Interplay of cell dynamics and epithelial tension during morphogenesis of the Drosophila pupal wing

How tissue shape emerges from the collective mechanical properties and behavior of individual cells is not understood. We combine experiment and theory to study this problem in the developing wing epithelium of Drosophila. At pupal stages, the wing-hinge contraction contributes to anisotropic tissue flows that reshape the wing blade. Here, we quantitatively account for this wing-blade shape change on the basis of cell divisions, cell rearrangements and cell shape changes. We show that cells both generate and respond to epithelial stresses during this process, and that the nature of this interplay specifies the pattern of junctional network remodeling that changes wing shape. We show that patterned constraints exerted on the tissue by the extracellular matrix are key to force the tissue into the right shape. We present a continuum mechanical model that quantitatively describes the relationship between epithelial stresses and cell dynamics, and how their interplay reshapes the wing. DOI: http://dx.doi.org/10.7554/eLife.07090.001

[1]  Pierre-François Lenne,et al.  Direct laser manipulation reveals the mechanics of cell contacts in vivo , 2015, Proceedings of the National Academy of Sciences.

[2]  A. Inutsuka,et al.  Vangl2 Regulates E-Cadherin in Epithelial Cells , 2014, Scientific Reports.

[3]  Corinna Blasse,et al.  The Balance of Prickle/Spiny-Legs Isoforms Controls the Amount of Coupling between Core and Fat PCP Systems , 2014, Current Biology.

[4]  Mariela D. Petkova,et al.  Fly wing vein patterns have spatial reproducibility of a single cell , 2014, Journal of The Royal Society Interface.

[5]  S. Hayashi,et al.  Balance between apical membrane growth and luminal matrix resistance determines epithelial tubule shape. , 2014, Cell reports.

[6]  Lars Hufnagel,et al.  Spatial constraints control cell proliferation in tissues , 2014, Proceedings of the National Academy of Sciences.

[7]  C. Heisenberg,et al.  Forces in Tissue Morphogenesis and Patterning , 2013, Cell.

[8]  H. Strutt,et al.  The Frizzled-dependent planar polarity pathway locally promotes E-cadherin turnover via recruitment of RhoGEF2 , 2013, Development.

[9]  R. Keller,et al.  Physical Biology Returns to Morphogenesis , 2012, Science.

[10]  G. Charras,et al.  Characterizing the mechanics of cultured cell monolayers , 2012, Proceedings of the National Academy of Sciences.

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

[12]  Philippe Marcq,et al.  Mechanical Control of Morphogenesis by Fat/Dachsous/Four-Jointed Planar Cell Polarity Pathway , 2012, Science.

[13]  Jonathan E. Gale,et al.  Live-cell delamination counterbalances epithelial growth to limit tissue overcrowding , 2012, Nature.

[14]  A. Sigal,et al.  Collective and single cell behavior in epithelial contact inhibition , 2011, Proceedings of the National Academy of Sciences.

[15]  Frank Jülicher,et al.  Cell flow and tissue polarity patterns. , 2011, Current opinion in genetics & development.

[16]  Nathan J. Harris,et al.  A contractile actomyosin network linked to adherens junctions by Canoe/afadin helps drive convergent extension , 2011, Molecular biology of the cell.

[17]  Jacques Prost,et al.  Dissipative particle dynamics simulations for biological tissues: rheology and competition , 2011, Physical biology.

[18]  Gaël Varoquaux,et al.  The NumPy Array: A Structure for Efficient Numerical Computation , 2011, Computing in Science & Engineering.

[19]  Yanlan Mao,et al.  Planar polarization of the atypical myosin Dachs orients cell divisions in Drosophila. , 2011, Genes & development.

[20]  Pierre-François Lenne,et al.  Planar polarized actomyosin contractile flows control epithelial junction remodelling , 2010, Nature.

[21]  Frank Jülicher,et al.  Fluidization of tissues by cell division and apoptosis , 2010, Proceedings of the National Academy of Sciences.

[22]  Frank Jülicher,et al.  Cell Flow Reorients the Axis of Planar Polarity in the Wing Epithelium of Drosophila , 2010, Cell.

[23]  M. Baron,et al.  dumpy interacts with a large number of genes in the developing wing of Drosophila melanogaster , 2010, Fly.

[24]  L. Mahadevan,et al.  Cell shape changes indicate a role for extrinsic tensile forces in Drosophila germ-band extension , 2009, Nature Cell Biology.

[25]  Wei Dong,et al.  Directed, efficient, and versatile modifications of the Drosophila genome by genomic engineering , 2009, Proceedings of the National Academy of Sciences.

[26]  L. Mahadevan,et al.  Tissue tectonics: morphogenetic strain rates, cell shape change and intercalation , 2009, Nature Methods.

