Mathematical modeling of evolution of cell networks in epithelial tissues
Ivan Krasnyakov
Mathematical modeling of evolution of cell networks in epithelial tissues
Epithelial cell networks imply a packing geometry characterized by various cell shapes and distributions in terms of number of cell neighbors and areas. Despite such simple characteristics describing cell sheets, the formation of bubble‐like cells during the morphogenesis of epithelial tissues remains poorly understood. This study proposes a topological mathematical model of morphogenesis in a squamous epithelial. We introduce a new potential that takes into account not only the elasticity of cell perimeter and area but also the elasticity of their internal angles. Additionally, we incorporate an integral equation for chemical signaling, allowing us to consider chemo‐mechanical cell interactions. In addition to the listed factors, the model takes into account essential processes in real epithelial, such as cell proliferation and intercalation. The presented mathematical model has yielded novel insights into the packing of epithelial sheets. It has been found that there are two main states: one consists of cells of the same size, and the other consists of “bubble” cells. An example is provided of the possibility of accounting for chemo‐mechanical interactions in a multicellular environment. The introduction of a parameter determining the flexibility of cell shapes enables the modeling of more complex cell behaviors, such as considering change of cell phenotype. The developed mathematical model of morphogenesis of squamous epithelium allows progress in understanding the processes of formation of cell networks. The results obtained from mathematical modeling are of significant importance for understanding the mechanisms of morphogenesis and development of epithelial tissues. Additionally, the obtained results can be applied in developing methods to influence morphogenetic processes in medical applications.
bubble‐like cells / growth epithelial tissue / mathematical model / tissue modeling / vertex model
[1] |
Aliee M , Roper JC , Landsberg KP , Pentzold C , Widmann TJ , Julicher F , et al. Physical mechanisms shaping the Drosophila dorsoventral compartment boundary. Curr Biol. 2012; 5 (11): 967- 76.
|
[2] |
Alt S , Ganguly P , Salbreux G . Vertex models: from cell mechanics to tissue morphogenesis. Phil Trans R Soc B. 2017; 372 (1720): 20150520.
|
[3] |
Scardaoni MP . Energetic convenience of cell division in biological tissues. Phys Rev E. 2022; 106 (5): 054405.
|
[4] |
Cockerell A , Wright L , Dattani A , Guo G , Smith A , Tsaneva-Atanasova K , et al. Biophysical models of early mammalian embryogenesis. Stem Cell Rep. 2023; 18 (1): 26- 46.
|
[5] |
Herold J , Behle E , Rosenbauer J , Ferruzzi J , Schung A . Development of a scoring function for comparing simulated and experimental tumor spheroids. PLoS Comput Biol. 2023; 19 (3): e1010471.
|
[6] |
Legaria-Pena JU , Sanchez-Morales F , Cortes-Poza Y . Evaluation of entropy and fractal dimension as biomarkers for tumor growth and treatment response using cellular automata. J Theor Biol. 2023; 564: 111462.
|
[7] |
Salm M , Pismen LM . Chemical and mechanical signaling in epithelial spreading. Phys Biol. 2012; 9 (2): 026009- 23.
|
[8] |
Bi D , Yang X , Marchetti CM , Manning ML . Motility-driven glass and jamming transitions in biological tissues. Phys Rev X. 2016; 6 (2): 021011.
|
[9] |
Bessonov N , Volpert V . Deformable cell model of tissue growth. Comput Times. 2017; 5 (4): 45.
|
[10] |
Bratsun DA , Krasnyakov IV , Pismen LM . Biomechanical modeling of invasive breast carcinoma under a dynamic change in cell phenotype: collective migration of large groups of cells. Biomech Model Mechanobiol. 2020; 19 (2): 723- 43.
|
[11] |
Krasnyakov IV , Bratsun DA , Pismen LM . Mathematical modeling of epithelial tissue growth. Russ J Biomech. 2020; 24 (4): 375- 88.
|
[12] |
Sato K , Umetsu D . A novel cell vertex model formulation that distinguishes the strength of contraction forces and adhesion at cell boundaries. Front Physiol. 2021; 9: 704878.
|
[13] |
Farhadifar R , Roper JC , Aigouy B , Eaton S , Julicher F . The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr Biol. 2007; 17 (24): 2095- 104.
|
[14] |
Bajpai S , Chelakkot R , Prabhakar R , Inamdar MM . Role of Delta-Notch signalling molecules on cell-cell adhesion in determining heterogeneous chemical and cell morphological patterning. Soft Matter. 2022; 18: 3505- 20.
|
[15] |
Finegan TM , Na D , Cammarota C , Skeeters AV , Nadasi TJ , Dawney NS , et al. Tissue tension and not interphase cell shape determines cell division orientation in the Drosophila follicular epithelium. EMBO J. 2019; 38 (3): e100072.
|
[16] |
Hannig J , Schafer H , Ackermann J , Hebel M , Schafer T , Doring C , et al. Bioinformatics analysis of whole slide images reveals significant neighborhood preferences of tumor cells in Hodgkin lymphoma. PLoS Comput Biol. 2020; 16 (1): e1007516.
