Autophagy-related and autophagy-regulatory genes are induced in human muscle after ultraendurance exercise
Open accessAbstract
The purpose of this study was to evaluate whether ultra endurance exercise changes the mRNA levels of the autophagy-related and autophagy-regulatory genes. Eight men (44 ± 1 years, range: 38-50 years) took part in a 200-km running race. The average running time was 28 h 03 min ± 2 h 01 min (range: 22 h 15 min-35 h 04 min). A muscle sample was taken from the vastus lateralis 2 weeks prior to the race and 3 h after arrival. Gene expression was assessed by RT-qPCR. Transcript levels of autophagy-related genes were increased by 49% for ATG4b (P = 0.025), 57% for ATG12 (P = 0.013), 286% for Gabarapl1 (P = 0.008) and 103% for LC3b (P = 0.011). The lysosomal enzyme cathepsin L mRNA was upregulated by 123% (P = 0.003). Similarly, transcript levels of the autophagy-regulatory genes BNIP3 and BNIP3l were both increased by 113% (P = 0.031 and P = 0.007, respectively). Since upregulation of these genes has been related with an increased autophagic flux in various models, our results strongly suggest that autophagy is activated in response to ultra endurance exercise.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Vastus lateralis biopsies from human runners after a 200-kilometer race showed increased transcription of autophagy factors ATG4B, ATG12, GABARAPL1, LC3B, CSTL, BNIP3, and BNIP3L.
“Similarly, vastus lateralis biopsies taken from human runners after a 200-kilometer race showed increased transcription of autophagy factors ATG4B, ATG12, GABARAPL1, LC3B, CSTL (cathepsin L), BNIP3, and BNIP3L [487],”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [487]
Increased transcription of autophagy factors after a 200-kilometer race may be an adaptive response to muscle injury related to long-distance running.
“which may be an adaptive response to muscle injury related to long-distance running.”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [487]
Cites
Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T., & Ohsumi, Y. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-09-0704 · Cited by 2,323 · see citing works
FoxO3 Controls Autophagy in Skeletal Muscle In Vivo
Mammucari, C., Milan, G., Romanello, V., Masiero, E., Rudolf, R., Del Piccolo, P., Burden, S. J., Di Lisi, R., Sandri, C., Zhao, J., et al. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.11.001 · Cited by 1,953 · see citing works
Autophagy Is Activated for Cell Survival after Endoplasmic ReticulumStress
Ogata, M., Hino, S.-I., Saito, A., Morikawa, K., Kondo, S., Kanemoto, S., Murakami, T., Taniguchi, M., Tanii, I., Yoshinaga, K., et al. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.01453-06 · Cited by 1,832 · see citing works
Zhao, J., Brault, J. J., Schild, A., Cao, P., Sandri, M., Schiaffino, S., Lecker, S. H., & Goldberg, A. L. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.11.004 · Cited by 1,489 · see citing works
A Unified Nomenclature for Yeast Autophagy-Related Genes
Klionsky, D. J., Cregg, J. M., Dunn, W. A., Emr, S. D., Sakai, Y., Sandoval, I. V., Sibirny, A. А., Subramani, S. E., Thumm, M., Marten Veenhuis, A., et al. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00296-x · Cited by 1,267 · see citing works
Autophagy: A lysosomal degradation pathway with a central role in health and disease
Eskelinen, E., & Säftig, P. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2008.07.014 · Cited by 699 · see citing works
Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy
Hamacher-Brady, A., Brady, N. R., Logue, S. E., Sayen, M. R., Jinno, M., Kirshenbaum, L. A., Gottlieb, R. A., & Gustafsson, Å. B. (2007) · Cell Death & Differentiation · doi:10.1038/sj.cdd.4401936 · Cited by 609 · see citing works
