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Stress Transmission within the Cell

Dimitrije Stamenović, Ning Wang

10.1002/cphy.c100019

Source: Volume 1, Issue 1, January 2011

Published online: January 2011

Full Article on Wiley Online Library



Abstract

An outstanding problem in cell biology is how cells sense mechanical forces and how those forces affect cellular functions. During past decades, it has become evident that the deformable cytoskeleton (CSK), an intracellular network of various filamentous biopolymers, provides a physical basis for transducing mechanical signals into biochemical responses. To understand how mechanical forces regulate cellular functions, it is necessary to first understand how the CSK develops mechanical stresses in response to applied forces, and how those stresses are propagated through the CSK where various signaling molecules are immobilized. New experimental techniques have been developed to quantify cytoskeletal mechanics, which together with new computational approaches have given rise to new theories and models for describing mechanics of living cells. In this article, we discuss current understanding of cell biomechanics by focusing on the biophysical mechanisms that are responsible for the development and transmission of mechanical stresses in the cell and their effect on cellular functions. We compare and contrast various theories and models of cytoskeletal mechanics, emphasizing common mechanisms that those theories are built upon, while not ignoring irreconcilable differences. We highlight most recent advances in the understanding of mechanotransduction in the cytoplasm of living cells and the central role of the cytoskeletal prestress in propagating mechanical forces along the cytoskeletal filaments to activate cytoplasmic enzymes. It is anticipated that advances in cell mechanics will help developing novel therapeutics to treat pulmonary diseases like asthma, pulmonary fibrosis, and chronic obstructive pulmonary disease. © 2011 American Physiological Society. Compr Physiol 1:499‐524, 2011.

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Figure 1. Figure 1.

Stiffness of actin networks cross‐linked with filamin‐A increases with increasing shear prestress. Measurements were carried out using a stress‐controlled parallel plate rheometer in gels with different actin concentration (cA) and different molar ratios of filamin‐A (R): cA = 36 μM, R = 1/100 (open squares); cA = 48 μM, R = 1/100 (solid squares); cA = 74 μM, R = 1/100 (diamonds); cA = 36 μM, R = 1/50 (left‐pointing triangles); cA = 53 μM, R = 1/50 (upward‐pointing triangles). For comparison, data from measurements in living airway smooth muscle cells 202 are included (solid circles near the top right corner). Modified from reference 66 with permission from Gardel et al.
Figure 2. Figure 2.

(A) Traction filed distribution measured by traction force micrscopy 19 in a living human airway smooth muscle cell treated with 10 μM histamine; white arrows indicate directions of local tractions and the color code indicates the magnitude of traction in Pa. Reproduced from reference 189 with permission from Tolić‐Nørrelykke. (B) The traction filed from (A) can be replaced by a pair of forces (dipole) of magnitude F and at distance d. The strength of the dipole or the net contractile moment is given as the product F·d.
Figure 3. Figure 3.

Stiffness of airway smooth muscle cells increases proportionally with various metrics of cell contractile stress. The relationship between the stiffness and the net contractile moment is shown. Top inset: relationship between the stiffness and the cytoskeletal prestress. Because the traction must balance the contractile prestress, the prestress is computed from a force balance at a section of the cell perpendicular to its long axis, where the prestress is given as the net force normalized by the cell cross‐sectional area. Bottom inset: relationship between stiffness and the maximum contractile force of the CSK. The stiffness is measured by the magnetic twisting cytometry technique 132. Reproduced from reference 202 with permission from Wang.
Figure 4. Figure 4.

A simple tensegrity structure comprising three compression‐supporting struts (thick gray bars) interconnected with nine pre‐tensed cables (thin black lines). At each node, compression of a single bar balances tension of three cables.
Figure 5. Figure 5.

Microtubules visualized over time in a beating cardiac muscle cell expressing green fluorescent protein‐tubulin. Whenever the cell contracts, the microtubule (highlighted in red) buckles indicating that it resists contraction of the cytoskeletal actin network. Scale bar = 3 μm. Reproduced from reference 12 with permission form Brangwynne et al.
Figure 6. Figure 6.

(A) Magnitude of the dynamic modulus of cultured airway smooth muscle cells increases with increasing frequency of loading according to a weak power law. Measurements were carried out using the oscillatory magnetic twisting cytometry technique 55 under control conditions and following treatments with a bronchoconstriction histamine (His) and bronchodilator isoproterenol (Iso). Data are means, SE do not exceed 5% and are not shown; solid lines are best fits. (B) The power‐law exponent decreases with increasing contractile prestress. Data are means ± SE obtained from the slopes of the power‐law relationships in (A); data for the prestress are means ± SE obtained from measurements in Figure 3 (top inset). Modified from reference 179 with permission from Stamenović et al.
Figure 7. Figure 7.

