The Promotion of Migration and Myogenic Differentiation in Skeletal Muscle Cells by Quercetin and Underlying Mechanisms
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cell Line and Reagents
2.2. Cell Differentiation and Migration
2.3. Cell Viability Assay (MTT Assay)
2.4. Immunofluorescence Staining and Morphology Analysis
2.5. Myoblast Cell Analysis and Flow Cytometry
2.6. Wound-Healing Assay
2.7. Transwell Migration Assay
2.8. AKT Inhibitor Treatments
2.9. Western Blot Analysis
2.10. Statistical Analysis
3. Results
3.1. Cytotoxicity of Quercetin in C2C12 Cells
3.2. Quercetin Significantly Promoted Myoblast Fusion and Myogenic Differentiation
3.3. Quercetin Did Not Affect the Exit of Myoblasts’ Cell Cycle at the Early Stage of Differentiation
3.4. Quercetin Significantly Enhanced Myoblast Migration
3.5. Quercetin Induced the Phosphorylation of AMPK
3.6. Quercetin Inhibited the Phosphorylation of PDGFR-β
3.7. Quercetin Induced Early Upregulation of IGF-1R, Promoted Myogenic Differentiation, and Protein Synthesis via Downstream of the IGF-1R Signaling Pathway
3.8. AKT Activation Is Required for Induction of Myogenic Differentiation by Quercetin
3.9. Quercetin Regulated Myoblast Migration through the ITGB1 Signaling Pathway
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Larsson, L.; Degens, H.; Li, M.; Salviati, L.; Lee, Y.I.; Thompson, W.; Kirkland, J.L.; Sandri, M. Sarcopenia: Aging-Related Loss of Muscle Mass and Function. Physiol. Rev. 2019, 99, 427–511. [Google Scholar] [CrossRef] [PubMed]
- Dumont, N.A.; Bentzinger, C.F.; Sincennes, M.C.; Rudnicki, M.A. Satellite Cells and Skeletal Muscle Regeneration. Compr. Physiol. 2015, 5, 1027–1059. [Google Scholar] [PubMed]
- Liu, X.; Gao, Y.; Long, X.; Hayashi, T.; Mizuno, K.; Hattori, S.; Fujisaki, H.; Ogura, T.; Wang, D.O.; Ikejima, T. Type I collagen promotes the migration and myogenic differentiation of C2C12 myoblasts via the release of interleukin-6 mediated by FAK/NF-kappaB p65 activation. Food Funct. 2020, 11, 328–338. [Google Scholar] [CrossRef] [PubMed]
- Jang, Y.N.; Baik, E.J. JAK-STAT pathway and myogenic differentiation. Jak-Stat 2013, 2, e23282. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boonen, K.J.; Post, M.J. The muscle stem cell niche: Regulation of satellite cells during regeneration. Tissue Eng. Part B Rev. 2008, 14, 419–431. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Geiger, B.; Spatz, J.P.; Bershadsky, A.D. Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 2009, 10, 21–33. [Google Scholar] [CrossRef] [PubMed]
- Grzelkowska-Kowalczyk, K. The Importance of Extracellular Matrix in Skeletal Muscle Development and Function. In Composition and Function of the Extracellular Matrix in the Human Body; Intech: London, UK, 2016. [Google Scholar]
- Lopez-Colome, A.M.; Lee-Rivera, I.; Benavides-Hidalgo, R.; Lopez, E. Paxillin: A crossroad in pathological cell migration. J. Hematol. Oncol. 2017, 10, 50. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, Y.; Liu, S.; Yan, Y.; Li, S.; Tong, H. SPARCL1 Influences Bovine Skeletal Muscle-Derived Satellite Cell Migration and Differentiation through an ITGB1-Mediated Signaling Pathway. Animals 2020, 10, 1361. [Google Scholar] [CrossRef]
- Contreras, O.; Cordova-Casanova, A.; Brandan, E. PDGF-PDGFR network differentially regulates the fate, migration, proliferation, and cell cycle progression of myogenic cells. Cell Signal. 2021, 84, 110036. [Google Scholar] [CrossRef] [PubMed]
