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

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 Castillo-Zeledón, Maite Loperena-Barber, Javier Celis-Gutierrez, Cyrille Mionnet, Mile Bosilkovski, Javier Solera, Eric Muraille, Elías Barquero-Calvo, Edgardo Moreno, Raquel Conde-Álvarez, Ignacio Moriyón, Jean-Pierre Gorvel and Sylvie Mémet ()
Additional contact information
Joaquin M. Pellegrini: CIML
Gabriela González-Espinoza: CIML
Raheleh R. Shayan: CIML
Lisiena Hysenaj: CIML
Thomas Rouma: University of Namur
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
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

Nature Communications, 2025, vol. 16, issue 1, 1-16

Abstract: 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.

Date: 2025
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DOI: 10.1038/s41467-024-55799-2

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