دورية أكاديمية
Unveiling the role of circRBBP7 in myoblast proliferation and differentiation: A novel regulator of muscle development.
| العنوان: | Unveiling the role of circRBBP7 in myoblast proliferation and differentiation: A novel regulator of muscle development. |
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| المؤلفون: | Yang Y; State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Animal Science and Technology, Guangxi University, Nanning, China.; The Animal Husbandry Research Institute of Guangxi Zhuang Autonomous Region, Guangxi Agricultural Vocational University, Nanning, China., Huang K; State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Animal Science and Technology, Guangxi University, Nanning, China.; Guangdong Provincial Key Laboratory of Animal Molecular Design and Precise Breeding, School of Life Science and Engineering, Foshan University, Foshan, China., Jiang H; State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Animal Science and Technology, Guangxi University, Nanning, China., Wang S; State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Animal Science and Technology, Guangxi University, Nanning, China., Xu X; State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Animal Science and Technology, Guangxi University, Nanning, China., Liu Y; Guangxi Zhuang Autonomous Region Center for Analysis and Test Research, Nanning, China., Liu Q; Guangdong Provincial Key Laboratory of Animal Molecular Design and Precise Breeding, School of Life Science and Engineering, Foshan University, Foshan, China., Wei M; The Animal Husbandry Research Institute of Guangxi Zhuang Autonomous Region, Guangxi Agricultural Vocational University, Nanning, China., Li Z; State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Animal Science and Technology, Guangxi University, Nanning, China. |
| المصدر: | FASEB journal : official publication of the Federation of American Societies for Experimental Biology [FASEB J] 2024 Jul 31; Vol. 38 (14), pp. e23808. |
| نوع المنشور: | Journal Article |
| اللغة: | English |
| بيانات الدورية: | Publisher: Federation of American Societies for Experimental Biology Country of Publication: United States NLM ID: 8804484 Publication Model: Print Cited Medium: Internet ISSN: 1530-6860 (Electronic) Linking ISSN: 08926638 NLM ISO Abbreviation: FASEB J Subsets: MEDLINE |
| أسماء مطبوعة: | Publication: 2020- : [Bethesda, Md.] : Hoboken, NJ : Federation of American Societies for Experimental Biology ; Wiley Original Publication: [Bethesda, Md.] : The Federation, [c1987- |
| مواضيع طبية MeSH: | Cell Differentiation* , Cell Proliferation* , Muscle Development*/physiology , Myoblasts*/metabolism , Myoblasts*/cytology , RNA, Circular*/genetics , RNA, Circular*/metabolism, Animals ; Male ; Mice ; Cell Line ; Mice, Inbred C57BL ; Muscle, Skeletal/metabolism ; Muscle, Skeletal/cytology ; Proto-Oncogene Proteins c-mdm2/metabolism ; Proto-Oncogene Proteins c-mdm2/genetics ; Signal Transduction ; Tumor Suppressor Protein p53/metabolism ; Tumor Suppressor Protein p53/genetics |
| مستخلص: | Muscle development is a multistep process regulated by diverse gene networks, and circRNAs are considered novel regulators mediating myogenesis. Here, we systematically analyzed the role and underlying regulatory mechanisms of circRBBP7 in myoblast proliferation and differentiation. Results showed that circRBBP7 has a typical circular structure and encodes a 13 -kDa protein. By performing circRBBP7 overexpression and RNA interference, we found that the function of circRBBP7 was positively correlated with the proliferation and differentiation of myoblasts. Using RNA sequencing, we identified 1633 and 532 differentially expressed genes (DEGs) during myoblast proliferation or differentiation, respectively. The DEGs were