A single-cell transcriptomic atlas of exercise-induced anti-inflammatory and geroprotective effects across the body
Exercise benefits the whole organism, yet, how tissues across the body orchestrally respond to exercise remains enigmatic. Here, in young and old mice, with or without exercise, and exposed to infectious injury, we characterized the phenotypic and molecular adaptations to a 12-month exercise across...
| Main Authors: | , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2023-01-01
|
| Series: | The Innovation |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2666675823000085 |
| _version_ | 1797944056567824384 |
|---|---|
| author | Shuhui Sun Shuai Ma Yusheng Cai Si Wang Jie Ren Yuanhan Yang Jiale Ping Xuebao Wang Yiyuan Zhang Haoteng Yan Wei Li Concepcion Rodriguez Esteban Yan Yu Feifei Liu Juan Carlos Izpisua Belmonte Weiqi Zhang Jing Qu Guang-Hui Liu |
| author_facet | Shuhui Sun Shuai Ma Yusheng Cai Si Wang Jie Ren Yuanhan Yang Jiale Ping Xuebao Wang Yiyuan Zhang Haoteng Yan Wei Li Concepcion Rodriguez Esteban Yan Yu Feifei Liu Juan Carlos Izpisua Belmonte Weiqi Zhang Jing Qu Guang-Hui Liu |
| author_sort | Shuhui Sun |
| collection | DOAJ |
| description | Exercise benefits the whole organism, yet, how tissues across the body orchestrally respond to exercise remains enigmatic. Here, in young and old mice, with or without exercise, and exposed to infectious injury, we characterized the phenotypic and molecular adaptations to a 12-month exercise across 14 tissues/organs at single-cell resolution. Overall, exercise protects tissues from infectious injury, although more effectively in young animals, and benefits aged individuals in terms of inflammaging suppression and tissue rejuvenation, with structural improvement in the central nervous system and systemic vasculature being the most prominent. In vascular endothelial cells, we found that readjusting the rhythmic machinery via the core circadian clock protein BMAL1 delayed senescence and facilitated recovery from infectious damage, recapitulating the beneficial effects of exercise. Our study underscores the effect of exercise in reconstituting the youthful circadian clock network and provides a foundation for further investigating the interplay between exercise, aging, and immune challenges across the whole organism. |
| first_indexed | 2024-04-10T20:33:36Z |
| format | Article |
| id | doaj.art-1b1e2ed4f9a647a8add861fa7719337b |
| institution | Directory Open Access Journal |
| issn | 2666-6758 |
| language | English |
| last_indexed | 2024-04-10T20:33:36Z |
| publishDate | 2023-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | The Innovation |
| spelling | doaj.art-1b1e2ed4f9a647a8add861fa7719337b2023-01-25T04:16:37ZengElsevierThe Innovation2666-67582023-01-0141100380A single-cell transcriptomic atlas of exercise-induced anti-inflammatory and geroprotective effects across the bodyShuhui Sun0Shuai Ma1Yusheng Cai2Si Wang3Jie Ren4Yuanhan Yang5Jiale Ping6Xuebao Wang7Yiyuan Zhang8Haoteng Yan9Wei Li10Concepcion Rodriguez Esteban11Yan Yu12Feifei Liu13Juan Carlos Izpisua Belmonte14Weiqi Zhang15Jing Qu16Guang-Hui Liu17State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; Institute for Stem Cell and Regeneration, CAS, Beijing 100101, China; Beijing Institute for Stem Cell and Regenerative Medicine, Beijing 100101, ChinaState Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; Institute for Stem Cell and Regeneration, CAS, Beijing 100101, China; Beijing Institute for Stem Cell and Regenerative Medicine, Beijing 100101, ChinaState Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; Beijing Institute for Stem Cell and Regenerative Medicine, Beijing 100101, ChinaAdvanced Innovation Center for Human Brain Protection, and National Clinical Research Center for Geriatric Disorders, Xuanwu Hospital Capital Medical University, Beijing 100053, China; Aging Translational Medicine Center, International Center for Aging and Cancer, Beijing Municipal Geriatric Medical Research Center, Xuanwu Hospital, Capital Medical University, Beijing 100053, ChinaInstitute for Stem Cell and Regeneration, CAS, Beijing 100101, China; CAS Key Laboratory of Genomic and Precision Medicine, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing 100101, China; China National Center for Bioinformation, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaState Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaCAS Key Laboratory of Genomic and Precision Medicine, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing 100101, China; China National Center for Bioinformation, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaState Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaState Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, ChinaAdvanced Innovation Center for Human Brain Protection, and National Clinical Research Center for Geriatric Disorders, Xuanwu Hospital Capital Medical University, Beijing 100053, China; Aging Translational Medicine Center, International Center for Aging and Cancer, Beijing Municipal Geriatric Medical Research Center, Xuanwu Hospital, Capital Medical University, Beijing 100053, ChinaAdvanced Innovation Center for Human Brain Protection, and National Clinical Research Center for Geriatric Disorders, Xuanwu Hospital Capital Medical University, Beijing 100053, China; Aging Translational Medicine Center, International Center for Aging and Cancer, Beijing Municipal Geriatric Medical Research Center, Xuanwu Hospital, Capital Medical University, Beijing 100053, ChinaAltos Labs, San Diego, CA 92121, USAState Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaState Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, ChinaAltos Labs, San Diego, CA 92121, USAInstitute for Stem Cell and Regeneration, CAS, Beijing 100101, China; CAS Key Laboratory of Genomic and Precision Medicine, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing 100101, China; China National Center for Bioinformation, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China; Corresponding