The Molecular Mechanism of Autophagy
Wang, C.-W., & Klionsky, D. J. (2003) · Molecular Medicine · doi:10.1007/bf03402040 · Cited by 530 · see citing works
Skeletal Muscle Is a Primary Target of SOD1G93A-Mediated Toxicity
Dobrowolny, G., Aucello, M., Rizzuto, E., Beccafico, S., Mammucari, C., Bonconpagni, S., Belia, S., Wannenes, F., Nicoletti, C., Del Prete, Z., et al. (2008) · Cell Metabolism · doi:10.1016/j.cmet.2008.09.002 · Cited by 513 · see citing works
Sandri, M. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.01.056 · Cited by 451 · see citing works
Injury to skeletal muscle fibers of mice following lengthening contractions
McCully, K. K., & Faulkner, J. A. (1985) · Journal of Applied Physiology · doi:10.1152/jappl.1985.59.1.119 · Cited by 408 · see citing works
Proteolytic and lipolytic responses to starvation
Finn, P. F., & Dice, J. F. (2006) · Nutrition · doi:10.1016/j.nut.2006.04.008 · Cited by 321 · see citing works
Downstream of Akt: FoxO3 and mTOR in the regulation of autophagy in skeletal muscle
Mammucari, C., Schiaffino, S., & Sandri, M. (2008) · Autophagy · doi:10.4161/auto.5905 · Cited by 295 · see citing works
Protein requirements for endurance athletes
Tarnopolsky, M. (2004) · Nutrition · doi:10.1016/j.nut.2004.04.008 · Cited by 242 · see citing works
The requirement of uncoordinated 51-like kinase 1 (ULK1) and ULK2 in the regulation of autophagy
Lee, E.-J., & Tournier, C. (2011) · Autophagy · doi:10.4161/auto.7.7.15450 · Cited by 186 · see citing works
Protein Requirements for Endurance Athletes
Tarnopolsky, M. A. (2004) · European Journal of Sport Science · doi:10.1080/17461390400074102 · Cited by 175 · see citing works
Coordinate activation of autophagy and the proteasome pathway by FoxO transcription factor
Zhao, J., Brault, J. J., Schild, A., & Goldberg, A. L. (2008) · Autophagy · doi:10.4161/auto.5633 · Cited by 164 · see citing works
Deldicque, L., Atherton, P. J., Patel, R. S., Theisen, D., Nielens, H., Rennie, M. J., & Francaux, M. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00873.2007 · Cited by 141 · see citing works
Self-citationFuel economy in food‐deprived skeletal muscle: signaling pathways and regulatory mechanisms
de Lange, P., Moreno, M., Silvestri, E., Lombardi, A., Goglia, F., & Lanni, A. (2007) · The FASEB Journal · doi:10.1096/fj.07-8527rev · Cited by 133 · see citing works
Feng, Z., Bai, L., Yan, J., Li, Y., Shen, W., Wang, Y., Wertz, K., Weber, P., Zhang, Y., Chen, Y., et al. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.03.001 · Cited by 111 · see citing works
Sahlin, K., Shabalina, I. G., Mattsson, C. M., Bakkman, L., Fernström, M., Rozhdestvenskaya, Z., Enqvist, J. K., Nedergaard, J., Ekblom, B. T., & Tonkonogi, M. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00966.2009 · Cited by 109 · see citing works
Autophagic response to strenuous exercise in mouse skeletal muscle fibers
Salminen, A., & Vihko, V. (1984) · Virchows Archiv B Cell Pathology Including Molecular Pathology · doi:10.1007/bf02889856 · Cited by 100 · see citing works
Kim, H. J., Jamart, C., Deldicque, L., An, G.-L., Lee, Y. H., Kim, C. K., Raymackers, J., & Francaux, M. (2010) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181e4c5d1 · Cited by 91 · see citing works
Self-citationRegulation of Mitochondrial Integrity, Autophagy and Cell Survival by BNIP3
Tracy, K., & Macleod, K. F. (2007) · Autophagy · doi:10.4161/auto.4892 · Cited by 69 · see citing works
Lysosomal changes in skeletal muscles during the repair of exercise injuries in muscle fibers.
