Autophagy gene expression in skeletal muscle of older individuals is associated with physical performance, muscle volume and mitochondrial function in the study of muscle, mobility and aging (SOMMA).

aging autophagy gene expression mTor mitochondria mobility oxidative metabolism

Journal

Aging cell
ISSN: 1474-9726
Titre abrégé: Aging Cell
Pays: England
ID NLM: 101130839

Informations de publication

Date de publication:
16 Apr 2024
Historique:
revised: 14 01 2024
received: 04 11 2023
accepted: 02 02 2024
medline: 17 4 2024
pubmed: 17 4 2024
entrez: 17 4 2024
Statut: aheadofprint

Résumé

Autophagy is essential for proteostasis, energetic balance, and cell defense and is a key pathway in aging. Identifying associations between autophagy gene expression patterns in skeletal muscle and physical performance outcomes would further our knowledge of mechanisms related with proteostasis and healthy aging. Muscle biopsies were obtained from participants in the Study of Muscle, Mobility, and Aging (SOMMA). For 575 participants, RNA was sequenced and expression of 281 genes related to autophagy regulation, mitophagy, and mTOR/upstream pathways was determined. Associations between gene expression and outcomes including mitochondrial respiration in muscle fiber bundles (MAX OXPHOS), physical performance (VO

Identifiants

pubmed: 38627910
doi: 10.1111/acel.14118
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e14118

Subventions

Organisme : NIA NIH HHS
ID : R01AG059416
Pays : United States

Informations de copyright

© 2024 The Authors. Aging Cell published by Anatomical Society and John Wiley & Sons Ltd.

