Cited by 399Apelin-related biomedical researchMuscle Physiology and DisordersNutrition and Health in Aging

The DOI matches its Crossref record; 64 of the 64 references it cites were found in a registry or an index.

The exerkine apelin reverses age-associated sarcopenia

Open access

Vinel, Claire, Lukjanenko, Laura, Batut, Aurelie, Deleruyelle, Simon, Pradère, Jean-Philippe, Le Gonidec, Sophie, Dortignac, Alizée, Geoffre, Nancy, Pereira, Ophelie, Karaz, Sonia, Lee, Umji, Camus, Mylène, Chaoui, Karima, Mouisel, Etienne, Bigot, Anne, Mouly, Vincent, Vigneau, Mathieu, Pagano, Allan F., Chopard, Angèle, Pillard, Fabien, Guyonnet, Sophie, Cesari, Matteo, Burlet-Schiltz, Odile, Pahor, Marco, Feige, Jerome N., Vellas, Bruno, Valet, Philippe, Dray, Cedric·2018·Nature Medicine

DOI 10.1038/s41591-018-0131-6

Open this paper in CoChat — free account

Abstract

Sarcopenia, the degenerative loss of skeletal muscle mass, quality and strength, lacks early diagnostic tools and new therapeutic strategies to prevent the frailty-to-disability transition often responsible for the medical institutionalization of elderly individuals. Herein we report that production of the endogenous peptide apelin, induced by muscle contraction, is reduced in an age-dependent manner in humans and rodents and is positively associated with the beneficial effects of exercise in older persons. Mice deficient in either apelin or its receptor (APLNR) presented dramatic alterations in muscle function with increasing age. Various strategies that restored apelin signaling during aging further demonstrated that this peptide considerably enhanced muscle function by triggering mitochondriogenesis, autophagy and anti-inflammatory pathways in myofibers as well as enhancing the regenerative capacity by targeting muscle stem cells. Taken together, these findings revealed positive regulatory feedback between physical activity, apelin and muscle function and identified apelin both as a tool for diagnosis of early sarcopenia and as the target of an innovative pharmacological strategy to prevent age-associated muscle weakness and restore physical autonomy.

Integrity signals

Registry

Crossref · 10.1038/s41591-018-0131-6

Cites

64 of 64 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Frailty in relation to the accumulation of deficits
Rockwood, K., & Mitnitski, A. (2007) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/62.7.722 · Cited by 3,076
Skeletal muscle fatigue: cellular mechanisms
Allen, D. G., Lamb, G. D., & Westerblad, H. (2008) · Physiological Reviews · doi:10.1152/physrev.00015.2007 · Cited by 2,495
The healthcare costs of sarcopenia in the United States
Janssen, I., Shepard, D. S., Katzmarzyk, P. T., & Roubenoff, R. (2004) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2004.52014.x · Cited by 1,546
Effect of Structured Physical Activity on Prevention of Major Mobility Disability in Older Adults: The LIFE Study Randomized Clinical Trial
Pahor, M., Guralnik, J. M., Ambrosius, W. T., Blair, S., Bonds, D. E., Church, T. S., Espeland, M. A., Fielding, R. A., Gill, T. M., Groessl, E. J., et al. (2014) · JAMA · doi:10.1001/jama.2014.5616 · Cited by 1,427
Self-citation
Urolithin A induces mitophagy and prolongs lifespan in C. elegans and increases muscle function in rodents
Ryu, D., Mouchiroud, L., Andreux, P. A., Katsyuba, E., Moullan, N., Nicolet-dit-Félix, A. A., Williams, E. G., Jha, P., Lo Sasso, G., Huzard, D., et al. (2016) · Nature Medicine · doi:10.1038/nm.4132 · Cited by 1,105
Welcome to the ICD‐10 code for sarcopenia
Anker, S. D., Morley, J. E., & von Haehling, S. (2016) · Journal of Cachexia, Sarcopenia and Muscle · doi:10.1002/jcsm.12147 · Cited by 983
Sarcopenia: alternative definitions and associations with lower extremity function
Newman, A. B., Kupelian, V., Visser, M., Simonsick, E., Goodpaster, B., Nevitt, M., Kritchevsky, S. B., Tylavsky, F. A., Rubin, S. M., Harris, T. B., et al. (2003) · Journal of the American Geriatrics Society · doi:10.1046/j.1532-5415.2003.51534.x · Cited by 981
Frailty and cognitive impairment—A review of the evidence and causal mechanisms
Robertson, D. A., Savva, G. M., & Kenny, R. A. (2013) · Ageing Research Reviews · doi:10.1016/j.arr.2013.06.004 · Cited by 784
Effects of a Physical Activity Intervention on Measures of Physical Performance: Results of the Lifestyle Interventions and Independence for Elders Pilot (LIFE-P) Study
The LIFE Study Investigators* [*See Appendix for List of LIFE Study Investigators] (2006) · The Journals of Gerontology Series A · doi:10.1093/gerona/61.11.1157 · Cited by 668
p38 MAPK signaling underlies a cell-autonomous loss of stem cell self-renewal in skeletal muscle of aged mice
Bernet, J. D., Doles, J. D., Hall, J. K., Kelly Tanaka, K., Carter, T. A., & Olwin, B. B. (2014) · Nature Medicine · doi:10.1038/nm.3465 · Cited by 573