Salminen, A. (1985) · PubMed · Cited by 27 · see citing works
Autophagy, proteases and the sense of balance
Cabrera, S., Mariño, G., Fernández, Á. F., & López-Otı́n, C. (2010) · Autophagy · doi:10.4161/auto.6.7.13065 · Cited by 27 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Protein breakdown in muscle wasting: Role of autophagy-lysosome and ubiquitin-proteasome
Sandri, M. (2013) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2013.04.023 · Cited by 689 · see citing works
Muscle wasting and cachexia in heart failure: mechanisms and therapies
von Haehling, S., Ebner, N., dos Santos, M. R., Springer, J., & Anker, S. D. (2017) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2017.51 · Cited by 427 · see citing works
Targeting autophagy in ischemic stroke: From molecular mechanisms to clinical therapeutics
Ajoolabady, A., Wang, S., Kroemer, G., Penninger, J. M., Uversky, V. N., Praticò, D., Henninger, N., Reiter, R. J., Bruno, A., JOSHIPURA, K. J., et al. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107848 · Cited by 334 · see citing works
Enhanced autophagy ameliorates cardiac proteinopathy
Bhuiyan, M. S., Pattison, J. S., Osinska, H., James, J., Gulick, J., McLendon, P. M., Hill, J. A., Sadoshima, J., & Robbins, J. (2013) · Journal of Clinical Investigation · doi:10.1172/jci70877 · Cited by 298 · see citing works
Muscle fiber type diversification during exercise and regeneration
Qaisar, R., Bhaskaran, S., & Van Remmen, H. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.03.025 · Cited by 283 · see citing works
Role of PGC-1α during acute exercise-induced autophagy and mitophagy in skeletal muscle
Vainshtein, A., Tryon, L. D., Pauly, M., & Hood, D. A. (2015) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00380.2014 · Cited by 273 · see citing works
Ferraro, E., Giammarioli, A. M., Chiandotto, S., Spoletini, I., & Rosano, G. M. C. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5773 · Cited by 265 · see citing works
Autophagy and aging: Maintaining the proteome through exercise and caloric restriction
Escobar, K. A., Cole, N. H., Mermier, C. M., & VanDusseldorp, T. A. (2018) · Aging Cell · doi:10.1111/acel.12876 · Cited by 226 · see citing works
Luo, L., Lu, A.-M., Wang, Y., Hong, A., Chen, Y., Hu, J., Li, X., & Qin, Z.-H. (2013) · Experimental Gerontology · doi:10.1016/j.exger.2013.02.009 · Cited by 192 · see citing works
Autophagy and ALS: mechanistic insights and therapeutic implications
Chua, J. P., De Calbiac, H., Kabashi, E., & Barmada, S. J. (2022) · Autophagy · doi:10.1080/15548627.2021.1926656 · Cited by 189 · see citing works
“Similarly, vastus lateralis biopsies taken from human runners after a 200-kilometer race showed increased transcription of autophagy factors ATG4B, ATG12, GABARAPL1, LC3B, CSTL (cathepsin L), BNIP3, and BNIP3L [487], which may be an adaptive response to muscle injury related to long-distance running.”
BackgroundJoseph, A., Adhihetty, P. J., & Leeuwenburgh, C. (2016) · The Journal of Physiology · doi:10.1113/jp270659 · Cited by 186 · see citing works
Schwalm, C., Jamart, C., Benoit, N., Naslain, D., Prémont, C., Prévet, J., Thienen, R. V., Deldicque, L., & Francaux, M. (2015) · The FASEB Journal · doi:10.1096/fj.14-267187 · Cited by 174 · see citing works
Self-citationUnravelling the mechanisms regulating muscle mitochondrial biogenesis
Hood, D. A., Tryon, L. D., Carter, H. N., Kim, Y., & Chen, C. C. W. (2016) · Biochemical Journal · doi:10.1042/bcj20160009 · Cited by 159 · see citing works
Modulation of autophagy and ubiquitin-proteasome pathways during ultra-endurance running
Jamart, C., Francaux, M., Millet, G. Y., Deldicque, L., Frère, D., & Féasson, L. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00952.2011 · Cited by 157 · see citing works
