Induction of autophagy supports the bioenergetic demands of quiescent muscle stem cell activation

Tang, Ann H; Rando, Thomas A

doi:10.15252/embj.201488278

Cited by 294Muscle Physiology and DisordersAutophagy in Disease and TherapyMetabolism, Diabetes, and Cancer

Induction of autophagy supports the bioenergetic demands of quiescent muscle stem cell activation

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Tang, Ann H, Rando, Thomas A·2014·The EMBO Journal

DOI 10.15252/embj.201488278PMC PMC4282556

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Abstract

The exit of a stem cell out of quiescence into an activated state is characterized by major metabolic changes associated with increased biosynthesis of proteins and macromolecules. The regulation of this transition is poorly understood. Using muscle stem cells, or satellite cells (SCs), we found that autophagy, which catabolizes intracellular contents to maintain proteostasis and to produce energy during nutrient deprivation, was induced during SC activation. Inhibition of autophagy suppressed the increase in ATP levels and delayed SC activation, both of which could be partially rescued by exogenous pyruvate as an energy source, suggesting that autophagy may provide nutrients necessary to meet bioenergetic demands during this critical transition from quiescence to activation. We found that SIRT1, a known nutrient sensor, regulates autophagic flux in SC progeny. A deficiency of SIRT1 led to a delay in SC activation that could also be partially rescued by exogenous pyruvate. These studies suggest that autophagy, regulated by SIRT1, may play an important role during SC activation to meet the high bioenergetic demands of the activation process. Tang and Rando report induction of autophagy by the nutrient sensor SIRT1 as crucial energy provider for efficient proliferation/differentiation in quiescent muscle satellite cells in vivo. Tang and Rando report induction of autophagy by the nutrient sensor SIRT1 as crucial energy provider for efficient proliferation/differentiation in quiescent muscle satellite cells in vivo.

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SIRT1 promotes autophagy in quiescent MuSCs, and loss of SIRT1 leads to a delay in MuSC activation out of quiescence.
“SIRT1 was also found to promote autophagy in quiescent MuSCs, and in this case, a loss of SIRT1 leads to a delay in MuSC activation out of quiescence — similar to what is observed in aged muscles109.”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [109]
Autophagy is also required for activation out of quiescence, and defects in autophagic activity with ageing lead to increased cell death during activation.
“Autophagy is also required for activation out of quiescence109, and defects in autophagic activity with ageing lead to increased cell death during activation110.”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [109]

