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

The DOI matches its Crossref record; 36 of the 36 references it cites were found in a registry or an index.

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

Open access

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

Open this paper in CoChat — free account

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1038/nature10758

Cites

36 of 36 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Repertoires of Autophagy in the Pathogenesis of Ocular Diseases
Li, Y., Jiang, Q. L., Cao, G.-F., Yao, J., & Yan, B. (2015) · Cellular Physiology and Biochemistry · doi:10.1159/000373980 · Cited by 16,351
Positional cloning of the mouse obese gene and its human homologue
Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L., & Friedman, J. M. (1994) · Nature · doi:10.1038/372425a0 · Cited by 13,419
Autophagy in the Pathogenesis of Disease
Levine, B., & Kroemer, G. (2008) · Cell · doi:10.1016/j.cell.2007.12.018 · Cited by 7,069
Self-citation
Autophagy and Viruses: Adversaries or Allies?
Dong, X., & Levine, B. (2013) · Journal of Innate Immunity · doi:10.1159/000346388 · Cited by 4,444
Self-citation
Antimicrobial Autophagy: A Conserved Innate Immune Response in Drosophila
Moy, R. H., & Cherry, S. R. (2013) · Journal of Innate Immunity · doi:10.1159/000350326 · Cited by 3,551
Induction of autophagy and inhibition of tumorigenesis by beclin 1
Liang, X. H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H., & Levine, B. (1999) · Nature · doi:10.1038/45257 · Cited by 3,347
Self-citation
A Novel Serum Protein Similar to C1q, Produced Exclusively in Adipocytes
Scherer, P. E., Williams, S. P., Fogliano, M., Baldini, G., & Lodish, H. F. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.45.26746 · Cited by 3,238
Self-citation
Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene
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
Self-citation
In Vivo Analysis of Autophagy in Response to Nutrient Starvation Using Transgenic Mice Expressing a Fluorescent Autophagosome Marker
Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T., & Ohsumi, Y. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-09-0704 · Cited by 2,105
Leptin levels reflect body lipid content in mice: Evidence for diet-induced resistance to leptin action
Frederich, R. C., Hamann, A., Anderson, S., Löllmann, B., Lowell, B. B., & Flier, J. S. (1995) · Nature Medicine · doi:10.1038/nm1295-1311 · Cited by 1,660