found mainly enriched in cell cycle- and skeletal muscle development-related pathways, such as the MDM2/p53 and PI3K-Akt signaling pathways. Further co-IP and IF co-localization analysis revealed that VEGFR-1 is a target of circRBBP7 in myoblasts. qRT-PCR and WB analysis further confirmed the positive correlation between VEGFR-1 and circRBBP7. Moreover, we found that in vivo transfection of circRBBP7 into injured muscle tissues significantly promoted the regeneration and repair of myofibers in mice. Therefore, we speculate that circRBBP7 may affect the activity of MDM2 by targeting VEGFR-1, altering the expression of muscle development-related genes by mediating p53 degradation, and ultimately promoting myoblast development and muscle regeneration. This study provides essential evidence that circRBBP7 can serve as a potential target for myogenesis regulation and a reference for the application of circRBBP7 in cattle genetic breeding and muscle injury treatment. (© 2024 Federation of American Societies for Experimental Biology.) |
| References: | Smiles WJ, Hawley JA, Camera DM. Effects of skeletal muscle energy availability on protein turnover responses to exercise. J Exp Biol. 2016;219:214‐225. Gao Q, Liu H, Wang Z, et al. Recent advances in feed and nutrition of beef cattle in China—a review. Anim Biosci. 2023;36:529‐539. Zanou N, Gailly P. Skeletal muscle hypertrophy and regeneration: interplay between the myogenic regulatory factors (MRFs) and insulin‐like growth factors (IGFs) pathways. Cell Mol Life Sci. 2013;70:4117‐4130. Hyatt JPK, McCall GE, Kander EM, Zhong H, Roy RR, Huey KA. PAX3/7 expression coincides with myod during chronic skeletal muscle overload. Muscle Nerve. 2008;38:861‐866. Lee S. Targeting the myostatin signaling pathway to treat muscle loss and metabolic dysfunction. J Clin Invest. 2021;131:e148372. Moretti I, Ciciliot S, Dyar KA, et al. MRF4 negatively regulates adult skeletal muscle growth by repressing MEF2 activity. Nat Commun. 2016;7:12397. Yang Y, Wang Y, Shan H, et al. Novel insights into the differences in nutrition value, gene regulation and network organization between muscles from pasture‐fed and barn‐fed goats. Foods. 2022;11:381. Chen M, Wei X, Song M, et al. Circular RNA circMYBPC1 promotes skeletal muscle differentiation by targeting MyHC. Mol Ther Nucleic Acids. 2021;24:352‐368. Chen CY, Sarnow P. Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science. 1995;268:415‐417. Yang Y, Fan X, Mao M, et al. Extensive translation of circular RNAs driven by N(6)‐methyladenosine. Cell Res. 2017;27:626‐641. Zhou B, Yang H, Yang C, et al. Translation of noncoding RNAs and cancer. Cancer Lett. 2021;497:89‐99. Chen Y, Yang C, Kao S, Liu C, Lin S, Chang K. MicroRNA‐211 enhances the oncogenicity of carcinogen‐induced oral carcinoma by repressing TCF12 and increasing antioxidant activity. Cancer Res. 2016;76:4872‐4886. Shen X, Cui C, Tang S, et al. MyoG‐enhanced circGPD2 regulates chicken skeletal muscle development by targeting miR‐203a. Int J Biol Macromol. 2022;222:2212‐2224. Huang K, Chen M, Zhong D, et al. Circular RNA profiling reveals an abundant circEch1 that promotes myogenesis and differentiation of bovine skeletal muscle. J Agric Food Chem. 2020;69:592‐601. Ye F, Gao G, Zou Y, et al. circFBXW7 inhibits malignant progression by sponging miR‐197‐3p and encoding a 185‐aa protein in triple‐negative breast cancer. Mol Ther Nucleic Acids. 2019;18:88‐98. Gu C, Zhou N, Wang Z, et al. circGprc5a promoted bladder oncogenesis and metastasis through Gprc5a‐targeting peptide. Mol Ther Nucleic Acids. 2018;13:633‐641. Floris G, Zhang L, Follesa P, Sun T. Regulatory role of circular RNAs and neurological disorders. Mol Neurobiol. 