bta-miR-23a Regulates the Myogenic Differentiation of Fetal Bovine Skeletal Muscle-Derived Progenitor Cells by Targeting MDFIC Gene

Hu, Xin; Xing, Yishen; Ren, Ling; Wang, Yahui; Li, Qian; Yang, Qiyuan; Du, Min; Xu, Lingyang; Willems, Luc; Li, Junya; Zhang, Lupei

doi:10.3390/genes11101232

Article (Scientific journals)

bta-miR-23a Regulates the Myogenic Differentiation of Fetal Bovine Skeletal Muscle-Derived Progenitor Cells by Targeting MDFIC Gene

Hu, Xin; Xing, Yishen; Ren, Ling et al.

2020 • In Genes, 20, p. 1232

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/252976

DOI
10.3390/genes11101232

PubMed
33092227

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Keywords :

bta-miR-23a; fetal muscle development; MDFIC

Abstract :

[en] miR-23a, a member of the miR-23a/24-2/27a cluster, has been demonstrated to play pivotal roles in many cellular activities. However, the mechanisms of how bta-miR-23a controls the myogenic differentiation (MD) of PDGFRα − bovine progenitor cells (bPCs) remain poorly understood. In the present work, bta-miR-23a expression was increased during the MD of PDGFRα− bPCs. Moreover, bta-miR-23a overexpression significantly promoted the MD of PDGFRα− bPCs. Luciferase reporter assays showed that the 3’-UTR region of MDFIC (MyoD family inhibitor domain containing) could be a promising target of bta-miR-23a, which resulted in its post-transcriptional down-regulation. Additionally, the knockdown of MDFIC by siRNA facilitated the MD of PDGFRα− bPCs, while the overexpression of MDFIC inhibited the activating effect of bta-miR-23a during MD. Of note, MDFIC might function through the interaction between MyoG transcription factor and MEF2C promoter. This study reveals that bta-miR-23a can promote the MD of PDGFRα− bPCs through post-transcriptional downregulation of MDFIC.

Disciplines :

Veterinary medicine & animal health

Author, co-author :

Hu, Xin

Xing, Yishen

Ren, Ling

Wang, Yahui

Li, Qian

Yang, Qiyuan

Du, Min

Xu, Lingyang

Willems, Luc ; Université de Liège - ULiège > Cancer-Cellular and Molecular Epigenetics

Li, Junya

Zhang, Lupei

Language :

English

Title :

bta-miR-23a Regulates the Myogenic Differentiation of Fetal Bovine Skeletal Muscle-Derived Progenitor Cells by Targeting MDFIC Gene

Publication date :

20 October 2020

Journal title :

Genes

ISSN :

2073-4425

Publisher :

Multidisciplinary Digital Publishing Institute (MDPI), Switzerland

Volume :

Pages :

1232

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

NSCF - National Natural Science Foundation of China
Cattle Breeding Innovative Research Team
Project of College Innovation Improvement under Beijing Municipality