- Guerit, E.; Arts, F.; Dachy, G.; Boulouadnine, B.; Demoulin, J.B. PDGF receptor mutations in human diseases. Cell. Mol. Life Sci. 2021, 78, 3867–3881. [Google Scholar] [CrossRef]
- Sugg, K.B.; Korn, M.A.; Sarver, D.C.; Markworth, J.F.; Mendias, C.L. Inhibition of platelet-derived growth factor signaling prevents muscle fiber growth during skeletal muscle hypertrophy. FEBS Lett. 2017, 591, 801–809. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Husmann, I.; Soulet, L.; Gautron, J.; Martelly, I.; Barritault, D. Growth factors in skeletal muscle regeneration. Cytokine Growth Factor Rev. 1996, 7, 249–258. [Google Scholar] [CrossRef]
- Coleman, M.E.; DeMayo, F.; Yin, K.C.; Lee, H.M.; Geske, R.; Montgomery, C.; Schwartz, R.J. Myogenic vector expression of insulin-like growth factor I stimulates muscle cell differentiation and myofiber hypertrophy in transgenic mice. J. Biol. Chem. 1995, 270, 12109–12116. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shen, X.; Tang, J.; Jiang, R.; Wang, X.; Yang, Z.; Huang, Y.; Lan, X.; Lei, C.; Chen, H. CircRILPL1 promotes muscle proliferation and differentiation via binding miR-145 to activate IGF1R/PI3K/AKT pathway. Cell Death Dis. 2021, 12, 142. [Google Scholar] [CrossRef] [PubMed]
- Zong, C.S.; Chan, J.; Levy, D.E.; Horvath, C.; Sadowski, H.B.; Wang, L.H. Mechanism of STAT3 activation by insulin-like growth factor I receptor. J. Biol. Chem. 2000, 275, 15099–15105. [Google Scholar] [CrossRef] [Green Version]
- Liu, X.; Wang, Y.; Zhao, S.; Li, X. Fibroblast Growth Factor 21 Promotes C2C12 Cells Myogenic Differentiation by Enhancing Cell Cycle Exit. Biomed. Res. Int. 2017, 2017, 1648715. [Google Scholar] [CrossRef] [Green Version]
- Vilchinskaya, N.A.; Krivoi, I.I.; Shenkman, B.S. AMP-Activated Protein Kinase as a Key Trigger for the Disuse-Induced Skeletal Muscle Remodeling. Int. J. Mol. Sci. 2018, 19, 3558. [Google Scholar] [CrossRef] [Green Version]
- Su, R.; Wang, B.; Zhang, M.; Luo, Y.; Wang, D.; Zhao, L.; Su, L.; Duan, Y.; Faucitano, L.; Jin, Y. Effects of energy supplements on the differentiation of skeletal muscle satellite cells. Food Sci. Nutr. 2021, 9, 357–366. [Google Scholar] [CrossRef]
- Li, Y.; Yao, J.; Han, C.; Yang, J.; Chaudhry, M.T.; Wang, S.; Liu, H.; Yin, Y. Quercetin, Inflammation and Immunity. Nutrients 2016, 8, 167. [Google Scholar] [CrossRef] [Green Version]
- Wang, L.; Xu, Z.; Ling, D.; Li, J.; Wang, Y.; Shan, T. The regulatory role of dietary factors in skeletal muscle development, regeneration and function. Crit. Rev. Food Sci. Nutr. 2022, 62, 764–782. [Google Scholar] [CrossRef]
- Le, N.H.; Kim, C.S.; Park, T.; Park, J.H.; Sung, M.K.; Lee, D.G.; Hong, S.M.; Choe, S.Y.; Goto, T.; Kawada, T.; et al. Quercetin protects against obesity-induced skeletal muscle inflammation and atrophy. Mediat. Inflamm. 2014, 2014, 834294. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vadlakonda, L.; Dash, A.; Pasupuleti, M.; Anil Kumar, K.; Reddanna, P. The Paradox of Akt-mTOR Interactions. Front. Oncol. 2013, 3, 165. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Figueiredo, V.C.; Markworth, J.F.; Cameron-Smith, D. Considerations on mTOR regulation at serine 2448: Implications for muscle metabolism studies. Cell. Mol. Life Sci. 2017, 74, 2537–2545. [Google Scholar] [CrossRef] [PubMed]
- Qu, Z.; Liu, C.; Li, P.; Xiong, W.; Zeng, Z.; Liu, A.; Xiao, W.; Huang, J.; Liu, Z.; Zhang, S. Theaflavin Promotes Myogenic Differentiation by Regulating the Cell Cycle and Surface Mechanical Properties of C2C12 Cells. J. Agric. Food Chem. 2020, 68, 9978–9992. [Google Scholar] [CrossRef] [PubMed]
