Cited by 1,136Autophagy in Disease and TherapyMetabolism, Diabetes, and CancerMuscle Physiology and Disorders

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Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis

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He, Congcong, Bassik, Michael C., Moresi, Viviana, Sun, Kai, Wei, Yongjie, Zou, Zhongju, An, Zhenyi, Loh, Joy, Fisher, Jill, Sun, Qihua, Korsmeyer, Stanley, Packer, Milton, May, Herman I., Hill, Joseph A., Virgin, Herbert W., Gilpin, Christopher, Xiao, Guanghua, Bassel-Duby, Rhonda, Scherer, Philipp E., Levine, Beth·2012·Nature

DOI 10.1038/nature10758PMC PMC3518436

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Abstract

Exercise has beneficial effects on human health, including protection against metabolic disorders such as diabetes. However, the cellular mechanisms underlying these effects are incompletely understood. The lysosomal degradation pathway, autophagy, is an intracellular recycling system that functions during basal conditions in organelle and protein quality control. During stress, increased levels of autophagy permit cells to adapt to changing nutritional and energy demands through protein catabolism. Moreover, in animal models, autophagy protects against diseases such as cancer, neurodegenerative disorders, infections, inflammatory diseases, ageing and insulin resistance. Here we show that acute exercise induces autophagy in skeletal and cardiac muscle of fed mice. To investigate the role of exercise-mediated autophagy in vivo, we generated mutant mice that show normal levels of basal autophagy but are deficient in stimulus (exercise- or starvation)-induced autophagy. These mice (termed BCL2 AAA mice) contain knock-in mutations in BCL2 phosphorylation sites (Thr69Ala, Ser70Ala and Ser84Ala) that prevent stimulus-induced disruption of the BCL2-beclin-1 complex and autophagy activation. BCL2 AAA mice show decreased endurance and altered glucose metabolism during acute exercise, as well as impaired chronic exercise-mediated protection against high-fat-diet-induced glucose intolerance. Thus, exercise induces autophagy, BCL2 is a crucial regulator of exercise- (and starvation)-induced autophagy in vivo, and autophagy induction may contribute to the beneficial metabolic effects of exercise.

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Qu, X., Yu, J., Bhagat, G., Furuya, N., Hibshoosh, H., Troxel, A., Rosen, J., Eskelinen, E.-L., Mizushima, N., Ohsumi, Y., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci20039 · Cited by 2,311
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Leptin levels reflect body lipid content in mice: Evidence for diet-induced resistance to leptin action
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Niu, M., Dai, X., Zou, W., Yu, X., Teng, W., Chen, Q., Sun, X., Yu, W., Ma, H., & Liu, P. (2017) · Translational Neuroscience · doi:10.1515/tnsci-2017-0008 · Cited by 56
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Araujo, T. F., Cordeiro, A. V., de Vasconcelos, D. A. A., Vitzel, K. F., & Silva, V. R. R. (2018) · Life Sciences · doi:10.1016/j.lfs.2018.08.024 · Cited by 56
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Yang, X., Li, Y., Ren, X., Xiong, X., Wu, L., Li, J., Wang, J., Gao, Y., Shang, H., & Xing, Y. (2017) · Scientific Reports · doi:10.1038/srep44789 · Cited by 55
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Fernández, Á. F., Liu, Y., Ginet, V., Shi, M., Nah, J., Zou, Z., Zhou, A., Posner, B. A., Xiao, G., Tanguy, M., et al. (2020) · JCI Insight · doi:10.1172/jci.insight.133282 · Cited by 58
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Li, Y., Wang, S., Ni, H., Huang, H., & Ding, W. (2014) · BioMed Research International · doi:10.1155/2014/498491 · Cited by 55
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Parousis, A., Carter, H. N., Tran, C., Erlich, A. T., Moosavi, Z. S. M., Pauly, M., & Hood, D. A. (2018) · Autophagy · doi:10.1080/15548627.2018.1491488 · Cited by 57
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Hulmi, J. J., Oliveira, B. M. S., Silvennoinen, M., Hoogaars, W. M. H., Pasternack, A. H., Kainulainen, H., & Ritvos, O. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00065.2013 · Cited by 45
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Exercise and the Regulation of Mitochondrial Turnover
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Environmental Triggers for IBD
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Meta-Analysis Identifies Gene-by-Environment Interactions as Demonstrated in a Study of 4,965 Mice
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The Case for Increased Physical Activity in Chronic Inflammatory Bowel Disease: A Brief Review
Shephard, R. J. (2016) · International Journal of Sports Medicine · doi:10.1055/s-0042-103157 · Cited by 44
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de Paula, T. G., Zanella, B. T. T., Fantinatti, B. E. A., de Moraes, L. N., Duran, B. O. D. S., de Oliveira, C. B., Salomão, R. A. S., da Silva‐Gomes, R. N., Padovani, C. R., dos Santos, V. B., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0177679 · Cited by 44
Two weeks of high-intensity interval training increases skeletal muscle mitochondrial respiration via complex-specific remodeling in sedentary humans
Batterson, P. M., McGowan, E. M., Stierwalt, H. D., Ehrlicher, S. E., Newsom, S. A., & Robinson, M. M. (2023) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00467.2022 · Cited by 44
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Ye, X., Sun, P., Lao, S., Wen, M., Zheng, R., Lin, Y., Gan, L., Fan, X., Wang, P., Li, Z., et al. (2023) · Life Sciences · doi:10.1016/j.lfs.2023.122231 · Cited by 45
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Maiese, K. (2015) · Current Neurovascular Research · doi:10.2174/1567202612666150305110929 · Cited by 43
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Effect of treadmill exercise on skeletal muscle autophagy in rats with obesity induced by a high-fat diet
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miR-16 controls myoblast proliferation and apoptosis through directly suppressing Bcl2 and FOXO1 activities
Jia, X., Ouyang, H., Abdalla, B. A., Xu, H., Nie, Q., & Zhang, X. (2017) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2017.02.010 · Cited by 41
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Exercise alters and β-alanine combined with exercise augments histidyl dipeptide levels and scavenges lipid peroxidation products in human skeletal muscle
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Fis1 deficiencies differentially affect mitochondrial quality in skeletal muscle
Zhang, Z., Sliter, D. A., Bleck, C. K. E., & Ding, S. (2019) · Mitochondrion · doi:10.1016/j.mito.2019.09.005 · Cited by 41
Dysregulation of metabolic flexibility: The impact of mTOR on autophagy in neurodegenerative disease
Maiese, K. (2020) · International review of neurobiology · doi:10.1016/bs.irn.2020.01.009 · Cited by 43

