Bta-miR-24-3p Controls the Myogenic Differentiation and Proliferation of Fetal, Bovine, Skeletal Muscle-Derived Progenitor Cells by Targeting ACVR1B

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

doi:10.3390/ani9110859

Article (Scientific journals)

Bta-miR-24-3p Controls the Myogenic Differentiation and Proliferation of Fetal, Bovine, Skeletal Muscle-Derived Progenitor Cells by Targeting ACVR1B

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

2019 • In Animals

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/244193

DOI
10.3390/ani9110859

PubMed
31652908

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

animals-09-00859.pdf

Publisher postprint (2.01 MB)

Request a copy

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

bta-miR-24-3p; bovine; fetal skeletal muscle; proliferation; differentiation; ACVR1B

Abstract :

[en] MicroRNAs modulate a variety of cellular events, including skeletal muscle development, but the molecular basis of their functions in fetal bovine skeletal muscle development is poorly understood. In this study, we report that bta-miR-24-3p promotes the myogenic di erentiation of fetal bovine PDGFR - progenitor cells. The expression of bta-miR-24-3p increased during myogenic differentiation. Overexpression of bta-miR-24-3p significantly promoted myogenic di erentiation, but inhibited proliferation. A dual-luciferase assay identified ACVR1B as a direct target of bta-miR-24-3p. Similarly, knocking down ACVR1B by RNA interference also significantly inhibited proliferation and promoted the di erentiation of bovine PDGFR - progenitor cells. Thus, our study provides a mechanism in which bta-miR-24-3p regulates myogenesis by inhibiting ACVR1B expression.

Disciplines :

Veterinary medicine & animal health

Author, co-author :

Hu, Xin

Xing, Yishen

Ren, Ling

Wang, Yahui

Li, Qian

Fu, Xing

Yang, Qiyuan

Xu, Lingyang

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

Li, Junya

Zhang, Lupei

Language :

English

Title :

Bta-miR-24-3p Controls the Myogenic Differentiation and Proliferation of Fetal, Bovine, Skeletal Muscle-Derived Progenitor Cells by Targeting ACVR1B

Publication date :

24 October 2019

Journal title :

Animals

eISSN :

2076-2615

Publisher :

MDPI AG, Switzerland

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

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

Available on ORBi :

since 28 January 2020

Statistics

Number of views

72 (9 by ULiège)