Show all 64 references

Sorted by citations

Sarcopenia
Cruz-Jentoft, A. J., & Sayer, A. A. (2019) · The Lancet · doi:10.1016/s0140-6736(19)31138-9 · Cited by 3,905
Senolytics in idiopathic pulmonary fibrosis: Results from a first-in-human, open-label, pilot study
Justice, J. N., Nambiar, A. M., Tchkonia, T., LeBrasseur, N. K., Pascual, R., Hashmi, S. K., Prata, L., Masternak, M. M., Kritchevsky, S. B., Musi, N., et al. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2018.12.052 · Cited by 1,261
Exerkines in health, resilience and disease
Chow, L. S., Gerszten, R. E., Taylor, J. M., Pedersen, B. K., van Praag, H., Trappe, S., Febbraio, M. A., Galis, Z. S., Gao, Y., Haus, J. M., et al. (2022) · Nature Reviews Endocrinology · doi:10.1038/s41574-022-00641-2 · Cited by 927
Physical activity and exercise: Strategies to manage frailty
Angulo, J., El Assar, M., Álvarez-Bustos, A., & Rodríguez-Mañas, L. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101513 · Cited by 771
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
Approaches to Assessment of Muscle Mass and Myosteatosis on Computed Tomography: A Systematic Review
Amini, B., Boyle, S. P., Boutin, R. D., & Lenchik, L. (2019) · The Journals of Gerontology: Series A · doi:10.1093/gerona/glz034 · Cited by 391
Biomarkers of aging
Bao, H., Cao, J., Chen, M., Min, C., Chen, W., Chen, X., Chen, Y., Chen, Y., Chen, Y., Chen, Z., et al. (2023) · Science China Life Sciences · doi:10.1007/s11427-023-2305-0 · Cited by 402
Effect of Physical Activity/Exercise on Oxidative Stress and Inflammation in Muscle and Vascular Aging
El Assar, M., Álvarez-Bustos, A., Sosa, P., Angulo, J., & Rodríguez-Mañas, L. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158713 · Cited by 371
Aging disrupts muscle stem cell function by impairing matricellular WISP1 secretion from fibro-adipogenic progenitors
Lukjanenko, L., Karaz, S., Stuelsatz, P., Gurriaran-Rodriguez, U., Michaud, J., Dammone, G., Sizzano, F., Mashinchian, O., Ancel, S., Migliavacca, E., et al. (2019) · Cell stem cell · doi:10.1016/j.stem.2018.12.014 · Cited by 374
Self-citation
A framework for selection of blood-based biomarkers for geroscience-guided clinical trials: report from the TAME Biomarkers Workgroup
Justice, J. N., Ferrucci, L., Newman, A. B., Aroda, V. R., Bahnson, J. L., Divers, J., Espeland, M. A., Marcovina, S., Pollak, M. N., Kritchevsky, S. B., et al. (2018) · GeroScience · doi:10.1007/s11357-018-0042-y · Cited by 359
Exercise Metabolism and Adaptation in Skeletal Muscle
Smith, J. A. B., Murach, K. A., Dyar, K. A., & Zierath, J. R. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-023-00606-x · Cited by 342
Tissue Stem Cells: Architects of Their Niches
Fuchs, E., & Blau, H. M. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.09.011 · Cited by 332
A focus shift from sarcopenia to muscle health in the Asian Working Group for Sarcopenia 2025 Consensus Update
Chen, L., Hsiao, F., Akishita, M., Assantachai, P., Lee, W., Lim, W. S., Muangpaisan, W., Kim, M., Merchant, R. A., Peng, L., et al. (2025) · Nature Aging · doi:10.1038/s43587-025-01004-y · Cited by 388
Molecular Responses to Acute Exercise and Their Relevance for Adaptations in Skeletal Muscle to Exercise Training
Egan, B., & Sharples, A. P. (2023) · Physiological Reviews · doi:10.1152/physrev.00054.2021 · Cited by 278
Multifactorial Mechanism of Sarcopenia and Sarcopenic Obesity. Role of Physical Exercise, Microbiota and Myokines
Bilski, J., Pierzchalski, P., Szczepanik, M., Bonior, J., & Zoladz, J. A. (2022) · Cells · doi:10.3390/cells11010160 · Cited by 271
Inhibition of prostaglandin-degrading enzyme 15-PGDH rejuvenates aged muscle mass and strength
Palla, A. R., Ravichandran, M., Wang, Y. X., Alexandrova, L., Yang, A. V., Kraft, P., Holbrook, C. A., Schürch, C. M., Ho, A. T. V., & Blau, H. M. (2021) · Science · doi:10.1126/science.abc8059 · Cited by 232
Current and investigational medications for the treatment of sarcopenia
Rolland, Y., Dray, C., Vellas, B., & Barreto, P. D. S. (2023) · Metabolism · doi:10.1016/j.metabol.2023.155597 · Cited by 195
Self-citation