Phase contrast (left) and corresponding birefringence microscopic images (right) of the CSK before (top) and after (bottom) forces are applied to integrins. The data show immediate molecular realignment in the cytoskeleton following force application. The appearance of nucleoli in distorted cells indicates molecular realignment in these regions. Reproduced from reference 134 with permission from Maniotis et al.
Figure 8. Figure 8.

Actin cytoskeleton displacement patterns measured by intracellular stress tomography 91 are modulated by prestress. An external displacement is applied to the human airway smooth muscle cell locally via a magnetic bead (position indicated by the pink dot) attached to an integrin receptor on the cell's apical surface, and islands of intracellular displacements are observed distal from the point of force application. Control yellow fluorescent protein‐actin cell (A). Cell infected with a low level of green fluorescent protein‐caldesmon before (B) and after (C) treatment with calcium ionophore A‐23187 (52 g/ml for 10 min), an inhibitor of caldesmon. The pink arrow represents the direction and the magnitude of the bead lateral displacement. Insets in A, B, and C are fluorescent images of the corresponding cells, showing patterns of stress fibers. Green ellipses represent the nuclei of the cells. Reproduced from reference 91 with permission from Hu et al.
Figure 9. Figure 9.

Rapid, long‐range strong Src activation sites in the cytoplasm colocalize with sites of large microtubule displacements. The cell was cotransfected with CFP‐YFP Src reporter and mCherry‐tubulin. A step function stress σ (17.5 Pa) was first applied for 3 s via an RGD‐coated bead, and FRET changes were recorded. Then the microtubule deformation map was acquired when an oscillatory stress was applied for ∼30 s (0.3 Hz; peak stress = 24.5 Pa, equivalent to a constant stress of 17.5 Pa; reference 91). In this representative cell, strong Src activation sites coincide with large deformation sites (>15 nm) of microtubules in the same cell at the same focal plane (∼1 μm above cell base). The overlay image is the YFP Src reporter image superimposed with the bead. Pink circles indicate bead center position; white arrows represent microtubule deformation direction. Red arrows point to strong Src activation sites. In the colocalization analysis panel, red represents strong Src activation, and black lines represent large microtubule displacements. Three other different cells showed similar results. Of strong Src activation sites, ∼80% (15 of 19) were colocalized with sites of microtubule deformation >15 nm. Scale bar = 10 μm. Reproduced from reference 143 with permission from Na et al.
Figure 10. Figure 10.

Schematic representation of the complementary force balance at the focal adhesion (FA) level. Tension (FSF) in the actin stress fiber (SF) is balanced by traction force (τ) at the FA attachment to the substrate and compression force (FMT) of the cytoskeletal microtubule (MT).


Figure 1.

Stiffness of actin networks cross‐linked with filamin‐A increases with increasing shear prestress. Measurements were carried out using a stress‐controlled parallel plate rheometer in gels with different actin concentration (cA) and different molar ratios of filamin‐A (R): cA = 36 μM, R = 1/100 (open squares); cA = 48 μM, R = 1/100 (solid squares); cA = 74 μM, R = 1/100 (diamonds); cA = 36 μM, R = 1/50 (left‐pointing triangles); cA = 53 μM, R = 1/50 (upward‐pointing triangles). For comparison, data from measurements in living airway smooth muscle cells 202 are included (solid circles near the top right corner). Modified from reference 66 with permission from Gardel et al.



Figure 2.

(A) Traction filed distribution measured by traction force micrscopy 19 in a living human airway smooth muscle cell treated with 10 μM histamine; white arrows indicate directions of local tractions and the color code indicates the magnitude of traction in Pa. Reproduced from reference 189 with permission from Tolić‐Nørrelykke. (B) The traction filed from (A) can be replaced by a pair of forces (dipole) of magnitude F and at distance d. The strength of the dipole or the net contractile moment is given as the product F·d.



Figure 3.

