The DOI matches its Crossref record; 35 of the 35 references it cites were found in a registry or an index.
mRNA Expression Signatures of Human Skeletal Muscle Atrophy Identify a Natural Compound that Increases Muscle Mass
Open accessAbstract
Skeletal muscle atrophy is a common and debilitating condition that lacks a pharmacologic therapy. To develop a potential therapy, we identified 63 mRNAs that were regulated by fasting in both human and mouse muscle, and 29 mRNAs that were regulated by both fasting and spinal cord injury in human muscle. We used these two unbiased mRNA expression signatures of muscle atrophy to query the Connectivity Map, which singled out ursolic acid as a compound whose signature was opposite to those of atrophy-inducing stresses. A natural compound enriched in apples, ursolic acid reduced muscle atrophy and stimulated muscle hypertrophy in mice. It did so by enhancing skeletal muscle insulin/IGF-I signaling and inhibiting atrophy-associated skeletal muscle mRNA expression. Importantly, ursolic acid's effects on muscle were accompanied by reductions in adiposity, fasting blood glucose, and plasma cholesterol and triglycerides. These findings identify a potential therapy for muscle atrophy and perhaps other metabolic diseases.
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“UA appeared to mediate its effects through enhancement of insulin/IGF-I signaling and a reduction in the expression of the atrophy-associated genes MuRF1 and MAFbx [187]”
From New strategies in sport nutrition to increase exercise performance (2016) · cites this paper as [187]
In the citing paper
“Therefore, it is presently unclear whether UA supplementation in humans can reproduce the anti-atrophy or pro-hypertrophic data reported previously [187].”
From New strategies in sport nutrition to increase exercise performance (2016) · cites this paper as [187]
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“whilst 5 weeks of supplemented diet (0.27% UA) induced hypertrophy [187].”
From New strategies in sport nutrition to increase exercise performance (2016) · cites this paper as [187]
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“UA supplementation in mice (200 mg / kg via i.p. injection twice daily for 7 days) reduced muscle atrophy following denervation”
From New strategies in sport nutrition to increase exercise performance (2016) · cites this paper as [187]
In the citing paper
“Ursolic acid, a pentacyclic triterpenoid abundant in apples, reduces fasting- and denervation-induced muscle atrophy by inhibiting the mRNA expression of MAFbx and MuRF1 and induces skeletal muscle hypertrophy in SD rats [145].”
From Nutraceuticals in the Prevention and Treatment of the Muscle Atrophy (2021) · cites this paper as [145]
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Citations
Cites
Lamb, J., Crawford, E. D., Peck, D., Modell, J. W., Blat, I. C., Wrobel, M. J., Lerner, J., Brunet, J.-P., Subramanian, A., Ross, K. N., et al. (2006) · Science · doi:10.1126/science.1132939 · Cited by 5,257 · cited 3×
“The connectivity score, represented on the y axis, is a measure of the strength of the correlation (Lamb et al., 2006). p < 0.004 for all compounds shown.”
InfluentialIdentification of ubiquitin ligases required for skeletal muscle atrophy.
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., et al. (2001) · Science · doi:10.1126/science.1065874 · Cited by 3,521 · cited 3×
“Previous studies demonstrated that skeletal muscle atrophy is driven by conserved changes in skeletal muscle gene expression (Bodine et al., 2001a; Sandri et al., 2004).”
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 · cited 2×
“Previous studies demonstrated that skeletal muscle atrophy is driven by conserved changes in skeletal muscle gene expression (Bodine et al., 2001a; Sandri et al., 2004).”
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“Previous studies demonstrated that skeletal muscle atrophy is driven by conserved changes in skeletal muscle gene expression (Bodine et al., 2001a; Sandri et al., 2004).”
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“We next examined whether ursolic acid might increase Akt activation in C2C12 skeletal myotubes, awell-established in vitro model of skeletal muscle (Sandri et al., 2004; Stitt et al., 2004).”
