Active Vertex Model for cell-resolution description of epithelial tissue mechanics

Abstract

We introduce an Active Vertex Model (AVM) for cell-resolution studies of the mechanics of confluent epithelial tissues consisting of tens of thousands of cells, with a level of detail inaccessible to similar methods. The AVM combines the Vertex Model for confluent epithelial tissues with active matter dynamics. This introduces a natural description of the cell motion and accounts for motion patterns observed on multiple scales. Furthermore, cell contacts are generated dynamically from positions of cell centres. This not only enables efficient numerical implementation, but provides a natural description of the T1 transition events responsible for local tissue rearrangements. The AVM also includes cell alignment, cell-specific mechanical properties, cell growth, division and apoptosis. In addition, the AVM introduces a flexible, dynamically changing boundary of the epithelial sheet allowing for studies of phenomena such as the fingering instability or wound healing. We illustrate these capabilities with a number of case studies.

Full text

Its licence does not allow us to show the full text. Read it at PubMed Central:

References 116

1. 1.

   Ilina O, Friedl P. Mechanisms of collective cell migration at a glance. Journal of cell science. 2009;122(18):3203–3208.

   Not in our library10.1242/jcs.036525

2. 2.

   Weijer CJ. Collective cell migration in development. Journal of cell science. 2009;122(18):3215–3223.

   Not in our library10.1242/jcs.036517

3. 3.

   Forgacs G, Newman SA. Biological physics of the developing embryo. Cambridge University Press; 2005.

   Not in our library

4. 4.

   Martin P. Wound healing–aiming for perfect skin regeneration. Science. 1997;276(5309):75–81.

   Not in our library10.1126/science.276.5309.75

5. 5.

   Brugués A, Anon E, Conte V, Veldhuis JH, Gupta M, Colombelli J, et al Forces driving epithelial wound healing. Nature Physics. 2014;10:683–690.

   Not in our library10.1038/nphys3040

6. 6.

   Wirtz D, Konstantopoulos K, Searson PC. The physics of cancer: the role of physical interactions and mechanical forces in metastasis. Nature Reviews Cancer. 2011;11(7):512–522.

   Not in our library10.1038/nrc3080

7. 7.

   Guillot C, Lecuit T. Mechanics of epithelial tissue homeostasis and morphogenesis. Science. 2013;340(6137):1185–1189.

   Not in our library10.1126/science.1235249

8. 8.

   Schatten GP, Schnell S, Maini P, Newman SA, Newman T. Multiscale modeling of developmental systems. vol. 81 Academic Press; 2007.

   Not in our library10.1016/s0070-2153(07)81018-0

9. 9.

   Lecuit T, Lenne PF, Munro E. Force generation, transmission, and integration during cell and tissue morphogenesis. Annual review of cell and developmental biology. 2011;27:157–184.

   Not in our library10.1146/annurev-cellbio-100109-104027

10. 10.

    Harris AK, Wild P, Stopak D. Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science. 1980;208(4440):177–179.

    Not in our library10.1126/science.6987736

11. 11.

    Angelini TE, Hannezo E, Trepat X, Marquez M, Fredberg JJ, Weitz DA. Glass-like dynamics of collective cell migration. Proceedings of the National Academy of Sciences. 2011;108(12):4714–4719.

    Not in our library10.1073/pnas.1010059108

12. 12.

    Tambe DT, Hardin CC, Angelini TE, Rajendran K, Park CY, Serra-Picamal X, et al Collective cell guidance by cooperative intercellular forces. Nature materials. 2011;10(6):469–475.

    Not in our library10.1038/nmat3025

13. 13.

    Trepat X, Fredberg JJ. Plithotaxis and emergent dynamics in collective cellular migration. Trends in cell biology. 2011;21(11):638–646.

    Not in our library10.1016/j.tcb.2011.06.006

14. 14.

    Sadati M, Qazvini NT, Krishnan R, Park CY, Fredberg JJ. Collective migration and cell jamming. Differentiation. 2013;86(3):121–125.

    Not in our library10.1016/j.diff.2013.02.005

15. 15.

    Berthier L, Biroli G, Bouchaud JP, Cipelletti L, van Saarloos W. Dynamical heterogeneities in glasses, colloids, and granular media. Oxford University Press; 2011.

    Not in our library

16. 16.

    Bazellières E, Conte V, Elosegui-Artola A, Serra-Picamal X, Bintanel-Morcillo M, Roca-Cusachs P, et al Control of cell–cell forces and collective cell dynamics by the intercellular adhesome. Nature cell biology. 2015;17(4):409–420.

    Not in our library10.1038/ncb3135

17. 17.

    Charras G, Sahai E. Physical influences of the extracellular environment on cell migration. Nature Reviews Molecular Cell Biology. 2014;15(12):813–824.

    Not in our library10.1038/nrm3897

18. 18.

    Discher DE, Janmey P, Wang Yl. Tissue cells feel and respond to the stiffness of their substrate. Science. 2005;310(5751):1139–1143.

    Not in our library10.1126/science.1116995

19. 19.

    Elosegui-Artola A, Bazellières E, Allen MD, Andreu I, Oria R, Sunyer R, et al Rigidity sensing and adaptation through regulation of integrin types. Nature materials. 2014;13(6):631–637.