Number of downloads

6 (6 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

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. [CrossRef] [PubMed]
Sabourin, L.A.; Rudnicki, M.A. The molecular regulation of myogenesis. Clin. Genet. 2000, 57, 16–25. [CrossRef] [PubMed]
Lassar, A.B.; Skapek, S.X.; Novitch, B. Regulatory mechanisms that coordinate skeletal muscle differentiation and cell cycle withdrawal. Curr. Opin. Cell Biol. 1994, 6, 788–794. [CrossRef]
Pownall, M.E.; Gustafsson, M.K.; Emerson, C.P., Jr. Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annu. Rev. Cell Dev. Biol. 2002, 18, 747–783. [CrossRef]
Yun, K.; Wold, B. Skeletal muscle determination and differentiation: Story of a core regulatory network and its context. Curr. Opin. Cell Biol. 1996, 8, 877–889. [CrossRef]
Bartel, D.P. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 2004, 116, 281–297. [CrossRef]
Wahid, F.; Shehzad, A.; Khan, T.; Kim, Y.Y. MicroRNAs: Synthesis, mechanism, function, and recent clinical trials. BBA Mol. Cell Res. 2010, 1803, 1231–1243. [CrossRef]
Xie, S.J.; Li, J.H.; Chen, H.F.; Tan, Y.Y.; Liu, S.R.; Zhang, Y.; Xu, H.; Yang, J.H.; Liu, S.; Zheng, L.L.; et al. Inhibition of the JNK/MAPK signaling pathway by myogenesis-associated miRNAs is required for skeletal muscle development. Cell Death Differ. 2018, 25, 1581–1597. [CrossRef]
Zhang, Y.; Yan, H.; Zhou, P.; Zhang, Z.; Liu, J.; Zhang, H. MicroRNA-152 Promotes Slow-Twitch Myofiber Formation via Targeting Uncoupling Protein-3 Gene. Animals 2019, 9. [CrossRef]
Zhang, W.R.; Zhang, H.N.; Wang, Y.M.; Dai, Y.; Liu, X.F.; Li, X.; Ding, X.B.; Guo, H. miR-143 regulates proliferation and differentiation of bovine skeletal muscle satellite cells by targeting IGFBP5. In Vitro Cell Dev. Biol. Anim. 2017, 53, 265–271. [CrossRef]
Song, C.; Yang, J.; Jiang, R.; Yang, Z.; Li, H.; Huang, Y.; Lan, X.; Lei, C.; Ma, Y.; Qi, X.; et al. miR-148a-3p regulates proliferation and apoptosis of bovine muscle cells by targeting KLF6. J. Cell. Physiol. 2019, 234. [CrossRef] [PubMed]
Tong, H.; Jiang, R.; Liu, T.; Wei, Y.; Li, S.; Yan, Y. bta-miR-378 promote the differentiation of bovine skeletal muscle-derived satellite cells. Gene 2018, 668, 246–251. [CrossRef] [PubMed]
Sun, Q.; Zhang, Y.; Yang, G.; Chen, X.; Zhang, Y.; Cao, G.; Wang, J.; Sun, Y.; Zhang, P.; Fan, M.; et al. Transforming growth factor-beta-regulated miR-24 promotes skeletal muscle differentiation. Nucleic Acids Res. 2008, 36, 2690–2699. [CrossRef] [PubMed]
Sun, Y.; Wang, H.; Li, Y.; Liu, S.; Chen, J.; Ying, H. miR-24 and miR-122 Negatively Regulate the Transforming Growth Factor-beta/Smad Signaling Pathway in Skeletal Muscle Fibrosis. Mol. Nucleic Acids 2018, 11, 528–537. [CrossRef]
Zimmerman, C.M.; Mathews, L.S. Activin receptors: Cellular signalling by receptor serine kinases. Biochem. Soc. Symp. 1996, 62, 25–38.
Reissmann, E.; Jornvall, H.; Blokzijl, A.; Andersson, O.; Chang, C.; Minchiotti, G.; Persico, M.G.; Ibanez, C.F.; Brivanlou, A.H. The orphan receptor ALK7 and the Activin receptor ALK4 mediate signaling by Nodal proteins during vertebrate development. Genes Dev. 2001, 15, 2010–2022. [CrossRef]
Ramsdell, A.F.; Bernanke, J.M.; Trusk, T.C. Left-right lineage analysis of the embryonic Xenopus heart reveals a novel framework linking congenital cardiac defects and laterality disease. Development 2006, 133, 1399–1410. [CrossRef]