Fibro-adipogenic progenitors in skeletal muscle homeostasis, regeneration and diseases
Molina, T., Fabre, P., & Dumont, N. A. (2021) · Open Biology · doi:10.1098/rsob.210110 · Cited by 205
Exercise-Induced Myokines With Therapeutic Potential for Muscle Wasting
Piccirillo, R. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00287 · Cited by 197
Myokines mediate the cross talk between skeletal muscle and other organs
Chen, W., Wang, L., You, W., & Shan, T. (2021) · Journal of Cellular Physiology · doi:10.1002/jcp.30033 · Cited by 162
Exercise-Released Myokines in the Control of Energy Metabolism
Laurens, C., Bergouignan, A., & Moro, C. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00091 · Cited by 159
Physical Exercise and Myokines: Relationships with Sarcopenia and Cardiovascular Complications
Barbalho, S. M., Flato, U. A. P., Tofano, R. J., Goulart, R. D. A., Guiguer, E. L., Detregiachi, C. R. P., Buchaim, D. V., Araújo, A. C., Buchaim, R. L., Reina, F. T. R., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21103607 · Cited by 156
“On the other hand, aged animals treated with a daily injection of apelin showed improvement of muscle capacity and myofiber hypertrophy [48].”
Background
Exercise therapy for people with sarcopenic obesity: myokines and adipokines as effective actors
Alizadeh Pahlavani, H. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.811751 · Cited by 145
“It was also emphasized that 4 weeks of exercise stimulates muscle apelin and then plasma apelin so that decreased muscle apelin production due to aging can be reversed by chronic exercise (101).”
BackgroundInfluential
Mechanisms by Which Skeletal Muscle Myokines Ameliorate Insulin Resistance
Balakrishnan, R., & Thurmond, D. C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23094636 · Cited by 143
International Union of Basic and Clinical Pharmacology. CVII. Structure and Pharmacology of the Apelin Receptor with a Recommendation that Elabela/Toddler Is a Second Endogenous Peptide Ligand
Read, C., Nyimanu, D., Williams, T., Huggins, D. J., Šulentić, P., Macrae, R. G. C., Yang, P. B., Glen, R. C., Maguire, J. J., & Davenport, A. P. (2019) · Pharmacological Reviews · doi:10.1124/pr.119.017533 · Cited by 130
Fusion and beyond: Satellite cell contributions to loading-induced skeletal muscle adaptation
Murach, K. A., Fry, C. S., Dupont‐Versteegden, E. E., McCarthy, J. J., & Peterson, C. A. (2021) · The FASEB Journal · doi:10.1096/fj.202101096r · Cited by 120
Revisiting the Hallmarks of Aging to Identify Markers of Biological Age
Guerville, F., Barreto, P. D. S., Ader, I., Andrieu, S., Casteilla, L., Dray, C., Fazilleau, N., Guyonnet, S., Langin, D., Liblau, R., et al. (2020) · The Journal of Prevention of Alzheimer s Disease · doi:10.14283/jpad.2019.50 · Cited by 122
Self-citation
Exercise-Induced Myokines can Explain the Importance of Physical Activity in the Elderly: An Overview
Kwon, J. H., Moon, K. M., & Min, K.-W. (2020) · Healthcare · doi:10.3390/healthcare8040378 · Cited by 116
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 117
Apelin/APJ system: an emerging therapeutic target for respiratory diseases
Yan, J., Wang, A., Cao, J., & Chen, L. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03461-7 · Cited by 109
Exerkines and long-term synaptic potentiation: Mechanisms of exercise-induced neuroplasticity
Vints, W. A. J., Levin, O., Fujiyama, H., Verbunt, J., & Masiulis, N. (2022) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2022.100993 · Cited by 119
Maternal exercise via exerkine apelin enhances brown adipogenesis and prevents metabolic dysfunction in offspring mice
Son, J. S., Zhao, L., Chen, Y., Chen, K., Chae, S. A., de Avila, J. M., Wang, H., Zhu, M.-J., Jiang, Z., & Du, M. (2020) · Science Advances · doi:10.1126/sciadv.aaz0359 · Cited by 101
The Novel Perspectives of Adipokines on Brain Health
Lee, T. H.-Y., Cheng, K. K. Y., Hoo, R. L. C., Siu, P. M., & Yau, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20225638 · Cited by 100
Exerkine fibronectin type-III domain-containing protein 5/irisin-enriched extracellular vesicles delay vascular ageing by increasing SIRT6 stability
