Skip to content
naulon

No retraction, correction or concern found when last checked on Oct 23, 2026.

Mechanical Stress Inference for Two Dimensional Cell Arrays

Kevin K. Chiou, Lars Hufnagel, Boris I. Shraiman

PLoS Computational Biology · 2012

doi:10.1371/journal.pcbi.1002512

Abstract

Many morphogenetic processes involve mechanical rearrangements of epithelial tissues that are driven by precisely regulated cytoskeletal forces and cell adhesion. The mechanical state of the cell and intercellular adhesion are not only the targets of regulation, but are themselves the likely signals that coordinate developmental process. Yet, because it is difficult to directly measure mechanical stress in vivo on sub-cellular scale, little is understood about the role of mechanics in development. Here we present an alternative approach which takes advantage of the recent progress in live imaging of morphogenetic processes and uses computational analysis of high resolution images of epithelial tissues to infer relative magnitude of forces acting within and between cells. We model intracellular stress in terms of bulk pressure and interfacial tension, allowing these parameters to vary from cell to cell and from interface to interface. Assuming that epithelial cell layers are close to mechanical equilibrium, we use the observed geometry of the two dimensional cell array to infer interfacial tensions and intracellular pressures. Here we present the mathematical formulation of the proposed Mechanical Inverse method and apply it to the analysis of epithelial cell layers observed at the onset of ventral furrow formation in the Drosophila embryo and in the process of hair-cell determination in the avian cochlea. The analysis reveals mechanical anisotropy in the former process and mechanical heterogeneity, correlated with cell differentiation, in the latter process. The proposed method opens a way for quantitative and detailed experimental tests of models of cell and tissue mechanics.

Full text

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

Read at PubMed Central

References 40

  1. 1.

    Lecuit T, Lenne PF. Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat Rev Mol Cell Biol. 2007;8:633-644.

    Not in our library10.1038/nrm2222

  2. 2.

    Huang S, Ingber DE. The structural and mechanical complexity of cell-growth control. Nat Cell Biol. 1999;1:E131-8.

    Not in our library10.1038/13043

  3. 3.

    Foty RA, Steinberg MS. The differential adhesion hypothesis: a direct evaluation. Dev Biol. 2005;278:255-263.

    Not in our library10.1016/j.ydbio.2004.11.012

  4. 4.

    Evans E, Yeung A. Apparent viscosity and cortical tension of blood granulocytes determined by micropipet aspiration. Biophys J. 1989;56:151-160.

    Not in our library10.1016/s0006-3495(89)82660-8

  5. 5.

    Kiehart DP, Galbraith CG, Edwards KA, Rickoll WL, Montague RA. Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J Cell Biol. 2000;149:471-490.

    Not in our library10.1083/jcb.149.2.471

  6. 6.

    Käfer J, Hayashi T, Marée AFM, Carthew RW, Graner F. Cell adhesion and cortex contractility determine cell patterning in the Drosophila retina. Proc Natl Acad Sci U S A. 2007;104:18549-18554.

    Not in our library10.1073/pnas.0704235104

  7. 7.

    Martin AC, Kaschube M, Wieschaus EF. Pulsed contractions of an actin-myosin network drive apical constriction. Nature. 2009;457:495-499.

    Not in our library10.1038/nature07522

  8. 8.

    Farhadifar R, Röper JC, Aigouy B, Eaton S, Jülicher F. The inuence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr Biol. 2007;17:2095-2104.

    Not in our library10.1016/j.cub.2007.11.049

  9. 9.

    Shraiman BI. Mechanical feedback as a possible regulator of tissue growth. Proc Natl Acad Sci U S A. 2005;102:3318-3323.

    Not in our library10.1073/pnas.0404782102

  10. 10.

    Hayashi T, Carthew RW. Surface mechanics mediate pattern formation in the developing retina. Nature. 2004;431:647-652.

    Not in our library10.1038/nature02952

  11. 11.

    Bertet C, Sulak L, Lecuit T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature. 2004;429:667-671.

    Not in our library10.1038/nature02590

  12. 12.

    Bao S, Cagan R. Preferential adhesion mediated by Hibris and Roughest regulates morphogenesis and patterning in the Drosophila eye. Dev Cell. 2005;8:925-935.

    Not in our library10.1016/j.devcel.2005.03.011

  13. 13.

    Köppen M, Fernández BG, Carvalho L, Jacinto A, Heisenberg CP. Coordinated cell-shape changes control epithelial movement in zebrafish and Drosophila. Development. 2006;133:2671-81.

    Not in our library10.1242/dev.02439

  14. 14.

    Mirabet V, Das P, Boudaoud A, Hamant O. The role of mechanical forces in plant morphogenesis. Annu Rev Plant Biol. 2011;62:365-385.

    Not in our library10.1146/annurev-arplant-042110-103852

  15. 15.

    Hamant O, Heisler MG, Jönsson H, Krupinski P, Uyttewaal M, et al. Developmental patterning by mechanical signals in Arabidopsis. Science. 2008;322:1650-5.