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since 23 November 2020

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Bibliography

Cossu, G.; Borello, U. Wnt signaling and the activation of myogenesis in mammals. EMBO J. 1999, 18, 6867–6872.
Stickland, N.C. A quantitative study of muscle development in the bovine foetus (Bos indicus). Anat. Histol. Embryol. 1978, 7, 193–205.
Du, M.; Tong, J.; Zhao, J.; Underwood, K.R.; Zhu, M.; Ford, S.P.; Nathanielsz, P.W. Fetal programming of skeletal muscle development in ruminant animals. J. Anim. Sci. 2010, 88, E51–E60.
Du, M.; Yan, X.; Tong, J.F.; Zhao, J.X.; Zhu, M.J. Maternal Obesity, Inflammation, and Fetal Skeletal Muscle Development. Biol. Reprod. 2010, 82, 4–12.
Wang, Y.K.; Schnegelsberg, P.N.J.; Dausman, J.; Jaenisch, R. Functional redundancy of the muscle-specific transcription factors Myf5 and myogenin. Nature 1996, 379, 823–825.
Bober, E.; Lyons, G.E.; Braun, T.; Cossu, G.; Buckingham, M.; Arnold, H.H. The muscle regulatory gene, Myf-6, has a biphasic pattern of expression during early mouse development. J. Cell Biol. 1991, 113, 1255–1265.
Sassoon, D.; Lyons, G.; Wright, W.E.; Lin, V.; Lassar, A.; Weintraub, H.; Buckingham, M. Expression of two myogenic regulatory factors myogenin and MyoDl during mouse embryogenesis. Nature 1989, 341, 303–307.
Ying, F.; Zhang, L.; Bu, G.; Xiong, Y.; Zuo, B. Muscle fiber-type conversion in the transgenic pigs with overexpression of PGC1α gene in muscle. Biochem. Biophys. Res. Commun. 2016, 480, 669–674.
Zhao, R.-Q.; Yang, X.-J.; Xu, Q.-F.; Wei, X.-H.; Xia, D.; Chen, J. Expression of GHR and PGC-lα in association with changes of MyHC isof orm types in longissimus muscle of Erhualian and Large White pigs (Sus scrofa) during postnatal growth. Anim. Sci. 2016, 79, 203–211.
Ambros, V. The functions of animal microRNAs. Nature 2004, 431, 350–355.
Bartel, D.P. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 2004, 116, 281–297.
Dai, Y.; Wang, Y.M.; Zhang, W.R.; Liu, X.F.; Li, X.; Ding, X.B.; Guo, H. The role of microRNA-1 and microRNA-206 in the proliferation and differentiation of bovine skeletal muscle satellite cells. Vitr. Cell Dev. Biol. Anim. 2016, 52, 27–34.
Wang, Y.M.; Ding, X.B.; Dai, Y.; Liu, X.F.; Guo, H.; Zhang, Y. Identification and bioinformatics analysis of miRNAs involved in bovine skeletal muscle satellite cell myogenic differentiation. Mol. Cell. Biochem. 2015, 404, 113–122.
Zhang, W.W.; Sun, X.F.; Tong, H.L.; Wang, Y.H.; Li, S.F.; Yan, Y.Q.; Li, G.P. Effect of differentiation on microRNA expression in bovine skeletal muscle satellite cells by deep sequencing. Cell. Mol. Biol. Lett. 2016, 21, 8.
Wu, J.Y.; He, D.D.; Yue, B.L.; Zhang, C.L.; Fang, X.T.; Chen, H. miR-101-1 expression pattern in Qinchuan cattle and its role in the regulation of cell differentiation. Gene 2017, 636, 64–69.
Miretti, S.; Martignani, E.; Accornero, P.; Baratta, M. Functional effect of mir-27b on myostatin expression: A relationship in piedmontese cattle with double-muscled phenotype. BMC Genom. 2013, 14, 194.
Song, C.C.; Yang, Z.X.; Dong, D.; Xu, J.W.; Wang, J.; Li, H.; Huang, Y.Z.; Lan, X.Y.; Lei, C.Z.; Ma, Y.; et al. miR-483 inhibits bovine myoblast cell proliferation and differentiation via IGF1/PI3K/AKT signal pathway. J. Cell. Physiol. 2019, 234, 9839–9848.
