Analysis of cellular behavior and cytoskeletal dynamics reveal a constriction mechanism driving optic cup morphogenesis

eLife - Tập 5
María Nicolás-Pérez1, Franz Kuchling2,1, Joaquín Letelier1, Rocío Polvillo1, Joachim Wittbrodt2, Juan Ramón Martínez-Morales1
1Centro Andaluz de Biología del Desarrollo, Seville, Spain
2Centre for Organismal Studies (COS), University of Heidelberg, Heidelberg, Germany

Tóm tắt

Contractile actomyosin networks have been shown to power tissue morphogenesis. Although the basic cellular machinery generating mechanical tension appears largely conserved, tensions propagate in unique ways within each tissue. Here we use the vertebrate eye as a paradigm to investigate how tensions are generated and transmitted during the folding of a neuroepithelial layer. We record membrane pulsatile behavior and actomyosin dynamics during zebrafish optic cup morphogenesis by live imaging. We show that retinal neuroblasts undergo fast oscillations and that myosin condensation correlates with episodic contractions that progressively reduce basal feet area. Interference with lamc1 function impairs basal contractility and optic cup folding. Mapping of tensile forces by laser cutting uncover a developmental window in which local ablations trigger the displacement of the entire tissue. Our work shows that optic cup morphogenesis is driven by a constriction mechanism and indicates that supra-cellular transmission of mechanical tension depends on ECM attachment.

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Tài liệu tham khảo

Aigouy, 2010, Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila, Cell, 142, 773, 10.1016/j.cell.2010.07.042

Barron, 1994, Performance of optical flow techniques, International Journal of Computer Vision, 12, 43, 10.1007/BF01420984

Behrndt, 2012, Forces driving epithelial spreading in zebrafish gastrulation, Science, 338, 257, 10.1126/science.1224143

Bogdanović, 2012, Numb/Numbl-Opo antagonism controls retinal epithelium morphogenesis by regulating integrin endocytosis, Developmental Cell, 23, 782, 10.1016/j.devcel.2012.09.004

Bradski, 2008, Learning OpenCV

Brown, 2010, Nlcam modulates midline convergence during anterior neural plate morphogenesis, Developmental Biology, 339, 14, 10.1016/j.ydbio.2009.12.003

Burkel, 2007, Versatile fluorescent probes for actin filaments based on the actin-binding domain of utrophin, Cell Motility and the Cytoskeleton, 64, 822, 10.1002/cm.20226

Chauhan, 2009, Cdc42- and IRSp53-dependent contractile filopodia tether presumptive lens and retina to coordinate epithelial invagination, Development, 136, 3657, 10.1242/dev.042242

Domogatskaya, 2012, Functional diversity of laminins, Annual Review of Cell and Developmental Biology, 28, 523, 10.1146/annurev-cellbio-101011-155750

Eiraku, 2012, Relaxation-expansion model for self-driven retinal morphogenesis: a hypothesis from the perspective of biosystems dynamics at the multi-cellular level, BioEssays, 34, 17, 10.1002/bies.201100070

Eiraku, 2011, Self-organizing optic-cup morphogenesis in three-dimensional culture, Nature, 472, 51, 10.1038/nature09941

England, 2006, A dynamic fate map of the forebrain shows how vertebrate eyes form and explains two causes of cyclopia, Development, 133, 4613, 10.1242/dev.02678

Fuhrmann, 2010, Eye morphogenesis and patterning of the optic vesicle, Current Topics in Developmental Biology, 93, 61, 10.1016/B978-0-12-385044-7.00003-5

Gago-Rodrigues, 2015, Analysis of opo cis-regulatory landscape uncovers Vsx2 requirement in early eye morphogenesis, Nature Communications, 6, 7054, 10.1038/ncomms8054

Gorfinkiel, 2011, Dynamics of actomyosin contractile activity during epithelial morphogenesis, Current Opinion in Cell Biology, 23, 531, 10.1016/j.ceb.2011.06.002

He, 2010, Tissue elongation requires oscillating contractions of a basal actomyosin network, Nature Cell Biology, 12, 1133, 10.1038/ncb2124

Heermann, 2015, Eye morphogenesis driven by epithelial flow into the optic cup facilitated by modulation of bone morphogenetic protein, eLife, 4, e05216, 10.7554/eLife.05216

Heisenberg, 2013, Forces in tissue morphogenesis and patterning, Cell, 153, 948, 10.1016/j.cell.2013.05.008

Hilfer, 1983, Development of the eye of the chick embryo, Scanning Electron Microscopy, 1353

Ivanovitch, 2013, Precocious acquisition of neuroepithelial character in the eye field underlies the onset of eye morphogenesis, Developmental Cell, 27, 293, 10.1016/j.devcel.2013.09.023

Jodoin, 2015, Stable force balance between epithelial cells arises from F-actin turnover, Developmental Cell, 35, 685, 10.1016/j.devcel.2015.11.018

Kim, 2011, Punctuated actin contractions during convergent extension and their permissive regulation by the non-canonical Wnt-signaling pathway, Journal of Cell Science, 124, 635, 10.1242/jcs.067579

Kimmel, 1995, Stages of embryonic development of the zebrafish, Developmental Dynamics, 203, 253, 10.1002/aja.1002030302

