Plasticity of Leukocytic Exudates in Resolving Acute Inflammation Is Regulated by MicroRNA and Proresolving Mediators

The magnitude and duration of acute inflammation are controlled by active resolution programs involving specialized proresolving mediators (SPMs; resolvins and maresins) and microRNAs (miRNAs). Here, we report that miR-466l was temporally regulated in murine exudate-infiltrating leukocytes. Neutroph...

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Published in	Immunity (Cambridge, Mass.) Vol. 39; no. 5; pp. 885 - 898
Main Authors	Li, Yongsheng, Dalli, Jesmond, Chiang, Nan, Baron, Rebecca M., Quintana, Carolina, Serhan, Charles N.
Format	Journal Article
Language	English
Published	United States Elsevier Inc 14.11.2013 Elsevier Limited
Subjects	Acute Disease Animals Apoptosis Biosynthesis Chemotaxis - physiology Docosahexaenoic Acids - metabolism Gene expression Gene Expression Regulation Human subjects Humans Inflammation Mediators - metabolism Leukocytes Macrophages - metabolism Male Mice MicroRNAs - biosynthesis MicroRNAs - genetics MicroRNAs - physiology Neutrophils - metabolism NF-kappa B - metabolism Peritonitis - chemically induced Peritonitis - immunology Peritonitis - metabolism Peritonitis - pathology Phagocytosis - physiology Sepsis Sepsis - blood Sepsis - mortality Transcription Factor AP-1 - metabolism Transcription, Genetic Zymosan - toxicity
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Abstract	The magnitude and duration of acute inflammation are controlled by active resolution programs involving specialized proresolving mediators (SPMs; resolvins and maresins) and microRNAs (miRNAs). Here, we report that miR-466l was temporally regulated in murine exudate-infiltrating leukocytes. Neutrophil miR-466l overexpression in vivo promoted initiation of inflammation that anteceded macrophage expression of this miRNA, which accelerated resolution when overexpressed. In macrophages, miR-466l overexpression increased prostanoids and SPMs (e.g., resolvin D1 [RvD1] and RvD5), which enhanced resolution. RvD1, RvD2, maresin 1 (MaR1), and apoptotic neutrophils reduced miR-466l expression within human macrophages, a feedback regulation that most likely prepares for homeostasis. miR-466l was upregulated in peripheral blood of sepsis patients, and its increase correlated with nonsurvival from sepsis. SPMs and miR-466l regulated transcription factors activator protein 1 and nuclear factor κB1 in miRNA biogenesis. These results demonstrate pivotal roles for SPMs and miR-466l in dynamic leukocyte plasticity during resolution of acute inflammatory responses. [Display omitted] •Acute inflammation upregulates miR-466l, which regulates resolution•Overexpression of miR-466l promotes specialized proresolving mediator production•Resolvin D1 and miR-466l each enhance efferocytosis, contributing to resolution•miR-466l is present and increased in sepsis nonsurvivors
AbstractList	The magnitude and duration of acute inflammation are controlled by active resolution programs involving specialized proresolving mediators (SPMs; resolvins and maresins) and microRNAs (miRNAs). Here, we report that miR-466l was temporally regulated in murine exudate-infiltrating leukocytes. Neutrophil miR-466l overexpression in vivo promoted initiation of inflammation that anteceded macrophage expression of this miRNA, which accelerated resolution when overexpressed. In macrophages, miR-466l overexpression increased prostanoids and SPMs (e.g., resolvin D1 [RvD1] and RvD5), which enhanced resolution. RvD1, RvD2, maresin 1 (MaR1), and apoptotic neutrophils reduced miR-466l expression within human macrophages, a feedback regulation that most likely prepares for homeostasis. miR-466l was upregulated in peripheral blood of sepsis patients, and its increase correlated with nonsurvival from sepsis. SPMs and miR-466l regulated transcription factors activator protein 1 and nuclear factor κB1 in miRNA biogenesis. These results demonstrate pivotal roles for SPMs and miR-466l in dynamic leukocyte plasticity during resolution of acute inflammatory responses. The magnitude and duration of acute inflammation are controlled by active resolution programs involving specialized proresolving mediators (SPMs; resolvins and maresins) and microRNAs (miRNAs). Here, we report that miR-466l was temporally regulated in murine exudate-infiltrating leukocytes. Neutrophil miR-466l overexpression in vivo promoted initiation of inflammation that anteceded macrophage expression of this miRNA, which accelerated resolution when overexpressed. In macrophages, miR-466l overexpression increased prostanoids and SPMs (e.g., resolvin D1 [RvD1] and RvD5), which enhanced resolution. RvD1, RvD2, maresin 1 (MaR1), and apoptotic neutrophils reduced miR-466l expression within human macrophages, a feedback regulation that most likely prepares for homeostasis. miR-466l was upregulated in peripheral blood of sepsis patients, and its increase correlated with nonsurvival from sepsis. SPMs and miR-466l regulated transcription factors activator protein 1 and nuclear factor κB1 in miRNA biogenesis. These results demonstrate pivotal roles for SPMs and miR-466l in dynamic leukocyte plasticity during resolution of acute inflammatory responses. [Display omitted] •Acute inflammation upregulates miR-466l, which regulates resolution•Overexpression of miR-466l promotes specialized proresolving mediator production•Resolvin D1 and miR-466l each enhance efferocytosis, contributing to resolution•miR-466l is present and increased in sepsis nonsurvivors The magnitude and duration of acute