Références

Aas, S. N., Hamarsland, H., Cumming, K. T., Rognlien, S. H., Aase, O. J., Nordseth, M., Karsrud, S., Godager, S., Tommerbakke, D., Handegard, V., & Raastad, T. (2019). The impact of age and frailty on skeletal muscle autophagy markers and specific strength: A cross‐sectional comparison. Experimental Gerontology, 125, 110687.
Balan, E., Schwalm, C., Naslain, D., Nielens, H., Francaux, M., & Deldicque, L. (2019). Regular endurance exercise promotes fission, mitophagy, and oxidative phosphorylation in human skeletal muscle independently of age. Frontiers in Physiology, 10, 1088.
Bar‐Peled, L., Chantranupong, L., Cherniack, A. D., Chen, W. W., Ottina, K. A., Grabiner, B. C., Spear, E. D., Carter, S. L., Meyerson, M., & Sabatini, D. M. (2013). A tumor suppressor complex with GAP activity for the rag GTPases that signal amino acid sufficiency to mTORC1. Science, 340, 1100–1106.
Bar‐Shai, M., Carmeli, E., & Reznick, A. Z. (2005). The role of NF‐kappaB in protein breakdown in immobilization, aging, and exercise: From basic processes to promotion of health. Annals of the New York Academy of Sciences, 1057, 431–447.
Bordi, M., De Cegli, R., Testa, B., Nixon, R. A., Ballabio, A., & Cecconi, F. (2021). A gene toolbox for monitoring autophagy transcription. Cell Death & Disease, 12, 1044.
Buford, T. W., Cooke, M. B., Manini, T. M., Leeuwenburgh, C., & Willoughby, D. S. (2010). Effects of age and sedentary lifestyle on skeletal muscle NF‐kappaB signaling in men. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 65, 532–537.
Cai, W., Wei, Y., Jarnik, M., Reich, J., & Lilly, M. A. (2016). The GATOR2 component Wdr24 regulates TORC1 activity and lysosome function. PLoS Genetics, 12, e1006036.
Carnio, S., LoVerso, F., Baraibar, M. A., Longa, E., Khan, M. M., Maffei, M., Reischl, M., Canepari, M., Loefler, S., Kern, H., Blaauw, B., Friguet, B., Bottinelli, R., Rudolf, R., & Sandri, M. (2014). Autophagy impairment in muscle induces neuromuscular junction degeneration and precocious aging. Cell Reports, 8, 1509–1521.
Cummings, S. R., Newman, A. B., Coen, P. M., Hepple, R. T., Collins, R., Kennedy, K., Danielson, M., Peters, K., Blackwell, T., Johnson, E., Mau, T., Shankland, E. G., Lui, L. Y., Patel, S., Young, D., Glynn, N. W., Strotmeyer, E. S., Esser, K. A., Marcinek, D. J., … Cawthon, P. M. (2023). The study of muscle, mobility and aging (SOMMA). A unique cohort study about the cellular biology of aging and age‐related loss of mobility. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 78(11), 2083–2093.
Day, N. J., Kelly, S. S., Lui, L. Y., Mansfield, T. A., Gaffrey, M. J., Trejo, J. B., Sagendorf, T. J., Attah, K., Moore, R. J., Douglas, C. M., Newman, A. B., Kritchevsky, S. B., Kramer, P. A., Marcinek, D. J., Coen, P. M., Goodpaster, B. H., Hepple, R. T., Cawthon, P. M., Petyuk, V. A., … Cummings, S. R. (2024). Signatures of cysteine oxidation on muscle structural and contractile proteins are associated with physical performance and muscle function in older adults: Study of muscle, mobility and aging (SOMMA). Aging Cell, e14094. https://doi.org/10.1111/acel.14094. Online ahead of print.
Distefano, G., Standley, R. A., Dube, J. J., Carnero, E. A., Ritov, V. B., Stefanovic‐Racic, M., Toledo, F. G. S., Piva, S. R., Goodpaster, B. H., & Coen, P. M. (2017). Chronological age does not influence ex‐vivo mitochondrial respiration and quality control in skeletal muscle. Journals of Gerontology Series a‐Biological Sciences and Medical Sciences, 72, 535–542.
Drummond, M. J., Addison, O., Brunker, L., Hopkins, P. N., McClain, D. A., LaStayo, P. C., & Marcus, R. L. (2014). Downregulation of E3 ubiquitin ligases and mitophagy‐related genes in skeletal muscle of physically inactive, frail older women: A cross‐sectional comparison. The journals of gerontology. Series A, Biological Sciences and Medical Sciences., 69, 1040–1048.
Du Bois, P., Pablo Tortola, C., Lodka, D., Kny, M., Schmidt, F., Song, K., Schmidt, S., Bassel‐Duby, R., Olson, E. N., & Fielitz, J. (2015). Angiotensin II induces skeletal muscle atrophy by activating TFEB‐mediated MuRF1 expression. Circulation Research, 117, 424–436.
Dulac, M., Leduc‐Gaudet, J. P., Reynaud, O., Ayoub, M. B., Guerin, A., Finkelchtein, M., Hussain, S. N., & Gouspillou, G. (2020). Drp1 knockdown induces severe muscle atrophy and remodelling, mitochondrial dysfunction, autophagy impairment and denervation. The Journal of Physiology, 598, 3691–3710.
