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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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“MuRF and MAFbx have also been shown to increase after starvation induced skeletal muscle atrophy (Gomes et al., 2001; Lecker et al., 2004) and are elevated in aging and cachexia (Gomes et al., 2001; Lecker et al., 2004; Clavel et al., 2006; Costelli et al., 2006; Raue et al., 2007; Altun et al.,…”
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“A major contribution in identifying the ubiquitin-ligases involved in the atrophy process was provided by the pioneering studies on gene expression profiling [37–39].”
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Anti-TNF Treatment Reduces Rat Skeletal Muscle Wasting in Monocrotaline-Induced Cardiac Cachexia
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“Furthermore, atrogin-1 and MuRF1 mRNA levels are increased in numerous in vitro and in vivo mouse models of muscle atrophy [51, 6, 23, 35].”
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“duction and late steps in glycolysis are down-regulated in atrophying muscles [9].”
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“AMPD3 mRNA is reported to be one of the most upregulated genes in atrophying muscles from cancer [149], diabetes [149], renal failure [150], aging [151], Huntington’s disease [152], fasting [149,153], unloading [154], and denervation [153,155,156].”
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“In particular, the transcriptional induction of a few ubiquitin ligases has been considered a standard response that occurs in multiple types of skeletal muscle atrophy induced by diverse stimuli, such as cancer-associated cachexia, starvation-induced atrophy, denervation, diabetes, kidney failure, and infections (Gom…”
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“These studies indicate that a common muscle atrophy program may underlie wasting as present in multiple experimental models (Lecker et al., 2004).”
BackgroundMalnutrition and wasting in renal disease
Muscaritoli, M., Molfino, A., Bollea, M. R., & Fanelli, F. R. (2009) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e32832c7ae1 · Cited by 66
Qin, W., Pan, J., Wu, Y., Bauman, W. A., & Cardozo, C. P. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.11.061 · Cited by 68
MacDonald, E. M., Andrés‐Mateos, E., Mejías, R., Simmers, J. L., Mi, R., Park, J.-S., Ying, S., Höke, A., Lee, S., & Cohn, R. D. (2014) · Disease Models & Mechanisms · doi:10.1242/dmm.014126 · Cited by 67
“Atrogenes have been shown to mediate the loss of muscle mass in multiple pathological conditions (Lecker and Goldberg, 2002; Lecker et al., 2004; Sacheck et al., 2007).”
BackgroundThe role of sex steroid hormones in the pathophysiology and treatment of sarcopenia
Kim, Y. J., Tamadon, A., Park, H. T., Kim, H., & Ku, S. (2016) · Osteoporosis and Sarcopenia · doi:10.1016/j.afos.2016.06.002 · Cited by 76
“[19] Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, et al.”
BackgroundJohns, N., Stretch, C., Tan, B. H. L., Solheim, T. S., Sørhaug, S., Stephens, N. A., Gioulbasanis, I., Skipworth, R. J. E., Deans, D. A. C., Vigano, A. A. L., et al. (2016) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12138 · Cited by 66
“The muscle transcriptome is altered in the presence of cancer cachexia.(33,34) In the present study, there was concordance between a proportion of the selected genes and”
BackgroundSelf-citationSMAD3 augments FoxO3-induced MuRF-1 promoter activity in a DNA-binding-dependent manner
Bollinger, L. M., Witczak, C. A., Houmard, J. A., & Brault, J. J. (2014) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00391.2013 · Cited by 67
Liu, Q., Xu, W., Luo, Y., Han, F., Yao, X., Yang, T., Zhang, Y., Pi, W., & Guo, X. (2011) · Journal of Cellular Biochemistry · doi:10.1002/jcb.23151 · Cited by 66
“Furthermore, USP-19 expression is negatively correlated with weight, muscle size, and MHC level and positively correlated with the length of CS exposure; these results suggest that USP-19 acts as a negative regulator in catabolic muscles similar to USP-14, a deubiquitinating enzyme associated with muscle atrophy [Leck…”
BackgroundHjorth, M., Norheim, F., Meen, A. J., Pourteymour, S., Lee-Ødegård, S., Holen, T., Jensen, J., Birkeland, K. I., Martinov, V. N., Langleite, T. M., et al. (2015) · Physiological Reports · doi:10.14814/phy2.12473 · Cited by 73
“…worth noting that most pathological conditions, insulin resistance, atrophy and aging in skeletal muscle are associated with alterations in the ECM (Lecker et al. 2004; Berria et al. 2006; Gillies and Lieber 2011; Kragstrup et al. 2011; Wood et al. 2014) and we suggest that exercise might…”
BackgroundRegulation of Muscle Growth in Early Postnatal Life in a Swine Model
Rudar, M., Fiorotto, M. L., & Davis, T. A. (2018) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-020518-115130 · Cited by 69
“The main muscle-specific Ub protein ligases atrogin-1 and muscle ring finger protein 1 (MuRF1) were first identified in rats (60) and were later recognized as key determinants of muscle atrophy in numerous catabolic states, including muscle unloading, nutrient deprivation, glucocorticoid administration, and sepsis (61…”
BackgroundReed, S. A., Senf, S. M., Cornwell, E. W., Kandarian, S. C., & Judge, S. M. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.01.059 · Cited by 62
“The mRNA expression of Foxo1 and Foxo3a is up-regulated in skeletal muscle during conditions of fasting, cancer cachexia, disuse and aging [2;11;12;13], and an increase in either Foxo1 or Foxo3a is alone sufficient to cause atrophy in normal skeletal muscle [3;14].”