Flagged first, then by citations

Show all 36 references

Sorted by citations

Items 601–700 of 1,000

Mitochondrial redox metabolism in aging: Effect of exercise interventions
Hai, B., Jiang, N., Ji, L. L., & Zhang, Y. (2013) · Journal of sport and health science/Journal of Sport and Health Science · doi:10.1016/j.jshs.2013.03.006 · Cited by 28
AMP kinase in exercise adaptation of skeletal muscle
Jessen, N., Sundelin, E. I. O., & Møller, A. B. (2014) · Drug Discovery Today · doi:10.1016/j.drudis.2014.03.009 · Cited by 28
MicroRNA‐204‐5p modulates mitochondrial biogenesis in C2C12 myotubes and associates with oxidative capacity in humans
Houzelle, A., Dahlmans, D., Nascimento, E. B. M., Schaart, G., Jörgensen, J. A., Moonen‐Kornips, E., Kersten, S., Wang, X., & Hoeks, J. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.29797 · Cited by 28
Nrf2 Pathway and Autophagy Crosstalk: New Insights into Therapeutic Strategies for Ischemic Cerebral Vascular Diseases
Hu, Y. H., Luo, Y., & Zheng, Y. (2022) · Antioxidants · doi:10.3390/antiox11091747 · Cited by 29
Cornerstone Cellular Pathways for Metabolic Disorders and Diabetes Mellitus: Non-Coding RNAs, Wnt Signaling, and AMPK
Maiese, K. (2023) · Cells · doi:10.3390/cells12222595 · Cited by 30
Muscle Glycogen Remodeling and Glycogen Phosphate Metabolism following Exhaustive Exercise of Wild Type and Laforin Knockout Mice
Irimia, J. M., Tagliabracci, V. S., Meyer, C. M., Segvich, D. M., DePaoli-Roach, A. A., & Roach, P. J. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.673897 · Cited by 28
Aerobic training as an adjunctive therapy to enzyme replacement in Pompe disease
Nilsson, M. I., Samjoo, I. A., Hettinga, B. P., Koeberl, D. D., Zhang, H., Hawke, T. J., Nissar, A. A., Ali, T., Brandt, L., Ansari, M. U., et al. (2012) · Molecular Genetics and Metabolism · doi:10.1016/j.ymgme.2012.09.010 · Cited by 28
Autophagy and Obesity-Related Lung Disease
Pabón, M. A., Ma, K. C., & Choi, A. M. K. (2016) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2016-0045ps · Cited by 30
Factors that Affect Pancreatic Islet Cell Autophagy in Adult Rats: Evaluation of a Calorie-Restricted Diet and a High-Fat Diet
Sun, Q., Nie, S., Wang, L., Yang, F., Meng, Z., Xiao, H., Xiang, B., Li, X., Fu, X., & Wang, S. (2016) · PLoS ONE · doi:10.1371/journal.pone.0151104 · Cited by 29
Self-citation
The Combination of Physical Exercise with Muscle‐Directed Antioxidants to Counteract Sarcopenia: A Biomedical Rationale for Pleiotropic Treatment with Creatine and Coenzyme Q10
Guescini, M., Tiano, L., Genova, M. L., Polidori, E., Silvestri, S., Orlando, P., Fimognari, C., Calcabrini, C., Stocchi, V., & Sestili, P. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/7083049 · Cited by 32
Effects of eccentric, concentric and eccentric/concentric training on muscle function and mass, functional performance, cardiometabolic health, quality of life and molecular adaptations of skeletal muscle in COPD patients: a multicentre randomised trial
Peñailillo, L., Valladares-Ide, D., Jannas-Vela, S., Flores‐Opazo, M., Jalón, M., I, L. M., Nuñez, I., & Orlando Díaz, P. (2022) · BMC Pulmonary Medicine · doi:10.1186/s12890-022-02061-4 · Cited by 31
Atg4B and Cathepsin B-Triggered in Situ Luciferin Formation for Precise Cancer Autophagy Bioluminescence Imaging
Cheng, X., Xia, T., Sun, X., Liang, G., Liu, X., & Liang, G. (2023) · ACS Central Science · doi:10.1021/acscentsci.3c00696 · Cited by 27
Aerobic exercise suppresses CCN2 secretion from senescent muscle stem cells and boosts muscle regeneration in aged mice
Li, F., Zhang, F., Shi, H., Xia, H., Wei, X., Liu, S., Wu, T., Li, Y., Feng, S., Chen, M., et al. (2024) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.13526 · Cited by 28
Mechanisms underlying the interplay between autophagy and the inflammasome in age-related diseases: Implications for exercise immunology
