Reinforcement versus fluidization in cytoskeletal mechanoresponsiveness

• Published in: PloS one Vol. 4; no. 5; p. e5486
• Main Authors: Krishnan, Ramaswamy, Park, Chan Young, Lin, Yu-Chun, Mead, Jere, Jaspers, Richard T, Trepat, Xavier, Lenormand, Guillaume, Tambe, Dhananjay, Smolensky, Alexander V, Knoll, Andrew H, Butler, James P, Fredberg, Jeffrey J
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 08.05.2009; Public Library of Science (PLoS)
• Subjects: Adaptation; Adaptations; Biomechanical Phenomena; Biophysics; Biophysics/Experimental Biophysical Methods; Bladder; Blood vessels; Cell Biology; Cell Biology/Cytoskeleton; Cells, Cultured; Cellular control mechanisms; Citosquelet; Colorectal cancer; Cytoskeletal proteins; Cytoskeleton; Cytoskeleton - physiology; Fluidization; Fluidizing; Fragility; Homeostasis; Humans; Lungs; Mechanics; Mechanotransduction, Cellular; Metabolism; Metastasis; Muscle contraction; Myocytes, Smooth Muscle - cytology; Nanotechnology; Physiology; Physiology/Respiratory Physiology; Polymerization; Proteïnes citosquelètiques; Public health; Regulació cel·lular; Reinforcement; Rheology; Science; Smooth muscle; Softness; Stress, Mechanical; Traction; Urinary bladder; United States > US; Massachusetts
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0005486

Every adherent eukaryotic cell exerts appreciable traction forces upon its substrate. Moreover, every resident cell within the heart, great vessels, bladder, gut or lung routinely experiences large periodic stretches. As an acute response to such stretches the cytoskeleton can stiffen, increase traction forces and reinforce, as reported by some, or can soften and fluidize, as reported more recently by our laboratory, but in any given circumstance it remains unknown which response might prevail or why. Using a novel nanotechnology, we show here that in loading conditions expected in most physiological circumstances the localized reinforcement response fails to scale up to the level of homogeneous cell stretch; fluidization trumps reinforcement. Whereas the reinforcement response is known to be mediated by upstream mechanosensing and downstream signaling, results presented here show the fluidization response to be altogether novel: it is a direct physical effect of mechanical force acting upon a structural lattice that is soft and fragile. Cytoskeletal softness and fragility, we argue, is consistent with early evolutionary adaptations of the eukaryotic cell to material properties of a soft inert microenvironment.