Individual Cell-Based Model for In-Vitro Mesothelial Invasion of Ovarian Cancer
Mathematical modelling of natural phenomena, Tome 5 (2010) no. 1, pp. 203-223.

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In vitro transmesothelial migration assays of ovarian cancer cells, isolated or aggregated in multicellular spheroids, are reproduced deducing suitable Cellular Potts Models (CPM). We show that the simulations are in good agreement with the experimental evidence and that the overall process is regulated by the activity of matrix metalloproteinases (MMPs) and by the interplay of the adhesive properties of the cells with the extracellular matrix and between cells, both of the same type and of different types. In particular, the process depends on the ability of the cell to induce the loosening of cadherin-mediated junctions. Coherently with experiments, it is found that single cell invasion is more conservative with a crucial role played by MMPs. A similar important role is played in cell spheroid invasion, which in comparison is more disruptive. It achieves monofocal or multifocal characteristics according to the relative adhesion affinity among cells or between them and the mesothelial layer.
DOI : 10.1051/mmnp/20105109

C. Giverso 1 ; M. Scianna 1 ; L. Preziosi 1 ; N. Lo Buono 2 ; A. Funaro 2

1 Department of Mathematics, Politecnico di Torino, Corso Duca degli Abruzzi, 24 10129 Torino, Italy
2 Laboratory of Immunogenetics, Department of Genetics, Biology and Biochemistry, University of Turin Medical School, Via Santena 19, 10126 Torino, Italy
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C. Giverso; M. Scianna; L. Preziosi; N. Lo Buono; A. Funaro. Individual Cell-Based Model for In-Vitro Mesothelial Invasion of Ovarian Cancer. Mathematical modelling of natural phenomena, Tome 5 (2010) no. 1, pp. 203-223. doi : 10.1051/mmnp/20105109. http://geodesic.mathdoc.fr/articles/10.1051/mmnp/20105109/

[1] N. Ahmed, E. W. Thomson, M. A. Quinn Epithelial - mesenchymal interconversions in normal ovarian surface epithelium and ovarian carcinomas: an exception to the norm J. Cell. Physiol. 2007 581 588

[2] J. Ahmedin, T. Murray, A. Samuels, A. Ghafoor, E. War, M. J. Thun Cancer statistics Cancer J. Clin. 2003 5 26

[3] K. M. Burleson, R. C. Casey, K. M. Skubitz, E. Pambuccian, T. R. Oegema Jr, A. P. Skubitz Ovarian carcinoma ascites spheroids adhere to extracellular matrix components and mesothelial cell monolayers Gynec. Oncol. 2004 170 181

[4] K. M. Burleson, M. P. Boente, S. E. Parmabuccian, A. P. Skubitz Ovarian carcinoma spheroids disaggregate on type I collagen and invade live mesothelial cell monolayers Clin. Exp. Metastasis 2004 685 697

[5] K. M. Burleson, M. P. Boente, S. E. Parmabuccian, A. P. Skubitz Disaggregation and invasion of ovarian carcinoma ascites spheroids J. Transl. Med. 2006 1 16

[6] S. A. Cannistra Cancer of the ovary N. Engl. J. Med. 1993 1550 1559

[7] R. C. Casey, K. M. Burleson, K. M. Skubitz, S. E. Parmabuccian, T. J. Oegema, L. E. Ruff, A. P. Skubitz β1–integrins regulate the formation and adhesion of ovarian carcinoma multicellular spheroids Am. J. Pathol. 2001 2071 2080

[8] M. Egeblad, Z. Werb New functions for the matrix metalloproteinases in cancer progression Nature 2002 2071 2080

[9] K. M. Feeley, M. Wells Precursor lesions of ovarian epithelial malignancy Histopathology 2001 87 95

[10] A. Feki, P. Berardi, G. Bellingan, A. Major, K. H. Krause, P. Petignat Dissemination of intraperitoneal ovarian cancer: Discussion of mechanisms and demonstration of lymphatic spreading in ovarian cancer model. Crit. Rev. Oncol. Hematol. 2009 1 9

