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Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression
Abstract
Skeletal muscle atrophy is a debilitating response to starvation and many systemic diseases including diabetes, cancer, and renal failure. We had proposed that a common set of transcriptional adaptations underlie the loss of muscle mass in these different states. To test this hypothesis, we used cDNA microarrays to compare the changes in content of specific mRNAs in muscles atrophying from different causes. We compared muscles from fasted mice, from rats with cancer cachexia, streptozotocin‐induced diabetes mellitus, uremia induced by subtotal nephrectomy, and from pair‐fed control rats. Although the content of >90% of mRNAs did not change, including those for the myofibrillar apparatus, we found a common set of genes (termed atrogins) that were induced or suppressed in muscles in these four catabolic states. Among the strongly induced genes were many involved in protein degradation, including polyubiquitins, Ub fusion proteins, the Ub ligases atrogin‐1/MAFbx and MuRF‐1, multiple but not all subunits of the 20S proteasome and its 19S regulator, and cathepsin L. Many genes required for ATP production and late steps in glycolysis were down‐regulated, as were many transcripts for extracellular matrix proteins. Some genes not previously implicated in muscle atrophy were dramatically up‐regulated (lipin, metallothionein, AMP deaminase, RNA helicase‐related protein, TG interacting factor) and several growth‐related mRNAs were down‐regulated (P311, JUN, IGF‐1‐BP5). Thus, different types of muscle atrophy share a common transcriptional program that is activated in many systemic diseases.—Lecker, S. H., Jagoe, R. T., Gilbert, A., Gomes, M., Baracos, V., Bailey, J., Price, S. R., Mitch, W. E., Goldberg, A. L. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression.—Stewart H. Lecker, R. Thomas Jagoe, Alexander Gilbert, Marcelo Gomes, Vickie Baracos, James Bailey, S. Russ Price, William E. Mitch, Alfred L. Goldberg Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 18, 39–51 (2004)
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“Genes encoding for glycolysis and oxidative phosphorylation enzymes are coordinately suppressed in atrophying muscles during denervation, disuse, diabetes, cancer, fasting, and chronic kidney disease [10, 11, 13, 20].”
From The connection between the dynamic remodeling of the mitochondrial network and the regulation of muscle mass (2021) · cites this paper as [11]
In the citing paper
“Muscle atrophy requires the activation of gene transcription programs that regulate the expression of a subset of genes that are named atrophy-related genes or atrogenes [10–14].”
From The connection between the dynamic remodeling of the mitochondrial network and the regulation of muscle mass (2021) · cites this paper as [11]
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“Therefore, this points to a concept that a common transcriptional program underlies the loss of skeletal muscle mass independently of the triggering factor (Lecker et al. 2004; Sandri et al. 2006).”
BackgroundFoxO transcription factors: their roles in the maintenance of skeletal muscle homeostasis
Sanchez, A. M. J., Candau, R. B., & Bernardi, H. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1513-z · Cited by 349
“FoxO1 and FoxO3 mRNAs are upregulated during dexamethasone treatment [47, 110] and glucocorticoids seem to induce the activation of FoxO factors by decreasing the activity of the PI3K/Akt pathway.”
Sanchez, A. M., Csibi, A., Raibon, A., Cornille, K., Gay, S., Bernardi, H., & Candau, R. (2012) · Journal of Cellular Biochemistry · doi:10.1002/jcb.23399 · Cited by 306
“, 1999], cancer cachexia, sepsis, diabetes, or AIDS, and exacerbated by glucocorticoid treatment, micro-gravity, and starvation [Mitch and Goldberg, 1996; Fitts et al., 2001; Lecker et al., 2004].”
BackgroundRegulation of Muscle Protein Degradation
Lee, S. W., Dai, G., Hu, Z., Wang, X., Du, J., & Mitch, W. E. (2004) · Journal of the American Society of Nephrology · doi:10.1097/01.asn.0000127211.86206.e1 · Cited by 324
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“muscles of rats with CKD, diabetes, starvation, or cancer (6) suggest that positive therapeutic interventions in one catabolic condition might apply to other conditions with these characteristics.”
BackgroundSelf-citationAcharyya, S., Butchbach, M. E. R., Sahenk, Z., Wang, H., Saji, M., Carathers, M., Ringel, M. D., Skipworth, R. J. E., Fearon, K. C. H., Hollingsworth, M. A., et al. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.10.004 · Cited by 323
Myostatin/activin pathway antagonism: molecular basis and therapeutic potential
Han, H. Q., Zhou, X., Mitch, W. E., & Goldberg, A. L. (2013) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2013.05.019 · Cited by 314
Self-citationComputed tomography-defined muscle and fat wasting are associated with cancer clinical outcomes
Kazemi‐Bajestani, S. M. R., Mazurak, V. C., & Baracos, V. E. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.09.001 · Cited by 322
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Psutka, S. P., Carrasco, A., Schmit, G. D., Moynagh, M. R., Boorjian, S. A., Frank, I., Stewart, S. B., Thapa, P. B., Tarrell, R. F., Cheville, J. C., et al. (2014) · Cancer · doi:10.1002/cncr.28798 · Cited by 298
“of lymph nodes dissected (IQR) 10 (4-24) 12 (5-18) 11 (5-20) .”
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 303
Development of proteasome inhibitors as research tools and cancer drugs
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“…atrophying muscles undergo a series of transcriptional adaptations involving FoxO transcription factors that enhance their capacity for proteolysis (Lecker et al., 2004; Sandri et al., 2004), including increased expression of ubiquitin and key ubiquitination enzymes (Bodine et al., 2001; Gomes et…”
BackgroundSelf-citationThe muscle fiber type–fiber size paradox: hypertrophy or oxidative metabolism?