Kovács, 2004, Mechanism of blebbistatin inhibition of myosin II, Journal of Biological Chemistry, 279, 35557, 10.1074/jbc.M405319200

Kwan, 2007, The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs, Developmental Dynamics, 236, 3088, 10.1002/dvdy.21343

Kwan, 2012, A complex choreography of cell movements shapes the vertebrate eye, Development, 139, 359, 10.1242/dev.071407

Lecuit, 2011, Force generation, transmission, and integration during cell and tissue morphogenesis, Annual Review of Cell and Developmental Biology, 27, 157, 10.1146/annurev-cellbio-100109-104027

Lee, 2007, Laminin beta1 and gamma1 containing laminins are essential for basement membrane integrity in the zebrafish eye, Investigative Opthalmology & Visual Science, 48, 2483, 10.1167/iovs.06-1211

Levayer, 2012, Biomechanical regulation of contractility: spatial control and dynamics, Trends in Cell Biology, 22, 61, 10.1016/j.tcb.2011.10.001

Li, 2000, The morphogenesis of the zebrafish eye, including a fate map of the optic vesicle, Developmental Dynamics, 218, 175, 10.1002/(SICI)1097-0177(200005)218:1<175::AID-DVDY15>3.0.CO;2-K

Lowery, 2004, Strategies of vertebrate neurulation and a re-evaluation of teleost neural tube formation, Mechanisms of Development, 121, 1189, 10.1016/j.mod.2004.04.022

Mammoto, 2013, Mechanobiology and developmental control, Annual Review of Cell and Developmental Biology, 29, 27, 10.1146/annurev-cellbio-101512-122340

Martin, 2009, Pulsed contractions of an actin-myosin network drive apical constriction, Nature, 457, 495, 10.1038/nature07522

Martinez-Morales, 2009, ojoplano-mediated basal constriction is essential for optic cup morphogenesis, Development, 136, 2165, 10.1242/dev.033563

Martinez-Morales, 2009, Shaping the vertebrate eye, Current Opinion in Genetics & Development, 19, 511, 10.1016/j.gde.2009.08.003

Medeiros, 2006, Myosin II functions in actin-bundle turnover in neuronal growth cones, Nature Cell Biology, 8, 215, 10.1038/ncb1367

Nakano, 2012, Self-formation of optic cups and storable stratified neural retina from human ESCs, Cell Stem Cell, 10, 771, 10.1016/j.stem.2012.05.009

Nishimura, 2012, Planar cell polarity links axes of spatial dynamics in neural-tube closure, Cell, 149, 1084, 10.1016/j.cell.2012.04.021

Papusheva, 2010, Spatial organization of adhesion: force-dependent regulation and function in tissue morphogenesis, The EMBO Journal, 29, 2753, 10.1038/emboj.2010.182

Parsons, 2002, Zebrafish mutants identify an essential role for laminins in notochord formation, Development, 129, 3137, 10.1242/dev.129.13.3137

Picker, 2009, Dynamic coupling of pattern formation and morphogenesis in the developing vertebrate retina, PLoS Biology, 7, e1000214, 10.1371/journal.pbio.1000214

Pollard, 2003, Cellular motility driven by assembly and disassembly of actin filaments, Cell, 112, 453, 10.1016/S0092-8674(03)00120-X

Rauzi, 2010, Planar polarized actomyosin contractile flows control epithelial junction remodelling, Nature, 468, 1110, 10.1038/nature09566

Rembold, 2006, Individual cell migration serves as the driving force for optic vesicle evagination, Science, 313, 1130, 10.1126/science.1127144

Roh-Johnson, 2012, Triggering a cell shape change by exploiting preexisting actomyosin contractions, Science, 335, 1232, 10.1126/science.1217869

Salbreux, 2012, Actin cortex mechanics and cellular morphogenesis, Trends in Cell Biology, 22, 536, 10.1016/j.tcb.2012.07.001

Sawyer, 2010, Apical constriction: a cell shape change that can drive morphogenesis, Developmental Biology, 341, 5, 10.1016/j.ydbio.2009.09.009

Schindelin, 2012, Fiji: an open-source platform for biological-image analysis, Nature Methods, 9, 676, 10.1038/nmeth.2019

Schmitt, 1994, Early eye morphogenesis in the zebrafish, Brachydanio rerio, The Journal of Comparative Neurology, 344, 532, 10.1002/cne.903440404

Schook, 1980, Morphogenetic movements during the early development of the chick eye. An ultrastructural and spatial reconstructive study. B. Invagination of the optic vesicle and fusion of its walls, Acta Morphologica Neerlando-Scandinavica, 18, 159

Shi, 1994, Good Features to Track. 9th IEEE Conference on Computer Vision and Pattern Recognition

Sinn, 2013, An eye on eye development, Mechanisms of Development, 130, 347, 10.1016/j.mod.2013.05.001

Solon, 2009, Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure, Cell, 137, 1331, 10.1016/j.cell.2009.03.050

Spemann, 1901, Über die korrelation der entwicklung des auges, Verhandlungen Der Anatomischen Gesellschaft, 15, 61

Westerfield, 2000, The Zebrafish Book. a Guide for the Laboratory Use of Zebrafish (Danio Rerio)

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