Proteome-wide Adaptations of Mouse Skeletal Muscles during a Full Month in SpaceClick to copy article linkArticle link copied!
- Georg Tascher
- Thomas Brioche
- Pauline Maes
- Angèle Chopard
- Donal O’Gorman
- Guillemette Gauquelin-Koch
- Stéphane Blanc
- Fabrice Bertile
Abstract
The safety of space flight is challenged by a severe loss of skeletal muscle mass, strength, and endurance that may compromise the health and performance of astronauts. The molecular mechanisms underpinning muscle atrophy and decreased performance have been studied mostly after short duration flights and are still not fully elucidated. By deciphering the muscle proteome changes elicited in mice after a full month aboard the BION-M1 biosatellite, we observed that the antigravity soleus incurred the greatest changes compared with locomotor muscles. Proteomics data notably suggested mitochondrial dysfunction, metabolic and fiber type switching toward glycolytic type II fibers, structural alterations, and calcium signaling-related defects to be the main causes for decreased muscle performance in flown mice. Alterations of the protein balance, mTOR pathway, myogenesis, and apoptosis were expected to contribute to muscle atrophy. Moreover, several signs reflecting alteration of telomere maintenance, oxidative stress, and insulin resistance were found as possible additional deleterious effects. Finally, 8 days of recovery post flight were not sufficient to restore completely flight-induced changes. Thus in-depth proteomics analysis unraveled the complex and multifactorial remodeling of skeletal muscle structure and function during long-term space flight, which should help define combined sets of countermeasures before, during, and after the flight.
Cited By
This article is cited by 33 publications.
- Helena C. Kenny, Georg Tascher, Anna Ziemianin, Floriane Rudwill, Alexandre Zahariev, Isabelle Chery, Guillemette Gauquelin-Koch, Marie-Pierre Barielle, Martina Heer, Stephane Blanc, Donal J. O’Gorman, Fabrice Bertile. Effectiveness of Resistive Vibration Exercise and Whey Protein Supplementation Plus Alkaline Salt on the Skeletal Muscle Proteome Following 21 Days of Bed Rest in Healthy Males. Journal of Proteome Research 2020, 19
(8)
, 3438-3451. https://doi.org/10.1021/acs.jproteome.0c00256
- Elisa Le Roux, Alexandre Zahariev, Isabelle Chery, Dale A. Schoeller, Pierre Bourdier, Alain Maillet, Cecile Thevenot, Maël Garnotel, Guillemette Gauquelin-Koch, Laurie Van Den Berghe, Stéphane Blanc, Chantal Simon, Audrey Bergouignan. Substrate metabolism in male astronauts onboard the International Space Station: the ENERGY study. npj Microgravity 2024, 10
(1)
https://doi.org/10.1038/s41526-024-00360-0
- Marta Murgia, Jörn Rittweger, Carlo Reggiani, Roberto Bottinelli, Matthias Mann, Stefano Schiaffino, Marco V. Narici. Spaceflight on the ISS changed the skeletal muscle proteome of two astronauts. npj Microgravity 2024, 10
(1)
https://doi.org/10.1038/s41526-024-00406-3
- Sneha Chopra, Som Nath Singh, Pulkit Mathur. Nutritional Fuelling for Microgravity Environment of Space Missions. Current Nutrition & Food Science 2024, 20
(4)
, 450-465. https://doi.org/10.2174/1573401319666230503162143