|
[17] |
Guillot C , Lecuit T . Mechanics of epithelial tissue homeostasis and morphogenesis. Science. 2013; 340 (6137): 1185- 9.
|
[18] |
LeBrasseur N . Cells have a bubbly look. J Cell Biol. 2004; 167 (2): 190.
|
[19] |
Liu TL , Upadhyayula S , Milkie DE , Singh V , Wang K , Swinburne IA , et al. Observing the cell in its native state: imaging subcellular dynamics in multicellular organisms. Science. 2018; 360 (6386): eaaq1392.
|
[20] |
Ramanathan SP , Krajnc M , Gibson MC . Cell-size pleomorphism drives aberrant clone dispersal in proliferating epithelia. Dev Cell. 2019; 51 (1): 49- 61.
|
[21] |
Thiery JP , Sleeman JP . Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol. 2006; 7 (2): 131- 42.
|
[22] |
Chan KY , Yan C-CS , Roan HY , Hsu SC , Tseng TL , Hsiao CD , et al. Skin cells undergo asynthetic fission to expand body surfaces in zebrafish. Nature. 2022; 605 (7908): 119- 25.
|
[23] |
Miklius MP , Hilgenfeldt S . Epithelial tissue statistics: eliminating bias reveals morphological and morphogenetic features. Eur Phys J E. 2011; 34 (5): 50.
|
[24] |
Kozyrska K , Pilia G , Vishwakarma M , Wagstaff L , Goschorska M , Cirillo S , et al. p53 directs leader cell behavior, migration, and clearance during epithelial repair. Science. 2022; 375 (6581): eabl8876.
|
[25] |
Gibson MG , Patel AB , Nagpal R , Perrimon N . The emergence of geometric order in proliferating metazoan epithelia. Nature. 2006; 442 (7106): 1038- 41.
|
[26] |
Gosak M , Milojevic M , Maja M , Skok K , Perc M . Networks behind the morphology and structural design of living systems. Phys Life Rev. 2022; 41: 1- 21.
|
[27] |
Basan M , Elgeti J , Hannezo E , Levine H . Alignment of cellular motility forces with tissue flow as a mechanism for efficient wound healing. Proc Natl Acad Sci USA. 2013; 110 (7): 2452- 9.
|
[28] |
Chung CA , Yang CW , Chen CW . Analysis of cell growth and diffusion in a scaffold for cartilage tissue engineering. Biotechnol Bioeng. 2006; 20 (6): 1138- 46.
|
[29] |
Bratsun D , Krasnyakov I . Modeling the cellular microenvironment near a tissue-liquid interface during cell growth in a porous scaffold. Interfacial Phenom Heat Tran. 2022; 10 (3): 25- 44.
|
[30] |
Krasnyakov IV . Mathematical modeling of invasive carcinoma under conditions of anisotropy of chemical fields: budding and migration of cancer cells. Russ J Biomech. 2022; 26: 38- 48.
|
[31] |
Alsubaie F , Khataee H , Neufeld Z . Modelling of tissue invasion in epithelial monolayers. Life. 2023; 13 (2): 427.
|
[32] |
Bratsun DA , Krasnyakov IV . Study of architectural forms of invasive carcinoma based on the measurement of pattern complexity. Math Model Nat Phenom. 2022; 17: 15.
|
[33] |
Krasnyakov IV , Bratsun DA . Mathematical modeling of the formation of small cell groups of invasive carcinoma. Russ J Biomech. 2021; 25 (2): 147- 58.
|
[34] |
Heisenberg C-P , Bellaiche Y . Forces in tissue morphogenesis and patterning. Cell. 2013; 153 (5): 948- 62.
|
[35] |
Lecuit T , Lenne P-F . Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat Rev Mol Cell Biol. 2007; 8: 633- 44.
|
[36] |
Maitre J-L , Berthoumieux H , Krens SFG , Salbreux G , Julicher F , Paluch E , et al. Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells. Science. 2012; 338 (6104): 253- 6.
|
[37] |
Bielmeier C , Alt S , Weichselberger V , La Fortezza M , Harz H , Julicher F , et al. Interface contractility between differently fated cells drives cell elimination and cyst formation. Curr Biol. 2016; 26 (5): 563- 74.
|
[38] |
Ray RP , Matamoro-Vidal A , Ribeiro PS , Tapon N , Houle D , Salazar-Ciudad I , et al. Patterned anchorage to the apical extracellular matrix defines tissue shape in the developing appendages of Drosophila. Dev Cell. 2015; 34 (3): 310- 22.
|
[39] |
Davidson LA . Mechanical design in embryos: mechanical signalling, robustness and developmental defects. Phil Trans R Soc B. 2017; 372 (1720): 20150516.
|
[40] |
Mao Y , Green JBA . Systems morphodynamics: understanding the development of tissue hardware. Phil Trans R Soc B. 2017; 372 (1720): 20160505.
|
[41] |
Chavey D . Tilings by regular polygons - Ⅱ: a catalog of tilings. Comput Math Appl. 1989; 17 (1‐3): 147- 65.
|
/
〈 | 〉 |