Ramos, E. L. P., Neto, I. V. D. S., Pinto, A. P., Cintra, D. E., Ropelle, E. R., Pauli, J., de Freitas, E. C., Mineo, T. W. P., & da Silva, A. S. R. (2025) · Ageing Research Reviews · doi:10.1016/j.arr.2025.102821 · Cited by 30
Impaired response to exercise intervention in the vasculature in metabolic syndrome
Knaub, L. A., McCune, S. A., Chicco, A. J., Miller, M. W., Moore, R. L., Birdsey, N., Lloyd, M. I., Villarreal, J., Keller, A. C., Watson, P. A., et al. (2012) · Diabetes and Vascular Disease Research · doi:10.1177/1479164112459664 · Cited by 27
Therapeutic Approaches in Mitochondrial Dysfunction, Inflammation, and Autophagy in Uremic Cachexia: Role of Aerobic Exercise
Zhang, Y., Liu, Y., Bi, X., Hu, C., Ding, F. H., & Ding, W. Q. (2019) · Mediators of Inflammation · doi:10.1155/2019/2789014 · Cited by 27
Exercise Enhances Branched-Chain Amino Acid Catabolism and Decreases Cardiac Vulnerability to Myocardial Ischemic Injury
Wu, G., Guo, Y., Li, M., Li, C., Tan, Y., Li, Y., Li, J., Wang, L., Zhang, X., & Gao, F. (2022) · Cells · doi:10.3390/cells11101706 · Cited by 28
Signaling pathways underlying skeletal muscle wasting in experimental pulmonary arterial hypertension
Moreira‐Gonçalves, D., Padrão, A. I., Ferreira, R. M., Justino, J., Nogueira‐Ferreira, R., Neuparth, M. J., Vitorino, R. M. P., Fonseca, H., Silva, A. F., Duarte, J. A., et al. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.10.002 · Cited by 27
Reviving the protein quality control system: Therapeutic target for cardiac disease in the elderly
Meijering, R. A. M., Henning, R. H., & Brundel, B. J. J. M. (2014) · Trends in Cardiovascular Medicine · doi:10.1016/j.tcm.2014.10.013 · Cited by 27
C-myb Regulates Autophagy for Pulp Vitality in Glucose Oxidative Stress
Lee, Y. H., Kim, H. S., Kim, J. S., Yu, M.-K., Cho, S. D., Jeon, J., & Yi, H. (2015) · Journal of Dental Research · doi:10.1177/0022034515622139 · Cited by 27
Induction of autophagy by ARHI (DIRAS3) alters fundamental metabolic pathways in ovarian cancer models
Ornelas, A., McCullough, C., Lü, Z., Zacharias, N. M., Kelderhouse, L. E., Gray, J. P., Yang, H., Engel, B. J., Wang, Y., Mao, W., et al. (2016) · BMC Cancer · doi:10.1186/s12885-016-2850-8 · Cited by 27
Mcl-1-mediated mitochondrial fission protects against stress but impairs cardiac adaptation to exercise
Moyzis, A. G., Lally, N. S., Liang, W., Leon, L. J., Najor, R. H., Orogo, A. M., & Gustafsson, Å. B. (2020) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2020.07.009 · Cited by 27
Late‐in‐life treadmill training rejuvenates autophagy, protein aggregate clearance, and function in mouse hearts
Cho, J. M., Park, S., Ghosh, R., Ly, K., Ramous, C., Thompson, L., Hansen, M., Mattera, M. S. D. L. C., Pires, K. M. P., Ferhat, M., et al. (2021) · Aging Cell · doi:10.1111/acel.13467 · Cited by 29
Effects of long-term resistance exercise training on autophagy in rat skeletal muscle of chloroquine-induced sporadic inclusion body myositis
Kwon, I., Lee, Y., Cosío-Lima, L., Cho, J., & Yeom, D.-C. (2015) · Physical Activity and Nutrition · doi:10.5717/jenb.2015.15090710 · Cited by 27
Understanding cellular senescence: pathways involved, therapeutics and longevity aiding
Kumar, A., & Thirumurugan, K. (2023) · Cell Cycle · doi:10.1080/15384101.2023.2287929 · Cited by 31
The physiological response of protease inhibition in dystrophic muscle
Hollinger, K., & Selsby, J. T. (2013) · Acta Physiologica · doi:10.1111/apha.12114 · Cited by 26
MiR-129-3p favors intracellular BCG survival in RAW264.7 cells by inhibiting autophagy via Atg4b
Qu, Y., Ding, S., Ma, Z., Jiang, D., Xu, X., Zhang, Y., Zhang, A., & Xu, G. (2019) · Cellular Immunology · doi:10.1016/j.cellimm.2019.01.004 · Cited by 27
Role of environmental factors in the pathogenesis of Crohn’s disease: a critical review
