Mannose receptor modulates macrophage polarization and allergic inflammation through miR-511-3p
Mannose receptor (MRC1/CD206) has been suggested to mediate allergic sensitization and asthma to multiple glycoallergens, including cockroach allergens. We sought to determine the existence of a protective mechanism through which MRC1 limits allergic inflammation through its intronic miR-511-3p. We...
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| Published in | Journal of allergy and clinical immunology Vol. 141; no. 1; pp. 350 - 364.e8 |
|---|---|
| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.01.2018
Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0091-6749 1097-6825 1085-8725 1097-6825 |
| DOI | 10.1016/j.jaci.2017.04.049 |
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| Abstract | Mannose receptor (MRC1/CD206) has been suggested to mediate allergic sensitization and asthma to multiple glycoallergens, including cockroach allergens.
We sought to determine the existence of a protective mechanism through which MRC1 limits allergic inflammation through its intronic miR-511-3p.
We examined MRC1-mediated cockroach allergen uptake by lung macrophages and lung inflammation using C57BL/6 wild-type (WT) and Mrc1−/− mice. The role of miR-511-3p in macrophage polarization and cockroach allergen–induced lung inflammation in mice transfected with adeno-associated virus (AAV)–miR-511-3p (AAV–cytomegalovirus–miR-511-3p–enhanced green fluorescent protein) was analyzed. Gene profiling of macrophages with or without miR-511-3p overexpression was also performed.
Mrc1−/− lung macrophages showed a significant reduction in cockroach allergen uptake compared with WT mice, and Mrc1−/− mice had an exacerbated lung inflammation with increased levels of cockroach allergen–specific IgE and TH2/TH17 cytokines in a cockroach allergen–induced mouse model compared with WT mice. Macrophages from Mrc1−/− mice showed significantly reduced levels of miR-511-3 and an M1 phenotype, whereas overexpression of miR-511-3p rendered macrophages to exhibit a M2 phenotype. Furthermore, mice transfected with AAV–miR-511-3p showed a significant reduction in cockroach allergen–induced inflammation. Profiling of macrophages with or without miR-511-3p overexpression identified 729 differentially expressed genes, wherein expression of prostaglandin D2 synthase (Ptgds) and its product PGD2 were significantly downregulated by miR-511-3p. Ptgds showed a robust binding to miR-511-3p, which might contribute to the protective effect of miR-511-3p. Plasma levels of miR-511-3p were significantly lower in human asthmatic patients compared with nonasthmatic subjects.
These studies support a critical but previously unrecognized role of MRC1 and miR-511-3p in protection against allergen-induced lung inflammation.
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| AbstractList | Mannose receptor (MRC1/CD206) has been suggested to mediate allergic sensitization and asthma to multiple glycoallergens, including cockroach allergens.
We sought to determine the existence of a protective mechanism through which MRC1 limits allergic inflammation through its intronic miR-511-3p.
We examined MRC1-mediated cockroach allergen uptake by lung macrophages and lung inflammation using C57BL/6 wild-type (WT) and Mrc1−/− mice. The role of miR-511-3p in macrophage polarization and cockroach allergen–induced lung inflammation in mice transfected with adeno-associated virus (AAV)–miR-511-3p (AAV–cytomegalovirus–miR-511-3p–enhanced green fluorescent protein) was analyzed. Gene profiling of macrophages with or without miR-511-3p overexpression was also performed.
Mrc1−/− lung macrophages showed a significant reduction in cockroach allergen uptake compared with WT mice, and Mrc1−/− mice had an exacerbated lung inflammation with increased levels of cockroach allergen–specific IgE and TH2/TH17 cytokines in a cockroach allergen–induced mouse model compared with WT mice. Macrophages from Mrc1−/− mice showed significantly reduced levels of miR-511-3 and an M1 phenotype, whereas overexpression of miR-511-3p rendered macrophages to exhibit a M2 phenotype. Furthermore, mice transfected with AAV–miR-511-3p showed a significant reduction in cockroach allergen–induced inflammation. Profiling of macrophages with or without miR-511-3p overexpression identified 729 differentially expressed genes, wherein expression of prostaglandin D2 synthase (Ptgds) and its product PGD2 were significantly downregulated by miR-511-3p. Ptgds showed a robust binding to miR-511-3p, which might contribute to the protective effect of miR-511-3p. Plasma levels of miR-511-3p were significantly lower in human asthmatic patients compared with nonasthmatic subjects.
These studies support a critical but previously unrecognized role of MRC1 and miR-511-3p in protection against allergen-induced lung inflammation.
