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J. Biol. Chem., Vol. 281, Issue 10, 6664-6672, March 10, 2006

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A Critical Role for Calponin 2 in Vascular Development^*

Jian Tang¹, Guang Hu¹, Jun-ichi Hanai, Ganesh Yadlapalli, Yanfeng Lin, Bo Zhang, Jenna Galloway, Nathan Bahary^¶, Sonia Sinha, Bernard Thisse^||, Christine Thisse^||, Jian-Ping Jin^**, Leonard I. Zon, and Vikas P. Sukhatme²

From the Renal Division and Center for Study of the Tumor Microenvironment, Department of Medicine, Beth Israel Deaconess Medical Center and Division of Hematology/Oncology, Department of Medicine, Children's Hospital, Boston, Massachusetts 02215, ^||Institut de Biologie Moleculaire et Cellulaire, CNRS, INSERM, Universite Louis Pasteur, 67404 Illkirch Cedex, C. U. de Strasbourg, France, ^**Section of Molecular Cardiology, Evanston Northwestern Healthcare, Northwestern University Feinberg School of Medicine, Evanston, Illinois 60201, and ^¶Molecular Genetics and Biochemistry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15261

Calponin 2 (h2 calponin, CNN2) is an actin-binding protein implicated in cytoskeletal organization. We have found that the expression of calponin 2 is relatively restricted to vasculature from 16 to 30 h post-fertilization during zebrafish (Danio rerio) development. Forty-eight hours after injecting antisense morpholino oligos against calponin 2 into embryos at the 1-4-cell stage, zebrafish demonstrated various cardiovascular defects, including sluggish axial and head circulation, absence of circulation in intersegmental vessels and in the dorsal longitudinal anastomotic vessel, enlarged cerebral ventricles, and pericardial edema, in addition to an excess bending, spiraling tail and twisting of the caudal fin. Knockdown of calponin 2 in the Tg(fli1:EGFP)^y1 zebrafish line (in which a fli1 promoter drives vascular-specific enhanced green fluorescent protein expression) indicated that diminished calponin 2 expression blocked the proper migration of endothelial cells during formation of intersegmental vessels. In vitro studies showed that basic fibroblast growth factor-induced human umbilical vein endothelial cell migration was down-regulated by knockdown of calponin 2 expression using an antisense adenovirus, and overexpression of calponin 2 enhanced migration and hastened wound healing. These events were correlated with activation of mitogen-activated protein kinase; moreover, inhibition of this pathway blocked the promigratory effect of calponin 2. Collectively, these data suggest that calponin 2 plays an important role in the migration of endothelial cells both in vivo and in vitro and that its expression is critical for proper vascular development.

Received for publication, June 27, 2005 , and in revised form, November 10, 2005.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) DQ104245 [GenBank] .

^* This work was supported by seed funds from the Beth Israel Deaconess Medical Center. 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 These authors contributed equally to this work.

² To whom correspondence should be addressed: Beth Israel Deaconess Medical Center, 330 Brookline Ave., RW 563, Boston, MA 02215. E-mail: vsukhatm{at}bidmc.harvard.edu.

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