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Sci. Signal., 8 December 2009
Vol. 2, Issue 100, p. ra81
[DOI: 10.1126/scisignal.2000610]


Delivery of MicroRNA-126 by Apoptotic Bodies Induces CXCL12-Dependent Vascular Protection

Alma Zernecke1,2*{dagger}, Kiril Bidzhekov1*, Heidi Noels1*, Erdenechimeg Shagdarsuren1, Lin Gan3, Bernd Denecke3, Mihail Hristov1, Thomas Köppel4, Maliheh Nazari Jahantigh1, Esther Lutgens1,5, Shusheng Wang6, Eric N. Olson6, Andreas Schober1, and Christian Weber1,5{dagger}

1 Institute of Molecular Cardiovascular Research (IMCAR), RWTH Aachen University, 52074 Aachen, Germany.
2 Rudolf-Virchow-Center–DFG Research Center for Experimental Biomedicine, University of Würzburg, 97080 Würzburg, Germany.
3 Interdisciplinary Centre for Clinical Research BIOMAT, Department of Vascular Surgery, RWTH Aachen University, 52074 Aachen, Germany.
4 Department of Vascular Surgery, RWTH Aachen University, 52074 Aachen, Germany.
5 Cardiovascular Research Institute Maastricht (CARIM), University of Maastricht, 6200 MD Maastricht, the Netherlands.
6 Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390–9148, USA.

* These authors contributed equally to this work.

Abstract: Apoptosis is a pivotal process in embryogenesis and postnatal cell homeostasis and involves the shedding of membranous microvesicles termed apoptotic bodies. In response to tissue damage, the CXC chemokine CXCL12 and its receptor CXCR4 counteract apoptosis and recruit progenitor cells. Here, we show that endothelial cell–derived apoptotic bodies are generated during atherosclerosis and convey paracrine alarm signals to recipient vascular cells that trigger the production of CXCL12. CXCL12 production was mediated by microRNA-126 (miR-126), which was enriched in apoptotic bodies and repressed the function of regulator of G protein (heterotrimeric guanosine triphosphate–binding protein) signaling 16, an inhibitor of G protein–coupled receptor (GPCR) signaling. This enabled CXCR4, a GPCR, to trigger an autoregulatory feedback loop that increased the production of CXCL12. Administration of apoptotic bodies or miR-126 limited atherosclerosis, promoted the incorporation of Sca-1+ progenitor cells, and conferred features of plaque stability on different mouse models of atherosclerosis. This study highlights functions of microRNAs in health and disease that may extend to the recruitment of progenitor cells during other forms of tissue repair or homeostasis.

{dagger} To whom correspondence should be addressed. E-mail: cweber{at} (C.W.) and alma.zernecke{at} (A.Z.)

Citation: A. Zernecke, K. Bidzhekov, H. Noels, E. Shagdarsuren, L. Gan, B. Denecke, M. Hristov, T. Köppel, M. N. Jahantigh, E. Lutgens, S. Wang, E. N. Olson, A. Schober, C. Weber, Delivery of MicroRNA-126 by Apoptotic Bodies Induces CXCL12-Dependent Vascular Protection. Sci. Signal. 2, ra81 (2009).

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