[11] D. A. Fishman, Y. Liu, S. M. Ellerbroek, M. S. Stack Lysophosphatidic acid promotes Matrix Metalloproteinase (MMP) activation and MMP-dependent invasion in ovarian cancer cells Cancer Res. 2001 3194 3199

[12] A. Funaro, E. Ortolan, P. Bovino, N. Lo Buono, G. Nacci, E. Parrotta, E. Ferrero, F. Malavasi Ectoenzymes and innate immunity: the role of human CD157 in leukocyte trafficking Front. Biosci. 2009 929 943

[13] J. A. Glazier, A. Balter, N. J. Poplawski. Magnetization to morphogenesis: a brief history of the Glazier–Graner–Hogeweg model. In A. R. A. Anderson, M. A. J. Chaplain, and K. A. Rejniak editors, Single-Cell-Based Models in Biology and Medicine, Mathematics and Biosciences in Interactions, pages 79–106. Birkaüser, 2007.

[14] J. A. Glazier, F. Graner Simulation of the differential adhesion driven rearrangement of biological cells Physical. Rev. E. 1993 2128 2154

[15] F. Graner, J. A. Glazier Simulation of biological cell sorting using a two-dimensional extended Potts model Phys. Rev. Letters 1992 2013 2017

[16] H. G. E. Hentschel, T. Glimm, J. A. Glazier, S. A. Newman Dynamical mechanisms for skeletal pattern formation in the vertebrate limb Proc. R. Soc. Lond. B 2004 1713 1722

[17] J. M. Kelm, N. E. Timmins, C. J. Brown, M. Fussenegger, L.K. Nielsen Method for generation of homogeneous ulticellular tumor spheroids applicable to a wide variety of cell types Biotechnol. Bioeng. 2003 173 180

[18] H. A. Kenny, S. Kaur, L. M. Coussens, E. Lengyel The initial steps of ovarian cancer cell metastasis are mediated by MMP-2 cleavage of vitronectin and fibronectin J. Clin. Invest. 2008 1367 1379

[19] K. Lessan, D. J. Aguiar, T. J. Oegema, L. Siebenson, A. P. Skubitz CD44 and β1–integrin mediate ovarian carcinoma cell adhesion to peritoneal mesothelial cells Am. J. Pathol. 1999 1525 1537

[20] J. S. Lowergrub, H. B. Frieboes, F. Jin, Y. L. Chuang, X. Li, P. Macklin, S. M. Wise, V. Cristini. Nonlinear modeling of cancer: bridging the gap between cells and tumor. Nonlinearity. In press.

[21] A. F. M. Marée, V. A. Grieneisen P. Hogeweg. The Cellular Potts Model and biophysical properties of cells, tissues and morphogenesis. In A. R. A. Anderson, M. A. J. Chaplain, and K. A. Rejniak editors, Single-Cell-Based Models in Biology and Medicine, Mathematics and Biosciences in Interactions, pages 107–136. Birkaüser, Basel, Switzerland, 2007.

[22] R. M. H. Merks, J. A. Glazier Dynamic mechanisms of blood vessel growth Institute of Physics Publishing 2006 C1 C10

[23] R. M. H. Merks, J. A. Glazier, A. Balter, N. J. Poplawski, M. Swat The Glazier-Graner-Hogeweg model: extensions, future directions, and opportunities for further study. Mathematics and Biosciences in Interaction 2007 151 167

[24] R. M. H. Merks, J. A. Glazier A cell-centered approach to developmental biology Physica. A. 2005 113 130

[25] S. E. Mutsaers Mesothelial cells: their structure, function and role in serosal repair Respirology 2002 171 191

[26] H. Naora, D. J. Montell Ovarian cancer metastasis: integrating insights from disparate model organisms Nat. Rev. Cancer 2005 355 366

[27] M. J. Niedbala, K. Crickard, R. J. Bernacki Interactions of human ovarian tumor cells with human mesothelial cells grown on extracellular matrix. An in vitro model system for studying tumor cell adhesion and invasion Exp. Cell. Res. 1985 499 513

