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The molecular basis of skeletal muscle atrophy
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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“Various stimuli, such as aging, genetics, denervation, starvation, unhealthy lifestyle (i.e., sedentariness, high fat diet (HFD)), systemic pathologies (i.e., diabetes, inflammation, cancer), and long-term drug therapy (i.e., glucocorticoids) are known to further skeletal muscle loss and weakness [2,3,4].”
From Nutraceuticals in the Prevention and Treatment of the Muscle Atrophy (2021) · cites this paper as [3]
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InfluentialWhat determines growth potential and juvenile quality of farmed fish species?
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“Protein degradation can be mediated by four main proteolytic systems: calpains, caspases, lysosomes and the ubiquitin-proteasome system (UPS; Jackman & Kandarian 2004).”
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“E3 ubiquitin ligases are a family of enzymes that determine which protein will be ubiquitinated and degraded [1, 145].”
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“Taken together, all four proteolytic systems have been demonstrated to be critically involved in skeletal muscle atrophy [14-16].”
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“However, proteolysis is the predominant factor responsible for disuse skeletal muscle atrophy and myofibrillar proteins are lost at a rate faster than other muscle proteins [2].”
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“by FOXO, muscle atrophy F-box (MAFbx; also called atrogin-1) and MuscleRING-Finger-1 (MuRF-1), mark proteins for degradation by covalent modification with polyubiquitin chains (Auclair et al., 1997; Jackman and Kandarian, 2004; Pickart, 2001).”
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“Myostatin inhibits muscle growth by inactivation of protein kinase B (also known as Akt), a promoter of protein synthesis, and by hampering muscle cell renewal (21).”
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“Atrophy of skeletal muscle occurs with disuse or denervation and systemically in fasting and disease states, including sepsis, cancer cachexia, and renal and cardiac failure (Jackman and Kandarian, 2004; Lecker et al., 2006).”
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“Although extended periods of disuse also lead to locomotor skeletal muscle atrophy [13,17–26], a unique characteristic of MV-induced diaphragmatic atrophy is the rapidity of the atrophic response [25,26].”
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“The down-regulation of thin filament proteins in the muscle proteome is in agreement with animal studies (Jackman & Kandarian, 2004), and with human studies, which showed a decreased number of thin filaments in disuse (Riley et al. 1998) and a decreased myosin concentration in individual muscle…”
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BackgroundThe association between COPD and heart failure risk: a review
de Miguel‐Díez, J., Morgan, C., & Jiménez‐García, R. (2013) · International Journal of COPD · doi:10.2147/copd.s31236 · Cited by 188
“The mechanisms involved in muscular atrophy in both diseases are unknown, although they seem to be related to muscular disease, systemic inflammation, and an increase in oxidative stress, which contributes to reducing protein synthesis and accelerating protein degradation.(29) High circulatory values of proinflammator…”
Levine, M. E., & Crimmins, E. M. (2012) · Obesity · doi:10.1038/oby.2012.20 · Cited by 186
Molecular determinants of skeletal muscle mass: getting the “AKT” together
Nader, G. A. (2005) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2005.02.026 · Cited by 184
“…muscle mass is a rather complex phenomenon, and several excellent reviews have been recently published addressing this topic in great detail (Glass, 2003; Jackman & Kandarian, 2004; Lecker, Solomon, Mitch, & Goldberg, 1999; Rennie, Wackerhage, Spangenburg, & Booth, 2004; Sartorelli & Fulco, 2004).”