Self-citationAutophagy is essential to support skeletal muscle plasticity in response to endurance exercise
Sanchez, A. M. J., Bernardi, H., Py, G., & Candau, R. B. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00187.2014 · Cited by 143 · see citing works
Protein breakdown in cancer cachexia
Sandri, M. (2016) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2015.11.002 · Cited by 134 · see citing works
The regulation of autophagy during exercise in skeletal muscle
Vainshtein, A., & Hood, D. A. (2015) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00550.2015 · Cited by 132 · see citing works
Exercise-induced skeletal muscle signaling pathways and human athletic performance
Camera, D. M., Smiles, W. J., & Hawley, J. A. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.02.007 · Cited by 128 · see citing works
Mitochondrial Function and Mitophagy in the Elderly: Effects of Exercise
Moreira, O. C., Estébanez, B., Martínez‐Flórez, S., Fernández, J. A. D. P., Cuevas, M. J., & González‐Gallego, J. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/2012798 · Cited by 120 · 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
Andonian, P., Viallon, M., Goff, C. M. L., de Bourguignon, C., Tourel, C., Morel, J., Giardini, G., Gergelé, L., Millet, G. P., & Croisille, P. (2016) · PLoS ONE · doi:10.1371/journal.pone.0161855 · Cited by 117 · see citing works
Boyer‐Guittaut, M., Poillet-Perez, L., Liang, Q., Bôle‐Richard, E., Ouyang, X., Benavides, G. A., Chakrama, F. Z., Fraîchard, A., Darley-Usmar, V. M., Despouy, G., et al. (2014) · Autophagy · doi:10.4161/auto.28390 · Cited by 114 · see citing works
Kaspy, M. S., Hannaian, S. J., Bell, Z. W., & Churchward‐Venne, T. A. (2023) · Nutrition Research Reviews · doi:10.1017/s0954422423000197 · Cited by 109 · see citing works
Autophagy as a Potential Target for Sarcopenia: AUTOPHAGY REGULATION IN SARCOPENIA
Fan, J., Kou, X., Jia, S., Yang, X., Yang, Y., & Chen, N. (2016) · Journal of Cellular Physiology · doi:10.1002/jcp.25260 · Cited by 101 · see citing works
ATG4B/autophagin-1 regulates intestinal homeostasis and protects mice from experimental colitis
Cabrera, S., Fernández, Á. F., Mariño, G., Aguirre, A., Suárez, M. F., Español, Y., Vega, J. A., Laurà, R., Fueyo, A., Fernández-García, M. S., et al. (2013) · Autophagy · doi:10.4161/auto.24797 · Cited by 99 · see citing works
Acquired Muscle Weakness in the Surgical Intensive Care Unit
Farhan, H. N., Moreno‐Duarte, I., Latronico, N., ZAFONTE, R. D., & Eikermann, M. (2015) · Anesthesiology · doi:10.1097/aln.0000000000000874 · Cited by 99 · see citing works
Combination of exercise training and erythropoietin prevents cancer-induced muscle alterations
Pin, F., Busquets, S., Toledo, M., Camperi, A., López-Soriano, F. J., Costelli, P., Argilés, J. M. A., & Penna, F. (2015) · Oncotarget · doi:10.18632/oncotarget.6439 · Cited by 95 · see citing works
Hector, A. J., McGlory, C., Damas, F., Mazara, N., Baker, S. K., & Phillips, S. M. (2018) · The FASEB Journal · doi:10.1096/fj.201700158rr · Cited by 91 · see citing works
Autophagy in Skeletal Muscle Homeostasis and in Muscular Dystrophies
Grumati, P., & Bonaldo, P. (2012) · Cells · doi:10.3390/cells1030325 · Cited by 87 · see citing works
Exercise‐mediated modulation of autophagy in skeletal muscle
Martín-Rincón, M., Morales‐Álamo, D., & Calbet, J. A. L. (2017) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.12945 · Cited by 76 · see citing works
Assessment of skeletal muscle proteolysis and the regulatory response to nutrition and exercise
Pasiakos, S. M., & Carbone, J. W. (2014) · IUBMB Life · doi:10.1002/iub.1291 · Cited by 74 · see citing works
Gil, S., Kirwan, J. P., Murai, I. H., Dantas, W. S., Merege‐Filho, C. A. A., Ghosh, S., Shinjo, S. K., Pereira, R. M. R., Teodoro, W. R., Felau, S. M., et al. (2021) · Journal of Cachexia, Sarcopenia and Muscle · doi:10.1002/jcsm.12815 · Cited by 72 · see citing works
