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Identification of ubiquitin ligases required for skeletal muscle atrophy.
Open accessAbstract
Skeletal muscle adapts to decreases in activity and load by undergoing atrophy. To identify candidate molecular mediators of muscle atrophy, we performed transcript profiling. Although many genes were up-regulated in a single rat model of atrophy, only a small subset was universal in all atrophy models. Two of these genes encode ubiquitin ligases: Muscle RING Finger 1 ( MuRF1 ), and a gene we designate Muscle Atrophy F-box ( MAFbx ), the latter being a member of the SCF family of E3 ubiquitin ligases. Overexpression of MAFbx in myotubes produced atrophy, whereas mice deficient in either MAFbx or MuRF1 were found to be resistant to atrophy. These proteins are potential drug targets for the treatment of muscle atrophy.
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“The E3 ligase muscle RING‐finger protein‐1 (MuRF1), encoded by Trim63, and the F‐Box protein Atrogin‐1, encoded by Fbxo32, are key factors for ubiquitin‐proteasome system‐mediated protein degradation in muscle atrophy.”
From Sepsis induces interleukin 6, gp130/JAK2/STAT3, and muscle wasting (2022) · cites this paper as [7]
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In the citing paper
“A study examining MuRF1 and Atrogin1 gene expression in several models of muscle atrophy has also reported that their gene expression is up-regulated at different time points (Bodine et al., 2001).”
From Inducible Rpt3, a Proteasome Component, Knockout in Adult Skeletal Muscle Results in Muscle Atrophy (2020) · cites this paper as Bodine et al., 2001
In the citing paper
“MuRF1 knockout mice are not protected from denervation-induced muscle loss at 7 days and only partially protected (around 30%) at 14 days39. Moreover, the absence of MuRF1 does not protect from fasting or microgravity induced atrophy, while muscle mass is spared following glucocorticoid treatment43,44.”
From Mechanisms of muscle atrophy and hypertrophy: implications in health and disease (2021) · cites this paper as [39]
In the citing paper
“The first ubiquitin ligases that were identified to play a role in muscle loss were Atrogin-1/MAFbx and MuRF1. These two E3s are strongly upregulated in all the catabolic conditions so far tested in animals and are considered the master genes of muscle atrophy39.”
From Mechanisms of muscle atrophy and hypertrophy: implications in health and disease (2021) · cites this paper as [39]
In the citing paper
“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 [10]
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 [10]
In the citing paper
“Animal models that lack MURF-1 expression are protected from atrophy [71,72].”
From Omega-3 Fatty Acids and Skeletal Muscle Health (2015) · cites this paper as [71]
In the citing paper
“Mice deficient in either MAFbx or MuRF1 were demonstrated to be resistant to atrophy [7].”
From Nutraceuticals in the Prevention and Treatment of the Muscle Atrophy (2021) · cites this paper as [7]
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Citations
Cites
A simplified system for generating recombinant adenoviruses
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Bodine, S. C., Stitt, T. N., Gonzalez, M., Kline, W. O., Stover, G. L., Bauerlein, R., Zlotchenko, E., Scrimgeour, A., Lawrence, J. C., Glass, D. J., et al. (2001) · Nature Cell Biology · doi:10.1038/ncb1101-1014 · Cited by 2,752
Self-citationRommel, C., Bodine, S. C., Clarke, B. A., Rossman, R., Nunez, L., Stitt, T. N., Yancopoulos, G. D., & Glass, D. J. (2001) · Nature Cell Biology · doi:10.1038/ncb1101-1009 · Cited by 1,583
Self-citationJoazeiro, C. A. P., & Weissman, A. M. (2000) · Cell · doi:10.1016/s0092-8674(00)00077-5 · Cited by 1,249
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Kipreos, E. T., & Pagano, M. (2000) · Genome biology · doi:10.1186/gb-2000-1-5-reviews3002 · Cited by 753
Ubiquitination: RING for destruction?
Freemont, P. S. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00287-6 · Cited by 522
Centner, T., Yano, J., Kimura, E., McElhinny, A., Pelin, K., Witt, C. C., Bang, M., Trombitás, K., Granzier, H., Gregorio, C. C., et al. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.4448 · Cited by 402
What do we really know about the ubiquitin-proteasome pathway in muscle atrophy?
