Spatial multi-omics of human skin reveals KRAS and inflammatory responses to spaceflight

Jiwoon Park, Eliah G. Overbey, S. Anand Narayanan, JangKeun Kim, Braden T. Tierney, Namita Damle, Deena Najjar, Krista A. Ryon, Jacqueline Proszynski, Ashley Kleinman, Jeremy Wain Hirschberg, Matthew MacKay, Evan E. Afshin, Richard Granstein, Justin Gurvitch, Briana M. Hudson, Aric Rininger, Sean Mullane, Sarah E. Church, Cem Meydan, George Church, Afshin Beheshti, Jaime Mateus and Christopher E. Mason ()
Additional contact information
Jiwoon Park: Weill Cornell Medicine
Eliah G. Overbey: Weill Cornell Medicine
S. Anand Narayanan: Florida State University
JangKeun Kim: Weill Cornell Medicine
Braden T. Tierney: Weill Cornell Medicine
Namita Damle: Weill Cornell Medicine
Deena Najjar: Weill Cornell Medicine
Krista A. Ryon: Weill Cornell Medicine
Jacqueline Proszynski: Weill Cornell Medicine
Ashley Kleinman: Weill Cornell Medicine
Jeremy Wain Hirschberg: Weill Cornell Medicine
Matthew MacKay: Weill Cornell Medicine
Evan E. Afshin: Weill Cornell Medicine
Richard Granstein: Weill Cornell Medicine
Justin Gurvitch: Weill Cornell Medicine
Briana M. Hudson: NanoString Technologies, Inc.
Aric Rininger: NanoString Technologies, Inc.
Sean Mullane: SpaceX
Sarah E. Church: NanoString Technologies, Inc.
Cem Meydan: Weill Cornell Medicine
George Church: Harvard Medical School
Afshin Beheshti: Broad Institute of MIT and Harvard
Jaime Mateus: SpaceX
Christopher E. Mason: Weill Cornell Medicine

Nature Communications, 2024, vol. 15, issue 1, 1-14

Abstract: Abstract Spaceflight can change metabolic, immunological, and biological homeostasis and cause skin rashes and irritation, yet the molecular basis remains unclear. To investigate the impact of short-duration spaceflight on the skin, we conducted skin biopsies on the Inspiration4 crew members before (L-44) and after (R + 1) flight. Leveraging multi-omics assays including GeoMx™ Digital Spatial Profiler, single-cell RNA/ATAC-seq, and metagenomics/metatranscriptomics, we assessed spatial gene expressions and associated microbial and immune changes across 95 skin regions in four compartments: outer epidermis, inner epidermis, outer dermis, and vasculature. Post-flight samples showed significant up-regulation of genes related to inflammation and KRAS signaling across all skin regions. These spaceflight-associated changes mapped to specific cellular responses, including altered interferon responses, DNA damage, epithelial barrier disruptions, T-cell migration, and hindered regeneration were located primarily in outer tissue compartments. We also linked epithelial disruption to microbial shifts in skin swab and immune cell activity to PBMC single-cell data from the same crew and timepoints. Our findings present the inaugural collection and examination of astronaut skin, offering insights for future space missions and response countermeasures.

Date: 2024
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DOI: 10.1038/s41467-024-48625-2

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