On the mechanochemical theory of biological pattern formation with application to vasculogenesis.

We first describe the Murray-Oster mechanical theory of pattern formation, the biological basis of which is experimentally well documented. The model quantifies the interaction of cells and the extracellular matrix via the cell-generated forces. The model framework is described in quantitative detail. Vascular endothelial cells, when cultured on gelled basement membrane matrix, rapidly aggregate into clusters while deforming the matrix into a network of cord-like structures tessellating the planar culture. We apply the mechanical theory of pattern formation to this culture system and show that neither strain-biased anisotropic cell traction nor cell migration are necessary for pattern formation: isotropic, strain-stimulated cell traction is sufficient to form the observed patterns. Predictions from the model were confirmed experimentally.

[1]  M. Koehl,et al.  The dorsal involuting marginal zone stiffens anisotropically during its convergent extension in the gastrula of Xenopus laevis. , 1995, Development.

[2]  G. Scherer,et al.  Thermal expansion of gels: a novel method for measuring permeability , 1991 .

[3]  R T Tranquillo,et al.  The fibroblast-populated collagen microsphere assay of cell traction force--Part 2: Measurement of the cell traction parameter. , 1995, Journal of biomechanical engineering.

[4]  G. Oster,et al.  Cell traction models for generating pattern and form in morphogenesis , 1984, Journal of mathematical biology.

[5]  J. Folkman Clinical Applications of Research on Angiogenesis , 1995 .

[6]  M. Iruela-Arispe,et al.  Reorganization of basement membrane matrices by cellular traction promotes the formation of cellular networks in vitro. , 1992, Laboratory investigation; a journal of technical methods and pathology.

[7]  A. Harris,et al.  Silicone rubber substrata: a new wrinkle in the study of cell locomotion. , 1980, Science.

[8]  H. Berg,et al.  Complex patterns formed by motile cells of Escherichia coli , 1991, Nature.

[9]  Stuart K Williams,et al.  Presented at the 1995 Microcirculatory Society Meeting , 1996 .

[10]  J. Murray,et al.  A minimal mechanism for bacterial pattern formation , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[11]  James D. Murray,et al.  A Mechanical Theory of In Vitro Vascular Network Formation , 1996 .

[12]  H. Berg,et al.  Spatio-temporal patterns generated by Salmonella typhimurium. , 1995, Biophysical journal.

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

[14]  G F Oster,et al.  Generation of biological pattern and form. , 1984, IMA journal of mathematics applied in medicine and biology.

[15]  H. Meinhardt Models of biological pattern formation , 1982 .

[16]  J. Murray,et al.  Size-dependent pigmentation-pattern formation in embryos of Alligator mississippiensis: time of initiation of pattern generation mechanism , 1990, Proceedings of the Royal Society of London. B. Biological Sciences.

[17]  G F Oster,et al.  A mechanical model for mesenchymal morphogenesis , 1983, Journal of mathematical biology.

[18]  Richard Thoma,et al.  Untersuchungen über die Histogenese und Histomechanik des Gefässsystems , 1894 .

[19]  Charles D. Little,et al.  Vascular Morphogenesis: In Vivo, In Vitro, In Mente , 2011, Cardiovascular Molecular Morphogenesis.

[20]  J. Murray,et al.  A mechanical model for the formation of vascular networks in vitro , 1996, Acta biotheoretica.

[21]  G. Buchsbaum,et al.  Rheology of the vitreous body. Part I: Viscoelasticity of human vitreous. , 1992, Biorheology.

[22]  M S Kolodney,et al.  Isometric contraction by fibroblasts and endothelial cells in tissue culture: a quantitative study , 1992, The Journal of cell biology.

[23]  L. Wolpert Positional information and pattern formation. , 1981, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[24]  J. Folkman,et al.  Angiostatin induces and sustains dormancy of human primary tumors in mice , 1996, Nature Medicine.

[25]  M. Litt,et al.  Rheology of the vitreous body: Part 2. Viscoelasticity of bovine and porcine vitreous. , 1994, Biorheology.

[26]  T. Jackson,et al.  Mathematical and experimental analysis of localization of anti-tumour antibody–enzyme conjugates , 1999, British Journal of Cancer.

[27]  G. Oster,et al.  Mechanical aspects of mesenchymal morphogenesis. , 1983, Journal of embryology and experimental morphology.

[28]  Y. Fung,et al.  Biomechanics: Mechanical Properties of Living Tissues , 1981 .

[29]  T. Skalak,et al.  The Role of Mechanical Stresses in Microvascular Remodeling , 1996, Microcirculation.

[30]  G. Rubanyi Mechanoreception by the vascular wall , 1993 .

[31]  P. Maini,et al.  Mathematical Models for Biological Pattern Formation , 2001 .

[32]  P. Tracqui,et al.  Modelling Biological Gel Contraction by Cells: Mechanocellular Formulation and Cell Traction Force Quantification , 1997, Acta biotheoretica.