Chi, C., Fu, H., Li, Y., Zhang, G., Zeng, F., Ji, Q., Shen, Q., Wang, X.-J., Li, Z., Zhou, C., et al. (2022) · European Heart Journal · doi:10.1093/eurheartj/ehac431 · Cited by 103
Mitochondrial Impairment in Sarcopenia
Bellanti, F., Buglio, A. L., & Vendemiale, G. (2021) · Biology · doi:10.3390/biology10010031 · Cited by 104
Understanding of sarcopenia: from definition to therapeutic strategies
Kim, J. W., Kim, R., Choi, H., Lee, S., & Bae, G. (2021) · Archives of Pharmacal Research · doi:10.1007/s12272-021-01349-z · Cited by 103
Autophagy, apoptosis, and mitochondria: molecular integration and physiological relevance in skeletal muscle
Bloemberg, D., & Quadrilatero, J. (2019) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00261.2018 · Cited by 100
Role of myokines in the development of skeletal muscle insulin resistance and related metabolic defects in type 2 diabetes
Garneau, L., & Aguer, C. (2019) · Diabetes & Metabolism · doi:10.1016/j.diabet.2019.02.006 · Cited by 95
Sarcopenic obesity: Myokines as potential diagnostic biomarkers and therapeutic targets?
Guo, A., Li, K., & Xiao, Q. (2020) · Experimental Gerontology · doi:10.1016/j.exger.2020.111022 · Cited by 83
Molecular insights of exercise therapy in disease prevention and treatment
Walzik, D., Chirino, T. Y. W., Zimmer, P., & Joisten, N. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01841-0 · Cited by 95
The Role of the Skeletal Muscle Secretome in Mediating Endurance and Resistance Training Adaptations
Leuchtmann, A. B., Adak, V., Dilbaz, S., & Handschin, C. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.709807 · Cited by 84
Elevated CD47 is a hallmark of dysfunctional aged muscle stem cells that can be targeted to augment regeneration
Porpiglia, E., Mai, T., Kraft, P. E., Holbrook, C. A., de Morrée, A., Gonzalez, V. D., Hilgendorf, K. I., Frésard, L., Trejo, A., Bhimaraju, S., et al. (2022) · Cell stem cell · doi:10.1016/j.stem.2022.10.009 · Cited by 84
Physical Exercise-Induced Myokines in Neurodegenerative Diseases
Lee, B., Shin, M., Park, Y., Won, S.-Y., & Cho, K. S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22115795 · Cited by 79
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 80
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
From Obesity to Hippocampal Neurodegeneration: Pathogenesis and Non-Pharmacological Interventions
Lee, T. H.-Y., & Yau, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010201 · Cited by 78
The wonder exerkines—novel insights: a critical state-of-the-art review
Magliulo, L., Bondi, D., Pini, N., Marramiero, L., & Filippo, E. S. D. (2021) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-021-04264-5 · Cited by 77
Iron Metabolism of the Skeletal Muscle and Neurodegeneration
Hałoń, M., Borkowska, A., Herman-Antosiewicz, A., & Antosiewicz, J. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00165 · Cited by 73
Mechanism and physical activities in bone-skeletal muscle crosstalk
Zhao, Z., Yan, K., Guan, Q., Guo, Q., & Zhao, C. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1287972 · Cited by 75
Interactions between gut microbiota and skeletal muscle
Gizard, F., Fernandez, A., & Vadder, F. D. (2020) · Nutrition and Metabolic Insights · doi:10.1177/1178638820980490 · Cited by 70
Stem cell aging in the skeletal muscle: The importance of communication
Hong, X., Campanario, S., Ramírez‐Pardo, I., Grima-Terrén, M., Isern, J., & Muñoz‐Cánoves, P. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101528 · Cited by 73
Exerkines and cardiometabolic benefits of exercise: from bench to clinic
Jin, L., Díaz-Cañestro, C., Wang, Y., Tse, M. A., & Xu, A. (2024) · EMBO Molecular Medicine · doi:10.1038/s44321-024-00027-z · Cited by 76
Aging Skeletal Muscles: What Are the Mechanisms of Age-Related Loss of Strength and Muscle Mass, and Can We Impede Its Development and Progression?
Gustafsson, T. P., & Ulfhake, B. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252010932 · Cited by 78
Apelin protects against abdominal aortic aneurysm and the therapeutic role of neutral endopeptidase resistant apelin analogs
