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Bridging of host-microbiota tryptophan partitioning by the serotonin pathway in fungal pneumonia

Author

Listed:
  • Giorgia Renga

    (University of Perugia)

  • Fiorella D’Onofrio

    (University of Perugia)

  • Marilena Pariano

    (University of Perugia)

  • Roberta Galarini

    (Istituto Zooprofilattico Sperimentale dell’Umbria e delle Marche “Togo Rosati,”)

  • Carolina Barola

    (Istituto Zooprofilattico Sperimentale dell’Umbria e delle Marche “Togo Rosati,”)

  • Claudia Stincardini

    (University of Perugia)

  • Marina M. Bellet

    (University of Perugia)

  • Helmut Ellemunter

    (CF Centre, Medical University Innsbruck)

  • Cornelia Lass-Flörl

    (Innsbruck Medical University)

  • Claudio Costantini

    (University of Perugia)

  • Valerio Napolioni

    (University of Camerino)

  • Allison K. Ehrlich

    (University of California)

  • Cinzia Antognelli

    (University of Perugia)

  • Massimo Fini

    (University San Raffaele and Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele)

  • Enrico Garaci

    (University San Raffaele and Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele)

  • Emilia Nunzi

    (University of Perugia)

  • Luigina Romani

    (University of Perugia
    University San Raffaele and Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele)

Abstract

The aromatic amino acid L-tryptophan (Trp) is essentially metabolized along the host and microbial pathways. While much is known about the role played by downstream metabolites of each pathways in intestinal homeostasis, their role in lung immune homeostasis is underappreciated. Here we have examined the role played by the Trp hydroxylase/5-hydroxytryptamine (5-HT) pathway in calibrating host and microbial Trp metabolism during Aspergillus fumigatus pneumonia. We found that 5-HT produced by mast cells essentially contributed to pathogen clearance and immune homeostasis in infection by promoting the host protective indoleamine-2,3-dioxygenase 1/kynurenine pathway and limiting the microbial activation of the indole/aryl hydrocarbon receptor pathway. This occurred via regulation of lung and intestinal microbiota and signaling pathways. 5-HT was deficient in the sputa of patients with Cystic fibrosis, while 5-HT supplementation restored the dysregulated Trp partitioning in murine disease. These findings suggest that 5-HT, by bridging host-microbiota Trp partitioning, may have clinical effects beyond its mood regulatory function in respiratory pathologies with an inflammatory component.

Suggested Citation

  • Giorgia Renga & Fiorella D’Onofrio & Marilena Pariano & Roberta Galarini & Carolina Barola & Claudia Stincardini & Marina M. Bellet & Helmut Ellemunter & Cornelia Lass-Flörl & Claudio Costantini & Val, 2023. "Bridging of host-microbiota tryptophan partitioning by the serotonin pathway in fungal pneumonia," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41536-8
    DOI: 10.1038/s41467-023-41536-8
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    References listed on IDEAS

    as
    1. Li-Fan Lu & Evan F. Lind & David C. Gondek & Kathy A. Bennett & Michael W. Gleeson & Karina Pino-Lagos & Zachary A. Scott & Anthony J. Coyle & Jennifer L. Reed & Jacques Van Snick & Terry B. Strom & X, 2006. "Mast cells are essential intermediaries in regulatory T-cell tolerance," Nature, Nature, vol. 442(7106), pages 997-1002, August.
    2. Henrik M. Roager & Tine R. Licht, 2018. "Microbial tryptophan catabolites in health and disease," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
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