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1 Cellular and Integrative Physiology, Indiana University, Indianapolis, IN, USA
2 Cell and Developmental Biology, SUNY Upstate Medical University, Syracuse, NY, USA
* To whom correspondence should be addressed. E-mail: sgunst{at}iupui.edu.
Cytoskeletal reorganization of the smooth muscle cell in response to contractile stimulation may be an important fundamental process in the regulation of tension development. We used confocal microscopy to analyze the effects of cholinergic stimulation on the localization of the cytoskeletal proteins vinculin, paxillin, talin and focal adhesion kinase (FAK) in freshly dissociated tracheal smooth muscle cells. All four proteins were localized at the membrane as well as throughout the cytoplasm of unstimulated cells, but their concentration at the membrane was greater in cells stimulated with acetylcholine (ACh). Antisense oligonucleotides were introduced into tracheal smooth muscle tissues to deplete paxillin protein, which also inhibited contraction in response to ACh. In cells dissociated from paxillin-depleted muscle tissues, the redistribution of vinculin to the membrane in response to ACh was prevented, but the redistribution of FAK and talin was not inhibited. Muscle tissues were transfected with plasmids encoding a paxillin mutant containing a deletion of the LIM3 domain (paxillin LIM3 dl 444-494), the primary determinant for targeting paxillin to focal adhesions. Expression of paxillin LIM3 dl in muscle tissues also inhibited contractile force and prevented the cellular redistribution of paxillin and vinculin to the membrane in response to ACh, but the LIM3 dl mutant paxillin did not inhibit increases in intracellular Ca2+ or myosin light chain phosphorylation. Our results demonstrate that the recruitment of paxillin and vinculin to the smooth muscle membrane is necessary for tension development, and that the recruitment of vinculin to the membrane is regulated by paxillin. Vinculin and paxillin may participate in regulating the formation of linkages between the cytoskeleton and integrin proteins that mediate tension transmission between the contractile apparatus and the extracellular matrix during smooth muscle contraction.
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