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Effect of RNA-binding proteins on osteogenic differentiation of bone marrow mesenchymal stem cells

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Abstract

Tissue regeneration mediated by mesenchymal stem cells (MSCs) is an ideal way to repair bone defects. RNA-binding proteins (RBPs) can affect cell function through post-transcriptional regulation. Exploring the role of RBPs in the process of osteogenic differentiation of bone marrow mesenchymal stem cells (BMSCs) is helpful to find a key method to promote the osteogenic efficiency of BMSCs. By reviewing the literature, we obtained a differentially expressed mRNA dataset during the osteogenic differentiation of BMSCs and a human RBP dataset. A total of 82 differentially expressed RBPs in the osteogenic differentiation of BMSCs were screened by intersection of the two datasets. Functional analysis showed that the differentially expressed RBPs were mainly involved in RNA transcription, translation and degradation through the formation of spliceosomes and ribonucleoprotein complexes. The top 15 RBPs determined by degree score were FBL, NOP58, DDX10, RPL9, SNRPD3, NCL, IFIH1, RPL18A, NAT10, EXOSC5, ALYREF, PA2G4, EIF5B, SNRPD1 and EIF6. The results of this study demonstrate that the expression of many RBPs changed during osteogenic differentiation of BMSCs.

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References

  1. Tan B, Tang Q, Zhong Y, Wei Y, He L, Wu Y, Wu J, Liao J (2021) Biomaterial-based strategies for maxillofacial tumour therapy and bone defect regeneration. Int J Oral Sci 13:9. https://doi.org/10.1038/s41368-021-00113-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Song W, Bo X, Ma X, Hou K, Li D, Geng W, Zeng J (2022) Craniomaxillofacial derived bone marrow mesenchymal stem/stromal cells (BMSCs) for craniomaxillofacial bone tissue engineering: a literature review. J Stomatol Oral Maxillofac Surg 123:e650–e659. https://doi.org/10.1016/j.jormas.2022.06.002

    Article  PubMed  Google Scholar 

  3. Dong CL, Liu XH, Wu L (2019) Research and development of osteogenic differentiation of bone marrow mesenchymal stem cells. Zhongguo Gu Shang 32:288–292. https://doi.org/10.3969/j.issn.1003-0034.2019.03.018

    Article  PubMed  Google Scholar 

  4. Zhao C, Xie W, Zhu H, Zhao M, Liu W, Wu Z, Wang L, Zhu B, Li S, Zhou Y, Jiang X, Xu Q, Ren C (2022) LncRNAs and their RBPs: how to influence the fate of stem cells? Stem Cell Res Ther 13:175. https://doi.org/10.1186/s13287-022-02851-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Qin H, Ni H, Liu Y, Yuan Y, Xi T, Li X, Zheng L (2020) RNA-binding proteins in tumor progression. J Hematol Oncol 13:90. https://doi.org/10.1186/s13045-020-00927-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Corley M, Burns MC, Yeo GW (2020) How RNA-binding proteins interact with RNA: molecules and mechanisms. Mol Cell 78:9–29. https://doi.org/10.1016/j.molcel.2020.03.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Padial-Molina M, Crespo-Lora V, Candido-Corral C, Martin-Morales N, Abril-Garcia D, Galindo-Moreno P, Hernandez-Cortes P, O’Valle F (2021) Expression of musashi-1 increases in bone healing. Int J Mol Sci. https://doi.org/10.3390/ijms22073395

    Article  PubMed  PubMed Central  Google Scholar 

  8. Kim DY, Kim KM, Kim EJ, Jang WG (2018) Hypothermia-induced RNA-binding motif protein 3 (RBM3) stimulates osteoblast differentiation via the ERK signaling pathway. Biochem Biophys Res Commun 498:459–465. https://doi.org/10.1016/j.bbrc.2018.02.209

    Article  CAS  PubMed  Google Scholar 

  9. Park JH, Park BW, Kang YH, Byun SH, Hwang SC, Kim DR, Woo DK, Byun JH (2017) Lin28a enhances in vitro osteoblastic differentiation of human periosteum-derived cells. Cell Biochem Funct 35:497–509. https://doi.org/10.1002/cbf.3305

