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Host-pathogen interactions in the Plasmodium-infected mouse liver at spatial and single-cell resolution

Author

Listed:
  • Franziska Hildebrandt

    (SE-106 91)

  • Miren Urrutia Iturritza

    (SE-106 91)

  • Christian Zwicker

    (Ghent University
    Technologiepark-Zwijnaarde 71)

  • Bavo Vanneste

    (Ghent University
    Technologiepark-Zwijnaarde 71
    Technologiepark-Zwijnaarde 71)

  • Noémi Van Hul

    (SE-171 77)

  • Elisa Semle

    (SE-106 91)

  • Jaclyn Quin

    (SE-106 91)

  • Tales Pascini

    (Rm 2E20A)

  • Sami Saarenpää

    (KTH Royal Institute of Technology)

  • Mengxiao He

    (KTH Royal Institute of Technology)

  • Emma R. Andersson

    (SE-171 77)

  • Charlotte L. Scott

    (Ghent University
    Technologiepark-Zwijnaarde 71)

  • Joel Vega-Rodriguez

    (Rm 2E20A)

  • Joakim Lundeberg

    (KTH Royal Institute of Technology)

  • Johan Ankarklev

    (SE-106 91)

Abstract

Upon infecting its vertebrate host, the malaria parasite initially invades the liver where it undergoes massive replication, whilst remaining clinically silent. The coordination of host responses across the complex liver tissue during malaria infection remains unexplored. Here, we perform spatial transcriptomics in combination with single-nuclei RNA sequencing over multiple time points to delineate host-pathogen interactions across Plasmodium berghei-infected liver tissues. Our data reveals significant changes in spatial gene expression in the malaria-infected tissues. These include changes related to lipid metabolism in the proximity to sites of Plasmodium infection, distinct inflammation programs between lobular zones, and regions with enrichment of different inflammatory cells, which we term ‘inflammatory hotspots’. We also observe significant upregulation of genes involved in inflammation in the control liver tissues of mice injected with mosquito salivary gland components. However, this response is considerably delayed compared to that observed in P. berghei-infected mice. Our study establishes a benchmark for investigating transcriptome changes during host-parasite interactions in tissues, it provides informative insights regarding in vivo study design linked to infection and offers a useful tool for the discovery and validation of de novo intervention strategies aimed at malaria liver stage infection.

Suggested Citation

  • Franziska Hildebrandt & Miren Urrutia Iturritza & Christian Zwicker & Bavo Vanneste & Noémi Van Hul & Elisa Semle & Jaclyn Quin & Tales Pascini & Sami Saarenpää & Mengxiao He & Emma R. Andersson & Cha, 2024. "Host-pathogen interactions in the Plasmodium-infected mouse liver at spatial and single-cell resolution," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51418-2
    DOI: 10.1038/s41467-024-51418-2
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    as
    1. Franziska Hildebrandt & Miren Urrutia Iturritza & Christian Zwicker & Bavo Vanneste & Noémi Van Hul & Elisa Semle & Jaclyn Quin & Tales Pascini & Sami Saarenpää & Mengxiao He & Emma R. Andersson & Cha, 2024. "Host-pathogen interactions in the Plasmodium-infected mouse liver at spatial and single-cell resolution," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Amichay Afriat & Vanessa Zuzarte-Luís & Keren Bahar Halpern & Lisa Buchauer & Sofia Marques & Ângelo Ferreira Chora & Aparajita Lahree & Ido Amit & Maria M. Mota & Shalev Itzkovitz, 2022. "A spatiotemporally resolved single-cell atlas of the Plasmodium liver stage," Nature, Nature, vol. 611(7936), pages 563-569, November.
    3. Franziska Hildebrandt & Alma Andersson & Sami Saarenpää & Ludvig Larsson & Noémi Van Hul & Sachie Kanatani & Jan Masek & Ewa Ellis & Antonio Barragan & Annelie Mollbrink & Emma R. Andersson & Joakim L, 2021. "Spatial Transcriptomics to define transcriptional patterns of zonation and structural components in the mouse liver," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
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    Cited by:

    1. Franziska Hildebrandt & Miren Urrutia Iturritza & Christian Zwicker & Bavo Vanneste & Noémi Van Hul & Elisa Semle & Jaclyn Quin & Tales Pascini & Sami Saarenpää & Mengxiao He & Emma R. Andersson & Cha, 2024. "Host-pathogen interactions in the Plasmodium-infected mouse liver at spatial and single-cell resolution," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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