A mechanochemical model of angiogenesis and vasculogenesis
ESAIM: Modélisation mathématique et analyse numérique, Special issue on Biological and Biomedical Applications, Tome 37 (2003) no. 4, pp. 581-599.

Vasculogenesis and angiogenesis are two different mechanisms for blood vessel formation. Angiogenesis occurs when new vessels sprout from pre-existing vasculature in response to external chemical stimuli. Vasculogenesis occurs via the reorganization of randomly distributed cells into a blood vessel network. Experimental models of vasculogenesis have suggested that the cells exert traction forces onto the extracellular matrix and that these forces may play an important role in the network forming process. In order to study the role of the mechanical and chemical forces in both of these stages of blood vessel formation, we present a mathematical model which assumes that (i) cells exert traction forces onto the extracellular matrix, (ii) the matrix behaves as a linear viscoelastic material, (iii) the cells move along gradients of exogenously supplied chemical stimuli (chemotaxis) and (iv) these stimuli diffuse or are uptaken by the cells. We study the equations numerically, present an appropriate finite difference scheme and simulate the formation of vascular networks in a plane. Our results compare very well with experimental observations and suggest that spontaneous formation of networks can be explained via a purely mechanical interaction between cells and the extracellular matrix. We find that chemotaxis alone is not a sufficient force to stimulate formation of pattern. Moreover, during vessel sprouting, we find that mechanical forces can help in the formation of well defined vascular structures.

DOI : 10.1051/m2an:2003046
Classification : 74H15, 92C10, 92C15, 92C17
Mots-clés : angiogenesis, vasculogenesis, chemotaxis, extracellular matrix, theoretical models, numerical solution
@article{M2AN_2003__37_4_581_0,
     author = {Manoussaki, Daphne},
     title = {A mechanochemical model of angiogenesis and vasculogenesis},
     journal = {ESAIM: Mod\'elisation math\'ematique et analyse num\'erique},
     pages = {581--599},
     publisher = {EDP-Sciences},
     volume = {37},
     number = {4},
     year = {2003},
     doi = {10.1051/m2an:2003046},
     mrnumber = {2018431},
     zbl = {1080.92012},
     language = {en},
     url = {http://archive.numdam.org/articles/10.1051/m2an:2003046/}
}
TY  - JOUR
AU  - Manoussaki, Daphne
TI  - A mechanochemical model of angiogenesis and vasculogenesis
JO  - ESAIM: Modélisation mathématique et analyse numérique
PY  - 2003
SP  - 581
EP  - 599
VL  - 37
IS  - 4
PB  - EDP-Sciences
UR  - http://archive.numdam.org/articles/10.1051/m2an:2003046/
DO  - 10.1051/m2an:2003046
LA  - en
ID  - M2AN_2003__37_4_581_0
ER  - 
%0 Journal Article
%A Manoussaki, Daphne
%T A mechanochemical model of angiogenesis and vasculogenesis
%J ESAIM: Modélisation mathématique et analyse numérique
%D 2003
%P 581-599
%V 37
%N 4
%I EDP-Sciences
%U http://archive.numdam.org/articles/10.1051/m2an:2003046/
%R 10.1051/m2an:2003046
%G en
%F M2AN_2003__37_4_581_0
Manoussaki, Daphne. A mechanochemical model of angiogenesis and vasculogenesis. ESAIM: Modélisation mathématique et analyse numérique, Special issue on Biological and Biomedical Applications, Tome 37 (2003) no. 4, pp. 581-599. doi : 10.1051/m2an:2003046. http://archive.numdam.org/articles/10.1051/m2an:2003046/

[1] S.G. Advani and C.L. Tucker, The use of tensors to describe and predict fiber orientation in short fiber composites. J. Rheol. 31 (1987) 751­784.

[2] A.R. Anderson and M.A. Chaplain, Continuous and discrete mathematical models of tumor-induced angiogenesis. B. Math. Biol. 60 (1998) 857­900. | Zbl

[3] D.H. Ausprunk and J. Folkman, Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumour angiogenesis. Microvasc. Res. 14 (1977) 53­65.

[4] M.A. Chaplain, Mathematical modelling of angiogenesis. J. Neuro. 50 (2000) 37­51.

[5] M.A. Chaplain and A.R. Anderson, Mathematical modelling, simulation and prediction of tumour-induced angiogenesis. Invasion Metastasis 16 (1996) 222­234.

[6] J. Cook, Mathematical Models for Dermal Wound Healing: Wound Contraction and Scar Formation. Ph.D. thesis, University of Washington (1995).