    Article  CAS  PubMed  Google Scholar 

  10. Zhang W, Dong R, Diao S, Du J, Fan Z, Wang F (2017) Differential long noncoding RNA/mRNA expression profiling and functional network analysis during osteogenic differentiation of human bone marrow mesenchymal stem cells. Stem Cell Res Ther 8:30. https://doi.org/10.1186/s13287-017-0485-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Gerstberger S, Hafner M, Tuschl T (2014) A census of human RNA-binding proteins. Nat Rev Genet 15:829–845. https://doi.org/10.1038/nrg3813

    Article  CAS  PubMed  Google Scholar 

  12. Park JW, Fu S, Huang B, Xu RH (2020) Alternative splicing in mesenchymal stem cell differentiation. Stem Cells 38:1229–1240. https://doi.org/10.1002/stem.3248

    Article  PubMed  Google Scholar 

  13. Komori T (2019) Regulation of proliferation, differentiation and functions of osteoblasts by Runx2. Int J Mol Sci. https://doi.org/10.3390/ijms20071694

    Article  PubMed  PubMed Central  Google Scholar 

  14. Almalki SG, Agrawal DK (2016) Key transcription factors in the differentiation of mesenchymal stem cells. Differentiation 92:41–51. https://doi.org/10.1016/j.diff.2016.02.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Makita N, Suzuki M, Asami S, Takahata R, Kohzaki D, Kobayashi S, Hakamazuka T, Hozumi N (2008) Two of four alternatively spliced isoforms of RUNX2 control osteocalcin gene expression in human osteoblast cells. Gene 413:8–17. https://doi.org/10.1016/j.gene.2007.12.025

    Article  CAS  PubMed  Google Scholar 

  16. Venables JP, Lapasset L, Gadea G, Fort P, Klinck R, Irimia M, Vignal E, Thibault P, Prinos P, Chabot B, Abou Elela S, Roux P, Lemaitre JM, Tazi J (2013) MBNL1 and RBFOX2 cooperate to establish a splicing programme involved in pluripotent stem cell differentiation. Nat Commun 4:2480. https://doi.org/10.1038/ncomms3480

    Article  ADS  CAS  PubMed  Google Scholar 

  17. Sinha KM, Zhou X (2013) Genetic and molecular control of osterix in skeletal formation. J Cell Biochem 114:975–984. https://doi.org/10.1002/jcb.24439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Milona MA, Gough JE, Edgar AJ (2003) Expression of alternatively spliced isoforms of human Sp7 in osteoblast-like cells. BMC Genomics 4:43. https://doi.org/10.1186/1471-2164-4-43

    Article  PubMed  PubMed Central  Google Scholar 

  19. Mayer H, Bertram H, Lindenmaier W, Korff T, Weber H, Weich H (2005) Vascular endothelial growth factor (VEGF-A) expression in human mesenchymal stem cells: autocrine and paracrine role on osteoblastic and endothelial differentiation. J Cell Biochem 95:827–839. https://doi.org/10.1002/jcb.20462

    Article  CAS  PubMed  Google Scholar 

  20. Faure C, Linossier MT, Malaval L, Lafage-Proust MH, Peyroche S, Vico L, Guignandon A (2008) Mechanical signals modulated vascular endothelial growth factor-A (VEGF-A) alternative splicing in osteoblastic cells through actin polymerisation. Bone 42:1092–1101. https://doi.org/10.1016/j.bone.2008.02.011

    Article  CAS  PubMed  Google Scholar 

  21. Zhang X, Zara J, Siu RK, Ting K, Soo C (2010) The role of NELL-1, a growth factor associated with craniosynostosis, in promoting bone regeneration. J Dent Res 89:865–878. https://doi.org/10.1177/0022034510376401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Pang S, Shen J, Liu Y, Chen F, Zheng Z, James AW, Hsu CY, Zhang H, Lee KS, Wang C, Li C, Chen X, Jia H, Zhang X, Soo C, Ting K (2015) Proliferation and osteogenic differentiation of mesenchymal stem cells induced by a short isoform of NELL-1. Stem Cells 33:904–915. https://doi.org/10.1002/stem.1884

