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Role of Macrophage Receptor with Collagenous Structure in Innate Immune Tolerance

Jian Jing, Ivana V. Yang, Lucy Hui, Jay A. Patel, Christopher M. Evans, Rytis Prikeris, Lester Kobzik, Brian P. O’Connor and David A. Schwartz
J Immunol June 15, 2013, 190 (12) 6360-6367; DOI: https://doi.org/10.4049/jimmunol.1202942
Jian Jing
*Department of Medicine, University of Colorado School of Medicine, Aurora, CO 80045;
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Ivana V. Yang
*Department of Medicine, University of Colorado School of Medicine, Aurora, CO 80045;
†Center for Genes, Environment, and Health, National Jewish Health, Denver, CO 80206;
‡Integrated Department of Immunology, University of Colorado Denver, Aurora, CO 80045;
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Lucy Hui
*Department of Medicine, University of Colorado School of Medicine, Aurora, CO 80045;
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Jay A. Patel
*Department of Medicine, University of Colorado School of Medicine, Aurora, CO 80045;
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Christopher M. Evans
*Department of Medicine, University of Colorado School of Medicine, Aurora, CO 80045;
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Rytis Prikeris
§Department of Cell and Developmental Biology, University of Colorado Denver, Aurora, CO 80045;
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Lester Kobzik
¶Harvard School of Public Health, Boston, MA 02115; and
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Brian P. O’Connor
†Center for Genes, Environment, and Health, National Jewish Health, Denver, CO 80206;
‡Integrated Department of Immunology, University of Colorado Denver, Aurora, CO 80045;
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David A. Schwartz
*Department of Medicine, University of Colorado School of Medicine, Aurora, CO 80045;
†Center for Genes, Environment, and Health, National Jewish Health, Denver, CO 80206;
‡Integrated Department of Immunology, University of Colorado Denver, Aurora, CO 80045;
‖Department of Medicine, National Jewish Health, Denver, CO 80206
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Abstract

Macrophages play a key role in host defense against microbes, in part, through phagocytosis. Macrophage receptor with collagenous structure (MARCO) is a scavenger receptor on the cell surface of macrophages that mediates opsonin-independent phagocytosis. The goal of our study is to investigate the role of MARCO in LPS or lipotechoic acid–induced macrophage tolerance. Although it has been established that expression of MARCO and phagocytosis is increased in tolerant macrophages, the transcriptional regulation and biological role of MARCO in tolerant macrophages have not been investigated. In this study, we confirm that tolerized mouse bone marrow–derived macrophages (BMDM) selectively increase expression of MARCO (both transcript and cell surface receptor) and increase phagocytosis. We found that H3K4me3 dynamic modification of a promoter site of MARCO was increased in tolerized BMDM. Blocking methylation by treatment with 5-aza-2′-deoxycytidine resulted in reduced H3K4me3 binding in the promoter of MARCO, decreased expression of MARCO, and impaired phagocytosis in tolerized BMDM. However, 5-aza-2′-deoxycytidine had no effect on the inflammatory component of innate immune tolerance. In aggregate, we found that histone methylation was critical to MARCO expression and phagocytosis in tolerized macrophages, but did not affect the inflammatory component of innate immune tolerance.

Footnotes

  • This work was supported in part by National Institutes of Health Grants R01-HL095393, P01-ES18181, and RC2-HL101715.

  • The online version of this article contains supplemental material.

  • Abbreviations used in this article:

    5-AZA
    5-aza-2′-deoxycytidine
    BMDM
    bone marrow–derived macrophage
    ChIP
    chromatin immunoprecipitation
    EU
    endotoxin unit
    LTA
    lipoteichoic acid
    MARCO
    macrophage receptor with collagenous structure
    qPCR
    quantitative PCR
    RT
    room temperature
    WT
    wild-type.

  • Received October 24, 2012.
  • Accepted April 4, 2013.
  • Copyright © 2013 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 190 (12)
The Journal of Immunology
Vol. 190, Issue 12
15 Jun 2013
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Role of Macrophage Receptor with Collagenous Structure in Innate Immune Tolerance
Jian Jing, Ivana V. Yang, Lucy Hui, Jay A. Patel, Christopher M. Evans, Rytis Prikeris, Lester Kobzik, Brian P. O’Connor, David A. Schwartz
The Journal of Immunology June 15, 2013, 190 (12) 6360-6367; DOI: 10.4049/jimmunol.1202942

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Role of Macrophage Receptor with Collagenous Structure in Innate Immune Tolerance
Jian Jing, Ivana V. Yang, Lucy Hui, Jay A. Patel, Christopher M. Evans, Rytis Prikeris, Lester Kobzik, Brian P. O’Connor, David A. Schwartz
The Journal of Immunology June 15, 2013, 190 (12) 6360-6367; DOI: 10.4049/jimmunol.1202942
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