Favaro, G., Romanello, V., Varanita, T., Andrea Desbats, M., Morbidoni, V., Tezze, C., Albiero, M., Canato, M., Gherardi, G., De Stefani, D., Mammucari, C., Blaauw, B., Boncompagni, S., Protasi, F., Reggiani, C., Scorrano, L., Salviati, L., & Sandri, M. (2019). DRP1‐mediated mitochondrial shape controls calcium homeostasis and muscle mass. Nature Communications, 10, 2576.
Frank, M., Duvezin‐Caubet, S., Koob, S., Occhipinti, A., Jagasia, R., Petcherski, A., Ruonala, M. O., Priault, M., Salin, B., & Reichert, A. S. (2012). Mitophagy is triggered by mild oxidative stress in a mitochondrial fission dependent manner. Biochimica et Biophysica Acta, 1823, 2297–2310.
Gouspillou, G., Sgarioto, N., Kapchinsky, S., Purves‐Smith, F., Norris, B., Pion, C. H., Barbat‐Artigas, S., Lemieux, F., Taivassalo, T., Morais, J. A., Aubertin‐Leheudre, M., & Hepple, R. T. (2014). Increased sensitivity to mitochondrial permeability transition and myonuclear translocation of endonuclease G in atrophied muscle of physically active older humans. The FASEB Journal, 28, 1621–1633.
Joseph, A. M., Adhihetty, P. J., Buford, T. W., Wohlgemuth, S. E., Lees, H. A., Nguyen, L. M., Aranda, J. M., Sandesara, B. D., Pahor, M., Manini, T. M., Marzetti, E., & Leeuwenburgh, C. (2012). The impact of aging on mitochondrial function and biogenesis pathways in skeletal muscle of sedentary high‐ and low‐functioning elderly individuals. Aging Cell, 11, 801–809.
Jung, C. H., Ro, S. H., Cao, J., Otto, N. M., & Kim, D. H. (2010). mTOR regulation of autophagy. FEBS Letters, 584, 1287–1295.
Kang, C., & Li Ji, L. (2012). Role of PGC‐1alpha signaling in skeletal muscle health and disease. Annals of the New York Academy of Sciences, 1271, 110–117.
Konopka, A. R., Suer, M. K., Wolff, C. A., & Harber, M. P. (2014). Markers of human skeletal muscle mitochondrial biogenesis and quality control: Effects of age and aerobic exercise training. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences., 69, 371–378.
Korolchuk, V. I., Saiki, S., Lichtenberg, M., Siddiqi, F. H., Roberts, E. A., Imarisio, S., Jahreiss, L., Sarkar, S., Futter, M., Menzies, F. M., O'Kane, C. J., Deretic, V., & Rubinsztein, D. C. (2011). Lysosomal positioning coordinates cellular nutrient responses. Nature Cell Biology, 13, 453–460.
Krause, G. J., Diaz, A., Jafari, M., Khawaja, R. R., Agullo‐Pascual, E., Santiago‐Fernandez, O., Richards, A. L., Chen, K. H., Dmitriev, P., Sun, Y., See, S. K., Abdelmohsen, K., Mazan‐Mamczarz, K., Krogan, N. J., Gorospe, M., Swaney, D. L., Sidoli, S., Bravo‐Cordero, J. J., Kampmann, M., & Cuervo, A. M. (2022). Reduced endosomal microautophagy activity in aging associates with enhanced exocyst‐mediated protein secretion. Aging Cell, 21, e13713.
Mammucari, C., Milan, G., Romanello, V., Masiero, E., Rudolf, R., Del Piccolo, P., Burden, S. J., Di Lisi, R., Sandri, C., Zhao, J., Goldberg, A. L., Schiaffino, S., & Sandri, M. (2007). FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metabolism, 6, 458–471.
Mansueto, G., Armani, A., Viscomi, C., D'Orsi, L., De Cegli, R., Polishchuk, E. V., Lamperti, C., Di Meo, I., Romanello, V., Marchet, S., Saha, P. K., Zong, H., Blaauw, B., Solagna, F., Tezze, C., Grumati, P., Bonaldo, P., Pessin, J. E., Zeviani, M., … Ballabio, A. (2017). Transcription factor EB controls metabolic flexibility during exercise. Cell Metabolism, 25, 182–196.
Masiero, E., Agatea, L., Mammucari, C., Blaauw, B., Loro, E., Komatsu, M., Metzger, D., Reggiani, C., Schiaffino, S., & Sandri, M. (2009). Autophagy is required to maintain muscle mass. Cell Metabolism, 10, 507–515.
Mau, T., Lui, L. Y., Distefano, G., Kramer, P. A., Ramos, S. V., Toledo, F. G. S., Santanasto, A. J., Shankland, E. G., Marcinek, D. J., Jurczak, M. J., Sipula, I., Bello, F. M., Duchowny, K. A., Molina, A. J. A., Sparks, L. M., Goodpaster, B. H., Hepple, R. T., Kritchevsky, S. B., Newman, A. B., … Coen, P. M. (2023). Mitochondrial energetics in skeletal muscle are associated with leg power and cardiorespiratory fitness in the study of muscle, mobility and aging. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 78, 1367–1375.
O'Leary, M. F., Vainshtein, A., Iqbal, S., Ostojic, O., & Hood, D. A. (2013). Adaptive plasticity of autophagic proteins to denervation in aging skeletal muscle. American Journal of Physiology. Cell Physiology, 304, C422–C430.
Penninx, B. W., Kritchevsky, S. B., Newman, A. B., Nicklas, B. J., Simonsick, E. M., Rubin, S., Nevitt, M., Visser, M., Harris, T., & Pahor, M. (2004). Inflammatory markers and incident mobility limitation in the elderly. Journal of the American Geriatrics Society, 52, 1105–1113.
