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http://dx.doi.org/10.5187/jast.2021.e87

Effect of ciglitazone on adipogenic transdifferentiation of bovine skeletal muscle satellite cells  

Zhang, Junfang (Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanbian University)
Li, Qiang (Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanbian University)
Yan, Yan (Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanbian University)
Sun, Bin (Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanbian University)
Wang, Ying (Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanbian University)
Tang, Lin (Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanbian University)
Wang, Enze (Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanbian University)
Yu Jia (Department of Animal Science, Chungbuk National University)
Nogoy, Kim Margarette Corpuz (Department of Animal Science, Chungbuk National University)
Li, Xiangzi (Engineering Research Center of North-East Cold Region Beef Cattle Science & Technology Innovation, Ministry of Education, Yanbian University)
Choi, Seong-Ho (Department of Animal Science, Chungbuk National University)
Publication Information
Journal of Animal Science and Technology / v.63, no.4, 2021 , pp. 934-953 More about this Journal
Abstract
Ciglitazone is a member of the thiazolidinedione family, and specifically binds to peroxisome proliferator-activated receptor-γ (PPARγ), thereby promoting adipocyte differentiation. We hypothesized that ciglitazone as a PPARγ ligand in the absence of an adipocyte differentiation cocktail would increase adiponectin and adipogenic gene expression in bovine satellite cells (BSC). Muscle-derived BSCs were isolated from six, 18-month-old Yanbian Yellow Cattle. The BSC were cultured for 96 h in differentiation medium containing 5 µM ciglitazone (CL), 10 µM ciglitazone (CM), or 20 µM ciglitazone (CH). Control (CON) BSC were cultured only in a differentiation medium (containing 2% horse serum). The presence of myogenin, desmin, and paired box 7 (Pax7) proteins was confirmed in the BSC by immunofluorescence staining. The CL, CM, and CH treatments produced higher concentrations of triacylglycerol and lipid droplet accumulation in myotubes than those of the CON treatment. Ciglitazone treatments significantly increased the relative expression of PPARγ, CCAAT/enhancer-binding protein alpha (C/EBPα), C/EBPβ, fatty acid synthase, stearoyl-CoA desaturase, and perilipin 2. Ciglitazone treatments increased gene expression of Pax3 and Pax7 and decreased expression of myogenic differentiation-1, myogenin, myogenic regulatory factor-5, and myogenin-4 (p < 0.01). Adiponectin concentration caused by ciglitazone treatments was significantly greater than CON (p < 0.01). RNA sequencing showed that 281 differentially expressed genes (DEGs) were found in the treatments of ciglitazone. DEGs gene ontology (GO) analysis showed that the top 10 GO enrichment significantly changed the biological processes such as protein trimerization, negative regulation of cell proliferation, adipocytes differentiation, and cellular response to external stimulus. Kyoto Encyclopedia of Genes and Genomes pathway analysis showed that DEGs were involved in the p53 signaling pathway, PPAR signaling pathway, biosynthesis of amino acids, tumor necrosis factor signaling pathway, non-alcoholic fatty liver disease, PI3K-Akt signaling pathway, and Wnt signaling pathway. These results indicate that ciglitazone acts as PPARγ agonist, effectively increases the adiponectin concentration and adipogenic gene expression, and stimulates the conversion of BSC to adipocyte-like cells in the absence of adipocyte differentiation cocktail.
