Extracellular matrix motion and early morphogenesis

For over a century, embryologists who studied cellular motion in early amniotes generally assumed that morphogenetic movement reflected migration relative to a static extracellular matrix (ECM) scaffold. However, as we discuss in this Review, recent investigations reveal that the ECM is also moving during morphogenesis. Time-lapse studies show how convective tissue displacement patterns, as visualized by ECM markers, contribute to morphogenesis and organogenesis. Computational image analysis distinguishes between cell-autonomous (active) displacements and convection caused by large-scale (composite) tissue movements. Modern quantification of large-scale ‘total’ cellular motion and the accompanying ECM motion in the embryo demonstrates that a dynamic ECM is required for generation of the emergent motion patterns that drive amniote morphogenesis. Summary: This Review considers the important, but often overlooked, role of the extracellular matrix in cell migration and tissue morphogenesis in amniotes.

[1]  A. Münsterberg,et al.  The Early Stages of Heart Development: Insights from Chicken Embryos , 2016, Journal of cardiovascular development and disease.

[2]  A. Alexander-Katz,et al.  Emergent ultra–long-range interactions between active particles in hybrid active–inactive systems , 2016, Proceedings of the National Academy of Sciences.

[3]  A. Czirók,et al.  The endoderm and myocardium join forces to drive early heart tube assembly. , 2015, Developmental biology.

[4]  S. Dallas,et al.  Novel approaches for two and three dimensional multiplexed imaging of osteocytes. , 2015, Bone.

[5]  S. Holley,et al.  The tissue mechanics of vertebrate body elongation and segmentation. , 2015, Current opinion in genetics & development.

[6]  David S. Koos,et al.  Dynamic imaging of the growth plate cartilage reveals multiple contributors to skeletal morphogenesis , 2015, Nature Communications.

[7]  H. Sang,et al.  Myosin II-mediated cell shape changes and cell intercalation contribute to primitive streak formation , 2015, Nature Cell Biology.

[8]  R. McLennan,et al.  Neural crest migration: trailblazing ahead , 2015, F1000prime reports.

[9]  Andras Czirok,et al.  Cell resolved, multiparticle model of plastic tissue deformations and morphogenesis , 2014, Physical biology.

[10]  L. Bodenstein,et al.  Local cell interactions and self-amplifying individual cell ingression drive amniote gastrulation , 2014, eLife.

[11]  Tamás Vicsek,et al.  Collective motion of cells: from experiments to models. , 2014, Integrative biology : quantitative biosciences from nano to macro.

[12]  T. Vicsek,et al.  Anomalous segregation dynamics of self-propelled particles , 2014, New journal of physics.

[13]  Kristie L. Rose,et al.  A unique covalent bond in basement membrane is a primordial innovation for tissue evolution , 2013, Proceedings of the National Academy of Sciences.

[14]  Olivier Pourquié,et al.  Formation and segmentation of the vertebrate body axis. , 2013, Annual review of cell and developmental biology.

[15]  H. Enomoto,et al.  Tissue Interactions in Neural Crest Cell Development and Disease , 2013, Science.

[16]  Roeland M. H. Merks,et al.  Mechanical Cell-Matrix Feedback Explains Pairwise and Collective Endothelial Cell Behavior In Vitro , 2013, PLoS Comput. Biol..

[17]  Thierry Emonet,et al.  Cell-Fibronectin Interactions Propel Vertebrate Trunk Elongation via Tissue Mechanics , 2013, Current Biology.

[18]  Y. Mishina,et al.  Establishment of left–right asymmetry in vertebrate development: the node in mouse embryos , 2013, Cellular and Molecular Life Sciences.

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

[20]  Thierry Emonet,et al.  Regulated tissue fluidity steers zebrafish body elongation , 2013, Development.

[21]  D. Sepich,et al.  Gastrulation: making and shaping germ layers. , 2012, Annual review of cell and developmental biology.

[22]  Vincent Fleury,et al.  Clarifying tetrapod embryogenesis by a dorso-ventral analysis of the tissue flows during early stages of chicken development , 2012, Biosyst..