Regulation of Exercise-Induced Autophagy in Skeletal Muscle
Rocchi, A., & He, C. (2017) · Current Pathobiology Reports · doi:10.1007/s40139-017-0135-9 · Cited by 68 · see citing works
Skeletal muscle atrogenes: From rodent models to human pathologies
Taillandier, D., & Polge, C. (2019) · Biochimie · doi:10.1016/j.biochi.2019.07.014 · Cited by 66 · see citing works
Reciprocal Crosstalk Between Autophagic and Endocrine Signaling in Metabolic Homeostasis
Sinha, R. A., Singh, B. K., & Yen, P. M. (2016) · Endocrine Reviews · doi:10.1210/er.2016-1103 · Cited by 63 · see citing works
Mitochondrial dynamics in exercise physiology
Tanaka, T., Nishimura, A., Nishiyama, K., Goto, T., Numaga‐Tomita, T., & Nishida, M. (2019) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-019-02258-3 · Cited by 66 · see citing works
Exercise and the control of muscle mass in human
Francaux, M., & Deldicque, L. (2018) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-018-2217-x · Cited by 61 · see citing works
Self-citationAutophagic Cellular Responses to Physical Exercise in Skeletal Muscle
Tam, B. T., & Siu, P. M. (2014) · Sports Medicine · doi:10.1007/s40279-013-0140-z · Cited by 59 · see citing works
Autophagy-Dependent Beneficial Effects of ExercisePreprint
Halling, J. F., & Pilegaard, H. (2017) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a029777 · Cited by 57 · see citing works
Wu, N., Zheng, W., Zhou, Y., Tian, Y., Tang, M., Feng, X., Ashrafizadeh, M., Wang, Y. Z., Niu, X., Tambuwala, M. M., et al. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102428 · Cited by 56 · see citing works
Roberts, F. L., & Markby, G. R. (2021) · Cells · doi:10.3390/cells10102639 · Cited by 53 · see citing works
Acute environmental hypoxia induces LC3 lipidation in a genotype‐dependent manner
Masschelein, E., Thienen, R. V., D’Hulst, G., Hespel, P., Thomis, M. A., & Deldicque, L. (2013) · The FASEB Journal · doi:10.1096/fj.13-239863 · Cited by 53 · see citing works
Exercise, Autophagy, and Apoptosis
Mooren, F. C., & Krüger, K. (2015) · Progress in Molecular Biology and Translational Science · doi:10.1016/bs.pmbts.2015.07.023 · Cited by 50 · see citing works
Castets, P., Frank, S., Sinnreich, M., & Rüegg, M. A. (2016) · Journal of Neuromuscular Diseases · doi:10.3233/jnd-160153 · Cited by 49 · see citing works
Tarpey, M. D., Davy, K. P., McMillan, R. P., Bowser, S. M., Halliday, T. M., Boutagy, N. E., Davy, B. M., Frisard, M. I., & Hulver, M. W. (2017) · Molecular Metabolism · doi:10.1016/j.molmet.2017.10.006 · Cited by 50 · see citing works
Effects of skeletal muscle energy availability on protein turnover responses to exercise
Smiles, W. J., Hawley, J. A., & Camera, D. M. (2016) · Journal of Experimental Biology · doi:10.1242/jeb.125104 · Cited by 48 · see citing works
The therapeutic potential of exercise to treat cachexia
Lira, F. S., Antunes, B. M., Seelaender, M. C. L., & Neto, J. C. R. (2015) · Current Opinion in Supportive and Palliative Care · doi:10.1097/spc.0000000000000170 · Cited by 48 · see citing works
Protein and Mitochondria Quality Control Mechanisms and Cardiac Aging
Ghosh, R., Vinod, V., Symons, J. D., & Boudina, S. (2020) · Cells · doi:10.3390/cells9040933 · Cited by 49 · see citing works
Lack of Activation of Mitophagy during Endurance Exercise in Human
Schwalm, C., Deldicque, L., & Francaux, M. (2017) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001256 · Cited by 47 · see citing works
Self-citationAcute Endurance Exercise Induces Nuclear p53 Abundance in Human Skeletal Muscle
Tachtsis, B., Smiles, W. J., Lane, S. C., Hawley, J. A., & CAMERA, D. M. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00144 · Cited by 44 · see citing works