Pasteuning-Vuhman, S.; Boertje-van der Meulen, J.W.; van Putten, M.; Overzier, M.; Ten Dijke, P.; Kielbasa, S.M.; Arindrarto, W.; Wolterbeek, R.; Lezhnina, K.V.; Ozerov, I.V.; et al. New function of the myostatin/activin type I receptor (ALK4) as a mediator of muscle atrophy and muscle regeneration. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2017, 31, 238–255. [CrossRef]
Mizuno, Y.; Tokuzawa, Y.; Ninomiya, Y.; Yagi, K.; Yatsuka-Kanesaki, Y.; Suda, T.; Fukuda, T.; Katagiri, T.; Kondoh, Y.; Amemiya, T.; et al. miR-210 promotes osteoblastic differentiation through inhibition of AcvR1b. FEBS Lett. 2009, 583, 2263–2268. [CrossRef]
Qiu, W.; Li, X.; Tang, H.; Huang, A.S.; Panteleyev, A.A.; Owens, D.M.; Su, G.H. Conditional activin receptor type 1B (Acvr1b) knockout mice reveal hair loss abnormality. J. Investig. Dermatol. 2011, 131, 1067–1076. [CrossRef]
Uezumi, A.; Fukada, S.; Yamamoto, N.; Takeda, S.; Tsuchida, K. Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat. Cell Biol. 2010, 12, 143–152. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
Yu, F.; Pang, G.; Zhao, G. ANRIL acts as onco-lncRNA by regulation of microRNA-24/c-Myc, MEK/ERK and Wnt/beta-catenin pathway in retinoblastoma. Int. J. Biol. Macromol. 2019, 128, 583–592. [CrossRef] [PubMed]
Zhu, Y.; Sun, Y.; Zhou, Y.; Zhang, Y.; Zhang, T.; Li, Y.; You, W.; Chang, X.; Yuan, L.; Han, X. MicroRNA-24 promotes pancreatic beta cells toward dedifferentiation to avoid endoplasmic reticulum stress-induced apoptosis. J. Mol. Cell Biol. 2019. [CrossRef] [PubMed]
Wang, J.; Yin, K.; Lv, X.; Yang, Q.; Shao, M.; Liu, X.; Sun, H. MicroRNA-24-3p regulates Hodgkin’s lymphoma cell proliferation, migration and invasion by targeting DEDD. Oncol. Lett. 2019, 17, 365–371. [CrossRef] [PubMed]
Lin, Y.; Yang, Y. MiR-24 inhibits inflammatory responses in LPS-induced acute lung injury of neonatal rats through targeting NLRP3. Pathol. Res. Pract. 2019, 215, 683–688. [CrossRef] [PubMed]
Xiao, X.; Lu, Z.; Lin, V.; May, A.; Shaw, D.H.; Wang, Z.; Che, B.; Tran, K.; Du, H.; Shaw, P.X. MicroRNA miR-24-3p Reduces Apoptosis and Regulates Keap1-Nrf2 Pathway in Mouse Cardiomyocytes Responding to Ischemia/Reperfusion Injury. Oxidative Med. Cell. Longev. 2018, 2018, 7042105. [CrossRef]
Yan, L.; Ma, J.; Zhu, Y.; Zan, J.; Wang, Z.; Ling, L.; Li, Q.; Lv, J.; Qi, S.; Cao, Y.; et al. miR-24-3p promotes cell migration and proliferation in lung cancer by targeting SOX7. J. Cell. Biochem. 2018, 119, 3989–3998. [CrossRef]
Wang, Q.; Huang, Z.; Xue, H.; Jin, C.; Ju, X.L.; Han, J.D.; Chen, Y.G. MicroRNA miR-24 inhibits erythropoiesis by targeting activin type I receptor ALK4. Blood 2008, 111, 588–595. [CrossRef]
Li, Z.; Sun, Y.; Cao, S.; Zhang, J.; Wei, J. Downregulation of miR-24-3p promotes osteogenic differentiation of human periodontal ligament stem cells by targeting SMAD family member 5. J. Cell. Physiol. 2019, 234, 7411–7419. [CrossRef]
Jin, L.; Li, Y.; Nie, L.; He, T.; Hu, J.; Liu, J.; Chen, M.; Shi, M.; Jiang, Z.; Gui, Y.; et al. MicroRNA242 is associated with cell proliferation, invasion, migration and apoptosis in renal cell carcinoma. Mol. Med. Rep. 2017, 16, 9157–9164. [CrossRef] [PubMed]
Hua, K.; Chen, Y.T.; Chen, C.F.; Tang, Y.S.; Huang, T.T.; Lin, Y.C.; Yeh, T.S.; Huang, K.H.; Lee, H.C.; Hsu, M.T.; et al. MicroRNA-23a/27a/24-2 cluster promotes gastric cancer cell proliferation synergistically. Oncol. Lett. 2018, 16, 2319–2325. [CrossRef] [PubMed]
