Transcriptional profiling of bovine muscle-derived satellite cells during differentiation in vitro by high throughput RNA sequencing
Abstract
In this study, we utilized high throughput RNA sequencing to obtain a comprehensive gene expression profile of muscle-derived satellite cells (MDSCs) upon induction of differentiation. MDSCs were cultured in vitro and RNA was extracted for sequencing prior to differentiation (MDSC-P), and again during the early and late differentiation (MDSC-D1, and MDSC-D3, respectively) stages. Sequence tags were assembled and analyzed by digital gene expression profile to screen for differentially expressed genes, Gene Ontology annotation, and pathway enrichment analysis. Quantitative real-time PCR was used to confirm the results of RNA sequencing. Our results indicate that certain of genes were changed during skeletal muscle cell development, cell cycle progression, and cell metabolism during differentiation of bovine MDSCs. Furthermore, we identified certain genes that could be used as novel candidates for future research of muscle development. Additionally, the sequencing results indicated that lipid metabolism might be the predominant cellular process that occurs during MDSC differentiation.
References
1. Jang, Y., Sinha, M., Cerletti, M., Dall'Osso, C. and Wagers, A. Skeletal muscle stem cells: effects of aging and metabolism on muscle regenerative function. Cold Spring Harb. Symp. 76 (2011) 101-111.10.1101/sqb.2011.76.010652Search in Google Scholar PubMed
2. Hill, M., Wernig, A. and Goldspink, G. Muscle satellite (stem) cell activation during local tissue injury and repair. J. Anat. 203 (2003) 89-99.Search in Google Scholar
3. Cerletti, M., Jurga, S., Witczak, C.A., Hirshman, M.F., Shadrach, J.L., Goodyear, L.J. and Wagers, A.J. Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles. Cell 134 (2008) 37-47.Search in Google Scholar
4. Datar, I. and Betti, M. Possibilities for an in vitro meat production system. Innov. Food Sci. Emerg. 11 (2010) 13-22.Search in Google Scholar
5. Gharaibeh, B., Lu, A., Tebbets, J., Zheng, B., Feduska, J., Crisan, M., Péault, B., Cummins, J. and Huard, J. Isolation of a slowly adhering cell fraction containing stem cells from murine skeletal muscle by the preplate technique. Nat. Protoc. 3 (2008) 1501-1509.Search in Google Scholar
6. Tong, H.L., Li, Q.Z., Gao, X.J. and Yin, D.Y. Establishment and characterization of a lactating dairy goat mammary gland epithelial cell line. In Vitro Cell. Dev. Biol. Anim. 48 (2012) 149-155.Search in Google Scholar
7. Audic, S. and Claverie, J.-M. The significance of digital gene expression profiles. Genome Res. 7 (1997) 986-995.Search in Google Scholar
8. Kanehisa, M., Araki, M., Goto, S., Hattori, M., Hirakawa, M., Itoh, M., Katayama, T., Kawashima, S., Okuda, S. and Tokimatsu, T. KEGG for linking genomes to life and the environment. Nucleic Acids Res. 36 (2008) D480-D484.10.1093/nar/gkm882Search in Google Scholar PubMed PubMed Central
9. Livak, K.J. and Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔC T method. Methods 25 (2001) 402-408.Search in Google Scholar
10. Padilla, J., Jenkins, N.T., Thorne, P.K., Martin, J.S., Rector, R.S., Davis, J.W. and Laughlin, M.H. Transcriptome-wide RNA sequencing analysis of rat skeletal muscle feed arteries. part II: impact of exercise training in obesity. J. Appl. Physiol. (1985) 116 (2014) 1033-1047.10.1152/japplphysiol.01234.2013Search in Google Scholar PubMed PubMed Central
11. Jiugang, Z., Jing, L. and Yonggang, L. A novel porcine gene-SLC9A3R2, differentially expressed in the longissimus muscle tissues from Meishan and Large White Pigs. Folia Biol. (Praha) 57 (2010) 20-25.Search in Google Scholar
12. Zhe, C., Tong-Jin, Z., Jie, L., Yan-Song, G., Fan-Guo, M., Yong-Bin, Y. and Hai-Meng, Z. Slow skeletal muscle myosin-binding protein-C (MyBPC1) mediates recruitment of muscle-type creatine kinase (CK) to myosin. Biochem. J. 436 (2011) 437-445.Search in Google Scholar
13. Schaefer, L. and Iozzo, R.V. Biological functions of the small leucine-rich proteoglycans: from genetics to signal transduction. J. Biol. Chem. 283 (2008) 21305-21309.Search in Google Scholar
14. Chan, T.A., Hermeking, H., Lengauer, C., Kinzler, K.W. and Vogelstein, B. 14-3-3σ is required to prevent mitotic catastrophe after DNA damage .Nature 401 (1999) 616-620.Search in Google Scholar
