001 · Cited by 47 · see citing works
Bryan, C. D., Chien, C.-B., & Kwan, K. M. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.06.025 · Cited by 46 · see citing works
Claudin‐5a in developing zebrafish brain barriers: another brick in the wall
Abdelilah‐Seyfried, S. (2010) · BioEssays · doi:10.1002/bies.201000045 · Cited by 45 · see citing works
Chen, X., An, Y., Gao, Y., Guo, L., Lei, R. L., Xie, H., Sun, M., Hung, S. L., Sheng, X., Zou, J., et al. (2016) · Human Mutation · doi:10.1002/humu.23153 · Cited by 47 · see citing works
Kieserman, E. K., & Wallingford, J. B. (2009) · Journal of Cell Science · doi:10.1242/jcs.042135 · Cited by 43 · see citing works
Cellular mechanisms of posterior neural tube morphogenesis in the zebrafish
Harrington, M., Chalasani, K., & Brewster, R. M. (2010) · Developmental Dynamics · doi:10.1002/dvdy.22184 · Cited by 43 · see citing works
Analysis of aPKCλ and aPKCζ reveals multiple and redundant functions during vertebrate retinogenesis
Cui, S., Otten, C., Rohr, S., Abdelilah‐Seyfried, S., & Link, B. A. (2007) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2006.11.016 · Cited by 43 · see citing works
Reugels, A. M., Boggetti, B., Scheer, N., & Campos‐Ortega, J. A. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20699 · Cited by 41 · see citing works
Self-citationCoordinating cell and tissue behavior during zebrafish neural tube morphogenesis
Araya, C., Ward, L., Girdler, G. C., & Miranda, M. (2015) · Developmental Dynamics · doi:10.1002/dvdy.24304 · Cited by 41 · see citing works
Bingham, S. M., Chaudhari, S. R., Vanderlaan, G., Itoh, M., Chitnis, A. B., & Chandrasekhar, A. (2003) · Developmental Dynamics · doi:10.1002/dvdy.10429 · Cited by 40 · see citing works
Mesoderm is required for coordinated cell movements within zebrafish neural plate in vivo
Araya, C., Tawk, M., Girdler, G. C., Costa, M., Carmona‐Fontaine, C., & Clarke, J. D. W. (2014) · Neural Development · doi:10.1186/1749-8104-9-9 · Cited by 39 · see citing works
Signaling in the third dimension: The peripodial epithelium in eye disc development
Atkins, M., & Mardon, G. (2009) · Developmental Dynamics · doi:10.1002/dvdy.22034 · Cited by 38 · see citing works
Oriented cell division in vertebrate embryogenesis
Castanon, I., & González‐Gaitán, M. (2011) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2011.09.009 · Cited by 37 · see citing works
miR-430 regulates oriented cell division during neural tube development in zebrafish
Takacs, C. M., & Giráldez, A. J. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.11.016 · Cited by 37 · see citing works
Stretching Morphogenesis of the Roof Plate and Formation of the Central Canal
Kondrychyn, I., Teh, C., Sin, M., & Korzh, V. P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056219 · Cited by 36 · see citing works
Cell Fate Decision Making through Oriented Cell Division
Dewey, E. B., Taylor, D. T., & Johnston, C. A. (2015) · Journal of Developmental Biology · doi:10.3390/jdb3040129 · Cited by 35 · see citing works
von Trotha, J. W., Campos‐Ortega, J. A., & Reugels, A. M. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20715 · Cited by 36 · see citing works
Self-citationBlasky, A. J., Pan, L., Moens, C. B., & Appel, B. (2014) · Developmental Dynamics · doi:10.1002/dvdy.24172 · Cited by 35 · see citing works
Telophase correction refines division orientation in stratified epithelia
Lough, K. J., Byrd, K. M., Descovich, C. P., Spitzer, D. C., Bergman, A. J., Beaudoin, G. M. J., Reichardt, L. F., & Williams, S. E. (2019) · eLife · doi:10.7554/elife.49249 · Cited by 31 · see citing works
