Modeling Gastrulation in the Chick Embryo: Formation of the Primitive Streak

The body plan of all higher organisms develops during gastrulation. Gastrulation results from the integration of cell proliferation, differentiation and migration of thousands of cells. In the chick embryo gastrulation starts with the formation of the primitive streak, the site of invagination of mesoderm and endoderm cells, from cells overlaying Koller's Sickle. Streak formation is associated with large-scale cell flows that carry the mesoderm cells overlying Koller's sickle into the central midline region of the embryo. We use multi-cell computer simulations to investigate possible mechanisms underlying the formation of the primitive streak in the chick embryo. Our simulations suggest that the formation of the primitive streak employs chemotactic movement of a subpopulation of streak cells, as well as differential adhesion between the mesoderm cells and the other cells in the epiblast. Both chemo-attraction and chemo-repulsion between various combinations of cell types can create a streak. However, only one combination successfully reproduces experimental observations of the manner in which two streaks in the same embryo interact. This finding supports a mechanism in which streak tip cells produce a diffusible morphogen which repels cells in the surrounding epiblast. On the other hand, chemotactic interaction alone does not reproduce the experimental observation that the large-scale vortical cell flows develop simultaneously with streak initiation. In our model the formation of large scale cell flows requires an additional mechanism that coordinates and aligns the motion of neighboring cells.

[1]  Glazier,et al.  Simulation of biological cell sorting using a two-dimensional extended Potts model. , 1992, Physical review letters.

[2]  C. Stern Gastrulation in the chick , 2004 .

[3]  K. Alitalo,et al.  Avian VEGF-C: cloning, embryonic expression pattern and stimulation of the differentiation of VEGFR2-expressing endothelial cell precursors. , 1998, Development.

[4]  I. Mason,et al.  Expression of FGFR1, FGFR2 and FGFR3 during early neural development in the chick embryo , 2000, Mechanisms of Development.

[5]  Viktor Hamburger,et al.  A series of normal stages in the development of the chick embryo , 1992, Journal of morphology.

[6]  James A Glazier,et al.  Analysis of tissue flow patterns during primitive streak formation in the chick embryo. , 2005, Developmental biology.

[7]  P. Devreotes,et al.  Eukaryotic Chemotaxis: Distinctions between Directional Sensing and Polarization* , 2003, Journal of Biological Chemistry.

[8]  M. Chuai,et al.  Regulation of cell migration during chick gastrulation. , 2009, Current opinion in genetics & development.

[9]  P. Hogeweg,et al.  Modelling Morphogenesis: From Single Cells to Crawling Slugs. , 1997, Journal of theoretical biology.

[10]  P. Maini,et al.  A chemotactic model for the advance and retreat of the primitive streak in avian development , 2000, Bulletin of mathematical biology.

[11]  G. Schoenwolf,et al.  Cell populations and morphogenetic movements underlying formation of the avian primitive streak and organizer , 2001, Genesis.

[12]  P. Hogeweg,et al.  How amoeboids self-organize into a fruiting body: Multicellular coordination in Dictyostelium discoideum , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Markus Affolter,et al.  Signaling to cytoskeletal dynamics during chemotaxis. , 2005, Developmental cell.

[14]  J. Cooke,et al.  Early developmental expression and experimental axis determination by the chicken Vg1 gene , 1996, Current Biology.

[15]  L. Wolpert,et al.  Determination of embryonic polarity in a regulative system: evidence for endogenous inhibitors acting sequentially during primitive streak formation in the chick embryo , 2004, Development.

[16]  C. Parent,et al.  Adenylyl Cyclase Expression and Regulation During the Differentiation of Dictyostelium Discoideum , 2004, IUBMB life.

[17]  T. Mikawa,et al.  Induction and patterning of the primitive streak, an organizing center of gastrulation in the amniote , 2004, Developmental dynamics : an official publication of the American Association of Anatomists.

[18]  S. Chapman,et al.  Analysis of spatial and temporal gene expression patterns in blastula and gastrula stage chick embryos. , 2002, Developmental biology.

[19]  Roeland M. H. Merks,et al.  A cell-centered approach to developmental biology , 2005 .

[20]  K. Knudsen,et al.  Hepatocyte growth factor/scatter factor promotes a switch from E- to N-cadherin in chick embryo epiblast cells. , 1999, Experimental cell research.

[21]  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.

[22]  R. Ladher,et al.  Comparison of the expression patterns of several fibroblast growth factors during chick gastrulation and neurulation , 2002, Anatomy and Embryology.

[23]  L. Bodenstein,et al.  Formation of the chick primitive streak as studied in computer simulations. , 2005, Journal of theoretical biology.

[24]  C. Stern Gastrulation : from cells to embryo , 2004 .

[25]  M. Chuai,et al.  The mechanisms underlying primitive streak formation in the chick embryo. , 2008, Current topics in developmental biology.

[26]  I. Brick,et al.  Primary hypoblast development in the chick , 1982, Wilhelm Roux's archives of developmental biology.

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

[28]  M. Sheetz,et al.  Cell migration: regulation of force on extracellular-matrix-integrin complexes. , 1998, Trends in cell biology.

[29]  L. Gräper Die Primitiventwicklung des Hühnchens nach stereokinematographischen Untersuchungen, kontrolliert durch vitale Farbmarkierung und verglichen mit der Entwicklung anderer Wirbeltiere , 1929, Wilhelm Roux' Archiv für Entwicklungsmechanik der Organismen.

[30]  Paulien Hogeweg,et al.  Computing an organism: on the interface between informatic and dynamic processes. , 2002, Bio Systems.

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

[32]  C. Stern,et al.  Interactions between Wnt and Vg1 signalling pathways initiate primitive streak formation in the chick embryo. , 2001, Development.

[33]  Y. Shimoni,et al.  Activin can generate ectopic axial structures in chick blastoderm explants. , 1992, Development.

[34]  Daniel Choquet,et al.  Extracellular Matrix Rigidity Causes Strengthening of Integrin–Cytoskeleton Linkages , 1997, Cell.

[35]  E. Gherardi,et al.  Epithelial scatter factor and development of the chick embryonic axis. , 1990, Development.

[36]  K. Storey,et al.  A spatial and temporal map of FGF/Erk1/2 activity and response repertoires in the early chick embryo. , 2007, Developmental biology.

[37]  Y. Shimoni,et al.  Induction by soluble factors of organized axial structures in chick epiblasts. , 1990, Science.

[38]  Christof Niehrs,et al.  Fibroblast growth factor signaling during early vertebrate development. , 2005, Endocrine reviews.

[39]  Lewis Wolpert,et al.  Principles of Development , 1997 .

[40]  James A Glazier,et al.  Cell movement during chick primitive streak formation. , 2006, Developmental biology.