Guardians of the Mitochondria: Space Mitochondria 2.0 Systemic Analysis Reveals Bioenergetic Dysregulation Across Species

Joseph Guarnieri, Zeynab Maghsoudi, Jangkeun Kim, Phi Bya, Gabrielle Widjaja, Richard Barker, Marissa Burke, Zimu Cen, Hossein Fazelinia, Sergey Tsoy, Rachel Tiersky, Anna Peczak, Jihan Kim, Ye-Ah Kim, Jeffrey Haltom, Michael Almeida, Michael A. Garris, Sarah Day, Rebekah Sanchez-Hodge, Aleeza H. ZilbermanNoah G. Allen, Angela J. Kukib, Elizabeth A. Blaber, Begum Mathyk, Frederick C. Harris, Kanhaiya Singh, Chandan K. Sen, Lucinda Innes, Nilufar Ali, Aaron J. Berliner, Upendra Kar, Eliah Overbey, Simona Giunta, Jason E. Podrabsky, Matthew D. Neal, Timothy R. Billiar, Colwyn Headley, Cem Meydan, Alexia Tasoula, Nathaniel J. Szewczyk, Yasutaka Ikeda, Aina Gotoh-Katoh, Jonathan C. Schisler, Man S. Kim, Robert E. Schwartz, Douglas C. Wallace, Christopher E. Mason, Tin Nguyen, Afshin Beheshti

Research output: Working paperPreprint

Abstract

Spaceflight imposes unique stressors that disrupt mitochondrial function, vital for energy production and immune regulation. Our multi-omics analysis (proteomics, bisulfite sequencing, RNA-seq, and single-nuclei RNA/ATAC-seq) on astronauts, rodents, and model organisms (flies, worms, plants) revealed progressive impairment of mitochondrial oxidative phosphorylation (OXPHOS) during spaceflight, with delayed recovery post-return across species. In rodents, radiation ≥10.34 mGy activated persistent mitochondrial stress pathways across multiple organs except in the spleen, with older and male C57BL/6 mice most affected. Astronaut data from the NASA Twins Study, JAXA, and Inspiration4 missions showed prolonged mitochondrial dysfunction, with OXPHOS suppression and TCA cycle inhibition lasting up to 82 days. Bisulfite sequencing confirmed lasting epigenetic changes in OXPHOS genes. Lastly, Kaempferol, an antioxidant and mitochondrial activator, mitigated radiation-induced liver atrophy in mice and preserved liver function in human organoids. This cross-species study underscores the need for targeted therapies to protect mitochondrial biogenesis during long-duration space missions.
Original languageAmerican English
Number of pages49
DOIs
StatePublished - Jan 2025

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