    Not in our library10.1038/nmat3960

20. 20.

    Kim JH, Serra-Picamal X, Tambe DT, Zhou EH, Park CY, Sadati M, et al Propulsion and navigation within the advancing monolayer sheet. Nature materials. 2013;12(9):856–863.

    Not in our library10.1038/nmat3689

21. 21.

    Das T, Safferling K, Rausch S, Grabe N, Boehm H, Spatz JP. A molecular mechanotransduction pathway regulates collective migration of epithelial cells. Nature cell biology. 2015;17(3):276–287.

    Not in our library10.1038/ncb3115

22. 22.
    Mechanics of epithelial closure over non-adherent environments · 2015

    No notice
23. 23.

    Serra-Picamal X, Conte V, Sunyer R, Muñoz JJ, Trepat X. Mapping forces and kinematics during collective cell migration. Methods in cell biology. 2015;125:309–330.

    Not in our library10.1016/bs.mcb.2014.11.003

24. 24.

    Keller PJ, Schmidt AD, Wittbrodt J, Stelzer EH. Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy. science. 2008;322(5904):1065–1069.

    Not in our library10.1126/science.1162493

25. 25.

    Manning ML, Foty RA, Steinberg MS, Schoetz EM. Coaction of intercellular adhesion and cortical tension specifies tissue surface tension. Proceedings of the National Academy of Sciences. 2010;107(28):12517–12522.

    Not in our library10.1073/pnas.1003743107

26. 26.

    Blanchard GB, Kabla AJ, Schultz NL, Butler LC, Sanson B, Gorfinkiel N, et al Tissue tectonics: morphogenetic strain rates, cell shape change and intercalation. Nature methods. 2009;6(6):458–464.

    Not in our library10.1038/nmeth.1327

27. 27.

    Butler LC, Blanchard GB, Kabla AJ, Lawrence NJ, Welchman DP, Mahadevan L, et al Cell shape changes indicate a role for extrinsic tensile forces in Drosophila germ-band extension. Nature cell biology. 2009;11(7):859–864.

    Not in our library10.1038/ncb1894

28. 28.

    Keller PJ, Schmidt AD, Santella A, Khairy K, Bao Z, Wittbrodt J, et al Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy. Nature methods. 2010;7(8):637–642.

    Not in our library10.1038/nmeth.1476

29. 29.

    Bosveld F, Bonnet I, Guirao B, Tlili S, Wang Z, Petitalot A, et al Mechanical control of morphogenesis by Fat/Dachsous/Four-jointed planar cell polarity pathway. Science. 2012;336(6082):724–727.

    Not in our library10.1126/science.1221071

30. 30.

    Collinet C, Rauzi M, Lenne PF, Lecuit T. Local and tissue-scale forces drive oriented junction growth during tissue extension. Nature cell biology. 2015;.

    Not in our library10.1038/ncb3226

31. 31.
    Interplay of cell dynamics and epithelial tension during morphogenesis of the Drosophila pupal wing · 2015

    No notice
32. 32.

    Etournay R, Merkel M, Popović M, Brandl H, Dye NA, Aigouy B, et al TissueMiner: a multiscale analysis toolkit to quantify how cellular processes create tissue dynamics. eLife. 2016;5:e14334

    Not in our library10.7554/elife.14334

33. 33.

    Rozbicki E, Chuai M, Karjalainen AI, Song F, Sang HM, Martin R, et al Myosin-II-mediated cell shape changes and cell intercalation contribute to primitive streak formation. Nature cell biology. 2015;17(4):397–408.

    Not in our library10.1038/ncb3138

34. 34.

    Anderson A, Rejniak K. Single-cell-based models in biology and medicine. Springer Science & Business Media; 2007.

    Not in our library

35. 35.

    Graner F, Glazier JA. Simulation of biological cell sorting using a two-dimensional extended Potts model. Physical review letters. 1992;69(13):2013

    Not in our library10.1103/physrevlett.69.2013

36. 36.

    Glazier JA, Graner F. Simulation of the differential adhesion driven rearrangement of biological cells. Physical Review E. 1993;47(3):2128

    Not in our library10.1103/physreve.47.2128

37. 37.

    Izaguirre JA, Chaturvedi R, Huang C, Cickovski T, Coffland J, Thomas G, et al CompuCell, a multi-model framework for simulation of morphogenesis. Bioinformatics. 2004;20(7):1129–1137.

    Not in our library10.1093/bioinformatics/bth050

38. 38.

    Swat MH, Thomas GL, Belmonte JM, Shirinifard A, Hmeljak D, Glazier JA. Multi-scale modeling of tissues using CompuCell3D. Methods in cell biology. 2012;110:325

    Not in our library10.1016/b978-0-12-388403-9.00013-8

39. 39.
    Cellular Potts Modeling of Tumor Growth, Tumor Invasion, and Tumor Evolution · 2013

    No notice
40. 40.

    Newman TJ. Modeling Multi-cellular Systems using Sub-cellular Elements. Mathematical Biosciences and Engineering. 2005;2:611–622.

    Not in our library10.3934/mbe.2005.2.613

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.