Cited by 1,008Muscle Physiology and DisordersMuscle metabolism and nutritionNutrition and Health in Aging

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The molecular basis of skeletal muscle atrophy

Jackman, Robert W., Kandarian, Susan C.·2004·American Journal of Physiology-Cell Physiology

DOI 10.1152/ajpcell.00579.2003

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Abstract

Skeletal muscle atrophy attributable to muscular inactivity has significant adverse functional consequences. While the initiating physiological event leading to atrophy seems to be the loss of muscle tension and a good deal of the physiology of muscle atrophy has been characterized, little is known about the triggers or the molecular signaling events underlying this process. Decreases in protein synthesis and increases in protein degradation both have been shown to contribute to muscle protein loss due to disuse, and recent work has delineated elements of both synthetic and proteolytic processes underlying muscle atrophy. It is also becoming evident that interactions among known proteolytic pathways (ubiquitin-proteasome, lysosomal, and calpain) are involved in muscle proteolysis during atrophy. Factors such as TNF-alpha, glucocorticoids, myostatin, and reactive oxygen species can induce muscle protein loss under specified conditions. Also, it is now apparent that the transcription factor NF-kappaB is a key intracellular signal transducer in disuse atrophy. Transcriptional profiles of atrophying muscle show both up- and downregulation of various genes over time, thus providing further evidence that there are multiple concurrent processes involved in muscle atrophy. The purpose of this review is to synthesize our current understanding of the molecular regulation of muscle atrophy. We also discuss how ongoing work should uncover more about the molecular underpinnings of muscle wasting, particularly that due to disuse.