Wang, W., Shen, M., Fischer, C., Basu, R., Hazra, S., Couvineau, P., Paul, M., Wang, F., Toth, S., Mix, D., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1900152116 · Cited by 63
Apelin/APJ system: A novel promising target for neurodegenerative diseases
Luo, H., Han, L., & Xu, J. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.29001 · Cited by 61
The apelinergic system: a perspective on challenges and opportunities in cardiovascular and metabolic disorders
Marsault, É., Llorens‐Cortés, C., Iturrioz, X., Chun, H. J., Lesur, O., Oudit, G. Y., & Auger‐Messier, M. (2019) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14123 · Cited by 60
Nrf2 contributes to the benefits of exercise interventions on age-related skeletal muscle disorder via regulating Drp1 stability and mitochondrial fission
Yan, X., Shen, Z.-L., Yu, D., Zhao, C., Zou, H., Ma, B., Dong, W.-X., Chen, W., Huang, D., & Yu, Z. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.11.030 · Cited by 60
Where Two Common Conditions of Aging Meet: Osteoarthritis and Sarcopenia
Pickering, M., & Chapurlat, R. D. (2020) · Calcified Tissue International · doi:10.1007/s00223-020-00703-5 · Cited by 61
Maternal Inactivity Programs Skeletal Muscle Dysfunction in Offspring Mice by Attenuating Apelin Signaling and Mitochondrial Biogenesis
Son, J. S., Chae, S. A., Wang, H., Chen, Y., Iniguez, A. B., de Avila, J. M., Jiang, Z., Zhu, M.-J., & Du, ‬. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108461 · Cited by 56
Autophagy in sarcopenia: Possible mechanisms and novel therapies
Xie, G., Jin, H., Mikhail, H., Pavel, V., Yang, G., Ji, B., Lu, B., & Li, Y. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.115147 · Cited by 62
ACE2, angiotensin 1-7 and skeletal muscle: review in the era of COVID-19
Yamamoto, K. I., Takeshita, H., & Rakugi, H. (2020) · Clinical Science · doi:10.1042/cs20200486 · Cited by 58
Myokines: Metabolic regulation in obesity and type 2 diabetes
Chen, Z.-T., Weng, Z.-X., Lin, J. D., & Meng, Z.-X. (2024) · Life Metabolism · doi:10.1093/lifemeta/loae006 · Cited by 58
The apelin/APJ system as a therapeutic target in metabolic diseases
Castan‐Laurell, I., Masri, B., & Valet, P. (2018) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2019.1561871 · Cited by 56
Self-citation
Current advances in our understanding of exercise as medicine in metabolic disease
Sylow, L., & Richter, E. A. (2019) · Current Opinion in Physiology · doi:10.1016/j.cophys.2019.04.008 · Cited by 54
Bifidobacterium animalis subsp. lactis A6 ameliorates bone and muscle loss via modulating gut microbiota composition and enhancing butyrate production
Chen, M., Li, Y., Zhai, Z., Wang, H., Lin, Y., Chang, F., Ge, S., Sun, X., Wei, W., Wang, D., et al. (2025) · Bone Research · doi:10.1038/s41413-024-00381-1 · Cited by 59
Molecular Transducers of Human Skeletal Muscle Remodeling under Different Loading States
Stokes, T., Timmons, J. A., Crossland, H., Tripp, T. R., Murphy, K., McGlory, C., Mitchell, C. J., Oikawa, S. Y., Morton, R. W., Phillips, B. E., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107980 · Cited by 52
Impact of Exercise and Aging on Mitochondrial Homeostasis in Skeletal Muscle: Roles of ROS and Epigenetics
Li, J., Wang, Z., Li, C., Song, Y., Wang, Y., Hai, B., & Zhang, Y. (2022) · Cells · doi:10.3390/cells11132086 · Cited by 56
CRISPR/Cas9-Mediated miR-29b Editing as a Treatment of Different Types of Muscle Atrophy in Mice
Li, J., Wang, L., Hua, X., Tang, H., Chen, R., Yang, T., Das, S., & Xiao, J. (2020) · Molecular Therapy · doi:10.1016/j.ymthe.2020.03.005 · Cited by 54
Elevated H3K27ac in aged skeletal muscle leads to increase in extracellular matrix and fibrogenic conversion of muscle satellite cells
Zhou, J., So, K. K. H., Li, Y., Li, Y., Yuan, J., Ding, Y., Chen, F., Huang, Y., Liu, J., Lee, W., et al. (2019) · Aging Cell · doi:10.1111/acel.12996 · Cited by 52
β- cell dynamics in type 2 diabetes and in dietary and exercise interventions
Lv, C.-A., Sun, Y., Zhang, Z. Y., Aboelela, Z., Qiu, X., & Meng, Z. (2022) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjac046 · Cited by 57
