Skip to main content
Log in

Tissue cell differentiation and multicellular evolution via cytoskeletal stiffening in mechanically stressed microenvironments

  • Research Paper
  • Published:
Acta Mechanica Sinica Aims and scope Submit manuscript

Abstract

Evolution of eukaryotes from simple cells to complex multicellular organisms remains a mystery. Our postulate is that cytoskeletal stiffening is a necessary condition for evolution of complex multicellular organisms from early simple eukaryotes. Recent findings show that embryonic stem (ES) cells are as soft as primitive eukaryotes/amoebae and that differentiated tissue cells can be two orders of magnitude stiffer than ES cells. Soft ES cells become stiff as they differentiate into tissue cells of the complex multicellular organisms to match their microenvironment stiffness. We perhaps see in differentiation of ES cells (derived from inner cell mass cells) the echo of those early evolutionary events. Early soft unicellular organisms might have evolved to stiffen their cytoskeleton to protect their structural integrity from external mechanical stresses while being able to maintain form, to change shape, and to move.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Pace, N.R.: Mapping the tree of life: progress and prospects. Microbiol. Mol. Biol. Rev. 73, 565–576 (2009)

    Article  Google Scholar 

  2. Cavalier-Smith, T.: Cell evolution and Earth history: stasis and revolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 969–1006 (2006)

    Article  Google Scholar 

  3. Cavalier-Smith, T.: Predation and eukaryote cell origins: a coevolutionary perspective. Int. J. Biochem. Cell Biol. 41, 307–322 (2009)

    Article  Google Scholar 

  4. Rasmussen, B., Fletcher, I.R., Brocks, J.J., et al.: Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455, 1101–1104 (2008)

    Article  Google Scholar 

  5. Cox, C.J., Foster, P.G., Hirt, R.P., et al.: The archaebacterial origin of eukaryotes. Proc. Natl. Acad. Sci. USA 105, 20356–20361 (2008)

    Article  Google Scholar 

  6. Davidov, Y., Jurkevitch, E.: Predation between prokaryotes and the origin of eukaryotes. BioEssays 31, 748–757 (2009)

    Article  Google Scholar 

  7. Ruiz-Trillo, I., Burger, G., Holland, P.W.H., et al.: The origins of multicellularity: a multi-taxon genome initiative. Trends Genet. 23, 113–118 (2007)

    Article  Google Scholar 

  8. Abedin, M., King, N.: The premetazoan ancestry of cadherins. Science 319, 946–948 (2008)

    Article  Google Scholar 

  9. Francius, G., Domenech, O., Mingeot-Leclercq, M.P., et al.: Direct observation of Staphylococcus aureus cell wall digestion by lysostaphin. J. Bacteriol. 190, 7904–7909 (2008)

    Article  Google Scholar 

  10. Engelhardt, H.: Mechanism of osmoprotection by archaeal S-layers: a theoretical study. J. Struct. Biol. 160, 190–199 (2007)

    Article  Google Scholar 

  11. Reichl, E.M., Ren, Y.X., Morphew, M.K., et al.: Interactions between myosin and actin crosslinkers control cytokinesis contractility dynamics and mechanics. Curr. Biol. 18, 471–480 (2008)

    Article  Google Scholar 

  12. Waugh, R., Evans, E.A.: Thermoelasticity of red blood-cell membrane. Biophys. J. 26, 115–131 (1979)

    Article  Google Scholar 

  13. Chowdhury, F., Na, S., Li, D., et al.: Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells. Nat. Mater. 9, 82–88 (2010)

    Article  Google Scholar 

  14. Discher, D.E., Janmey, P., Wang, Y.L.: Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139–1143 (2005)

    Article  Google Scholar 

  15. Engler, A.J., Sen, S., Sweeney, H.L., et al.: Matrix elasticity directs stem cell lineage specification. Cell 126, 677–689 (2006)

    Article  Google Scholar 

  16. Janmey, P.A., McCulloch, C.A.: Cell mechanics: integrating cell responses to mechanical stimuli. Annu. Rev. Biomed. Eng. 9, 1–34 (2007)

    Article  Google Scholar 

  17. Engler, A.J., Griffin, M.A., Sen, S., et al.: Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J. Cell Biol. 166, 877–887 (2004)

    Article  Google Scholar 

  18. Meshel, A.S., Wei, Q., Adelstein, R.S., et al.: Basic mechanism of three-dimensional collagen fibre transport by fibroblasts. Nat. Cell Biol. 7, 157–164 (2005)

    Article  Google Scholar 

  19. Darling, E.M., Topel, M., Zauscher, S., et al.: Viscoelastic properties of human mesenchymally-derived stem cells and primary osteoblasts, chondrocytes, and adipocytes. J. Biomech. 41, 454–464 (2008)

