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Single-cell multi-ome and immune profiles of the Inspiration4 crew reveal conserved, cell-type, and sex-specific responses to spaceflight

Author

Listed:
  • JangKeun Kim

    (Weill Cornell Medicine
    Weill Cornell Medicine)

  • Braden T. Tierney

    (Weill Cornell Medicine
    Weill Cornell Medicine)

  • Eliah G. Overbey

    (Weill Cornell Medicine
    Weill Cornell Medicine
    University of Austin
    BioAstra, Inc)

  • Ezequiel Dantas

    (Weill Cornell Medicine
    Weill Cornell Medicine)

  • Matias Fuentealba

    (Buck Institute for Research on Aging)

  • Jiwoon Park

    (Weill Cornell Medicine
    Weill Cornell Medicine)

  • S. Anand Narayanan

    (Florida State University)

  • Fei Wu

    (Buck Institute for Research on Aging)

  • Deena Najjar

    (Weill Cornell Medicine)

  • Christopher R. Chin

    (Weill Cornell Medicine
    Weill Cornell Medicine)

  • Cem Meydan

    (Weill Cornell Medicine
    Weill Cornell Medicine
    Weill Cornell Medicine)

  • Conor Loy

    (Meinig School of Biomedical Engineering)

  • Begum Mathyk

    (University of South Florida Morsani College of Medicine)

  • Remi Klotz

    (University of Southern California)

  • Veronica Ortiz

    (University of Southern California)

  • Khiem Nguyen

    (Buck Institute for Research on Aging)

  • Krista A. Ryon

    (Weill Cornell Medicine)

  • Namita Damle

    (Weill Cornell Medicine)

  • Nadia Houerbi

    (Weill Cornell Medicine
    Weill Cornell Medicine)

  • Laura I. Patras

    (Weill Cornell Medicine
    Babes-Bolyai University)

  • Nathan Schanzer

    (New York Medical College)

  • Gwyneth A. Hutchinson

    (NASA Center for the Utilization of Biological Engineering in Space (CUBES)
    University of California, Berkeley
    University of California, San Francisco)

  • Jonathan Foox

    (Weill Cornell Medicine
    Weill Cornell Medicine)

  • Chandrima Bhattacharya

    (Weill Cornell Medicine
    Weill Cornell Medicine)

  • Matthew Mackay

    (Weill Cornell Medicine)

  • Evan E. Afshin

    (Weill Cornell Medicine
    Weill Cornell Medicine)

  • Jeremy Wain Hirschberg

    (Weill Cornell Medicine
    Weill Cornell Medicine)

  • Ashley S. Kleinman

    (Weill Cornell Medicine
    Weill Cornell Medicine)

  • Julian C. Schmidt

    (Sovaris Aerospace
    Advanced Pattern Analysis & Human Performance Group)

  • Caleb M. Schmidt

    (Sovaris Aerospace
    Advanced Pattern Analysis & Human Performance Group
    Colorado State University)

  • Michael A. Schmidt

    (Sovaris Aerospace
    Advanced Pattern Analysis & Human Performance Group)

  • Afshin Beheshti

    (Broad Institute of MIT and Harvard
    NASA Ames Research Center)

  • Irina Matei

    (Weill Cornell Medicine
    Weill Cornell Medicine)

  • David Lyden

    (Weill Cornell Medicine
    Weill Cornell Medicine)

  • Sean Mullane

    (Space Exploration Technologies Corporation (SpaceX))

  • Amran Asadi

    (Space Exploration Technologies Corporation (SpaceX))

  • Joan S. Lenz

    (Meinig School of Biomedical Engineering)

  • Omary Mzava

    (Meinig School of Biomedical Engineering)

  • Min Yu

    (University of Southern California)

  • Saravanan Ganesan

    (Weill Cornell Medicine
    Weill Cornell Medicine)

  • Iwijn Vlaminck

    (Meinig School of Biomedical Engineering)

  • Ari M. Melnick

    (Weill Cornell Medicine
    Weill Cornell Medicine)

  • Darko Barisic

    (Weill Cornell Medicine
    Weill Cornell Medicine)

  • Daniel A. Winer

    (Buck Institute for Research on Aging
    University of Southern California
    University of Toronto
    University Health Network)

  • Sara R. Zwart

    (University of Texas Medical Branch)

  • Brian E. Crucian

    (NASA Johnson Space Center, Human Health and Performance Directorate)

  • Scott M. Smith

    (NASA Johnson Space Center, Human Health and Performance Directorate)

  • Jaime Mateus

    (NASA Ames Research Center)

  • David Furman

    (Buck Institute for Research on Aging
    Stanford School of Medicine
    CONICET)

  • Christopher E. Mason

    (Weill Cornell Medicine
    Weill Cornell Medicine
    Weill Cornell Medicine
    Weill Cornell Medicine)

Abstract

Spaceflight induces an immune response in astronauts. To better characterize this effect, we generated single-cell, multi-ome, cell-free RNA (cfRNA), biochemical, and hematology data for the SpaceX Inspiration4 (I4) mission crew. We found that 18 cytokines/chemokines related to inflammation, aging, and muscle homeostasis changed after spaceflight. In I4 single-cell multi-omics data, we identified a “spaceflight signature” of gene expression characterized by enrichment in oxidative phosphorylation, UV response, immune function, and TCF21 pathways. We confirmed the presence of this signature in independent datasets, including the NASA Twins Study, the I4 skin spatial transcriptomics, and 817 NASA GeneLab mouse transcriptomes. Finally, we observed that (1) T cells showed an up-regulation of FOXP3, (2) MHC class I genes exhibited long-term suppression, and (3) infection-related immune pathways were associated with microbiome shifts. In summary, this study reveals conserved and distinct immune disruptions occurring and details a roadmap for potential countermeasures to preserve astronaut health.

Suggested Citation

  • JangKeun Kim & Braden T. Tierney & Eliah G. Overbey & Ezequiel Dantas & Matias Fuentealba & Jiwoon Park & S. Anand Narayanan & Fei Wu & Deena Najjar & Christopher R. Chin & Cem Meydan & Conor Loy & Be, 2024. "Single-cell multi-ome and immune profiles of the Inspiration4 crew reveal conserved, cell-type, and sex-specific responses to spaceflight," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49211-2
    DOI: 10.1038/s41467-024-49211-2
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    References listed on IDEAS

    as
    1. Nicholas Arpaia & Clarissa Campbell & Xiying Fan & Stanislav Dikiy & Joris van der Veeken & Paul deRoos & Hui Liu & Justin R. Cross & Klaus Pfeffer & Paul J. Coffer & Alexander Y. Rudensky, 2013. "Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation," Nature, Nature, vol. 504(7480), pages 451-455, December.
    2. Braden T. Tierney & Yingxuan Tan & Aleksandar D. Kostic & Chirag J. Patel, 2021. "Gene-level metagenomic architectures across diseases yield high-resolution microbiome diagnostic indicators," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    3. Jeffrey M. Perkel, 2021. "Single-cell analysis enters the multiomics age," Nature, Nature, vol. 595(7868), pages 614-616, July.
    4. Simon N. Willis & Julie Tellier & Yang Liao & Stephanie Trezise & Amanda Light & Kristy O’Donnell & Lee Ann Garrett-Sinha & Wei Shi & David M. Tarlinton & Stephen L. Nutt, 2017. "Environmental sensing by mature B cells is controlled by the transcription factors PU.1 and SpiB," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
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