Wada, S.; Kato, Y.; Okutsu, M.; Miyaki, S.; Suzuki, K.; Yan, Z.; Schiaffino, S.; Asahara, H.; Ushida, T.; Akimoto, T. Translational suppression of atrophic regulators by microRNA-23a integrates resistance to skeletal muscle atrophy. J. Biol. Chem. 2011, 286, 38456–38465.
Yong, F.L.; Wang, C.W.; Roslani, A.C.; Law, C.W. The involvement of miR-23a/APAF1 regulation axis in colorectal cancer. Int. J. Mol. Sci. 2014, 15, 11713–11729.
Shang, J.; Yang, F.; Wang, Y.; Wang, Y.; Xue, G.; Mei, Q.; Wang, F.; Sun, S. MicroRNA-23a antisense enhances 5-fluorouracil chemosensitivity through APAF-1/caspase-9 apoptotic pathway in colorectal cancer cells. J. Cell. Biochem. 2014, 115, 772–784.
Zhang, Y.; Wang, J.; Hui, B.; Sun, W.; Li, B.; Shi, F.; Che, S.; Chai, L.; Song, L. Pristimerin enhances the effect of cisplatin by inhibiting the miR-23a/Akt/GSK3β signaling pathway and suppressing autophagy in lung cancer cells. Int. J. Mol. Med. 2019, 43, 1382–1394.
Chen, B.; Zhu, A.; Tian, L.; Xin, Y.; Liu, X.; Peng, Y.; Zhang, J.; Miao, Y.; Wei, J. miR-23a suppresses pancreatic cancer cell progression by inhibiting PLK-1 expression. Mol. Med. Rep. 2018, 18, 105–112.
Ma, G.; Dai, W.; Sang, A.; Yang, X.; Gao, C. Upregulation of microRNA-23a/b promotes tumor progression and confers poor prognosis in patients with gastric cancer. Int. J. Clin. Exp. Pathol. 2014, 7, 8833–8840.
Wang, N.; Zhu, M.; Tsao, S.W.; Man, K.; Zhang, Z.; Feng, Y. MiR-23a-mediated inhibition of topoisomerase 1 expression potentiates cell response to etoposide in human hepatocellular carcinoma. Mol. Cancer 2013, 12, 119.
Thebault, S.; Gachon, F.; Lemasson, I.; Devaux, C.; Mesnard, J.M. Molecular cloning of a novel human I-mfa domain-containing protein that differently regulates human T-cell leukemia virus type I and HIV-1 expression. J. Biol. Chem. 2000, 275, 4848–4857.
Thebault, S.; Mesnard, J.M. How the sequestration of a protein interferes with its mechanism of action: Example of a new family of proteins characterized by a particular cysteine-rich carboxy-terminal domain involved in gene expression regulation. Curr. Protein Pept. Sci. 2001, 2, 155–167.
Chen, C.M.A.; Kraut, N.; Groudine, M.; Weintraub, H. I-mf, a Novel Myogenic Repressor, Interacts with Members of the MyoD Family. Cell 1996, 86, 731–741.
Kraut, N.; Snider, L.; Chen, C.M.A.; Tapscott, S.J.; Groudine, M. Requirement of the mouse I-mfa gene for placental development and skeletal patterning. Embo J. 1998, 17, 6276–6288.
Zhang, L.; Zhou, X.; Michal, J.J.; Ding, B.; Li, R.; Jiang, Z. Genome wide screening of candidate genes for improving piglet birth weight using high and low estimated breeding value populations. Int. J. Biol. Sci. 2014, 10, 236–244.
Guan, L.; Hu, X.; Liu, L.; Xing, Y.S.; Zhou, Z.K.; Liang, X.W.; Yang, Q.Y.; Jin, S.Y.; Bao, J.S.; Gao, H.J.; et al. bta-miR-23a involves in adipogenesis of progenitor cells derived from fetal bovine skeletal muscle. Sci. Rep.-UK 2017, 7, 43716.
Xing, Y.S.H.X.; Ren, L.; Wang, Y.H.; Xing, L.Y.; Li, J.Y.; Zhang, L.P. Identification of microRNAs Involved in Myogenic Differentiation of Bovine Fetal Skeletal Muscle Derived Myoblasts. Acta Vet. Zootech. Sin. 2018, 49, 1134–1144.
Wang, D.Z.; Valdez, M.R.; McAnally, J.; Richardson, J.; Olson, E.N. The Mef2c gene is a direct transcriptional target of myogenic bHLH and MEF2 proteins during skeletal muscle development. Dev. (Camb. Engl.) 2001, 128, 4623–4633.
