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Translocated Legionella pneumophila small RNAs mimic eukaryotic microRNAs targeting the host immune response

Author

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  • Tobias Sahr

    (Institut Pasteur, Université de Paris, Biologie des Bactéries Intracellulaires and CNRS UMR 6047)

  • Pedro Escoll

    (Institut Pasteur, Université de Paris, Biologie des Bactéries Intracellulaires and CNRS UMR 6047)

  • Christophe Rusniok

    (Institut Pasteur, Université de Paris, Biologie des Bactéries Intracellulaires and CNRS UMR 6047)

  • Sheryl Bui

    (Université de Paris, INSERM ERL U1316, UMR 7057/CNRS)

  • Gérard Pehau-Arnaudet

    (Unité de Technologie et Service BioImagerie Ultrastructurale and CNRS UMR 3528)

  • Gregory Lavieu

    (Université de Paris, INSERM ERL U1316, UMR 7057/CNRS)

  • Carmen Buchrieser

    (Institut Pasteur, Université de Paris, Biologie des Bactéries Intracellulaires and CNRS UMR 6047)

Abstract

Legionella pneumophila is an intracellular bacterial pathogen that can cause a severe form of pneumonia in humans, a phenotype evolved through interactions with aquatic protozoa in the environment. Here, we show that L. pneumophila uses extracellular vesicles to translocate bacterial small RNAs (sRNAs) into host cells that act on host defence signalling pathways. The bacterial sRNA RsmY binds to the UTR of ddx58 (RIG-I encoding gene) and cRel, while tRNA-Phe binds ddx58 and irak1 collectively reducing expression of RIG-I, IRAK1 and cRel, with subsequent downregulation of IFN-β. Thus, RsmY and tRNA-Phe are bacterial trans-kingdom regulatory RNAs downregulating selected sensor and regulator proteins of the host cell innate immune response. This miRNA-like regulation of the expression of key sensors and regulators of immunity is a feature of L. pneumophila host-pathogen communication and likely represents a general mechanism employed by bacteria that interact with eukaryotic hosts.

Suggested Citation

  • Tobias Sahr & Pedro Escoll & Christophe Rusniok & Sheryl Bui & Gérard Pehau-Arnaudet & Gregory Lavieu & Carmen Buchrieser, 2022. "Translocated Legionella pneumophila small RNAs mimic eukaryotic microRNAs targeting the host immune response," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28454-x
    DOI: 10.1038/s41467-022-28454-x
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    References listed on IDEAS

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    1. Emeline Bonsergent & Eleonora Grisard & Julian Buchrieser & Olivier Schwartz & Clotilde Théry & Grégory Lavieu, 2021. "Quantitative characterization of extracellular vesicle uptake and content delivery within mammalian cells," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    2. Shaeri Mukherjee & Xiaoyun Liu & Kohei Arasaki & Justin McDonough & Jorge E. Galán & Craig R. Roy, 2011. "Modulation of Rab GTPase function by a protein phosphocholine transferase," Nature, Nature, vol. 477(7362), pages 103-106, September.
    3. Yunhao Tan & Zhao-Qing Luo, 2011. "Legionella pneumophila SidD is a deAMPylase that modifies Rab1," Nature, Nature, vol. 475(7357), pages 506-509, July.
    4. Anna Lena Jung & Cornelia Stoiber & Christina E Herkt & Christine Schulz & Wilhelm Bertrams & Bernd Schmeck, 2016. "Legionella pneumophila-Derived Outer Membrane Vesicles Promote Bacterial Replication in Macrophages," PLOS Pathogens, Public Library of Science, vol. 12(4), pages 1-26, April.
    5. Alyssa Ingmundson & Anna Delprato & David G. Lambright & Craig R. Roy, 2007. "Legionella pneumophila proteins that regulate Rab1 membrane cycling," Nature, Nature, vol. 450(7168), pages 365-369, November.
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    Cited by:

    1. Rahul Sharma & Michael Adams & Simonne Griffith-Jones & Tobias Sahr & Laura Gomez-Valero & Felix Weis & Michael Hons & Sarah Gharbi & Rayene Berkane & Alexandra Stolz & Carmen Buchrieser & Sagar Bhoga, 2023. "Structural basis for the toxicity of Legionella pneumophila effector SidH," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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