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J. Biol. Chem., Vol. 280, Issue 51, 42442-42453, December 23, 2005

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h2-calponin Is Regulated by Mechanical Tension and Modifies the Function of Actin Cytoskeleton^*

M. Moazzem Hossain, James F. Crish, Richard L. Eckert, Jim J.-C. Lin¶, and Jian-Ping Jin1

From the Section of Molecular Cardiology, Evanston Northwestern Healthcare and Northwestern University Fienberg School of Medicine, Evanston, Illinois 60201, Department of Physiology and Biophysics, Case Western Reserve University School of Medicine, Cleveland, Ohio 44106, and ^¶Department of Biological Sciences, University of Iowa, Iowa City, Iowa 52242

Calponin is an extensively studied actin-binding protein, but its function is not well understood. Among three isoforms of calponin, h2-calponin is found in both smooth muscle and non-muscle cells. The present study demonstrates that epidermal keratinocytes and fibroblast cells express significant amounts of h2-calponin. The expression of h2-calponin is cell anchorage-dependent. The levels of h2-calponin decrease when cells are rounded up and remain low when cells are prevented from adherence to a culture dish. h2-calponin expression resumes after the floating cells are allowed to form a monolayer in plastic dish. Cell cultures on polyacrylamide gels of different stiffness demonstrated that h2-calponin expression is affected by the mechanical properties of the culture matrix. When cells are cultured on soft gel that applies less traction force to the cell and, therefore, lower mechanical tension in the cytoskeleton, the level of h2-calponin is significantly lower than that in cells cultured on hard gel or rigid plastic dish. Force-expression of h2-calponin enhanced the resistance of the actin filaments to cytochalasin B treatment. Keratinocyte differentiation is accompanied by a mechanical tension-related up-regulation of h2-calponin. Lowering the tension of actin cytoskeleton by inhibiting non-muscle myosin II ATPase decreased h2-calponin expression. In contrast to the mechanical tension regulation of endogenous h2-calponin, the expression of h2-calponin using a cytomegalovirus promotor was independent of the stiffness of culture matrix. The results suggest that h2-calponin represents a novel manifestation of mechanical tension responsive gene regulation that may modify cytoskeleton function.

Received for publication, September 9, 2005 , and in revised form, October 12, 2005.

^* This study was supported by National Institutes of Health Grants AR039750-130037, AR048816, and HD044824 (to J.-P. J.), AR046494 and AR045357 (to R. L. E.), and HD018577 (to J. J.-C. L.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ To whom correspondence should be addressed: Molecular Cardiology, Evanston Northwestern Healthcare, Evanston, IL 60201. Tel.: 847-570-1960; Fax: 847-570-1865; E-mail: jpjin{at}northwestern.edu.

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