BackgroundPKB signaling and atrogene expression in skeletal muscle of aged mice
Gaugler, M., Brown, A., Merrell, E., DiSanto‐Rose, M., Rathmacher, J. A., & Reynolds, T. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00175.2011 · Cited by 66
“Using real-time quantitative PCR, we assessed several mRNA transcripts to genes that have been shown to be increased following experimentally induced muscle atrophy (atrogenes) (4, 16, 25, 34).”
BackgroundMethodInfluentialKeller, J., Ringseis, R., Koc, A., Lukas, I., Kluge, H., & Eder, K. (2011) · animal · doi:10.1017/s1751731111001327 · Cited by 65
Neurofibromin (Nf1) is required for skeletal muscle development
Kossler, N., Stricker, S., Rödelsperger, C., Robinson, P. N., Kim, J., Dietrich, C., Osswald, M., Kühnisch, J., Stevenson, D. A., Braun, T. W., et al. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr149 · Cited by 64
“Additionally, in line with what was previously reported to be a common feature of several muscle dystrophies (19), Nf1-deficient muscles showed downregulation of multiple genes encoding key mitochondrial energy production and glucose metabolism regulating proteins (Supplementary Material, Table S3).”
BackgroundInfluentialInsulin-Like Growth Factor I: The Yin and Yang of Muscle Atrophy
Heszele, M. F. C., & Price, S. R. (2004) · Endocrinology · doi:10.1210/en.2004-1037 · Cited by 64
Self-citationEssex, A. L., Pin, F., Huot, J. R., Bonewald, L. F., Plotkin, L. I., & Bonetto, A. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00809 · Cited by 63
“Of note, the improvement inmusclemass andmuscle strength was also accompanied by a normalization of the levels of Atrogin-1, a ubiquitin ligase normally upregulated in conditions characterized by skeletal muscle atrophy (43), also suggesting that enhanced muscle hypercatabolism could play a role in cisplatin-induced m…”
BackgroundResultDiabetic sarcopenia: metabolic and molecular appraisal
Giha, H. A., Alamin, O. A. O., & Sater, M. S. (2022) · Acta Diabetologica · doi:10.1007/s00592-022-01883-2 · Cited by 66
“At gene level, there are different genes involved in muscle atrophy, collectively known as atrogenes [41].”
BackgroundTLR4 Activation Is Required for IL-17–Induced Multiple Tissue Inflammation and Wasting in Mice
Tang, H., Pang, S., Wang, M., Xiao, X., Rong, Y., Wang, H., & Zang, Y. Q. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0903664 · Cited by 63
“Moreover, the mRNA levels of two critical ubiquitin ligases, MuRF-1 and MAFbx, for which the expression is elevated in various muscle atrophy models (17), were increased in the gastrocnemius muscle of Ad–IL-17– infected mice from days 4–28 (Fig.”
BackgroundCleveland, B. M., & Evenhuis, J. P. (2010) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2010.06.010 · Cited by 64
“An increase in the capacity to polyubiquitinate proteins via increases in expression of ubiquitination machinery, namely the F-box protein atrogin-1/FBXO32, is largely responsible for faster rates of protein degradation associated with atrophy (Bodine et al., 2001; Lecker et al., 2004; Nakashima et al., 2005).”
