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IL-1α Is Essential for Oviduct Pathology during Genital Chlamydial Infection in Mice

Clare E. Gyorke, Avinash Kollipara, John Allen IV, Yugen Zhang, J. Ashley Ezzell, Toni Darville, Stephanie A. Montgomery and Uma M. Nagarajan
J Immunol December 1, 2020, 205 (11) 3037-3049; DOI: https://doi.org/10.4049/jimmunol.2000600
Clare E. Gyorke
*Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599;
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Avinash Kollipara
*Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599;
†Department of Pediatrics, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599;
‡Department of Pathology and Laboratory Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599;
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John Allen IV
†Department of Pediatrics, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599;
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Yugen Zhang
†Department of Pediatrics, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599;
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J. Ashley Ezzell
§Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599; and
¶Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599
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Toni Darville
*Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599;
†Department of Pediatrics, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599;
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Stephanie A. Montgomery
‡Department of Pathology and Laboratory Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599;
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Uma M. Nagarajan
*Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599;
†Department of Pediatrics, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599;
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Key Points

  • IL-1α drives oviduct pathology during genital Chlamydia infection in mice.

  • IL-1α promotes neutrophil recruitment to the genital tract.

  • Infection increases IL-1α expression in genital tract epithelial cells.

Abstract

Chlamydia trachomatis infection of the female genital tract can lead to irreversible fallopian tube scarring. In the mouse model of genital infection using Chlamydia muridarum, IL-1R signaling plays a critical role in oviduct tissue damage. In this study, we investigated the pathologic role of IL-1α, one of the two proinflammatory cytokines that bind to IL-1R. Il1a−/− mice infected with C. muridarum cleared infection at their cervix at the same rate as wild-type (WT) mice, but were significantly protected from end point oviduct damage and fibrosis. The contribution of IL-1α to oviduct pathology was more dramatic than observed in mice deficient for IL-1β. Although chlamydial burden was similar in WT and Il1a−/− oviduct during peak days of infection, levels of IL-1β, IL-6, CSF3, and CXCL2 were reduced in Il1a−/− oviduct lysates. During infection, Il1a−/− oviducts and uterine horns exhibited reduced neutrophil infiltration, and this reduction persisted after the infection resolved. The absence of IL-1α did not compromise CD4 T cell recruitment or function during primary or secondary chlamydial infection. IL-1α is expressed predominantly by luminal cells of the genital tract in response to infection, and low levels of expression persisted after the infection cleared. Ab-mediated depletion of IL-1α in WT mice prevented infection-induced oviduct damage, further supporting a key role for IL-1α in oviduct pathology.

Footnotes

  • This work was supported by National Institutes of Health (NIH), National Institute of Allergy and Infectious Diseases Grants AI067678 to U.M.N. and AI007001 to C.E.G., and was partly supported by University of North Carolina (UNC) North Carolina Translational and Clinical Sciences Institute Grant UL1TR002489 and a UNC-Boost Award to U.M.N. This study used the UNC Translational Pathology Laboratory, which is supported in part by grants from the National Cancer Institute (5P30CA016086-42), the NIH (U54-CA156733), the National Institute of Environmental Health Sciences (5 P30 ES010126-17), the University Cancer Research Fund, and the North Carolina Birding Trail (2015-IDG-1007), and the UNC Flow Cytometry Core Facility, which is supported in part by a P30 CA016086 Cancer Center Core Support Grant to the UNC Lineberger Comprehensive Cancer Center. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

  • The online version of this article contains supplemental material.

  • Abbreviations used in this article:

    d.p.i.
    day postinfection
    IFU
    inclusion forming unit
    SPG
    sucrose–sodium phosphate–glutamic acid
    UNC-CH
    University of North Carolina at Chapel Hill
    WT
    wild-type.

  • Received May 26, 2020.
  • Accepted September 22, 2020.
  • Copyright © 2020 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 205 (11)
The Journal of Immunology
Vol. 205, Issue 11
1 Dec 2020
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IL-1α Is Essential for Oviduct Pathology during Genital Chlamydial Infection in Mice
Clare E. Gyorke, Avinash Kollipara, John Allen, Yugen Zhang, J. Ashley Ezzell, Toni Darville, Stephanie A. Montgomery, Uma M. Nagarajan
The Journal of Immunology December 1, 2020, 205 (11) 3037-3049; DOI: 10.4049/jimmunol.2000600

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IL-1α Is Essential for Oviduct Pathology during Genital Chlamydial Infection in Mice
Clare E. Gyorke, Avinash Kollipara, John Allen, Yugen Zhang, J. Ashley Ezzell, Toni Darville, Stephanie A. Montgomery, Uma M. Nagarajan
The Journal of Immunology December 1, 2020, 205 (11) 3037-3049; DOI: 10.4049/jimmunol.2000600
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