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Coordinated inflammatory responses dictate Marburg virus control by reservoir bats

Author

Listed:
  • Jonathan C. Guito

    (Centers for Disease Control and Prevention)

  • Shannon G. M. Kirejczyk

    (Centers for Disease Control and Prevention
    Emory University
    StageBio)

  • Amy J. Schuh

    (Centers for Disease Control and Prevention)

  • Brian R. Amman

    (Centers for Disease Control and Prevention)

  • Tara K. Sealy

    (Centers for Disease Control and Prevention)

  • James Graziano

    (Centers for Disease Control and Prevention)

  • Jessica R. Spengler

    (Centers for Disease Control and Prevention)

  • Jessica R. Harmon

    (Centers for Disease Control and Prevention)

  • David M. Wozniak

    (Robert Koch Institute
    Bernhard-Nocht-Institute for Tropical Medicine)

  • Joseph B. Prescott

    (Centers for Disease Control and Prevention
    Robert Koch Institute)

  • Jonathan S. Towner

    (Centers for Disease Control and Prevention)

Abstract

Bats are increasingly recognized as reservoirs of emerging zoonotic pathogens. Egyptian rousette bats (ERBs) are the known reservoir of Marburg virus (MARV), a filovirus that causes deadly Marburg virus disease (MVD) in humans. However, ERBs harbor MARV asymptomatically, likely due to a coadapted and specific host immunity-pathogen relationship. Recently, we measured transcriptional responses in MARV-infected ERB whole tissues, showing that these bats possess a disease tolerant strategy that limits pro-inflammatory gene induction, presumably averting MVD-linked immunopathology. However, the host resistant strategy by which ERBs actively limit MARV burden remains elusive, which we hypothesize requires localized inflammatory responses unresolvable at bulk-tissue scale. Here, we use dexamethasone to attenuate ERB pro-inflammatory responses and assess MARV replication, shedding and disease. We show that MARV-infected ERBs naturally mount coordinated pro-inflammatory responses at liver foci of infection, comprised of recruited mononuclear phagocytes and T cells, the latter of which proliferate with likely MARV-specificity. When pro-inflammatory responses are diminished, ERBs display heightened MARV replication, oral/rectal shedding and severe MVD-like liver pathology, demonstrating that ERBs balance immunoprotective tolerance with discreet MARV-resistant pro-inflammatory responses. These data further suggest that natural ERB immunomodulatory stressors like food scarcity and habitat disruption may potentiate viral shedding, transmission and therefore outbreak risk.

Suggested Citation

  • Jonathan C. Guito & Shannon G. M. Kirejczyk & Amy J. Schuh & Brian R. Amman & Tara K. Sealy & James Graziano & Jessica R. Spengler & Jessica R. Harmon & David M. Wozniak & Joseph B. Prescott & Jonatha, 2024. "Coordinated inflammatory responses dictate Marburg virus control by reservoir bats," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46226-7
    DOI: 10.1038/s41467-024-46226-7
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    References listed on IDEAS

    as
    1. Aaron T. Irving & Matae Ahn & Geraldine Goh & Danielle E. Anderson & Lin-Fa Wang, 2021. "Lessons from the host defences of bats, a unique viral reservoir," Nature, Nature, vol. 589(7842), pages 363-370, January.
    2. Brian R. Amman & Brian H. Bird & Ibrahim A. Bakarr & James Bangura & Amy J. Schuh & Jonathan Johnny & Tara K. Sealy & Immah Conteh & Alusine H. Koroma & Ibrahim Foday & Emmanuel Amara & Abdulai A. Ban, 2020. "Isolation of Angola-like Marburg virus from Egyptian rousette bats from West Africa," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
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