Nyholm, M. K., Abdelilah‐Seyfried, S., & Grinblat, Y. (2009) · Journal of Cell Science · doi:10.1242/jcs.043471 · Cited by 35 · see citing works
Yang, X., Zou, J., Hyde, D. R., Davidson, L. A., & Wei, X. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1880-09.2009 · Cited by 33 · see citing works
Control of convergent yolk syncytial layer nuclear movement in zebrafish
Carvalho, L., Stühmer, J., Bois, J. S., Kalaidzidis, Y. L., Lecaudey, V., & Heisenberg, C. (2009) · Development · doi:10.1242/dev.026922 · Cited by 32 · see citing works
Apicobasal polarity and neural tube closure
Eom, D. S., Amarnath, S., & Agarwala, S. (2012) · Development Growth & Differentiation · doi:10.1111/dgd.12030 · Cited by 30 · see citing works
N-cadherin–mediated cell adhesion restricts cell proliferation in the dorsal neural tube
Chalasani, K., & Brewster, R. M. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e10-08-0675 · Cited by 28 · see citing works
Žigman, M., Laumann-Lipp, N., Titus, T. A., Postlethwait, J. H., & Moens, C. B. (2014) · Development · doi:10.1242/dev.098731 · Cited by 27 · see citing works
Zhang, S. O., & Weisblat, D. A. (2005) · Development · doi:10.1242/dev.01802 · Cited by 26 · see citing works
Organization and physiology of the zebrafish nervous system
Bally‐Cuif, L., & Vernier, P. (2010) · Fish physiology · doi:10.1016/s1546-5098(10)02902-x · Cited by 25 · see citing works
Methods for Expressing and Analyzing GFP-Tubulin and GFP-Microtubule-Associated ProteinsPreprint
Goodson, H. V., Dzurisin, J. S., & Wadsworth, P. (2010) · Cold Spring Harbor Protocols · doi:10.1101/pdb.top85 · Cited by 25 · see citing works
Subnuclear development of the zebrafish habenular nuclei requires ER translocon function
Doll, C. A., Burkart, J. T., Hope, K. D., Halpern, M. E., & Gamse, J. T. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.09.003 · Cited by 22 · see citing works
Wu, M., Wu, Z., Zou, Q., Wang, J., Kam, C., Chen, S., & Feng, S. (2022) · Chemical Engineering Journal · doi:10.1016/j.cej.2022.140189 · Cited by 23 · see citing works
Characterization of harpy/Rca1/emi1 mutants: Patterning in the absence of cell division
Riley, B. B., Sweet, E. M., Heck, R., Evans, A., McFarland, K. N., Warga, R. M., & Kane, D. A. (2010) · Developmental Dynamics · doi:10.1002/dvdy.22227 · Cited by 22 · see citing works
Rajagopalan, S., Bimbó, A., Balasubramanian, M. K., & Oliferenko, S. (2004) · Current Biology · doi:10.1016/j.cub.2003.12.027 · Cited by 22 · see citing works
Association Study of PARD3 Gene Polymorphisms With Neural Tube Defects in a Chinese Han Population
Gao, Y., Chen, X., Shangguan, S., Bao, Y., Lü, X.-L., Zou, J., Guo, J., Dai, Y., & Zhang, T. (2012) · Reproductive Sciences · doi:10.1177/1933719111433886 · Cited by 25 · see citing works
Basement Membrane Diseases in Zebrafish
Feitosa, N. M., Richardson, R. J., Bloch, W., & Hammerschmidt, M. (2011) · Methods in cell biology · doi:10.1016/b978-0-12-381320-6.00008-4 · Cited by 21 · see citing works
Girdler, G. C., Araya, C., Ren, X., & Clarke, J. D. W. (2013) · Neural Development · doi:10.1186/1749-8104-8-5 · Cited by 20 · see citing works
Discs large 1 controls daughter-cell polarity after cytokinesis in vertebrate morphogenesis
Li, Y., Junge, J. A., Arnesano, C., Gross, G. G., Miner, J. H., Moats, R. A., Roberts, R. W., Arnold, D. B., & Fraser, S. E. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1713959115 · Cited by 18 · see citing works
Notch-mediated inhibition of neurogenesis is required for zebrafish spinal cord morphogenesis