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Tantiwong, P., Shanmugasundaram, K., Monroy, A., Ghosh, S., Li, M., DeFronzo, R. A., Cersósimo, E., Sriwijitkamol, A., Mohan, S., & Musi, N. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00776.2009 · Cited by 93
Tumor necrosis factor α signaling in skeletal muscle: effects of age and caloric restriction
Dirks, A. J., & Leeuwenburgh, C. (2005) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2005.11.002 · Cited by 95
“There exists five different potential subunits in skeletal muscle (p65, p50, p52, Rel B, c-Rel) in which combinations of two make up the NFnB transcription factor [54].”
Background
Denervation Induces Cytosolic Phospholipase A2-mediated Fatty Acid Hydroperoxide Generation by Muscle Mitochondria
Bhattacharya, A., Müller, F. L., Liu, Y., Sabia, M., Liang, H., Song, W. J., Jang, Y. C., Ran, Q., & Remmen, H. V. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m806311200 · Cited by 90
Molecular biomarkers monitoring human skeletal muscle fibres and microvasculature following long‐term bed rest with and without countermeasures
Salanova, M., Schiffl, G., Püttmann, B., Schoser, B. G., & Blottner, D. (2008) · Journal of Anatomy · doi:10.1111/j.1469-7580.2008.00854.x · Cited by 98
“Disuse-induced atrophy is characterized by considerable protein degradation (Ferrando et al. 2002) and possibly activation of the ubiquitin (Ub)–proteasome pathway (Jackman & Kandarian, 2004).”
Background
Ghrelin for cachexia
Akamizu, T., & Kangawa, K. (2010) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1007/s13539-010-0011-5 · Cited by 88
“Cachexia and muscular wasting occur via protein degradation by the ubiquitin–proteasome pathway [49].”
Background
Antioxidant Apigenin Relieves Age-Related Muscle Atrophy by Inhibiting Oxidative Stress and Hyperactive Mitophagy and Apoptosis in Skeletal Muscle of Mice
Wang, D., Yang, Y., Zou, X., Zhang, J., Zheng, Z., & Wang, Z. (2020) · The Journals of Gerontology Series A · doi:10.1093/gerona/glaa214 · Cited by 87
“Muscle atrophy is often manifested as loss of muscle mass and functions, specifically as smaller myofiber sizes, reduced myofiber mass, transition of myofiber types, and an imbalance between synthesis and degradation of proteins in muscles (4).”
Background
Ubiquitin ligase gene expression in healthy volunteers with 20‐day bedrest
Ogawa, T., Furochi, H., Mameoka, M., Hirasaka, K., Onishi, Y., Suzue, N., Oarada, M., Akamatsu, M., Akima, H., Fukunaga, T., et al. (2006) · Muscle & Nerve · doi:10.1002/mus.20611 · Cited by 90
TWEAK causes myotube atrophy through coordinated activation of ubiquitin‐proteasome system, autophagy, and caspases
Bhatnagar, S., Mittal, A., Gupta, S. K., & Kumar, A. (2011) · Journal of Cellular Physiology · doi:10.1002/jcp.22821 · Cited by 90
“…of many catabolic conditions such as diabetes, cancer, sepsis, AIDS, heart failure, denervation, immobilization, and sarcopenia and is associated with reduced quality of life and increased mortality (Kandarian and Stevenson, 2002; Jackman and Kandarian, 2004; Acharyya and Guttridge, 2007).”
Background
Bed Rest in Health and Critical Illness
Winkelman, C. (2009) · AACN Advanced Critical Care · doi:10.1097/nci.0b013e3181ac838d · Cited by 87
Mechanical ventilation promotes redox status alterations in the diaphragm
Falk, D. J., DeRuisseau, K. C., Gammeren, D. V., Deering, M. A., Kavazis, A. N., & Powers, S. K. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00104.2006 · Cited by 87
“IT IS WELL ESTABLISHED that extended periods of skeletal muscle disuse lead to the development of muscle atrophy (12, 14, 16, 25, 26, 36).”
Background
Testosterone protects against dexamethasone-induced muscle atrophy, protein degradation and MAFbx upregulation
Zhao, W., Pan, J., Zhao, Z., Wu, Y., Bauman, W. A., & Cardozo, C. P. (2008) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2008.03.024 · Cited by 89
“Glucocorticoids reduce skeletal muscle mass through mechanisms that include accelerated protein degradation [1–3] which largely reflects activation of the ubiquitin–proteasome system [2,4].”
Glycogen synthase kinase-3β is required for the induction of skeletal muscle atrophy
Verhees, K. J. P., Schols, A. M. W. J., KELDERS, M. C. J. M., den Kamp, C. M. O., van der Velden, J. L. J., & LANGEN, R. C. J. (2011) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00520.2010 · Cited by 90
Genomic Profiling of Messenger RNAs and MicroRNAs Reveals Potential Mechanisms of TWEAK-Induced Skeletal Muscle Wasting in Mice
Panguluri, S. K., Bhatnagar, S., Kumar, A., McCarthy, J. J., Srivastava, A. K., Cooper, N. G. F., Lundy, R. F., & Kumar, A. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008760 · Cited by 85
“Skeletal muscle wasting or atrophy is a major cause of human morbidity [1,2,3].”
Mitochondrial dysregulation and muscle disuse atrophy
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Reactive oxygen species promote endurance exercise-induced adaptations in skeletal muscles
Powers, S. K., Radak, Z. O., Ji, L. L., & Jackson, M. J. (2024) · Journal of sport and health science/Journal of Sport and Health Science · doi:10.1016/j.jshs.2024.05.001 · Cited by 97
“109 Although NF-k B is regulated, in part, by redox inﬂuences, the control of NF-k B activity is subject to complex regulation.”
Background
Calpain 1–titin interactions concentrate calpain 1 in the Z‐band edges and in the N2‐line region within the skeletal myofibril
Raynaud, F., Fernandez, E., Coulis, G., Aubry, L., Vignon, X., Bleimling, N., Gautel, M., Benyamin, Y., & Ouali, A. (2005) · FEBS Journal · doi:10.1111/j.1742-4658.2005.04683.x · Cited by 85
Energy sensing and regulation of gene expression in skeletal muscle
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Endogenous Muscle Atrophy F-Box Mediates Pressure Overload–Induced Cardiac Hypertrophy Through Regulation of Nuclear Factor-κB
Usui, S., Maejima, Y., Pain, J., Hong, C., Cho, J., Park, J. Y., Zablocki, D., Tian, B., Glass, D. J., & Sadoshima, J. (2011) · Circulation Research · doi:10.1161/circresaha.110.238717 · Cited by 82
Metabolism and the heart: An overview of muscle, fat, and bone metabolism in heart failure
Loncar, G., Fülster, S., von Haehling, S., & POPOVIC, V. M. (2011) · International Journal of Cardiology · doi:10.1016/j.ijcard.2011.09.079 · Cited by 85
“include cytokines or reactive oxygen species [51,52].”
Angiotensin-(1–7) decreases skeletal muscle atrophy induced by angiotensin II through a Mas receptor-dependent mechanism
Cisternas, F., Morales, M. G., Meneses, C., Simon, F., Brandan, E., Abrigo, J., Vazquez, Y., & Cabello-Verrugio, C. (2015) · Clinical Science · doi:10.1042/cs20140215 · Cited by 83
Pgc-1α overexpression Via local transfection attenuates mitophagy pathway in muscle disuse atrophy
Kang, C., & Ji, L. L. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.12.032 · Cited by 83
Saikosaponin A and D attenuate skeletal muscle atrophy in chronic kidney disease by reducing oxidative stress through activation of PI3K/AKT/Nrf2 pathway
