Abstract
In this communication, we propose a model to study the non-equilibrium process by which actin stress fibers develop force in contractile cells. The emphasis here is on the non-equilibrium thermodynamics, which is necessary to address the mechanics as well as the chemistry of dynamic cell contractility. In this setting, we are able to develop a framework that relates (a) the dynamics of force generation within the cell and (b) the cell’s response to external stimuli to the chemical processes occurring within the cell, as well as to the mechanics of linkage between the stress fibers, focal adhesions and extracellular matrix.
Similar content being viewed by others
References
Aratyn-Schaus Y, Gardel ML (2010) Transient frictional slip between integrin and the ecm in focal adhesions under myosin ii tension. Curr Biol 20:1145–1153
Balaban N, Schwarz U, Riveline D, Goichberg P, Tzur G, Sabanay I et al (2001) Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat Cell Biol 3:466–473
Bell G (1978) Models for the specific adhesion of cells to cells. Science 200:618–627
Besser A, Safran S (2006) Force-induced adsorption and anisotropic growth of focal adhesions. Biophys J 90:3469–3484
Besser A, Schwartz U (2007) Coupling biochemistry and mechanics in cell adhesion a model for inhomogeneous stress fiber contraction. New J Phys 9:425–452
Besser A, Colombelli J, Stelzer E, Schwartz U (2011) Viscoelastic response of contractile filament bundles. Phys Rev 83(5):051902
Califano J, Reinhart-King C (2010) Substrate stiffness and cell area predict cellular traction stresses in single cells and cells in contact. Cell Mol Bioeng 3:68–75
Callen H (1985) Thermodynamics and an introduction to thermostatistics. Wiley, New York
Chan C, Odde D (2008) Traction dynamics of filopodia on compliant substrates. Science 322:1687–1691
Chrzanowska-Wodnicka M, Burridge K (1996) Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J Cell Biol 113:1403–1415
Colombelli J, Besser A, Kress H, Reynaud E, Girard P, Caussinus E et al (2009) Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization. J Cell Sci 122:1665–1679
de Groot S, Mazur P (1984) Nonequilibrium thermodynamics. Dover, New York
Debold E, Patlak J, Warshaw D (2005) Slip sliding away: load-dependence of velocity generated by skeletal muscle myosin molecules in the laser trap. Biophy J 89:L34–L36
Deshpande V, McMeeking R, Evans A (2006) A bio-chemo-mechanical model for cell contractility. Proc Natl Acad Sci 103:14015–14020
Deshpande V, Mrkisch M, McMeeking R, Evans A (2008) A bio-chemo–mechanical model for coupling cell contractility with focal adhesion formation. J Mech Phys Solids 56:1484–1510
Engler A, Sen S, Sweeney H, Discher D (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677–689
Franke R, Grafe M, Schnittler H, Seiffge D, Mittermayer C, Drenckhahn D (1984) Induction of human vascular endothelial stress fibers by fluid shear stress. Nature 307:648–649
Gardel ML, Schneider IC, Aratyn-Schaus Y, M WC (2010) Mechanical integration of actin and adhesion dynamics in cell migration. Annu Rev Cell Dev Biol 26:315–333
Geiger B, Bershadsky A, Pankov R, Yamada K (2001) Transmembrane extracellular matrix-cytoskeleton crosstalk. Nat Rev Mol Cell Biol 2:793–805
Ghibaudo M, Saez A, Trichet L, Xayaphoummine A, Browaeys J, Silberzan P, Buguin A, Ladoux B (2008) Traction forces and rigidity sensing regulate cell functions. Soft Matter 4:1836–1843
Harland B, Walcott B, Sun S (2011) Adhesion dynamics and durotaxis in migrating cells. Phys Biol 8:015011-1–015011-10
Hill A (1938) The heat of shortening and the dynamics constants of muscle. Proc R Soc Lond Ser B 126:136–195
