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MicroRNA-155 aggravates ischemia–reperfusion injury by modulation of inflammatory cell recruitment and the respiratory oxidative burst

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Abstract

The inflammatory sequelae of ischemia–reperfusion injury (IRI) are a major causal factor of tissue injury in various clinical settings. MicroRNAs (miRs) are short, non-coding RNAs, which regulate protein expression. Here, we investigated the role of miR-155 in IR-related tissue injury. Quantifying microRNA-expression levels in a human muscle tissue after IRI, we found miR-155 expression to be significantly increased and to correlate with the increased expression of TNF-α, IL-1β, CD105, and Caspase3 as well as with leukocyte infiltration. The direct miR-155 target gene SOCS-1 was downregulated. In a mouse model of myocardial infarction, temporary LAD ligation and reperfusion injury resulted in a smaller area of necrosis in miR-155−/− animals compared to wildtype animals. To investigate the underlying mechanisms, we evaluated the effect of miR-155 on inflammatory cell recruitment by intravital microscopy and on the generation of reactive oxygen species (ROS) of macrophages. Our intravital imaging results demonstrated a decreased recruitment of inflammatory cells in miR-155−/− animals during IRI. The generation of ROS in leukocytic cells of miR-155−/− animals was also reduced. RNA silencing of the direct miR-155 target gene SOCS-1 abrogated this effect. In conclusion, miR-155 aggravates the inflammatory response, leukocyte infiltration and tissue damage in IRI via modulation of SOCS-1-dependent generation of ROS. MiR-155 is thus a potential target for the treatment or prevention of IRI.

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Abbreviations

BMDM:

Bone marrow derived macrophages

IRI:

Ischemia–reperfusion injury

ROS:

Reactive oxygen species

SOCS-1:

Suppressor of cytokine signaling 1

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Acknowledgments

Funding received for this work: this work was supported by the “Else-Kröner-Fresenius Stiftung” Grant #2011_A191 to SUE and SG.

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    Authors and Affiliations

    1. Department of Plastic and Handsurgery, University of Freiburg Medical Center, Freiburg, Germany

      Steffen U. Eisenhardt, Jakob B. W. Weiss, Jan R. Thiele, Yvonne Schmidt & G. Bjoern Stark

    2. Cardiology and Angiology I, Heart Center Freiburg University, Hugstetter Strasse 55, 79106, Freiburg, Germany

      Christian Smolka, Johanna Maxeiner, Franziska Pankratz, Xavier Bemtgen, Max Kustermann, Martin Moser, Christoph Bode & Sebastian Grundmann

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    S. U. Eisenhardt and J. B.W. Weiss contributed equally to this work.

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    Eisenhardt, S.U., Weiss, J.B.W., Smolka, C. et al. MicroRNA-155 aggravates ischemia–reperfusion injury by modulation of inflammatory cell recruitment and the respiratory oxidative burst. Basic Res Cardiol 110, 32 (2015). https://doi.org/10.1007/s00395-015-0490-9

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