Stiffness of airway smooth muscle cells increases proportionally with various metrics of cell contractile stress. The relationship between the stiffness and the net contractile moment is shown. Top inset: relationship between the stiffness and the cytoskeletal prestress. Because the traction must balance the contractile prestress, the prestress is computed from a force balance at a section of the cell perpendicular to its long axis, where the prestress is given as the net force normalized by the cell cross‐sectional area. Bottom inset: relationship between stiffness and the maximum contractile force of the CSK. The stiffness is measured by the magnetic twisting cytometry technique 132. Reproduced from reference 202 with permission from Wang.



Figure 4.

A simple tensegrity structure comprising three compression‐supporting struts (thick gray bars) interconnected with nine pre‐tensed cables (thin black lines). At each node, compression of a single bar balances tension of three cables.



Figure 5.

Microtubules visualized over time in a beating cardiac muscle cell expressing green fluorescent protein‐tubulin. Whenever the cell contracts, the microtubule (highlighted in red) buckles indicating that it resists contraction of the cytoskeletal actin network. Scale bar = 3 μm. Reproduced from reference 12 with permission form Brangwynne et al.



Figure 6.

(A) Magnitude of the dynamic modulus of cultured airway smooth muscle cells increases with increasing frequency of loading according to a weak power law. Measurements were carried out using the oscillatory magnetic twisting cytometry technique 55 under control conditions and following treatments with a bronchoconstriction histamine (His) and bronchodilator isoproterenol (Iso). Data are means, SE do not exceed 5% and are not shown; solid lines are best fits. (B) The power‐law exponent decreases with increasing contractile prestress. Data are means ± SE obtained from the slopes of the power‐law relationships in (A); data for the prestress are means ± SE obtained from measurements in Figure 3 (top inset). Modified from reference 179 with permission from Stamenović et al.



Figure 7.

Phase contrast (left) and corresponding birefringence microscopic images (right) of the CSK before (top) and after (bottom) forces are applied to integrins. The data show immediate molecular realignment in the cytoskeleton following force application. The appearance of nucleoli in distorted cells indicates molecular realignment in these regions. Reproduced from reference 134 with permission from Maniotis et al.



Figure 8.

Actin cytoskeleton displacement patterns measured by intracellular stress tomography 91 are modulated by prestress. An external displacement is applied to the human airway smooth muscle cell locally via a magnetic bead (position indicated by the pink dot) attached to an integrin receptor on the cell's apical surface, and islands of intracellular displacements are observed distal from the point of force application. Control yellow fluorescent protein‐actin cell (A). Cell infected with a low level of green fluorescent protein‐caldesmon before (B) and after (C) treatment with calcium ionophore A‐23187 (52 g/ml for 10 min), an inhibitor of caldesmon. The pink arrow represents the direction and the magnitude of the bead lateral displacement. Insets in A, B, and C are fluorescent images of the corresponding cells, showing patterns of stress fibers. Green ellipses represent the nuclei of the cells. Reproduced from reference 91 with permission from Hu et al.



Figure 9.

Rapid, long‐range strong Src activation sites in the cytoplasm colocalize with sites of large microtubule displacements. The cell was cotransfected with CFP‐YFP Src reporter and mCherry‐tubulin. A step function stress σ (17.5 Pa) was first applied for 3 s via an RGD‐coated bead, and FRET changes were recorded. Then the microtubule deformation map was acquired when an oscillatory stress was applied for ∼30 s (0.3 Hz; peak stress = 24.5 Pa, equivalent to a constant stress of 17.5 Pa; reference 91). In this representative cell, strong Src activation sites coincide with large deformation sites (>15 nm) of microtubules in the same cell at the same focal plane (∼1 μm above cell base). The overlay image is the YFP Src reporter image superimposed with the bead. Pink circles indicate bead center position; white arrows represent microtubule deformation direction. Red arrows point to strong Src activation sites. In the colocalization analysis panel, red represents strong Src activation, and black lines represent large microtubule displacements. Three other different cells showed similar results. Of strong Src activation sites, ∼80% (15 of 19) were colocalized with sites of microtubule deformation >15 nm. Scale bar = 10 μm. Reproduced from reference 143 with permission from Na et al.



Figure 10.

Schematic representation of the complementary force balance at the focal adhesion (FA) level. Tension (FSF) in the actin stress fiber (SF) is balanced by traction force (τ) at the FA attachment to the substrate and compression force (FMT) of the cytoskeletal microtubule (MT).

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Article Title: Stress Transmission within the Cell
 

How to Cite

Dimitrije Stamenović, Ning Wang. Stress Transmission within the Cell. Compr Physiol 2011, 1: 499-524. doi: 10.1002/cphy.c100019