Circ_ST6GAL1-mediated competing endogenous RNA network regulates TGF-β1-stimulated matrix Metalloproteinase-13 expression via Runx2 acetylation in osteoblasts

Silva, 2015, Biology of bone tissue: structure, function, and factors that influence bone cells, BioMed Res. Int., 2015 Scheinpflug, 2018, Journey into bone models: a review, Genes, 9, 247, 10.3390/genes9050247 Katsimbri, 2017, The biology of normal bone remodeling, Eur. J. Cancer Care, 26, 10.1111/ecc.12740 Hadjidakis, 2006, Bone remodeling, Ann. N. Y. Acad. Sci., 1092, 385, 10.1196/annals.1365.035 Saranya, 2022, Regulation of Wnt signaling by non-coding RNAs during osteoblast differentiation, Different.; Res. Biol. Diversity, 128, 57, 10.1016/j.diff.2022.10.003 Poniatowski Ł, 2015, Transforming growth factor Beta family: insight into the role of growth factors in regulation of fracture healing biology and potential clinical applications, Mediat. Inflamm., 2015, 10.1155/2015/137823 Crane, 2014, Bone marrow mesenchymal stem cells and TGF-β signaling in bone remodeling, J. Clin. Invest., 124, 466, 10.1172/JCI70050 Aiken, 2010, Unraveling metalloproteinase function in skeletal biology and disease using genetically altered mice, Biochim. Biophys. Acta, 1803, 121, 10.1016/j.bbamcr.2009.07.002 Selvamurugan, 2004, Transforming growth factor-beta 1 regulation of collagenase-3 expression in osteoblastic cells by cross-talk between the Smad and MAPK signaling pathways and their components, Smad2 and Runx2, J. Biol. Chem., 279, 19327, 10.1074/jbc.M314048200 Selvamurugan, 2009, Identification and characterization of Runx2 phosphorylation sites involved in matrix metalloproteinase-13 promoter activation, FEBS Lett., 583, 1141, 10.1016/j.febslet.2009.02.040 Arumugam, 2018, Characterization of Runx2 phosphorylation sites required for TGF-β1-mediated stimulation of matrix metalloproteinase-13 expression in osteoblastic cells, J. Cell. Physiol., 233, 1082, 10.1002/jcp.25964 Yoda, 2004, Delayed tooth eruption and suppressed osteoclast number in the eruption pathway of heterozygous Runx2/Cbfa1 knockout mice, Arch. Oral Biol., 49, 435, 10.1016/j.archoralbio.2004.01.010 Schroeder, 2005, Runx2: a master organizer of gene transcription in developing and maturing osteoblasts, Birth Defects Res. Part C Embryo Today - Rev., 75, 213, 10.1002/bdrc.20043 Jiménez, 1999, Collagenase 3 is a target of Cbfa1, a transcription factor of the runt gene family involved in bone formation, Mol. Cell Biol., 19, 4431, 10.1128/MCB.19.6.4431 Behonick, 2007, Role of matrix metalloproteinase 13 in both endochondral and intramembranous ossification during skeletal regeneration, PLoS One, 2, e1150, 10.1371/journal.pone.0001150 Gomathi, 2021, Regulation of transforming growth factor-β1-stimulation of Runx2 acetylation for matrix metalloproteinase 13 expression in osteoblastic cells, Biol. Chem., 403, 305, 10.1515/hsz-2021-0292 Gomathi, 2022, Identification and characterization of TGF-β1-responsive Runx2 acetylation sites for matrix Metalloproteinase-13 expression in osteoblastic cells, Biochimie, 201, 1, 10.1016/j.biochi.2022.06.013 Gomathi, 2021, Histone acetyl transferases and their epigenetic impact on bone remodeling, Int. J. Biol. Macromol., 170, 326, 10.1016/j.ijbiomac.2020.12.173 Vimalraj, 2013, MicroRNAs: synthesis, gene regulation and osteoblast differentiation, Curr. Issues Mol. Biol., 15, 7 Yang, 2017, Small non-coding RNAs-based bone regulation and targeting therapeutic strategies, Mol. Cell. Endocrinol., 456, 16, 10.1016/j.mce.2016.11.018 Jonas, 2015, Towards a molecular