Pharmacology of oleanolic acid and ursolic acid
Liu, J. (1995) · Journal of Ethnopharmacology · doi:10.1016/0378-8741(95)90032-2 · Cited by 1,431 · cited 1×
“Interestingly, because it exerts beneficial effects in animal models of diabetes and hyperlipidemia (Liu, 1995; Wang et al., 2009), ursolic acid is thought to be the active component in a variety of folkloric antidiabetic herbal medicines (Liu, 1995, 2005).”
Normal growth and development in the absence of hepatic insulin-like growth factor I
Yakar, S., Liu, J., STANNARD, B. S., Butler, A. A., Accili, D., Sauer, B., & LeRoith, D. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.13.7324 · Cited by 1,418 · cited 1×
“We also measured the effect of ursolic acid on plasma IGF-I levels, which primarily reflect growth hormone-mediated hepatic IGF-I production (Yakar et al., 1999).”
Klaman, L. D., Boss, O., Peroni, O. D., Kim, J. K., Martino, J. L., Zabolotny, J. M., Moghal, N., Lubkin, M., Kim, Y.-B., Sharpe, A. H., et al. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.15.5479-5489.2000 · Cited by 1,235 · cited 1×
“However, neither global nor muscle-specific PTP1B knockout mice were found to possess increased muscle mass (Delibegovic et al., 2007; Klaman et al., 2000).”
Musarò, A., McCullagh, K., Paul, A., Houghton, L., Dobrowolny, G., Molinaro, M., Barton, E. R., L Sweeney, H., & Rosenthal, N. (2001) · Nature Genetics · doi:10.1038/84839 · Cited by 1,137 · cited 2×
“, 2005) and stimulatesmuscle hypertrophy (Barton-Davis et al., 1998; Musaro et al., 2001).”
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“Of these, PGC-1a mRNA encodes a protein that inhibits atrophy-associated gene expression and skeletal muscle atrophy in mice (Sandri et al., 2006).”
Reversal of Cancer Cachexia and Muscle Wasting by ActRIIB Antagonism Leads to Prolonged Survival
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“It may be useful as a monotherapy or in combination with other strategies that have been considered, such as myostatin inhibition (Zhou et al., 2010).”
REGULATION OF MUSCLE MASS BY MYOSTATIN
Lee, S.-J. (2004) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.20.012103.135836 · Cited by 819 · cited 1×
“However, ursolic acid did not alter levels of mRNAs encoding myostatin (which reduces muscle mass [Lee, 2004]), or twist or myogenin (which are induced by IGF-I during development [Dupont et al., 2001; Tureckova et al., 2001]).”
Oleanolic acid and ursolic acid: Research perspectives
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“Interestingly, because it exerts beneficial effects in animal models of diabetes and hyperlipidemia (Liu, 1995; Wang et al., 2009), ursolic acid is thought to be the active component in a variety of folkloric antidiabetic herbal medicines (Liu, 1995, 2005).”
Barton-Davis, E. R., Shoturma, D. I., Musarò, A., Rosenthal, N. A., & Sweeney, H. L. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.26.15603 · Cited by 700 · cited 1×
“In addition, increased skeletal muscle IGF1 expression reduces denervation-induced muscle atrophy (Shavlakadze et al., 2005) and stimulates muscle hypertrophy (Barton-Davis et al., 1998; Musaro et al., 2001).”
Sacheck, J. M., Ohtsuka, A., McLary, S. C., & Goldberg, A. L. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00073.2004 · Cited by 606 · cited 4×
“…signaling, IGF-I represses atrogin-1 and MuRF1 mRNAs (Frost et al., 2009; Sacheck et al., 2004) as well as DDIT4L mRNA (Frost et al., 2009; Sacheck et al., 2004), which, after atrogin-1 mRNA, was the second most highly repressed mRNA in muscle from ursolic acid-treated mice (Figure 5A).”
