MiR-320-3p Regulates the Proliferation and Differentiation of Myogenic Progenitor Cells by Modulating Actin Remodeling
Abstract
:1. Introduction
2. Results
2.1. PA Impaired Differentiation but Induced miR-320-3p in Myoblasts
2.2. CFL2 Is a Direct Target of miR-320-3p
2.3. MiR-320-3p Increased F-Actin and Nuclear YAP1
2.4. MiR-320-3p Activated the Proliferation of Myoblasts
2.5. MiR-320-3p Suppressed Myogenic Factors Expression
2.6. MiR-320-3p Impeded Myoblast Differentiation
3. Discussion
4. Materials and Methods
4.1. Cell Culture and PA Treatment
4.2. Transfection of Oligonucleotides
4.3. RNA Preparation and Quantitative Real-Time PCR (qRT-PCR)
4.4. Dual-Luciferase Reporter Analysis
4.5. Immunoblot Analysis
4.6. Immunofluorescence Staining Analysis
4.7. Cell Proliferation Assays
4.8. Flow Cytometry
4.9. Bioinformatic and Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Chal, J.; Pourquie, O. Making muscle: Skeletal myogenesis in vivo and in vitro. Development 2017, 144, 2104–2122. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cruz-Jentoft, A.J.; Sayer, A.A. Sarcopenia. Lancet 2019, 393, 2636–2646. [Google Scholar] [CrossRef]
- Sartori, R.; Romanello, V.; Sandri, M. Mechanisms of muscle atrophy and hypertrophy: Implications in health and disease. Nat. Commun. 2021, 12, 330. [Google Scholar] [CrossRef] [PubMed]
- Akhmedov, D.; Berdeaux, R. The effects of obesity on skeletal muscle regeneration. Front. Physiol. 2013, 4, 371. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Teng, S.; Huang, P. The effect of type 2 diabetes mellitus and obesity on muscle progenitor cell function. Stem Cell Res. Ther. 2019, 10, 103. [Google Scholar] [CrossRef] [PubMed]
- Ji, C.; Guo, X. The clinical potential of circulating microRNAs in obesity. Nat. Rev. Endocrinol. 2019, 15, 731–743. [Google Scholar] [CrossRef] [PubMed]
- Barbiera, A.; Pelosi, L.; Sica, G.; Scicchitano, B.M. Nutrition and microRNAs: Novel Insights to Fight Sarcopenia. Antioxidants 2020, 9, 951. [Google Scholar] [CrossRef]
- Krol, J.; Loedige, I.; Filipowicz, W. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 2010, 11, 597–610. [Google Scholar] [CrossRef]
- Zhao, Y.; Chen, M.; Lian, D.; Li, Y.; Li, Y.; Wang, J.; Deng, S.; Yu, K.; Lian, Z. Non-Coding RNA Regulates the Myogenesis of Skeletal Muscle Satellite Cells, Injury Repair and Diseases. Cells 2019, 8, 988. [Google Scholar] [CrossRef] [Green Version]
- Mok, G.F.; Lozano-Velasco, E.; Munsterberg, A. microRNAs in skeletal muscle development. Semin. Cell Dev. Biol. 2017, 72, 67–76. [Google Scholar] [CrossRef] [Green Version]
- Sannicandro, A.J.; Soriano-Arroquia, A.; Goljanek-Whysall, K. Micro(RNA)-managing muscle wasting. J. Appl. Physiol. 2019, 127, 619–632. [Google Scholar] [CrossRef]
- Du, H.; Zhao, Y.; Yin, Z.; Wang, D.W.; Chen, C. The role of miR-320 in glucose and lipid metabolism disorder-associated diseases. Int. J. Biol. Sci. 2021, 17, 402–416. [Google Scholar] [CrossRef] [PubMed]
- McCreight, J.C.; Schneider, S.E.; Wilburn, D.B.; Swanson, W.J. Evolution of microRNA in primates. PLoS ONE 2017, 12, e0176596. [Google Scholar] [CrossRef] [PubMed]
- Liang, Y.; Li, S.; Tang, L. MicroRNA 320, an Anti-Oncogene Target miRNA for Cancer Therapy. Biomedicines 2021, 9, 591. [Google Scholar] [CrossRef] [PubMed]
- Tian, Z.Q.; Jiang, H.; Lu, Z.B. MiR-320 regulates cardiomyocyte apoptosis induced by ischemia-reperfusion injury by targeting AKIP1. Cell Mol. Biol. Lett. 2018, 23, 41. [Google Scholar] [CrossRef] [Green Version]
- Li, Q.Q.; Zhang, L.; Wan, H.Y.; Liu, M.; Li, X.; Tang, H. CREB1-driven expression of miR-320a promotes mitophagy by down-regulating VDAC1 expression during serum starvation in cervical cancer cells. Oncotarget 2015, 6, 34924–34940. [Google Scholar] [CrossRef] [Green Version]