[Display omitted] Background Mannose receptor (MRC1/CD206) has been suggested to mediate allergic sensitization and asthma to multiple glycoallergens, including cockroach allergens. Objective We sought to determine the existence of a protective mechanism through which MRC1 limits allergic inflammation through its intronic miR-511-3p. Methods We examined MRC1-mediated cockroach allergen uptake by lung macrophages and lung inflammation using C57BL/6 wild-type (WT) andMrc1−/−mice. The role of miR-511-3p in macrophage polarization and cockroach allergen-induced lung inflammation in mice transfected with adeno-associated virus (AAV)-miR-511-3p (AAV-cytomegalovirus-miR-511-3p-enhanced green fluorescent protein) was analyzed. Gene profiling of macrophages with or without miR-511-3p overexpression was also performed. Results Mrc1−/−lung macrophages showed a significant reduction in cockroach allergen uptake compared with WT mice, andMrc1−/−mice had an exacerbated lung inflammation with increased levels of cockroach allergen-specific IgE and TH2/TH17 cytokines in a cockroach allergen-induced mouse model compared with WT mice. Macrophages fromMrc1−/−mice showed significantly reduced levels of miR-511-3 and an M1 phenotype, whereas overexpression of miR-511-3p rendered macrophages to exhibit a M2 phenotype. Furthermore, mice transfected with AAV-miR-511-3p showed a significant reduction in cockroach allergen-induced inflammation. Profiling of macrophages with or without miR-511-3p overexpression identified 729 differentially expressed genes, wherein expression of prostaglandin D2synthase(Ptgds)and its product PGD2were significantly downregulated by miR-511-3p.Ptgdsshowed a robust binding to miR-511-3p, which might contribute to the protective effect of miR-511-3p. Plasma levels of miR-511-3p were significantly lower in human asthmatic patients compared with nonasthmatic subjects. Conclusion These studies support a critical but previously unrecognized role of MRC1 and miR-511-3p in protection against allergen-induced lung inflammation. Mannose receptor (MRC1/CD206) has been suggested to mediate allergic sensitization and asthma to multiple glycoallergens, including cockroach allergens. We sought to determine the existence of a protective mechanism through which MRC1 limits allergic inflammation through its intronic miR-511-3p. We examined MRC1-mediated cockroach allergen uptake by lung macrophages and lung inflammation using C57BL/6 wild-type (WT) and Mrc1 mice. The role of miR-511-3p in macrophage polarization and cockroach allergen-induced lung inflammation in mice transfected with adeno-associated virus (AAV)-miR-511-3p (AAV-cytomegalovirus-miR-511-3p-enhanced green fluorescent protein) was analyzed. Gene profiling of macrophages with or without miR-511-3p overexpression was also performed. Mrc1 lung macrophages showed a significant reduction in cockroach allergen uptake compared with WT mice, and Mrc1 mice had an exacerbated lung inflammation with increased levels of cockroach allergen-specific IgE and T 2/T 17 cytokines in a cockroach allergen-induced mouse model compared with WT mice. Macrophages from Mrc1 mice showed significantly reduced levels of miR-511-3 and an M1 phenotype, whereas overexpression of miR-511-3p rendered macrophages to exhibit a M2 phenotype. Furthermore, mice transfected with AAV-miR-511-3p showed a significant reduction in cockroach allergen-induced inflammation. Profiling of macrophages with or without miR-511-3p overexpression identified 729 differentially expressed genes, wherein expression of prostaglandin D synthase (Ptgds) and its product PGD were significantly downregulated by miR-511-3p. Ptgds showed a robust binding to miR-511-3p, which might contribute to the protective effect of miR-511-3p. Plasma levels of miR-511-3p were significantly lower in human asthmatic patients compared with nonasthmatic subjects. These studies support a critical but previously unrecognized role of MRC1 and miR-511-3p in protection against allergen-induced lung inflammation. Mannose receptor (MRC1/CD206) has been suggested to mediate allergic sensitization and asthma to multiple glycoallergens, including cockroach allergens.BACKGROUNDMannose receptor (MRC1/CD206) has been suggested to mediate allergic sensitization and asthma to multiple glycoallergens, including cockroach allergens.We sought to determine the existence of a protective mechanism through which MRC1 limits allergic inflammation through its intronic miR-511-3p.OBJECTIVEWe sought to determine the existence of a protective mechanism through which MRC1 limits allergic