Sarcopenia and the biological determinants of aging: A narrative review from a geroscience perspective
Nunes-Pinto, M., de Mello, R. G. B., Pinto, M. N., Moro, C., Vellas, B. J., Martinez, L. O., Rolland, Y., & Barreto, P. D. S. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102587 · Cited by 52
Self-citation
Exercise and exerkines: Mechanisms and roles in anti-aging and disease prevention
Lu, X., Chen, Y., Shi, Y., Shi, Y., Su, X., Chen, P., Wu, D., & Shi, H. (2025) · Experimental Gerontology · doi:10.1016/j.exger.2025.112685 · Cited by 50
Magnesium supplementation enhances mTOR signalling to facilitate myogenic differentiation and improve aged muscle performance
Liu, Y., Wang, Q., Zhang, Z., Fu, R., Zhou, T., Long, C., He, T., Yang, D., Li, Z., & Peng, S. (2021) · Bone · doi:10.1016/j.bone.2021.115886 · Cited by 44
Time Course and Role of Exercise-Induced Cytokines in Muscle Damage and Repair After a Marathon Race
Zocoler, C. A. S., Sierra, A., Galán, B. S. M., Maciel, J. F. D. S., Manoel, R., Barbeiro, H. V., de Souza, H. P., & Cury‐Boaventura, M. F. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.752144 · Cited by 51
Myokines and Microbiota: New Perspectives in the Endocrine Muscle–Gut Axis
Saponaro, F., Bertolini, A., Baragatti, R., Galfo, L., Chiellini, G., Saba, A., & D’Urso, G. (2024) · Nutrients · doi:10.3390/nu16234032 · Cited by 55
Impact and Lessons From the Lifestyle Interventions and Independence for Elders (LIFE) Clinical Trials of Physical Activity to Prevent Mobility Disability
Pahor, M., Guralnik, J. M., Anton, S. D., Ambrosius, W. T., Blair, S. N., Church, T. S., Espeland, M. A., Fielding, R. A., Gill, T. M., Glynn, N. W., et al. (2020) · Journal of the American Geriatrics Society · doi:10.1111/jgs.16365 · Cited by 42
Self-citation
A focused review of myokines as a potential contributor to muscle hypertrophy from resistance-based exercise
Cornish, S. M., Bugera, E. M., Duhamel, T. A., Peeler, J. D., & Anderson, J. E. (2020) · European Journal of Applied Physiology · doi:10.1007/s00421-020-04337-1 · Cited by 43
Maternal exercise intergenerationally drives muscle-based thermogenesis via activation of apelin-AMPK signaling
Son, J. S., Chae, S. A., Zhao, L., Wang, H., de Avila, J. M., Zhu, M. J., Jiang, Z., & Du, ‬. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2022.103842 · Cited by 40
A First-in-Human Study of AMG 986, a Novel Apelin Receptor Agonist, in Healthy Subjects and Heart Failure Patients
Winkle, P. J., Goldsmith, S. R., Koren, M. J., Lepage, S., Hellawell, J. L., Trivedi, A., Tsirtsonis, K., Abbasi, S. A., Kaufman, A., Troughton, R. W., et al. (2022) · Cardiovascular Drugs and Therapy · doi:10.1007/s10557-022-07328-w · Cited by 40
The myokine Fibcd1 is an endogenous determinant of myofiber size and mitigates cancer-induced myofiber atrophy
Graça, F. A., Rai, M., Hunt, L. C., Stephan, A., Wang, Y., Gordon, B., Wang, R., Quarato, G., Xu, B., Fan, Y., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-30120-1 · Cited by 41
DOK7 Gene Therapy Enhances Neuromuscular Junction Innervation and Motor Function in Aged Mice
Ueta, R., Sugita, S., Minegishi, Y., Shimotoyodome, A., Ota, N., Ogiso, N., Eguchi, T., & Yamanashi, Y. (2020) · iScience · doi:10.1016/j.isci.2020.101385 · Cited by 40
Neuroprotective gain of Apelin/APJ system
Zhou, J.-X., Shuai, N., Wang, B., Jin, X., Kuang, X., & Tian, S. (2021) · Neuropeptides · doi:10.1016/j.npep.2021.102131 · Cited by 40
Skeletal Muscle as a Mediator of Interorgan Crosstalk During Exercise: Implications for Aging and Obesity
Shero, J. A., Lindholm, M. E., Sandri, M. F., & Stanford, K. I. (2025) · Circulation Research · doi:10.1161/circresaha.124.325614 · Cited by 45
Circulating plasma factors involved in rejuvenation
Kang, J. S., & Yang, Y. R. (2020) · Aging · doi:10.18632/aging.103933 · Cited by 39
Body composition and aging: cross-sectional results from the INSPIRE study in people 20 to 93 years old
Briand, M., Raffin, J., González-Bautista, E., Ritz, P., van Kan, G. A., Pillard, F., Faruch, M., Guyonnet, S., Dray, C., Vellas, B. J., et al. (2024) · GeroScience · doi:10.1007/s11357-024-01245-6 · Cited by 48