15. Kennedy, M.A., Barrera, G.C., Nakamura, K., Baldán, Á., Tarr, P., Fishbein, M.C., Frank, J., Francone, O.L. and Edwards, P.A. ABCG1 has a critical role in mediating cholesterol efflux to HDL and preventing cellular lipid accumulation. Cell Metab. 1 (2005) 121-131.Search in Google Scholar
16. Hibuse, T., Maeda, N., Funahashi, T., Yamamoto, K., Nagasawa, A., Mizunoya, W., Kishida, K., Inoue, K., Kuriyama, H. and Nakamura, T. Aquaporin 7 deficiency is associated with development of obesity through activation of adipose glycerol kinase. Proc. Natl. Acad. Sci. USA 102 (2005) 10993-10998.Search in Google Scholar
17. Barnes, B.R., Marklund, S., Steiler, T.L., Walter, M., Hjälm, G., Amarger, V., Mahlapuu, M., Leng, Y., Johansson, C. and Galuska, D. The 5′-AMPactivated protein kinase γ3 isoform has a key role in carbohydrate and lipid metabolism in glycolytic skeletal muscle. J. Biol. Chem. 279 (2004) 38441-38447.Search in Google Scholar
18. Marhamati, D.J., Bellas, R.E., Arsura, M., Kypreos, K.E. and Sonenshein, G.E. A-myb is expressed in bovine vascular smooth muscle cells during the late G1-to-S phase transition and cooperates with c-myc to mediate progression to S phase. Mol. Cell. Biol. 17 (1997) 2448-2457.Search in Google Scholar
19. Lee, J.-H., Jang, S.-I., Yang, J.-M., Markova, N.G. and Steinert, P.M. The proximal promoter of the human transglutaminase 3 gene stratified squamous epithelial-specific expression in cultured cells is mediated by binding of sp1 and ets transcription factors to a proximal promoter element. J. Biol. Chem. 271 (1996) 4561-4568.Search in Google Scholar
20. Lee, K.-Y., Fu, H., Aladjem, M.I. and Myung, K. ATAD5 regulates the lifespan of DNA replication factories by modulating PCNA level on the chromatin. J. Cell Biol. 200 (2013) 31-44.Search in Google Scholar
21. Wu, H., Naya, F.J., McKinsey, T.A., Mercer, B., Shelton, J.M., Chin, E.R., Simard, A.R., Michel, R.N., Bassel-Duby, R. and Olson, E.N. MEF2 responds to multiple calcium-regulated signals in the control of skeletal muscle fiber type. EMBO J. 19 (2000) 1963-1973.Search in Google Scholar
22. Nakagawa, O., Arnold, M., Nakagawa, M., Hamada, H., Shelton, J.M., Kusano, H., Harris, T.M., Childs, G., Campbell, K.P. and Richardson, J.A. Centronuclear myopathy in mice lacking a novel muscle-specific protein kinase transcriptionally regulated by MEF2. Genes. Dev. 19 (2005) 2066-2077. Search in Google Scholar
23. MacLean, H., Chiu, W., Notini, A., Axell, A., Davey, R., McManus, J., Ma, C., Plant, D., Lynch, G. and Zajac, J. Impaired skeletal muscle development and function in male, but not female, genomic androgen receptor knockout mice. FASEB J. 22 (2008) 2676-2689.Search in Google Scholar
24. Nakamura, M.T., Yudell, B.E. and Loor, J.J. Regulation of energy metabolism by long-chain fatty acids. Prog. Lipid Res. 53 (2014) 124-144.Search in Google Scholar
25. Ryall, J.G. Metabolic reprogramming as a novel regulator of skeletal muscle development and regeneration. FEBS J. 280 (2013) 4004-4013. Search in Google Scholar
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Articles in the same Issue
- Transcriptional profiling of bovine muscle-derived satellite cells during differentiation in vitro by high throughput RNA sequencing
- Inhibition of CEA release from epithelial cells by lipid A of Gram-negative bacteria
- Neurotrophine-3 may contribute to neuronal differentiation of mesenchymal stem cells through the activation of the bone morphogenetic protein pathway
- In vitro and in vivo analysis of human fibroblast reprogramming and multipotency
- The pharmacological features of bilirubin: the question of the century
- Evaluation of the expressions pattern of miR-10b, 21, 200c, 373 and 520c to find the correlation between epithelial-to-mesenchymal transition and melanoma stem cell potential in isolated cancer stem cells
- Effects of neuritin on the migration, senescence and proliferation of human bone marrow mesenchymal stem cells
- Lipoxin A4 methyl ester alleviates vascular cognition impairment by regulating the expression of proteins related to autophagy and ER stress in the rat hippocampus
- Biomedical and agricultural applications of energy dispersive X-ray spectroscopy in electron microscopy
- The effect of the bioactive sphingolipids S1P and C1P on multipotent stromal cells – new opportunities in regenerative medicine