Keywords
Bovine satellite cells; Ciglitazone; Adipogenesis; Myogenesis; Differentially expressed genes;
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1 Choi SH, Park SK, Johnson BJ, Chung KY, Choi CW, Kim KH, et al. AMPKα, C/EBPβ, CPT1β, GPR43, PPARγ, and SCD gene expression in single- and co-cultured bovine satellite cells and intramuscular preadipocytes treated with palmitic, stearic, oleic, and linoleic acid. Asian-Australas J Anim Sci. 2015;28:411-9. https://doi.org/10.5713/ajas.14.0598   DOI
2 Teboul L, Gaillard D, Staccini L, Inadera H, Amri EZ, Grimaldi PA. Thiazolidinediones and fatty acids convert myogenic cells into adipose-like cells. J Biol Chem. 1995;270:28183-7. https://doi.org/10.1074/jbc.270.47.28183   DOI
3 Lizcano F, Romero C, Vargas D. Regulation of adipogenesis by nuclear receptor PPARγ is modulated by the histone demethylase JMJD2C. Genet Mol Biol. 2011;34:19-24. https://doi.org/10.1590/s1415-47572010005000105   DOI
4 Minnaard R, Schrauwen P, Schaart G, Jorgensen JA, Lenaers E, Mensink M, et al. Adipocyte differentiation-related protein and OXPAT in rat and human skeletal muscle: involvement in lipid accumulation and type 2 diabetes mellitus. J Clin Endocrinol Metab. 2009;94:4077-85. https://doi.org/10.1210/jc.2009-0352   DOI
5 Kageyama H, Hirano T, Okada K, Ebara T, Kageyama A, Murakami T, et al. Lipoprotein lipase mRNA in white adipose tissue but not in skeletal muscle is increased by pioglitazone through PPAR-γ. Biochem Biophys Res Commun. 2003;305:22-7. https://doi.org/10.1016/s0006-291x(03)00663-6   DOI
6 Kim JB, Wright HM, Wright M, Spiegelman BM. ADD1/SREBP1 activates PPARγ through the production of endogenous ligand. Proc Natl Acad Sci USA. 1998;95:4333-7. https://doi.org/10.1073/pnas.95.8.4333   DOI
7 Dodson MV, Wei S, Duarte M, Du M, Jiang Z, Hausman GJ, et al. Cell supermarket: adipose tissue as a source of stem cells. J Genomics. 2013;1:39-44. https://doi.org/10.7150/jgen.3949   DOI
8 Yablonka-Reuveni Z, Day K, Vine A, Shefer G. Defining the transcriptional signature of skeletal muscle stem cells. J Anim Sci. 2008;86:E207-16. https://doi.org/10.2527/jas.2007-0473   DOI
9 Moseti D, Regassa A, Kim WK. Molecular regulation of adipogenesis and potential anti-adipogenic bioactive molecules. Int J Mol Sci. 2016;17:124. https://doi.org/10.3390/ijms17010124   DOI
10 Lefterova MI, Lazar MA. New developments in adipogenesis. Trends Endocrinol Metab. 2009;20:P107-14. https://doi.org/10.1016/j.tem.2008.11.005   DOI
11 Yi X, Liu J, Wu P, Gong Y, Xu X, Li W. The whole transcriptional profiling of cellular metabolism during adipogenesis from hMSCs. J Cell Physiol. 2020;235:349-63. https://doi.org/10.1002/jcp.28974   DOI
12 Cossu G, Borello U. Wnt signaling and the activation of myogenesis in mammals. EMBO J. 1999;18:6867-72. https://doi.org/10.1093/emboj/18.24.6867   DOI
13 Stewart CEH, Rittweger J. Adaptive processes in skeletal muscle: molecular regulators and genetic influences. J Musculoskelet Neuronal Interact. 2006;6:73-86.
14 Wang C, Liu W, Nie Y, Qaher M, Horton HE, Yue F, et al. Loss of MyoD promotes fate transdifferentiation of myoblasts into brown adipocytes. EBioMedicine. 2017;16:212-23. https://doi.org/10.1016/j.ebiom.2017.01.015   DOI
15 Barthel A, Okino ST, Liao J, Nakatani K, Li J, Whitlock JP Jr, et al. Regulation of GLUT1 gene transcription by the serine/threonine kinase Akt1. J Biol Chem. 1999;274:20281-6. https://doi.org/10.1074/jbc.274.29.20281   DOI
16 Ross SE, Hemati N, Longo KA, Bennett CN, Lucas PC, Erickson RL, et al. Inhibition of adipogenesis by Wnt signaling. Science. 2000;289:950-3. https://doi.org/10.1126/science.289.5481.950   DOI
17 Kang S, Bajnok L, Longo KA, Petersen RK, Hansen JB, Kristiansen K, et al. Effects of Wnt signaling on brown adipocyte differentiation and metabolism mediated by PGC-1α. Mol Cell Biol. 2005;25:1272-82. https://doi.org/10.1128/mcb.25.4.1272-1282.2005   DOI
