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MiR-188-5p regulates the proliferation and differentiation of goat skeletal muscle satellite cells by targeting calcium/calmodulin dependent protein kinase II beta

  • Jing Jing (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Sihuan Zhang (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Jinbo Wei (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Yuhang Yang (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Qi Zheng (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Cuiyun Zhu (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Shuang Li (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Hongguo Cao (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Fugui Fang (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Yong Liu (Key Laboratory of Embryo Development and Reproductive Regulation of Anhui Province, Fuyang Normal University) ;
  • Ying-hui Ling (College of Animal Science and Technology, Anhui Agricultural University)
  • Received : 2023.03.13
  • Accepted : 2023.06.14
  • Published : 2023.12.01

Abstract

Objective: The aim of this study was to reveal the role and regulatory mechanism of miR-188-5p in the proliferation and differentiation of goat muscle satellite cells. Methods: Goat skeletal muscle satellite cells isolated in the pre-laboratory were used as the test material. First, the expression of miR-188-5p in goat muscle tissues at different developmental stages was detected by quantitative reverse transcription polymerase chain reaction (qRT-PCR). In addition, miR-188-5p was transfected into goat skeletal muscle satellite cells by constructing mimics and inhibitors of miR-188-5p, respectively. The changes of differentiation marker gene expression were detected by qPCR method. Results: It was highly expressed in adult goat latissimus dorsi and leg muscles, goat fetal skeletal muscle, and at the differentiation stage of muscle satellite cells. Overexpression and interference of miR-188-5p showed that miR-188-5p inhibited the proliferation and promoted the differentiation of goat muscle satellite cells. Target gene prediction and dual luciferase assays showed that miR-188-5p could target the 3'untranslated region of the calcium/calmodulin dependent protein kinase II beta (CAMK2B) gene and inhibit luciferase activity. Further functional studies revealed that CAMK2B promoted the proliferation and inhibited the differentiation of goat muscle satellite cells, whereas si-CAMK2B restored the function of miR-188-5p inhibitor. Conclusion: These results suggest that miR-188-5p inhibits the proliferation and promotes the differentiation of goat muscle satellite cells by targeting CAMK2B. This study will provide a theoretical reference for future studies on the molecular mechanisms of skeletal muscle development in goats.

Keywords

Acknowledgement

This research was supported by the National Natural Science Foundation of China (32172695), the Natural Science Foundation of Anhui Province (2108085Y11), and the 2021 annual mutton goat industry development pilot technology project of Linquan County (LQRJK2021-03) and Open project of Anhui Key Laboratory of embryonic development and reproductive regulation (FSKFKT019D).

