Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-19T04:17:08.622Z Has data issue: false hasContentIssue false
  • English
  • Français

Individual Cell-Based Model for In-Vitro Mesothelial Invasionof Ovarian Cancer

Published online by Cambridge University Press:  03 February 2010

C. Giverso ,
M. Scianna ,
L. Preziosi ,
N. Lo Buono  and
A. Funaro
C. Giverso
Affiliation:
Department of Mathematics, Politecnico di Torino, Corso Duca degli Abruzzi, 24 10129 Torino, Italy
M. Scianna
Affiliation:
Department of Mathematics, Politecnico di Torino, Corso Duca degli Abruzzi, 24 10129 Torino, Italy
L. Preziosi*
Affiliation:
Department of Mathematics, Politecnico di Torino, Corso Duca degli Abruzzi, 24 10129 Torino, Italy
N. Lo Buono
Affiliation:
Laboratory of Immunogenetics, Department of Genetics, Biology and Biochemistry, University of Turin Medical School, Via Santena 19, 10126 Torino, Italy
A. Funaro
Affiliation:
Laboratory of Immunogenetics, Department of Genetics, Biology and Biochemistry, University of Turin Medical School, Via Santena 19, 10126 Torino, Italy
*
* Corresponding author. E-mail:[email protected]
Get access

Abstract

In vitro transmesothelial migration assays of ovarian cancer cells, isolated oraggregated in multicellular spheroids, are reproduced deducing suitable Cellular PottsModels (CPM). We show that the simulations are in good agreement with the experimentalevidence and that the overall process is regulated by the activity of matrixmetalloproteinases (MMPs) and by the interplay of the adhesive properties of the cellswith the extracellular matrix and between cells, both of the same type and of differenttypes. In particular, the process depends on the ability of the cell to induce theloosening of cadherin-mediated junctions. Coherently with experiments, it is found thatsingle cell invasion is more conservative with a crucial role played by MMPs. A similarimportant role is played in cell spheroid invasion, which in comparison is moredisruptive. It achieves monofocal or multifocal characteristics according to the relativeadhesion affinity among cells or between them and the mesothelial layer.