- Louie, G.H.; Ward, M.M. Sex disparities in self-reported physical functioning: True differences, reporting bias, or incomplete adjustment for confounding? J. Am. Geriatr. Soc. 2010, 58, 1117–1122. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Franco, I.; Johansson, A.; Olsson, K.; Vrtacnik, P.; Lundin, P.; Helgadottir, H.T.; Larsson, M.; Revechon, G.; Bosia, C.; Pagnani, A.; et al. Somatic mutagenesis in satellite cells associates with human skeletal muscle aging. Nat. Commun. 2018, 9, 800. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Blau, H.M.; Cosgrove, B.D.; Ho, A.T. The central role of muscle stem cells in regenerative failure with aging. Nat. Med. 2015, 21, 854–862. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hollinger, K.; Shanely, R.A.; Quindry, J.C.; Selsby, J.T. Long-term quercetin dietary enrichment decreases muscle injury in mdx mice. Clin. Nutr. 2015, 34, 515–522. [Google Scholar] [CrossRef]
- Rather, R.A.; Bhagat, M. Quercetin as an innovative therapeutic tool for cancer chemoprevention: Molecular mechanisms and implications in human health. Cancer Med. 2020, 9, 9181–9192. [Google Scholar] [CrossRef]
- Garcia, L.A.; King, K.K.; Ferrini, M.G.; Norris, K.C.; Artaza, J.N. 1,25(OH)2vitamin D3 stimulates myogenic differentiation by inhibiting cell proliferation and modulating the expression of promyogenic growth factors and myostatin in C2C12 skeletal muscle cells. Endocrinology 2011, 152, 2976–2986. [Google Scholar] [CrossRef]
- Louis, M.; Zanou, N.; Van Schoor, M.; Gailly, P. TRPC1 regulates skeletal myoblast migration and differentiation. J. Cell Sci. 2008, 121, 3951–3959. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pang, Y.; Zhang, Z.; Wang, Z.; Wang, Y.; Yan, Y.; Li, S.; Tong, H. Platelet endothelial aggregation receptor-1 regulates bovine muscle satellite cell migration and differentiation via integrin beta-1 and focal adhesion kinase. Cell Adhes. Migr. 2019, 13, 192–202. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jorgensen, S.B.; Richter, E.A.; Wojtaszewski, J.F. Role of AMPK in skeletal muscle metabolic regulation and adaptation in relation to exercise. J. Physiol. 2006, 574, 17–31. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.; Liang, D.; Huang, Z.; Jia, G.; Zhao, H.; Liu, G. Quercetin regulates skeletal muscle fiber type switching via adiponectin signaling. Food Funct. 2021, 12, 2693–2702. [Google Scholar] [CrossRef] [PubMed]
- Wu, C.N.; Tien, K.J. The Impact of Antidiabetic Agents on Sarcopenia in Type 2 Diabetes: A Literature Review. J. Diabetes Res. 2020, 2020, 9368583. [Google Scholar] [CrossRef]
- Fiaschi, T.; Chiarugi, P.; Buricchi, F.; Giannoni, E.; Taddei, M.L.; Magnelli, L.; Cozzi, G.; Raugei, G.; Ramponi, G. Down-regulation of platelet-derived growth factor receptor signaling during myogenesis. Cell. Mol. Life Sci. 2003, 60, 2721–2735. [Google Scholar] [CrossRef]
- Pinol-Jurado, P.; Gallardo, E.; de Luna, N.; Suarez-Calvet, X.; Sanchez-Riera, C.; Fernandez-Simon, E.; Gomis, C.; Illa, I.; Diaz-Manera, J. Platelet-Derived Growth Factor BB Influences Muscle Regeneration in Duchenne Muscle Dystrophy. Am. J. Pathol. 2017, 187, 1814–1827. [Google Scholar] [CrossRef] [Green Version]
- Huang, M.B.; Xu, H.; Xie, S.J.; Zhou, H.; Qu, L.H. Insulin-like growth factor-1 receptor is regulated by microRNA-133 during skeletal myogenesis. PLoS ONE 2011, 6, e29173. [Google Scholar] [CrossRef] [Green Version]