BackgroundSharples, A. P., Stewart, C. E., & Seaborne, R. A. (2016) · Aging Cell · doi:10.1111/acel.12486 · Cited by 180
“NF-jB’s signalling has also been shown to be involved in atrophy of skeletal muscle via protein degradation (reviewed in Jackman & Kandarian, 2004; Bakkar et al., 2008), but also plays a role in early muscle cell survival where NF-jB inhibition in the presence of an apoptotic dose of tumour…”
BackgroundVentilator-induced diaphragmatic dysfunction
Petrof, B. J., Jaber, S., & Matecki, S. (2009) · Current Opinion in Critical Care · doi:10.1097/mcc.0b013e328334b166 · Cited by 180
Díaz, F., Thomas, C. K., García, S., Hernandez, D., & Moraes, C. T. (2005) · Human Molecular Genetics · doi:10.1093/hmg/ddi307 · Cited by 179
“The molecular mechanisms of muscle wasting are not completely understood but involve reduced protein synthesis, increased proteolysis (calpain, cathepsins and ubiquitin) and oxidative stress (28,29).”
BackgroundEffect of pulmonary rehabilitation on muscle remodelling in cachectic patients with COPD
Vogiatzis, I., Simoes, D. C. M., Stratakos, G. K., Kourepini, E., Terzis, G. D., Manta, P., Athanasopoulos, D., Roussos, C., Wagner, P. D., & Zakynthinos, S. G. (2010) · European Respiratory Journal · doi:10.1183/09031936.00112909 · Cited by 173
“In muscle, NF-κB can also inhibit mRNA and protein expression of MyoD [14, 25], an essential transcription factor in myogenesis [9].”
BackgroundInfluentialServais, S., Letexier, D., Favier, R. J. M., Duchamp, C., & Dominique Desplanches, C. (2006) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2006.12.001 · Cited by 174
“regulators in the enhanced proteolysis leading to muscle atrophy in various diseases (2, 42).”
BackgroundCunha, T. F., Bacurau, A. V. N., Moreira, J. B. N., da Paixão, N. A., Campos, J. C., Ferreira, J. C. B., Leal, M. L., Negrão, C. E., Moriscot, A. S., Wisløff, U., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041701 · Cited by 174
“Overwhelming evidence demonstrates a striking association between disease-induced skeletal muscle atrophy and UPS activation [4], which also occurs in HF [34,35].”
BackgroundGut microbiota–bile acid–skeletal muscle axis
Mancin, L., Wu, G. D., & Paoli, A. (2022) · Trends in Microbiology · doi:10.1016/j.tim.2022.10.003 · Cited by 183
Renin‐Angiotensin System: An Old Player with Novel Functions in Skeletal Muscle
Cabello‐Verrugio, C., Morales, M. G., Rivera, J. C. A., Cabrera, D., & Simón, F. (2015) · Medicinal Research Reviews · doi:10.1002/med.21343 · Cited by 170
Kumar, A., Lin, Z., SenBanerjee, S., & Jain, M. K. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.14.5893-5903.2005 · Cited by 165
“For example, TNF- is known to induce muscle wasting and atrophy (9, 14).”
BackgroundIn vivo time-lapse microscopy reveals no loss of murine myonuclei during weeks of muscle atrophy
Bruusgaard, J. C., & Gundersen, K. (2008) · Journal of Clinical Investigation · doi:10.1172/jci34022 · Cited by 162
“4), and this has been related to a loss of myonuclei (5–17) by apoptosis (6, 8, 9, 12, 15, 18–27).”
Doxorubicin acts via mitochondrial ROS to stimulate catabolism in C2C12 myotubes
Gilliam, L. A. A., Moylan, J. S., Patterson, E. W., Smith, J. D., Wilson, A. S., Rabbani, Z., & Reid, M. B. (2011) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00217.2011 · Cited by 170
“systems including caspase-3 and the ubiquitin-proteasome pathway (3, 4, 21).”
BackgroundDurieux, A., Amirouche, A., Banzet, S., Koulmann, N., Bonnefoy, R., Pasdeloup, M., Mouret, C., Bigard, X. A., Peinnequin, A., & Freyssenet, D. G. (2007) · Endocrinology · doi:10.1210/en.2006-1500 · Cited by 162
Increased Proteolysis, Myosin Depletion, and Atrophic AKT-FOXO Signaling in Human Diaphragm Disuse
Levine, S., Biswas, C., Dierov, J. K., Barsotti, R., Shrager, J. B., Nguyen, T., Sonnad, S. S., Kucharchzuk, J. C., Kaiser, L. R., Singhal, S. K., et al. (2010) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200910-1487oc · Cited by 162
“, noncanonical) nuclear factor–kB (29, 32, 33); P-38 mitogenactivated protein kinase (34, 35); myostatin (28, 35), other members of the transforming growth factor–b family (28, 36, 37).”