References

  1. Wang Y, Liu W, Liu Y, et al. Long noncoding RNA H19 mediates LCoR to impact the osteogenic and adipogenic differentiation of mBMSCs in mice through sponging miR-188. J Cell Physiol 2018;233:7435-46. https://doi.org/10.1002/jcp.26589 
  2. Lyu M, Wang X, Meng X, et al. chi-miR-487b-3p inhibits goat myoblast proliferation and differentiation by targeting IRS1 through the IRS1/PI3K/Akt signaling pathway. Int J Mol Sci 2021;23:115. https://doi.org/10.3390/ijms23010115 
  3. Zammit PS. Function of the myogenic regulatory factors Myf5, MyoD, Myogenin and MRF4 in skeletal muscle, satellite cells and regenerative myogenesis. Semin Cell Dev Biol 2017;72:19-32. https://doi.org/10.1016/j.semcdb.2017.11.011 
  4. Tierney MT, Sacco A. Satellite cell heterogeneity in skeletal muscle homeostasis. Trends Cell Biol 2016;26:434-44. https://doi.org/10.1016/j.tcb.2016.02.004 
  5. Hindi SM, Millay DP. All for one and one for all: regenerating skeletal muscle. Cold Spring Harb Perspect Biol 2022;14:a040824. https://doi.org/10.1101/cshperspect.a040824 
  6. Giuliani G, Rosina M, Reggio A. Signaling pathways regulating the fate of fibro/adipogenic progenitors (FAPs) in skeletal muscle regeneration and disease. FEBS J 2022;289:6484-517. https://doi.org/10.1111/febs.16080 
  7. Ling YH, Sui MH, Zheng Q, et al. miR-27b regulates myogenic proliferation and differentiation by targeting Pax3 in goat. Sci Rep 2018;8:3909. https://doi.org/10.1038/s41598-018-22262-4 
  8. Punch VG, Jones AE, Rudnicki MA. Transcriptional networks that regulate muscle stem cell function. Wiley Interdiscip Rev Syst Biol Med 2009;1:128-40. https://doi.org/10.1002/wsbm.11 
  9. Lu TX, Rothenberg ME. MicroRNA. J Allergy Clin Immunol 2018;141:1202-7. https://doi.org/10.1016/j.jaci.2017.08.034 
  10. Bjorkman KK, Guess MG, Harrison BC, et al. miR-206 enforces a slow muscle phenotype. J Cell Sci 2020;133:jcs243162. https://doi.org/10.1242/jcs.243162 
  11. Chen JF, Mandel EM, Thomson JM, et al. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 2006;38:228-33. https://doi.org/10.1038/ng1725 
  12. Cardinali B, Cappella M, Provenzano C, et al. MicroRNA-222 regulates muscle alternative splicing through Rbm24 during differentiation of skeletal muscle cells. Cell Death Dis 2016;7:e2086. https://doi.org/10.1038/cddis.2016.10 
  13. Ling Y, Zheng Q, Jing J, et al. RNA-Seq reveals miRNA role shifts in seven stages of skeletal muscles in goat fetuses and kids. Front Genet 2020;11:684. https://doi.org/10.3389/fgene.2020.00684 
  14. Shibasaki H, Imamura M, Arima S, et al. Characterization of a novel microRNA, miR-188, elevated in serum of muscular dystrophy dog model. PLoS One 2019;14:e0211597. https://doi.org/10.1371/journal.pone.0211597 
  15. Mi S, Wang P, Lin L. miR-188-3p inhibits vascular smooth muscle cell proliferation and migration by targeting fibroblast growth factor 1 (FGF1). Med Sci Monit 2020;26:e924394. https://doi.org/10.12659/MSM.924394 
  16. Ying-hui L, Qi Z, Jing J, et al. Switches in transcriptome functions during seven skeletal muscle development stages from fetus to kid in Capra hircus. J Integr Agric 2021;20:212-26. https://doi.org/10.1016/S2095-3119(20)63268-3 
  17. Kim DY, Sung JH. Regulatory role of microRNAs in the proliferation and differentiation of adipose-derived stem cells. Histol Histopathol 2017;32:1-10. https://doi.org/10.14670/HH-11-798 
  18. Ran X, Xiao CH, Xiang GM, Ran XZ. Regulation of embryonic stem cell self-renewal and differentiation by MicroRNAs. Cell Reprogram 2017;19:150-8. https://doi.org/10.1089/cell.2016.0048 
  19. Zhao Y, Ponnusamy M, Dong Y, Zhang L, Wang K, Li P. Effects of miRNAs on myocardial apoptosis by modulating mitochondria related proteins. Clin Exp Pharmacol Physiol 2017;44:431-40. https://doi.org/10.1111/1440-1681.12720 
