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Cellular Microbiology: Pathogen-Host Cell Molecular Interactions

Brucella abortus and Pregnancy in Mice: Impact of Chronic Infection on Fertility and the Role of Regulatory T Cells in Tissue Colonization

Shakirat A. Adetunji, Denise L. Faustman, L. Garry Adams, Daniel G. Garcia-Gonzalez, Martha E. Hensel, Omar H. Khalaf, Angela M. Arenas-Gamboa
Craig R. Roy, Editor
Shakirat A. Adetunji
aDepartment of Veterinary Pathobiology, Texas A&M University, College Station, Texas, USA
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  • ORCID record for Shakirat A. Adetunji
Denise L. Faustman
bMassachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, USA
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L. Garry Adams
aDepartment of Veterinary Pathobiology, Texas A&M University, College Station, Texas, USA
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Daniel G. Garcia-Gonzalez
aDepartment of Veterinary Pathobiology, Texas A&M University, College Station, Texas, USA
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Martha E. Hensel
aDepartment of Veterinary Pathobiology, Texas A&M University, College Station, Texas, USA
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Omar H. Khalaf
aDepartment of Veterinary Pathobiology, Texas A&M University, College Station, Texas, USA
cDepartment of Veterinary Pathology & Poultry Diseases, College of Veterinary Medicine, University of Baghdad, Baghdad, Iraq
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Angela M. Arenas-Gamboa
aDepartment of Veterinary Pathobiology, Texas A&M University, College Station, Texas, USA
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Craig R. Roy
Yale University School of Medicine
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DOI: 10.1128/IAI.00257-20
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ABSTRACT

Stealthy intracellular bacterial pathogens are known to establish persistent and sometimes lifelong infections. Some of these pathogens also have a tropism for the reproductive system, thereby increasing the risk of reproductive disease and infertility. To date, the pathogenic mechanism involved remains poorly understood. Here, we demonstrate that Brucella abortus, a notorious reproductive pathogen, has the ability to infect the nonpregnant uterus, sustain infection, and induce inflammatory changes during both acute and chronic stages of infection. In addition, we demonstrated that chronically infected mice had a significantly reduced number of pregnancies compared to naive controls. To investigate the immunologic mechanism responsible for uterine tropism, we explored the role of regulatory T cells (Tregs) in the pathogenesis of Brucella abortus infection. We show that highly suppressive CD4+FOXP3+TNFR2+ Tregs contribute to the persistence of Brucella abortus infection and that inactivation of Tregs with tumor necrosis factor receptor II (TNFR2) antagonistic antibody protected mice by significantly reducing bacterial burden both systemically and within reproductive tissues. These findings support a critical role of Tregs in the pathogenesis of persistence induced by intracellular bacterial pathogens, including B. abortus. Results from this study indicate that adverse reproductive outcomes can occur as sequelae of chronic infection in nonpregnant animals and that fine-tuning Treg activity may provide novel immunotherapeutic and prevention strategies against intracellular bacterial infections such as brucellosis.

FOOTNOTES

    • Received 25 April 2020.
    • Returned for modification 15 June 2020.
    • Accepted 10 July 2020.
    • Accepted manuscript posted online 20 July 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

All Rights Reserved.

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Brucella abortus and Pregnancy in Mice: Impact of Chronic Infection on Fertility and the Role of Regulatory T Cells in Tissue Colonization
Shakirat A. Adetunji, Denise L. Faustman, L. Garry Adams, Daniel G. Garcia-Gonzalez, Martha E. Hensel, Omar H. Khalaf, Angela M. Arenas-Gamboa
Infection and Immunity Sep 2020, 88 (10) e00257-20; DOI: 10.1128/IAI.00257-20

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Brucella abortus and Pregnancy in Mice: Impact of Chronic Infection on Fertility and the Role of Regulatory T Cells in Tissue Colonization
Shakirat A. Adetunji, Denise L. Faustman, L. Garry Adams, Daniel G. Garcia-Gonzalez, Martha E. Hensel, Omar H. Khalaf, Angela M. Arenas-Gamboa
Infection and Immunity Sep 2020, 88 (10) e00257-20; DOI: 10.1128/IAI.00257-20
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KEYWORDS

antagonism
antibody
Brucella
regulatory T cells
TNFR2
tropism

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