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

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, Begum Mathyk, Remi Klotz, Veronica Ortiz, Khiem Nguyen, Krista A. Ryon, Namita Damle, Nadia Houerbi, Laura I. Patras, Nathan Schanzer, Gwyneth A. Hutchinson, Jonathan Foox, Chandrima Bhattacharya, Matthew Mackay, Evan E. Afshin, Jeremy Wain Hirschberg, Ashley S. Kleinman, Julian C. Schmidt, Caleb M. Schmidt, Michael A. Schmidt, Afshin Beheshti, Irina Matei, David Lyden, Sean Mullane, Amran Asadi, Joan S. Lenz, Omary Mzava, Min Yu, Saravanan Ganesan, Iwijn Vlaminck, Ari M. Melnick, Darko Barisic, Daniel A. Winer, Sara R. Zwart, Brian E. Crucian, Scott M. Smith, Jaime Mateus, David Furman () and Christopher E. Mason ()
Additional contact information
JangKeun Kim: Weill Cornell Medicine
Braden T. Tierney: Weill Cornell Medicine
Eliah G. Overbey: Weill Cornell Medicine
Ezequiel Dantas: Weill Cornell Medicine
Matias Fuentealba: Buck Institute for Research on Aging
Jiwoon Park: 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
Cem Meydan: 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
Laura I. Patras: Weill Cornell Medicine
Nathan Schanzer: New York Medical College
Gwyneth A. Hutchinson: NASA Center for the Utilization of Biological Engineering in Space (CUBES)
Jonathan Foox: Weill Cornell Medicine
Chandrima Bhattacharya: Weill Cornell Medicine
Matthew Mackay: Weill Cornell Medicine
Evan E. Afshin: Weill Cornell Medicine
Jeremy Wain Hirschberg: Weill Cornell Medicine
Ashley S. Kleinman: Weill Cornell Medicine
Julian C. Schmidt: Sovaris Aerospace
Caleb M. Schmidt: Sovaris Aerospace
Michael A. Schmidt: Sovaris Aerospace
Afshin Beheshti: Broad Institute of MIT and Harvard
Irina Matei: Weill Cornell Medicine
David Lyden: 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
Iwijn Vlaminck: Meinig School of Biomedical Engineering
Ari M. Melnick: Weill Cornell Medicine
Darko Barisic: Weill Cornell Medicine
Daniel A. Winer: Buck Institute for Research on Aging
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
Christopher E. Mason: Weill Cornell Medicine

Nature Communications, 2024, vol. 15, issue 1, 1-18

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-49211-2

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