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The PI3K, Metabolic, and Autophagy Networks: Interactive Partners in Cellular Health and Disease
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Tightrope act: autophagy in stem cell renewal, differentiation, proliferation, and aging
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Autophagy induced by the class III histone deacetylase Sirt1 prevents prion peptide neurotoxicity
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Autophagy in Myf5+ progenitors regulates energy and glucose homeostasis through control of brown fat and skeletal muscle development
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Intracellular recognition of pathogens and autophagy as an innate immune host defence
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Metabolic plasticity and hematopoietic stem cell biology
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Autophagy maintains stemness by preventing senescence
García-Prat, L., Martínez-Vicente, M., Perdiguero, E., Ortet, L., Rodríguez-Ubreva, J., Rebollo, E., Ruiz-Bonilla, V., Gutarra, S., Ballestar, E., Serrano, A. L., et al. (2016) · Nature · doi:10.1038/nature16187 · Cited by 1,355 · see citing works
Autophagy maintains the metabolism and function of young and old stem cells
Ho, T. T., Warr, M. R., Adelman, E. R., Lansinger, O. M., Flach, J., Verovskaya, E. V., Figueroa, M. E., & Passegué, E. (2017) · Nature · doi:10.1038/nature21388 · Cited by 896 · see citing works
Autophagy as a promoter of longevity: insights from model organisms
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Skeletal muscle: A review of molecular structure and function, in health and disease
Mukund, K., & Subramaniam, S. (2019) · Wiley Interdisciplinary Reviews: Systems Biology and Medicine · doi:10.1002/wsbm.1462 · Cited by 601 · see citing works
Lysosome activation clears aggregates and enhances quiescent neural stem cell activation during aging
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The NAD+-Dependent SIRT1 Deacetylase Translates a Metabolic Switch into Regulatory Epigenetics in Skeletal Muscle Stem Cells
Ryall, J. G., Dell’Orso, S., Derfoul, A., Juan, A., Zare, H., Feng, X., Clermont, D., Koulnis, M., Gutierrez-Cruz, G., Fulco, M., et al. (2015) · Cell Stem Cell · doi:10.1016/j.stem.2014.12.004 · Cited by 575 · see citing works
Intrinsic and extrinsic mechanisms regulating satellite cell function
Dumont, N. A., Wang, Y. X., & Rudnicki, M. A. (2015) · Development · doi:10.1242/dev.114223 · Cited by 491 · see citing works
Control of satellite cell function in muscle regeneration and its disruption in ageing
Sousa-Victor, P., García-Prat, L., & Muñoz-Cánoves, P. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00421-2 · Cited by 476 · see citing works
Isolation of skeletal muscle stem cells by fluorescence-activated cell sorting
Liu, L. A., Cheung, T. H., Charville, G. W., & Rando, T. A. (2015) · Nature Protocols · doi:10.1038/nprot.2015.110 · Cited by 396 · see citing works
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Ageing and rejuvenation of tissue stem cells and their niches
Brunet, A., Goodell, M. A., & Rando, T. A. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00510-w · Cited by 407 · see citing works
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Autophagy in metabolic disease and ageing
Kitada, M., & Koya, D. (2021) · Nature Reviews Endocrinology · doi:10.1038/s41574-021-00551-9 · Cited by 413 · see citing works
Metabolic Reprogramming of Stem Cell Epigenetics
Ryall, J. G., Cliff, T. S., Dalton, S., & Sartorelli, V. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.11.012 · Cited by 325 · see citing works
Molecular circuitry of stem cell fate in skeletal muscle regeneration, ageing and disease
Almada, A. E., & Wagers, A. J. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.7 · Cited by 315 · see citing works
Stem Cell Quiescence: Dynamism, Restraint, and Cellular Idling
van Velthoven, C. T. J., & Rando, T. A. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.01.001 · Cited by 313 · see citing works