Exercise and the Regulation of Mitochondrial Turnover
Hood, D. A., Tryon, L. D., Vainshtein, A., Memme, J. M., Chen, C., Pauly, M., Crilly, M. J., & Carter, H. (2015) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2015.07.007 · Cited by 44 · see citing works
Self-Eating for Muscle Fitness: Autophagy in the Control of Energy Metabolism
Sebastián, D., & Antonio Zorzano, A. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.06.030 · Cited by 42 · see citing works
Huang, Y., Huang, X., Yang, Y., Wang, W., Yu, Y., & Qin, Q. (2014) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2014.12.031 · Cited by 37 · see citing works
Exercise-Induced Autophagy in Fatty Liver Disease
Chun, S. K., Lee, S., Yang, M., Leeuwenburgh, C., & Js, K. (2017) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000116 · Cited by 37 · see citing works
Gharehbagh, S. A., Azar, J. T., & Razi, M. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119585 · Cited by 36 · see citing works
Contrasting views on the role of AMPK in autophagy
Kim, D. (2024) · BioEssays · doi:10.1002/bies.202300211 · Cited by 37 · see citing works
Bayod, S., del Valle, J., Pelegrı́, C., Vilaplana, J., Canudas, A. M., Camins, A., Jiménez, A., Sanchez‐Roige, S., Lalanza, J. F., Escorihuela, R. M., et al. (2014) · PubMed · Cited by 35 · see citing works
Calbet, J. A. L., Ponce-González, J. G., Calle-Herrero, J. D. L., Perez-Suarez, I., Martin-Rincon, M., Santana, A., Morales-Alamo, D., & Holmberg, H.-C. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00483 · Cited by 34 · see citing works
Autophagic adaptation is associated with exercise‐induced fibre‐type shifting in skeletal muscle
Tam, B. T., Pei, X. M., Yu, A. P., Sin, T. K., Leung, K. K., Au, K., Chong, J. T., Yung, B. Y., Yip, S. P., Chan, L., et al. (2015) · Acta Physiologica · doi:10.1111/apha.12503 · Cited by 33 · see citing works
Exercise and Regulation of Protein Metabolism
Atherton, P. J., Phillips, B. E., & Wilkinson, D. J. (2015) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2015.06.015 · Cited by 34 · see citing works
Jiang, D., Chen, K., Lu, X., Gao, H., Qin, Z., & Lin, F. (2013) · Acta Pharmacologica Sinica · doi:10.1038/aps.2013.144 · Cited by 32 · see citing works
The Nuclear Receptor, Nor-1, Induces the Physiological Responses Associated With Exercise
Goode, J. M., Pearen, M. A., Tuong, Z. K., Wang, S.-C., Oh, T. G., Shao, E. X., & Muscat, G. E. O. (2016) · Molecular Endocrinology · doi:10.1210/me.2015-1300 · Cited by 31 · see citing works
Key considerations for investigating and interpreting autophagy in skeletal muscle
Rahman, F. A., Baechler, B. L., & Quadrilatero, J. (2024) · Autophagy · doi:10.1080/15548627.2024.2373676 · Cited by 29 · see citing works
Batatinha, H., Diniz, T. A., Teixeira, A. A. D. S., Krüger, K., & Neto, J. C. R. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.28318 · Cited by 29 · see citing works
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 · see citing works
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 · see citing works
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 27 · see citing works
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 · see citing works
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 · see citing works
Park, W., Kim, J., Kim, H. J., Choi, J., Park, J.-W., Cho, H.-W., Kim, B.-W., Park, M. H., Shin, T.-S., Cho, S., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091418 · Cited by 21 · see citing works
Self-citationAutophagy 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 · see citing works
Opichka, M. A., Shute, R. J., Marshall, K., & Slivka, D. R. (2019) · Cryobiology · doi:10.1016/j.cryobiol.2019.08.007 · Cited by 19 · see citing works
