Mesoscopic and continuum modelling of angiogenesis

Angiogenesis is the formation of new blood vessels from pre-existing ones in response to chemical signals secreted by, for example, a wound or a tumour. In this paper, we propose a mesoscopic lattice-based model of angiogenesis, in which processes that include proliferation and cell movement are considered as stochastic events. By studying the dependence of the model on the lattice spacing and the number of cells involved, we are able to derive the deterministic continuum limit of our equations and compare it to similar existing models of angiogenesis. We further identify conditions under which the use of continuum models is justified, and others for which stochastic or discrete effects dominate. We also compare different stochastic models for the movement of endothelial tip cells which have the same macroscopic, deterministic behaviour, but lead to markedly different behaviour in terms of production of new vessel cells.

[1]  S. McDougall,et al.  Mathematical modeling of tumor-induced angiogenesis. , 2006, Annual review of biomedical engineering.

[2]  D. Gillespie Exact Stochastic Simulation of Coupled Chemical Reactions , 1977 .

[3]  Robert J. Gillies,et al.  Multiscale Modelling of Vascular Tumour Growth in 3D: The Roles of Domain Size and Boundary Conditions , 2011, PloS one.

[4]  H M Byrne,et al.  A mathematical model to study the effects of drug resistance and vasculature on the response of solid tumors to chemotherapy. , 2000, Mathematical biosciences.

[5]  P. Carmeliet,et al.  Angiogenesis in cancer and other diseases , 2000, Nature.

[6]  P. Carmeliet Mechanisms of angiogenesis and arteriogenesis , 2000, Nature Medicine.

[7]  Kenneth Falconer,et al.  Fractal Geometry: Mathematical Foundations and Applications , 1990 .

[8]  R. Jain Normalization of Tumor Vasculature: An Emerging Concept in Antiangiogenic Therapy , 2005, Science.

[9]  Vincenzo Capasso,et al.  Stochastic modelling of tumour-induced angiogenesis , 2009, Journal of mathematical biology.

[10]  Robert S. Kerbel,et al.  Antiangiogenic therapy: impact on invasion, disease progression, and metastasis , 2011, Nature Reviews Clinical Oncology.

[11]  Howard A. Levine,et al.  Partial differential equations of chemotaxis and angiogenesis , 2001 .

[12]  D. Gillespie A General Method for Numerically Simulating the Stochastic Time Evolution of Coupled Chemical Reactions , 1976 .

[13]  Helen M Byrne,et al.  A multiphase model describing vascular tumour growth , 2003, Bulletin of mathematical biology.

[14]  M J Plank,et al.  A reinforced random walk model of tumour angiogenesis and anti-angiogenic strategies. , 2003, Mathematical medicine and biology : a journal of the IMA.

[15]  Lei Xu,et al.  Normalization of the vasculature for treatment of cancer and other diseases. , 2011, Physiological reviews.

[16]  B. Sleeman,et al.  Mathematical modeling of the onset of capillary formation initiating angiogenesis , 2001, Journal of mathematical biology.

[17]  J. T. Henriksson,et al.  Dimensions and morphology of the cornea in three strains of mice. , 2009, Investigative ophthalmology & visual science.

[18]  Anusuya Das,et al.  A hybrid continuum–discrete modelling approach to predict and control angiogenesis: analysis of combinatorial growth factor and matrix effects on vessel-sprouting morphology , 2010, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[19]  Yi Jiang,et al.  A cell-based model exhibiting branching and anastomosis during tumor-induced angiogenesis. , 2007, Biophysical journal.

[20]  A.A. Qutub,et al.  Multiscale models of angiogenesis , 2009, IEEE Engineering in Medicine and Biology Magazine.

[21]  Andreas Deutsch,et al.  Cellular Automaton Models of Tumor Development: a Critical Review , 2002, Adv. Complex Syst..

[22]  K. Painter,et al.  A User's Guide to Pde Models for Chemotaxis , 2022 .

[23]  K. Alitalo,et al.  VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia , 2003, The Journal of cell biology.

[24]  Eugenia Corvera Poiré,et al.  Tumor Angiogenesis and Vascular Patterning: A Mathematical Model , 2011, PloS one.

[25]  M. Chaplain,et al.  A model mechanism for the chemotactic response of endothelial cells to tumour angiogenesis factor. , 1993, IMA journal of mathematics applied in medicine and biology.

[26]  G. Yancopoulos,et al.  New model of tumor angiogenesis: dynamic balance between vessel regression and growth mediated by angiopoietins and VEGF , 1999, Oncogene.

[27]  S. McDougall,et al.  Mathematical modelling of flow through vascular networks: Implications for tumour-induced angiogenesis and chemotherapy strategies , 2002, Bulletin of mathematical biology.

[28]  Holger Gerhardt,et al.  Basic and Therapeutic Aspects of Angiogenesis , 2011, Cell.

[29]  M. J. Holmes,et al.  A mathematical model of tumour angiogenesis incorporating cellular traction and viscoelastic effects. , 2000, Journal of theoretical biology.

[30]  D. Sherrington Stochastic Processes in Physics and Chemistry , 1983 .

[31]  Vittorio Cristini,et al.  Three-dimensional multispecies nonlinear tumor growth-II: Tumor invasion and angiogenesis. , 2010, Journal of theoretical biology.

[32]  S. McDougall,et al.  Multiscale modelling and nonlinear simulation of vascular tumour growth , 2009, Journal of mathematical biology.

[33]  W. Ebeling Stochastic Processes in Physics and Chemistry , 1995 .

[34]  Leah Edelstein,et al.  The propagation of fungal colonies: a model for tissue growth , 1982 .