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The role of mitochondria in stem cell fate and aging
Zhang, H., Menzies, K. J., & Auwerx, J. H. (2018) · Development · doi:10.1242/dev.143420 · Cited by 285 · see citing works
Autophagy and the hallmarks of aging
Kaushik, S., Tasset, I., Arias, E., Pampliega, O., Wong, E., Martinez-Vicente, M., & Cuervo, A. M. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101468 · Cited by 285 · see citing works
Regulation of Stem Cell Aging by Metabolism and Epigenetics
Ren, R., Ocampo, A., Liu, G., & Belmonte, J. C. I. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.07.019 · Cited by 269 · see citing works
Restraining Lysosomal Activity Preserves Hematopoietic Stem Cell Quiescence and Potency
Liang, R. H.-S., Arif, T., Kalmykova, S., Kasianov, A. S., Miao, L., Menon, V., Qiu, J., Bernitz, J. M., Moore, K. A., Lin, F., et al. (2020) · Cell stem cell · doi:10.1016/j.stem.2020.01.013 · Cited by 248 · see citing works
Regulation of adult stem cell quiescence and its functions in the maintenance of tissue integrity
de Morrée, A., & Rando, T. A. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00568-6 · Cited by 243 · see citing works
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Single cell analysis of adult mouse skeletal muscle stem cells in homeostatic and regenerative conditions
Dell'Orso, S., Juan, A. H., Ko, K.-D., Naz, F., Perovanovic, J., Gutierrez-Cruz, G., Feng, X., & Sartorelli, V. (2019) · Development · doi:10.1242/dev.174177 · Cited by 243 · see citing works
New Insights for Oxidative Stress and Diabetes Mellitus
Maiese, K. (2015) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2015/875961 · Cited by 227 · see citing works
Mitochondrial dynamics maintain muscle stem cell regenerative competence throughout adult life by regulating metabolism and mitophagy
Hong, X., Isern, J., Campanario, S., Perdiguero, E., Ramírez-Pardo, I., Segalés, J., Hernansanz-Agustín, P., Curtabbi, A., Deryagin, O., Pollán, A., et al. (2022) · Cell stem cell · doi:10.1016/j.stem.2022.07.009 · Cited by 213 · see citing works
Satellite Cells in Muscular Dystrophy – Lost in Polarity
Chang, N. C., Chevalier, F. P., & Rudnicki, M. A. (2016) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2016.04.002 · Cited by 200 · see citing works
Autophagy in stem cells: repair, remodelling and metabolic reprogramming
Boya, P., Codogno, P., & Rodriguez-Muela, N. (2018) · Development · doi:10.1242/dev.146506 · Cited by 197 · see citing works
Redox Control of Skeletal Muscle Regeneration
Moal, E. L., Pialoux, V., Juban, G., Groussard, C., Zouhal, H., Chazaud, B., & Mounier, R. (2016) · Antioxidants and Redox Signaling · doi:10.1089/ars.2016.6782 · Cited by 197 · see citing works
Stem cell activation in skeletal muscle regeneration
Fu, X., Wang, H.-T., & Hu, P. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1819-5 · Cited by 161 · see citing works
Skeletal muscle autophagy and its role in sarcopenia and organismal aging
Jiao, J., & Demontis, F. (2017) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2017.03.009 · Cited by 184 · see citing works
Distinct metabolic states govern skeletal muscle stem cell fates during prenatal and postnatal myogenesis
Pala, F., Di Girolamo, D., Mella, S., Yennek, S., Chatre, L., Ricchetti, M., & Tajbakhsh, S. (2018) · Journal of Cell Science · doi:10.1242/jcs.212977 · Cited by 184 · see citing works
Divergent Roles of Inflammation in Skeletal Muscle Recovery From Injury
Howard, E. E., Pasiakos, S. M., Blesso, C. N., Fussell, M. A., & Rodriguez, N. R. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00087 · Cited by 176 · see citing works
Autophagy and Stem Cells: Self-Eating for Self-Renewal
Chang, N. C. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00138 · Cited by 174 · see citing works
Stem Cell Aging in Skeletal Muscle Regeneration and Disease
Yamakawa, H., Kusumoto, D., Hashimoto, H., & Yuasa, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21051830 · Cited by 156 · see citing works
Muscle stem cell aging: regulation and rejuvenation
