Opposing views on tensegrity as a structural framework for understanding cell mechanics

Abstract

Important new theories in science often ignite heated debates. If they do not, they are probably of little significance. Thus a strong argument in support of the importance of the tensegrity model of cell and tissue architecture first proposed almost 20 years ago (23, 24) is the large number of public and private criticisms that have been mounted against this theory. Demonstration of the ability of the tensegrity model to explain complex mechanical behaviors in viruses, nuclei, cells, tissues, and organs in animals as well as in insects and plants (reviewed in Refs. 4, 5, 7, 10, 17, 20-24, 26, 30, 32, 42) has led to a drastic reduction in the number of these confrontations. Nevertheless, some intransigent critics remain. However, their remaining objections are limited in scope and largely result, I believe, from an overly concrete definition of what tensegrity is and how it can be applied. My purpose here, at the request of the Editor and Associate Editors of this journal, is to present the argument in support of the tensegrity model and to respond to some of these remaining concerns. The tensegrity model states that cells, tissues, and other biological structures at smaller and larger size scales in the hierarchy of life gain their shape stability and their ability to exhibit integrated mechanical behavior through use of the structural principles of tensegrity architecture (5, 20, 22-24). The term, "tensegrity" (contraction of "tensional integrity") was first created by the architect R. Buckminster Fuller, who first explored use of this form of structural stabilization as early as 1927 in his plan for the Wichita Dymaxion house, which minimized weight by separating compression members from tension members (31). To create this cylindrical building, Fuller proposed to set a central mast in the earth as a vertical compression strut and to suspend from it multiple circular floors (horizontal wheels) using tension cables. Tensile guy wires that linked the mast to surrounding anchors in the ground provided the balancing tension necessary to stabilize the entire structure. "Fuller called this special discontinuous-compression, continuous-tension

Mechanical behavior in living cells consistent with the tensegrity model

“…Furthermore, the cellular tensegrity theory also can incorporate increasing levels of complexity, including multimodularity and the existence of structural hierarchies (7,11,39), which have not yet been incorporated into the theoretical model. These features of tensegrity may help to explain how molecular structures in specialized regions of the cell (filopodia, microvilli), organelles (mitotic spindle, transport vesicles), viruses, and enzyme complexes are independently stabilized on progressively smaller size scales while, at the same time, displaying integrated mechanical behavior as part of the whole cell.…”

“…A theoretical formulation of the model developed starting from first principles also has shown qualitative and quantitative consistencies with experimental results in various cell types and has led to several a priori predictions (8,9). Nevertheless, tensegrity remains controversial because key pieces of evidence that are essential for its validation are missing (11). These critical experiments include unequivocal demonstration that the CSK behaves as a discrete network composed of different types of CSK filaments; direct evidence that microtubules function as compression struts and contribute significantly to cell mechanics; quantitative measurements demonstrating that CSK prestress is a major determinant of cell deformability; and experimental confirmation of a priori predictions of the theoretical tensegrity model.…”

Anterograde Microtubule Transport Drives Microtubule Bending in LLC-PK1 Epithelial Cells

“…The mechanical stiffness of MTs has been proposed to play an important role in the mechanics of the cell (Wang et al, 1993Ingber et al, 2000;Howard, 2001;Stamenovic et al, 2001;Ingber, 2003;Brangwynne et al, 2006). This hypothesis derives in part from the observation that in interphase animal tissue cells, MTs are commonly observed to form a radial array, which qualitatively resembles the spokes of a bicycle wheel.…”

Cyclic stretch-induced reorganization of the cytoskeleton and its role in enhanced gene transfer

“…2 A whole field of mechanotransduction has emerged, and models such as tensegrity have been developed in an effort to describe how cells behave under various forms of stress, and how these stresses are translated into biochemical cascades and other cellular responses. [3][4][5] This is particularly true in the lung, a dynamic organ that undergoes continuously modulating exogenous forces due to cyclical respiratory patterns. In the injured lung, these forces can be even more prevalent, owing to mechanical ventilation or decreased airway space resulting from edema or compromised lung tissue.…”