InfluentialSacheck, J. M., Hyatt, J. K., Raffaello, A., Thomas Jagoe, R., Roy, R. R., Reggie Edgerton, V., Lecker, S. H., & Goldberg, A. L. (2007) · The FASEB Journal · doi:10.1096/fj.06-6604com · Cited by 585 · cited 2×
“As discussed above, atrogin-1 and MuRF1 are transcriptionally upregulated by atrophy-inducing stresses (Sacheck et al., 2007; and Figure 1B), and they are required for muscle atrophy (Bodine et al., 2001a).”
Conditional Activation of Akt in Adult Skeletal Muscle Induces Rapid Hypertrophy
Lai, K.-M. V., Gonzalez, M., Poueymirou, W. T., Kline, W. O., Na, E., Zlotchenko, E., Stitt, T. N., Economides, A. N., Yancopoulos, G. D., & Glass, D. J. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.21.9295-9304.2004 · Cited by 442 · cited 4×
“Because ursolic acid increasedAkt activity (Figure 5), and because muscle-specific increases in Akt activity reduce adiposity as a secondary consequence of muscle hypertrophy (Izumiya et al., 2008; Lai et al., 2004), we hypothesized that ursolic acid-treated mice might contain less fat.”
InfluentialKenner, K. A., Anyanwu, E., Olefsky, J. M., & Kusari, J. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.33.19810 · Cited by 435 · cited 2×
“, 2006), a tyrosine phosphatase that dephosphorylates (inactivates) the IGF-I and insulin receptors (Kenner et al., 1996).”
Fast/Glycolytic Muscle Fiber Growth Reduces Fat Mass and Improves Metabolic Parameters in Obese Mice
Izumiya, Y., Hopkins, T., Morris, C., Sato, K., Zeng, L., Viereck, J., Hamilton, J. A., Ouchi, N., LeBrasseur, N. K., & Walsh, K. (2008) · Cell Metabolism · doi:10.1016/j.cmet.2007.11.003 · Cited by 395 · cited 4×
“Because ursolic acid increasedAkt activity (Figure 5), and because muscle-specific increases in Akt activity reduce adiposity as a secondary consequence of muscle hypertrophy (Izumiya et al., 2008; Lai et al., 2004), we hypothesized that ursolic acid-treated mice might contain less fat.”
InfluentialAdams, G. R., & Haddad, F. (1996) · Journal of Applied Physiology · doi:10.1152/jappl.1996.81.6.2509 · Cited by 287 · cited 1×
“IGF1 mRNA is known to be transcriptionally induced in hypertrophic muscle (Adams and Haddad, 1996; Gentile et al., 2010; Hameed et al., 2004).”
Zhang, W., Hong, D., Zhou, Y., Zhang, Y., Shen, Q., Li, J., Hu, L., & Li, J. (2006) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2006.05.009 · Cited by 266 · cited 4×
“The latter possibility is supported by previous in vitro data showing that ursolic acid directly inhibits PTP1B (Zhang et al., 2006), a tyrosine phosphatase that dephosphorylates (inactivates) the IGF-I and insulin receptors (Kenner et al.”
InfluentialTime course of changes in markers of myogenesis in overloaded rat skeletal muscles
Adams, G. R., Haddad, F., & Baldwin, K. M. (1999) · Journal of Applied Physiology · doi:10.1152/jappl.1999.87.5.1705 · Cited by 218 · cited 3×
“Although muscle-specific IGF1 induction is characteristic of, and contributes to, muscle hypertrophy, it may be a relatively late event that promotes hypertrophy after it has been initiated by other stimuli (Adams et al., 1999).”
InfluentialHameed, M., Lange, K. H. W., Andersen, J. L., Schjerling, P., Kjær, M., Harridge, S. D. R., & Goldspink, G. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.051722 · Cited by 197 · cited 1×
“IGF1 mRNA is known to be transcriptionally induced in hypertrophic muscle (Adams and Haddad, 1996; Gentile et al., 2010; Hameed et al., 2004).”