18 Prestwich TC, Macdougald OA. Wnt/β-catenin signaling in adipogenesis and metabolism. Curr Opin Cell Biol. 2007;19:612-7. https://doi.org/10.1016/j.ceb.2007.09.014   DOI
19 Budi EH, Duan D, Derynck R. Transforming growth factor-β receptors and Smads: regulatory complexity and functional versatility. Trends Cell Biol. 2017;27:658-72. https://doi.org/10.1016/j.tcb.2017.04.005   DOI
20 Kang JS, Liu C, Derynck R. New regulatory mechanisms of TGF-β receptor function. Trends Cell Biol. 2009;19:385-94. https://doi.org/10.1016/j.tcb.2009.05.008   DOI
21 Fabregat A, Jupe S, Matthews L, Sidiropoulos K, Gillespie M, Garapati P, et al. The reactome pathway knowledgebase. Nucleic Acids Res. 2018;46:D649-55. https://doi.org/10.1093/nar/gkx1132   DOI
22 Yue Y, Meng K, Pu Y, Zhang X. Transforming growth factor beta (TGF-β) mediates cardiac fibrosis and induces diabetic cardiomyopathy. Diabetes Res Clin Pract. 2017;133:124-30. https://doi.org/10.1016/j.diabres.2017.08.018   DOI
23 Yeow K, Phillips B, Dani C, Cabane C, Amri EZ, Derijard B. Inhibition of myogenesis enables adipogenic trans-differentiation in the C2C12 myogenic cell line. FEBS Lett. 2001;506:157-62. https://doi.org/10.1016/S0014-5793(01)02900-3   DOI
24 Singh NK, Chae HS, Hwang IH, Yoo YM, Ahn CN, Lee SH, et al. Transdifferentiation of porcine satellite cells to adipoblasts with ciglitizone. J Anim Sci. 2007;85:1126-35. https://doi.org/10.2527/jas.2006-524   DOI
25 Li XZ, Yan Y, Zhang JF, Sun JF, Sun B, Yan CG, et al. Oleic acid in the absence of a PPARγ agonist increases adipogenic gene expression in bovine muscle satellite cells. J Anim Sci. 2019;97:4114-23. https://doi.org/10.1093/jas/skz269   DOI
26 Chung KY, Lunt DK, Choi CB, Chae SH, Rhoades RD, Adams TH, et al. Lipid characteristics of subcutaneous adipose tissue and M. longissimus thoracis of Angus and Wagyu steers fed to US and Japanese endpoints. Meat Sci. 2006;73:432-41. https://doi.org/10.1016/j.meatsci.2006.01.002   DOI
27 Haakonsson AK, Stahl Madsen M, Nielsen R, Sandelin A, Mandrup S. Acute genome-wide effects of rosiglitazone on PPARγ transcriptional networks in adipocytes. Mol Endocrinol. 2013;27:1536-49. https://doi.org/10.1210/me.2013-1080   DOI
28 Hu E, Tontonoz P, Spiegelman BM. Transdifferentiation of myoblasts by the adipogenic transcription factors PPAR gamma and C/EBP alpha. Proc Natl Acad Sci USA. 1995;92:9856-60. https://doi.org/10.1073/pnas.92.21.9856   DOI
29 Cheguru P, Chapalamadugu KC, Doumit ME, Murdoch GK, Hill RA. Adipocyte differentiation-specific gene transcriptional response to C18 unsaturated fatty acids plus insulin. Pflugers Arch Eur J Physiol. 2012;463:429-47. https://doi.org/10.1007/s00424-011-1066-7   DOI
30 Rehfeldt C, Kuhn G. Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis. J Anim Sci. 2006;84. https://doi.org/10.2527/2006.8413_supple113x   DOI
31 Cornelison DDW, Olwin BB, Rudnicki MA, Wold BJ. MyoD-/- satellite cells in single-fiber culture are differentiation defective and MRF4 deficient. Dev Biol. 2000;224:122-37. https://doi.org/10.1006/dbio.2000.9682   DOI
32 Hassumi MY, Silva-Filho VJ, Campos-Junior JC, Vieira SM, Cunha FQ, Alves PM, et al. PPARγ agonist rosiglitazone prevents inflammatory periodontal bone loss by inhibiting osteoclastogenesis. Int Immunopharmacol. 2009;9:1150-8. https://doi.org/10.1016/j.intimp.2009.06.002   DOI
33 Deutsch MJ, Schriever SC, Roscher AA, Ensenauer R. Digital image analysis approach for lipid droplet size quantitation of oil red O-stained cultured cells. Anal Biochem. 2014;445:87-9. https://doi.org/10.1016/j.ab.2013.10.001   DOI
34 Fux C, Mitta B, Kramer BP, Fussenegger M. Dual-regulated expression of C/EBP-α and BMP-2 enables differential differentiation of C2C12 cells into adipocytes and osteoblasts. Nucleic Acids Res. 2004;32:e1. https://doi.org/10.1093/nar/gnh001   DOI
35 Li WC, Yu WY, Quinlan JM, Burke ZD, Tosh D. The molecular basis of transdifferentiation. J Cell Mol Med. 2005;9:569-82. https://doi.org/10.1111/j.1582-4934.2005.tb00489.x   DOI