Emergent patterns of growth controlled by multicellular form and mechanics.

Spatial patterns of cellular growth generate mechanical stresses that help to push, fold, expand, and deform tissues into their specific forms. Genetic factors are thought to specify patterns of growth and other behaviors to drive morphogenesis. Here, we show that tissue form itself can feed back to regulate patterns of proliferation. Using micro-fabrication to control the organization of sheets of cells, we demonstrated the emergence of stable patterns of proliferative foci. Regions of concentrated growth corresponded to regions of high tractional stress generated within the sheet, as predicted by a finite-element model of multicellular mechanics and measured directly by using a micromechanical force sensor array. Inhibiting actomyosin-based tension or cadherin-mediated connections between cells disrupted the spatial pattern of proliferation. These findings demonstrate the existence of patterns of mechanical forces that originate from the contraction of cells, emerge from their multicellular organization, and result in patterns of growth. Thus, tissue form is not only a consequence but also an active regulator of tissue growth.

[1]  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.

[2]  Donald E Ingber,et al.  Control of basement membrane remodeling and epithelial branching morphogenesis in embryonic lung by Rho and cytoskeletal tension , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[3]  Yuzhi Zhang,et al.  Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis-susceptible and -resistant regions of human vasculature. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Celeste M Nelson,et al.  Vascular Endothelial-cadherin Regulates Cytoskeletal Tension, Cell Spreading, and Focal Adhesions by Stimulating Rhoa □ D Changes in Vascular Endothelial (ve)-cadherin–mediated Cell-cell Adhesion and Integrin-mediated Cell-matrix Adhesion Coordinate to Affect the Physical and Mechanical Rearrangemen , 2022 .

[5]  Jamie A Davies,et al.  Pattern and regulation of cell proliferation during murine ureteric bud development , 2004, Journal of anatomy.

[6]  Christopher S. Chen,et al.  Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. , 2004, Developmental cell.

[7]  E. Farge Mechanical Induction of Twist in the Drosophila Foregut/Stomodeal Primordium , 2003, Current Biology.

[8]  Rakesh K Jain,et al.  Molecular regulation of vessel maturation , 2003, Nature Medicine.

[9]  S. Shvartsman,et al.  Discrete models of autocrine cell communication in epithelial layers. , 2003, Biophysical journal.

[10]  Isaac Salazar-Ciudad,et al.  Mechanisms of pattern formation in development and evolution , 2003, Development.

[11]  Ray Keller,et al.  How we are shaped: the biomechanics of gastrulation. , 2003, Differentiation; research in biological diversity.

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

[13]  Christopher S. Chen,et al.  Cells lying on a bed of microneedles: An approach to isolate mechanical force , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Nobuyuki Itoh,et al.  Tube or not tube: remodeling epithelial tissues by branching morphogenesis. , 2003, Developmental cell.

[15]  Paul Martin,et al.  Epithelial fusions in the embryo. , 2002, Current opinion in cell biology.

[16]  Keith E. Mostov,et al.  Building epithelial architecture: insights from three-dimensional culture models , 2002, Nature Reviews Molecular Cell Biology.

[17]  S. Dudek,et al.  Cytoskeletal regulation of pulmonary vascular permeability. , 2001, Journal of applied physiology.

[18]  F. Lanni,et al.  Cell traction forces on soft biomaterials. I. Microrheology of type I collagen gels. , 2001, Biophysical journal.

[19]  Tetsuya Tabata,et al.  Genetics of morphogen gradients , 2001, Nature Reviews Genetics.

[20]  Benjamin Geiger,et al.  Focal Contacts as Mechanosensors Externally Applied Local Mechanical Force Induces Growth of Focal Contacts by an Mdia1-Dependent and Rock-Independent Mechanism , 2001 .

[21]  G. Garcı́a-Cardeña,et al.  Biomechanical activation of vascular endothelium as a determinant of its functional phenotype , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[22]  J. Kohn,et al.  Tissue spreading on implantable substrates is a competitive outcome of cell–cell vs. cell–substratum adhesivity , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[23]  M. Schwartz,et al.  Coordinate signaling by integrins and receptor tyrosine kinases in the regulation of G1 phase cell-cycle progression. , 2001, Current opinion in genetics & development.

