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Epithelial cells maintain memory of prior infection with Streptococcus pneumoniae through di-methylation of histone H3

Author

Listed:
  • Christine Chevalier

    (Université Paris Cité, Chromatin and Infection Laboratory)

  • Claudia Chica

    (Université Paris Cité, Bioinformatics and Biostatistics Hub)

  • Justine Matheau

    (Université Paris Cité, Chromatin and Infection Laboratory
    Université Paris Cité)

  • Adrien Pain

    (Université Paris Cité, Bioinformatics and Biostatistics Hub)

  • Michael G. Connor

    (Université Paris Cité, Chromatin and Infection Laboratory)

  • Melanie A. Hamon

    (Université Paris Cité, Chromatin and Infection Laboratory)

Abstract

Epithelial cells are the first point of contact for bacteria entering the respiratory tract. Streptococcus pneumoniae is an obligate human pathobiont of the nasal mucosa, carried asymptomatically but also the cause of severe pneumoniae. The role of the epithelium in maintaining homeostatic interactions or mounting an inflammatory response to invasive S. pneumoniae is currently poorly understood. However, studies have shown that chromatin modifications, at the histone level, induced by bacterial pathogens interfere with the host transcriptional program and promote infection. Here, we uncover a histone modification induced by S. pneumoniae infection maintained for at least 9 days upon clearance of bacteria with antibiotics. Di-methylation of histone H3 on lysine 4 (H3K4me2) is induced in an active manner by bacterial attachment to host cells. We show that infection establishes a unique epigenetic program affecting the transcriptional response of epithelial cells, rendering them more permissive upon secondary infection. Our results establish H3K4me2 as a unique modification induced by infection, distinct from H3K4me3 or me1, which localizes to enhancer regions genome-wide. Therefore, this study reveals evidence that bacterial infection leaves a memory in epithelial cells after bacterial clearance, in an epigenomic mark, thereby altering cellular responses to subsequent infections and promoting infection.

Suggested Citation

  • Christine Chevalier & Claudia Chica & Justine Matheau & Adrien Pain & Michael G. Connor & Melanie A. Hamon, 2024. "Epithelial cells maintain memory of prior infection with Streptococcus pneumoniae through di-methylation of histone H3," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49347-1
    DOI: 10.1038/s41467-024-49347-1
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    References listed on IDEAS

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    2. Shruti Naik & Samantha B. Larsen & Nicholas C. Gomez & Kirill Alaverdyan & Ataman Sendoel & Shaopeng Yuan & Lisa Polak & Anita Kulukian & Sophia Chai & Elaine Fuchs, 2017. "Inflammatory memory sensitizes skin epithelial stem cells to tissue damage," Nature, Nature, vol. 550(7677), pages 475-480, October.
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