Chen, Y., Wang, Y., & Shen, J. (2019) · International Journal of Colorectal Disease · doi:10.1007/s00384-019-03441-9 · Cited by 26
Energy Metabolism in Exercise-Induced Physiologic Cardiac Hypertrophy
Xiang, K., Qin, Z., Zhang, H., & Liu, X. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.01133 · Cited by 26
Quantitative phosphoproteomic analyses identify STK11IP as a lysosome-specific substrate of mTORC1 that regulates lysosomal acidification
Zi, Z., Zhang, Z., Feng, Q., Kim, C., Wang, X., Scherer, P. E., Gao, J., Levine, B., & Yu, Y. (2022) · Nature Communications · doi:10.1038/s41467-022-29461-8 · Cited by 26
Self-citation
Evidence for a neuromuscular circuit involving hypothalamic interleukin-6 in the control of skeletal muscle metabolism
Katashima, C. K., Micheletti, T. O., Braga, R. R., Gaspar, R. S., Goeminne, L. J. E., Moura‐Assis, A., Crisol, B., Brícola, R. S., Silva, V. R. R., Ramos, C. D. O., et al. (2022) · Science Advances · doi:10.1126/sciadv.abm7355 · Cited by 26
Detrimental effects of proteasome inhibition activity in Drosophila melanogaster: implication of ER stress, autophagy, and apoptosis
Velentzas, P. D., Velentzas, A. D., Mpakou, V., Antonelou, M. H., Margaritis, L. H., Papassideri, I. S., & Stravopodis, D. J. (2012) · Cell Biology and Toxicology · doi:10.1007/s10565-012-9235-9 · Cited by 29
Differences in the starvation-induced autophagy response in MDA-MB-231 and MCF-7 breast cancer cells
Zhu, W., Qu, H., Xu, K., Jia, B., Li, H., Yi-min, D., Liu, G., Wei, H., & Zhao, H. (2017) · Animal Cells and Systems · doi:10.1080/19768354.2017.1330763 · Cited by 26
Changes in Autophagy Levels in Rat Myocardium During Exercise Preconditioning-Initiated Cardioprotective Effects
Li, J.-Y., Pan, S.-S., Wang, J., & Lu, J. (2019) · International Heart Journal · doi:10.1536/ihj.18-310 · Cited by 26
The balance of apoptosis and autophagy via regulation of the AMPK signal pathway in aging rat striatum during regular aerobic exercise
Liu, W., Wang, Z., Xia, Y., Kuang, H., Liu, S., Li, L., Tang, C., & Yin, D. (2019) · Experimental Gerontology · doi:10.1016/j.exger.2019.110647 · Cited by 26
Exercise Mitigates the Loss of Muscle Mass by Attenuating the Activation of Autophagy during Severe Energy Deficit
Martín-Rincón, M., Pérez‐López, A., Morales‐Álamo, D., Pérez-Suárez, I., de Pablos-Velasco, P. L., Perez‐Valera, M., Pérez-Regalado, S., Martinez‐Canton, M., Gelabert‐Rebato, M., Juan-Habib, J. W., et al. (2019) · Nutrients · doi:10.3390/nu11112824 · Cited by 26
Vascular ageing in hypertension: Focus on mitochondria
Forte, M., Stanzione, R., Cotugno, M., Bianchi, F., Marchitti, S., & Rubattu, S. D. (2020) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2020.111267 · Cited by 26
Degradation of Misfolded Proteins by Autophagy: Is it a Strategy for Huntington's Disease Treatment?
Lin, F., & Qin, Z. (2013) · Journal of Huntington s Disease · doi:10.3233/jhd-130052 · Cited by 26
A Healthy Heart and a Healthy Brain: Looking at Mitophagy
Luo, H., Zhang, R., Krigman, J., McAdams, A., Ozgen, S., & Sun, N. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00294 · Cited by 25
An Intronic Risk SNP rs12454712 for Central Obesity Acts As an Allele-Specific Enhancer To Regulate BCL2 Expression
Dong, S., Zhu, D., Zhou, X., Rong, Y., Zeng, M., Chen, J., Jiang, F., Tuo, X.-M., Feng, Z., Yang, T., et al. (2021) · Diabetes · doi:10.2337/db20-1151 · Cited by 25
Effects and Mechanisms of Saikosaponin D Improving the Sensitivity of Human Gastric Cancer Cells to Cisplatin
Hu, J., Li, P., Shi, B., & Tie, J. (2021) · ACS Omega · doi:10.1021/acsomega.1c01795 · Cited by 25
Apoptosis in Type 2 Diabetes: Can It Be Prevented? Hippo Pathway Prospects
Kilanowska, A., & Ziółkowska, A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23020636 · Cited by 25