Hirata H, Tatsumi H, Sokabe M (2008) Mechanical forces facilitate actin polymerization at focal adhesions in a zyxin-independent manner. J Cell Sci 121:2795–2804
Ingber D (2003) Tensegrity i. cell structure and hierarchical systems biology. J Cell Sci 116:1157–1173
Kaunas R (2008) Modeling cellular adaptation to mechanical stress. In: Artmann G, Chien S (eds) Bioengineering in cell and tissue research. Springer, New York, pp 317–348
Kaunas K, Huang Z, Hahn J (2010) A kinematic model coupling stress fiber dynamics with jnk activation in response to matrix stretching. J Theor Biol 264:593–603
Kaunas R, Nguyen P, Usami S, Chien S (2005) Cooperative effects of rho and mechanical stretch on stress fiber organization. Proc Natl Acad Sci 102:15895–15900
Kong H, Polte T, Alsberg E, Mooney D (2005) Fret measurements of cell-traction forces and nano-scale clustering of adhesion ligands varied by substrate stiffness. Proc Natl Acad Sci 102:4300–4305
Kruse K, Julicher F (2000) Actively contracting bundles of polar filaments. Phys Rev Lett 85:1778–1781
Kumar S, Maxwell I, Heisterkamp A, Polte T, Lele T (2006) Viscoelastic relaxation of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophys J 90:3762–3773
Lo CM, Wang HB, Dembo M, Wang YI (2000) Cell movement is guided by the rigidity of the substrate. Biophys J 79:144–152
Mann J, Lam R, Weng S, Sun Y, Fu J (2012) A siliconebased stretchable micropost array membrane for monitoring livecell subcellular cytoskeletal response. Lab Chip 12:731–740
Maraldi M, Valero C, Garikipati K (2014) A computational study of stress fiber-focal adhesion dynamics governing cell contractility. Biophys J 106:1–12
Olberding J, Thouless M, Arruda E, Garikipati K (2010) The non-equilibrium thermodynamics and kinetics of focal adhesion dynamics. PLoS One 4(e12):043
Pelham R Jr, Wang Y (1997) Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci 94:13661–13665
Pellegrin S, Mellor H (2007) Actin stress fibres. J Cell Sci 120:3491–3499
Peterson L, Rajfur Z, Maddox A, Freel C, Chen Y, Edlund M et al (2004) Simultaneous stretching and contraction of stress fibers in vivo. Mol Biol Cell 15:3497–3508
Pollard T, Borisy G (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453–465
Riveline D, Zamir E, Balaban N, Schwarz U, Ishikazi T, Narumiya S et al (2001) Externally applied local mechanical force induces growth of focal contacts by an mdia1-dependent and rock-independent mechanism. J Cell Biol 153:1175–1185
Schwarz US, Gardel ML (2012) United we stand integrating the actin cytoskeleton and cellmatrix adhesions in cellular mechanotransduction. J Cell Sci 125:1–10
Shemesh T, Geiger B, Bershadsky A, Kozlov M (2005) Focal adhesions as mechanosensors: a physical mechanism. Proc Natl Acad Sci 102(12):383–388
Stachowiak M, O’Shaughnessy B (2008) Kinetics of stress fibers. New J Phys 10:025002-1–025002-26
Stachowiak M, O’Shaughnessy B (2009) Recoil after severing reveals stress fiber contraction mechanisms. Biophys J 97:462–471
Tan J, Tien J, Pirone D, Gray D, Bhadriraju K, Chen C (2003) Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc Natl Acad Sci 100:1484–1489
Walcott S, Sun S (2010) A mechanical model of actin stress fiber formation and substrate elasticity sensing in adherent cells. Proc Natl Acad Sci 107:7757–7762
Wu JQ, Pollard T (2005) Counting cytokinesis proteins globally and locally in fission yeast. Science 310:310–314
Zamir E, Geiger B (2001) Molecular complexity and dynamics of cell-matrix adhesions. J Cell Sc 114:3583–3590
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Maraldi, M., Garikipati, K. The mechanochemistry of cytoskeletal force generation. Biomech Model Mechanobiol 14, 59–72 (2015). https://doi.org/10.1007/s10237-014-0588-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10237-014-0588-2