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Brucella effectors NyxA and NyxB target SENP3 to modulate the subcellular localisation of nucleolar proteins

Author

Listed:
  • Arthur Louche

    (Université de Lyon)

  • Amandine Blanco

    (Université de Lyon)

  • Thais Lourdes Santos Lacerda

    (Université de Lyon)

  • Lison Cancade-Veyre

    (Université de Lyon)

  • Claire Lionnet

    (Université de Lyon, ENS de Lyon, UCBL, INRA, CNRS)

  • Célia Bergé

    (Université de Lyon)

  • Monica Rolando

    (Biologie des Bactéries Intracellulaires)

  • Frédérique Lembo

    (Centre de Recherche en Cancérologie de Marseille (CRCM))

  • Jean-Paul Borg

    (Centre de Recherche en Cancérologie de Marseille (CRCM)
    Institut Universitaire de France)

  • Carmen Buchrieser

    (Biologie des Bactéries Intracellulaires)

  • Masami Nagahama

    (Meiji Pharmaceutical University)

  • Francine C. A. Gérard

    (Université de Lyon)

  • Jean-Pierre Gorvel

    (CIML)

  • Virginie Gueguen-Chaignon

    (ENS de Lyon)

  • Laurent Terradot

    (Université de Lyon)

  • Suzana P. Salcedo

    (Université de Lyon)

Abstract

The cell nucleus is a primary target for intracellular bacterial pathogens to counteract immune responses and hijack host signalling pathways to cause disease. Here we identify two Brucella abortus effectors, NyxA and NyxB, that interfere with host protease SENP3, and this facilitates intracellular replication of the pathogen. The translocated Nyx effectors directly interact with SENP3 via a defined acidic patch (identified from the crystal structure of NyxB), preventing nucleolar localisation of SENP3 at late stages of infection. By sequestering SENP3, the effectors promote cytoplasmic accumulation of nucleolar AAA-ATPase NVL and ribosomal protein L5 (RPL5) in effector-enriched structures in the vicinity of replicating bacteria. The shuttling of ribosomal biogenesis-associated nucleolar proteins is inhibited by SENP3 and requires the autophagy-initiation protein Beclin1 and the SUMO-E3 ligase PIAS3. Our results highlight a nucleomodulatory function of two Brucella effectors and reveal that SENP3 is a crucial regulator of the subcellular localisation of nucleolar proteins during Brucella infection, promoting intracellular replication of the pathogen.

Suggested Citation

  • Arthur Louche & Amandine Blanco & Thais Lourdes Santos Lacerda & Lison Cancade-Veyre & Claire Lionnet & Célia Bergé & Monica Rolando & Frédérique Lembo & Jean-Paul Borg & Carmen Buchrieser & Masami Na, 2023. "Brucella effectors NyxA and NyxB target SENP3 to modulate the subcellular localisation of nucleolar proteins," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-022-35763-8
    DOI: 10.1038/s41467-022-35763-8
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    References listed on IDEAS

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    1. Heeseon An & Alban Ordureau & Maria Körner & Joao A. Paulo & J. Wade Harper, 2020. "Systematic quantitative analysis of ribosome inventory during nutrient stress," Nature, Nature, vol. 583(7815), pages 303-309, July.
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