- He, M.; Wang, J.; Yin, Z.; Zhao, Y.; Hou, H.; Fan, J.; Li, H.; Wen, Z.; Tang, J.; Wang, Y.; et al. MiR-320a induces diabetic nephropathy via inhibiting MafB. Aging 2019, 11, 3055–3079. [Google Scholar] [CrossRef]
- Liu, L.; Li, X. Downregulation of miR-320 Alleviates Endoplasmic Reticulum Stress and Inflammatory Response in 3T3-L1 Adipocytes. Exp. Clin. Endocrinol. Diabetes 2021, 129, 131–137. [Google Scholar] [CrossRef]
- Guerin, C.M.; Kramer, S.G. Cytoskeletal remodeling during myotube assembly and guidance: Coordinating the actin and microtubule networks. Commun. Integr. Biol. 2009, 2, 452–457. [Google Scholar] [CrossRef] [Green Version]
- Heng, Y.W.; Koh, C.G. Actin cytoskeleton dynamics and the cell division cycle. Int. J. Biochem. Cell Biol. 2010, 42, 1622–1633. [Google Scholar] [CrossRef]
- Kanellos, G.; Frame, M.C. Cellular functions of the ADF/cofilin family at a glance. J. Cell Sci. 2016, 129, 3211–3218. [Google Scholar] [CrossRef] [Green Version]
- Vartiainen, M.K.; Mustonen, T.; Mattila, P.K.; Ojala, P.J.; Thesleff, I.; Partanen, J.; Lappalainen, P. The three mouse actin-depolymerizing factor/cofilins evolved to fulfill cell-type-specific requirements for actin dynamics. Mol. Biol. Cell 2002, 13, 183–194. [Google Scholar] [CrossRef] [Green Version]
- Agrawal, P.B.; Joshi, M.; Savic, T.; Chen, Z.; Beggs, A.H. Normal myofibrillar development followed by progressive sarcomeric disruption with actin accumulations in a mouse Cfl2 knockout demonstrates requirement of cofilin-2 for muscle maintenance. Hum. Mol. Genet. 2012, 21, 2341–2356. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- De Winter, J.M.; Ottenheijm, C.A.C. Sarcomere Dysfunction in Nemaline Myopathy. J. Neuromuscul. Dis. 2017, 4, 99–113. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aragona, M.; Panciera, T.; Manfrin, A.; Giulitti, S.; Michielin, F.; Elvassore, N.; Dupont, S.; Piccolo, S. A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 2013, 154, 1047–1059. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bernstein, B.W.; Bamburg, J.R. ADF/cofilin: A functional node in cell biology. Trends Cell Biol. 2010, 20, 187–195. [Google Scholar] [CrossRef] [Green Version]
- Nguyen, M.T.; Min, K.H.; Kim, D.; Park, S.Y.; Lee, W. CFL2 is an essential mediator for myogenic differentiation in C2C12 myoblasts. Biochem. Biophys. Res. Commun. 2020, 533, 710–716. [Google Scholar] [CrossRef]
- Dupont, S. Role of YAP/TAZ in cell-matrix adhesion-mediated signalling and mechanotransduction. Exp. Cell Res. 2016, 343, 42–53. [Google Scholar] [CrossRef]
- Dumont, N.A.; Bentzinger, C.F.; Sincennes, M.-C.; Rudnicki, M.A. Satellite cells and skeletal muscle regeneration. Compr. Physiol. 2015, 5, 1027–1059. [Google Scholar]
- Wang, W.; Zhao, L.; Wei, X.; Wang, L.; Liu, S.; Yang, Y.; Wang, F.; Sun, G.; Zhang, J.; Ma, Y.; et al. MicroRNA-320a promotes 5-FU resistance in human pancreatic cancer cells. Sci. Rep. 2016, 6, 27641. [Google Scholar] [CrossRef]
- Kim, B.M.; Choi, M.Y. Non-canonical microRNAs miR-320 and miR-702 promote proliferation in Dgcr8-deficient embryonic stem cells. Biochem. Biophys. Res. Commun. 2012, 426, 183–189. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shen, W.; Lu, Y.; Hu, J.; Le, H.; Yu, W.; Xu, W.; Yu, W.; Zheng, J. Mechanism of miR-320 in Regulating Biological Characteristics of Ischemic Cerebral Neuron by Mediating Nox2/ROS Pathway. J. Mol. Neurosci. 2020, 70, 449–457. [Google Scholar] [CrossRef] [PubMed]
- Li, C.; Shi, J.; Zhao, Y. MiR-320 promotes B cell proliferation and the production of aberrant glycosylated IgA1 in IgA nephropathy. J. Cell Biochem. 2018, 119, 4607–4614. [Google Scholar] [CrossRef]
- Wang, W.; Yang, J.; Xiang, Y.Y.; Pi, J.; Bian, J. Overexpression of Hsa-miR-320 Is Associated with Invasion and Metastasis of Ovarian Cancer. J. Cell. Biochem. 2017, 118, 3654–3661. [Google Scholar] [CrossRef] [PubMed]