[23]  A. Czirók,et al.  Pattern formation during vasculogenesis. , 2012, Birth defects research. Part C, Embryo today : reviews.

[24]  B. Potetz,et al.  Spatial Anisotropies and Temporal Fluctuations in Extracellular Matrix Network Texture during Early Embryogenesis , 2012, PloS one.

[25]  Victor D. Varner,et al.  Not just inductive: a crucial mechanical role for the endoderm during heart tube assembly , 2012, Development.

[26]  L. G. Morelli,et al.  Computational Approaches to Developmental Patterning , 2012, Science.

[27]  R. Hynes The evolution of metazoan extracellular matrix , 2012, The Journal of cell biology.

[28]  A. Czirók,et al.  Convective tissue movements play a major role in avian endocardial morphogenesis. , 2012, Developmental biology.

[29]  Evan A. Zamir,et al.  In vivo imaging of basement membrane movement: ECM patterning shapes Hydra polyps , 2011, Journal of Cell Science.

[30]  A. Czirók,et al.  Extracellular matrix fluctuations during early embryogenesis , 2011, Physical biology.

[31]  Josephine C. Adams,et al.  The Evolution of Extracellular Matrix , 2010, Molecular biology of the cell.

[32]  Ralph Weissleder,et al.  WNT5A/JNK and FGF/MAPK Pathways Regulate the Cellular Events Shaping the Vertebrate Limb Bud , 2010, Current Biology.

[33]  A. Czirók,et al.  Dynamic Analysis of Vascular Morphogenesis Using Transgenic Quail Embryos , 2010, PloS one.

[34]  Douglas W DeSimone,et al.  The extracellular matrix in development and morphogenesis: a dynamic view. , 2010, Developmental biology.

[35]  R. Lansford,et al.  Dynamic positional fate map of the primary heart-forming region. , 2009, Developmental biology.

[36]  Charles D. Little,et al.  A random cell motility gradient downstream of FGF controls elongation of an amniote embryo , 2009, Nature.

[37]  D. E. Discher,et al.  Matrix elasticity directs stem cell lineage — Soluble factors that limit osteogenesis , 2009 .

[38]  C. Tabin,et al.  Cell Movements at Hensen’s Node Establish Left/Right Asymmetric Gene Expression in the Chick , 2009, Science.

[39]  B. Rongish,et al.  Rotation of Organizer Tissue Contributes to Left–Right Asymmetry , 2009, Anatomical record.

[40]  K. Anderson,et al.  Morphogenesis of the node and notochord: The cellular basis for the establishment and maintenance of left–right asymmetry in the mouse , 2008, Developmental dynamics : an official publication of the American Association of Anatomists.

[41]  Evan A. Zamir,et al.  The ECM Moves during Primitive Streak Formation—Computation of ECM Versus Cellular Motion , 2008, PLoS biology.

[42]  L. Bonewald,et al.  Time Lapse Imaging Techniques for Comparison of Mineralization Dynamics in Primary Murine Osteoblasts and the Late Osteoblast/Early Osteocyte-Like Cell Line MLO-A5 , 2008, Cells Tissues Organs.

[43]  Erica D. Perryn,et al.  Vascular sprout formation entails tissue deformations and VE-cadherin-dependent cell-autonomous motility. , 2008, Developmental biology.

[44]  L. Wolpert,et al.  The amniote primitive streak is defined by epithelial cell intercalation before gastrulation , 2007, Nature.

[45]  M. Farach-Carson,et al.  Potential Role for Heparan Sulfate Proteoglycans in Regulation of Transforming Growth Factor-β (TGF-β) by Modulating Assembly of Latent TGF-β-binding Protein-1* , 2007, Journal of Biological Chemistry.

[46]  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.

[47]  M. Blum,et al.  Cilia-Driven Leftward Flow Determines Laterality in Xenopus , 2007, Current Biology.

[48]  András Czirók,et al.  Mesodermal cell displacements during avian gastrulation are due to both individual cell-autonomous and convective tissue movements , 2006, Proceedings of the National Academy of Sciences.

[49]  S. Sen,et al.  Matrix Elasticity Directs Stem Cell Lineage Specification , 2006, Cell.