inflammation through its intronic miR-511-3p.We examined MRC1-mediated cockroach allergen uptake by lung macrophages and lung inflammation using C57BL/6 wild-type (WT) and Mrc1-/- mice. The role of miR-511-3p in macrophage polarization and cockroach allergen-induced lung inflammation in mice transfected with adeno-associated virus (AAV)-miR-511-3p (AAV-cytomegalovirus-miR-511-3p-enhanced green fluorescent protein) was analyzed. Gene profiling of macrophages with or without miR-511-3p overexpression was also performed.METHODSWe examined MRC1-mediated cockroach allergen uptake by lung macrophages and lung inflammation using C57BL/6 wild-type (WT) and Mrc1-/- mice. The role of miR-511-3p in macrophage polarization and cockroach allergen-induced lung inflammation in mice transfected with adeno-associated virus (AAV)-miR-511-3p (AAV-cytomegalovirus-miR-511-3p-enhanced green fluorescent protein) was analyzed. Gene profiling of macrophages with or without miR-511-3p overexpression was also performed.Mrc1-/- lung macrophages showed a significant reduction in cockroach allergen uptake compared with WT mice, and Mrc1-/- mice had an exacerbated lung inflammation with increased levels of cockroach allergen-specific IgE and TH2/TH17 cytokines in a cockroach allergen-induced mouse model compared with WT mice. Macrophages from Mrc1-/- mice showed significantly reduced levels of miR-511-3 and an M1 phenotype, whereas overexpression of miR-511-3p rendered macrophages to exhibit a M2 phenotype. Furthermore, mice transfected with AAV-miR-511-3p showed a significant reduction in cockroach allergen-induced inflammation. Profiling of macrophages with or without miR-511-3p overexpression identified 729 differentially expressed genes, wherein expression of prostaglandin D2 synthase (Ptgds) and its product PGD2 were significantly downregulated by miR-511-3p. Ptgds showed a robust binding to miR-511-3p, which might contribute to the protective effect of miR-511-3p. Plasma levels of miR-511-3p were significantly lower in human asthmatic patients compared with nonasthmatic subjects.RESULTSMrc1-/- lung macrophages showed a significant reduction in cockroach allergen uptake compared with WT mice, and Mrc1-/- mice had an exacerbated lung inflammation with increased levels of cockroach allergen-specific IgE and TH2/TH17 cytokines in a cockroach allergen-induced mouse model compared with WT mice. Macrophages from Mrc1-/- mice showed significantly reduced levels of miR-511-3 and an M1 phenotype, whereas overexpression of miR-511-3p rendered macrophages to exhibit a M2 phenotype. Furthermore, mice transfected with AAV-miR-511-3p showed a significant reduction in cockroach allergen-induced inflammation. Profiling of macrophages with or without miR-511-3p overexpression identified 729 differentially expressed genes, wherein expression of prostaglandin D2 synthase (Ptgds) and its product PGD2 were significantly downregulated by miR-511-3p. Ptgds showed a robust binding to miR-511-3p, which might contribute to the protective effect of miR-511-3p. Plasma levels of miR-511-3p were significantly lower in human asthmatic patients compared with nonasthmatic subjects.These studies support a critical but previously unrecognized role of MRC1 and miR-511-3p in protection against allergen-induced lung inflammation.CONCLUSIONThese studies support a critical but previously unrecognized role of MRC1 and miR-511-3p in protection against allergen-induced lung inflammation. Abstract Background Mannose receptor (MRC1/CD206) has been suggested to mediate allergic sensitization and asthma to multiple glyco-allergens, including cockroach allergens. Objective Determine the existence of a protective mechanism through which MRC1 limits allergic inflammation through its intronic miR-511-3p. Methods We examined the MRC1-mediated cockroach allergen uptake by lung macrophages and lung inflammation using C57BL/6 wild-type (WT) and Mrc1-/- mice. Role of miR-511-3p in macrophage polarization and cockroach allergen-induced lung inflammation in mice transfected with Adeno-Associated Virus (AAV)-miR-511-3p (AAV-CMV-miR-511-3p-eGFP) was analyzed. Gene profiling of macrophages with or without miR-511-3p overexpression was also performed. Results Mrc1-/- lung macrophages showed significant reduction in cockroach allergen uptake compared with WT mice, and Mrc1-/- mice had an exacerbated lung inflammation with increased levels of cockroach allergen-specific IgE and Th2/Th17 cytokines in a cockroach allergen-induced mouse model compared to WT mice. Macrophages from Mrc1-/- mice showed significantly reduced levels of