2017;54:5156‐5165. Memczak S, Jens M, Elefsinioti A, et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 2013;495:333‐338. Huang K, Li Z, Zhong D, et al. A circular RNA generated from nebulin (NEB) gene splicing promotes skeletal muscle myogenesis in cattle as detected by a multi‐omics approach. Adv Sci. 2024;11(3):e2300702. Chen B, You W, Wang Y, Shan T. The regulatory role of Myomaker and Myomixer–Myomerger–Minion in muscle development and regeneration. Cell Mol Life Sci. 2020;77:1551‐1569. Jeck WR, Sorrentino JA, Wang K, et al. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA. 2013;19:141‐157. Wang Y, Wang Z. Efficient backsplicing produces translatable circular mRNAs. RNA. 2015;21:172‐179. Pamudurti NR, Bartok O, Jens M, et al. Translation of circRNAs. Mol Cell. 2017;66:9‐21. Legnini I, Di Timoteo G, Rossi F, et al. Circ‐ZNF609 is a circular RNA that can be translated and functions in myogenesis. Mol Cell. 2017;66:22‐37. Zeng K, Chen X, Xu MU, et al. CircHIPK3 promotes colorectal cancer growth and metastasis by sponging miR‐7. Cell Death Dis. 2018;9:417. Zhao J, Wu J, Xu T, Yang Q, He J, Song X. IRESfinder: identifying RNA internal ribosome entry site in eukaryotic cell using framed k‐mer features. J Genet Genomics. 2018;45:403‐406. Tang C, Xie Y, Yu T, et al. m6A‐dependent biogenesis of circular RNAs in male germ cells. Cell Res. 2020;30:211‐228. Rong D, Sun H, Li Z, et al. An emerging function of circRNA‐miRNAs‐mRNA axis in human diseases. Oncotarget. 2017;8:73271‐73281. Li D, Li Z, Yang Y, et al. Circular RNAs as biomarkers and therapeutic targets in environmental chemical exposure‐related diseases. Environ Res. 2020;180:108825. Kotake Y, Nakagawa T, Kitagawa K, et al. Long non‐coding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15INK4B tumor suppressor gene. Oncogene. 2011;30:1956‐1962. Burd CE, Jeck WR, Liu Y, Sanoff HK, Wang Z, Sharpless NE. Expression of linear and novel circular forms of an INK4/ARF‐associated non‐coding RNA correlates with atherosclerosis risk. PLoS Genet. 2010;6:e1001233. Holdt LM, Stahringer A, Sass K, et al. Circular non‐coding RNA ANRIL modulates ribosomal RNA maturation and atherosclerosis in humans. Nat Commun. 2016;7:12429. Yan X, Zhang Z, Meng Y, et al. Genome‐wide identification and analysis of circular RNAs differentially expressed in the longissimus dorsi between Kazakh cattle and Xinjiang brown cattle. PeerJ. 2020;8:e8646. Shen L, Gan M, Tang Q, et al. Comprehensive analysis of lncRNAs and circRNAs reveals the metabolic specialization in oxidative and glycolytic skeletal muscles. Int J Mol Sci. 2019;20:2855. Yue B, Wang J, Ru W, et al. The circular RNA circHUWE1 sponges the miR‐29b‐AKT3 axis to regulate myoblast development. Mol Ther Nucleic Acids. 2020;19:1086‐1097. Pandey PR, Yang J, Tsitsipatis D, et al. circSamd4 represses myogenic transcriptional activity of PUR proteins. Nucleic Acids Res. 2020;48:3789‐3805. Zeng Y, Du WW, Wu Y, et al. A circular RNA binds to and activates AKT phosphorylation and nuclear localization reducing apoptosis and enhancing cardiac repair. Theranostics. 2017;7:3842‐3855. Du WW, Yang W, Liu E, Yang Z, Dhaliwal P, Yang BB. Foxo3 circular RNA retards cell cycle progression via forming ternary complexes with p21 and CDK2. Nucleic Acids Res. 2016;44:2846‐2858. Neganova I, Zhang X, Atkinson S, Lako M. Expression and functional analysis of G1 to S regulatory components reveals an important role for CDK2 in cell cycle regulation in human embryonic stem cells. Oncogene. 2009;28:20‐30. Shibuya M. Vascular endothelial growth factor and its receptor system: physiological functions in angiogenesis and pathological roles in various diseases. J Biochem. 2013;153:13‐19. Verma M, Shimizu‐Motohashi Y, Asakura Y, et al. Inhibition of FLT1 ameliorates muscular dystrophy phenotype by increased vasculature in a mouse model of Duchenne muscular dystrophy. PLoS Genet. 