understanding of microRNA-mediated gene silencing, Nat. Rev. Genet., 16, 421, 10.1038/nrg3965 Zhao, 2014, MicroRNAs regulate bone metabolism, J. Bone Miner. Metabol., 32, 221, 10.1007/s00774-013-0537-7 Akshaya, 2020, A computational study of non-coding RNAs on the regulation of activating transcription factor 3 in human breast cancer cells, Comput. Biol. Chem., 89, 10.1016/j.compbiolchem.2020.107386 Wesselhoeft, 2018, Engineering circular RNA for potent and stable translation in eukaryotic cells, Nat. Commun., 9, 2629, 10.1038/s41467-018-05096-6 Li, 2022, CircRNA_0001795 sponges miRNA-339-5p to regulate yes-associated protein 1 expression and attenuate osteoporosis progression, Bioengineered, 13, 2803, 10.1080/21655979.2021.2022074 Mohanakrishnan, 2018, Parathyroid hormone-induced down-regulation of miR-532-5p for matrix metalloproteinase-13 expression in rat osteoblasts, J. Cell. Biochem., 119, 6181, 10.1002/jcb.26827 Malavika, 2020, miR-873-3p targets HDAC4 to stimulate matrix metalloproteinase-13 expression upon parathyroid hormone exposure in rat osteoblasts, J. Cell. Physiol., 235, 7996, 10.1002/jcp.29454 Akshaya, 2022, Parathyroid hormone-regulation of Runx2 by MiR-290 for matrix metalloproteinase-13 expression in rat osteoblastic cells, Curr. Mol. Med., 22, 549, 10.2174/1566524021666210830093232 Paiva, 2014, Bone tissue remodeling and development: focus on matrix metalloproteinase functions, Arch. Biochem. Biophys., 561, 74, 10.1016/j.abb.2014.07.034 Mattot, 1995, Expression of interstitial collagenase is restricted to skeletal tissue during mouse embryogenesis, J. Cell Sci., 108, 529, 10.1242/jcs.108.2.529 Wang, 2004, Regulation of MMP-13 expression by RUNX2 and FGF2 in osteoarthritic cartilage, Osteoarthritis Cartilage, 12, 963, 10.1016/j.joca.2004.08.008 Wu, 2020, Delivering siRNA to control osteogenic differentiation and real-time detection of cell differentiation in human mesenchymal stem cells using multifunctional gold nanoparticles, J. Mater. Chem. B, 8, 3016, 10.1039/C9TB02899D Howes, 2014, The recognition of collagen and triple-helical toolkit peptides by MMP-13: sequence specificity for binding and cleavage, J. Biol. Chem., 289, 24091, 10.1074/jbc.M114.583443 Barthelemi, 2012, Mechanical forces-induced human osteoblasts differentiation involves MMP-2/MMP-13/MT1-MMP proteolytic cascade, J. Cell. Biochem., 113, 760, 10.1002/jcb.23401 Tang, 2012, Matrix metalloproteinase-13 is required for osteocytic perilacunar remodeling and maintains bone fracture resistance, J. Bone Miner. Res. : Off. J. Am. Soc. Bone Mineral Res., 27, 1936, 10.1002/jbmr.1646 Kosaki, 2007, Impaired bone fracture healing in matrix metalloproteinase-13 deficient mice, Biochem. Biophys. Res. Commun., 354, 846, 10.1016/j.bbrc.2006.12.234 Yue, 2012, Role of integrins in regulating proteases to mediate extracellular matrix remodeling, Cancer Microenviron, 5, 275, 10.1007/s12307-012-0101-3 Lee, 2013, RUNX2 mutations in cleidocranial dysplasia, Genet. Mol. Res.: GMR, 12, 4567, 10.4238/2013.October.15.5 Lee, 2000, Runx2 is a common target of transforming growth factor beta1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell line C2C12, Mol. Cell Biol., 20, 8783, 10.1128/MCB.20.23.8783-8792.2000 Wu, 2016, TGF-β and BMP signaling in osteoblast, skeletal development, and bone formation, homeostasis and disease, Bone Res., 4, 10.1038/boneres.2016.9 Arumugam, 2019, Parathyroid hormone-stimulation of Runx2 during osteoblast differentiation via the regulation of lnc-SUPT3H-1:16 (RUNX2-AS1:32) and miR-6797-5p, Biochimie, 