Phillips, T., & Leeuwenburgh, C. (2005). Muscle fiber specific apoptosis and TNF‐alpha signaling in sarcopenia are attenuated by life‐long calorie restriction. The FASEB Journal, 19, 668–670.
Picca, A., Triolo, M., Wohlgemuth, S. E., Martenson, M. S., Mankowski, R. T., Anton, S. D., Marzetti, E., Leeuwenburgh, C., & Hood, D. A. (2023). Relationship between mitochondrial quality control markers, lower extremity tissue composition, and physical performance in physically inactive older adults. Cell, 12, 183.
Rabanal‐Ruiz, Y., Otten, E. G., & Korolchuk, V. I. (2017). mTORC1 as the main gateway to autophagy. Essays in Biochemistry, 61, 565–584.
Rasmussen, B. B., Fujita, S., Wolfe, R. R., Mittendorfer, B., Roy, M., Rowe, V. L., & Volpi, E. (2006). Insulin resistance of muscle protein metabolism in aging. The FASEB Journal, 20, 768–769.
Sakellariou, G. K., Pearson, T., Lightfoot, A. P., Nye, G. A., Wells, N., Giakoumaki, I. I., Vasilaki, A., Griffiths, R. D., Jackson, M. J., & McArdle, A. (2016). Mitochondrial ROS regulate oxidative damage and mitophagy but not age‐related muscle fiber atrophy. Scientific Reports, 6, 33944.
Sandri, M. (2010). Autophagy in skeletal muscle. The FEBS Letters, 584, 1411–1416.
Sandri, M., Lin, J., Handschin, C., Yang, W., Arany, Z. P., Lecker, S. H., Goldberg, A. L., & Spiegelman, B. M. (2006). PGC‐1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy‐specific gene transcription. Proceedings of the National Academy of Sciences of the United States of America, 103, 16260–16265.
Sardiello, M., Palmieri, M., di Ronza, A., Medina, D. L., Valenza, M., Gennarino, V. A., Di Malta, C., Donaudy, F., Embrione, V., Polishchuk, R. S., Banfi, S., Parenti, G., Cattaneo, E., & Ballabio, A. (2009). A gene network regulating lysosomal biogenesis and function. Science, 325, 473–477.
St‐Jean‐Pelletier, F., Pion, C. H., Leduc‐Gaudet, J. P., Sgarioto, N., Zovile, I., Barbat‐Artigas, S., Reynaud, O., Alkaterji, F., Lemieux, F. C., Grenon, A., Gaudreau, P., Hepple, R. T., Chevalier, S., Belanger, M., Morais, J. A., Aubertin‐Leheudre, M., & Gouspillou, G. (2017). The impact of ageing, physical activity, and pre‐frailty on skeletal muscle phenotype, mitochondrial content, and intramyocellular lipids in men. Journal of Cachexia, Sarcopenia and Muscle, 8, 213–228.
Takikita, S., Schreiner, C., Baum, R., Xie, T., Ralston, E., Plotz, P. H., & Raben, N. (2010). Fiber type conversion by PGC‐1alpha activates lysosomal and autophagosomal biogenesis in both unaffected and Pompe skeletal muscle. PLoS One, 5, e15239.
Terman, A. (1995). The effect of age on formation and elimination of autophagic vacuoles in mouse hepatocytes. Gerontology, 41(Suppl 2), 319–326.
Tezze, C., Romanello, V., Desbats, M. A., Fadini, G. P., Albiero, M., Favaro, G., Ciciliot, S., Soriano, M. E., Morbidoni, V., Cerqua, C., Loefler, S., Kern, H., Franceschi, C., Salvioli, S., Conte, M., Blaauw, B., Zampieri, S., Salviati, L., Scorrano, L., & Sandri, M. (2017). Age‐associated loss of OPA1 in muscle impacts muscle mass, metabolic homeostasis, systemic inflammation, and epithelial senescence. Cell Metabolism, 25, 1374–1389.e1376.
Tranah, G. J., Barnes, H. N., Cawthon, P. M., Coen, P. M., Esser, K. A., Hepple, R. T., Huo, Z., Kramer, P. A., Toledo, F. G. S., Evans, D. S., & Cummings, S. R. (2023). Expression of mitochondrial oxidative stress response genes in muscle is associated with mitochondrial respiration, physical performance, and muscle mass in the study of muscle, mobility and aging (SOMMA). medRxiv, 2023.11.05.23298108. https://doi.org/10.1101/2023.11.05.23298108
Triolo, M., Oliveira, A. N., Kumari, R., & Hood, D. A. (2022). The influence of age, sex, and exercise on autophagy, mitophagy, and lysosome biogenesis in skeletal muscle. Skeletal Muscle, 12, 13.
Triolo, M., Slavin, M., Moradi, N., & Hood, D. A. (2022). Time‐dependent changes in autophagy, mitophagy and lysosomes in skeletal muscle during denervation‐induced disuse. The Journal of Physiology, 600, 1683–1701.
Vainshtein, A., Desjardins, E. M., Armani, A., Sandri, M., & Hood, D. A. (2015). PGC‐1alpha modulates denervation‐induced mitophagy in skeletal muscle. Skeletal Muscle, 5, 9.
Yang, S., Loro, E., Wada, S., Kim, B., Tseng, W. J., Li, K., Khurana, T. S., & Arany, Z. (2020). Functional effects of muscle PGC‐1alpha in aged animals. Skeletal Muscle, 10, 14.
Zeng, N., D'Souza, R. F., Mitchell, C. J., & Cameron‐Smith, D. (2018). Sestrins are differentially expressed with age in the skeletal muscle of men: A cross‐sectional analysis. Experimental Gerontology, 110, 23–34.