    Not in our library10.1126/science.1165594

  16. 16.

    Folkman J, Moscona A. Role of cell shape in growth control. Nature. 1978;273:345-349.

    Not in our library10.1038/273345a0

  17. 17.

    Huang S, Ingber DE. Shape-dependent control of cell growth, differentiation, and apoptosis: switching between attractors in cell regulatory networks. Exp Cell Res. 2000;261:91-103.

    Not in our library10.1006/excr.2000.5044

  18. 18.

    Wozniak MA, Chen CS. Mechanotransduction in development: a growing role for contractility. Nat Rev Mol Cell Biol. 2009;10:34-43.

    Not in our library10.1038/nrm2592

  19. 19.

    Puliafito A, Hufnagel L, Neveu P, Streichan S, Sigal A, et al. Collective and single cell behavior in epithelial contact inhibition. Proc Natl Acad Sci U S A. 2012;109:739-44.

    Not in our library10.1073/pnas.1007809109

  20. 20.

    Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell. 2006;126:677-689.

    Not in our library10.1016/j.cell.2006.06.044

  21. 21.

    Hufnagel L, Teleman AA, Rouault H, Cohen SM, Shraiman BI. On the mechanism of wing size determination in y development. Proc Natl Acad Sci U S A. 2007;104:3835-3840.

    Not in our library10.1073/pnas.0607134104

  22. 22.

    Affolter M, Basler K. The Decapentaplegic morphogen gradient: from pattern formation to growth regulation. Nat Rev Genet. 2007;8:663-674.

    Not in our library10.1038/nrg2166

  23. 23.

    Choquet D, Felsenfeld DP, Sheetz MP. Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell. 1997;88:39-48.

    Not in our library10.1016/s0092-8674(00)81856-5

  24. 24.

    Dembo M, Wang YL. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys J. 1999;76:2307-2316.

    Not in our library10.1016/s0006-3495(99)77386-8

  25. 25.

    Hutson SM, Yoichiro T, Chang MS, Bloor JW, Venakides S, et al. Forces for morphogenesis investigated with laser microsurgery and quantitative modelling. Science. 2003;300:145-149.

    Not in our library10.1126/science.1079552

  26. 26.

    Rauzi M, Verant P, Lecuit T, Lenne PF. Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis. Nat Cell Biol. 2008;10:1401-1410.

    Not in our library10.1038/ncb1798

  27. 27.

    Martin AC, Gelbart M, Fernandez-Gonzalez R, Kaschube M, Wieschaus EF. Integration of contractile forces during tissue invagination. J Cell Biol. 2010;188:735-749.

    Not in our library10.1083/jcb.200910099

  28. 28.

    Brodland GW, Conte V, Cranston PG, Veldhuis J, Narasimhan S, et al. Video force microscopy reveals the mechanics of ventral furrow invagination in Drosophila. Proc Natl Acad Sci U S A. 2010;107:22111-22116.

    Not in our library10.1073/pnas.1006591107

  29. 29.

    Goodyear R, Richardson G. Pattern formation in the basilar papilla: evidence for cell rearrangement. J Neurosci. 1997;17:6289-6301.

    Not in our library10.1523/jneurosci.17-16-06289.1997

  30. 30.

    Blankenship JT, Backovic ST, Sanny JSP, Weitz O, Zallen JA. Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev Cell. 2006;11:459-470.

    Not in our library10.1016/j.devcel.2006.09.007

  31. 31.

    Campbell SL, Meyer CD. Generalized Inverses of Linear Transformations. 1979.

    Not in our library

  32. 32.

    Wyart M. On the Rigidity of Amorphous Solids. Ann Phys-Paris. 2005;30:1-96.

    Not in our library

  33. 33.

    Bray SJ. Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol. 2006;7:678-89.

    Not in our library10.1038/nrm2009

  34. 34.

    Wolpert L. Principles of Development. 2002.

    Not in our library

  35. 35.

    Gilbert S. Developmental Biology. 2003.

    Not in our library

  36. 36.

    Graner F, Glazier JA. Simulation of Biological Cell Sorting Using a Two-Dimensional Extended Potts Model. Phys Rev Lett. 1992;69:2013-2016.

    Not in our library10.1103/physrevlett.69.2013

  37. 37.

    Stavans J. The evolution of cellular structures. Rep Prog Phys. 1993;56:733.

    Not in our library

  38. 38.

    Weaire D, Rivier N. Soap, cells and statistics - random patterns in two dimensions. Contemp Phys. 1984;25:59-99.

    Not in our library

  39. 39.

    He L, Wang X, Tang HL, Montell DJ. Tissue elongation requires oscillating contractions of a basal actomyosin network. Nat Cell Biol. 2010;12:1133-1142.

    Not in our library10.1038/ncb2124

  40. 40.

    Meng F, Sachs F. Visualizing dynamic cytoplasmic forces with a compliance-matched FRET sensor. J Cell Sci. 2011;124:261-269.

    Not in our library10.1242/jcs.071928

Cited by papers we hold 6

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

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.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.