Balmori‐Cedeño, J., Liu, J., Misk, E., Lillie, B. N., & Lumsden, J. S. (2019) · Journal of Fish Diseases · doi:10.1111/jfd.12959 · Cited by 18 · see citing works
Martinez‐Canton, M., Galván-Álvarez, V., Gallego-Selles, Á., Gelabert‐Rebato, M., García-Gonzalez, E., González, J. J., Martín-Rincón, M., & Calbet, J. A. L. (2024) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2024.07.012 · Cited by 16 · see citing works
Rosa‐Caldwell, M. E., Brown, J. L., Lee, D. E., Blackwell, T. A., Turner, K. W., Brown, L. A., Perry, R. A., Haynie, W. S., Washington, T. A., & Greene, N. P. (2017) · Experimental Physiology · doi:10.1113/ep086406 · Cited by 16 · see citing works
Escobar, K. A., Welch, A. M., Wells, A. D., Fennel, Z. J., Nava, R. C., Li, Z., Moriarty, T. A., Nitta, C. H., Zuhl, M., VanDusseldorp, T. A., et al. (2020) · Human Nutrition & Metabolism · doi:10.1016/j.hnm.2020.200118 · Cited by 16 · see citing works
Du, N. H., Ngoc, T. T. B., Cang, H. Q., Luyến, N. T., Tran, T. L., Tran, Q. L., & Thảo, Đ. T. P. (2023) · Scientific Reports · doi:10.1038/s41598-023-47199-1 · Cited by 13 · see citing works
Keeping the beat against time: Mitochondrial fitness in the aging heart
Mendoza, A., & Karch, J. M. (2022) · Frontiers in Aging · doi:10.3389/fragi.2022.951417 · Cited by 13 · see citing works
Zhang, D., Lee, J. H., Kwak, S. E., Shin, H. E., Zhang, Y., Moon, H. Y., Shin, D. M., Seong, J. K., Tang, L. V., & Song, W. J. (2019) · Journal of Obesity & Metabolic Syndrome · doi:10.7570/jomes.2019.28.3.175 · Cited by 13 · see citing works
Wang, P., Li, C. G., Zhou, X., Cui, D., Ouyang, T., Chen, W., & Ding, S. (2022) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/1440-1681.13632 · Cited by 12 · see citing works
Sanchez, A. M. J., Candau, R. B., Raibon, A., & Bernardi, H. (2015) · InTech eBooks · doi:10.5772/60698 · Cited by 12 · see citing works
Pinto, A. P., Vieira, T. S., Marafon, B. B., Batitucci, G., Barrón‐Cabrera, E., da Rocha, A. L., Kohama, E. B., Rodrigues, K. C. D. C., de Moura, L. P., Pauli, J. R., et al. (2020) · Nutrients · doi:10.3390/nu12030641 · Cited by 10 · see citing works
Hayat, M. A. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-812146-7.00001-9 · Cited by 9 · see citing works
Exercise suppresses DEAF1 to normalize mTORC1 activity and reverse muscle aging
Choy, S. M., Goh, K. Y., Lee, W. X., Jiang, W., Gou, Q., Krishnan, P. D. G., Ong, S. C., Chua, K., Harmston, N., & Tang, H.-W. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2508893122 · Cited by 7 · see citing works
Perrey, S., Joyner, M. J., Ruiz, J. R., Lucía, A., Nosaka, K., Louis, J. B., Pitsiladis, Y. P., Smoliga, J. M., Zavorsky, G. S., Hunter, G. R., et al. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00666.2012 · Cited by 7 · see citing works
Self-citationImpact of combined exercise on blood DNA methylation and physical health in older women with obesity
Dawangpa, A., Chitta, P., Rodrigues, G. D. S., Iadsee, N., Noronha, N. Y., Nonino, C. B., Júnior, C. R. B., & Sae‐Lee, C. (2024) · PLoS ONE · doi:10.1371/journal.pone.0315250 · Cited by 7 · see citing works
pathways during ultra-endurance running Modulation of autophagy and ubiquitin-proteasome
Féasson, L., Jamart, C., Francaux, M., Millet, G. Y., Deldicque, L., & Frère, D. (2012) · Cited by 6 · see citing works
Self-citationBerkemeier, Q., Deyhle, M. R., McCormick, J. J., Escobar, K. A., & Mermier, C. M. (2024) · High Altitude Medicine & Biology · doi:10.1089/ham.2023.0090 · Cited by 5 · see citing works
Antioxidants and Polyphenols Mediate Mitochondrial Mediated Muscle Death Signaling in Sarcopenia
Alway, S. E. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-810422-4.00026-9 · Cited by 6 · see citing works
Identification of mitophagy-related genes in patients with acute myocardial infarction