Sousa-Victor, P., García-Prat, L., Serrano, A. L., Perdiguero, E., & Muñoz-Cánoves, P. (2015) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2015.03.006 · Cited by 163 · see citing works
Interactions between muscle stem cells, mesenchymal-derived cells and immune cells in muscle homeostasis, regeneration and disease
Farup, J., Madaro, L., Puri, P., & Mikkelsen, U. R. (2015) · Cell Death and Disease · doi:10.1038/cddis.2015.198 · Cited by 156 · see citing works
Glucose Metabolism Drives Histone Acetylation Landscape Transitions that Dictate Muscle Stem Cell Function
Yucel, N., Wang, Y. X., Mai, T., Porpiglia, E., Lund, P. J., Markov, G., Garcia, B. A., Bendall, S. C., Angelo, M., & Blau, H. M. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.05.092 · Cited by 159 · see citing works
GCN2 inhibition sensitizes arginine-deprived hepatocellular carcinoma cells to senolytic treatment
Missiaen, R., Anderson, N. M., Kim, L. C., Nance, B., Burrows, M., Skuli, N., Carens, M., Riscal, R., Steensels, A., Li, F., et al. (2022) · Cell Metabolism · doi:10.1016/j.cmet.2022.06.010 · Cited by 154 · see citing works
Mitochondria initiate and regulate sarcopenia
Alway, S. E., Mohamed, J. S., & Myers, M. J. (2017) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000101 · Cited by 153 · see citing works
“Deacetylation of FOXO1 and FOXO3a by SIRT1 (19,20) mediates autophagic signaling in muscle cells, and aging attenuates SIRT1, which reduces autophagy (134).”
Background
Stimulation of Hair Growth by Small Molecules that Activate Autophagy
Chai, M., Jiang, M., Vergnes, L., Fu, X., de Barros, S. C., Doan, N., Huang, W., Chu, J., Jiao, J., Herschman, H. R., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.05.070 · Cited by 155 · see citing works
Autophagy in stem cell aging
Revuelta, M., & Matheu, A. (2017) · Aging Cell · doi:10.1111/acel.12655 · Cited by 146 · see citing works
Autophagy regulates satellite cell ability to regenerate normal and dystrophic muscles
Fiacco, E., Castagnetti, F., Bianconi, V., Madaro, L., Bardi, M. D., Nazio, F., D’Amico, A., Bertini, E., Cecconi, F., Puri, P., et al. (2016) · Cell Death and Differentiation · doi:10.1038/cdd.2016.70 · Cited by 147 · see citing works
AMPKα1‐LDH pathway regulates muscle stem cell self‐renewal by controlling metabolic homeostasis
Théret, M., Gsaier, L., Schaffer, B. E., Juban, G., Larbi, S. B., Weiss‐Gayet, M., Bultot, L., Collodet, C., Foretz, M., Dominique Desplanches, C., et al. (2017) · The EMBO Journal · doi:10.15252/embj.201695273 · Cited by 138 · see citing works
Oxidative Stress in Stem Cell Aging
Chen, F., Liu, Y., Wong, N.-K., Xiao, J., & So, K. (2017) · Cell Transplantation · doi:10.1177/0963689717735407 · Cited by 134 · see citing works
Proteostatic and Metabolic Control of Stemness
García‐Prat, L., Sousa‐Victor, P., & Muñoz‐Cánoves, P. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.04.011 · Cited by 123 · see citing works
Macrophage-released ADAMTS1 promotes muscle stem cell activation
Du, H., Shih, C., Wosczyna, M. N., Mueller, A. A., Cho, J., Aggarwal, A., Rando, T. A., & Feldman, B. J. (2017) · Nature Communications · doi:10.1038/s41467-017-00522-7 · Cited by 128 · see citing works
Self-citation
The Role of Autophagy in Skeletal Muscle Diseases
Xia, Q., Huang, X., Huang, J., Zheng, Y., March, M., Li, J., & Wei, Y. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.638983 · Cited by 130 · see citing works
Metabolic regulation of the hallmarks of stem cell biology
Jackson, B. T., & Finley, L. W. S. (2024) · Cell stem cell · doi:10.1016/j.stem.2024.01.003 · Cited by 122 · see citing works
The beneficial role of proteolysis in skeletal muscle growth and stress adaptation
Bell, R. A. V., Al-Khalaf, M. H., & Megeney, L. A. (2016) · Skeletal Muscle · doi:10.1186/s13395-016-0086-6 · Cited by 117 · see citing works
Islr regulates canonical Wnt signaling-mediated skeletal muscle regeneration by stabilizing Dishevelled-2 and preventing autophagy
Zhang, K., Zhang, Y., Gu, L., Lan, M., Liu, C., Wang, M., Su, Y., Ge, M., Wang, T., Yu, Y., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-07638-4 · Cited by 117 · see citing works