BackgroundThe central role of hypothalamic inflammation in the acute illness response and cachexia
Burfeind, K. G., Michaelis, K. A., & Marks, D. L. (2016) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2015.10.038 · Cited by 156
“TNFα—Although TNFα has direct effects on various target tissues [84,86,87], its most potent actions in regard to cachexia occur in the hypothalamus.”
BackgroundUbiquitin–protein ligases in muscle wasting
Cao, P., Kim, H. J., & Lecker, S. H. (2004) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2004.11.010 · Cited by 157
“…to atrogin-1 and MuRF1, Kandarian and coworkers have evidence that mRNA for Nedd4, a HECT-domain E3 is increased in muscles atrophying from disuse (Jackman & Kandarian, 2004), though act f atr dent led K sc , a for u ome ( o - e pec h aneb le in s tates ( as U , f inat ed in myosin assembly…”
BackgroundBuild it up-Tear it down: protein quality control in the cardiac sarcomere
Willis, M. S., Schisler, J. C., Portbury, A. L., & Patterson, C. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvn289 · Cited by 156
“Various members of the calpain family have been localized to skeletal muscle where they are purported to be involved in both muscle growth and atrophy.(75,76) Calpain 1 has been found in tight association with skeletal muscle myofibrils where it binds tightly to the giant protein titin in a calciumdependent manner.”
BackgroundHuijing, P. A., & Jaspers, R. T. (2005) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2005.00457.x · Cited by 159
“During muscle atrophy in response to disuse or immobilization, protein degradation is enhanced by activation of proteolytic pathways (see for detailed review, Jackman & Kandarian, 2004).”
BackgroundControl of Muscle Size During Disuse, Disease, and Aging
Degens, H., & Alway, S. E. (2006) · International Journal of Sports Medicine · doi:10.1055/s-2005-837571 · Cited by 155
Diaphragm adaptations in patients with COPD
Ottenheijm, C. A. C., Heunks, L. M. A., & Dekhuijzen, R. P. N. (2008) · Respiratory Research · doi:10.1186/1465-9921-9-12 · Cited by 163
“In general, striated muscle atrophy results from increased proteolysis, rather than decreased synthesis [ 50 ].”
Response of the ubiquitin-proteasome pathway to changes in muscle activity
Reid, M. B. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00545.2004 · Cited by 161
“Among many excellent reviews published recently, those by Glass (14), Jackman and Kandarian (24), Jagoe and Goldberg (25), and Lecker (32) provide especially good overviews of this complex topic for readers who seek greater detail.”
BackgroundAssessing the role of muscle protein breakdown in response to nutrition and exercise in humans.
Tipton, K. D., Hamilton, D. L., & Gallagher, I. J. (2018) · Sports Medicine · doi:10.1007/s40279-017-0845-5 · Cited by 152
“Whereas mechanistic data are lacking from human studies, data from animal models suggest that the UPP and calpain systems play a much larger role than autophagy [17].”
BackgroundTherapeutic approaches for muscle wasting disorders
Lynch, G. S., Schertzer, J. D., & Ryall, J. G. (2006) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2006.11.004 · Cited by 155
Fediuc, S., Campbell, J. E., & Riddell, M. C. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01416.2005 · Cited by 148
“DYSREGULATION AND HYPERRESPONSIVENESS of the hypothalamicpituitary-adrenal (HPA) axis have been linked to a number of pathological conditions such as increased insulin resistance (45), increased adiposity (34), immune suppression (28, 36), depression (18), osteoporosis (37), muscle wasting (21), and cardiovascular dis…”
BackgroundPressure support ventilation attenuates ventilator-induced protein modifications in the diaphragm
Futier, E., Constantin, J., Combaret, L., Mosoni, L., Roszyk, L., Sapin, V., Attaix, D., Jung, B., Jaber, S., & Bazin, J.-É. (2008) · Critical Care · doi:10.1186/cc7010 · Cited by 145
“Is protein oxidation a real trigger? Little is currently known concerning the triggers or molecular signals of MV-induced protein metabolism modifications and muscle atrophy [51, 54 ].”