    Article  Google Scholar 

  20. Wang, N., Butler, J.P., Ingber, D.E.: Mechanotransduction across the cell-surface and through the cytoskeleton. Science 260, 1124–1127 (1993)

    Article  Google Scholar 

  21. Roca-Cusachs, P., Gauthier, N.C., del Rio, A., et al.: Clustering of alpha(5)beta(1) integrins determines adhesion strength whereas alpha(v)beta(3) and talin enable mechanotransduction. Proc. Natl. Acad. Sci. USA 106, 16245–16250 (2009)

    Article  Google Scholar 

  22. le Duc, Q., Shi, Q., Blonk, I., et al.: Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J. Cell Biol. 189, 1107–1115 (2010)

    Article  Google Scholar 

  23. Na, S., Chowdhury, F., Tay, B., et al.: Plectin contributes to mechanical properties of living cells. Am. J. Physiol. Cell Physiol. 96, C868–C877 (2009)

    Article  Google Scholar 

  24. Kasza, K.E., Nakamura, F., Hu, S., et al.: Filamin A is essential for active cell stiffening but not passive stiffening under external force. Biophys. J. 96, 4326–4335 (2009)

    Article  Google Scholar 

  25. Thompson, R.F., Langford, G.M.: Myosin superfamily evolutionary history. Anat. Rec. 268, 276–289 (2002)

    Article  Google Scholar 

  26. Wang, N., Naruse, K., Stamenovic, D., et al.: Mechanical behavior in living cells consistent with the tensegrity model. Proc. Natl. Acad. Sci. USA 98, 7765–7770 (2001)

    Article  Google Scholar 

  27. Wang, N., Tolic-Norrelykke, I.M., Chen, J.X., et al.: Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. Am. J. Physiol. Cell Physiol. 282, C606–C616 (2002)

    Article  Google Scholar 

  28. Gardel, M.L., Nakamura, F., Hartwig, J.H., et al.: Prestressed F-actin networks cross-linked by hinged filamins replicate mechanical properties of cells. Proc. Natl. Acad. Sci. USA 103, 1762–1767 (2006)

    Article  Google Scholar 

  29. Pajerowski, J.D., Dahl, K.N., Zhong, F.L., et al.: Physical plasticity of the nucleus in stem cell differentiation. Proc. Natl. Acad. Sci. USA 104, 15619–15624 (2007)

    Article  Google Scholar 

  30. Smith, L., Cho, S., Discher, D.E.: Mechanosensing of matrix by stem cells: from matrix heterogeneity, contractility, and the nucleus in pore-migration to cardiogenesis and muscle stem cells in vivo. Semin. Cell Dev. Biol. 71, 84–98 (2017)

    Article  Google Scholar 

  31. Kirby, T.J., Lammerding, J.: Emerging views of the nucleus as a cellular mechanosensor. Nat. Cell Biol. 20, 373–381 (2018)

    Article  Google Scholar 

  32. Swift, J., Ivanovska, I.L., Buxboim, A., et al.: Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 341, 2140104 (2013)

    Article  Google Scholar 

  33. Ho, C.Y., Jaalouk, D.E., Vartiainen, M.K., et al.: Lamin A/C and emerin regulate MKL1-SRF activity by modulating actin dynamics. Nature 497, 507–511 (2013)

    Article  Google Scholar 

  34. Wang, N., Tytell, J.D., Ingber, D.E.: Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10, 75–82 (2009)

    Article  Google Scholar 

  35. Tajik, A., Zhang, Y.J., Wei, F.X., et al.: Transcription upregulation via force-induced direct stretching of chromatin. Nat. Mater. 15, 1287–1296 (2016)

    Article  Google Scholar 

  36. Maniotis, A.J., Chen, C.S., Ingber, D.E.: Demonstration of mechanical connections between integrins cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc. Natl. Acad. Sci. USA 94, 849–854 (1997)

    Article  Google Scholar 

  37. Majkut, S., Idema, T., Swift, J., et al.: Heart-specific stiffening in early embryos parallels matrix and myosin expression to optimize beating. Curr. Biol. 2, 2434–2439 (2013)

    Article  Google Scholar 

  38. Poh, Y.C., Chen, J.W., Hong, Y., et al.: Generation of organized germ layers from a single mouse embryonic stem cell. Nat. Commun. 5, 4000 (2014)

    Article  Google Scholar 

  39. Miller, J.P., Borde, B.H., Bordeleau, F., et al.: Clinical doses of radiation reduce collagen matrix stiffness. APL Bioeng. 2, 031901 (2018)