2019;15:e1008468. Ling M, Lai X, Quan L, et al. Knockdown of VEGFB/VEGFR1 signaling promotes white adipose tissue browning and skeletal muscle development. Int J Mol Sci. 2022;23:7524. Ling M, Quan L, Lai X, et al. VEGFB promotes myoblasts proliferation and differentiation through VEGFR1‐PI3K/Akt signaling pathway. Int J Mol Sci. 2021;22:13352. Ogawara Y, Kishishita S, Obata T, et al. Akt enhances Mdm2‐mediated ubiquitination and degradation of p53. J Biol Chem. 2002;277:21843‐21850. Sibuh BZ, Gupta PK, Taneja P, et al. Synthesis, in silico study, and anti‐cancer activity of thiosemicarbazone derivatives. Biomedicine. 2021;9:1375. Kennedy RA. The regulation of Mdm2 expression in cardiac myocytes. Imperial College London. 2007. Lion M, Bisio A, Tebaldi T, et al. Interaction between p53 and estradiol pathways in transcriptional responses to chemotherapeutics. Cell Cycle. 2013;12:1211‐1224. Mayo LD, Donner DB. A phosphatidylinositol 3‐kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus. Proc Natl Acad Sci USA. 2001;98:11598‐11603. Almada AE, Wagers AJ. Molecular circuitry of stem cell fate in skeletal muscle regeneration, ageing and disease. Nat Rev Mol Cell Biol. 2016;17:267‐279. Sato K, Li Y, Foster W, et al. Improvement of muscle healing through enhancement of muscle regeneration and prevention of fibrosis. Muscle Nerve. 2003;28:365‐372. Smith C, Kruger MJ, Smith RM, Myburgh KH. The inflammatory response to skeletal muscle injury: illuminating complexities. Sports Med. 2008;38:947‐969. Morgan JE, Partridge TA. Muscle satellite cells. Int J Biochem Cell Biol. 2003;35:1151‐1156. Le Grand F, Rudnicki MA. Skeletal muscle satellite cells and adult myogenesis. Curr Opin Cell Biol. 2007;19:628‐633. Cheung TH, Rando TA. Molecular regulation of stem cell quiescence. Nat Rev Mol Cell Biol. 2013;14:329‐340. Jones DL, Rando TA. Emerging models and paradigms for stem cell ageing. Nat Cell Biol. 2011;13:506‐512. Rodgers JT, King KY, Brett JO, et al. mTORC1 controls the adaptive transition of quiescent stem cells from G0 to G(Alert). Nature. 2014;510:393‐396. Rodgers JT, Schroeder MD, Ma C, Rando TA. HGFA is an injury‐regulated systemic factor that induces the transition of stem cells into GAlert. Cell Rep. 2017;19:479‐486. Voellenkle C, Perfetti A, Carrara M, et al. Dysregulation of circular RNAs in myotonic dystrophy type 1. Int J Mol Sci. 1938;2019:20. Reinoso‐Sánchez JF, Baroli G, Duranti G, et al. Emerging role for linear and circular spermine oxidase RNAs in skeletal muscle physiopathology. Int J Mol Sci. 2020;21:8227. Zeng Z, Xia L, Fan S, et al. Circular RNA CircMAP3K5 acts as a MicroRNA‐22‐3p sponge to promote resolution of intimal hyperplasia via TET2‐mediated smooth muscle cell differentiation. Circulation. 2021;143:354‐371. |
| معلومات مُعتمدة: | U20A2051 MOST | National Natural Science Foundation of China (NSFC); 2023GXNSFAA026350 Natural Science Foundation of Guangxi Zhuang Autonomous Region (Guangxi Natural Science Foundation); 20210006 Bama County for Talents in Science and Technology; 20210007 Bama County for Talents in Science and Technology; XKJ2333 Natural Science Foundation of Guangxi Agricultural Vocational University |
| فهرسة مساهمة: | Keywords: VEGFR‐1; circRBBP7; muscle repair; myogenesis; proliferation and differentiation |
| المشرفين على المادة: | EC 2.3.2.27 (Mdm2 protein, mouse) EC 2.3.2.27 (Proto-Oncogene Proteins c-mdm2) 0 (RNA, Circular) 0 (Tumor Suppressor Protein p53) 0 (Rbbp7 protein, mouse) |
| تواريخ الأحداث: | Date Created: 20240712 Date Completed: 20240712 Latest Revision: 20240718 |
| رمز التحديث: | 20240718 |
| DOI: | 10.1096/fj.202302599RR |
| PMID: | 38994637 |
| قاعدة البيانات: | MEDLINE |
| تدمد: | 1530-6860 |
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| DOI: | 10.1096/fj.202302599RR |