A non-cell-autonomous actin redistribution enables isotropic retinal growth

Tissue shape is often established early in development and needs to be scaled isotropically during growth. However, the cellular contributors and ways in which cells interact inside tissues to enable coordinated isotropic tissue scaling are not yet understood. Here, we follow cell and tissue shape changes in the zebrafish retinal neuroepithelium, which forms a cup with a smooth surface early in development and maintains this architecture as it grows. By combining 3D analysis and theory, we show that a global increase in cell height is necessary to maintain this tissue shape during growth. Timely cell height increase is governed by non-cell autonomous actin redistribution. Blocking actin redistribution and cell height increase perturbs isotropic scaling and leads to disturbed, folded tissue shape. Taken together, our data show how global changes in cell shape enable isotropic growth of the developing retinal neuroepithelium, a concept that could also apply to other systems.

[1]  Jakob Grove,et al.  Common schizophrenia alleles are enriched in mutation-intolerant genes and in regions under strong background selection , 2018, Nature Genetics.

[2]  S. Pașca,et al.  The rise of three-dimensional human brain cultures , 2018, Nature.

[3]  James K. Chen,et al.  Basal constriction during midbrain–hindbrain boundary morphogenesis is mediated by Wnt5b and focal adhesion kinase , 2018, Biology Open.

[4]  Marius Ader,et al.  Organoid technology for retinal repair. , 2018, Developmental biology.

[5]  C. Norden,et al.  Phototoxicity in live fluorescence microscopy, and how to avoid it , 2017, BioEssays : news and reviews in molecular, cellular and developmental biology.

[6]  J. C. Pastor-Pareja,et al.  Basement Membrane Manipulation in Drosophila Wing Discs Affects Dpp Retention but Not Growth Mechanoregulation. , 2017, Developmental cell.

[7]  Ana Rolo,et al.  Biomechanical coupling facilitates spinal neural tube closure in mouse embryos , 2017, Proceedings of the National Academy of Sciences.

[8]  C. Norden,et al.  Pseudostratified epithelia – cell biology, diversity and roles in organ formation at a glance , 2017, Journal of Cell Science.

[9]  Natalie A. Dye,et al.  Cell dynamics underlying oriented growth of the Drosophila wing imaginal disc , 2017, Development.

[10]  C. Norden,et al.  Concerted action of neuroepithelial basal shrinkage and active epithelial migration ensures efficient optic cup morphogenesis , 2017, bioRxiv.

[11]  Maurício Rocha-Martins,et al.  Independent modes of ganglion cell translocation ensure correct lamination of the zebrafish retina , 2016, bioRxiv.

[12]  K. Anderson,et al.  The tumor suppressor PTEN and the PDK1 kinase regulate formation of the columnar neural epithelium , 2016, eLife.

[13]  Lars Hufnagel,et al.  Embryo-scale tissue mechanics during Drosophila gastrulation movements , 2015, Nature Communications.

[14]  P. Strzyz,et al.  Centriole Amplification in Zebrafish Affects Proliferation and Survival but Not Differentiation of Neural Progenitor Cells. , 2015, Cell reports.

[15]  Pierre-François Lenne,et al.  Local and tissue-scale forces drive oriented junction growth during tissue extension , 2015, Nature Cell Biology.

[16]  Corinna Blasse,et al.  Interplay of cell dynamics and epithelial tension during morphogenesis of the Drosophila pupal wing , 2015, eLife.

[17]  A. Kawaguchi,et al.  Interkinetic nuclear migration generates and opposes ventricular-zone crowding: insight into tissue mechanics , 2015, Front. Cell. Neurosci..

[18]  P. Strzyz,et al.  Interkinetic nuclear migration is centrosome independent and ensures apical cell division to maintain tissue integrity. , 2015, Developmental cell.

[19]  Kenneth M. Yamada,et al.  Local and global dynamics of the basement membrane during branching morphogenesis require protease activity and actomyosin contractility. , 2014, Developmental biology.

[20]  K. Kwan.  Coming into focus: The role of extracellular matrix in vertebrate optic cup morphogenesis , 2014, Developmental dynamics : an official publication of the American Association of Anatomists.

[21]  J. García-Aznar,et al.  Image Analysis for the Quantitative Comparison of Stress Fibers and Focal Adhesions , 2014, PloS one.

[22]  W. Harris,et al.  Spectrum of Fates: a new approach to the study of the developing zebrafish retina , 2014, Development.

[23]  Elias T. Zambidis,et al.  Generation of three dimensional retinal tissue with functional photoreceptors from human iPSCs , 2014, Nature Communications.

[24]  G. Blanchard,et al.  Article a Dynamic Microtubule Cytoskeleton Directs Medial Actomyosin Function during Tube Formation , 2022 .

[25]  William A. Harris,et al.  Spectrum of Fates: a new approach to the study of the developing zebrafish retina , 2014, Development.

[26]  P. Strzyz,et al.  Mitotic position and morphology of committed precursor cells in the zebrafish retina adapt to architectural changes upon tissue maturation. , 2014, Cell reports.

[27]  Periklis Pantazis,et al.  Advances in whole-embryo imaging: a quantitative transition is underway , 2014, Nature Reviews Molecular Cell Biology.