Zhou, N.; Yan, H.L. MiR-24 promotes the proliferation and apoptosis of lung carcinoma via targeting MAPK7. Eur. Rev. Med. Pharmacol. Sci. 2018, 22, 6845–6852. [CrossRef] [PubMed]
Liu, L.; Pan, J.; Wang, H.; Ma, Z.; Yin, J.; Yuan, F.; Yuan, Q.; Zhou, L.; Liu, X.; Zhang, Y.; et al. von Willebrand factor rescued by miR-24 inhibition facilitates the proliferation and migration of osteosarcoma cells in vitro. Biosci. Rep. 2018, 38. [CrossRef] [PubMed]
Yu, G.; Jia, Z.; Dou, Z. miR-24-3p regulates bladder cancer cell proliferation, migration, invasion and autophagy by targeting DEDD. Oncol. Rep. 2017, 37, 1123–1131. [CrossRef] [PubMed]
Yang, J.; Chen, L.; Ding, J.; Fan, Z.; Li, S.; Wu, H.; Zhang, J.; Yang, C.; Wang, H.; Zeng, P.; et al. MicroRNA-24 inhibits high glucose-induced vascular smooth muscle cell proliferation and migration by targeting HMGB1. Gene 2016, 586, 268–273. [CrossRef]
Lal, A.; Navarro, F.; Maher, C.A.; Maliszewski, L.E.; Yan, N.; O’Day, E.; Chowdhury, D.; Dykxhoorn, D.M.; Tsai, P.; Hofmann, O.; et al. miR-24 Inhibits cell proliferation by targeting E2F2, MYC, and other cell-cycle genes via binding to “seedless” 3’UTR microRNA recognition elements. Mol. Cell 2009, 35, 610–625. [CrossRef]
Feng, X.H.; Derynck, R. Specificity and versatility in tgf-beta signaling through Smads. Annu. Rev. Cell Dev. Biol. 2005, 21, 659–693. [CrossRef]
Song, C.; Fan, B.; Xiao, Z. Overexpression of ALK4 inhibits cell proliferation and migration through the inactivation of JAK/STAT3 signaling pathway in glioma. Biomed. Pharmacother. 2018, 98, 440–445. [CrossRef]
Zhu, S.; Goldschmidt-Clermont, P.J.; Dong, C. Transforming growth factor-beta-induced inhibition of myogenesis is mediated through Smad pathway and is modulated by microtubule dynamic stability. Circ. Res. 2004, 94, 617–625. [CrossRef]
De Angelis, L.; Borghi, S.; Melchionna, R.; Berghella, L.; Baccarani-Contri, M.; Parise, F.; Ferrari, S.; Cossu, G. Inhibition of myogenesis by transforming growth factor beta is density-dependent and related to the translocation of transcription factor MEF2 to the cytoplasm. Proc. Natl. Acad. Sci. USA 1998, 95, 12358–12363. [CrossRef] [PubMed]
Liu, D.; Black, B.L.; Derynck, R. TGF-beta inhibits muscle differentiation through functional repression of myogenic transcription factors by Smad3. Genes Dev. 2001, 15, 2950–2966. [CrossRef] [PubMed]
Murakami, M.; Ohkuma, M.; Nakamura, M. Molecular mechanism of transforming growth factor-beta-mediated inhibition of growth arrest and differentiation in a myoblast cell line. Dev. Growth Differ. 2008, 50, 121–130. [CrossRef] [PubMed]
Matsumoto, Y.; Otsuka, F.; Hino, J.; Miyoshi, T.; Takano, M.; Miyazato, M.; Makino, H.; Kangawa, K. Bone morphogenetic protein-3b (BMP-3b) inhibits osteoblast differentiation via Smad2/3 pathway by counteracting Smad1/5/8 signaling. Mol. Cell. Endocrinol. 2012, 350, 78–86. [CrossRef] [PubMed]
Rebbapragada, A.; Benchabane, H.; Wrana, J.L.; Celeste, A.J.; Attisano, L. Myostatin Signals through a Transforming Growth Factor β-Like Signaling Pathway To Block Adipogenesis. Mol. Cell. Biol. 2003, 23, 7230–7242. [CrossRef] [PubMed]
Levine, A.J.; Brivanlou, A.H. GDF3 at the crossroads of TGF-beta signaling. Cell Cycle 2006, 5, 1069–1073. [CrossRef]
Hata, A.; Chen, Y.G. TGF-beta Signaling from Receptors to Smads. Cold Spring Harb. Perspect. Biol. 2016, 8. [CrossRef]