Insulin-like Growth Factor-mediated Muscle Differentiation
Turečková, J., Wilson, E. M., Cappalonga, J. L., & Rotwein, P. S. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104991200 · Cited by 178 · cited 2×
“However, ursolic acid did not alter levels of mRNAs encoding myostatin (which reduces muscle mass (Lee, 2004)), or twist or myogenin (which are induced by IGF-I during development (Dupont et al., 2001; Tureckova et al., 2001)).”
Delibegović, M., Bence, K. K., Mody, N., Hong, E., Ko, H. J., Kim, J. K., Kahn, B. B., & Neel, B. G. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00959-07 · Cited by 173 · cited 1×
“However, neither global nor muscle-specific PTP1B knockout mice were found to possess increased muscle mass (Delibegovic et al., 2007; Klaman et al., 2000).”
A novel ubiquitin‐binding protein ZNF216 functioning in muscle atrophy
Hishiya, A., Iemura, S., Natsume, T., Takayama, S.-I. J., Ikeda, K., & Watanabe, K. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7600945 · Cited by 142 · cited 1×
“Of these, atrogin-1, MuRF1, and ZFAND5 mRNAs encode proteins known to be required for skeletal muscle atrophy in mice (Bodine et al., 2001a; Hishiya et al., 2006).”
Jung, S. H., Ha, Y. J., Shim, E. K., Choi, S. Y., Jin, J., Yun‐Choi, H. S., & Lee, J. R. (2007) · Biochemical Journal · doi:10.1042/bj20061123 · Cited by 135 · cited 1×
“In a previous study of nonmuscle cell lines (CHO/IR and 3T3-L1 cells), ursolic acid enhanced insulin-mediated Akt activation (Jung et al., 2007).”
The Transcription Factor ATF4 Promotes Skeletal Myofiber Atrophy during Fasting
Ebert, S. M., Monteys, A. M., Fox, D. K., Bongers, K. S., Shields, B. E., Malmberg, S. E., Davidson, B. L., Suneja, M., & Adams, C. M. (2010) · Molecular Endocrinology · doi:10.1210/me.2009-0345 · Cited by 130 · cited 3×
“muscle, and the effects of spinal cord injury on human skeletal muscle were described previously (Adams et al., 2011; Ebert et al., 2010).”
Self-citationIsolation of ursolic acid from apple peels by high speed counter-current chromatography
Frighetto, R. T. S., Welendorf, R. M., Nigro, E. N., Frighetto, N., & Siani, A. C. (2007) · Food Chemistry · doi:10.1016/j.foodchem.2007.06.003 · Cited by 128 · cited 1×
“A water-insoluble pentacyclic triterpenoid, ursolic acid is the major waxy component in apple peels (Frighetto et al., 2008).”
Anti-glycative effects of oleanolic acid and ursolic acid in kidney of diabetic mice
Wang, Z., Hsu, C., Huang, C., & Yin, M. (2009) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2009.11.019 · Cited by 126 · cited 1×
“Interestingly, because it exerts beneficial effects in animal models of diabetes and hyperlipidemia (Liu, 1995; Wang et al., 2009), ursolic acid is thought to be the active component in a variety of folkloric antidiabetic herbal medicines (Liu, 1995, 2005).”
Dupont, J., Fernandez, A. M., Glackin, C. A., Helman, L. J., & LeRoith, D. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m102664200 · Cited by 107 · cited 1×
“However, ursolic acid did not alter levels of mRNAs encoding myostatin (which reduces muscle mass [Lee, 2004]), or twist or myogenin (which are induced by IGF-I during development [Dupont et al., 2001; Tureckova et al., 2001]).”