- Sgro, P.; Ceci, R.; Lista, M.; Patrizio, F.; Sabatini, S.; Felici, F.; Sacchetti, M.; Bazzucchi, I.; Duranti, G.; Di Luigi, L. Quercetin Modulates IGF-I and IGF-II Levels After Eccentric Exercise-Induced Muscle-Damage: A Placebo-Controlled Study. Front. Endocrinol. 2021, 12, 745959. [Google Scholar] [CrossRef]
- Schmidt, M.; Schuler, S.C.; Huttner, S.S.; von Eyss, B.; von Maltzahn, J. Adult stem cells at work: Regenerating skeletal muscle. Cell. Mol. Life Sci. 2019, 76, 2559–2570. [Google Scholar] [CrossRef]
- Kim, J.H.; Choi, T.G.; Park, S.; Yun, H.R.; Nguyen, N.N.Y.; Jo, Y.H.; Jang, M.; Kim, J.; Kim, J.; Kang, I.; et al. Mitochondrial ROS-derived PTEN oxidation activates PI3K pathway for mTOR-induced myogenic autophagy. Cell Death Differ. 2018, 25, 1921–1937. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ge, Y.; Chen, J. Mammalian target of rapamycin (mTOR) signaling network in skeletal myogenesis. J. Biol. Chem. 2012, 287, 43928–43935. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tavares, M.R.; Pavan, I.C.; Amaral, C.L.; Meneguello, L.; Luchessi, A.D.; Simabuco, F.M. The S6K protein family in health and disease. Life Sci. 2015, 131, 1–10. [Google Scholar] [CrossRef] [PubMed]
- van der Velden, J.L.; Langen, R.C.; Kelders, M.C.; Wouters, E.F.; Janssen-Heininger, Y.M.; Schols, A.M. Inhibition of glycogen synthase kinase-3beta activity is sufficient to stimulate myogenic differentiation. Am. J. Physiol. Cell Physiol. 2006, 290, C453–C462. [Google Scholar] [CrossRef] [PubMed]
- Rochat, A.; Fernandez, A.; Vandromme, M.; Moles, J.P.; Bouschet, T.; Carnac, G.; Lamb, N.J. Insulin and wnt1 pathways cooperate to induce reserve cell activation in differentiation and myotube hypertrophy. Mol. Biol. Cell 2004, 15, 4544–4555. [Google Scholar] [CrossRef] [PubMed]
- Wu, M.; Falasca, M.; Blough, E.R. Akt/protein kinase B in skeletal muscle physiology and pathology. J. Cell. Physiol. 2011, 226, 29–36. [Google Scholar] [CrossRef]
- Gardner, S.; Anguiano, M.; Rotwein, P. Defining Akt actions in muscle differentiation. Am. J. Physiol. Cell Physiol. 2012, 303, C1292–C1300. [Google Scholar] [CrossRef] [Green Version]
- Negri, A.; Naponelli, V.; Rizzi, F.; Bettuzzi, S. Molecular Targets of Epigallocatechin-Gallate (EGCG): A Special Focus on Signal Transduction and Cancer. Nutrients 2018, 10, 1936. [Google Scholar] [CrossRef] [Green Version]
- Yan, X.; Li, Y.; Yu, H.; Wang, W.; Wu, C.; Yang, Y.; Hu, Y.; Shi, X.; Li, J. Epigallocatechin-3-gallate inhibits H2O2-induced apoptosis in Mouse Vascular Smooth Muscle Cells via 67kD Laminin Receptor. Sci. Rep. 2017, 7, 7774. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Hour, T.-C.; Vo, T.C.T.; Chuu, C.-P.; Chang, H.-W.; Su, Y.-F.; Chen, C.-H.; Chen, Y.-K. The Promotion of Migration and Myogenic Differentiation in Skeletal Muscle Cells by Quercetin and Underlying Mechanisms. Nutrients 2022, 14, 4106. https://doi.org/10.3390/nu14194106
Hour T-C, Vo TCT, Chuu C-P, Chang H-W, Su Y-F, Chen C-H, Chen Y-K. The Promotion of Migration and Myogenic Differentiation in Skeletal Muscle Cells by Quercetin and Underlying Mechanisms. Nutrients. 2022; 14(19):4106. https://doi.org/10.3390/nu14194106
Chicago/Turabian StyleHour, Tzyh-Chyuan, Thi Cam Tien Vo, Chih-Pin Chuu, Hsi-Wen Chang, Ying-Fang Su, Chung-Hwan Chen, and Yu-Kuei Chen. 2022. "The Promotion of Migration and Myogenic Differentiation in Skeletal Muscle Cells by Quercetin and Underlying Mechanisms" Nutrients 14, no. 19: 4106. https://doi.org/10.3390/nu14194106