Huang, M., Yan, Y., Deng, Z., Zhou, L., She, M., Yang, Y., Zhang, M., & Wang, D. (2023) · Phytomedicine · doi:10.1016/j.phymed.2023.154766 · Cited by 83
AMP-activated protein kinase conducts the ischemic stress response orchestra
Young, L. H. (2008) · Circulation · doi:10.1161/circulationaha.107.713115 · Cited by 82
Quantitative and temporal differential recovery of articular and muscular limitations of knee joint contractures; results in a rat model
Trudel, G., Laneuville, O., Coletta, E., Goudreau, L., & Uhthoff, H. K. (2014) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00409.2014 · Cited by 82
“However, atrophy characterized by decrease in protein synthesis and increase in protein degradation resulting in a decreased protein content, smaller fiber diameter, force production, fatigue resistance, and muscle volume was shown to decrease the muscle passive extensibility (4, 13, 14, 22, 56).”
Background
Growth Factors for Skeletal Muscle Tissue Engineering
Syverud, B. C., VanDusen, K. W., & Larkin, L. M. (2016) · Cells Tissues Organs · doi:10.1159/000444671 · Cited by 82
Dynamic changes in the skeletal muscle proteome during denervation-induced atrophy
Lang, F., Aravamudhan, S., Nolte, H., Tuerk, C., Hölper, S., Müller, S., Günther, S., Blaauw, B., Braun, T. W., & Krüger, M. (2017) · Disease Models & Mechanisms · doi:10.1242/dmm.028910 · Cited by 85
“Reduced muscle recruitment, such as occurs during extended bed rest or spinal cord injury, results in a severe loss of muscle mass, which is also termed muscle atrophy (Gutmann, 1962; Jackman and Kandarian, 2004).”
Background
Little change in markers of protein breakdown and oxidative stress in humans in immobilization-induced skeletal muscle atrophy
Glover, E. I., Yasuda, N., Tarnopolsky, M. A., Abadi, A., & Phillips, S. M. (2010) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h09-137 · Cited by 84
“The bulk of our knowledge in this area is based on animal work, and the overall picture that emerges from these studies indicates that proteolysis is significantly elevated and is considered to be primarily responsible for the lean tissue loss that occurs with unweighting (Goldspink et al. 1986; Jackman and Kandarian…”
Background
Proteomics of skeletal muscle aging
Doran, P., Donoghue, P. M., O’Connell, K. M., Gannon, J. M., & Ohlendieck, K. (2009) · PROTEOMICS · doi:10.1002/pmic.200800365 · Cited by 81
Microtubule-mediated NF-κB activation in the TNF-α signaling pathway
Jackman, R. W., Rhoads, M. G., Cornwell, E. W., & Kandarian, S. C. (2009) · Experimental Cell Research · doi:10.1016/j.yexcr.2009.08.020 · Cited by 79
“In skeletal muscle, this system is thought to be important in the atrophyof cachexia [9,17,18] andhas been shown to be required for atrophy due to disuse [19].”
Proteomics of skeletal muscle glycolysis
Ohlendieck, K. (2010) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2010.08.001 · Cited by 83
Glucocorticoid-induced Leucine Zipper (GILZ) and Long GILZ Inhibit Myogenic Differentiation and Mediate Anti-myogenic Effects of Glucocorticoids
Bruscoli, S., Donato, V., Velardi, E., Sante, M. D., Migliorati, G., Donato, R., & Riccardi, C. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.070136 · Cited by 85
Amyotrophic Lateral Sclerosis and Skeletal Muscle: An Update
Pansarasa, O., Rossi, D., Berardinelli, A. L., & Cereda, C. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8578-4 · Cited by 79
“However, under inactivity, aging or neuromuscular diseases, skeletal muscles undergo decline in functional performance and adaptability, and this becomes a hallmark of those pathological conditions [4].”
Background
Muscle immobilization activates mitophagy and disrupts mitochondrial dynamics in mice
Kang, C., Yeo, D., & Ji, L. L. (2016) · Acta Physiologica · doi:10.1111/apha.12690 · Cited by 81
Deep RNA Sequencing of the Skeletal Muscle Transcriptome in Swimming Fish
Palstra, A. P., Beltrán, S., Burgerhout, E., Brittijn, S. A., Magnoni, L. J., Henkel, C. V., Jansen, H. J., van den Thillart, G. E. E. J. M., Spaink, H. P., & Planas, J. V. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053171 · Cited by 78
“Finally, we identified a large set of genes involved in the regulation of protein degradation, mostly belonging to the ubiquitinproteasome pathway, but also calpain proteases 1 and 3, with known roles in myofibrillar protein turnover (reviewed in [39]), and NF-kB p100 subunit and NF-kB inhibitor epsilon, two signallin…”
Background
The administration of Fructus Schisandrae attenuates dexamethasone-induced muscle atrophy in mice
Kim, J. W., Ku, S., Han, M. H., Kim, K. Y., Kim, S. G., Kim, G., Hwang, H. J., Kim, B. W., Kim, C. M., & Choi, Y. H. (2015) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2015.2200 · Cited by 79
“Four systems of proteolytic degradation are involved in muscle atrophy: the lysosomal protease system (cathepsin), calpain calcium-dependent signaling, caspase signaling and the ubiquitin-proteasome system (5,6).”
The role of vitamin D in skeletal and cardiac muscle function
Polly, P., & Tan, T. C. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00145 · Cited by 80
“…2008) and is characterized by weight loss; up-regulation of inflammatory markers such as IL-6, IL-1, TNF-α and interferon gamma (IFN)γ; hypercalcemia; and insulin resistance (Argiles et al., 2003; Sato et al., 2003; Jackman and Kandarian, 2004; Evans et al., 2008; Tisdale, 2009; Asp et al., 2010).”
Background
Leucine Supplementation Improves Skeletal Muscle Regeneration after Cryolesion in Rats
Pereira, M. G., Baptista, I. L., Carlassara, E. O. C., Moriscot, A. S., Aoki, M. S., & Miyabara, E. H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085283 · Cited by 79
“Finally, the termini of ubiquitinated proteins are tagged for degradation in the proteasome [20,21,22].”
Background
REDD1 Is a Major Target of Testosterone Action in Preventing Dexamethasone-Induced Muscle Loss
Wu, Y., Zhao, W., Zhao, J., Zhang, Y., Qin, W., Pan, J., Bauman, W. A., Blitzer, R. D., & Cardozo, C. P. (2009) · Endocrinology · doi:10.1210/en.2009-0530 · Cited by 81
Inhibition of Atrogin-1/MAFbx Expression by Adenovirus-Delivered Small Hairpin RNAs Attenuates Muscle Atrophy in Fasting Mice
Cong, H., Sun, L., Liu, C.-M., & Tien, P. (2010) · Human Gene Therapy · doi:10.1089/hum.2010.057 · Cited by 87
“During this process, massive changes in the expression of some atrophy genes and growth factors have been shown to be involved, leading to muscle protein loss ( Jackman and Kandarian, 2004).”
Turning the gun on cancer: Utilizing lysosomal P-glycoprotein as a new strategy to overcome multi-drug resistance
Seebacher, N. A., Lane, D. J. R., Richardson, D. R., & Jansson, P. J. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.04.201 · Cited by 77
A Novel Glycerophosphodiester Phosphodiesterase, GDE5, Controls Skeletal Muscle Development via a Non-enzymatic Mechanism
Okazaki, Y., Ohshima, N., Yoshizawa, I., Kamei, Y., Mariggiò, S., Okamoto, K., Maeda, M., Nogusa, Y., Fujioka, Y., Izumi, T., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.106708 · Cited by 76