Authors: He, C., Bassik, M. C., Moresi, V., Sun, K., Wei, Y., Zou, Z., An, Z., Loh, J., Fisher, J., Sun, Q., Korsmeyer, S., Packer, M., May, H. I., Hill, J. A., Virgin, H. W., Gilpin, C., Xiao, G., Bassel-Duby, R., Scherer, P. E., & Levine, B.
Affiliations: The University of Texas Southwestern Medical Center (US)
Dana-Farber Cancer Institute (US)
Howard Hughes Medical Institute (US)
Washington University in St. Louis (US)
Corresponding author: Levine, Beth
ORCID: He, Congcong
Bassik, Michael C.
Moresi, Viviana
Sun, Kai
Zou, Zhongju
Packer, Milton
May, Herman I.
Hill, Joseph A.
Virgin, Herbert W.
Gilpin, Christopher
Xiao, Guanghua
Scherer, Philipp E.
Levine, Beth
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2012-01-18
Volume: 481
Issue: 7382
Pages: 511-515
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature10758
PMC: PMC3518436
OpenAlex: W2082476985
Cited by: 1,136
References: 36
Citations by year: 2026: 40 · 2025: 47 · 2024: 49 · 2023: 55 · 2022: 64 · 2021: 90 · 2020: 93 · 2019: 76 · 2018: 93 · 2017: 99 · 2016: 94 · 2015: 112 · 2014: 82 · 2013: 80 · 2012: 61
FWCI: 79.93
Type: journal article
Language: en
Update notices: erratum (2013-11-06)
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
Funders: Howard Hughes Medical Institute
National Heart, Lung, and Blood Institute (R0I HL090842, R0I HL080244, R01HL090842)
National Cancer Institute (R01CA112023, R01CA109618, P30CA142543)
National Institute of Allergy and Infectious Diseases (R01AI084887, R0I AI084887)
National Institute of Diabetes and Digestive and Kidney Diseases (RCI DK086629, R01DK055758, 1P01 DK0887761, RC1DK086629, P01DK088761)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Keywords: Bcl-2, Bcl-2 phosphorylation, skeletal muscle, myocardium, glucose metabolism, impaired glucose tolerance, high-fat diet, endurance, starvation-induced autophagy, exercise metabolism, diabetes protection
MeSH terms: Beclin-1, Animals, Autophagy, Cells, Cultured, Dietary Fats, Physical Exertion, Food Deprivation, Glucose, Glucose Tolerance Test, Homeostasis, Male, Mice, Transgenic, Mutation, Myocardium, Phosphorylation, Physical Conditioning, Animal, Physical Endurance, Protein Binding, Proto-Oncogene Proteins, Running, Glucose Intolerance, Muscle, Skeletal, Proto-Oncogene Proteins c-bcl-2, Leptin, Apoptosis Regulatory Proteins, Mice, Adiponectin, Gene Knock-In Techniques

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Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis

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