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Brucella abortus impairs T lymphocyte responsiveness by mobilizing IL-1RA-secreting omental neutrophils

Author

Listed:
  • Joaquin M. Pellegrini

    (CIML)

  • Gabriela González-Espinoza

    (CIML)

  • Raheleh R. Shayan

    (CIML)

  • Lisiena Hysenaj

    (CIML)

  • Thomas Rouma

    (University of Namur
    Université Libre de Bruxelles)

  • Vilma Arce-Gorvel

    (CIML)

  • Hugues Lelouard

    (CIML)

  • Dimitri Popoff

    (CIML)

  • Yun Zhao

    (CIML)

  • Sean Hanniffy

    (CIML)

  • Amanda Castillo-Zeledón

    (Escuela de Medicina Veterinaria)

  • Maite Loperena-Barber

    (Instituto de Salud Tropical e Departamento de Microbiología y Parasitología)

  • Javier Celis-Gutierrez

    (CIML)

  • Cyrille Mionnet

    (CIML)

  • Mile Bosilkovski

    (University Clinic for Infectious Diseases and Febrile Conditions)

  • Javier Solera

    (Universidad Castilla la Mancha Albacete)

  • Eric Muraille

    (University of Namur
    Université Libre de Bruxelles)

  • Elías Barquero-Calvo

    (Escuela de Medicina Veterinaria)

  • Edgardo Moreno

    (Escuela de Medicina Veterinaria)

  • Raquel Conde-Álvarez

    (Instituto de Salud Tropical e Departamento de Microbiología y Parasitología)

  • Ignacio Moriyón

    (Instituto de Salud Tropical e Departamento de Microbiología y Parasitología)

  • Jean-Pierre Gorvel

    (CIML)

  • Sylvie Mémet

    (CIML)

Abstract

Immune evasion strategies of Brucella, the etiologic agent of brucellosis, a global zoonosis, remain partially understood. The omentum, a tertiary lymphoid organ part of visceral adipose tissue, has never been explored as a Brucella reservoir. We report that B. abortus infects and replicates within murine omental macrophages. Throughout the chronic phase of infection, the omentum accumulates macrophages, monocytes and neutrophils. The maintenance of PD-L1+Sca-1+ macrophages, monocytes and neutrophils in the omentum depends on the wadC-encoded determinant of Brucella LPS. We demonstrate that PD-L1+Sca-1+ murine omental neutrophils produce high levels of IL-1RA leading to T cell hyporesponsiveness. These findings corroborate brucellosis patient analysis of whole blood displaying upregulation of PDL1 and Ly6E genes, and of serum exhibiting high levels of IL-1RA. Overall, the omentum, a reservoir for B. abortus, promotes bacterial persistence and causes CD4+ and CD8+ T cell immunosuppression by IL-1RA secreted by PD-L1+Sca-1+ neutrophils.

Suggested Citation

  • Joaquin M. Pellegrini & Gabriela González-Espinoza & Raheleh R. Shayan & Lisiena Hysenaj & Thomas Rouma & Vilma Arce-Gorvel & Hugues Lelouard & Dimitri Popoff & Yun Zhao & Sean Hanniffy & Amanda Casti, 2025. "Brucella abortus impairs T lymphocyte responsiveness by mobilizing IL-1RA-secreting omental neutrophils," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-024-55799-2
    DOI: 10.1038/s41467-024-55799-2
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    References listed on IDEAS

    as
    1. Kaitao Li & Zhou Yuan & Jintian Lyu & Eunseon Ahn & Simon J. Davis & Rafi Ahmed & Cheng Zhu, 2021. "PD-1 suppresses TCR-CD8 cooperativity during T-cell antigen recognition," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    2. Konrad Buscher & Huiyu Wang & Xueli Zhang & Paul Striewski & Benedikt Wirth & Gurpanna Saggu & Stefan Lütke-Enking & Tanya N. Mayadas & Klaus Ley & Lydia Sorokin & Jian Song, 2016. "Protection from septic peritonitis by rapid neutrophil recruitment through omental high endothelial venules," Nature Communications, Nature, vol. 7(1), pages 1-7, April.
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