Wessel, T. V., HAAN, A. D., van der Laarse, W. J., & Jaspers, R. T. (2010) · European Journal of Applied Physiology · doi:10.1007/s00421-010-1545-0 · Cited by 303
“proteasome activity and protein degradation (Lecker et al. 2004; Sandri et al. 2004; Stitt et al. 2004) (Suppl.”
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The muscle-specific ubiquitin ligase atrogin-1/MAFbx mediates statin-induced muscle toxicity
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“amyotrophic lateral sclerosis, and might also be implied in cancer-related muscle atrophy [9,13].”
Intensive care unit-acquired weakness
Griffiths, R., & Hall, J. B. (2010) · Critical Care Medicine · doi:10.1097/ccm.0b013e3181cc4b53 · Cited by 277
“The ubiquitin ligases atrogin-1 and MuRF1 are marked features of muscle atrophy in sepsis (82, 83) and appear upregulated by the FoxO family (Forkhead box O) transcription factors in many different situations.”
BackgroundThe regulation of muscle mass by endogenous glucocorticoids
Braun, T. P., & Marks, D. L. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2015.00012 · Cited by 273
“Both are expressed exclusively in skeletal muscle and requisite for the process of normal atrophy (Jagoe et al., 2002; Lecker et al., 2004; Sacheck et al., 2007).”
BackgroundInflammation induced loss of skeletal muscle
Londhe, P., & Guttridge, D. C. (2015) · Bone · doi:10.1016/j.bone.2015.03.015 · Cited by 276
“During the induction of muscle atrophy, distinct transcriptional pathways are activated, which catalyze increased protein turnover and degradation [14,15].”
Muscle Atrophy Induced by Mechanical Unloading: Mechanisms and Potential Countermeasures
Gao, Y., Arfat, Y., Wang, H., & Goswami, N. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00235 · Cited by 289
“For more details see text. rapidly increasing and thought to play a crucial role in the initiation of the atrophy process (Bodine et al., 2001a; Lecker et al., 2004; Murton et al., 2008; Allen et al., 2009; Baehr et al., 2017; Gambara et al., 2017).”
BackgroundThe involvement of the ubiquitin proteasome system in human skeletal muscle remodelling and atrophy
Murton, A. J., Constantin, D., & Greenhaff, P. L. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2008.10.011 · Cited by 286
Mechanical Ventilation–induced Diaphragm Disuse in Humans Triggers Autophagy
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“Lecker and colleagues (52) have reported that FOXO1 gene expression is substantially induced in atrophied muscles of fasted mice, rats with cancer cachexia, streptozotocin-induced diabetes mellitus, and uremia.”
BackgroundStat3 Activation Links a C/EBPδ to Myostatin Pathway to Stimulate Loss of Muscle Mass
Zhang, L., Pan, J. S.-C., Dong, Y., Tweardy, D. J., Dong, Y., Garibotto, G., & Mitch, W. E. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.07.012 · Cited by 263
“degradation via the ubiquitin-proteasome system (UPS) (Zhang et al., 2011; Lecker et al., 2004).”
Self-citationMuscle Giants: Molecular Scaffolds in Sarcomerogenesis
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“expression of autophagy [26,31] and lysosomal [31] related”
The role of E3 ubiquitin-ligases MuRF-1 and MAFbx in loss of skeletal muscle mass
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Mechanisms Modulating Skeletal Muscle Phenotype
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Metadata
- Authors
- Lecker, S. H., Jagoe, R. T., Gilbert, A., Gomes, M., Baracos, V., Bailey, J., Price, S. R., Mitch, W. E., & Goldberg, A. L.
- Affiliations
- Beth Israel Deaconess Medical Center (US)
- Aintree University Hospitals NHS Foundation Trust (GB)
- Harvard University (US)
- University of Alberta (CA)
- Emory University (US)
- The University of Texas Medical Branch at Galveston (US)
- Venue
- The FASEB Journal
- Publisher
- Wiley
- Published
- 2004-01
- Volume
- 18
- Issue
- 1
- Pages
- 39-51
- ISSN
- 0892-6638 (ISSN-L)
- 1530-6860
- OpenAlex
- W2169448756
- Cited by
- 1,539
- References
- 89
- Citations by year
- 2026: 18 · 2025: 27 · 2024: 41 · 2023: 62 · 2022: 49 · 2021: 70 · 2020: 51 · 2019: 70 · 2018: 73 · 2017: 66 · 2016: 77 · 2015: 76 · 2014: 86 · 2013: 91 · 2012: 111
- FWCI
- 28.36
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The FASEB Journal (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (DK02727)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Physiology (medical) › Nutrition and Health in Aging
- Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
- Keywords
- skeletal muscle atrophy, gene expression, protein degradation, ubiquitin ligase, atrogin-1/MAFbx, MuRF1, proteasome, cathepsin L, cancer cachexia, diabetes mellitus, uremia, starvation, transcriptional programs, extracellular matrix, lipin, metallothionein, AMP deaminase
- MeSH terms
- Adenosine Triphosphate, Animals, Gene Expression Regulation, Metallothionein, Muscular Atrophy, Nitrogen, Proteins, RNA, Messenger, Transcription Factors, Transcription, Genetic, Protein Biosynthesis, Extracellular Matrix Proteins, Muscle, Skeletal, Gene Expression Profiling, Ubiquitin-Protein Ligases, Mice, Rats
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