[28] N. J. Poplawski, A. Shirinifard, M. Swat, J. A. Glazier Simulation of single–species bacterical–biofilm growth using the Glazier–Graner–Hogeweg model and the CompuCell3D modeling environment Math. Biosci. Eng. 2008 355 388

[29] S. Patel, P. Madan, S. Getsios, M. A. Bertr, C. D. Maccalman Cadherin switching in ovarian cancer progression Int. J. Cancer. 2003 172 177

[30] L. Preziosi, A. Tosin Multiphase and multiscale trends in cancer modelling Math. Model Nat. Phenomena 2009 1 11

[31] M. L. Puiffe, C. La Page, A. Filali–Mouhim, M. Zietarska, V. Ouellet, P. N. Toniny, M. Chevrette, D. M. Provencher, A. M. Mes–Masson Characterization of ovarian cancer ascites on cell invasion, proliferation, spheroid formation, and gene expression in an in vitro model of epithelial ovarian cancer Neoplasia 2007 820 829

[32] N. J. Savill, P. Hogeweg Modelling morphogenesis: from single cells to crawling slugs J. Theor. Biol. 1997 118 124

[33] K. Sawada, A. K. Mitra, A. Reza Radjabi, V. Bhaskar, E. O. Kistner, M. Tretiakova, S. Jagadeeswaran, A. Montag, A. Becker, H. A. Kenny, M. E. Peter, V. Ramakrishnan, S. D. Yamada, E. Lengyel Loss of E-cadherin promotes ovarian cancer metastasis via α5-integrin, which is a therapeutic target Cancer Res. 2008 2329 2339

[34] M. Sawada, J. Shii, H. Akedo, O. Tanizawa An experimental model for ovarian tumor invasion of cultured mesothelial cell monolayer Lab. Invest. 1994 333 338

[35] M. Scianna, R. M. H. Merks, L. Preziosi, E. Medico Individual cell-based models of cell scatter of ARO and MLP-29 cells in response to hepatocyte growth factor J. Theor. Biol. 2009 151 160

[36] K. Shield, M. L. Ackl, N. Ahnmed, G. E. Rice Multicellular spheroids in ovarian cancer metastases: Biology and pathology Gynec. Oncol. 2008 143 148

[37] K. Shield, C. Riley, M. A. Quinn, G. E. Rice, M. L. Ackl, N. Ahnmed α2β1–integrin affects metastatic potential of ovarian carcinoma spheroids by supporting disaggregation and proteolysis J. Carcinog. 2007 6 11

[38] P. N. Skubitz, R. C. Bast Jr, E. A. Wayner, P. C. Letourneau, M. S. Wilke Expression of α6 and β4 integrins in serous ovarian carcinoma correlates with expression of the basement membrane protein laminin Am. J. Pathol. 1996 1445 1461

[39] K. Sundfeldt Cell–cell adhesion in the normal ovary and ovarian tumors of epithelial origin Molecular and Cellular Endocrinology 2003 89 96

[40] S. Yung, F. K. Li, T. M. Chan Peritoneal mesothelial cell culture and biology Perit. Dial. Int. 2006 162 173

[41] F. Wang, J. So, S. Reierstad, D. A. Fishman Vascular endothelial growth factor regulated ovarian cancer invasion and migration involves expression and activation of matrix metalloproteinases Int. J. Cancer 2006 879 888

[42] H. S. Wang, Y. Hung, C. H. Su, S. T. Peng, Y. J. Guo, M. C. Lai Mc CD44 cross-linking induces integrin-mediated adhesion and transendothelial migration in breast cancer cell line by up-regulation of LFA-1 (αLβ2) and VLA-4 (α4β1). Exp. Cell. Res. 2005 116 126

[43] Y. Zhu, K. Sunfeldt Tight junction formation in epithelial ovarian adenocarcinoma Acta Obstetricia et Gynecologica 2007 1011 1019

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