BackgroundChen, Y., Cao, L., Ye, J., & Zhu, D. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.07.129 · Cited by 64
Zhao, T., Yan, Y., Liu, Y., & Hai‐Meng, Z. H. O. U. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m610363200 · Cited by 63
The cathepsin L gene is a direct target of FOXO1 in skeletal muscle
Yamazaki, Y., Kamei, Y., Sugita, S., Akaike, F., Kanai, S., Miura, S., Hirata, Y., Troen, B. R., Kitamura, T., Nishino, I., et al. (2010) · Biochemical Journal · doi:10.1042/bj20091346 · Cited by 63
Dumitru, A. V., Radu, B. M., Radu, M., & Creţoiu, S. M. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-981-13-1435-3_4 · Cited by 66
Buso, A., Comelli, M., Picco, R., Isola, M., Magnesa, B., Pišot, R., Rittweger, J., Salvadego, D., Šimunič, B., Grassi, B., et al. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00474 · Cited by 67
“atrophy in humans (Lecker et al., 2004) and their increased expression in muscle undergoing atrophy may be necessary to detoxify metals released by metal-containing compounds, such as myoglobin and mitochondrial cytochromes, during muscle protein degradation.”
BackgroundSerum amyloid A1 mediates myotube atrophy via Toll‐like receptors
Hahn, A., Kny, M., Pablo‐Tortola, C., Todiras, M., Willenbrock, M., Schmidt, S., Schmoeckel, K., Jorde, I., Nowak, M., Jarosch, E., et al. (2020) · Journal of Cachexia, Sarcopenia and Muscle · doi:10.1002/jcsm.12491 · Cited by 67
Cellular and molecular features of neurogenic skeletal muscle atrophy
Ehmsen, J. T., & Höke, A. (2020) · Experimental Neurology · doi:10.1016/j.expneurol.2020.113379 · Cited by 63
The Impact of Immune Cells on the Skeletal Muscle Microenvironment During Cancer Cachexia
VanderVeen, B. N., Murphy, E. A., & Carson, J. A. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.01037 · Cited by 61
Identification of the MuRF1 Skeletal Muscle Ubiquitylome Through Quantitative Proteomics
Baehr, L. M., Hughes, D. C., Lynch, S. A., Haver, D. V., Maia, T. M., Marshall, A. G., Radoshevich, L., Impens, F., Waddell, D. S., & Bodine, S. C. (2021) · Function · doi:10.1093/function/zqab029 · Cited by 63
Cleveland, B. M., Weber, G. M., Blemings, K. P., & Silverstein, J. T. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00272.2009 · Cited by 63
Musolino, V., Palus, S., Tschirner, A., Drescher, C., Gliozzi, M., Carresi, C., Vitale, C., Muscoli, C., Doehner, W., von Haehling, S., et al. (2016) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12116 · Cited by 62
“However, there is a general consensus that cancer cachexia is essentially because of a sustained proteolysis.(4)”
BackgroundVolodin, A., Kosti, I., Goldberg, A. L., & Cohen, S. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1612988114 · Cited by 62
“Recent biochemical studies of atrophying muscles have generally emphasized a single common mechanism that stimulates net protein degradation by the UPS throughout the process of atrophy (3, 8, 45, 46).”
BackgroundInfluentialSelf-citationFisher, A. G., Seaborne, R. A., Hughes, T. M., Gutteridge, A., Stewart, C., Coulson, J., Sharples, A., & Jarvis, J. (2017) · The FASEB Journal · doi:10.1096/fj.201700089rr · Cited by 54
Sarcopenia targeting with autophagy mechanism by exercise
Park, S. S., Seo, Y., & Kwon, K. (2019) · BMB Reports · doi:10.5483/bmbrep.2019.52.1.292 · Cited by 64
“LC3 is also overexpressed in muscle atrophy states, such as cachexia, diabetes, and fasting (6).”
BackgroundProteolytic Mechanisms, Not Malnutrition, Cause Loss of Muscle Mass in Kidney Failure
Mitch, W. E. (2006) · Journal of Renal Nutrition · doi:10.1053/j.jrn.2006.04.014 · Cited by 61
Self-citationGregorio, C. C., Perry, C. N., & McElhinny, A. (2006) · Journal of Muscle Research and Cell Motility · doi:10.1007/s10974-005-9021-x · Cited by 64
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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