158, 43, 10.1016/j.biochi.2018.12.006 Chandran, 2019, Osteostimulatory effect of biocomposite scaffold containing phytomolecule diosmin by Integrin/FAK/ERK signaling pathway in mouse mesenchymal stem cells, Sci. Rep., 9, 10.1038/s41598-019-48429-1 Balagangadharan, 2019, Sinapic acid-loaded chitosan nanoparticles in polycaprolactone electrospun fibers for bone regeneration in vitro and in vivo, Carbohydr. Polym., 216, 1, 10.1016/j.carbpol.2019.04.002 Ravid, 2008, Diversity of degradation signals in the ubiquitin-proteasome system, Nat. Rev. Mol. Cell Biol., 9, 679, 10.1038/nrm2468 Drazic, 2016, The world of protein acetylation, Biochim. Biophys. Acta, 1864, 1372, 10.1016/j.bbapap.2016.06.007 Bruderer, 2014, Role and regulation of RUNX2 in osteogenesis, Eur. Cell. Mater., 28, 269, 10.22203/eCM.v028a19 Norris, 2009, Acetylation goes global: the emergence of acetylation biology, Sci. Signal., 2, pe76, 10.1126/scisignal.297pe76 Hu, 2015, miRNA-132-3p inhibits osteoblast differentiation by targeting Ep300 in simulated microgravity, Sci. Rep., 5, 10.1038/srep18655 Vimalraj, 2014, A positive role of microRNA-15b on regulation of osteoblast differentiation, J. Cell. Physiol., 229, 1236, 10.1002/jcp.24557 Yin, 2019, MiR-135-5p promotes osteoblast differentiation by targeting HIF1AN in MC3T3-E1 cells, Cell. Mol. Biol. Lett., 24, 51, 10.1186/s11658-019-0177-6 Bhushan, 2013, miR-181a promotes osteoblastic differentiation through repression of TGF-β signaling molecules, Int. J. Biochem. Cell Biol., 45, 696, 10.1016/j.biocel.2012.12.008 Bai, 2019, Expression of microRNA-27a in a rat model of osteonecrosis of the femoral head and its association with TGF-β/Smad7 signaling in osteoblasts, Int. J. Mol. Med., 43, 850 Lee, 2008, Systematic evaluation of microRNA processing patterns in tissues, cell lines, and tumors, RNA, 14, 35, 10.1261/rna.804508 Gan, 2013, Profiling pre-MicroRNA and mature MicroRNA expressions using a single microarray and avoiding separate sample preparation, Microarrays, 2, 24, 10.3390/microarrays2010024 Schmittgen, 2008, Real-time PCR quantification of precursor and mature microRNA, Methods, 44, 31, 10.1016/j.ymeth.2007.09.006 Akshaya, 2022, MiR-4638-3p regulates transforming growth factor-β1-induced activating transcription factor-3 and cell proliferation, invasion, and apoptosis in human breast cancer cells, Int. J. Biol. Macromol., 222, 1974, 10.1016/j.ijbiomac.2022.09.286 Rohini, 2018, miR-590-3p inhibits proliferation and promotes apoptosis by targeting activating transcription factor 3 in human breast cancer cells, Biochimie, 154, 10, 10.1016/j.biochi.2018.07.023 Ventura, 2010, Multisite phosphorylation provides an effective and flexible mechanism for switch-like protein degradation, PLoS One, 5 Drazic, 2016, The world of protein acetylation, Biochim. Biophys. Acta, 1864, 1372, 10.1016/j.bbapap.2016.06.007 Boumah, 2009, Runx2 recruits p300 to mediate parathyroid hormone's effects on histone acetylation and transcriptional activation of the matrix metalloproteinase-13 gene, Mol. Endocrinol. (Baltimore, Md, 23, 1255, 10.1210/me.2008-0217 Gomathi, 2020, Regulation of Runx2 by post-translational modifications in osteoblast differentiation, Life Sci., 245, 10.1016/j.lfs.2020.117389 Hj, 2020, Post-translational regulations of transcriptional activity of RUNX2, Mol. Cell., 43, 160 Shen, 2020, CircFOXP1/FOXP1 promotes osteogenic differentiation in adipose-derived mesenchymal stem cells and bone regeneration in osteoporosis via miR-33a-5p, J. Cell Mol. Med., 24, 12513, 10.1111/jcmm.15792 