miR-511-3 and a M1 phenotype whereas over-expression of miR-511-3p rendered macrophages to exhibit a M2 phenotype. Furthermore, mice transfected with AAV-miR-511-3p showed a significant reduction in cockroach allergen-induced inflammation. Profiling of macrophages with or without miR-511-3p over-expression identified 729 differentially expressed genes, wherein the levels of Ptgds and its product PGD2 were significantly down-regulated by miR-511-3p. Ptgds showed a robust binding to miR-511-3p, which might contribute to the protective effect of miR-511-3p. The plasma levels of miR-511-3p were significantly lower in human asthmatics compared to non-asthmatic subjects. Conclusion These studies support a critical but previously unrecognized role of MRC1 and miR-511-3p in protection against allergen-induced lung inflammation. |
| Author | Ishmael, Faoud T. Becker, Kevin G. Zhou, Yufeng Wan, Mei Li, Changjun Squadrito, Mario Leonardo Tang, Ho Lam Tang, Ho Man Qiu, Lipeng Gao, Peisong Hsu, Man-Hsun Zhang, Yongqing Huang, Shau-Ku Do, Danh C. |
| AuthorAffiliation | k Lou-Hu Hospital, Shen-Zhen University c Swiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne f Gene Expression & Genomics Unit, National Institute on Aging, National Institutes of Health, Baltimore g Department of Orthopedic Surgery, Johns Hopkins University School of Medicine, Baltimore a Johns Hopkins Asthma & Allergy Center, Johns Hopkins University School of Medicine, Baltimore d Institute for Basic Biomedical Sciences, Johns Hopkins University School of Medicine, Baltimore i National Institute of Environmental Health Sciences, National Health Research Institutes, Zhunan h Children’s Hospital and the Institute of Biomedical Sciences, Fudan University, and Key Laboratory of Neonatal Diseases, Ministry of Health, Shanghai b Department of Medicine, Division of Pulmonary, Allergy, and Critical Care Medicine, Pennsylvania State University Milton S. Hershey Medical Center e Department of Molecular Microbiolo |
| AuthorAffiliation_xml | – name: c Swiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne – name: e Department of Molecular Microbiology and Immunology, Johns Hopkins University Bloomberg School of Public Health, Baltimore – name: a Johns Hopkins Asthma & Allergy Center, Johns Hopkins University School of Medicine, Baltimore – name: j Research Center for Environmental Medicine, Kaohsiung Medical University – name: h Children’s Hospital and the Institute of Biomedical Sciences, Fudan University, and Key Laboratory of Neonatal Diseases, Ministry of Health, Shanghai – name: k Lou-Hu Hospital, Shen-Zhen University – name: b Department of Medicine, Division of Pulmonary, Allergy, and Critical Care Medicine, Pennsylvania State University Milton S. Hershey Medical Center – name: d Institute for Basic Biomedical Sciences, Johns Hopkins University School of Medicine, Baltimore – name: f Gene Expression & Genomics Unit, National Institute on Aging, National Institutes of Health, Baltimore – name: g Department of Orthopedic Surgery, Johns Hopkins University School of Medicine, Baltimore – name: i National Institute of Environmental Health Sciences, National Health Research Institutes, Zhunan |
| Author_xml | – sequence: 1 givenname: Yufeng surname: Zhou fullname: Zhou, Yufeng organization: Johns Hopkins Asthma & Allergy Center, Johns Hopkins University School of Medicine, Baltimore, Md – sequence: 2 givenname: Danh C. surname: Do fullname: Do, Danh C. organization: Johns Hopkins Asthma & Allergy Center, Johns Hopkins University School of Medicine, Baltimore, Md – sequence: 3 givenname: Faoud T. surname: Ishmael fullname: Ishmael, Faoud T. organization: Department of Medicine, Division of Pulmonary, Allergy, and Critical Care Medicine, Pennsylvania State University Milton S. Hershey Medical Center, Hershey, Pa – sequence: 4 givenname: Mario Leonardo surname: Squadrito fullname: Squadrito, Mario Leonardo organization: Swiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland – sequence: 5 givenname: Ho Man surname: Tang fullname: Tang, Ho Man organization: Institute for Basic Biomedical Sciences, Johns Hopkins University School of Medicine, Baltimore, Md – sequence: 6 givenname: Ho Lam surname: Tang fullname: Tang, Ho Lam organization: Department of Molecular Microbiology and Immunology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, Md – sequence: 7 givenname: Man-Hsun surname: Hsu fullname: Hsu, Man-Hsun organization: Department of Medicine, Division of Pulmonary, Allergy, and Critical Care Medicine, Pennsylvania State University Milton S. Hershey Medical Center, Hershey, Pa – sequence: 8 givenname: Lipeng surname: Qiu fullname: Qiu, Lipeng organization: Johns Hopkins Asthma & Allergy Center, Johns Hopkins University School of Medicine, Baltimore, Md – sequence: 9 givenname: Changjun surname: Li fullname: Li, Changjun organization: Department of Orthopedic Surgery, Johns Hopkins University School of Medicine, Baltimore, Md – sequence: 10 givenname: Yongqing surname: Zhang fullname: Zhang, Yongqing organization: Gene Expression & Genomics Unit, National Institute on Aging, National Institutes of Health, Baltimore, Md – sequence: 11 givenname: Kevin G. surname: Becker fullname: Becker, Kevin G. organization: Gene Expression & Genomics Unit, National Institute on Aging, National Institutes of Health, Baltimore, Md – sequence: 12 givenname: Mei surname: Wan fullname: Wan, Mei organization: Department of Orthopedic Surgery, Johns Hopkins University School of Medicine, Baltimore, Md – sequence: 13 givenname: Shau-Ku surname: Huang fullname: Huang, Shau-Ku email: skhuang@nhri.org.tw organization: Johns Hopkins Asthma & Allergy Center, Johns Hopkins University School of Medicine, Baltimore, Md – sequence: 14 givenname: Peisong surname: Gao fullname: Gao, Peisong email: pgao1@jhmi.edu organization: Johns Hopkins Asthma & Allergy Center, Johns Hopkins University School of Medicine, Baltimore, Md |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28629744$$D View this record in MEDLINE/PubMed |
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| Copyright | 2017 American Academy of Allergy, Asthma & Immunology Copyright © 2017 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved. Copyright Elsevier Science Ltd. Jan 1, 2018 |
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| Keywords | PAS M-CSF ROCK2 CLR LV BM LTBP1 GFP FITC FDR MRC1 Mannose receptor miRNA qPCR PTGDS WT SSC miR-511-3p AF H&E macrophage asthma BAL CMV AAV CRE TLR4 DC CEBPA Cockroach extract Auto-fluorescence C-type lectin-like domains Bronchoalveolar lavage CCAAT/Enhancer Binding Protein Alpha MiR-511-3p C-type lectin receptor Rho Associated Coiled-Coil Containing Protein Kinase 2 Prostaglandin D2 Synthase False Discovery Rate Adeno-associated virus Toll-like receptor 4 Mannose receptor (MRC1/CD206) Lentivirus CTLD microRNA Latent Transforming Growth Factor Beta Binding Protein 1 Macrophage |
| Language | English |
| License | Copyright © 2017 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved. cc-by-nc-nd |
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| Snippet | Mannose receptor (MRC1/CD206) has been suggested to mediate allergic sensitization and asthma to multiple glycoallergens, including cockroach allergens.
We... Abstract Background Mannose receptor (MRC1/CD206) has been suggested to mediate allergic sensitization and asthma to multiple glyco-allergens, including... Background Mannose receptor (MRC1/CD206) has been suggested to mediate allergic sensitization and asthma to multiple glycoallergens, including cockroach... Mannose receptor (MRC1/CD206) has been suggested to mediate allergic sensitization and asthma to multiple glycoallergens, including cockroach... |
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| SubjectTerms | Allergens - immunology Allergies Allergy and Immunology Animals Antigens Asthma Asthma - etiology Asthma - metabolism Asthma - pathology Bone marrow Cockroaches - immunology Cytokines Flow cytometry Gene expression Gene Expression Profiling Gene Expression Regulation Genetic Vectors - genetics Green fluorescent protein Helper cells Hypersensitivity Hypersensitivity - etiology Hypersensitivity - metabolism Hypersensitivity - pathology Immunoglobulin E Inflammation Inner city Laboratories Lectins, C-Type - metabolism Lungs Lymphocytes T macrophage Macrophage Activation - genetics Macrophage Activation - immunology Macrophages Macrophages - immunology Macrophages - metabolism Macrophages, Alveolar - immunology Macrophages, Alveolar - metabolism Mannose Mannose Receptor Mannose-Binding Lectins - metabolism Membrane Glycoproteins - genetics Membrane Glycoproteins - metabolism Mice Mice, Knockout MicroRNAs MicroRNAs - genetics Microscopy miR-511-3p Models, Biological Plasma levels Pneumonia - etiology Pneumonia - metabolism Pneumonia - pathology Polarization Receptors, Cell Surface - genetics Receptors, Cell Surface - metabolism Receptors, Immunologic RNA Interference Rodents |
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| Title | Mannose receptor modulates macrophage polarization and allergic inflammation through miR-511-3p |
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