Authors: Jackman, R. W., & Kandarian, S. C.
Affiliations: Boston University (US)
Venue: American Journal of Physiology-Cell Physiology
Publisher: American Physiological Society
Published: 2004-10
Volume: 287
Issue: 4
Pages: C834-C843
ISSN: 0363-6143 (ISSN-L)
1522-1563
DOI: 10.1152/ajpcell.00579.2003
OpenAlex: W2127808488
Cited by: 1,008
References: 118
Citations by year: 2026: 18 · 2025: 21 · 2024: 53 · 2023: 34 · 2022: 33 · 2021: 35 · 2020: 45 · 2019: 50 · 2018: 38 · 2017: 41 · 2016: 52 · 2015: 59 · 2014: 49 · 2013: 64 · 2012: 49
FWCI: 3.83
Type: journal article
Language: en
Open access: closed
Locations: American Journal of Physiology-Cell Physiology (publishedVersion)
PubMed (publishedVersion)
Funders: National Space Biomedical Research Institute
National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01 AR-41705, R01AR041705)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
Health Sciences › Medicine › Physiology (medical) › Nutrition and Health in Aging
Keywords: skeletal muscle atrophy, disuse atrophy, muscle protein degradation, muscle protein synthesis, ubiquitin-proteasome system, lysosomal proteolysis, calpain, TNF-α, glucocorticoids, myostatin, reactive oxygen species, NF-κB, transcriptional regulation, muscle atrophy
MeSH terms: Muscle Proteins, Muscular Atrophy, Transcription, Genetic, Signal Transduction, Gene Expression, NF-kappa B, Muscle, Skeletal, Muscular Disorders, Atrophic

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The molecular basis of skeletal muscle atrophy

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