Turing's next steps: the mechanochemical basis of morphogenesis

Nearly 60 years ago, Alan Turing showed theoretically how two chemical species, termed morphogens, diffusing and reacting with each other can generate spatial patterns. Diffusion plays a crucial part in transporting chemical signals through space to establish the length scale of the pattern. When coupled to chemical reactions, mechanical processes — forces and flows generated by motor proteins — can also define length scales and provide a mechanochemical basis for morphogenesis. forces and flows generated by motor proteins — can also define length scales and provide a mechanochemical basis for morphogenesis.

[1]  W. Bialek,et al.  Stability and Nuclear Dynamics of the Bicoid Morphogen Gradient , 2007, Cell.

[2]  Y. Kalaidzidis,et al.  Kinetics of Morphogen Gradient Formation , 2007, Science.

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

[4]  Xinhua Lin,et al.  Drosophila Dpp Morphogen Movement Is Independent of Dynamin-Mediated Endocytosis but Regulated by the Glypican Members of Heparan Sulfate Proteoglycans , 2004, Cell.

[5]  Linda Wordeman,et al.  The kinesin-8 motor Kif18A suppresses kinetochore movements to control mitotic chromosome alignment. , 2008, Developmental cell.

[6]  Scott T. Brady,et al.  A novel brain ATPase with properties expected for the fast axonal transport motor , 1985, Nature.

[7]  Claire Wilhelm,et al.  Out-of-equilibrium microrheology inside living cells. , 2008, Physical review letters.

[8]  M. Sheetz,et al.  Local force and geometry sensing regulate cell functions , 2006, Nature Reviews Molecular Cell Biology.

[9]  Michael P. Sheetz,et al.  Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility , 1985, Cell.

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

[11]  J. Priess,et al.  Cortical flows powered by asymmetrical contraction transport PAR proteins to establish and maintain anterior-posterior polarity in the early C. elegans embryo. , 2004, Developmental cell.

[12]  A. Kicheva,et al.  Morphogen gradient formation. , 2009, Cold Spring Harbor perspectives in biology.

[13]  Shigeru Kondo,et al.  Reaction-Diffusion Model as a Framework for Understanding Biological Pattern Formation , 2010, Science.

[14]  C. Nüsslein-Volhard,et al.  A gradient of bicoid protein in Drosophila embryos , 1988, Cell.

[15]  Jonathon Howard,et al.  The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends , 2006, Nature.

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

[17]  B N Kholodenko,et al.  Spatial gradients of cellular phospho‐proteins , 1999, FEBS letters.

[18]  Ingmar H. Riedel-Kruse,et al.  How molecular motors shape the flagellar beat , 2007, HFSP journal.

[19]  H. Gutzeit,et al.  Time-lapse film analysis of cytoplasmic streaming during late oogenesis of Drosophila , 1982 .

[20]  A. Huxley,et al.  Structural Changes in Muscle During Contraction: Interference Microscopy of Living Muscle Fibres , 1954, Nature.

[21]  Hans Meinhardt,et al.  The Algorithmic Beauty of Sea Shells , 2003, The Virtual Laboratory.

[22]  G. Banker,et al.  Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Mark E. Schneider,et al.  A New Compartment at Stereocilia Tips Defined by Spatial and Temporal Patterns of Myosin IIIa Expression , 2006, The Journal of Neuroscience.

[24]  Tony J. C. Harris,et al.  The PAR complex regulates pulsed actomyosin contractions during amnioserosa apical constriction in Drosophila , 2010, Development.

[25]  S. Grill,et al.  Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows , 2010, Nature.

[26]  A. Hyman,et al.  Microtubule polymerases and depolymerases. , 2007, Current opinion in cell biology.

[27]  Karsten Weis,et al.  Visualization of a Ran-GTP Gradient in Interphase and Mitotic Xenopus Egg Extracts , 2002, Science.

[28]  U. Manor,et al.  Regulation of Stereocilia Length by Myosin XVa and Whirlin Depends on the Actin-Regulatory Protein Eps8 , 2011, Current Biology.