- Min Wang, Sheng Chen, Changqing Zhong, Lei Liu, Guodong Wang, Xin Huang, Xiaoman Yang, Heming Yang, Lianyong Li. The influence of simulated weightlessness on the composition and function of gut microbiota and bile acid metabolism products. Life Sciences in Space Research 2024, 41 , 18-28. https://doi.org/10.1016/j.lssr.2024.01.002
- Takashi Ohira, Yoko Ino, Naoyuki Kawao, Yuya Mizukami, Kiyotaka Okada, Osamu Matsuo, Hisashi Hirano, Yayoi Kimura, Hiroshi Kaji. Plasminogen deficiency exacerbates skeletal muscle loss during mechanical unloading in developing mice. Journal of Applied Physiology 2024, 136
(3)
, 643-658. https://doi.org/10.1152/japplphysiol.00300.2023
- Jingjing ZHANG, Yong LÜ, Tao ZHANG, Fangwu LIU. Research Progress of Spaceflight Rodent Culture Devices and Experimental Techniques. Chinese Journal of Space Science 2024, 44
(3)
, 544. https://doi.org/10.11728/cjss2024.03.2023-0096
- Deeksha Malhan, Müge Yalçin, Britt Schoenrock, Dieter Blottner, Angela Relógio. Skeletal muscle gene expression dysregulation in long-term spaceflights and aging is clock-dependent. npj Microgravity 2023, 9
(1)
https://doi.org/10.1038/s41526-023-00273-4
- Yoko Ino, Takashi Ohira, Ken Kumagai, Yusuke Nakai, Tomoko Akiyama, Kayano Moriyama, Yuriko Takeda, Tomoyuki Saito, Akihide Ryo, Yutaka Inaba, Hisashi Hirano, Yayoi Kimura. Identification of mouse soleus muscle proteins altered in response to changes in gravity loading. Scientific Reports 2023, 13
(1)
https://doi.org/10.1038/s41598-023-42875-8
- Ryan W. Baranowski, Jessica L. Braun, Briana L. Hockey, Jenalyn L. Yumol, Mia S. Geromella, Colton J.F. Watson, Nigel Kurgan, Holt N. Messner, Kennedy C. Whitley, Adam J. MacNeil, Guillemette Gauquelin-Koch, Fabrice Bertile, William Gittings, Rene Vandenboom, Wendy E. Ward, Val A. Fajardo. Toward countering muscle and bone loss with spaceflight: GSK3 as a potential target. iScience 2023, 26
(7)
, 107047. https://doi.org/10.1016/j.isci.2023.107047
- Lauren M. Sanders, Hamed Chok, Finsam Samson, Ana Uriarte Acuna, San-Huei Lai Polo, Valery Boyko, Yi-Chun Chen, Marie Dinh, Samrawit Gebre, Jonathan M. Galazka, Sylvain V. Costes, Amanda M. Saravia-Butler. Batch effect correction methods for NASA GeneLab transcriptomic datasets. Frontiers in Astronomy and Space Sciences 2023, 10 https://doi.org/10.3389/fspas.2023.1200132
- Daniil V. Popov, Pavel A. Makhnovskii, Viktor G. Zgoda, Guzel R. Gazizova, Tatiana F. Vepkhvadze, Egor M. Lednev, Evgeniia S. Motanova, Evgeny A. Lysenko, Oleg I. Orlov, Elena S. Tomilovskaya. Rapid changes in transcriptomic profile and mitochondrial function in human soleus muscle after 3-day dry immersion. Journal of Applied Physiology 2023, 134
(5)
, 1256-1264. https://doi.org/10.1152/japplphysiol.00048.2023
- Simon J. S. Cameron, Arwyn Edwards, Robert J. Lambert, Mike Stroud, Luis A. J. Mur. Participants in the Trans-Antarctic Winter Traverse Expedition Showed Increased Bacterial Load and Diversity in Saliva but Maintained Individual Differences within Stool Microbiota and Across Metabolite Fingerprints. International Journal of Molecular Sciences 2023, 24
(5)
, 4850. https://doi.org/10.3390/ijms24054850
- Jin Chen, Zihua Li, Yudian Zhang, Xu Zhang, Shujie Zhang, Zonghan Liu, Huimei Yuan, Xiangsheng Pang, Yaxuan Liu, Wuchen Tao, Xiaoping Chen, Peng Zhang, Guo-Qiang Chen. Mechanism of reduced muscle atrophy via ketone body (D)-3-hydroxybutyrate. Cell & Bioscience 2022, 12