Auteurs

Paul M Coen (PM)

Translational Research Institute, AdventHealth, Orlando, Florida, USA.

Zhiguang Huo (Z)

Department of Biostatistics, College of Public Health & Health Professions, College of Medicine University of Florida, Gainesville, Florida, USA.

Gregory J Tranah (GJ)

California Pacific Medical Center Research Institute, San Francisco, California, USA.

Haley N Barnes (HN)

California Pacific Medical Center Research Institute, San Francisco, California, USA.

Xiping Zhang (X)

Department of Physiology and Aging, College of Medicine, University of Florida, Gainesville, Florida, USA.

Christopher A Wolff (CA)

Department of Physiology and Aging, College of Medicine, University of Florida, Gainesville, Florida, USA.

Kevin Wu (K)

Department of Physiology and Aging, College of Medicine, University of Florida, Gainesville, Florida, USA.

Peggy M Cawthon (PM)

California Pacific Medical Center Research Institute, San Francisco, California, USA.
Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, California, USA.

Russell T Hepple (RT)

Department of Physical Therapy, University of Florida, Gainesville, Florida, USA.

Frederico G S Toledo (FGS)

Department of Medicine, Division of Endocrinology and Metabolism, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.

Daniel S Evans (DS)

California Pacific Medical Center Research Institute, San Francisco, California, USA.
Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, California, USA.

Olaya Santiago-Fernández (O)

Department of Developmental & Molecular Biology, Albert Einstein College of Medicine, New York, New York, USA.

Ana Maria Cuervo (AM)

Department of Developmental & Molecular Biology, Albert Einstein College of Medicine, New York, New York, USA.

Stephen B Kritchevsky (SB)

Department of Internal Medicine, Wake Forest University School of Medicine, Winston-Salem, North Carolina, USA.

Anne B Newman (AB)

Department of Epidemiology, School of Public Health, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.

Steven R Cummings (SR)

California Pacific Medical Center Research Institute, San Francisco, California, USA.
Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, California, USA.

Karyn A Esser (KA)

Department of Physiology and Aging, College of Medicine, University of Florida, Gainesville, Florida, USA.

Classifications MeSH