[29]  C. Nüsslein-Volhard,et al.  Organization of anterior pattern in the Drosophila embryo by the maternal gene bicoid , 1986, Nature.

[30]  Jonathon Howard,et al.  Mechanical signaling in networks of motor and cytoskeletal proteins. , 2009, Annual review of biophysics.

[31]  Sujoy Ganguly,et al.  Flows driven by flagella of multicellular organisms enhance long-range molecular transport. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Francis Lin,et al.  Intracellular actin-based transport: how far you go depends on how often you switch. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[33]  H. Huxley,et al.  Changes in the Cross-Striations of Muscle during Contraction and Stretch and their Structural Interpretation , 1954, Nature.

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

[35]  H. Meinhardt,et al.  A theory of biological pattern formation , 1972, Kybernetik.

[36]  Anthony A. Hyman,et al.  Yeast kinesin-8 depolymerizes microtubules in a length-dependent manner , 2006, Nature Cell Biology.

[37]  Michael Brand,et al.  Fgf8 morphogen gradient forms by a source-sink mechanism with freely diffusing molecules , 2009, Nature.

[38]  N. Gov,et al.  Protein localization by actin treadmilling and molecular motors regulates stereocilia shape and treadmilling rate. , 2008, Biophysical journal.

[39]  A. Rowe,et al.  Dynein: A Protein with Adenosine Triphosphatase Activity from Cilia , 1965, Science.

[40]  A. Geitmann,et al.  Polar growth in pollen tubes is associated with spatially confined dynamic changes in cell mechanical properties. , 2009, Developmental biology.

[41]  Y. Couder,et al.  Developmental Patterning by Mechanical Signals in Arabidopsis , 2009 .

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

[43]  T. Davis,et al.  Kip3, the yeast kinesin-8, is required for clustering of kinetochores at metaphase , 2010, Cell cycle.

[44]  Stefan Hümmer,et al.  The Human Kinesin Kif18A Is a Motile Microtubule Depolymerase Essential for Chromosome Congression , 2007, Current Biology.

[45]  G. Salbreux,et al.  Hydrodynamics of cellular cortical flows and the formation of contractile rings. , 2009, Physical review letters.

[46]  Nathalie Dostatni,et al.  High mobility of bicoid captured by fluorescence correlation spectroscopy: implication for the rapid establishment of its gradient. , 2010, Biophysical journal.

[47]  D. St Johnston,et al.  In Vivo Imaging of oskar mRNA Transport Reveals the Mechanism of Posterior Localization , 2008, Cell.

[48]  Frank Jülicher,et al.  Pattern formation in active fluids. , 2011, Physical review letters.

[49]  J. Howard,et al.  Mechanics of Motor Proteins and the Cytoskeleton , 2001 .

[50]  K. Luby-Phelps,et al.  Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area. , 2000, International review of cytology.

[51]  Hans Meinhardt,et al.  The Algorithmic Beauty of Sea Shells , 1998, The Virtual Laboratory.

[52]  Jonathon Howard,et al.  Kinesin-8 Motors Act Cooperatively to Mediate Length-Dependent Microtubule Depolymerization , 2009, Cell.

[53]  Shigeru Kondo,et al.  Interactions between zebrafish pigment cells responsible for the generation of Turing patterns , 2009, Proceedings of the National Academy of Sciences.

[54]  I. Tuval,et al.  Microfluidics of cytoplasmic streaming and its implications for intracellular transport , 2008, Proceedings of the National Academy of Sciences.

[55]  W. Bialek,et al.  Diffusion and scaling during early embryonic pattern formation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[57]  Eric Karsenti,et al.  Spatial Coordination of Spindle Assembly by Chromosome-Mediated Signaling Gradients , 2005, Science.

[58]  Alexander Spirov,et al.  Formation of the bicoid morphogen gradient: an mRNA gradient dictates the protein gradient , 2009, Development.