Zhou, 2021, Circular RNA circ_0000020 promotes osteogenic differentiation to reduce osteoporosis via sponging microRNA miR-142-5p to up-regulate Bone Morphogenetic Protein BMP2, Bioengineered, 12, 3824, 10.1080/21655979.2021.1949514 Guo, 2021, Circular RNA Hsa_circ_0006766 targets microRNA miR-4739 to regulate osteogenic differentiation of human bone marrow mesenchymal stem cells, Bioengineered, 12, 5679, 10.1080/21655979.2021.1967712 Yu, 2019, The emerging roles and functions of circular RNAs and their generation, J. Biomed. Sci., 26, 29, 10.1186/s12929-019-0523-z Dodbele, 2021, Best practices to ensure robust investigation of circular RNAs: pitfalls and tips, EMBO Rep., 22, 10.15252/embr.202052072 Chen, 2019, Circular RNAs in immune responses and immune diseases, Theranostics, 9, 588, 10.7150/thno.29678 Li, 2018, Identification of circRNAs for miRNA targets by Argonaute2 RNA immunoprecipitation and luciferase screening assays, Methods Mol. Biol., 1724, 209, 10.1007/978-1-4939-7562-4_17 Tian, 2018, Involvement of circular RNA SMARCA5/microRNA-620 axis in the regulation of cervical cancer cell proliferation, invasion and migration, Eur. Rev. Med. Pharmacol. Sci., 22, 8589 Zhu, 2019, CircRNA ZNF609 promotes growth and metastasis of nasopharyngeal carcinoma by competing with microRNA-150-5p, Eur. Rev. Med. Pharmacol. Sci., 23, 2817 Saikishore, 2020, The circular RNA-miRNA Axis: a special RNA signature regulatory transcriptome as a potential biomarker for OSCC, Mol. Ther. Nucleic Acids, 22, 352, 10.1016/j.omtn.2020.09.001 Mohanapriya, 2022, A regulatory role of circRNA-miRNA-mRNA network in osteoblast differentiation, Biochimie, 193, 137, 10.1016/j.biochi.2021.11.001 Lavenniah, 2020, Engineered circular RNA sponges act as miRNA inhibitors to attenuate pressure overload-induced cardiac hypertrophy, Mol. Ther. : J. Am. Soc. Gene Therapy, 28, 1506, 10.1016/j.ymthe.2020.04.006 Memczak, 2013, Circular RNAs are a large class of animal RNAs with regulatory potency, Nature, 495, 333, 10.1038/nature11928 Bartel, 2009, MicroRNAs: target recognition and regulatory functions, Cell, 136, 215, 10.1016/j.cell.2009.01.002 Ni, 2015, Dynamic miRNA-mRNA paradigms: new faces of miRNAs, Biochem. Biophys. Rep., 4, 337 Yu, 2019, The emerging roles and functions of circular RNAs and their generation, J. Biomed. Sci., 26, 29, 10.1186/s12929-019-0523-z Krishnan, 2022, Circ_CUX1/miR-130b-5p/p300 axis for parathyroid hormone-stimulation of Runx2 activity in rat osteoblasts: a combined bioinformatic and experimental approach, Int. J. Biol. Macromol., S0141–8130 Huang, 2021, Circ_0067680 expedites the osteogenic differentiation of human bone marrow-derived mesenchymal stem cells through miR-4429/CTNNB1/Wnt/β-catenin pathway, Biol. Direct, 16, 16, 10.1186/s13062-021-00302-w Yue, 2020, The circular RNA circHUWE1 sponges the miR-29b-AKT3 Axis to regulate myoblast development, Mol. Ther. Nucleic Acids, 19, 1086, 10.1016/j.omtn.2019.12.039 Ji, 2021, CircRNA hsa_circ_0006215 promotes osteogenic differentiation of BMSCs and enhances osteogenesis-angiogenesis coupling by competitively binding to miR-942-5p and regulating RUNX2 and VEGF, Aging (Albany NY), 13, 10275, 10.18632/aging.202791 Zhao, 2018, Hsa_Circ_0001275: a potential novel diagnostic biomarker for postmenopausal osteoporosis, Cell. Physiol. Biochem. : int. J. Experiment. Cellul. Physiol. Biochem. Pharmacol., 46, 2508, 10.1159/000489657 Yin, 2018, CircRUNX2 through has-miR-203 regulates RUNX2 to prevent osteoporosis, J. Cell Mol. Med., 22, 6112, 10.1111/jcmm.13888