(1)
https://doi.org/10.1186/s13578-022-00826-2
- K. A. Sharlo, I. D. Lvova, B. S. Shenkman. Interaction of Oxidative Metabolism and Epigenetic Regulation of Gene Expression under Muscle Functional Unloading. Journal of Evolutionary Biochemistry and Physiology 2022, 58
(3)
, 625-643. https://doi.org/10.1134/S0022093022030012
- Colleen S. Deane, Colleen S. Deane, Joseph Borg, Thomas Cahill, Eugénie Carnero-Diaz, Timothy Etheridge, Gary Hardiman, Natalie Leys, Pedro Madrigal, Aránzazu Manzano, Felice Mastroleo, F. Javier Medina, Manuel A. Fernandez-Rojo, Keith Siew, Nathaniel J. Szewczyk, Alicia Villacampa, Stephen B. Walsh, Silvio Weging, Daniela Bezdan, Stefania Giacomello, Willian A. da Silveira, Raúl Herranz, Willian A. da Silveira, Raúl Herranz. Space omics research in Europe: Contributions, geographical distribution and ESA member state funding schemes. iScience 2022, 25
(3)
, 103920. https://doi.org/10.1016/j.isci.2022.103920
- Kim Ngan Tran, Jong-il Choi. Mimic microgravity effect on muscle transcriptome under ionizing radiation. Life Sciences in Space Research 2022, 32 , 96-104. https://doi.org/10.1016/j.lssr.2021.12.002
- Herbert Schulz, Sebastian M. Strauch, Peter Richter, Markus Wehland, Marcus Krüger, Jayashree Sahana, Thomas J. Corydon, Petra Wise, Ronni Baran, Michael Lebert, Daniela Grimm. Latest knowledge about changes in the proteome in microgravity. Expert Review of Proteomics 2022, 19
(1)
, 43-59. https://doi.org/10.1080/14789450.2022.2030711
- Takashi Ohira, Yoko Ino, Yayoi Kimura, Yusuke Nakai, Ayuko Kimura, Yoichi Kurata, Hiroyuki Kagawa, Mitsuo Kimura, Kenji Egashira, Chie Matsuda, Yoshinobu Ohira, Satoshi Furukawa, Hisashi Hirano. Effects of microgravity exposure and fructo-oligosaccharide ingestion on the proteome of soleus and extensor digitorum longus muscles in developing mice. npj Microgravity 2021, 7
(1)
https://doi.org/10.1038/s41526-021-00164-6
- Hong Phuong Nguyen, Phuong Hoa Tran, Kyu-Sung Kim, Su-Geun Yang. The effects of real and simulated microgravity on cellular mitochondrial function. npj Microgravity 2021, 7
(1)
https://doi.org/10.1038/s41526-021-00171-7
- Jessica L. Braun, Mia S. Geromella, Sophie I. Hamstra, Holt N. Messner, Val A. Fajardo. Characterizing SERCA Function in Murine Skeletal Muscles after 35–37 Days of Spaceflight. International Journal of Molecular Sciences 2021, 22
(21)
, 11764. https://doi.org/10.3390/ijms222111764
- D Moosavi, D Wolovsky, A Depompeis, D Uher, D Lennington, R Bodden, CE Garber. The effects of spaceflight microgravity on the musculoskeletal system of humans and animals, with an emphasis on exercise as a countermeasure: a systematic scoping review. Physiological Research 2021, , 119-151. https://doi.org/10.33549/physiolres.934550
- Fabrice Bertile, Caroline Habold, Yvon Le Maho, Sylvain Giroud. Body Protein Sparing in Hibernators: A Source for Biomedical Innovation. Frontiers in Physiology 2021, 12 https://doi.org/10.3389/fphys.2021.634953
- San-Huei Lai Polo, Amanda M. Saravia-Butler, Valery Boyko, Marie T. Dinh, Yi-Chun Chen, Homer Fogle, Sigrid S. Reinsch, Shayoni Ray, Kaushik Chakravarty, Oana Marcu, Rick B. Chen, Sylvain V. Costes, Jonathan M. Galazka. RNAseq Analysis of Rodent Spaceflight Experiments Is Confounded by Sample Collection Techniques. iScience 2020, 23