Self-citation
Angiotensin 1-7 alleviates aging-associated muscle weakness and bone loss, but is not associated with accelerated aging in ACE2-knockout mice
Nozato, S., Yamamoto, K. I., Takeshita, H., Nozato, Y., Imaizumi, Y., Fujimoto, T., Yokoyama, S., Nagasawa, M., Takeda, M., Hongyo, K., et al. (2019) · Clinical Science · doi:10.1042/cs20190573 · Cited by 37
An embryonic CaVβ1 isoform promotes muscle mass maintenance via GDF5 signaling in adult mouse
Traoré, M., Gentil, C., Benedetto, C., Hogrel, J.-Y., De la Grange, P., Cadot, B., Benkhelifa-Ziyyat, S., Julien, L., Lemaitre, M., Ferry, A., et al. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aaw1131 · Cited by 36
Skeletal Muscle Injury in Chronic Kidney Disease—From Histologic Changes to Molecular Mechanisms and to Novel Therapies
Heitman, K., Alexander, M. S., & Faul, C. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25105117 · Cited by 39
Differentially methylated gene patterns between age‐matched sarcopenic and non‐sarcopenic women
He, L., Khanal, P., Morse, C. I., Williams, A. G., & Thomis, M. A. (2019) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12478 · Cited by 35
Age-dependent decline in remyelination capacity is mediated by apelin–APJ signaling
Ito, M., Muramatsu, R., Kato, Y., Sharma, B., Uyeda, A., Tanabe, S., Fujimura, H., Kidoya, H., Takakura, N., Kawahara, Y., et al. (2021) · Nature Aging · doi:10.1038/s43587-021-00041-7 · Cited by 35
Abnormalities of Skeletal Muscle, Adipocyte Tissue, and Lipid Metabolism in Heart Failure: Practical Therapeutic Targets
Takada, S., Sabe, H., & Kinugawa, S. (2020) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2020.00079 · Cited by 34
Research Progress on Mechanism of Neuroprotective Roles of Apelin-13 in Prevention and Treatment of Alzheimer’s Disease
Wan, T., Fu, M., Jiang, Y., Jiang, W., Li, P., & Zhou, S. (2021) · Neurochemical Research · doi:10.1007/s11064-021-03448-1 · Cited by 38
Clinical-grade human umbilical cord-derived mesenchymal stem cells improved skeletal muscle dysfunction in age-associated sarcopenia mice
Wang, C., Zhao, B., Zhai, J., Wang, A., Cao, N., Liao, T., Su, R., He, L., Li, Y., Pei, X., et al. (2023) · Cell Death and Disease · doi:10.1038/s41419-023-05843-8 · Cited by 35
Exploring exercise-driven exerkines: unraveling the regulation of metabolism and inflammation
Zhou, N., Gong, L., Zhang, E., & Wang, X. (2024) · PeerJ · doi:10.7717/peerj.17267 · Cited by 35
Adipogenic progenitors in different organs: Pathophysiological implications
Favaretto, F., Bettini, S., Busetto, L., Milan, G., & Vettor, R. (2021) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-021-09686-6 · Cited by 35
Effects of exercise-induced apelin on muscle function and cognitive function in aged mice
Kwak, S. E., Cho, S. C., Bae, J. H., Lee, J., Shin, H. E., Di Zhang, D., Lee, Y.-I., & Song, W. (2019) · Experimental Gerontology · doi:10.1016/j.exger.2019.110710 · Cited by 32
Pathophysiological changes of muscle after ischemic stroke: a secondary consequence of stroke injury
Hu, Q., Tian, D., Luan, F., Yang, R., & Zeng, N. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.382221 · Cited by 35
Apelin regulates skeletal muscle adaptation to exercise in a high-intensity interval training model
Kilpiö, T., Skarp, S., Perjés, Á., Swan, J., Kaikkonen, L., Saarimäki, S., Szokodi, I., Penninger, J. M., Szabó, Z., Magga, J. M., et al. (2024) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00427.2023 · Cited by 32
Myokine, a key cytokine for physical exercise to alleviate sarcopenic obesity
Zhang, L., Lv, J., Wang, C., Ren, Y., & Ming, Y. (2022) · Molecular Biology Reports · doi:10.1007/s11033-022-07821-3 · Cited by 33
Looking at frailty and intrinsic capacity through a geroscience lens: the ICFSR & Geroscience Task Force
Barreto, P. D. S., Rolland, Y., Ferrucci, L., Arai, H., Bischoff-Ferrari, H. A., Duque, G., Fielding, R. A., Beard, J., Muscedere, J., Sierra, F., et al. (2023) · Nature Aging · doi:10.1038/s43587-023-00531-w · Cited by 30
Self-citation