Li, J.-Y., Chen, H.-K., Huang, Y.-H., Zhi, Y.-P., Li, Y., Lin, K., Chen, C., & Guo, Y. (2025) · Hereditas · doi:10.1186/s41065-025-00424-5 · Cited by 4 · see citing works
Influence of skeletal muscle heterogeneity on autophagic signaling and response
Rahman, F. A., & Quadrilatero, J. (2025) · Autophagy Reports · doi:10.1080/27694127.2025.2562429 · Cited by 4 · see citing works
Resende-Coelho, A., Ali, M. M., James, A., Warren, A. D., Gatrell, L. B., Kadhim, I., Fu, Q., Xiong, J., Onal, M., & Almeida, M. (2025) · Aging · doi:10.18632/aging.206213 · Cited by 5 · see citing works
Guts for Self-Eating: Role of Autophagy in Gastrointestinal Health and Disease
Nighot, P. K., Stine, J. G., & Clarke, K. (2025) · Gastro Hep Advances · doi:10.1016/j.gastha.2025.100654 · Cited by 3 · see citing works
Implementation of the ergogenic action of antioxidative agents
Гунина, Л. (2015) · Sporto mokslas / Sport Science · doi:10.15823/sm.2015.12 · Cited by 3 · see citing works
Fan, K., Li, X., & Wang, Z. (2025) · The FASEB Journal · doi:10.1096/fj.202501901r · Cited by 2 · see citing works
Autophagy decline during ageing: Molecular regulation, tissue specificity, and therapeutic potential
Goyal, A., Kumari, A., Agrawal, N., & Yadav, H. N. (2026) · Pathology - Research and Practice · doi:10.1016/j.prp.2026.156568 · Cited by 2 · see citing works
Hayat, M. A. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-805420-8.00001-9 · Cited by 2 · see citing works
Li, J., Zhao, Q., He, H., & Song, X. (2026) · Brain and Development · doi:10.1016/j.braindev.2026.104547 · Cited by 1 · see citing works
The Autophagy-Dependent Signaling in Skeletal Muscle
Sakuma, K., Aizawa, M., Wakabayashi, H., & Yamaguchi, A. (2017) · Springer eBooks · doi:10.1007/978-981-10-3292-9_4 · Cited by 1 · see citing works
Boyer‐Guittaut, M., Varambally, S., Darley-Usmar, V. M., & Zhang, J. (2017) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2017.10.163 · Cited by 1 · see citing works
- Authors
- Jamart, C., Benoit, N., Raymackers, J.-M., Kim, H. J., Kim, C. K., & Francaux, M.
- Affiliations
- UCLouvain (BE)
- Korea National Sport University (KR)
- Corresponding author
- Francaux, Marc
- Venue
- European Journal of Applied Physiology
- Published
- 2011-12-23
- Volume
- 112
- Issue
- 8
- Pages
- 3173-3177
- ISSN
- 0020-9376 (ISSN-L)
- 1439-6319
- 1439-6327
- OpenAlex
- W2009618449
- Cited by
- 121
- References
- 26
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 8 · 2023: 3 · 2022: 5 · 2021: 9 · 2020: 5 · 2019: 9 · 2018: 8 · 2017: 16 · 2016: 11 · 2015: 16 · 2014: 12 · 2013: 6 · 2012: 4
- FWCI
- 5.28
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- other-oa
- www.springer.com/tdm (tdm)
- Locations
- European Journal of Applied Physiology (publishedVersion)
- PubMed (publishedVersion)
- Digital Access to Libraries (Université catholique de Louvain (UCL), l'Université de Namur (UNamur) and the Université Saint-Louis (USL-B)) (submittedVersion, other-oa)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Keywords
- autophagy, skeletal muscle, gene expression, ATG4B, ATG12, GABARAPL1, LC3B, cathepsin L, BNIP3, BNIP3L, autophagic flux, vastus lateralis, endurance running
- MeSH terms
- Autophagy-Related Proteins, Autophagy-Related Protein 12, Adult, Autophagy, Biopsy, Cysteine Endopeptidases, Genetic Markers, Humans, Male, Membrane Proteins, Microtubule-Associated Proteins, Middle Aged, Muscle Contraction, Physical Endurance, Proto-Oncogene Proteins, RNA, Messenger, Running, Time Factors, Transcription, Genetic, Up-Regulation, Reverse Transcriptase Polymerase Chain Reaction, Tumor Suppressor Proteins, Small Ubiquitin-Related Modifier Proteins, Adaptor Proteins, Signal Transducing, Quadriceps Muscle, Cathepsin L, Real-Time Polymerase Chain Reaction
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