[50]  Á. Raya,et al.  Left–right asymmetry in the vertebrate embryo: from early information to higher-level integration , 2006, Nature Reviews Genetics.

[51]  Andras Czirok,et al.  Elastic fiber formation: A dynamic view of extracellular matrix assembly using timer reporters , 2006, Journal of cellular physiology.

[52]  Olivier Pourquié,et al.  Control of the segmentation process by graded MAPK/ERK activation in the chick embryo. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[53]  András Czirók,et al.  A Digital Image-Based Method for Computational Tissue Fate Mapping During Early Avian Morphogenesis , 2005, Annals of Biomedical Engineering.

[54]  Roeland M. H. Merks,et al.  Contact-Inhibited Chemotaxis in De Novo and Sprouting Blood-Vessel Growth , 2005, PLoS Comput. Biol..

[55]  H. Yost,et al.  Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut , 2005, Development.

[56]  M. S. Steinberg,et al.  The differential adhesion hypothesis: a direct evaluation. , 2005, Developmental biology.

[57]  Michael Levin,et al.  Left–right asymmetry in embryonic development: a comprehensive review , 2005, Mechanisms of Development.

[58]  Andras Czirok,et al.  αvβ3 integrin-dependent endothelial cell dynamics in vivo , 2004 .

[59]  A. Spicer,et al.  Hyaluronan and morphogenesis. , 2004, Birth defects research. Part C, Embryo today : reviews.

[60]  A. Czirók,et al.  Novel approaches for the study of vascular assembly and morphogenesis in avian embryos. , 2003, Trends in cardiovascular medicine.

[61]  A. Graham,et al.  The neural crest , 2003, Current Biology.

[62]  L. Preziosi,et al.  Modeling the early stages of vascular network assembly , 2003, The EMBO journal.

[63]  L Preziosi,et al.  Percolation, morphogenesis, and burgers dynamics in blood vessels formation. , 2003, Physical review letters.

[64]  C. Stern,et al.  The hypoblast of the chick embryo positions the primitive streak by antagonizing nodal signaling. , 2002, Developmental cell.

[65]  Cornelis J Weijer,et al.  Cell movement patterns during gastrulation in the chick are controlled by positive and negative chemotaxis mediated by FGF4 and FGF8. , 2002, Developmental cell.

[66]  N. Zagris Extracellular matrix in development of the early embryo. , 2001, Micron.

[67]  B. Toole,et al.  Hyaluronan in morphogenesis. , 2001, Journal of internal medicine.

[68]  S. Klewer,et al.  Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. , 2000, The Journal of clinical investigation.

[69]  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.

[70]  R. Perris,et al.  Role of the extracellular matrix during neural crest cell migration , 2000, Mechanisms of Development.

[71]  N. Hirokawa,et al.  Randomization of Left–Right Asymmetry due to Loss of Nodal Cilia Generating Leftward Flow of Extraembryonic Fluid in Mice Lacking KIF3B Motor Protein , 1999, Cell.

[72]  J. Buckwalter,et al.  Changes in cell, matrix compartment, and fibrillar collagen volumes between growth‐plate zones , 1998, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[73]  S. Brandt,et al.  TAL1/SCL is expressed in endothelial progenitor cells/angioblasts and defines a dorsal-to-ventral gradient of vasculogenesis. , 1997, Developmental biology.

[74]  P. Brauer,et al.  Latent transforming growth factor‐β is present in the extracellular matrix of embryonic hearts in situ , 1996, Developmental dynamics : an official publication of the American Association of Anatomists.

[75]  J. Shih,et al.  Cell motility driving mediolateral intercalation in explants of Xenopus laevis. , 1992, Development.

[76]  M. Bronner‐Fraser,et al.  Spatial and temporal changes in the distribution of proteoglycans during avian neural crest development. , 1991, Development.

[77]  C. Little,et al.  Avian vasculogenesis and the distribution of collagens I, IV, laminin, and fibronectin in the heart primordia. , 1990, The Journal of experimental zoology.

[78]  H. Frisch,et al.  Wetting, percolation and morphogenesis in a model tissue system. , 1989, Journal of theoretical biology.