Authors: Vinel, C., Lukjanenko, L., Batut, A., Deleruyelle, S., Pradère, J.-P., Le Gonidec, S., Dortignac, A., Geoffre, N., Pereira, O., Karaz, S., Lee, U., Camus, M., Chaoui, K., Mouisel, E., Bigot, A., Mouly, V., Vigneau, M., Pagano, A. F., Chopard, A., Pillard, F., Guyonnet, S., Cesari, M., Burlet-Schiltz, O., Pahor, M., Feige, J. N., Vellas, B., Valet, P., & Dray, C.
Affiliations: Université Toulouse III - Paul Sabatier (FR)
Nestlé (Switzerland) (CH)
École Polytechnique Fédérale de Lausanne (CH)
Centre National de la Recherche Scientifique (FR)
Institut des Technologies Avancées en sciences du Vivant (FR)
Université de Montpellier (FR)
University of Florida (US)
ORCID: Vinel, Claire
Deleruyelle, Simon
Pradère, Jean-Philippe
Lee, Umji
Camus, Mylène
Chaoui, Karima
Bigot, Anne
Mouly, Vincent
Pagano, Allan F.
Chopard, Angèle
Pillard, Fabien
Guyonnet, Sophie
Cesari, Matteo
Vellas, Bruno
Valet, Philippe
Venue: Nature Medicine
Publisher: Springer Science and Business Media LLC
Published: 2018-07-30
Volume: 24
Issue: 9
Pages: 1360-1371
ISSN: 1078-8956 (ISSN-L)
1546-170X
DOI: 10.1038/s41591-018-0131-6
OpenAlex: W2884388698
Cited by: 398
References: 64
Citations by year: 2026: 61 · 2025: 54 · 2024: 54 · 2023: 38 · 2022: 59 · 2021: 47 · 2020: 46 · 2019: 33 · 2018: 5
FWCI: 21.14
Type: journal article
Language: en
Open access: green
infoscience.epfl.ch
Licence: www.springer.com/tdm (tdm)
Locations: Nature Medicine (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
Funders: Agence Nationale de la Recherche (ANR-16-CE18-0022)
Topics: Health Sciences › Medicine › Pharmacology (medical) › Apelin-related biomedical research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Health Sciences › Medicine › Physiology (medical) › Nutrition and Health in Aging
Keywords: apelin, sarcopenia, aging, skeletal muscle function, physical activity, apelin receptor, mitochondrial biogenesis, autophagy, muscle stem cells, muscle regeneration, frailty, anti-inflammatory signaling, exerkines, muscle weakness
MeSH terms: Apelin, Apelin Receptors, Adenylate Kinase, Adolescent, Adult, Aged, Aged, 80 and over, Aging, Animals, Organelle Biogenesis, Body Weight, Humans, Kinetics, Mice, Inbred C57BL, Regeneration, Protein Biosynthesis, Exercise, Muscle, Skeletal, Muscle Weakness, Muscle Cells, Satellite Cells, Skeletal Muscle, Ribosomal Protein S6 Kinases, 70-kDa, Proto-Oncogene Proteins c-akt, Sarcopenia

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

The exerkine apelin reverses age-associated sarcopenia

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks