Cited by 345Muscle Physiology and DisordersNutrition and Health in AgingAdipose Tissue and Metabolism

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mRNA Expression Signatures of Human Skeletal Muscle Atrophy Identify a Natural Compound that Increases Muscle Mass

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Kunkel, Steven D., Suneja, Manish, Ebert, Scott M., Bongers, Kale S., Fox, Daniel K., Malmberg, Sharon E., Alipour, Fariborz, Shields, Richard K., Adams, Christopher M.·2011·Cell Metabolism

DOI 10.1016/j.cmet.2011.03.020PMC PMC3120768

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Abstract

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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The Connectivity Map: Using Gene-Expression Signatures to Connect Small Molecules, Genes, and Disease
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.”
Influential
Identification 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).”
Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy.
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).”
Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo
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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).”
The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors.
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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).”
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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).”
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Increased Energy Expenditure, Decreased Adiposity, and Tissue-Specific Insulin Sensitivity in Protein-Tyrosine Phosphatase 1B-Deficient Mice
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×
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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).”

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“in the skeletal muscle, leading to Akt activation, muscle hypertrophy, and reduced adiposity and blood glucose normalization.(16) Another study has found that ursolic acid increases the Akt activity in the muscle of high-fat fed mice.”
The transcription regulator ATF4 is a mediator of skeletal muscle aging
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“…muscle atrophy and weakness [90–92], and ursolic acid and tomatidine, two small molecules that reduce age-related skeletal muscle atrophy and weakness in mouse models, also reduce ATF4-medi-ated gene expression in aged skeletal muscle, consistent with the phenotype of ATF4 mKO mice [11, 14, 15].”
MethodResult
l -Leucine Increases Skeletal Muscle IGF-1 but Does Not Differentially Increase Akt/mTORC1 Signaling and Serum IGF-1 Compared to Ursolic Acid in Response to Resistance Exercise in Resistance-Trained Men
Church, D. D., Schwarz, N. A., Spillane, M., McKinley-Barnard, S. K., Andre, T. L., Ramirez, A. J., & Willoughby, D. S. (2016) · Journal of the American College of Nutrition · doi:10.1080/07315724.2015.1132019 · Cited by 33
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BackgroundResultInfluential
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“UA treatment could improve subcutaneous mTOR expression in mice with severe SCI lesions, and improve the defects of body and subinjury muscle mass caused by SCI, which may be a potential therapeutic strategy to improve SCI muscle-specific pathological consequences (Kunkel et al., 2011; Bigford et al., 2018).”
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Background
gCMAP: user-friendly connectivity mapping with R
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“This strategy for establishing links between perturbations can then be used, for example, to identify bioactive compounds (Kunkel et al. , 2011; Stumpel et al. , 2012), elucidate their mode of action (Coombs et al. , 2012) or reposition approved pharmaceuticals for use in new indications (Dudley et…”
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Background
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“The effects of two small molecules on cellular messenger RNA (mRNA) expression negatively correlate with mRNA expression signatures of human muscle atrophy: ursolic acid (from the peels of apples and other fruit) and tomatidine (from unripe tomatoes).(8,9) These compounds can increase muscle mass and strength in anima…”
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BackgroundMethod
Mining the transcriptome for rare disease therapies: a comparison of the efficiencies of two data mining approaches and a targeted cell-based drug screen
Mears, A. J., Schock, S., Hadwen, J., Putos, S., Dyment, D. A., Boycott, K. M., & MacKenzie, A. (2017) · npj Genomic Medicine · doi:10.1038/s41525-017-0018-3 · Cited by 20
Use of mRNA expression signatures to discover small molecule inhibitors of skeletal muscle atrophy
Adams, C. M., Ebert, S. M., & Dyle, M. C. (2015) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000159 · Cited by 21
“This is supported by our findings that ursolic acid increases skeletal muscle Akt activity in vivo [4,19], and direct addition of ursolic acid to cultured skeletal myotubes rapidly stimulates Akt and one of its key downstream effectors, mTOR complex 1 (mTORC1) [4].”
BackgroundInfluential
The Signature of MicroRNA Dysregulation in Muscle Paralyzed by Spinal Cord Injury Includes Downregulation of MicroRNAs that Target Myostatin Signaling
De Gasperi, R., Graham, Z. A., Harlow, L. M., Bauman, W. A., Qin, W., & Cardozo, C. P. (2016) · PLOS ONE · doi:10.1371/journal.pone.0166189 · Cited by 19
An Integrative Transcriptome-Wide Analysis of Amyotrophic Lateral Sclerosis for the Identification of Potential Genetic Markers and Drug Candidates
Park, S., Kim, D., Song, J., & Joo, J. W. J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22063216 · Cited by 19
Aronia Upregulates Myogenic Differentiation and Augments Muscle Mass and Function Through Muscle Metabolism
Yun, C., So, H.-K., Vuong, T. A., Na, M. W., Anh, S., Lee, H.-K., Kim, K. H., Kang, J., Bae, G., & Lee, S.-J. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.753643 · Cited by 20
“The treatment with ursolic acid, one of the main components of aronia, increases muscle mass in mice through enhancing muscle insulin/IGFI signaling and inhibiting atrophy-associated muscle mRNA expression (52).”
Background
Synergistic effects of MFG-E8 and whey protein on mitigating d-galactose-induced sarcopenia through PI3K/AKT/PGC-1α and MAPK/ERK signaling pathways
Li, H., Guan, K., Wang, R., Zhu, A., & Ma, Y. (2023) · Journal of Dairy Science · doi:10.3168/jds.2023-23637 · Cited by 22
“…that regulates energy metabolism and cellular respiration, has been shown to be upregulated by activating the PI3K/Akt signaling pathway, further to alleviate sarcopenia through regulating skeletal muscle mitochondrial biogenesis and protein synthesis (Kunkel et al., 2011; Liu et al., 2019).”
Background
Monocyte-macrophage differentiation of acute myeloid leukemia cell lines by small molecules identified through interrogation of the Connectivity Map database
Manzotti, G., Parenti, S., Ferrari‐Amorotti, G., Soliera, A. R., Cattelani, S., Montanari, M., Cavalli, D., Ertel, A., Grande, A., & Calabretta, B. (2015) · Cell Cycle · doi:10.1080/15384101.2015.1033591 · Cited by 19
Effects of Vitamin D Use on Outcomes of Psychotic Symptoms in Alzheimer Disease Patients
Wang, L., Ying, J., Fan, P., Weamer, E. A., DeMichele‐Sweet, M. A. A., López, O. L., Kofler, J., & Sweet, R. A. (2019) · American Journal of Geriatric Psychiatry · doi:10.1016/j.jagp.2019.03.016 · Cited by 20
“For example, ursolic acid was identified as an inhibitor of fasting-induced muscle atrophy by gene-signature comparison(17).”
Background
Effect of Ursolic Acid on Insulin Resistance and Hyperinsulinemia in Rats with Diet-Induced Obesity: Role of Adipokines Expression
González-Garibay, A. S., López-Vázquez, A., Garcia-Bañuelos, J. J., Sánchez‐Enríquez, S., Sandoval-Rodriguez, A. S., del Toro‐Arreola, S., Bueno‐Topete, M. R., Muñóz-Valle, J. F., González-Hita, M. E., Domı́nguez-Rosales, J. A., et al. (2019) · Journal of Medicinal Food · doi:10.1089/jmf.2019.0154 · Cited by 20
“44,51,52 However, further studies could help to better understand UA participation in adipocytes maturation or hypertrophic processes.”
The use of gene arrays and corresponding connectivity mapping (Cmap) to identify novel anti‐ageing ingredients
Gillbro, J. M., Merinville, E., Olsson, M., Al‐Bader, T., Klack, A., Visdal‐Johnsen, L., & Mavon, A. (2015) · International Journal of Cosmetic Science · doi:10.1111/ics.12251 · Cited by 18
“Recently, agents have also been identified for drug development within Gaucher’s disease [3], pain management [10], muscle atrophy [11], inflammatory bowel disease [12], smoking cessation [13] and Alzheimer’s disease [14].”
Background
Natural constituents from food sources: potential therapeutic agents against muscle wasting
Shen, S., Yu, H., Gan, L., Yang, Y., & Lin, L. (2019) · Food & Function · doi:10.1039/c9fo00912d · Cited by 20
High-methionine diet in skeletal muscle remodeling: epigenetic mechanism of homocysteine-mediated growth retardation
Singh, M., George, A. K., Eyob, W., Homme, R. P., Stanišić, D., & Tyagi, S. C. (2020) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2020-0093 · Cited by 20
A novel oral nutritional supplement improves gait speed and mitochondrial functioning compared to standard care in older adults with (or at risk of) undernutrition: results from a randomized controlled trial
Grootswagers, P., Smeets, E. T. H. C., Oteng, A., & de Groot, C. P. G. M. (2021) · Aging · doi:10.18632/aging.202912 · Cited by 19
“vitamin D that previously was found to provide additional benefits [19, 20] and reinforced with UA that may affect muscle metabolism [17].”
BackgroundInfluential
Ursolic acid plays a protective role in obesity-induced cardiovascular diseases
Lin, Y.-T., Yu, Y.-M., Chang, W.-C., Chiang, S.-Y., Chan, H.-C., & Lee, M.-F. (2016) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2015-0407 · Cited by 17
“In addition, ursolic acid may increase energy reserves in muscles by enhancing glycogen storage and lean muscle mass through increased sensitivity to insulin and insulin-like growth factor 1 (Kunkel et al. 2011).”
Background
Maslinic acid activates mTORC1 and human TGR5 and induces skeletal muscle hypertrophy
Murata, S., Sasaki, T., Yamauchi, Y., Shimizu, M., & Sato, R. (2021) · Bioscience Biotechnology and Biochemistry · doi:10.1093/bbb/zbab151 · Cited by 22
IRF8 and its related molecules as potential diagnostic biomarkers or therapeutic candidates and immune cell infiltration characteristics in steroid-induced osteonecrosis of the femoral head
Liang, X., Liu, X., Li, S., Wen, M., Chen, Y.-R., Luo, D., Xu, B., Li, N., & Li, G. (2023) · Journal of Orthopaedic Surgery and Research · doi:10.1186/s13018-022-03381-1 · Cited by 17
“This strategy had successfully been applied for different types of diseases, such as cancer [20], muscle atrophy [21], acute myelogenous leukemia [22] and Parkinson’s disease [23].”
Method
Developing models for cachexia and their implications in drug discovery
Konishi, M., Ebner, N., von Haehling, S., Anker, S. D., & Springer, J. (2015) · Expert Opinion on Drug Discovery · doi:10.1517/17460441.2015.1041914 · Cited by 17
Gene expression profile-based drug screen identifies SAHA as a novel treatment for NAFLD
Cheng, Z., Wen, Y., Liang, B., Chen, S., Liu, Y., Wang, Z., Cheng, J., Tang, X., Xin, H., & Deng, L. (2019) · Molecular Omics · doi:10.1039/c8mo00214b · Cited by 17
Promotion of epithelial hyperplasia by interleukin‐8—CXCR axis in human prostate
Smith, D. K., Hasanali, S. L., Wang, J., Kallifatidis, G., Morera, D. S., Jordan, A. R., Terris, M. K., Klaassen, Z. W. A., Bollag, R. J., Lokeshwar, V. B., et al. (2020) · The Prostate · doi:10.1002/pros.24026 · Cited by 17
Ficus carica L. Attenuates Denervated Skeletal Muscle Atrophy via PPARα/NF-κB Pathway
Dai, J., Xiang, Y., Fu, D., Xu, L., Jiang, J., & Xu, J. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.580223 · Cited by 17
Ursolic acid ameliorates hypobaric hypoxia‐induced skeletal muscle protein loss via upregulating Akt pathway: An experimental study using rat model
Rathor, R., Agrawal, A., Kumar, R. S., Suryakumar, G., & Singh, S. N. (2020) · IUBMB Life · doi:10.1002/iub.2435 · Cited by 17
“To consider the severity of the above phenomenon, Kunkel et al.42 identified two mRNA regions, 63 mRNA and 29 mRNA, which were regulated by fasting in both human and mouse muscle and by both fasting and spinal cord injury in human muscle, respectively.”
Background
Effects of Antioxidant Activities in Ethanol Extract of Apple Peel, Grape Peel, and Sweet Potato Peel as Natural Antioxidant
Kim, M., 김영기, 김현순, Cheong, C., Jang, K., & 강순아 (2014) · Journal of the Korea Academia-Industrial cooperation Society · doi:10.5762/kais.2014.15.6.3766 · Cited by 17
“3769 이로 인한 항염증을 예방한다는 것이 보고되었고[6], 이 외에도 사과 껍질에 다량 존재하는 성분인 ursolic acid가 노화시에 나타나는 근위축증을 근육량을 증가시켜 주므 로써 완화시킨다는 연구보고[21]가 있어, 사과 껍질이 관 심의 대상이 되고 있다.”
Altered m6A RNA methylation governs denervation-induced muscle atrophy by regulating ubiquitin proteasome pathway
Sun, J., Zhou, H., Chen, Z., Zhang, H., Cao, Y., Yao, X., Chen, X., Liu, B., Gao, Z., Shen, Y., et al. (2023) · Journal of Translational Medicine · doi:10.1186/s12967-023-04694-3 · Cited by 16
LINCS dataset-based repositioning of rosiglitazone as a potential anti-human adenovirus drug
Wang, X., He, S., Zhou, Z., Bo, X., Qi, D., Fu, X., Wang, Z., Yang, J., & Wang, S. (2020) · Antiviral Research · doi:10.1016/j.antiviral.2020.104789 · Cited by 16
Natural Antioxidant Application on Fat Accumulation: Preclinical Evidence
Roy, P., Tomassoni, D., Traini, E., Martinelli, I., Bonaventura, M. V. M. D., Cifani, C., Amenta, F., & Tayebati, S. K. (2021) · Antioxidants · doi:10.3390/antiox10060858 · Cited by 18
“Furthermore, ursolic acid may increase energy reserves in muscles by enhancing glycogen storage and lean muscle mass through increased sensitivity to insulin and insulin-like growth factor 1 (IGF-1) [204].”
Background
Role for Plant-Derived Antioxidants in Attenuating Cancer Cachexia
Li, W., Swiderski, K., Murphy, K. T., & Lynch, G. S. (2022) · Antioxidants · doi:10.3390/antiox11020183 · Cited by 16
The vagal ganglia transcriptome identifies candidate therapeutics for airway hyperreactivity
Reznikov, L. R., Meyerholz, D. K., Alaiwa, M. H. A., Kuan, S., Liao, Y.-S. J., Bormann, N. L., Bair, T., Price, M. P., Stoltz, D. A., & Welsh, M. J. (2018) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00557.2017 · Cited by 16
A novel nutritional supplement prevents muscle loss and accelerates muscle mass recovery in caloric-restricted mice
van den Hoek, A. M., Zondag, G. C. M., Verschuren, L., de Ruiter, C., Attema, J., de Wit, E. C., Schwerk, A. M. K., Guigas, B., Lek, S., Rietman, A., et al. (2019) · Metabolism · doi:10.1016/j.metabol.2019.05.012 · Cited by 16
The Role of Nutrition in Attenuating Age-Related Skeletal Muscle Atrophy
Abiri, B., & Vafa, M. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-42667-5_12 · Cited by 14
Ursolic acid has no additional effect on muscle strength and mass in active men undergoing a high-protein diet and resistance training: A double-blind and placebo-controlled trial
Lobo, P. C. B., Vieira, I. P., Pichard, C., Marques, B. S., Gentil, P., da Silva, E. L., & Pimentel, G. D. (2020) · Clinical Nutrition · doi:10.1016/j.clnu.2020.06.004 · Cited by 16
Molecular targets of exercise mimetics and their natural activators
Jang, Y. J., & Byun, S. (2021) · BMB Reports · doi:10.5483/bmbrep.2021.54.12.151 · Cited by 17
Disturbance of the intestinal microbial community by ursolic acid contributes to its function as a regulator of fat deposition
Feng, Z., Wu, C., Zhou, J., Wu, F., Li, J., Li, T., & Yin, Y. (2015) · Journal of Functional Foods · doi:10.1016/j.jff.2015.02.015 · Cited by 15
Discovery of ursolic acid prodrug (NX-201): Pharmacokinetics and in vivo antitumor effects in PANC-1 pancreatic cancer
Yoon, Y., Lim, J. W., Kim, J., Kim, Y., & Chun, K. H. (2016) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2016.10.008 · Cited by 15
Korean mistletoe (Viscum album coloratum) extract regulates gene expression related to muscle atrophy and muscle hypertrophy
Jeong, J., Park, C.-H., Kim, I., Kim, Y.-H., Yoon, J.-M., Kim, K., & Kim, J. (2017) · BMC Complementary and Alternative Medicine · doi:10.1186/s12906-017-1575-9 · Cited by 15
“Discussion Previous reports regarding muscle atrophy and hypertrophy have shown that muscle atrophy induced by various kinds of mechanisms—such as fasting, illness (cancer and diabetes), and muscle disuse—all result in similar specific increases of mRNA expression [30, 31].”
Background
Effects of ursolic acid on muscle mass and bone microstructure in rats with casting-induced muscle atrophy
Kang, Y. S., Noh, E. B., & Kim, S. H. (2019) · Physical Activity and Nutrition · doi:10.20463/jenb.2019.0022 · Cited by 15
Genome-wide association study identifies 12 new genetic loci associated with growth traits in pigs
Zeng, M., Wang, B., Liu, L., Yang, Y., & Tang, Z. (2023) · Journal of Integrative Agriculture · doi:10.1016/j.jia.2023.02.040 · Cited by 14
Systematic computational strategies for identifying protein targets and lead discovery
Kataria, A., Srivastava, A., Singh, D. D., Haque, S., Han, I., & Yadav, D. K. (2024) · RSC Medicinal Chemistry · doi:10.1039/d4md00223g · Cited by 15
Leveraging 3D chemical similarity, target and phenotypic data in the identification of drug-protein and drug-adverse effect associations
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From drug repositioning to target repositioning: prediction of therapeutic targets using genetically perturbed transcriptomic signatures
Namba, S., Iwata, M., & Yamanishi, Y. (2022) · Bioinformatics · doi:10.1093/bioinformatics/btac240 · Cited by 14
Manipulation of Cell Physiology Enables Gene Silencing in Well-differentiated Airway Epithelia
Krishnamurthy, S., Behlke, M. A., Ramachandran, S. S., Salem, A. K., McCray, P. B., & Davidson, B. L. (2012) · Molecular Therapy — Nucleic Acids · doi:10.1038/mtna.2012.36 · Cited by 14
Computational Drug Repurposing for Neurodegenerative Diseases
Savva, K., Zachariou, M., Oulas, A., Minadakis, G., Sokratous, K., Dietis, N., & Spyrou, G. M. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-816125-8.00004-3 · Cited by 15
Comparing gene expression similarity metrics for connectivity map
Cheng, J., & Yang, L. (2013) · IEEE International Conference on Bioinformatics and Biomedicine (BIBM) · doi:10.1109/bibm.2013.6732481 · Cited by 13
“Although several hypotheses generated from CMAP have been validated experimentally [4-8], it is challenging to systematically evaluate the performance of drug-indication association of this technique due to lack of high quality gold standard data set and high quality disease gene expression signatures.”
Background
Limb-girdle Muscular Dystrophy and Therapy: Insights into Cell and Gene-based Approaches
Taheri, F., Taghizadeh, E., Pour, M. J. R., Rostami, D., Renani, P. G., Rastgar‐Moghadam, A., & Hayat, S. M. G. (2020) · Current Gene Therapy · doi:10.2174/1566523220666200218113526 · Cited by 13
Effects of Maca on Muscle Hypertrophy in C2C12 Skeletal Muscle Cells
Yi, D., Yoshikawa, M., Sugimoto, T., Tomoo, K., Okada, Y., & Hashimoto, T. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23126825 · Cited by 13
Ursolic acid directly promotes protein accretion in myotubes but does not affect myoblast proliferation
Figueiredo, V. C., & Nader, G. A. (2012) · Cell Biochemistry and Function · doi:10.1002/cbf.2821 · Cited by 13
“In whole animals, UA has been shown to prevent muscle atrophy and increase muscle mass and strength.(2) These observations make UA an interesting candidate for the treatment of muscle wasting conditions in humans.”
BackgroundResultInfluential
A novel oleanolic acid derivative HA-19 ameliorates muscle atrophy via promoting protein synthesis and preventing protein degradation
Cui, W., Liu, C., Zhang, Y., Shen, Q., Feng, Z., Wang, J., Lu, S.-F., Wu, J., & Li, J. (2019) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2019.114625 · Cited by 13
Drug perturbation gene set enrichment analysis (dpGSEA): a new transcriptomic drug screening approach
Fang, M., Richardson, B., Cameron, C., Dazard, J.-E., & Cameron, M. J. (2021) · BMC Bioinformatics · doi:10.1186/s12859-020-03929-0 · Cited by 14
Targeting Reactive Oxygen Species and Inflammation in Sepsis-Induced Liver Injury with Naturally Derived Superoxide Dismutase-Mimicking Carbon Dots
Zhong, C.-L., Song, N., Huang, P., Han, L., Zhang, J., Lu, Z., & Wang, L. (2025) · Biomaterials Research · doi:10.34133/bmr.0249 · Cited by 12
“This database can enable rapid comparisons of gene expression profiles to identify drugs closely associated with diseases while also enabling researchers to draw inferences regarding the mechanisms through which a given drug may function [ 27 ].”
Computational drug repurposing against SARS-CoV-2 reveals plasma membrane cholesterol depletion as key factor of antiviral drug activity
Barsi, S., Papp, H., Valdeolivas, A., Tóth, D. J., Kuczmog, A., Madai, M., Hunyady, L., Várnai, P., Sáez-Rodríguez, J., Jakab, F., et al. (2022) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1010021 · Cited by 12
“Despite its simplicity, it has been used successfully to identify repurposable drugs for different diseases from cancer [48,49] through inflammatory [50] to metabolic [51] diseases.”
Method

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: Suneja, Manish
Ebert, Scott M.
Bongers, Kale S.
Alipour, Fariborz
Shields, Richard K.
Adams, Christopher M.
Venue: Cell Metabolism
Publisher: Elsevier BV
Published: 2011-06
Volume: 13
Issue: 6
Pages: 627-638
ISSN: 1550-4131 (ISSN-L)
DOI: 10.1016/j.cmet.2011.03.020
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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mRNA Expression Signatures of Human Skeletal Muscle Atrophy Identify a Natural Compound that Increases Muscle Mass

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