Potential molecular mechanism of exercise reversing insulin resistance and improving neurodegenerative diseases
Shen, J., Wang, X., Wang, M., & Zhang, H. (2024) · Frontiers in Physiology · doi:10.3389/fphys.2024.1337442 · Cited by 25
1α,25(OH)2D3 downregulates gene expression levels of muscle ubiquitin ligases MAFbx and MuRF1 in human myotubes
Hayakawa, N., Fukumura, J., Yasuno, H., Fujimoto-Ouchi, K., & Kitamura, H. (2015) · Biomedical Research · doi:10.2220/biomedres.36.71 · Cited by 25
Targeting intracellular degradation pathways for treatment of liver disease caused by α1-antitrypsin deficiency
Wang, Y., & Perlmutter, D. H. (2013) · Pediatric Research · doi:10.1038/pr.2013.190 · Cited by 26
Derailed Proteostasis as a Determinant of Cardiac Aging
Wiersma, M., Henning, R. H., & Brundel, B. J. J. M. (2016) · Canadian Journal of Cardiology · doi:10.1016/j.cjca.2016.03.005 · Cited by 26
Cardioprotection of exercise preconditioning involving heat shock protein 70 and concurrent autophagy: a potential chaperone-assisted selective macroautophagy effect
Yuan, Y., Pan, S.-S., & Shen, Y. (2016) · The Journal of Physiological Sciences · doi:10.1007/s12576-016-0507-7 · Cited by 25
Current Status of Autophagy Enhancers in Metabolic Disorders and Other Diseases
Park, K., & Lee, M. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.811701 · Cited by 24
Unacylated ghrelin restores insulin and autophagic signaling in skeletal muscle of diabetic mice
Tam, B. T., Pei, X. M., Yung, B. Y., Yip, S. P., Chan, L., Wong, S. C. C., & Siu, P. M. (2015) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-015-1721-5 · Cited by 24
Emerging role of protein kinase C in energy homeostasis: A brief overview
Mehta, K. D. (2014) · World Journal of Diabetes · doi:10.4239/wjd.v5.i3.385 · Cited by 25
Cardiac Kinetophagy Coincides with Activation of Anabolic Signaling
Lee, Y., Kang, E., Kwon, I., Cosío-Lima, L., Cavnar, P. J., & Javan, G. T. (2015) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000774 · Cited by 24
A ketogenic amino acid rich diet benefits mitochondrial homeostasis by altering the AKT/4EBP1 and autophagy signaling pathways in the gastrocnemius and soleus
Li, J., Kanasaki, M., Xu, L., Kitada, M., Nagao, K., Adachi, Y., Jinzu, H., Noguchi, Y., Kohno, M., Kanasaki, K., et al. (2018) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2018.03.013 · Cited by 26
AMP-Activated Protein Kinase Mediates the Effect of Leptin on Avian Autophagy in a Tissue-Specific Manner
Piekarski, A., Nagarajan, G., Ishola, P., Flees, J. J., Greene, E. S., Kuenzel, W. J., Ohkubo, T., Maier, H. J., Bottje, W. G., Cline, M. A., et al. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00541 · Cited by 25
The TOR Pathway at the Neuromuscular Junction: More Than a Metabolic Player?
Castets, P., Ham, D. J., & Rüegg, M. A. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.00162 · Cited by 29
Autophagy in Muscle of Glucose-Infusion Hyperglycemia Rats and Streptozotocin-Induced Hyperglycemia Rats via Selective Activation of m-TOR or FoxO3
Lv, P., Huang, J. Y., Yang, J., Deng, Y., Xu, J. H., Zhang, X., Li, W., Zhang, H., & Yang, Y. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087254 · Cited by 23
Retracted
Autophagy is required for performance adaptive response to resistance training and exercise‐induced adult neurogenesis
Codina‐Martínez, H., Fernández‐Garcia, B., Díez‐Planelles, C., Fernández, Á. F., Higarza, S. G., Fernández‐Sanjurjo, M., Díez‐Robles, S., Iglesias‐Gutiérrez, E., & Tomás‐Zapico, C. (2019) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.13586 · Cited by 23
Exercise and Training Regulation of Autophagy Markers in Human and Rat Skeletal Muscle
Botella, J., Jamnick, N. A., Granata, C., Genders, A. J., Perri, E., Jabar, T., GARNHAM, A. P., Lazarou, M., & Bishop, D. J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052619 · Cited by 24