[24]  Wayne L. Rickoll,et al.  Multiple Forces Contribute to Cell Sheet Morphogenesis for Dorsal Closure in Drosophila , 2000, The Journal of cell biology.

[25]  D. Andrew,et al.  Organ shape in the Drosophila salivary gland is controlled by regulated, sequential internalization of the primordia. , 2000, Development.

[26]  A. Singer,et al.  Cutaneous wound healing. , 1999, The New England journal of medicine.

[27]  Donald E. Ingber,et al.  The structural and mechanical complexity of cell-growth control , 1999, Nature Cell Biology.

[28]  Philip Ball,et al.  The Self-Made Tapestry: Pattern Formation in Nature , 1999 .

[29]  C. S. Chen,et al.  Control of cyclin D1, p27(Kip1), and cell cycle progression in human capillary endothelial cells by cell shape and cytoskeletal tension. , 1998, Molecular biology of the cell.

[30]  C. L. Adams,et al.  Cytomechanics of cadherin-mediated cell-cell adhesion. , 1998, Current opinion in cell biology.

[31]  W. Cardoso,et al.  Bud formation precedes the appearance of differential cell proliferation during branching morphogenesis of mouse lung epithelium in vitro , 1998, Developmental dynamics : an official publication of the American Association of Anatomists.

[32]  M. Kinch,et al.  Rho-stimulated contractility contributes to the fibroblastic phenotype of Ras-transformed epithelial cells. , 1997, Molecular biology of the cell.

[33]  C. S. Chen,et al.  Geometric control of cell life and death. , 1997, Science.

[34]  A. Mccarthy Development , 1996, Current Opinion in Neurobiology.

[35]  F. Breviario,et al.  Catenin-dependent and -independent Functions of Vascular Endothelial Cadherin (*) , 1995, The Journal of Biological Chemistry.

[36]  M. Loeffler,et al.  Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. , 1990, Development.

[37]  R M Nerem,et al.  Application of the micropipette technique to the measurement of cultured porcine aortic endothelial cell viscoelastic properties. , 1990, Journal of biomechanical engineering.

[38]  Peter Davies Gene Expression During Normal and Malignant Differentiation , 1986 .

[39]  J. Wyke Gene Expression during Normal and Malignant Differentiation , 1986 .

[40]  C. Gahmberg,et al.  Gene expression during normal and malignant differentiation , 1985 .

[41]  N. K. Wessells,et al.  The role of cell proliferation and cellular shape change in branching morphogenesis of the embryonic mouse lung: analysis using aphidicolin and cytochalasins. , 1984, The Journal of experimental zoology.

[42]  G. Schoenwolf,et al.  Quantitative analyses of changes in cell shapes during bending of the avian neural plate. , 1984, Developmental biology.

[43]  R. Keller,et al.  The cellular basis of epiboly: an SEM study of deep-cell rearrangement during gastrulation in Xenopus laevis. , 1980, Journal of embryology and experimental morphology.

[44]  J. Folkman,et al.  Role of cell shape in growth control , 1978, Nature.

[45]  J. Folkman,et al.  Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. , 1977, Microvascular research.

[46]  J. Folkman,et al.  Influence of geometry on control of cell growth. , 1975, Biochimica et biophysica acta.

[47]  F. Crick Diffusion in Embryogenesis , 1970, Nature.

[48]  L. Wolpert Positional information and the spatial pattern of cellular differentiation. , 1969, Journal of theoretical biology.

[49]  J. Bonner,et al.  Differentiation , 1968, Nature.

[50]  G. Phillips The Generation of Animals , 1963, The Classical Review.

[51]  M. S. Steinberg,et al.  Mechanism of Tissue Reconstruction by Dissociated Cells, II: Time-Course of Events , 1962, Science.

[52]  A. M. Turing,et al.  The chemical basis of morphogenesis , 1952, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[53]  Aristotle,et al.  Generation of animals , 1942 .

[54]  D'arcy W. Thompson On Growth and Form , 1917, Nature.

[55]  Unsere Körperform und das physiologische Problem ihrer Enstehung , .