Jagoe, R. T., & Goldberg, A. L. (2001) · Current Opinion in Clinical Nutrition and Metabolic Care · doi:10.1097/00075197-200105000-00003 · Cited by 399
Identification of a family of human F-box proteins
Cenciarelli, C., Chiaur, D. S., Guardavaccaro, D., Parks, W. P., Vidal, M., & Pagano, M. (1999) · Current Biology · doi:10.1016/s0960-9822(00)80020-2 · Cited by 365
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Research works printed but not linked: 2
- Additional data and methods used in this study are described in the supplementary Web material available on Science Online at www.sciencemag.org/cgi/content/full/1065874/DC1. GenBank accession numbers are as follows: rat MAFbx ; human MAFbx ; and rat MuRF1 . For Northern methods and probe details ref. (2) of Web material. Knockouts were done with the proprietary Velocigene technology which allows for the rapid and high-throughput generation of custom gene mutations in mice (T. M. De Chiara W. T. Poueymirou D. M. Valenzuela G. D. Yancopoulos unpublished data).
- Bains W., Ponte P., Blau H. M., Kedes L., Mol. Cell. Biol. 4, 1449 (1984).
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Klionsky, D. J., Abdelmohsen, K., Abe, A., Abedin, M. J., Abeliovich, H., Acevedo Arozena, A., Adachi, H., Adams, C. M., Adams, P. D., Adeli, K., et al. (2016) · Autophagy · doi:10.1080/15548627.2015.1100356 · Cited by 5,894
The Ubiquitin-Proteasome Proteolytic Pathway: Destruction for the Sake of Construction
Glickman, M. H., & Ciechanover, A. J. (2002) · Physiological Reviews · doi:10.1152/physrev.00027.2001 · Cited by 4,296
Sandri, M., Sandri, C., Gilbert, A., Skurk, C., Calabria, E., Picard, A., Walsh, K., Schiaffino, S., Lecker, S. H., & Goldberg, A. L. (2004) · Cell · doi:10.1016/s0092-8674(04)00400-3 · Cited by 3,012
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Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition) 1
Klionsky, D. J., Abdel-Aziz, A. K., Abdelfatah, S., Abdellatif, M., Abdoli, A., Abel, S., Abeliovich, H., Abildgaard, M. H., Abudu, Y. P., Acevedo-Arozena, A., et al. (2021) · Autophagy · doi:10.1080/15548627.2020.1797280 · Cited by 2,897
Metadata
- Authors
- Bodine, S. C., Latres, E., Baumhueter, S., Lai, V. K.-M., Nunez, L., Clarke, B. A., Poueymirou, W. T., Panaro, F. J., Na, E., Dharmarajan, K., Pan, Z.-Q., Valenzuela, D. M., DeChiara, T. M., Stitt, T. N., Yancopoulos, G. D., & Glass, D. J.
- Affiliations
- Regeneron (United States) (US)
- Applied Biosystems, 850 Lincoln Center Drive, Foster City, CA 94404, USA.
- Regeneron Pharmaceuticals, 777 Old Saw Mill River Road, Tarrytown, NY, 10591–6707, USA.
- Icahn School of Medicine at Mount Sinai (US)
- Corresponding author
- Glass, David J.
- ORCID
- Venue
- Science
- Published
- 2001-11-23
- Volume
- 294
- Issue
- 5547
- Pages
- 1704-1708
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2167033587
- Cited by
- 3,521
- References
- 18
- Citations by year
- 2026: 124 · 2025: 133 · 2024: 141 · 2023: 139 · 2022: 157 · 2021: 151 · 2020: 202 · 2019: 175 · 2018: 180 · 2017: 175 · 2016: 175 · 2015: 178 · 2014: 182 · 2013: 190 · 2012: 173
- FWCI
- 15.71
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
- Keywords
- skeletal muscle atrophy, ubiquitin ligase, MuRF1, atrogin-1, SCF ubiquitin ligase, F-box protein, myotubes
- MeSH terms
- Amino Acid Sequence, Animals, Cloning, Molecular, Creatine Kinase, DNA-Binding Proteins, Humans, Immobilization, Isoenzymes, Molecular Sequence Data, Muscle Denervation, Muscle Proteins, Muscular Atrophy, Peptide Synthases, Phenotype, Protein Binding, RNA, Messenger, Trans-Activators, Up-Regulation, Rats, Sprague-Dawley, Gene Deletion, MyoD Protein, Myogenin, Mice, Knockout, Muscle, Skeletal, Hindlimb Suspension, Gene Expression Profiling, SKP Cullin F-Box Protein Ligases, Mice, Rats, Myogenic Regulatory Factor 5, Creatine Kinase, MM Form
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