Mechanical behavior in living cells consistent with the tensegrity model

Ning Wang, Keiji Naruse, Dimitrije Stamenović, Jeffrey J. Fredberg, Srboljub M. Mijailovich, Iva Marija Tolić-Nørrelykke, Thomas Polte, Robert Mannix, Donald E. Ingber

Research output: Contribution to journalArticle

481 Citations (Scopus)

Abstract

Alternative models of cell mechanics depict the living cell as a simple mechanical continuum, porous filament gel, tensed cortical membrane, or tensegrity network that maintains a stabilizing prestress through incorporation of discrete structural elements that bear compression. Real-time microscopic analysis of cells containing GFP-labeled microtubules and associated mitochondria revealed that living cells behave like discrete structures composed of an interconnected network of actin microfilaments and microtubules when mechanical stresses are applied to cell surface integrin receptors. Quantitation of cell tractional forces and cellular prestress by using traction force microscopy confirmed that microtubules bear compression and are responsible for a significant portion of the cytoskeletal prestress that determines cell shape stability under conditions in which myosin light chain phosphorylation and intracellular calcium remained unchanged. Quantitative measurements of both static and dynamic mechanical behaviors in cells also were consistent with specific a priori predictions of the tensegrity model. These findings suggest that tensegrity represents a unified model of cell mechanics that may help to explain how mechanical behaviors emerge through collective interactions among different cytoskeletal filaments and extracellular adhesions in living cells.

Original languageEnglish
Pages (from-to)7765-7770
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume98
Issue number14
DOIs
Publication statusPublished - 2001
Externally publishedYes

Fingerprint

Microtubules
Mechanics
Myosin Light Chains
Mechanical Stress
Cell Shape
Atomic Force Microscopy
Traction
Cell Surface Receptors
Cytoskeleton
Actin Cytoskeleton
Integrins
Mitochondria
Gels
Phosphorylation
Calcium
Membranes

Keywords

  • Cell mechanics
  • Cytoskeleton
  • Mechanotransduction
  • Microtubules
  • Myosin light chain phosphorylation

ASJC Scopus subject areas

  • Genetics
  • General

Cite this

Wang, N., Naruse, K., Stamenović, D., Fredberg, J. J., Mijailovich, S. M., Tolić-Nørrelykke, I. M., ... Ingber, D. E. (2001). Mechanical behavior in living cells consistent with the tensegrity model. Proceedings of the National Academy of Sciences of the United States of America, 98(14), 7765-7770. https://doi.org/10.1073/pnas.141199598

Mechanical behavior in living cells consistent with the tensegrity model. / Wang, Ning; Naruse, Keiji; Stamenović, Dimitrije; Fredberg, Jeffrey J.; Mijailovich, Srboljub M.; Tolić-Nørrelykke, Iva Marija; Polte, Thomas; Mannix, Robert; Ingber, Donald E.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 98, No. 14, 2001, p. 7765-7770.

Research output: Contribution to journalArticle

Wang, N, Naruse, K, Stamenović, D, Fredberg, JJ, Mijailovich, SM, Tolić-Nørrelykke, IM, Polte, T, Mannix, R & Ingber, DE 2001, 'Mechanical behavior in living cells consistent with the tensegrity model', Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 14, pp. 7765-7770. https://doi.org/10.1073/pnas.141199598
Wang, Ning ; Naruse, Keiji ; Stamenović, Dimitrije ; Fredberg, Jeffrey J. ; Mijailovich, Srboljub M. ; Tolić-Nørrelykke, Iva Marija ; Polte, Thomas ; Mannix, Robert ; Ingber, Donald E. / Mechanical behavior in living cells consistent with the tensegrity model. In: Proceedings of the National Academy of Sciences of the United States of America. 2001 ; Vol. 98, No. 14. pp. 7765-7770.
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