[27]  Stephan Saalfeld,et al.  Globally optimal stitching of tiled 3D microscopic image acquisitions , 2009, Bioinform..

[28]  Pierre-François Lenne,et al.  Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis , 2008, Nature Cell Biology.

[29]  Dragana Rogulja,et al.  Morphogen control of wing growth through the Fat signaling pathway. , 2008, Developmental cell.

[30]  Ana Rolo,et al.  Convergence and extension at gastrulation require a myosin IIB-dependent cortical actin network , 2008, Development.

[31]  Justin Hogan,et al.  The Frizzled Planar Cell Polarity signaling pathway controls Drosophila wing topography. , 2008, Developmental biology.

[32]  Frank Jülicher,et al.  The Influence of Cell Mechanics, Cell-Cell Interactions, and Proliferation on Epithelial Packing , 2007, Current Biology.

[33]  F Graner,et al.  Discrete rearranging disordered patterns, part I: Robust statistical tools in two or three dimensions , 2007, The European physical journal. E, Soft matter.

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

[35]  Brian E. Granger,et al.  IPython: A System for Interactive Scientific Computing , 2007, Computing in Science & Engineering.

[36]  John D. Hunter,et al.  Matplotlib: A 2D Graphics Environment , 2007, Computing in Science & Engineering.

[37]  G Wayne Brodland,et al.  A new cell-based FE model for the mechanics of embryonic epithelia , 2007, Computer methods in biomechanics and biomedical engineering.

[38]  P. Marmottant,et al.  Discrete rearranging disordered patterns, part II: 2D plasticity, elasticity and flow of a foam , 2006, The European physical journal. E, Soft matter.

[39]  G. Wayne Brodland,et al.  A cell-based constitutive model for embryonic epithelia and other planar aggregates of biological cells , 2006 .

[40]  S. Eaton,et al.  Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. , 2005, Developmental cell.

[41]  J. Joanny,et al.  Generic theory of active polar gels: a paradigm for cytoskeletal dynamics , 2004, The European physical journal. E, Soft matter.

[42]  L. Sulak,et al.  Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation , 2004, Nature.

[43]  G. Edwards,et al.  Forces for Morphogenesis Investigated with Laser Microsurgery and Quantitative Modeling , 2003, Science.

[44]  Anthony A. Hyman,et al.  Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo , 2001, Nature.

[45]  G W Brodland,et al.  Cell-level finite element studies of viscous cells in planar aggregates. , 2000, Journal of biomechanical engineering.

[46]  I. Campbell,et al.  Drosophila Dumpy is a gigantic extracellular protein required to maintain tension at epidermal–cuticle attachment sites , 2000, Current Biology.

[47]  A. A. Stein,et al.  Tension-dependent collective cell movements in the early gastrula ectoderm of Xenopus laevis embryos , 2000, Development Genes and Evolution.

[48]  C. Lehner,et al.  Cell cycle progression, growth and patterning in imaginal discs despite inhibition of cell division after inactivation of Drosophila Cdc2 kinase. , 1997, Development.

[49]  J. McCaskill,et al.  Monte Carlo approach to tissue-cell populations. , 1995, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[50]  A. Garcı́a-Bellido,et al.  Cell interactions in the control of size in Drosophila wings. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[51]  K D Irvine,et al.  Cell intercalation during Drosophila germband extension and its regulation by pair-rule segmentation genes. , 1994, Development.

[52]  Glazier,et al.  Simulation of biological cell sorting using a two-dimensional extended Potts model. , 1992, Physical review letters.

[53]  H. Honda,et al.  Cell behaviour in a polygonal cell sheet. , 1984, Journal of embryology and experimental morphology.

[54]  C. Waddington The genetic control of wing development inDrosophila , 1940, Journal of Genetics.

[55]  C. Waddington Preliminary Notes on the Development of the Wings in Normal and Mutant Strains of Drosophila. , 1939, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Winfried Kaballo Aufbaukurs Funktionalanalysis und Operatortheorie , 2014 .

[57]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[58]  Ole Tange,et al.  GNU Parallel: The Command-Line Power Tool , 2011, login Usenix Mag..

[59]  A. Giangrande,et al.  Imaging Drosophila pupal wing morphogenesis. , 2008, Methods in molecular biology.

[60]  Eric Jones,et al.  SciPy: Open Source Scientific Tools for Python , 2001 .

[61]  A. Prasad Particle image velocimetry , 2000 .

[62]  C. Lehner,et al.  Genetic analysis of the Drosophila cdc2 homolog. , 1993, Development.

[63]  L. Lourenço Particle Image Velocimetry , 1989 .

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

[65]  A. Sturtevant,et al.  Contributions to the genetics of Drosophila simulans and Drosophila melanogaster , 1929 .