Keywords

ovarian cancer metastasismesotheliumcellular potts modelhybrid model
Type
Research Article
Information
Mathematical Modelling of Natural Phenomena , Volume 5 , Issue 1: Cell migration , 2010 , pp. 203 - 223
Copyright
© EDP Sciences, 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmed, N., Thomson, E. W. Quinn, M. A.. Epithelial - mesenchymal interconversions in normal ovarian surface epithelium and ovarian carcinomas: an exception to the norm . J. Cell. Physiol., 213 (2007), 581–588 CrossRefGoogle ScholarPubMed
Ahmedin, J., Murray, T., Samuels, A., Ghafoor, A., War, E. Thun, M. J.. Cancer statistics . Cancer J. Clin., 53 (2003), 5–26 Google Scholar
Burleson, K. M., Casey, R. C., Skubitz, K. M., Pambuccian, E., Oegema Jr, T. R. Skubitz, A. P.. Ovarian carcinoma ascites spheroids adhere to extracellular matrix components and mesothelial cell monolayers . Gynec. Oncol., 93 (2004), 170–181 CrossRefGoogle ScholarPubMed
Burleson, K. M., Boente, M. P., Parmabuccian, S. E. Skubitz, A. P.. Ovarian carcinoma spheroids disaggregate on type I collagen and invade live mesothelial cell monolayers . Clin. Exp. Metastasis, 21 (2004), 685–697 CrossRefGoogle ScholarPubMed
Burleson, K. M., Boente, M. P., Parmabuccian, S. E., Skubitz, A. P.. Disaggregation and invasion of ovarian carcinoma ascites spheroids . J. Transl. Med., 4 (2006), 1–16. CrossRefGoogle ScholarPubMed
Cannistra, S. A.. Cancer of the ovary . N. Engl. J. Med. 329 (1993), 1550–1559. CrossRefGoogle ScholarPubMed
Casey, R. C., Burleson, K. M., Skubitz, K. M., Parmabuccian, S. E., Oegema, T. J., Ruff, L. E. Skubitz, A. P.. β 1–integrins regulate the formation and adhesion of ovarian carcinoma multicellular spheroids . Am. J. Pathol., 159 (2001), 2071–2080 CrossRefGoogle Scholar
Egeblad, M. Werb, Z.. New functions for the matrix metalloproteinases in cancer progression . Nature, 2 (2002), 2071–2080 Google ScholarPubMed
Feeley, K. M., Wells, M.. Precursor lesions of ovarian epithelial malignancy . Histopathology, 38 (2001), 87–95. CrossRefGoogle ScholarPubMed
Feki, A., Berardi, P., Bellingan, G., Major, A., Krause, K. H., Petignat, P.. Dissemination of intraperitoneal ovarian cancer: Discussion of mechanisms and demonstration of lymphatic spreading in ovarian cancer model. Crit. Rev. Oncol. Hematol., 72 (2009), 1–9. CrossRefGoogle ScholarPubMed
Fishman, D. A., Liu, Y., Ellerbroek, S. M. Stack, M. S.. Lysophosphatidic acid promotes Matrix Metalloproteinase (MMP) activation and MMP-dependent invasion in ovarian cancer cells . Cancer Res., 61 (2001), 3194–3199 Google ScholarPubMed
Funaro, A., Ortolan, E., Bovino, P., Lo Buono, N., Nacci, G., Parrotta, E., Ferrero, E. Malavasi, F.. Ectoenzymes and innate immunity: the role of human CD157 in leukocyte trafficking . Front. Biosci., 14 (2009), 929–943 CrossRefGoogle ScholarPubMed
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.
Glazier, J. A. Graner, F. Simulation of the differential adhesion driven rearrangement of biological cells . Physical. Rev. E., 47 (1993), 2128–2154 CrossRefGoogle ScholarPubMed
Graner, F. Glazier, J. A.. Simulation of biological cell sorting using a two-dimensional extended Potts model . Phys. Rev. Letters, 69 (1992), 2013–2017 CrossRefGoogle ScholarPubMed
Hentschel, H. G. E., Glimm, T., Glazier, J. A., Newman, S. A.. Dynamical mechanisms for skeletal pattern formation in the vertebrate limb . Proc. R. Soc. Lond. B (2004), 1713–1722. CrossRefGoogle ScholarPubMed
Kelm, J. M., Timmins, N. E., Brown, C. J., Fussenegger, M. Nielsen, L.K.. Method for generation of homogeneous ulticellular tumor spheroids applicable to a wide variety of cell types . Biotechnol. Bioeng., 83 (2003), 173–180 CrossRefGoogle ScholarPubMed
Kenny, H. A., Kaur, S., Coussens, L. M., Lengyel, E.. The initial steps of ovarian cancer cell metastasis are mediated by MMP-2 cleavage of vitronectin and fibronectin . J. Clin. Invest. 118 (2008), 1367–1379. CrossRefGoogle ScholarPubMed
Lessan, K., Aguiar, D. J., Oegema, T. J., Siebenson, L. Skubitz, A. P.. CD44 and β 1–integrin mediate ovarian carcinoma cell adhesion to peritoneal mesothelial cells . Am. J. Pathol., 154 (1999), 1525–1537 CrossRefGoogle Scholar
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.
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.
Merks, R. M. H. Glazier, J. A.. Dynamic mechanisms of blood vessel growth . Institute of Physics Publishing, 19 (2006), C1–C10 Google ScholarPubMed