Mitochondrial Quality Control in the Heart: The Balance between Physiological and Pathological Stress
Fajardo, G., Coronado, M. J., Matthews, M. D., & Bernstein, D. (2022) · Biomedicines · doi:10.3390/biomedicines10061375 · Cited by 23
Autophagy downregulation contributes to insulin resistance mediated injury in insulin receptor knockout podocytes in vitro
Xu, Y., Zhou, Q., Xin, W., Li, Z., Chen, L., & Wan, Q. (2016) · PeerJ · doi:10.7717/peerj.1888 · Cited by 23
Erythropoietin Reduces Insulin Resistance via Regulation of Its Receptor-Mediated Signaling Pathways in db/db Mice Skeletal Muscle
Pan, Y., Yang, X. H., Guo, L., Gu, Y. H., Qiao, Q. Y., & Jin, H. M. (2017) · International Journal of Biological Sciences · doi:10.7150/ijbs.19752 · Cited by 23
Training state and skeletal muscle autophagy in response to 36 h of fasting
Dethlefsen, M. M., Bertholdt, L., Gudiksen, A., Stankiewicz, T., Bangsbo, J., van Hall, G., Plomgaard, P., & Pilegaard, H. (2018) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01146.2017 · Cited by 23
Downhill Running Acutely Elicits Mitophagy in Rat Soleus Muscle
Shang, H., Xia, Z., Bai, S.-C., ZHANG, H., Gu, B., & Wang, R. (2019) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001906 · Cited by 23
Nutrition and exercise in Pompe disease
Tarnopolsky, M. A., & Nilsson, M. I. (2019) · Annals of Translational Medicine · doi:10.21037/atm.2019.05.52 · Cited by 23
Moderate, but Not Excessive, Training Attenuates Autophagy Machinery in Metabolic Tissues
da Rocha, A. L., Pinto, A. P., Morais, G. P., Marafon, B. B., Rovina, R. L., Veras, A. S. C., Teixeira, G. R., Pauli, J. R., de Moura, L. P., Cintra, D. E., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228416 · Cited by 24
Cellular Protein Quality Control in Diabetic Cardiomyopathy: From Bench to Bedside
Kaur, N., Raja, R., Ruiz‐Velasco, A., & Liu, W. (2020) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2020.585309 · Cited by 24
Autophagy in Skeletal MusclePreprint
Franco‐Romero, A., Sandri, M., & Schiaffino, S. (2024) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a041565 · Cited by 23
Sexual dimorphisms in skeletal muscle: current concepts and research horizons
Emmert, M. E., Emmert, A. S., Goh, Q., & Cornwall, R. (2024) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00529.2023 · Cited by 24
Autophagy transduces physical constraints into biological responses
Dupont, N., & Codogno, P. (2016) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2016.08.021 · Cited by 22
Endurance exercise-induced expression of autophagy-related protein coincides with anabolic expression and neurogenesis in the hippocampus of the mouse brain
Jang, Y. (2020) · Neuroreport · doi:10.1097/wnr.0000000000001431 · Cited by 22
Autophagy takes it all – autophagy inducers target immune aging
Zinecker, H., & Simon, A. K. (2022) · Disease Models & Mechanisms · doi:10.1242/dmm.049345 · Cited by 22
AMPK, a metabolic sensor, is involved in isoeugenol-induced glucose uptake in muscle cells
Kim, N., Lee, J. O., Lee, H., Lee, Y. W., Kim, H. I., Kim, S. J., Park, S. H., Lee, C. S., Ryoo, S. W., Hwang, G., et al. (2015) · Journal of Endocrinology · doi:10.1530/joe-15-0302 · Cited by 22
Cardiac hypertrophy is stimulated by altered training intensity and correlates with autophagy modulation in male Wistar rats
Gunadi, J. W., Tarawan, V. M., Setiawan, I. B., Lesmana, R., Wahyudianingsih, R., & Supratman, U. (2019) · BMC Sports Science Medicine and Rehabilitation · doi:10.1186/s13102-019-0121-0 · Cited by 24
Trends and risk factors of elderly-onset Crohn’s disease: A nationwide cohort study
Moon, J. M., Kang, E. A., Han, K., Hong, S. W., Soh, H., Park, S., Lee, J., Lee, H. J., Im, J. P., & Kim, J. S. (2020) · World Journal of Gastroenterology · doi:10.3748/wjg.v26.i4.404 · Cited by 22
