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Am J Physiol Cell Physiol (April 7, 2004). doi:10.1152/ajpcell.00374.2003
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Submitted on September 2, 2003
Accepted on April 2, 2004

Localized mechanical stress induces time-dependent actin cytoskeletal remodeling and stiffening in cultured airway smooth muscle cells

Linhong Deng1, Nigel J Fairbank1, Ben Fabry2, Paul G Smith3, and Geoffrey N Maksym1*

1 School of Biomedical Engineering, Dalhousie University, Halifax, NS, Canada
2 Physiology Program, Harvard School of Public Health, Boston, MA, USA
3 Pediatrics Department, Case Western Reserve University, Cleveland, OH, USA

* To whom correspondence should be addressed. E-mail: geoff.maksym{at}dal.ca.

Mechanical stress is known to cause changes to the cytoskeleton (CSK) that can lead to altered function in a variety of cell types. Such changes in airway smooth muscle (ASM) cells might contribute to the pathophysiology of asthma. We have shown previously that periodic mechanical strain applied to cultured ASM cells caused dramatic changes in the structure and expression of CSK proteins, and led to increased cell stiffness and contractility [Smith et al. Am J Physiol 272:L20-L27, 1997 and Am J Physiol Lung Cell Mol Physiol 285:L456-L463, 2003]. However, the relationship between the mechanically induced changes in CSK structure and altered cellular function and their time courses are not well understood. Here we have studied the remodeling of actin CSK structure and the changes in CSK stiffness that occurred in cultured ASM cells in response to localized mechanical stress. The stress was applied to the CSK by magnetically oscillating ferrimagnetic beads that were bound to the CSK via integrin receptors, providing a localized mechanical stimulation (MS) of 56 Pa specific torque (torque per bead volume) at 0.3 Hz. We quantified CSK remodeling by measuring actin accumulation at the sites of applied mechanical stress using fluorescence microscopy. We also measured CSK stiffness using optical magnetic twisting cytometry. We found that during MS of up to 120 minutes, the percentage of beads associated with actin structures increased with time. At 60 min, 68.1±1.6 % of the beads were associated with actin structures compared to only 6.7±2.8 % prior to MS and 38.4±5.5 % in time-matched controls that did not receive MS (p<0.05). Similarly, CSK stiffness increased more than 2-fold in response to the MS compared to time-matched controls. Although we found that contractile stimulation with 80 mM KCl and 10-4M acetylcholine (ACh) also induced actin remodeling and increased stiffness in those cells, the changes achieved with MS were more pronounced. Together, these findings imply that mechanical stress is a potent stimulus that can enhance stiffness and contractility of airway smooth muscle cells through CSK remodeling, which may have important implications in airway narrowing and dilation in asthma.




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