- Costa, C.; Indovina, P.; Mattioli, E.; Forte, I.M.; Iannuzzi, C.A.; Luzzi, L.; Bellan, C.; De Summa, S.; Bucci, E.; Di Marzo, D.; et al. P53-regulated miR-320a targets PDL1 and is downregulated in malignant mesothelioma. Cell Death Dis. 2020, 11, 748. [Google Scholar] [CrossRef]
- Watt, K.I.; Goodman, C.A.; Hornberger, T.A.; Gregorevic, P. The Hippo Signaling Pathway in the Regulation of Skeletal Muscle Mass and Function. Exerc. Sport Sci. Rev. 2018, 46, 92–96. [Google Scholar] [CrossRef]
- Bravo-Cordero, J.J.; Magalhaes, M.A.; Eddy, R.J.; Hodgson, L.; Condeelis, J. Functions of cofilin in cell locomotion and invasion. Nat. Rev. Mol. Cell Biol. 2013, 14, 405–415. [Google Scholar] [CrossRef] [Green Version]
- Mendez, M.G.; Janmey, P.A. Transcription factor regulation by mechanical stress. Int. J. Biochem. Cell Biol. 2012, 44, 728–732. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zou, R.; Xu, Y.; Feng, Y.; Shen, M.; Yuan, F.; Yuan, Y. YAP nuclear-cytoplasmic translocation is regulated by mechanical signaling, protein modification, and metabolism. Cell Biol. Int. 2020, 44, 1416–1425. [Google Scholar] [CrossRef]
- Dupont, S.; Morsut, L.; Aragona, M.; Enzo, E.; Giulitti, S.; Cordenonsi, M.; Zanconato, F.; Le Digabel, J.; Forcato, M.; Bicciato, S.; et al. Role of YAP/TAZ in mechanotransduction. Nature 2011, 474, 179–183. [Google Scholar] [CrossRef]
- Kim, J.; Jo, H.; Hong, H.; Kim, M.H.; Kim, J.M.; Lee, J.K.; Heo, W.D.; Kim, J. Actin remodelling factors control ciliogenesis by regulating YAP/TAZ activity and vesicle trafficking. Nat. Commun. 2015, 6, 6781. [Google Scholar] [CrossRef]
- Torrini, C.; Cubero, R.J.; Dirkx, E.; Braga, L.; Ali, H.; Prosdocimo, G.; Gutierrez, M.I.; Collesi, C.; Licastro, D.; Zentilin, L.; et al. Common Regulatory Pathways Mediate Activity of MicroRNAs Inducing Cardiomyocyte Proliferation. Cell Rep. 2019, 27, 2759–2771. [Google Scholar] [CrossRef] [Green Version]
- Hu, Z.; Tie, Y.; Lv, G.; Zhu, J.; Fu, H.; Zheng, X. Transcriptional activation of miR-320a by ATF2, ELK1 and YY1 induces cancer cell apoptosis under ionizing radiation conditions. Int. J. Oncol. 2018, 53, 1691–1702. [Google Scholar] [CrossRef] [Green Version]
- Wu, G.Y.; Rui, C.; Chen, J.Q.; Sho, E.; Zhan, S.S.; Yuan, X.W.; Ding, Y.T. MicroRNA-122 Inhibits Lipid Droplet Formation and Hepatic Triglyceride Accumulation via Yin Yang 1. Cell Physiol. Biochem. 2017, 44, 1651–1664. [Google Scholar] [CrossRef]
- Lu, Y.; Ma, Z.; Zhang, Z.; Xiong, X.; Wang, X.; Zhang, H.; Shi, G.; Xia, X.; Ning, G.; Li, X. Yin Yang 1 promotes hepatic steatosis through repression of farnesoid X receptor in obese mice. Gut 2014, 63, 170–178. [Google Scholar] [CrossRef] [PubMed]
- Pang, L.; You, L.; Ji, C.; Shi, C.; Chen, L.; Yang, L.; Huang, F.; Zhou, Y.; Zhang, J.; Chen, X.; et al. miR-1275 inhibits adipogenesis via ELK1 and its expression decreases in obese subjects. J. Mol. Endocrinol. 2016, 57, 33–43. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kung, C.P.; Murphy, M.E. The role of the p53 tumor suppressor in metabolism and diabetes. J. Endocrinol. 2016, 231, R61–R75. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Nguyen, M.T.; Lee, W. MiR-320-3p Regulates the Proliferation and Differentiation of Myogenic Progenitor Cells by Modulating Actin Remodeling. Int. J. Mol. Sci. 2022, 23, 801. https://doi.org/10.3390/ijms23020801
Nguyen MT, Lee W. MiR-320-3p Regulates the Proliferation and Differentiation of Myogenic Progenitor Cells by Modulating Actin Remodeling. International Journal of Molecular Sciences. 2022; 23(2):801. https://doi.org/10.3390/ijms23020801
Chicago/Turabian StyleNguyen, Mai Thi, and Wan Lee. 2022. "MiR-320-3p Regulates the Proliferation and Differentiation of Myogenic Progenitor Cells by Modulating Actin Remodeling" International Journal of Molecular Sciences 23, no. 2: 801. https://doi.org/10.3390/ijms23020801