Topological determination of early morphogenesis in Metazoa

This paper presents a topological interpretation of some developmental events through the use of well-known concepts and theorems of combinatorial geometry. The organization of early embryo using a simulation of cleavage considering only blastomere contacts is examined. Each blastomere is modeled as a topological cell and whole embryo—as cell packing. The egg cleavage results in a pattern of cellular contacts on the surface of each blastomere and whole embryo, a discrete morphogenetic field. We find topological distinctions between different types of early egg cleavage and suggest a topological classification of cleavage. Blastulation and gastrulation may be related to an inevitable emergence of discrete curvature that directs development in three-dimensional space. The relationship between local and global orders in metazoan development, i.e., between local morphogenetic processes and integral developmental patterns, is established. Thus, this methodology reveals a topological imperative: a certain set of topological rules that constrains and directs biological morphogenesis.

[1]  E. B. Matzke The Three-Dimensional Shapes of Bubbles in Foams. , 1945, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Norbert Peyerimhoff,et al.  Curvature and Geometry of Tessellating Plane Graphs , 2001, Discret. Comput. Geom..

[3]  R. Hinegardner Morphology and Genetics of Sea Urchin Development , 1975 .

[4]  T. Hales Cannonballs and Honeycombs , 2000 .

[5]  D. Weigel Patterning the Arabidopsis embryo , 1993, Current Biology.

[6]  L. Zammataro,et al.  Embryonic cleavage modeling as a computational approach to sphere packing problem. , 2007, Journal of theoretical biology.

[7]  John M. Sullivan,et al.  Curvatures of Smooth and Discrete Surfaces , 2007, 0710.4497.

[8]  Nikolai P. Dolbilin,et al.  How Many Facets on Average can a Tile Have in a Tiling , 2006 .

[9]  G. Eguchi,et al.  Studies on the mechanism of blastula formation in starfish embryos denuded of fertilization membrane. , 1986, Cell differentiation.

[11]  E. Saff,et al.  Discretizing Manifolds via Minimum Energy Points , 2004 .

[12]  Tatsuzo Nagai,et al.  A three-dimensional vertex dynamics cell model of space-filling polyhedra simulating cell behavior in a cell aggregate. , 2004, Journal of theoretical biology.

[13]  Q. Du,et al.  Modelling and simulations of multi-component lipid membranes and open membranes via diffuse interface approaches , 2006, Journal of Mathematical Biology.

[14]  D. Weaire,et al.  A counter-example to Kelvin's conjecture on minimal surfaces , 1994 .

[15]  N. Perrimon,et al.  The emergence of geometric order in proliferating metazoan epithelia , 2006, Nature.

[16]  R. Korn The changing shape of plant cells: transformations during cell proliferation. , 1980 .

[17]  W. Hoffman A system of axioms for mathematical biology , 1973 .

[18]  G. Giudice,et al.  Restitution of whole larvae from disaggregated cells of sea urchin embryos. , 1962, Developmental biology.

[19]  D. Klein Topo-combinatoric categorization of quasi-local graphitic defects , 2002 .

[20]  G. Beer,et al.  Order and Life , 1936, Nature.

[21]  E. Conklin The embryology of crepidula, A contribution to the cell lineage and early development of some marine gasteropods , 1897 .

[22]  C. D. The early development of Arenicola and Sternaspis , 2005, Archiv für Entwicklungsmechanik der Organismen.

[23]  E. Presnov,et al.  Topological approach to embryogenesis. , 1985, Journal of theoretical biology.

[24]  Simulation of cellular compaction and internalization in mammalian embryo development—II. Models for spherical embryos , 1988, Bulletin of mathematical biology.

[25]  M. Glicksman,et al.  Topological and metrical analysis of normal grain growth in three dimensions , 2007 .

[26]  K. Dormer,et al.  Fundamental tissue geometry for biologists , 1980 .

[27]  Alexey Chernyshev,et al.  Topological Patterns in Metazoan Evolution and Development , 2006, Bulletin of mathematical biology.