Recent progress regarding the role of autophagy in cardiac disease
Maejima, Y., Titus, A. S., Zablocki, D., & Sadoshima, J. (2025) · Cardiovascular Research · doi:10.1093/cvr/cvaf203 · Cited by 22
Yunpi Heluo decoction attenuates insulin resistance by regulating SIRT1-FoxO1 autophagy pathway in skeletal muscle of Zucker diabetic fatty rats
Mao, Z.-J., Xia, W.-S., & Chai, F. (2021) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2021.113828 · Cited by 21
Autophagic response to exercise in peripheral blood mononuclear cells from young men is intensity-dependent and is altered by exposure to environmental heat
McCormick, J. J., Côté, M. D., King, K. E., McManus, M. K., Goulet, N., Dokładny, K., Moseley, P. L., & Kenny, G. P. (2022) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00110.2022 · Cited by 21
CHCHD4-TRIAP1 regulation of innate immune signaling mediates skeletal muscle adaptation to exercise
Ma, J., Wang, P., Zhuang, J., Son, A. Y., Karius, A. K., Syed, A. M., Nishi, M., Wu, Z., Mori, M. P., Kim, Y., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113626 · Cited by 21
Anticancer activities of self-assembled molecular bowls containing a phenanthrene-based donor and Ru(II) acceptors
An, S. S. A., Chi, K., Kim, I., Song, Y. H., Singh, N., Jeong, Y. J., Kwon, J. E., Kim, H., Cho, Y. H., & Kang, S. C. (2015) · International Journal of Nanomedicine · doi:10.2147/ijn.s88287 · Cited by 21
Role of the ubiquitin-proteasome system and autophagy in regulation of insulin sensitivity in serum-starved 3T3-L1 adipocytes
Zhang, Y., Ye, M., Chen, L. J., Li, M., Tang, Z., & Wang, C. (2015) · Endocrine Journal · doi:10.1507/endocrj.ej15-0030 · Cited by 21
Endurance exercise training induces fat depot-specific differences in basal autophagic activity
Tanaka, G., Kato, H., & Izawa, T. (2015) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.09.061 · Cited by 21
201st ENMC International Workshop: Autophagy in muscular dystrophies – Translational approach, 1–3 November 2013, Bussum, The Netherlands
Merlini, L., & Nishino, I. (2014) · Neuromuscular Disorders · doi:10.1016/j.nmd.2014.03.009 · Cited by 22
Effects of exercise and dietary epigallocatechin gallate and β-alanine on skeletal muscle in aged mice
Pence, B. D., Gibbons, T. E., Bhattacharya, T. K., Mach, H. C., Ossyra, J. M., Petr, G. T., Martin, S. A., Wang, L., Rubakhin, S. S., Sweedler, J. V., et al. (2015) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2015-0372 · Cited by 21
High‐intensity interval training changes the expression of muscle RING‐finger protein‐1 and muscle atrophy F‐box proteins and proteins involved in the mechanistic target of rapamycin pathway and autophagy in rat skeletal muscle
Cui, X., Zhang, Y., Wang, Z., Yu, J., Kong, Z., & Ružić, L. (2019) · Experimental Physiology · doi:10.1113/ep087601 · Cited by 21
Repeated eccentric contractions positively regulate muscle oxidative metabolism and protein synthesis during cancer cachexia in mice
Hardee, J. P., Fix, D. K., Koh, H., Wang, X., Goldsmith, E. C., & Carson, J. A. (2020) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00908.2019 · Cited by 21
Adaptation of rat fast‐twitch muscle to endurance activity is underpinned by changes to protein degradation as well as protein synthesis
Hesketh, S. J., Sutherland, H., Lisboa, P. J. G., Jarvis, J. C., & Burniston, J. G. (2020) · The FASEB Journal · doi:10.1096/fj.202000668rr · Cited by 21
Autophagy plays a positive role in induction of epidermal proliferation
Wang, J., Kaplan, N., Wang, S., Yang, W., Wang, L., He, C., & Peng, H. (2020) · The FASEB Journal · doi:10.1096/fj.202000770rr · Cited by 21
Self-citation
Regular exercise stimulates endothelium autophagy via IL‐1 signaling in ApoE deficient mice