[28]  Taiji Adachi,et al.  TAG-1–assisted progenitor elongation streamlines nuclear migration to optimize subapical crowding , 2013, Nature Neuroscience.

[29]  Y. Bellaïche,et al.  PTEN controls junction lengthening and stability during cell rearrangement in epithelial tissue. , 2013, Developmental cell.

[30]  Felix Oswald,et al.  Forces Driving Epithelial Spreading in Zebrafish Gastrulation , 2012, Science.

[31]  Guillaume Charras,et al.  Actin cortex mechanics and cellular morphogenesis. , 2012, Trends in cell biology.

[32]  W. Harris,et al.  How Variable Clones Build an Invariant Retina , 2012, Neuron.

[33]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[34]  M. Eiraku,et al.  Mouse embryonic stem cell culture for generation of three-dimensional retinal and cortical tissues , 2011, Nature Protocols.

[35]  Joachim Wittbrodt,et al.  One for All—A Highly Efficient and Versatile Method for Fluorescent Immunostaining in Fish Embryos , 2011, PloS one.

[36]  D. Montell,et al.  Tissue elongation requires oscillating contractions of a basal actomyosin network , 2010, Nature Cell Biology.

[37]  Eric F. Wieschaus,et al.  Integration of contractile forces during tissue invagination , 2010, The Journal of cell biology.

[38]  N. Shimizu,et al.  FAK-mediated extracellular signals are essential for interkinetic nuclear migration and planar divisions in the neuroepithelium , 2010, Journal of Cell Science.

[39]  Carl-Philipp Heisenberg,et al.  Biology and Physics of Cell Shape Changes in Development , 2009, Current Biology.

[40]  C. Dahmann,et al.  Dpp signaling promotes the cuboidal-to-columnar shape transition of Drosophila wing disc epithelia by regulating Rho1 , 2009, Journal of Cell Science.

[41]  H. Kennedy,et al.  Making bigger brains–the evolution of neural-progenitor-cell division , 2008, Journal of Cell Science.

[42]  C. Haslett,et al.  Mammalian NOTCH-1 Activates β1 Integrins via the Small GTPase R-Ras* , 2007, Journal of Biological Chemistry.

[43]  T. Lecuit,et al.  Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis , 2007, Nature Reviews Molecular Cell Biology.

[44]  M. Blank,et al.  Dystroglycan regulates structure, proliferation and differentiation of neuroepithelial cells in the developing vertebrate CNS. , 2007, Developmental biology.

[45]  C. Brenner,et al.  p53 Activation by Knockdown Technologies , 2007, PLoS genetics.

[46]  R. Geisler,et al.  Histone deacetylase 1 is required for cell cycle exit and differentiation in the zebrafish retina , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[47]  H. Okamoto,et al.  Histone deacetylase 1 regulates retinal neurogenesis in zebrafish by suppressing Wnt and Notch signaling pathways , 2005, Development.

[48]  Timothy J Mitchison,et al.  Screening for cell migration inhibitors via automated microscopy reveals a Rho-kinase inhibitor. , 2005, Chemistry & biology.

[49]  B. Shraiman,et al.  Mechanical feedback as a possible regulator of tissue growth. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[50]  M. S. Cooper,et al.  Visualizing morphogenesis in transgenic zebrafish embryos using BODIPY TR methyl ester dye as a vital counterstain for GFP , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[51]  Timothy J Mitchison,et al.  Dissecting Temporal and Spatial Control of Cytokinesis with a Myosin II Inhibitor , 2003, Science.

[52]  L. Hood,et al.  Activated Notch4 Inhibits Angiogenesis: Role of β1-Integrin Activation , 2002, Molecular and Cellular Biology.

[53]  S. Narumiya,et al.  Rho-kinase/ROCK is involved in cytokinesis through the phosphorylation of myosin light chain and not ezrin/radixin/moesin proteins at the cleavage furrow , 2000, Oncogene.

[54]  David A. Calderwood,et al.  Integrins and Actin Filaments: Reciprocal Regulation of Cell Adhesion and Signaling* , 2000, The Journal of Biological Chemistry.

[55]  D. Andrew,et al.  Salivary gland development in Drosophila melanogaster , 2000, Mechanisms of Development.

[56]  C. Kimmel,et al.  Stages of embryonic development of the zebrafish , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[57]  S. Ih.  Proliferative characteristics of the ependymal layer during the early development of the spinal cord in the mouse. , 1972 .

[58]  P. Strzyz,et al.  Heterogeneity, Cell Biology and Tissue Mechanics of Pseudostratified Epithelia: Coordination of Cell Divisions and Growth in Tightly Packed Tissues. , 2016, International review of cell and molecular biology.

[59]  S. Fuhrmann.  Eye morphogenesis and patterning of the optic vesicle. , 2010, Current topics in developmental biology.

[60]  L. Hood,et al.  Activated Notch4 inhibits angiogenesis: role of beta 1-integrin activation. , 2002, Molecular and cellular biology.

[61]  I. Smart.  Proliferative characteristics of the ependymal layer during the early development of the spinal cord in the mouse. , 1972, Journal of anatomy.

[62]  L. Wolpert.  Developmental Biology , 1968, Nature.