[35]  N. Kampen,et al.  Stochastic processes in physics and chemistry , 1981 .

[36]  P. Carmeliet,et al.  Molecular mechanisms and clinical applications of angiogenesis , 2011, Nature.

[37]  H. Othmer,et al.  Mathematical modeling of tumor-induced angiogenesis , 2004, Journal of mathematical biology.

[38]  P. Hahnfeldt,et al.  Tumor development under angiogenic signaling: a dynamical theory of tumor growth, treatment response, and postvascular dormancy. , 1999, Cancer research.

[39]  M. Chaplain,et al.  Continuous and discrete mathematical models of tumor-induced angiogenesis , 1998, Bulletin of mathematical biology.

[40]  P. Maini,et al.  A practical guide to stochastic simulations of reaction-diffusion processes , 2007, 0704.1908.

[41]  Didier Bresch,et al.  A pharmacologically based multiscale mathematical model of angiogenesis and its use in investigating the efficacy of a new cancer treatment strategy. , 2009, Journal of theoretical biology.

[42]  M. Chaplain Avascular growth, angiogenesis and vascular growth in solid tumours: The mathematical modelling of the stages of tumour development , 1996 .

[43]  D. Hanahan,et al.  The Hallmarks of Cancer , 2000, Cell.

[44]  D A Lauffenburger,et al.  Analysis of the roles of microvessel endothelial cell random motility and chemotaxis in angiogenesis. , 1991, Journal of theoretical biology.

[45]  H. Byrne Dissecting cancer through mathematics: from the cell to the animal model , 2010, Nature Reviews Cancer.

[46]  J Folkman,et al.  Transplacental carcinogenesis by stilbestrol. , 1971, The New England journal of medicine.

[47]  M. Roizen,et al.  Hallmarks of Cancer: The Next Generation , 2012 .

[48]  Shayn M Peirce,et al.  Computational and Mathematical Modeling of Angiogenesis , 2008, Microcirculation.

[49]  Alberto Gandolfi,et al.  Tumour eradication by antiangiogenic therapy: analysis and extensions of the model by Hahnfeldt et al. (1999). , 2004, Mathematical biosciences.

[50]  Mark A. J. Chaplain,et al.  A mathematical model of vascular tumour growth and invasion , 1996 .

[51]  J. Folkman Angiogenesis in cancer, vascular, rheumatoid and other disease , 1995, Nature Medicine.

[52]  R. Erban,et al.  Reactive boundary conditions for stochastic simulations of reaction–diffusion processes , 2007, Physical biology.

[53]  M. Chaplain,et al.  Mathematical Modelling of Angiogenesis , 2000, Journal of Neuro-Oncology.

[54]  S. McDougall,et al.  Mathematical modelling of dynamic adaptive tumour-induced angiogenesis: clinical implications and therapeutic targeting strategies. , 2006, Journal of theoretical biology.

[55]  J. Folkman Tumor angiogenesis: therapeutic implications. , 1971, The New England journal of medicine.

[56]  H. M. Byrne,et al.  Mathematical models for tumour angiogenesis: Numerical simulations and nonlinear wave solutions , 1995 .

[57]  D L S McElwain,et al.  A history of the study of solid tumour growth: The contribution of mathematical modelling , 2004, Bulletin of mathematical biology.

[58]  L. Preziosi,et al.  Mechanics and Chemotaxis in the Morphogenesis of Vascular Networks , 2006, Bulletin of mathematical biology.

[59]  Hans G. Othmer,et al.  Aggregation, Blowup, and Collapse: The ABC's of Taxis in Reinforced Random Walks , 1997, SIAM J. Appl. Math..

[60]  K. Painter,et al.  Volume-filling and quorum-sensing in models for chemosensitive movement , 2002 .

[61]  Philip Hahnfeldt,et al.  Simple ODE models of tumor growth and anti-angiogenic or radiation treatment , 2001 .

[62]  S. Jonathan Chapman,et al.  Mathematical Models of Avascular Tumor Growth , 2007, SIAM Rev..

[63]  Helen M. Byrne,et al.  A Multiple Scale Model for Tumor Growth , 2005, Multiscale Model. Simul..

[64]  M. Plank,et al.  Lattice and non-lattice models of tumour angiogenesis , 2004, Bulletin of mathematical biology.

[65]  J. Folkman What is the evidence that tumors are angiogenesis dependent? , 1990, Journal of the National Cancer Institute.

[66]  P. Wen,et al.  Antiangiogenic therapies for high-grade glioma , 2009, Nature Reviews Neurology.

[67]  Philip K Maini,et al.  Angiogenesis and vascular remodelling in normal and cancerous tissues , 2009, Journal of mathematical biology.

[68]  Xiaoming Zheng,et al.  A Cell-based Model of Endothelial Cell Migration, Proliferation and Maturation During Corneal Angiogenesis , 2010, Bulletin of mathematical biology.

[69]  B. Sleeman,et al.  Mathematical modeling of capillary formation and development in tumor angiogenesis: Penetration into the stroma , 2001, Bulletin of mathematical biology.

[70]  Nitzan Resnick,et al.  Fluid shear stress and the vascular endothelium: for better and for worse. , 2003, Progress in biophysics and molecular biology.

[71]  F. M. Gabhann,et al.  receptors on endothelial cells growth factor and placental growth factor to VEGF Model of competitive binding of vascular endothelial , 2005 .

[72]  D. Balding,et al.  A mathematical model of tumour-induced capillary growth. , 1985, Journal of theoretical biology.

[73]  W. Risau,et al.  Mechanisms of angiogenesis , 1997, Nature.