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J. Biol. Chem., Vol. 280, Issue 3, 2361-2369, January 21, 2005

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Pro-angiogenic Signaling by the Endothelial Presence of CEACAM1^*

Nerbil Kilic, Leticia Oliveira-Ferrer, Jan-Henner Wurmbach, Sonja Loges¶, Fariba Chalajour, Samira Neshat Vahid, Joachim Weil||, Malkanthi Fernando, and Suleyman Ergun**

From the Institute of Anatomy, Medical Clinic I, ^¶Department of Hematology/Oncology, University Hospital Eppendorf, D-20246 Hamburg, Germany and ^||Department of Cardiology, University Hospital Regensburg, D-93042 Regensburg, Germany

Here, we demonstrate the expression of carcinoembryonic antigen-related cell adhesion molecule-1 (CEACAM1) in angiogenic sprouts but not in large mother blood vessels within tumor tissue. Correspondingly, only human microvascular endothelial cells involved in in vitro tube formation exhibit CEACAM1. CEACAM1-overexpressing versus CEACAM1-silenced human microvascular endothelial cells were used in migration and tube formation assays. CEACAM1-overexpressing microvascular endothelial cells showed prolonged survival and increased tube formation when they were stimulated with vascular endothelial growth factor (VEGF), whereas CEACAM1 silencing via small interfering RNA blocks these effects. Gene array and LightCycler analyses show an up-regulation of angiogenic factors such as VEGF, VEGF receptor 2, angiopoietin-1, angiopoietin-2, tie-2, angiogenin, and interleukin-8 but a down-regulation of collagen XVIII/endostatin and Tie-1 in CEACAM1-overexpressing microvascular endothelial cells. Western blot analyses confirm these results for VEGF and endostatin at the protein level. These results suggest that constitutive expression of CEACAM1 in microvascular endothelial cells switches them to an angiogenic phenotype, whereas CEACAM1 silencing apparently abrogates the VEGF-induced morphogenetic effects during capillary formation. Thus, strategies targeting the endothelial up-regulation of CEACAM1 might be promising for antiangiogenic tumor therapy.

Received for publication, August 17, 2004 , and in revised form, October 27, 2004.

^* This work was supported by the Deutsche Forschungsgemeinschaft as part of the Priority Program Angiogenesis, SPP1069. 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental data.

^** To whom correspondence should be addressed: Center of Experimental Medicine, Institute of Anatomy I, University Hospital Hamburg-Eppendorf, Martinistrasse 52, D-20246 Hamburg, Germany. Tel: 49-40-428-03-4333; Fax: 49-40-428-03-8416; E-mail: erguen{at}uke.unihamburg.de.

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