authorState Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; Institute for Stem Cell and Regeneration, CAS, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China; Beijing Institute for Stem Cell and Regenerative Medicine, Beijing 100101, China; Corresponding authorState Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; Advanced Innovation Center for Human Brain Protection, and National Clinical Research Center for Geriatric Disorders, Xuanwu Hospital Capital Medical University, Beijing 100053, China; Institute for Stem Cell and Regeneration, CAS, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China; Beijing Institute for Stem Cell and Regenerative Medicine, Beijing 100101, China; Corresponding authorExercise benefits the whole organism, yet, how tissues across the body orchestrally respond to exercise remains enigmatic. Here, in young and old mice, with or without exercise, and exposed to infectious injury, we characterized the phenotypic and molecular adaptations to a 12-month exercise across 14 tissues/organs at single-cell resolution. Overall, exercise protects tissues from infectious injury, although more effectively in young animals, and benefits aged individuals in terms of inflammaging suppression and tissue rejuvenation, with structural improvement in the central nervous system and systemic vasculature being the most prominent. In vascular endothelial cells, we found that readjusting the rhythmic machinery via the core circadian clock protein BMAL1 delayed senescence and facilitated recovery from infectious damage, recapitulating the beneficial effects of exercise. Our study underscores the effect of exercise in reconstituting the youthful circadian clock network and provides a foundation for further investigating the interplay between exercise, aging, and immune challenges across the whole organism.http://www.sciencedirect.com/science/article/pii/S2666675823000085exerciseaginginflammationcircadian clockBMAL1single-cell RNA sequencing |
| spellingShingle | Shuhui Sun Shuai Ma Yusheng Cai Si Wang Jie Ren Yuanhan Yang Jiale Ping Xuebao Wang Yiyuan Zhang Haoteng Yan Wei Li Concepcion Rodriguez Esteban Yan Yu Feifei Liu Juan Carlos Izpisua Belmonte Weiqi Zhang Jing Qu Guang-Hui Liu A single-cell transcriptomic atlas of exercise-induced anti-inflammatory and geroprotective effects across the body The Innovation exercise aging inflammation circadian clock BMAL1 single-cell RNA sequencing |
| title | A single-cell transcriptomic atlas of exercise-induced anti-inflammatory and geroprotective effects across the body |
| title_full | A single-cell transcriptomic atlas of exercise-induced anti-inflammatory and geroprotective effects across the body |
| title_fullStr | A single-cell transcriptomic atlas of exercise-induced anti-inflammatory and geroprotective effects across the body |
| title_full_unstemmed | A single-cell transcriptomic atlas of exercise-induced anti-inflammatory and geroprotective effects across the body |
| title_short | A single-cell transcriptomic atlas of exercise-induced anti-inflammatory and geroprotective effects across the body |
| title_sort | single cell transcriptomic atlas of exercise induced anti inflammatory and geroprotective effects across the body |
| topic | exercise aging inflammation circadian clock BMAL1 single-cell RNA sequencing |
| url | http://www.sciencedirect.com/science/article/pii/S2666675823000085 |
| work_keys_str_mv | AT shuhuisun asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT shuaima asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT yushengcai asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT siwang asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT jieren asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT yuanhanyang asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT jialeping asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT xuebaowang asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT yiyuanzhang asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT haotengyan asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT weili asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT concepcionrodriguezesteban asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT yanyu asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT feifeiliu asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT juancarlosizpisuabelmonte asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT weiqizhang asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT jingqu asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT guanghuiliu asinglecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT shuhuisun singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT shuaima singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT yushengcai singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT siwang singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT jieren singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT yuanhanyang singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT jialeping singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT xuebaowang singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT yiyuanzhang singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT haotengyan singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT weili singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT concepcionrodriguezesteban singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT yanyu singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT feifeiliu singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT juancarlosizpisuabelmonte singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT weiqizhang singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT jingqu singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody AT guanghuiliu singlecelltranscriptomicatlasofexerciseinducedantiinflammatoryandgeroprotectiveeffectsacrossthebody |