Autophagy is essential for oligodendrocyte differentiation, survival, and proper myelination
Bankston, A. N., Forston, M. D., Howard, R. M., Andres, K. R., Smith, A. E., Ohri, S. S., Bates, M. L., Bunge, M. B., & Whittemore, S. R. (2019) · Glia · doi:10.1002/glia.23646 · Cited by 112 · see citing works
Satellite cells in ageing: use it or lose it
Chen, W., Datzkiw, D., & Rudnicki, M. A. (2020) · Open Biology · doi:10.1098/rsob.200048 · Cited by 116 · see citing works
Understanding muscle regenerative decline with aging: new approaches to bring back youthfulness to aged stem cells
Muñoz‐Cánoves, P., Neves, J., & Sousa‐Victor, P. (2019) · FEBS Journal · doi:10.1111/febs.15182 · Cited by 111 · see citing works
Pompe Disease: New Developments in an Old Lysosomal Storage Disorder
Meena, N. K., & Raben, N. (2020) · Biomolecules · doi:10.3390/biom10091339 · Cited by 112 · see citing works
Quiescence: Good and Bad of Stem Cell Aging
Tümpel, S., & Rudolph, K. L. (2019) · Trends in Cell Biology · doi:10.1016/j.tcb.2019.05.002 · Cited by 108 · see citing works
Metabolic switching and cell fate decisions: implications for pluripotency, reprogramming and development
Cliff, T. S., & Dalton, S. (2017) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2017.06.008 · Cited by 104 · see citing works
YY1 regulates skeletal muscle regeneration through controlling metabolic reprogramming of satellite cells
Chen, F., Zhou, J., Li, Y., Zhao, Y. F., Yuan, J., Cao, Y., Wang, L., Zhang, Z., Zhang, B., Wang, C. C., et al. (2019) · The EMBO Journal · doi:10.15252/embj.201899727 · Cited by 103 · see citing works
The AMPK/p27Kip1 Axis Regulates Autophagy/Apoptosis Decisions in Aged Skeletal Muscle Stem Cells
White, J. P., Billin, A. N., Campbell, M. E., Russell, A. J., Huffman, K. M., & Kraus, W. E. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.06.014 · Cited by 104 · see citing works
The Role of Autophagy in the Maintenance of Stemness and Differentiation of Mesenchymal Stem Cells
Sbrana, F. V., Cortini, M., Avnet, S., Perut, F., Columbaro, M., Milito, A. D., & Baldini, N. (2016) · Stem Cell Reviews and Reports · doi:10.1007/s12015-016-9690-4 · Cited by 103 · see citing works
Quiescence Entry, Maintenance, and Exit in Adult Stem Cells
Mohammad, K., Dakik, P., Medkour, Y., Mitrofanova, D., & Titorenko, V. I. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20092158 · Cited by 90 · see citing works
The roles of autophagy in vascular smooth muscle cells
Tai, S., Hu, X., Peng, D., Zhou, S., & Zheng, X. (2016) · International Journal of Cardiology · doi:10.1016/j.ijcard.2016.02.128 · Cited by 88 · see citing works
Differentiation Drives Widespread Rewiring of the Neural Stem Cell Chaperone Network
Vonk, W. I. M., Rainbolt, T. K., Dolan, P. T., Webb, A. E., Brunet, A., & Frydman, J. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.03.009 · Cited by 84 · see citing works
The role of Pitx2 and Pitx3 in muscle stem cells gives new insights into P38α MAP kinase and redox regulation of muscle regeneration
L’honoré, A., Commère, P., Négroni, E., Pallafacchina, G., Friguet, B., Drouin, J., BUCKINGHAM, M. E., & Montarras, D. (2018) · eLife · doi:10.7554/elife.32991 · Cited by 87 · see citing works
Energy metabolism as therapeutic target for aged wound repair by engineered extracellular vesicle
Zhuang, Y., Jiang, S., Deng, X., Lao, A., Hua, X., Xie, Y., Jiang, L., Wang, X., & Lin, K. (2024) · Science Advances · doi:10.1126/sciadv.adl0372 · Cited by 91 · see citing works
Metabolic regulation of somatic stem cells in vivo
Meacham, C. E., DeVilbiss, A. W., & Morrison, S. J. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00462-1 · Cited by 85 · see citing works
Distinct role of autophagy on angiogenesis: highlights on the effect of autophagy in endothelial lineage and progenitor cells
Hassanpour, M., Rezabakhsh, A., Pezeshkian, M., Rahbarghazi‬, R., & Nouri, M. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-1060-5 · Cited by 80 · see citing works
Autophagy in muscle regeneration: potential therapies for myopathies