[7] C.J. Drake and A.G. Jacobson, A survey by scanning electron microscopy of the extracellular matrix and endothelial compo- nents of the primordial chick heart. Anat. Rec. 222 (1988) 391­400.

[8] C.J. Drake and C.D. Little, The morphogenesis of primordial vascular networks. In Vascular Morphogenesis: In Vivo, In Vitro, In Mente, Charles D. Little, Vladimir Mironov and E. Helene Sage Eds., Chap. 1.1, Birkauser, Boston, MA (1998) 3­19.

[9] J. Folkman and C. Haudenschild, Angiogenesis in vitro. Nature 288 (1980) 551­556.

[10] E.A. Gaffney, K. Pugh, P.K. Maini and F. Arnold, Investigating a simple model of cutaneous would healing angiogenesis. J. Math. Biol. 45 (200) 2337­374. | MR | Zbl

[11] D. Hanahan, Signaling vascular morphogenesis and maintenance. Science 227 (1997) 48­50.

[12] M.J. Holmes and B.D. Sleeman, A mathematical model of tumor angiogenesis incorporating cellular traction and viscoelastic effects. J. Theor. Biol. 202 (2000) 95­112.

[13] Y. Lanir, Constitutive equations for fibrous connective tissues. J. Biomech. 16 (1983) 1­12.

[14] H.A. Levine, B.D. Sleeman and M. Nilsen-Hamilton, Mathematical modeling of the onset of capillary formation initiating angiogenesis. J. Math. Biol. 42 (2001) 195­238. | MR | Zbl

[15] D. Manoussaki, Modelling the formation of vascular networks in vitro. Ph.D. thesis, University of Washington (1996).

[16] D. Manoussaki, S.R. Lubkin, R.B. Vernon and J.D. Murray, A mechanical model for the formation of vascular networks in vitro. Acta Biotheoretica 44 (1996) 271­282.

[17] R.R. Markwald, T.P. Fitzharris, D.L. Bolender and D.H. Bernanke, Sturctural analysis of cell: matrix association during the morphogenesis of atrioventricular cushion tissue. Developmental Biology 69 (1979) 634­54.

[18] H. Meinhardt, Models for the formation of netline structures, in Vascular Morphogenesis: In Vivo, In Vitro, In Mente, Charles D. Little, Vladimir Mironov and E. Helene Sage Eds., Chap. 3.1, Birkauser, Boston, MA (1998) 147­172.

[19] J.D. Murray, D. Manoussaki, S.R. Lubkin and R.B. Vernon, A mechanical theory of in vitro vascular network formation, in Vascular Morphogenesis: In Vivo, In Vitro, In Mente, Charles D. Little, Vladimir Mironov and E. Helene Sage Eds., Chapter 3.2, Birkauser, Boston, MA (1998) 173­188.

[20] J.D. Murray, G.F. Oster and A.K. Harris, A mechanical model for mesenchymal morphogenesis. J. Math. Biol. 17 (1983) 125­129. | Zbl

[21] G.F. Oster, J.D. Murray and A.K. Harris, Mechanical aspects of mesenchymal morphogenesis. J. Embryol. Exp. Morph. 78 (1983) 83­125.

[22] L. Pardanaud, F. Yassine and F. Dieterlen-Lievre, Relationship between vasculogenesis, angiogenesis and haemopoiesis during avian ontogeny. Development 105 (1989) 473­485.

[23] W. Risau, H. Sariola, H.G. Zerwes, J. Sasse, P. Ekblom, R. Kemler and T. Doetschmann, Vasculogenesis and angiogenesis in embryonic-system-cell-derived embryoid bodies. Development 102 (1988) 471­478.

[24] S. Tong and F. Yuan, Numerical simulations of angiogenesis in the cornea. Microvasc. Res. 61 (2001) 14­27.

[25] R.B. Vernon, J.C. Angello, M.L. Iruela-Arispe, T.F. Lane and E.H. Sage, Reorganization of basement membrane matrices by cellular traction promotes the formation of cellular networks in vitro. Lab. Invest. 66 (1992) 536­547.

[26] R.B. Vernon, S.L. Lara, C.J. Drake, M.L. Iruela-Arispe, J.C. Angello, C.D. Little, T.N. Wight and E.H. Sage, Organized type I collagen influences endothelial patterns during “spontaneous angiogenesis in vitro”: Planar cultures as models of vascular development. In Vitro Cellular and Developmental Biology 31 (1995) 120­131.

[27] R.B. Vernon and E.H. Sage, Between molecules and morphology: extracellular matrix and the creation of vascular form. Am. J. Pathol. 147 (1995) 873­883.

Cité par Sources :