Sharma, P., Saraswathy, V. M., Xiang, L., & Fürthauer, M. (2019) · Scientific Reports · doi:10.1038/s41598-019-46067-1 · Cited by 18 · see citing works
Takamiya, M., & Campos‐Ortega, J. A. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20720 · Cited by 18 · see citing works
Self-citationNeurulation: coordinating cell polarisation and lumen formation
Compagnon, J., & Heisenberg, C. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.325 · Cited by 17 · see citing works
Apical Cell-Cell Adhesions Reconcile Symmetry and Asymmetry in Zebrafish Neurulation
Guo, C., Zou, J., Wen, Y., Fang, W., Stolz, D. B., Sun, M., & Wei, X. (2018) · iScience · doi:10.1016/j.isci.2018.04.007 · Cited by 17 · see citing works
Rgma-Induced Neo1 Proteolysis Promotes Neural Tube Morphogenesis
Brown, S. P., Jayachandran, P., Negesse, M. Y., Olmo, V. N., Vital, E., & Brewster, R. M. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.3262-18.2019 · Cited by 17 · see citing works
Chapouton, P., & Bally‐Cuif, L. (2004) · Methods in cell biology · doi:10.1016/s0091-679x(04)76010-0 · Cited by 17 · see citing works
Oriented cell division: new roles in guiding skin wound repair and regeneration
Yang, S., Ma, K., Geng, Z., Sun, X., & Fu, X. (2015) · Bioscience Reports · doi:10.1042/bsr20150225 · Cited by 16 · see citing works
Mitotic, but not meiotic, oriented cell divisions in rat spermatogenesis
Lagos‐Cabré, R., & Moreno, R. D. (2008) · Reproduction · doi:10.1530/rep-07-0389 · Cited by 16 · see citing works
The cfy mutation disrupts cell divisions in a stage-dependent manner in zebrafish embryos
Song, M. H., Brown, N. L., & Kuwada, J. Y. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.08.041 · Cited by 15 · see citing works
Wnt Signaling Mediates Diverse Developmental Processes in Zebrafish
Verkade, H. M., & Heath, J. K. (2008) · Methods in molecular biology · doi:10.1007/978-1-60327-469-2_17 · Cited by 14 · see citing works
Apical polarity protein PrkCi is necessary for maintenance of spinal cord precursors in zebrafish
Roberts, R. K., & Appel, B. (2009) · Developmental Dynamics · doi:10.1002/dvdy.21970 · Cited by 14 · see citing works
Stretching cell morphogenesis during late neurulation and mild neural tube defects
Korzh, V. P. (2014) · Development Growth & Differentiation · doi:10.1111/dgd.12143 · Cited by 14 · see citing works
- Authors
- Geldmacher-Voss, B., Reugels, A. M., Pauls, S., & Campos-Ortega, J. A.
- Affiliations
- University of Cologne (DE)
- Institut für Entwicklungsbiologie, Universität zu Köln,50923 Köln, Germany
- Corresponding author
- Pauls, Stefan
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2003-08-15
- Volume
- 130
- Issue
- 16
- Pages
- 3767-3780
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- OpenAlex
- W2035602354
- Cited by
- 144
- References
- 64
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 2 · 2023: 3 · 2022: 4 · 2021: 2 · 2020: 4 · 2019: 4 · 2018: 6 · 2017: 2 · 2016: 5 · 2015: 6 · 2014: 6 · 2013: 9 · 2012: 5
- FWCI
- 3.52
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Development (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- neuroepithelial cells, neural plate, cell junctions, adherens junctions, tight junctions, epithelial polarity, ASIP, neural tube patterning, cell division
- MeSH terms
- Protein Kinase C zeta, Protein Kinase C-lambda, Animals, Carrier Proteins, Cell Movement, Central Nervous System, Epithelial Cells, Isoenzymes, Microinjections, Mitosis, Spindle Apparatus, Protein Kinase C, Recombinant Fusion Proteins, RNA, Messenger, Zebrafish, Biomarkers, Oligonucleotides, Antisense, Cell Polarity, Transgenes, Zebrafish Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
