Iranian Journal of Biomedical Engineering (IJBME)
نشریه علمی مهندسی پزشکی زیستی

Effect of Matrix Fiber Orientation under Fluid Flow on Endothelial Vasculogenesis using Cellular Potts Model

Document Type : Full Research Paper

Authors

Pooya Abdi 1
Bahman Vahidi 2

1 Ph.D. in Biomedical Engineering, Department of Medical Technologies and Tissue Engineering, Faculty of New Sciences and Technologies (FNST), University of Tehran, Tehran, Iran

2 Associate Professor, Department of Medical Technologies and Tissue Engineering, Faculty of New Sciences and Technologies (FNST), University of Tehran, Tehran, Iran

https://doi.org/10.22041/ijbme.2023.1998780.1835
Abstract
Topography of extracellular matrix plays a major role in many biological events including tissue healing, morphogenesis and growth. It is known that matrix constitution and mechanical properties are deciding factors in governing the fate of its inhabitant cells. Besides the direct mechanical cues, matrices also facilitate the release and uptake of certain chemicals and participate in cell-cell and cell-ECM crosstalk. Mechanical strains in the matrix are proved to direct endothelial cell migration and elongation leading to angiogenesis, and there is a consensus that matrix stiffness, fiber density and fiber orientation can enhance angiogenesis in the preferred direction of stiffness gradient. In this study, we specifically investigated the role of topography in guidance of endothelial self-reorganization prompted by the effect of fluid flow hindrance and facilitation in certain directions. We adopted our previous model of fluid flow guided angiogenesis for cellular responses. Lattice Boltzmann model of fluid flow was adopted and modified to study the effect of unidirectional and randomly oriented fibers. To study the effect of fiber orientation, we customized a previously proposed model of porosity in lattice Boltzmann to suit this purpose. This model could reproduce the effects of fiber orientations in matrix on endothelial migration and vasculogenesis. Simulations showed better confluency of formed lumens when prescribed flow is in the direction of fiber orientation. These results can have further implications in understanding endothelial complications in certain diseases as well as in tumor angiogenesis and metastasis.

Keywords

Cellular Potts Model
Angiogenesis
Extracellular Matrix
Fiber Orientation
Cellular Guidance
Subjects
  1. van Oers RF, Rens EG, LaValley DJ, Reinhart-King CA, Merks RM. Mechanical cell-matrix feedback explains pairwise and collective endothelial cell behavior in vitro. PLoS computational biology. 2014 Aug 14; 10 (8): e1003774.
  2. JBauer AL, Jackson TL, Jiang Y. Topography of extracellular matrix mediates vascular morphogenesis and migration speeds in angiogenesis. PLoS computational biology. 2009 Jul 24; 5(7): e1000445.
  3. Zheng Y, Nan H, Liu Y, Fan Q, Wang X, Liu R, Liu L, Ye F, Sun B, Jiao Y. Modeling cell migration regulated by cell extracellular-matrix micromechanical coupling. Physical Review E. 2019 Oct 11; 100(4): 043303.
  4. Suveges S, Chamseddine I, Rejniak KA, Eftimie R, Trucu D. Collective Cell Migration in a Fibrous Environment: A Hybrid Multiscale Modelling Approach. Frontiers in applied mathematics and statistics. 2021 Jun 25; 7: 680029.
  5. Kim MC, Silberberg YR, Abeyaratne R, Kamm RD, Asada HH. Computational modeling of three-dimensional ECM-rigidity sensing to guide directed cell migration. Proceedings of the National Academy of Sciences. 2018 Jan 16; 115(3): E390-9.
  6. Scianna M, Preziosi L. Multiscale developments of the cellular Potts model. Multiscale Modeling & Simulation. 2012; 10(2): 342-82.
  7. Chen S, Doolen GD. Lattice Boltzmann method for fluid flows. Annual review of fluid mechanics. 1998 Jan; 30(1): 329-64.
  8. Abdi P, Vahidi B. A vasculogenesis model based on flow-induced stresses on endothelial cells. AIP Advances. 2022 May 1; 12(5): 055306.
  9. Spaid MA, Phelan Jr FR. Lattice Boltzmann methods for modeling microscale flow in fibrous porous media. Physics of fluids. 1997 Sep; 9(9): 2468-74.
  10. Oakley C, Jaeger NA, Brunette DM. Sensitivity of fibroblasts and their cytoskeletons to substratum topographies: topographic guidance and topographic compensation by micromachined grooves of different dimensions. Experimental cell research. 1997 Aug 1; 234(2): 413-24.
  11. Park J, Kim DH, Levchenko A. Topotaxis: a new mechanism of directed cell migration in topographic ECM gradients. Biophysical journal. 2018 Mar 27; 114(6): 1257-63.
  12. Fischer RS, Sun X, Baird MA, Hourwitz MJ, Seo BR, Pasapera AM, Mehta SB, Losert W, Fischbach C, Fourkas JT, Waterman CM. Contractility, focal adhesion orientation, and stress fiber orientation drive cancer cell polarity and migration along wavy ECM substrates. Proceedings of the National Academy of Sciences. 2021 Jun 1; 118 (22): e2021135118.
  13. Dessalles CA, Leclech C, Castagnino A, Barakat AI. Integration of substrate-and flow-derived stresses in endothelial cell mechanobiology. Communications Biology. 2021 Jun 21;4(1):1-5.
  14. Azimzade Y, Saberi AA, Sahimi M. Regulation of migration of chemotactic tumor cells by the spatial distribution of collagen fiber orientation. Physical Review E. 2019 Jun 27; 99(6):062414.
  15. McCoy MG, Wei JM, Choi S, Goerger JP, Zipfel W, Fischbach C. Collagen fiber orientation regulates 3D vascular network formation and alignment. ACS Biomaterials Science & Engineering. 2018 Jun 26; 4(8): 2967-76.
  16. Du Y, Herath SC, Wang QG, Wang DA, Asada HH, Chen PC. Three-dimensional characterization of mechanical interactions between endothelial cells and extracellular matrix during angiogenic sprouting. Scientific Reports. 2016 Feb 23; 6(1): 1-4.
  17. Yi B, Shen Y, Tang H, Wang X, Zhang Y. Stiffness of the aligned fibers affects structural and functional integrity of the oriented endothelial cells. Acta biomaterialia. 2020 May 1; 108: 237-49.
  18. Balcioglu HE, van de Water B, Danen EH. Tumor-induced remote ECM network orientation steers angiogenesis. Scientific reports. 2016 Mar 2; 6(1): 1-2.
  19. Roghani Yazdi, Mahdie, Nadia Naghavi, and Faride Sadat Hosseini. "Modeling and simulation of vascular tumor growth." Iranian Journal of Biomedical Engineering 9.2 (2015): 143-161.
Iranian Journal of Biomedical Engineering (IJBME)
Volume 17, Issue 1
Spring 2023
Pages 15-24

  • Receive Date 20 March 2023
  • Revise Date 25 October 2023
  • Accept Date 25 October 2023

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