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The Class A Scavenger Receptor, Macrophage Receptor with Collagenous Structure, Is the Major Phagocytic Receptor for Clostridium sordellii Expressed by Human Decidual Macrophages

Tennille Thelen, Yibai Hao, Alexandra I. Medeiros, Jeffrey L. Curtis, Carlos H. Serezani, Lester Kobzik, Lisa H. Harris and David M. Aronoff
J Immunol October 1, 2010, 185 (7) 4328-4335; DOI: https://doi.org/10.4049/jimmunol.1000989
Tennille Thelen
*Molecular, Cellular, and Developmental Biology Graduate Program, Eastern Michigan University, Ypsilanti, MI 48197;
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Yibai Hao
†Division of Infectious Diseases,
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Alexandra I. Medeiros
‡Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine,
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Jeffrey L. Curtis
‡Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine,
§Graduate Program in Immunology, and
¶Pulmonary and Critical Care Medicine Section, Medical Service, Department of Veterans Affairs Care System, Ann Arbor, MI 48105;
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Carlos H. Serezani
‡Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine,
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Lester Kobzik
‖Molecular and Integrative Physiological Sciences Program, Department of Environmental Health, Harvard School of Public Health; and
#Department of Pathology, Brigham and Women's Hospital, Boston, MA 02115
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Lisa H. Harris
**Department of Obstetrics and Gynecology, University of Michigan Health System, Ann Arbor, MI 48109;
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David M. Aronoff
*Molecular, Cellular, and Developmental Biology Graduate Program, Eastern Michigan University, Ypsilanti, MI 48197;
§Graduate Program in Immunology, and
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Abstract

Clostridium sordellii is an emerging pathogen associated with highly lethal female reproductive tract infections following childbirth, abortion, or cervical instrumentation. Gaps in our understanding of the pathogenesis of C. sordellii infections present major challenges to the development of better preventive and therapeutic strategies against this problem. We sought to determine the mechanisms whereby uterine decidual macrophages phagocytose this bacterium and tested the hypothesis that human decidual macrophages use class A scavenger receptors to internalize unopsonized C. sordellii. In vitro phagocytosis assays with human decidual macrophages incubated with pharmacological inhibitors of class A scavenger receptors (fucoidan, polyinosinic acid, and dextran sulfate) revealed a role for these receptors in C. sordellii phagocytosis. Soluble macrophage receptor with collagenous structure (MARCO) receptor prevented C. sordellii internalization, suggesting that MARCO is an important class A scavenger receptor in decidual macrophage phagocytosis of this microbe. Peritoneal macrophages from MARCO-deficient mice, but not wild-type or scavenger receptor AI/II–deficient mice, showed impaired C. sordellii phagocytosis. MARCO-null mice were more susceptible to death from C. sordellii uterine infection than wild-type mice and exhibited impaired clearance of this bacterium from the infected uterus. Thus, MARCO is an important phagocytic receptor used by human and mouse macrophages to clear C. sordellii from the infected uterus.

Footnotes

  • This work was supported by National Institutes of Health Grants HD057176 (to D.M.A.), ES11008 (to L.K.), and HL056309 (to J.L.C.). Support for nonanimal portions of this work was provided by a Doris Duke Charitable Fund Clinical Scientist Development Award (to D.M.A.).

  • Abbreviations used in this paper:

    AcLDL
    acetylated low-density lipoprotein
    CASR
    class A scavenger receptor
    CBSR
    class B scavenger receptor
    ChdSO4
    chondroitan sulfate
    DM
    decidual macrophage
    DxSO4
    dextran sulfate
    KO
    knockout
    MARCO
    macrophage receptor with collagenous structure
    PI
    phagocytic index
    poly(C)
    polycytidylic acid
    poly(I)
    polyinosinic acid
    RFU
    relative fluorescence unit
    SCARA-5
    scavenger receptor A5
    sMARCO
    soluble MARCO
    SR-AI/II
    scavenger receptor AI and AII
    SRCL
    scavenger receptor with C-type lectin
    WT
    wild type.

  • Received March 26, 2010.
  • Accepted July 20, 2010.
  • Copyright © 2010 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 185 (7)
The Journal of Immunology
Vol. 185, Issue 7
1 Oct 2010
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The Class A Scavenger Receptor, Macrophage Receptor with Collagenous Structure, Is the Major Phagocytic Receptor for Clostridium sordellii Expressed by Human Decidual Macrophages
Tennille Thelen, Yibai Hao, Alexandra I. Medeiros, Jeffrey L. Curtis, Carlos H. Serezani, Lester Kobzik, Lisa H. Harris, David M. Aronoff
The Journal of Immunology October 1, 2010, 185 (7) 4328-4335; DOI: 10.4049/jimmunol.1000989

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The Class A Scavenger Receptor, Macrophage Receptor with Collagenous Structure, Is the Major Phagocytic Receptor for Clostridium sordellii Expressed by Human Decidual Macrophages
Tennille Thelen, Yibai Hao, Alexandra I. Medeiros, Jeffrey L. Curtis, Carlos H. Serezani, Lester Kobzik, Lisa H. Harris, David M. Aronoff
The Journal of Immunology October 1, 2010, 185 (7) 4328-4335; DOI: 10.4049/jimmunol.1000989
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