[28]  Topology of cleavage in the light of Pierre Curie principle , 2006, Russian Journal of Developmental Biology.

[29]  Pierre Barbier de Reuille,et al.  Computer simulations reveal novel properties of the cell-cell signaling network at the shoot apex in /Arabidopsis , 2005 .

[30]  D'arcy W. Thompson,et al.  On Growth and Form , 1917, Nature.

[31]  R. Thom Topological models in biology , 1969 .

[32]  Johann Benedict Listing,et al.  Vorstudien zur Topologie , 1848 .

[33]  E. Presnov SYNCHRONIZATION OF CELL DIVISION , 1999 .

[34]  Hirofumi Doi Graph‐Theoretical Analysis of Cleavage Pattern: Graph Developmental System and Its Application to Cleavage Pattern of Ascidian Egg , 1984 .

[35]  J. Sullivan New Tetrahedrally Close-Packed Structures , 2010 .

[36]  M. Dan-sohkawa,et al.  Cell dynamics of the blastulation process in the starfish, Asterina pectinifera. , 1980, Developmental biology.

[37]  A. Dress,et al.  From sphere to torus: A topological view of the metazoan body plan , 2003, Bulletin of mathematical biology.

[38]  M. Atiyah,et al.  Polyhedra in Physics, Chemistry and Geometry , 2003, math-ph/0303071.

[39]  Ralph I. Smith,et al.  Embryology and Phylogeny in Annelids and Arthropods , 1974 .

[40]  A. Campbell,et al.  SYNCHRONIZATION OF CELL DIVISION , 1957, Bacteriological reviews.

[41]  P. Lemaire,et al.  A Quantitative Approach to the Study of Cell Shapes and Interactions during Early Chordate Embryogenesis , 2006, Current Biology.

[42]  Sergei Petrovich Novikov,et al.  Modern Geometry-Methods and Applications(Part II. The Geometry and Topology of Manifolds) , 2010 .

[43]  Peter Fratzl,et al.  The effect of geometry on three-dimensional tissue growth , 2008, Journal of The Royal Society Interface.

[44]  Yusuke Higuchi Combinatorial curvature for planar graphs , 2001, J. Graph Theory.

[45]  L. Segel,et al.  On Topological Simulations in Developmental Biology , 1994 .

[46]  Pascale Le Gall,et al.  Topology-based abstraction of complex biological systems: application to the Golgi apparatus , 2008, Theory in Biosciences.

[47]  F. T. Lewis A GEOMETRIC ACCOUNTING FOR DIVERSE SHAPES OF 14‐HEDRAL CELLS: THE TRANSITION FROM DODECAHEDRA TO TETRAKAIDECAHEDRA , 1943 .

[48]  J. Kolega,et al.  The cellular basis of epithelial morphogenesis. , 1986, Developmental biology.

[49]  Michael O'Keeffe Crystal structures: Tiling by numbers , 1999, Nature.

[50]  Sergei Petrovich Novikov,et al.  The geometry of surfaces, transformation groups, and fields , 1984 .

[51]  N. Rivier,et al.  Plasticity and topological defects in cellular structures: Extra matter, folds and crab moulting , 2005 .

[52]  Jennifer A Zallen,et al.  Planar Polarity and Tissue Morphogenesis , 2007, Cell.

[53]  Florian Pfender,et al.  Kissing numbers, sphere packings, and some unexpected proofs , 2004 .

[54]  Three-dimensional bubble clusters: shape, packing, and growth rate. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[55]  V. Morris,et al.  The Topology of Cleavage Patterns with Examples from Embryos of Nereis, Styela and Xenopus , 1989 .

[56]  J. Haldane Organisers and Genes , 1940, Nature.

[57]  R. L. Hulbary THREE‐DIMENSIONAL CELL SHAPE IN THE TUBEROUS ROOTS OF ASPARAGUS AND IN THE LEAF OF RHOEO , 1948 .

[58]  M. Pyshnov Topological solution for cell proliferation in intestinal crypt. I. Elastic growth without cell loss. , 1980, Journal of theoretical biology.