Hill, C.S. Transcriptional Control by the SMADs. Cold Spring Harb. Perspect. Biol. 2016, 8. [CrossRef]
Hinck, A.P. Structural studies of the TGF-betas and their receptors-insights into evolution of the TGF-beta superfamily. FEBS Lett. 2012, 586, 1860–1870. [CrossRef]
Clop, A.; Marcq, F.; Takeda, H.; Pirottin, D.; Tordoir, X.; Bibe, B.; Bouix, J.; Caiment, F.; Elsen, J.M.; Eychenne, F.; et al. A mutation creating a potential illegitimate microRNA target site in the myostatin gene affects muscularity in sheep. Nat. Genet. 2006, 38, 813–818. [CrossRef]
McPherron, A.C.; Lawler, A.M.; Lee, S.J. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 1997, 387, 83–90. [CrossRef] [PubMed]
McPherron, A.C.; Lee, S.J. Double muscling in cattle due to mutations in the myostatin gene. Proc. Natl. Acad. Sci. USA 1997, 94, 12457–12461. [CrossRef] [PubMed]
Kemaladewi, D.U.; de Gorter, D.J.; Aartsma-Rus, A.; van Ommen, G.J.; ten Dijke, P.; ’t Hoen, P.A.; Hoogaars, W.M. Cell-type specific regulation of myostatin signaling. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2012, 26, 1462–1472. [CrossRef] [PubMed]
Langley, B.; Thomas, M.; Bishop, A.; Sharma, M.; Gilmour, S.; Kambadur, R. Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J. Biol. Chem. 2002, 277, 49831–49840. [CrossRef] [PubMed]
Joulia, D.; Bernardi, H.; Garandel, V.; Rabenoelina, F.; Vernus, B.; Cabello, G. Mechanisms involved in the inhibition of myoblast proliferation and differentiation by myostatin. Exp. Cell Res. 2003, 286, 263–275. [CrossRef]
Taylor, W.E.; Bhasin, S.; Artaza, J.; Byhower, F.; Azam, M.; Willard, D.H., Jr.; Kull, F.C., Jr.; Gonzalez-Cadavid, N. Myostatin inhibits cell proliferation and protein synthesis in C2C12 muscle cells. Am. J. Physiol. Endocrinol. Metab. 2001, 280, E221–E228. [CrossRef]
Thomas, M.; Langley, B.; Berry, C.; Sharma, M.; Kirk, S.; Bass, J.; Kambadur, R. Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J. Biol. Chem. 2000, 275, 40235–40243. [CrossRef]
Garikipati, D.K.; Rodgers, B.D. Myostatin inhibits myosatellite cell proliferation and consequently activates differentiation: Evidence for endocrine-regulated transcript processing. J. Endocrinol. 2012, 215, 177–187. [CrossRef]
Rodgers, B.D.; Wiedeback, B.D.; Hoversten, K.E.; Jackson, M.F.; Walker, R.G.; Thompson, T.B. Myostatin stimulates, not inihibits, C2C12 myoblast proliferation. Endocrinology 2014, 155, 670–675. [CrossRef]
Manceau, M.; Gros, J.; Savage, K.; Thome, V.; McPherron, A.; Paterson, B.; Marcelle, C. Myostatin promotes the terminal differentiation of embryonic muscle progenitors. Genes Dev. 2008, 22, 668–681. [CrossRef]
Chen, X.; Huang, Z.; Chen, D.; Yang, T.; Liu, G. Role of microRNA-27a in myoblast differentiation. Cell Biol. Int. 2014, 38, 266–271. [CrossRef] [PubMed]
Zhang, A.; Li, M.; Wang, B.; Klein, J.D.; Price, S.R.; Wang, X.H. miRNA-23a/27a attenuates muscle atrophy and renal fibrosis through muscle-kidney crosstalk. J. Cachexia Sarcopenia Muscle 2018, 9, 755–770. [CrossRef]
Wang, B.; Zhang, C.; Zhang, A.; Cai, H.; Price, S.R.; Wang, X.H. MicroRNA-23a and MicroRNA-27a Mimic Exercise by Ameliorating CKD-Induced Muscle Atrophy. J. Am. Soc. Nephrol. JASN 2017, 28, 2631–2640. [CrossRef] [PubMed]
Wang, Y.; Luo, J.; Zhang, H.; Lu, J. microRNAs in the Same Clusters Evolve to Coordinately Regulate Functionally Related Genes. Mol. Biol. Evol. 2016, 33, 2232–2247. [CrossRef] [PubMed]