BackgroundSriwijitkamol, A., Christ-Roberts, C. Y., Berria, R., Eagan, P. A., Pratipanawatr, T., DeFronzo, R. A., Mandarino, L. J., & Musi, N. (2006) · Diabetes · doi:10.2337/diabetes.55.03.06.db05-0677 · Cited by 146
The ubiquitin-proteasome pathway as a therapeutic target for muscle wasting.
Tisdale, M. J. (2005) · PubMed · Cited by 145
Tang, H., Inoki, K., Lee, M. C., Wright, E., Khuong, A., Khuong, A., Sugiarto, S., Garner, M. S., Paik, J., DePinho, R. A., et al. (2014) · Science Signaling · doi:10.1126/scisignal.2004809 · Cited by 145
Tang, H., Macpherson, P. C. D., Marvin, M. C., Meadows, E., Klein, W. H., Yang, X., & Goldman, D. J. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-07-0759 · Cited by 142
“Nerve activity also plays a crucial role in maintaining muscle mass (Jackman and Kandarian, 2004) and in shaping the formation of the neuromuscular junction (NMJ) (Sunesen and Changeux, 2003; Kummer et al.”
BackgroundNuclear domains during muscle atrophy: nuclei lost or paradigm lost?
Gundersen, K., & Bruusgaard, J. C. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.154369 · Cited by 140
“…are not lost, atrophy and recovery from it simply reflect changes in the balance between protein synthesis and proteolysis (for reviews see Glass, 2003, 2005; Jackman & Kandarian, 2004), and intervention therapies should concentrate on such mechanisms rather than on regeneration from stem cells.”
BackgroundCalorie restriction accelerates the catabolism of lean body mass during 2 wk of bed rest
Biolo, G., Ciocchi, B., Stulle, M., Bosutti, A., Barazzoni, R., Zanetti, M., Antonione, R., Lebenstedt, M., Platen, P., Heer, M. A., et al. (2007) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/86.2.366 · Cited by 139
“The specific effects of inactivity on physiologic functions include decreased turnover of skeletal muscle proteins (1–3) and impaired dietary amino acid utilization (4), which lead to muscle dysfunction and atrophy (5, 6).”
BackgroundHudson, M. B., Woodworth-Hobbs, M. E., Zheng, B., Rahnert, J. A., Blount, M. A., Gooch, J. L., Searles, C. D., & Price, S. R. (2014) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00266.2013 · Cited by 137
“, mechanical ventilation, diabetes, chronic kidney disease, and glucocorticoid-induced insulin resistance) that decreases the quality of life for patients and increases their risk of mortality (13, 15, 25, 34).”
Dyle, M. C., Ebert, S. M., Cook, D. P., Kunkel, S. D., Fox, D. K., Bongers, K. S., Bullard, S. A., Dierdorff, J. M., & Adams, C. M. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.556241 · Cited by 138
Redox homeostasis, oxidative stress and disuse muscle atrophy
Pellegrino, M. A., Desaphy, J., Brocca, L., Pierno, S., Camerino, D. C., & Bottinelli, R. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2010.203232 · Cited by 143
Intensive Care Unit-Acquired Weakness: Not Just Another Muscle Atrophying Condition
Lad, H., Saumur, T. M., Herridge, M. S., dos Santos, C. C., Mathur, S., Batt, J. A. E., & Gilbert, P. M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21217840 · Cited by 150
Metadata
- 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
- 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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