Gentile, M. A., Nantermet, P. V., Vogel, R. L., Phillips, R., Holder, D., Hodor, P. G., Cheng, C., Dai, H. A., Freedman, L. P., & Ray, W. J. (2009) · Journal of Molecular Endocrinology · doi:10.1677/jme-09-0048 · Cited by 75 · cited 1×
“IGF1 mRNA is known to be transcriptionally induced in hypertrophic muscle (Adams and Haddad, 1996; Gentile et al., 2010; Hameed et al., 2004).”
Insulin-like growth factor I slows the rate of denervation induced skeletal muscle atrophy
Shavlakadze, T., White, J. D., Davies, M. J., Hoh, J. F. Y., & Grounds, M. D. (2005) · Neuromuscular Disorders · doi:10.1016/j.nmd.2004.10.013 · Cited by 51 · cited 2×
“In addition, increased skeletal muscle IGF1 expression reduces denervation-induced muscle atrophy (Shavlakadze et al., 2005) and stimulatesmuscle hypertrophy (Barton-Davis et al.”
Adams, C. M., Suneja, M., Dudley‐Javoroski, S., & Shields, R. K. (2010) · Muscle & Nerve · doi:10.1002/mus.21831 · Cited by 46 · cited 3×
“Our study protocol of humans with SCI was described previously (Adams et al., 2011).”
Regulation of REDD1 by insulin‐like growth factor‐I in skeletal muscle and myotubes
Frost, R. A., Huber, D. S., Pruznak, A. M., & Lang, C. H. (2009) · Journal of Cellular Biochemistry · doi:10.1002/jcb.22349 · Cited by 42 · cited 4×
“Moreover, by stimulating skeletal muscle insulin/IGF-I signaling, IGF-I represses atrogin-1 and MuRF1 mRNAs (Frost et al., 2009; Sacheck et al., 2004) as well as DDIT4L mRNA (Frost et al., 2009; Sacheck et al., 2004), which, after atrogin-1 mRNA, was the second most highly repressed mRNA in muscle…”
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Metadata
- Authors
- Kunkel, S. D., Suneja, M., Ebert, S. M., Bongers, K. S., Fox, D. K., Malmberg, S. E., Alipour, F., Shields, R. K., & Adams, C. M.
- Affiliations
- University of Iowa (US)
- Corresponding author
- Adams, Christopher M.
- ORCID
- Venue
- Cell Metabolism
- Publisher
- Elsevier BV
- Published
- 2011-06
- Volume
- 13
- Issue
- 6
- Pages
- 627-638
- ISSN
- 1550-4131 (ISSN-L)
- PMC
- PMC3120768
- OpenAlex
- W2099582158
- Cited by
- 345
- References
- 35
- Citations by year
- 2026: 15 · 2025: 17 · 2024: 18 · 2023: 22 · 2022: 23 · 2021: 36 · 2020: 24 · 2019: 35 · 2018: 26 · 2017: 24 · 2016: 25 · 2015: 27 · 2014: 16 · 2013: 19 · 2012: 16
- FWCI
- 6.71
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 777 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- American Diabetes Association (1R01AR059115-01)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases
- U.S. Department of Veterans Affairs
- Doris Duke Charitable Foundation
- Institute of Clinical and Translational Sciences
- National Institutes of Health (HL007121, T32 GM073610)
- University of Georgia Research Foundation
- 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 › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Keywords
- skeletal muscle atrophy, ursolic acid, muscle hypertrophy, fasting, spinal cord injury, mRNA expression signature, adiposity, metabolic disorders, natural compounds, apple
- MeSH terms
- Ursolic Acid, Animals, Cell Line, Fasting, Gene Expression Regulation, Hindlimb, Humans, Insulin, Insulin-Like Growth Factor I, Mice, Inbred C57BL, Muscle Denervation, Muscular Atrophy, Triterpenes, Signal Transduction, Gene Expression, Muscle, Skeletal, Muscle Fibers, Skeletal, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Mice, Muscle Strength
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