    Article  CAS  PubMed  Google Scholar 

  23. Akopian D, Shen K, Zhang X, Shan SO (2013) Signal recognition particle: an essential protein-targeting machine. Annu Rev Biochem 82:693–721. https://doi.org/10.1146/annurev-biochem-072711-164732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Leung E, Brown JD (2010) Biogenesis of the signal recognition particle. Biochem Soc Trans 38:1093–1098. https://doi.org/10.1042/BST0381093

    Article  CAS  PubMed  Google Scholar 

  25. Traianedes K, Findlay DM, Martin TJ, Gillespie MT (1995) Modulation of the signal recognition particle 54-kDa subunit (SRP54) in rat preosteoblasts by the extracellular matrix. J Biol Chem 270:20891–20894. https://doi.org/10.1074/jbc.270.36.20891

    Article  CAS  PubMed  Google Scholar 

  26. Zvereva MI, Shcherbakova DM, Dontsova OA (2010) Telomerase: structure, functions, and activity regulation. Biochemistry (Mosc) 75:1563–1583. https://doi.org/10.1134/s0006297910130055

    Article  CAS  PubMed  Google Scholar 

  27. Saeed H, Qiu W, Li C, Flyvbjerg A, Abdallah BM, Kassem M (2015) Telomerase activity promotes osteoblast differentiation by modulating IGF-signaling pathway. Biogerontology 16:733–745. https://doi.org/10.1007/s10522-015-9596-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Wu J, Zeng Z, Li Y, Qin H, Zuo C, Zhou C, Xu D (2021) Cycloastragenol protects against glucocorticoid-induced osteogenic differentiation inhibition by activating telomerase. Phytother Res 35:2034–2044. https://doi.org/10.1002/ptr.6946

    Article  CAS  PubMed  Google Scholar 

  29. Ramakrishnan V (2002) Ribosome structure and the mechanism of translation. Cell 108:557–572. https://doi.org/10.1016/s0092-8674(02)00619-0

    Article  CAS  PubMed  Google Scholar 

  30. Moss T, Langlois F, Gagnon-Kugler T, Stefanovsky V (2007) A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell Mol Life Sci 64:29–49. https://doi.org/10.1007/s00018-006-6278-1

    Article  CAS  PubMed  Google Scholar 

  31. Ali SA, Zaidi SK, Dacwag CS, Salma N, Young DW, Shakoori AR, Montecino MA, Lian JB, van Wijnen AJ, Imbalzano AN, Stein GS, Stein JL (2008) Phenotypic transcription factors epigenetically mediate cell growth control. Proc Natl Acad Sci U S A 105:6632–6637. https://doi.org/10.1073/pnas.0800970105

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  32. Hayashi Y, Kuroda T, Kishimoto H, Wang C, Iwama A, Kimura K (2014) Downregulation of rRNA transcription triggers cell differentiation. PLoS One 9:e98586. https://doi.org/10.1371/journal.pone.0098586

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  33. Zhang Q, Shalaby NA, Buszczak M (2014) Changes in rRNA transcription influence proliferation and cell fate within a stem cell lineage. Science 343:298–301. https://doi.org/10.1126/science.1246384

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  34. Ali SA, Dobson JR, Lian JB, Stein JL, van Wijnen AJ, Zaidi SK, Stein GS (2012) A RUNX2-HDAC1 co-repressor complex regulates rRNA gene expression by modulating UBF acetylation. J Cell Sci 125:2732–2739. https://doi.org/10.1242/jcs.100909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Neben CL, Idoni B, Salva JE, Tuzon CT, Rice JC, Krakow D, Merrill AE (2014) Bent bone dysplasia syndrome reveals nucleolar activity for FGFR2 in ribosomal DNA transcription. Hum Mol Genet 23:5659–5671. https://doi.org/10.1093/hmg/ddu282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Trainor PA, Merrill AE (2014) Ribosome biogenesis in skeletal development and the pathogenesis of skeletal disorders. Biochim Biophys Acta 1842:769–778. https://doi.org/10.1016/j.bbadis.2013.11.010

    Article  CAS  PubMed  Google Scholar 

  37. Wang Y, Chun RF, Adhikari S, Lopez CM, Xing Y (2020) Elucidating dynamics and regulation of alternative splicing in osteogenic differentiation. bioRxiv 2020.10.30.362384. https://doi.org/10.1101/2020.10.30.362384