Merks, R. M. H., Glazier, J. A., Balter, A., Poplawski, N. J., Swat, M.. The Glazier-Graner-Hogeweg model: extensions, future directions, and opportunities for further study. Mathematics and Biosciences in Interaction (2007), 151–167. Google Scholar
Merks, R. M. H. Glazier, J. A.. A cell-centered approach to developmental biology . Physica. A., 352 (2005), 113–130 CrossRefGoogle Scholar
Mutsaers, S. E.. Mesothelial cells: their structure, function and role in serosal repair . Respirology, 7 (2002), 171–191 CrossRefGoogle ScholarPubMed
Naora, H., Montell, D. J.. Ovarian cancer metastasis: integrating insights from disparate model organisms . Nat. Rev. Cancer, 5 (2005), 355–366. CrossRefGoogle ScholarPubMed
Niedbala, M. J., Crickard, K. Bernacki, R. J.. 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., 160 (1985), 499–513 CrossRefGoogle Scholar
Poplawski, N. J., Shirinifard, A., Swat, M. Glazier, J. A.. Simulation of single–species bacterical–biofilm growth using the Glazier–Graner–Hogeweg model and the CompuCell3D modeling environment . Math. Biosci. Eng., 5 (2008), 355–388 Google ScholarPubMed
Patel, S., Madan, P., Getsios, S., Bertr, M. A. Maccalman, C. D.. Cadherin switching in ovarian cancer progression . Int. J. Cancer., 106 (2003), 172–177 CrossRefGoogle ScholarPubMed
Preziosi, L. Tosin, A.. Multiphase and multiscale trends in cancer modelling . Math. Model Nat. Phenomena, 4 (2009), 1–11 CrossRefGoogle Scholar
Puiffe, M. L., La Page, C., Filali–Mouhim, A., Zietarska, M., Ouellet, V., Toniny, P. N., Chevrette, M., Provencher, D. M. Mes–Masson, A. M.. Characterization of ovarian cancer ascites on cell invasion, proliferation, spheroid formation, and gene expression in an in vitro model of epithelial ovarian cancer . Neoplasia, 9 (2007), 820–829 CrossRefGoogle Scholar
Savill, N. J. Hogeweg, P.. Modelling morphogenesis: from single cells to crawling slugs . J. Theor. Biol., 184 (1997), 118–124 CrossRefGoogle Scholar
Sawada, K., Mitra, A. K., Reza Radjabi, A., Bhaskar, V., Kistner, E. O., Tretiakova, M., Jagadeeswaran, S., Montag, A., Becker, A., Kenny, H. A., Peter, M. E., Ramakrishnan, V., Yamada, S. D. Lengyel, E.. Loss of E-cadherin promotes ovarian cancer metastasis via α 5-integrin, which is a therapeutic target . Cancer Res., 68 (2008), 2329–2339 CrossRefGoogle ScholarPubMed
Sawada, M., Shii, J., Akedo, H. Tanizawa, O.. An experimental model for ovarian tumor invasion of cultured mesothelial cell monolayer . Lab. Invest., 70 (1994), 333–338 Google ScholarPubMed
Scianna, M., Merks, R. M. H., Preziosi, L., Medico, E.. Individual cell-based models of cell scatter of ARO and MLP-29 cells in response to hepatocyte growth factor . J. Theor. Biol. 260 (2009), 151–160. CrossRefGoogle ScholarPubMed
Shield, K., Ackl, M. L., Ahnmed, N. Rice, G. E.. Multicellular spheroids in ovarian cancer metastases: Biology and pathology . Gynec. Oncol., 113 (2008), 143–148 CrossRefGoogle ScholarPubMed
Shield, K., Riley, C., Quinn, M. A., Rice, G. E., Ackl, M. L. Ahnmed, N.. α 2 β 1–integrin affects metastatic potential of ovarian carcinoma spheroids by supporting disaggregation and proteolysis . J. Carcinog., 6 (2007), 6–11 CrossRefGoogle Scholar
Skubitz, P. N., Bast Jr, R. C., Wayner, E. A., Letourneau, P. C. Wilke, M. S.. Expression of α 6 and β 4 integrins in serous ovarian carcinoma correlates with expression of the basement membrane protein laminin . Am. J. Pathol., 148 (1996), 1445–1461 Google ScholarPubMed
Sundfeldt, K.. Cell–cell adhesion in the normal ovary and ovarian tumors of epithelial origin; an exception to the rule . Molecular and Cellular Endocrinology, 202 (2003), 89–96. CrossRefGoogle Scholar
Yung, S., Li, F. K. Chan, T. M.. Peritoneal mesothelial cell culture and biology . Perit. Dial. Int., 26 (2006), 162–173 Google Scholar
Wang, F., So, J., Reierstad, S. Fishman, D. A.. Vascular endothelial growth factor regulated ovarian cancer invasion and migration involves expression and activation of matrix metalloproteinases . Int. J. Cancer, 118 (2006), 879–888 CrossRefGoogle Scholar
Wang, H. S., Hung, Y., Su, C. H., Peng, S. T., Guo, Y. J., Lai MC, M. C.. 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., 304 (2005), 116–126. CrossRefGoogle Scholar
Zhu, Y. Sunfeldt, K.. Tight junction formation in epithelial ovarian adenocarcinoma . Acta Obstetricia et Gynecologica, 86 (2007), 1011–1019 CrossRefGoogle ScholarPubMed