    Article  Google Scholar 

  40. Guo, M., Pegoraro, A.F., Mao, A., et al.: Cell volume change through water efflux impacts cell stiffness and stem cell fate. Proc. Natl. Acad. Sci. USA 114, E8618–E8627 (2017)

    Article  Google Scholar 

  41. Valentine, M.T., Perlman, Z.E., Mitchison, T.J., et al.: Mechanical properties of Xenopus egg cytoplasmic extracts. Biophys J. 88, 680–689 (2005)

    Article  Google Scholar 

  42. Ingber, D.E.: Mechanical control of tissue growth: function follows form. Proc. Natl. Acad. Sci. USA 102, 11571–11572 (2005)

    Article  Google Scholar 

  43. Krishnan, R., Park, C.Y., Lin, Y.C., et al.: Reinforcement versus fluidization in cytoskeletal mechanoresponsiveness. PLoS ONE 4, e5486 (2009)

    Article  Google Scholar 

  44. Li, S., Niu, G., Dong, N.X., et al.: Osteoporosis affects both post-yield microdamage accumulation and plasticity degradation in vertebra of ovariectomized rats. Acta. Mech. Sin. 33, 267–273 (2017)

    Article  Google Scholar 

  45. Tan, Y., Tajik, A., Chen, J., et al.: Matrix softness regulates plasticity of tumour-repopulating cells via H3K9 demethylation and Sox2 expression. Nat. Commun. 5, 4619 (2014)

    Article  Google Scholar 

  46. Chen, J., Zhou, W., Jia, Q., et al.: Efficient extravasation of tumor-repopulating cells depends on cell deformability. Sci. Rep. 6, 19304 (2016)

    Article  Google Scholar 

  47. Engler, A.J., Carag-Krieger, C., Johnson, C.P., et al.: Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. J. Cell Sci. 121, 3794–3802 (2008)

    Article  Google Scholar 

  48. Kolahi, K.S., Donjacour, A., Liu, X., et al.: Effect of substrate stiffness on early mouse embryo development. PLoS ONE 7, e41717 (2012)

    Article  Google Scholar 

  49. Sehgel, N.L., Vatner, S.F., Meininger, G.A.: “Smooth muscle cell stiffness syndrome”—revisiting the structural basis of arterial stiffness. Front. Physiol. 6, 335 (2015)

    Article  Google Scholar 

  50. Cheng, T., Yue, M., Aslam, M.N., et al.: Neuronal Protein 3.1 deficiency leads to reduced cutaneous scar collagen deposition and tensile strength due to impaired transforming growth factor-β1 to -β3 translation. Am. J. Pathol. 187, 292–303 (2016)

    Article  Google Scholar 

  51. Solon, J., Levental, I., Sengupta, K., et al.: Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys. J. 93, 4453 (2007)

    Article  Google Scholar 

  52. Marquez, J.P., Genin, G.M., Zahalak, G.I., et al.: The relationship between cell and tissue strain in three-dimensional bio-artificial tissues. Biophys. J. 88, 778–789 (2005)

    Article  Google Scholar 

  53. Marquez, J.P., Elson, E.L., Genin, G.M.: Whole cell mechanics of contractile fibroblasts: relations between effective cellular and extracellular matrix moduli. Philos. Trans. A. Math. Phys. Eng. Sci. 368, 635–654 (2010)

    Article  Google Scholar 

  54. Woese, C.R., Kandler, O., Wheelis, M.L.: Towards a natural system of organisms: proposal for the domains archaea, bacteria, and eucarya. Proc. Natl. Acad. Sci. USA 87, 4576–4579 (1990)

    Article  Google Scholar 

  55. Woese, C.R.: The universal ancestor. Proc. Natl. Acad. Sci. USA 95, 6854 (1998)

    Article  Google Scholar 

  56. Eme, L., Spang, A., Lombard, J., et al.: Archaea and the origin of eukaryotes. Nat. Rev. Microbiol. 15, 711–723 (2017)

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Institutes of Health of US (Grant GM072744) and funds from Huazhong University of Science and Technology. Ning Wang acknowledges the support from the Hoeft Endowed Professorship in Engineering at University of Illinois at Urbana-Champaign. The authors thank former and current lab members for their experimental findings that have contributed to the formation of the current postulate.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ning Wang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, J., Wang, N. Tissue cell differentiation and multicellular evolution via cytoskeletal stiffening in mechanically stressed microenvironments. Acta Mech. Sin. 35, 270–274 (2019). https://doi.org/10.1007/s10409-018-0814-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10409-018-0814-8

Keywords

Navigation