(12)
, 101733. https://doi.org/10.1016/j.isci.2020.101733
- Jia-Qi Yang, Nan Jiang, Zheng-Peng Li, Song Guo, Zheng-Yang Chen, Bin-Bin Li, Shao-Bin Chai, Sheng-Yu Lu, Hong-Feng Yan, Pei-Ming Sun, Tao Zhang, Hong-Wei Sun, Jian-Wu Yang, Jin-Lian Zhou, He-Ming Yang, Yan Cui. The effects of microgravity on the digestive system and the new insights it brings to the life sciences. Life Sciences in Space Research 2020, 27 , 74-82. https://doi.org/10.1016/j.lssr.2020.07.009
- Takashi Ohira, Yoko Ino, Yusuke Nakai, Hironobu Morita, Ayuko Kimura, Yoichi Kurata, Hiroyuki Kagawa, Mitsuo Kimura, Kenji Egashira, Shunsuke Moriya, Kyoko Hiramatsu, Masao Kawakita, Yayoi Kimura, Hisashi Hirano. Proteomic analysis revealed different responses to hypergravity of soleus and extensor digitorum longus muscles in mice. Journal of Proteomics 2020, 217 , 103686. https://doi.org/10.1016/j.jprot.2020.103686
- Chiara De Cesari, Ivana Barravecchia, Olga V. Pyankova, Matteo Vezza, Marco M. Germani, Francesca Scebba, Jack J. W. A. van Loon, Debora Angeloni. Hypergravity Activates a Pro-Angiogenic Homeostatic Response by Human Capillary Endothelial Cells. International Journal of Molecular Sciences 2020, 21
(7)
, 2354. https://doi.org/10.3390/ijms21072354
- D. Greaves, P. Arbeille, L. Guillon, K. Zuj, E. G. Caiani. Effects of exercise countermeasure on myocardial contractility measured by 4D speckle tracking during a 21-day head-down bed rest. European Journal of Applied Physiology 2019, 119
(11-12)
, 2477-2486. https://doi.org/10.1007/s00421-019-04228-0
- Marie Mortreux, Daniela Riveros, Mary L. Bouxsein, Seward B. Rutkove. A Moderate Daily Dose of Resveratrol Mitigates Muscle Deconditioning in a Martian Gravity Analog. Frontiers in Physiology 2019, 10 https://doi.org/10.3389/fphys.2019.00899
- Victoria Gulimova, Alexandra Proshchina, Anastasia Kharlamova, Yuliya Krivova, Valery Barabanov, Rustam Berdiev, Victor Asadchikov, Alexey Buzmakov, Denis Zolotov, Sergey Saveliev. Reptiles in Space Missions: Results and Perspectives. International Journal of Molecular Sciences 2019, 20
(12)
, 3019. https://doi.org/10.3390/ijms20123019
- Sebastian M. Strauch, Daniela Grimm, Thomas J. Corydon, Marcus Krüger, Johann Bauer, Michael Lebert, Petra Wise, Manfred Infanger, Peter Richter. Current knowledge about the impact of microgravity on the proteome. Expert Review of Proteomics 2019, 16
(1)
, 5-16. https://doi.org/10.1080/14789450.2019.1550362
- Maude Gerbaix, Heather White, Guillaume Courbon, Boris Shenkman, Guillemette Gauquelin-Koch, Laurence Vico. Eight Days of Earth Reambulation Worsen Bone Loss Induced by 1-Month Spaceflight in the Major Weight-Bearing Ankle Bones of Mature Mice. Frontiers in Physiology 2018, 9 https://doi.org/10.3389/fphys.2018.00746
- Afshin Beheshti, Jack Miller, Yared Kidane, Daniel Berrios, Samrawit G. Gebre, Sylvain V. Costes. NASA GeneLab Project: Bridging Space Radiation Omics with Ground Studies. Radiation Research 2018, 189
(6)
, 553-559. https://doi.org/10.1667/RR15062.1
Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.
Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.
The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.