inflammation are controlled by active resolution programs involving specialized proresolving mediators (SPMs; resolvins and maresins) and microRNAs (miRNAs). Here, we report that miR-466l was temporally regulated in murine exudate-infiltrating leukocytes. Neutrophil miR-466l overexpression in vivo promoted initiation of inflammation that anteceded macrophage expression of this miRNA, which accelerated resolution when overexpressed. In macrophages, miR-466l overexpression increased prostanoids and SPMs (e.g., resolvin D1 [RvD1] and RvD5), which enhanced resolution. RvD1, RvD2, maresin 1 (MaR1), and apoptotic neutrophils reduced miR-466l expression within human macrophages, a feedback regulation that most likely prepares for homeostasis. miR-466l was upregulated in peripheral blood of sepsis patients, and its increase correlated with nonsurvival from sepsis. SPMs and miR-466l regulated transcription factors activator protein 1 and nuclear factor κB1 in miRNA biogenesis. These results demonstrate pivotal roles for SPMs and miR-466l in dynamic leukocyte plasticity during resolution of acute inflammatory responses. The magnitude and duration of acute inflammation are controlled by active resolution programs involving specialized proresolving mediators (SPMs; resolvins and maresins) and microRNAs (miRNAs). Here, we report that miR-466l was temporally regulated in murine exudate-infiltrating leukocytes. Neutrophil miR-466l overexpression in vivo promoted initiation of inflammation that anteceded macrophage expression of this miRNA, which accelerated resolution when overexpressed. In macrophages, miR-466l overexpression increased prostanoids and SPMs (e.g., resolvin D1 [RvD1] and RvD5), which enhanced resolution. RvD1, RvD2, maresin 1 (MaR1), and apoptotic neutrophils reduced miR-466l expression within human macrophages, a feedback regulation that most likely prepares for homeostasis. miR-466l was upregulated in peripheral blood of sepsis patients, and its increase correlated with nonsurvival from sepsis. SPMs and miR-466l regulated transcription factors activator protein 1 and nuclear factor Kappa B1 in miRNA biogenesis. These results demonstrate pivotal roles for SPMs and miR-466l in dynamic leukocyte plasticity during resolution of acute inflammatory responses.
Author	Quintana, Carolina Serhan, Charles N. Chiang, Nan Dalli, Jesmond Li, Yongsheng Baron, Rebecca M.
AuthorAffiliation	1 Center for Experimental Therapeutics and Reperfusion Injury, Harvard Institutes of Medicine, Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115, USA 2 Division of Pulmonary and Critical Care Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115, USA
AuthorAffiliation_xml	– name: 1 Center for Experimental Therapeutics and Reperfusion Injury, Harvard Institutes of Medicine, Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115, USA – name: 2 Division of Pulmonary and Critical Care Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115, USA
Author_xml	– sequence: 1 givenname: Yongsheng surname: Li fullname: Li, Yongsheng organization: Center for Experimental Therapeutics and Reperfusion Injury, Harvard Institutes of Medicine, Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115, USA – sequence: 2 givenname: Jesmond surname: Dalli fullname: Dalli, Jesmond organization: Center for Experimental Therapeutics and Reperfusion Injury, Harvard Institutes of Medicine, Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115, USA – sequence: 3 givenname: Nan surname: Chiang fullname: Chiang, Nan organization: Center for Experimental Therapeutics and Reperfusion Injury, Harvard Institutes of Medicine, Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115, USA – sequence: 4 givenname: Rebecca M. surname: Baron fullname: Baron, Rebecca M. organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115, USA – sequence: 5 givenname: Carolina surname: Quintana fullname: Quintana, Carolina organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115, USA – sequence: 6 givenname: Charles N. surname: Serhan fullname: Serhan, Charles N. email: cnserhan@zeus.bwh.harvard.edu organization: Center for Experimental Therapeutics and Reperfusion Injury, Harvard Institutes of Medicine, Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/24238341$$D View this record in MEDLINE/PubMed
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Copyright	2013 Elsevier Inc. Copyright © 2013 Elsevier Inc. All rights reserved. Copyright Elsevier Limited Nov 14, 2013 2013 Elsevier Inc. 2013
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Snippet	The magnitude and duration of acute inflammation are controlled by active resolution programs involving specialized proresolving mediators (SPMs; resolvins and...
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SubjectTerms	Acute Disease Animals Apoptosis Biosynthesis Chemotaxis - physiology Docosahexaenoic Acids - metabolism Gene expression Gene Expression Regulation Human subjects Humans Inflammation Mediators - metabolism Leukocytes Macrophages - metabolism Male Mice MicroRNAs - biosynthesis MicroRNAs - genetics MicroRNAs - physiology Neutrophils - metabolism NF-kappa B - metabolism Peritonitis - chemically induced Peritonitis - immunology Peritonitis - metabolism Peritonitis - pathology Phagocytosis - physiology Sepsis Sepsis - blood Sepsis - mortality Transcription Factor AP-1 - metabolism Transcription, Genetic Zymosan - toxicity
Title	Plasticity of Leukocytic Exudates in Resolving Acute Inflammation Is Regulated by MicroRNA and Proresolving Mediators
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