Chen, W., Chen, Y., Liu, Y., & Wang, X. (2022) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.13000 · Cited by 77 · see citing works
Novel nervous and multi-system regenerative therapeutic strategies for diabetes mellitus with mTOR
Maiese, K. (2016) · Neural Regeneration Research · doi:10.4103/1673-5374.179032 · Cited by 78 · see citing works
Ulk1-mediated autophagy plays an essential role in mitochondrial remodeling and functional regeneration of skeletal muscle
Call, J. A., Wilson, R. J., Laker, R. C., Zhang, M., Kundu, M., & Yan, Z. (2017) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00348.2016 · Cited by 77 · see citing works
Muscle Stem Cells and Aging
Hwang, A. B., & Brack, A. S. (2017) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2017.08.008 · Cited by 80 · see citing works
Contribution of muscle satellite cells to sarcopenia
Huo, F., Liu, Q., & Liu, H. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.892749 · Cited by 74 · see citing works
Interaction between epigenetic and metabolism in aging stem cells
Brunet, A., & Rando, T. A. (2017) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2016.12.009 · Cited by 76 · see citing works
Self-citation
Mitochondrial Dysfunction in Cancer Cachexia: Impact on Muscle Health and Regeneration
Beltrà, M., Pin, F., Ballarò, R., Costelli, P., & Penna, F. (2021) · Cells · doi:10.3390/cells10113150 · Cited by 76 · see citing works
Autophagy in Stem Cell Biology: A Perspective on Stem Cell Self-Renewal and Differentiation
Chen, X., He, Y., & Lu, F. (2018) · Stem Cells International · doi:10.1155/2018/9131397 · Cited by 72 · see citing works
Changes in Redox Signaling in the Skeletal Muscle with Aging
Szentesi, P., Csernoch, L., Dux, L., & Keller-Pintér, A. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/4617801 · Cited by 71 · see citing works
Autophagy Defects in Skeletal Myopathies
Margeta, M. (2019) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathmechdis-012419-032618 · Cited by 71 · see citing works
Autophagy in the Regulation of Tissue Differentiation and Homeostasis
Perrotta, C., Cattaneo, M. G., Molteni, R., & Palma, C. D. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.602901 · Cited by 72 · see citing works
The Skeletal Muscle as an Active Player Against Cancer Cachexia
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Authors: Tang, A. H., & Rando, T. A.
Affiliations: Stanford Medicine (US)
VA Palo Alto Health Care System (US)
Corresponding author: Rando, Thomas A
ORCID: Rando, Thomas A
Venue: The EMBO Journal
Publisher: Springer Science and Business Media LLC
Published: 2014-10-14
Volume: 33
Issue: 23
Pages: 2782-2797
ISSN: 0261-4189 (ISSN-L)
1460-2075
DOI: 10.15252/embj.201488278
PMC: PMC4282556
OpenAlex: W2082121028
Cited by: 294
References: 97
Citations by year: 2026: 13 · 2025: 24 · 2024: 26 · 2023: 19 · 2022: 30 · 2021: 26 · 2020: 28 · 2019: 26 · 2018: 28 · 2017: 34 · 2016: 19 · 2015: 20 · 2014: 1
FWCI: 10.12
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: public-domain
www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: The EMBO Journal (publishedVersion, public-domain)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Glenn Foundation for Medical Research
NIH (R01 AG23806, R01 AG047820, P01 AG036695)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Keywords: autophagy, muscle stem cells, satellite cells, stem cell quiescence, stem cell activation, SIRT1, pyruvate, bioenergetics, ATP levels, nutrient sensing, proteostasis, muscle regeneration
MeSH terms: Adenosine Triphosphate, Animals, Autophagy, Cell Differentiation, Deoxyuridine, Energy Metabolism, Fluorescent Antibody Technique, Gene Expression Regulation, Mice, Transgenic, Microtubule-Associated Proteins, Stem Cells, Muscle, Skeletal, Reverse Transcriptase Polymerase Chain Reaction, Immunoprecipitation, Green Fluorescent Proteins, Mice, Sirtuin 1

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Induction of autophagy supports the bioenergetic demands of quiescent muscle stem cell activation

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