Ma, M.; Dai, J.; Tang, H.; Xu, T.; Yu, S.; Si, L.; Cui, C.; Sheng, X.; Chi, Z.; Mao, L.; et al. MicroRNA-23a-3p Inhibits Mucosal Melanoma Growth and Progression through Targeting Adenylate Cyclase 1 and Attenuating cAMP and MAPK Pathways. Theranostics 2019, 9, 945–960.
Zhuang, R.J.; Bai, X.X.; Liu, W. MicroRNA-23a depletion promotes apoptosis of ovarian cancer stem cell and inhibits cell migration by targeting DLG2. Cancer Biol. Ther. 2019, 1–15.
Gao, P.; Tchernyshyov, I.; Chang, T.C.; Lee, Y.S.; Kita, K.; Ochi, T.; Zeller, K.I.; De Marzo, A.M.; Van Eyk, J.E.; Mendell, J.T.; et al. c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 2009, 458, 762–765.
Hadjimichael, C.; Nikolaou, C.; Papamatheakis, J.; Kretsovali, A. MicroRNAs for Fine-Tuning of Mouse Embryonic Stem Cell Fate Decision through Regulation of TGF-β Signaling. Stem Cell Rep. 2016, 6, 292–301.
Guo, Q.; Chen, Y.S.; Guo, L.J.; Jiang, T.J.; Lin, Z.Y. miR-23a/b regulates the balance between osteoblast and adipocyte differentiation in bone marrow mesenchymal stem cells. Bone Res. 2016, 4, 16022.
Hassan, M.Q.; Gordon, J.A.; Beloti, M.M.; Croce, C.M.; van Wijnen, A.J.; Stein, J.L.; Stein, G.S.; Lian, J.B. A network connecting Runx2, SATB2, and the miR-23a~27a~24-2 cluster regulates the osteoblast differentiation program. Proc. Natl. Acad. Sci. USA 2010, 107, 19879–19884.
Ying, Z.; Rong-Lin, X.; Jonathan, G.; Kimberly, L.B.; Stein, J.L.; Lian, J.B.; Van Wijnen, A.J.; Stein, G.S. Control of mesenchymal lineage progression by microRNAs targeting skeletal gene regulators Trps1 and Runx2. J. Biol. Chem. 2012, 287, 21926–21935.
Tanay, G.; Julieta, A.; Jeannette, N.; Hannes, E.; Christian, S.; Cedric, M.; Thomas, L.; Imane, M.; Leslie, S.; Martina, D. MicroRNAs establish robustness and adaptability of a critical gene network to regulate progenitor fate decisions during cortical neurogenesis. Cell Rep. 2014, 7, 1779–1788.
Ubaldo, G.; Valerio, D.C.; Pasquale, C.; Camilla, T.; Antonella, C.; Marcella, M.; Pietro, L.; Stefano, B.; Irene, B.; Emanuele, C. Mir-23a and mir-125b regulate neural stem/progenitor cell proliferation by targeting Musashi1. RNA Biol. 2014, 11, 1105–1112.
Murata, M.; Nonaka, H.; Komatsu, S.; Goto, M.; Mai, M.; Yamada, S.; Lin, I.C.; Yamashita, S.; Tachibana, H. Delphinidin Prevents Muscle Atrophy and Upregulates miR-23a Expression. J. Agric. Food Chem. 2016, 65, 45–50.
Zhiqiang, L.; Iram, M.; Kun, W.; Jianqin, J.; Jie, G.; Pei-Feng, L. miR-23a functions downstream of NFATc3 to regulate cardiac hypertrophy. Proc. Natl. Acad. Sci. USA 2009, 106, 12103–12108.
Mercatelli, N.; Fittipaldi, S.; Paola, E.D.; Dimauro, I.; Paronetto, M.P.; Jackson, M.J.; Caporossi, D. MiR-23-TrxR1 as a novel molecular axis in skeletal muscle differentiation. Sci. Rep. 2017, 7, 7219.
Wang, L.; Chen, X.; Zheng, Y.; Li, F.; Lu, Z.; Chen, C.; Liu, J.; Wang, Y.; Peng, Y.; Shen, Z.; et al. MiR-23a inhibits myogenic differentiation through down regulation of fast myosin heavy chain isoforms. Exp. Cell Res. 2012, 318, 2324–2334.
Snider, L.; Thirlwell, H.; Miller, J.R.; Moon, R.T.; Groudine, M.; Tapscott, S.J. Inhibition of Tcf3 binding by I-mfa domain proteins. Mol. Cell. Biol. 2001, 21, 1866–1873.
Weijun, P.; Yingying, J.; Tao, H.; Jiyong, W.; Donglei, T.; Xiaoqing, G.; Lin, L. Beta-catenin relieves I-mfa-mediated suppression of LEF-1 in mammalian cells. J. Cell Sci. 2006, 119, 4850.