Mechanical behavior in living cells consistent with the tensegrity model

By Ning Wang, Keiji Naruse, D. Stamenović, Jeffrey J. Fredberg, S. Mijailovich, I. Tolic-Nørrelykke, Tom Polte, R. Mannix, Donald E. Ingber. Proceedings of the National Academy of Sciences of the United States of America, 2001

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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.

Subfields: Cell Biology, Ecology, Evolution, Behavior and Systematics, Physiology

View Paper: https://www.semanticscholar.org/paper/f9cb2812f95767ea2254bac8ee019c91dcc6738d

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Citations in the corpus

Design and control of compliant tensegrity robots through simulation and hardware validation (2014, background): “The tensegrity concept appears at various scales, from the cytoskeleton of individual cells (see Figure 1) [2, 3, 4] to mammalian physiology [5].”
Tensegrity frameworks: Dynamic analysis review and open problems (2009, neutral): “[100] or Sultan et al.”
Harnessing nanotopography and integrin-matrix interactions to influence stem cell fate. (2014, background): “correlates with actin cytoskeletal organization and force generation [104].”
Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus (2009, background): “The hard-wired cell Experimental studies that are designed to test predictions of the cellular tensegrity model have confirmed that when surface integrins are directly stressed by applying large forces with ligand-coated micropipettes or magnetic particles, or by physically deforming cells that a”
Solitary waves on tensegrity lattices (2012, background): “…recognized in recent years that they well describe the mechanics of a number of biological structures, such as cell cytoskeletons (Ingber, 1998; Wang et al., 2001; Canadas et al., 2002; Mofrad and Kamm, 2006), the red blood cell membrane (Vera et al., 2005), spider fibers (Termonia, 1994), the…”
Tensegrity I. Cell structure and hierarchical systems biology (2003, methodology): “Altering cytoskeletal prestress by modulating actomyosin-based contractility using drugs (Hubmayr et al., 1996; Wang et al., 2001), varying transmembrane osmotic forces (Cai et al.”
Tensegrity II. How structural networks influence cellular information processing networks (2003, background): “Cytoskeletal restructuring in response to external stress through integrins also normally requires maintenance of cytoskeletal tension generation (i.e. cellular prestress) (Chicurel et al., 1998b; Wang et al., 2001a; Balaban et al., 2001).”
Myotubes differentiate optimally on substrates with tissue-like stiffness (2004, background): “The mechanism of coalignment is understood, from theory (Bischofs and Schwartz, 2003), to involve a propagation of cell-induced substrate contractions (Pelham and Wang, 1997; Wang et al., 2001; Tan et al., 2003).”
Review Article: Rheological Properties of Living Materials. From Cells to Tissues (2003, positive): “Finally, a more refined analysis (Wang et al., 2001), including microscopic observations revealed recently that cells behave like discrete structures composed of an interconnected network of actin filaments and microtubules.”
Mechanical control of tissue and organ development (2010, background): “…cytoskeleton are also resisted by these adhesive tethers to neighboring cells and the ECM, and by internal cytoskeletal structures that resist being compressed, such as microtubules or cross-linked actin filaments within filopodia (Wang et al., 2001; Brangwynne et al., 2006; Ingber, 2006).”
Rapid prototyping in tissue engineering: challenges and potential. (2004, background): “Mechanical strength of scaffolds: Cells are able to detect with high sensitivity the mechanical properties of the adhesion substrate, and to regulate integrin binding and the assembly of focal adhesion plaques and the cytoskeleton accordingly [ 57 ].”
Optimization of tensegrity structures (2006, background): “This may explain why these configurations occur in some biological structures, and the success of class-one tensegrities in modeling cytoskeleton (see, e.g., Coughlin and Stamenovic´, 1997; Wang et al., 2001).”