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Cytoskeletal targeting of calponin in differentiated, contractile smooth muscle cells of the ferret

Christopher A. Parker * ¹, Katsuhito Takahashi ², Jay X. Tang ³, Terence Tao ¹ ¶ and Kathleen G. Morgan * ¹

1. Biochemical and quantitative image analysis methods were used to investigate the anatomical basis for the previously described agonist-induced redistribution of calponin.

2. At 140 nm resolution, the quantitative distribution of calponin in resting cells was statistically indistinguishable from that of filament bundles containing -smooth muscle actin and myosin, but was significantly different from that of filaments containing -non-muscle actin. Conversely, in stimulated cells, the distribution of calponin was not significantly different from that of -actin filaments in the subplasmalemmal cell cortex but was significantly different from the distribution of -actin- and myosin-containing filamentous bundles.

3. The distribution of calponin significantly differed from that of the intermediate filament proteins vimentin and desmin as well as that of the dense body protein -actinin either by ratio analysis of the subcellular distribution or by colocalization analysis.

4. The imaging results, although limited to 140 nm spatial resolution, suggested the hypothesis that the agonist-induced redistribution involves the binding of calponin to isoform-specific actin filaments. This hypothesis was tested by quantifying the relative affinity of calponin for purified - and -actin. Light scattering measurements showed that calponin induces bundle formation with -actin more readily than -actin, indicating that calponin may be preferentially sequestered by -actin under appropriate conditions.

5. These results are consistent with a model whereby agonist activation decreases calponin's binding to filaments, but the tighter binding to -actin filaments results in a spatial redistribution of calponin to the submembranous cortex.

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