[79]  E. Hay,et al.  Extracellular matrix, cell skeletons, and embryonic development. , 1989, American journal of medical genetics.

[80]  T J Poole,et al.  Vasculogenesis and angiogenesis: two distinct morphogenetic mechanisms establish embryonic vascular pattern. , 1989, The Journal of experimental zoology.

[81]  S. Newman,et al.  Matrix-driven translocation of cells and nonliving particles. , 1985, Science.

[82]  M. Bronner‐Fraser Distribution of latex beads and retinal pigment epithelial cells along the ventral neural crest pathway. , 1982, Developmental biology.

[83]  C. Tickle,et al.  Cell movement and the mechanism of invasiveness: a survey of the behaviour of some normal and malignant cells implanted into the developing chick wing bud. , 1978, Journal of cell science.

[84]  M. Abercrombie,et al.  Concepts in morphogenesis , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[85]  Malcolm S. Steinberg,et al.  Reconstruction of Tissues by Dissociated Cells , 1963 .

[86]  Philip L. Townes,et al.  Directed movements and selective adhesion of embryonic amphibian cells , 1955 .

[87]  N. Spratt Development of the early chick blastoderm on synthetic media. , 1948, The Journal of experimental zoology.

[88]  E. Conklin The embryology of amphioxus , 1932 .

[89]  W. H. Lewis Amniotic ectoderm in tissue‐cultures , 1923 .

[90]  R. G. Harrison The cultivation of tissues in extraneous media as a method of morpho‐genetic study , 1912 .

[91]  R. G. Harrison The outgrowth of the nerve fiber as a mode of protoplasmic movement. , 1910, The Journal of experimental zoology.

[92]  Ulrich Eggers,et al.  Emergence From Chaos To Order , 2016 .

[93]  A. Czirók,et al.  Active cell and ECM movements during development. , 2015, Methods in molecular biology.

[94]  H. Kronenberg,et al.  Overview of skeletal development. , 2014, Methods in molecular biology.

[95]  Josephine C. Adams,et al.  Extracellular Matrix Evolution: An Overview , 2013 .

[96]  Sarah L Dallas,et al.  Live imaging of bone cell and organ cultures. , 2012, Methods in molecular biology.

[97]  Abbas Shirinifard,et al.  Multi-scale modeling of tissues using CompuCell3D. , 2012, Methods in cell biology.

[98]  D. Ingber,et al.  Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus , 2009, Nature Reviews Molecular Cell Biology.

[99]  T. Newman,et al.  Grid-free models of multicellular systems, with an application to large-scale vortices accompanying primitive streak formation. , 2008, Current topics in developmental biology.

[100]  M. Farach-Carson,et al.  Potential role for heparan sulfate proteoglycans in regulation of transforming growth factor-beta (TGF-beta) by modulating assembly of latent TGF-beta-binding protein-1. , 2007, The Journal of biological chemistry.

[101]  Andras Czirok,et al.  Extracellular matrix macroassembly dynamics in early vertebrate embryos. , 2006, Current topics in developmental biology.

[102]  Roeland M. H. Merks,et al.  Cell elongation is key to in silico replication of in vitro vasculogenesis and subsequent remodeling. , 2006, Developmental biology.

[103]  F. Harrisson,et al.  Transfer of extracellular matrix components between germ layers in chimaeric chicken-quail blastoderms , 2004, Cell and Tissue Research.

[104]  András Czirók,et al.  alphavbeta3 integrin-dependent endothelial cell dynamics in vivo. , 2004, Development.

[105]  E. Hay,et al.  Neural crest migration in 3D extracellular matrix utilizes laminin, fibronectin, or collagen. , 1988, Developmental biology.

[106]  I. Summerhayes,et al.  Possible role of fibronectin in malignancy. , 1979, Journal of supramolecular structure.

[107]  J. Trinkaus The cellular basis of Fundulus epiboly. Adhesivity of blastula and gastrula cells in culture. , 1963, Developmental biology.

[108]  M. S. Steinberg,et al.  Reconstruction of tissues by dissociated cells. Some morphogenetic tissue movements and the sorting out of embryonic cells may have a common explanation. , 1963, Science.