  20. Hu Z, Li Z. miRNAs in synapse development and synaptic plasticity. Curr Opin Neurobiol 2017;45:24-31. https://doi.org/10.1016/j.conb.2017.02.014 
  21. Bhattacharya M, Sharma AR, Sharma G, et al. The crucial role and regulations of miRNAs in zebrafish development. Protoplasma 2017;254:17-31. https://doi.org/10.1007/s00709-015-0931-1 
  22. Baradaran B, Shahbazi R, Khordadmehr M. Dysregulation of key microRNAs in pancreatic cancer development. Biomed Pharmacother 2019;109:1008-15. https://doi.org/10.1016/j.biopha.2018.10.177 
  23. Zhu X, Qiu J, Zhang T, et al. MicroRNA-188-5p promotes apoptosis and inhibits cell proliferation of breast cancer cells via the MAPK signaling pathway by targeting Rap2c. J Cell Physiol 2020;235:2389-402. https://doi.org/10.1002/jcp.29144 
  24. Ma J, Qin C, Yuan Z, Liu S. LncRNA PAPAS promotes hepatocellular carcinoma by interacting with miR-188-5p. J Cell Biochem 2019;120:13494-500. https://doi.org/10.1002/jcb.28623 
  25. Riaz F, Chen Q, Lu K, et al. Inhibition of miR-188-5p alleviates hepatic fibrosis by significantly reducing the activation and proliferation of HSCs through PTEN/PI3K/AKT pathway. J Cell Mol Med 2021;25:4073-87. https://doi.org/10.1111/jcmm.16376 
  26. Zhu X, Luo X, Song Z, et al. miR-188-5p promotes oxaliplatin resistance by targeting RASA1 in colon cancer cells. Oncol Lett 2021;21:481. https://doi.org/10.3892/ol.2021.12742 
  27. Zhang Q, Zhang K, Zhang C, et al. MicroRNAs as big regulators of neural stem/progenitor cell proliferation, differentiation and migration: a potential treatment for stroke. Curr Pharm Des 2017;23:2252-7. https://doi.org/10.2174/1381612823666170228124657 
  28. Fang F, Chang R, Yu L, et al. MicroRNA-188-5p suppresses tumor cell proliferation and metastasis by directly targeting FGF5 in hepatocellular carcinoma. J Hepatol 2015;63:874-85. https://doi.org/10.1016/j.jhep.2015.05.008 
  29. Valenti MT, Deiana M, Cheri S, et al. Physical exercise modulates miR-21-5p, miR-129-5p, miR-378-5p, and miR-188-5p expression in progenitor cells promoting osteogenesis. Cells 2019;8:742. https://doi.org/10.3390/cells8070742 
  30. Kury S, van Woerden GM, Besnard T, et al. De novo mutations in protein kinase genes CAMK2A and CAMK2B cause intellectual disability. Am J Hum Genet 2017;101:768-88. https://doi.org/10.1016/j.ajhg.2017.10.003 
  31. Nicole O, Pacary E. CaMKIIβ in Neuronal development and plasticity: an emerging candidate in brain diseases. Int J Mol Sci 2020;21:7272. https://doi.org/10.3390/ijms21197272 
  32. Akita T, Aoto K, Kato M, et al. De novo variants in CAMK2A and CAMK2B cause neurodevelopmental disorders. Ann Clin Transl Neurol 2018;5:280-96. https://doi.org/10.1002/acn3.528 
  33. Franz A, Weber AI, Preussner M, et al. Branch point strength controls species-specific CAMK2B alternative splicing and regulates LTP. Life Sci Alliance 2023;6:e202201826. https://doi.org/10.26508/lsa.202201826 
  34. Dwyer BK, Veenma DCM, Chang K, Schulman H, Van Woerden GM. Case report: developmental delay and acute neuropsychiatric episodes associated with a de novo mutation in the CAMK2B gene (c.328G>A p.Glu110Lys). Front Pharmacol 2022;13:794008. https://doi.org/10.3389/fphar.2022.794008 
  35. Kool MJ, van de Bree JE, Bodde HE, Elgersma Y, van Woerden GM. The molecular, temporal and region-specific requirements of the beta isoform of Calcium/Calmodulin-dependent protein kinase type 2 (CAMK2B) in mouse locomotion. Sci Rep 2016;6:26989. https://doi.org/10.1038/srep26989 
  36. Yuasa K, Okubo K, Yoda M, et al. Targeted ablation of p38α MAPK suppresses denervation-induced muscle atrophy. Sci Rep 2018;8:9037. https://doi.org/10.1038/s41598-018-26632-w 
  37. Brentnall M, Rodriguez-Menocal L, De Guevara RL, Cepero E, Boise LH. Caspase-9, caspase-3 and caspase-7 have distinct roles during intrinsic apoptosis. BMC Mol Cell Biol 2013;14:32. https://doi.org/10.1186/1471-2121-14-32