Okutsu, M., Yamada, M., Tokizawa, K., Marui, S., Suzuki, K., Lira, V. A., & Nagashima, K. (2021) · The FASEB Journal · doi:10.1096/fj.202002790rr · Cited by 21
Short-term intensified training temporarily impairs mitochondrial respiratory capacity in elite endurance athletes
Cardinale, D. A., Gejl, K. D., Petersen, K. G., Nielsen, J., Ørtenblad, N., & Larsen, F. J. (2021) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00829.2020 · Cited by 22
Cardioprotective responses to aerobic exercise-induced physiological hypertrophy in zebrafish heart
Chen, Z., Zhou, Z., Peng, X., Sun, C., Yang, D. K., Li, C., Zhu, R., Zhang, P., Zheng, L., & Tang, C. (2021) · The Journal of Physiological Sciences · doi:10.1186/s12576-021-00818-w · Cited by 21
Electroacupuncture preconditioning and postconditioning inhibit apoptosis and neuroinflammation induced by spinal cord ischemia reperfusion injury through enhancing autophagy in rats
Fang, B., Qin, M., Li, Y., Li, X., Tan, W., Zhang, Y., & Ma, H. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.02.010 · Cited by 20
Metabolic Remodeling in Skeletal Muscle Atrophy as a Therapeutic Target
Renzini, A., Riera, C. S., Minic, I., D’Ercole, C., Lozanoska‐Ochser, B., Cedola, A., Gigli, G., Moresi, V., & Madaro, L. (2021) · Metabolites · doi:10.3390/metabo11080517 · Cited by 22
Self-citation
Occupational physical activity differentially affects the risk for developing later-onset Crohn’s disease and ulcerative colitis among middle-aged and older populations
Furuya, Y., Fukai, K., Nakazawa, S., Kojimahara, N., Hoshi, K., Toyota, A., & Tatemichi, M. (2021) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365521.2021.1999495 · Cited by 20
Exercise alters the circadian rhythm of REV-ERB-α and downregulates autophagy-related genes in peripheral and central tissues
da Rocha, A. L., Pinto, A. P., Bedo, B. L. S., Morais, G. P., Oliveira, L. C., Carolino, R. O. G., Pauli, J. R., Simabuco, F. M., de Moura, L. P., Ropelle, E. R., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-24277-4 · Cited by 21
Autophagy and Macropinocytosis: Keeping an Eye on the Corneal/Limbal Epithelia
Peng, H., Park, J. K., & Lavker, R. M. (2017) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.16-21111 · Cited by 20
High intensity aerobic exercise training improves chronic intermittent hypoxia-induced insulin resistance without basal autophagy modulation
Pauly, M., Assense, A., Rondon, A., Thomas, A., Dubouchaud, H., Freyssenet, D. G., Benoit, H., Castells, J., & Flore, P. (2017) · Scientific Reports · doi:10.1038/srep43663 · Cited by 21
Genetic enhancement of macroautophagy in vertebrate models of neurodegenerative diseases
Ejlerskov, P., Ashkenazi, A., & Rubinsztein, D. C. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.04.001 · Cited by 20
Autophagy Is a Promoter for Aerobic Exercise Performance during High Altitude Training
Zhang, Y., & Chen, N. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/3617508 · Cited by 20
Impact of liver PGC-1α on exercise and exercise training-induced regulation of hepatic autophagy and mitophagy in mice on HFF
Dethlefsen, M. M., Kristensen, C. M., Tøndering, A. S., Lassen, S. B., Ringholm, S., & Pilegaard, H. (2018) · Physiological Reports · doi:10.14814/phy2.13731 · Cited by 20
Alterations of Cardiac KATP Channels and Autophagy Contribute in the Late Cardioprotective Phase of Exercise Preconditioning
Lu, J., Pan, S.-S., Wang, Q., & Yuan, Y. (2018) · International Heart Journal · doi:10.1536/ihj.17-003 · Cited by 20
Exercise and Hormesis
Radak, Z. O., & Taylor, A. W. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-814253-0.00005-x · Cited by 20

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

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

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

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks