Vertex sliding drives intercalation by radial coupling of adhesion and actomyosin networks during Drosophila germband extension

Oriented cell intercalation is an essential developmental process that shapes tissue morphologies through the directional insertion of cells between their neighbors. Previous research has focused on properties of cell–cell interfaces, while the function of tricellular vertices has remained unaddressed. Here, we identify a highly novel mechanism in which vertices demonstrate independent sliding behaviors along cell peripheries to produce the topological deformations responsible for intercalation. Through systematic analysis, we find that the motion of vertices connected by contracting interfaces is not physically coupled, but instead possess strong radial coupling. E-cadherin and Myosin II exist in previously unstudied populations at cell vertices and undergo oscillatory cycles of accumulation and dispersion that are coordinated with changes in cell area. Additionally, peak enrichment of vertex E-cadherin/Myosin II coincides with interface length stabilization. Our results suggest a model in which asymmetric radial force balance directs the progressive, ratcheted motion of individual vertices to drive intercalation.

[1]  Timothy E. Vanderleest,et al.  Planar polarized Rab35 functions as an oscillatory ratchet during cell intercalation in the Drosophila epithelium , 2017, Nature Communications.

[2]  Toyotaka Ishibashi,et al.  Apical constriction is driven by a pulsatile apical myosin network in delaminating Drosophila neuroblasts , 2017, Development.

[3]  R. Fernandez-Gonzalez,et al.  Myosin II promotes the anisotropic loss of the apical domain during Drosophila neuroblast ingression , 2017, The Journal of cell biology.

[4]  Yusuke Hara,et al.  Basolateral protrusion and apical contraction cooperatively drive Drosophila germ-band extension , 2017, Nature Cell Biology.

[5]  D. Walker,et al.  Tricellular junctions regulate intestinal stem cell behaviour to maintain homeostasis , 2016, Nature Cell Biology.

[6]  Guillaume Salbreux,et al.  Myosin II Controls Junction Fluctuations to Guide Epithelial Tissue Ordering , 2016, bioRxiv.

[7]  Alexander G Fletcher,et al.  Unipolar distributions of junctional Myosin II identify cell stripe boundaries that drive cell intercalation throughout Drosophila axis extension , 2016, eLife.

[8]  David K. Lubensky,et al.  Epithelial tricellular junctions act as interphase cell shape sensors to orient mitosis , 2016, Nature.

[9]  Rodrigo Fernandez-Gonzalez,et al.  Local mechanical forces promote polarized junctional assembly and axis elongation in Drosophila , 2016, eLife.

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

[11]  Edwin Munro,et al.  A self-organized biomechanical network drives shape changes during tissue morphogenesis , 2015, Nature.

[12]  Zulfeqhar A. Syed,et al.  The Triple-Repeat Protein Anakonda Controls Epithelial Tricellular Junction Formation in Drosophila. , 2015, Developmental cell.

[13]  Dene L. Farrell,et al.  Spatiotemporal control of epithelial remodeling by regulated myosin phosphorylation , 2014, Proceedings of the National Academy of Sciences.

[14]  J. Zallen,et al.  Rho GTPase and Shroom direct planar polarized actomyosin contractility during convergent extension , 2014, The Journal of cell biology.

[15]  E. Wieschaus,et al.  Distinct Rap1 activity states control the extent of epithelial invagination via α-catenin. , 2013, Developmental cell.

[16]  Olaf Ronneberger,et al.  Vertebrate kidney tubules elongate using a planar cell polarity–dependent, rosette-based mechanism of convergent extension , 2012, Nature Genetics.

[17]  Michael A Thompson,et al.  Analytical tools to distinguish the effects of localization error, confinement, and medium elasticity on the velocity autocorrelation function. , 2012, Biophysical journal.

[18]  M. Kaschube,et al.  Differential positioning of adherens junctions is associated with initiation of epithelial folding , 2012, Nature.

[19]  Bob Goldstein,et al.  Triggering a Cell Shape Change by Exploiting Preexisting Actomyosin Contractions , 2012, Science.

[20]  M. Hsu,et al.  OVERCOMING THE NEGATIVE FREQUENCIES - INSTANTANEOUS FREQUENCY AND AMPLITUDE ESTIMATION USING OSCULATING CIRCLE METHOD , 2011 .

[21]  J. Zallen,et al.  Oscillatory behaviors and hierarchical assembly of contractile structures in intercalating cells , 2011, Physical biology.

[22]  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.

[23]  T. Lecuit,et al.  Spatial regulation of Dia and Myosin-II by RhoGEF2 controls initiation of E-cadherin endocytosis during epithelial morphogenesis , 2011, Nature Cell Biology.

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

[25]  Jennifer A Zallen,et al.  Myosin II dynamics are regulated by tension in intercalating cells. , 2009, Developmental cell.

[26]  Eric F. Wieschaus,et al.  Pulsed contractions of an actin–myosin network drive apical constriction , 2009, Nature.

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

[28]  Jennifer A Zallen,et al.  Multicellular rosette formation links planar cell polarity to tissue morphogenesis. , 2006, Developmental cell.

[29]  S. Tsukita,et al.  Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells , 2005, The Journal of cell biology.

[30]  Xi Lin,et al.  Regulation of polarized extension and planar cell polarity in the cochlea by the vertebrate PCP pathway , 2005, Nature Genetics.

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

[32]  J. Schulte,et al.  Gliotactin, a novel marker of tricellular junctions, is necessary for septate junction development in Drosophila , 2003, The Journal of cell biology.

[33]  M. Ferguson,et al.  TGF-beta3 is required for the adhesion and intercalation of medial edge epithelial cells during palate fusion. , 2002, The International journal of developmental biology.

[34]  P. Skoglund,et al.  Mechanisms of convergence and extension by cell intercalation. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[35]  J. Slack,et al.  The Xenopus tadpole gut: fate maps and morphogenetic movements. , 2000, Development.

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

[37]  C. Noirot,et al.  The specialization of septate junctions in regions of tricellular junctions. I. Smooth septate junctions (=continuous junctions). , 1982, Journal of ultrastructure research.

[38]  L. Staehelin.  Further observations on the fine structure of freeze-cleaved tight junctions. , 1973, Journal of cell science.

[39]  Yu-Chiun Wang,et al.  A homeostatic apical microtubule network shortens cells for epithelial folding via a basal polarity shift , 2017, Nature Cell Biology.