  38. Simone LE, Keene JD (2013) Mechanisms coordinating ELAV/Hu mRNA regulons. Curr Opin Genet Dev 23:35–43. https://doi.org/10.1016/j.gde.2012.12.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Kota SK, Lim ZW, Kota SB (2021) Elavl1 impacts osteogenic differentiation and mRNA levels of genes involved in ECM organization. Front Cell Dev Biol 9:606971. https://doi.org/10.3389/fcell.2021.606971

    Article  PubMed  PubMed Central  Google Scholar 

  40. Lee MH, Wu X, Zhu Y (2020) RNA-binding protein PUM2 regulates mesenchymal stem cell fate via repression of JAK2 and RUNX2 mRNAs. J Cell Physiol 235:3874–3885. https://doi.org/10.1002/jcp.29281

    Article  CAS  PubMed  Google Scholar 

  41. Liu Z, Li B, Hu H, Li X, Zhang X (2022) Potential of RNA-binding protein human antigen R as a driver of osteogenic differentiation in osteoporosis. J Orthop Surg Res 17:234. https://doi.org/10.1186/s13018-022-03073-w

    Article  PubMed  PubMed Central  Google Scholar 

  42. Zhou Z, Chen S, Wu T, Chen Y, Cao Y, Huang Y, Liu D (2022) IGF2BP2, an RNA-binding protein regulates cell proliferation and osteogenic differentiation by stabilizing SRF mRNA. J Cell Physiol. https://doi.org/10.1002/jcp.30919

    Article  PubMed  PubMed Central  Google Scholar 

  43. Guo Y, Tang CY, Man XF, Tang HN, Tang J, Zhou CL, Tan SW, Wang M, Feng YZ, Zhou HD (2017) Insulin-like growth factor-1 promotes osteogenic differentiation and collagen I alpha 2 synthesis via induction of mRNA-binding protein LARP6 expression. Dev Growth Differ 59:94–103. https://doi.org/10.1111/dgd.12342

    Article  CAS  PubMed  Google Scholar 

  44. Suo J, Zou S, Wang J, Han Y, Zhang L, Lv C, Jiang B, Ren Q, Chen L, Yang L, Ji P, Zheng X, Hu P, Zou W (2022) The RNA-binding protein Musashi2 governs osteoblast-adipocyte lineage commitment by suppressing PPARgamma signaling. Bone Res 10:31. https://doi.org/10.1038/s41413-022-00202-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Wang J, Liu S, Li J, Zhao S, Yi Z (2019) Roles for miRNAs in osteogenic differentiation of bone marrow mesenchymal stem cells. Stem Cell Res Ther 10:197. https://doi.org/10.1186/s13287-019-1309-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Hong IS, Lee HY, Choi SW, Kim HS, Yu KR, Seo Y, Jung JW, Kang KS (2013) The effects of hedgehog on RNA binding protein Msi1 during the osteogenic differentiation of human cord blood-derived mesenchymal stem cells. Bone 56:416–425. https://doi.org/10.1016/j.bone.2013.07.016

    Article  CAS  PubMed  Google Scholar 

  47. Kuan II, Lee CC, Chen CH, Lu J, Kuo YS, Wu HC (2019) The extracellular domain of epithelial cell adhesion molecule (EpCAM) enhances multipotency of mesenchymal stem cells through EGFR-LIN28-LET7 signaling. J Biol Chem 294:7769–7786. https://doi.org/10.1074/jbc.RA119.007386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Mao Y, Ni N, Huang L, Fan J, Wang H, He F, Liu Q, Shi D, Fu K, Pakvasa M, Wagstaff W, Tucker AB, Chen C, Reid RR, Haydon RC, Ho SH, Lee MJ, He TC, Yang J, Shen L, Cai L, Luu HH (2021) Argonaute (AGO) proteins play an essential role in mediating BMP9-induced osteogenic signaling in mesenchymal stem cells (MSCs). Genes Dis 8:918–930. https://doi.org/10.1016/j.gendis.2021.04.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Zhang Y, Gu X, Li D, Cai L, Xu Q (2019) METTL3 regulates osteoblast differentiation and inflammatory response via smad signaling and MAPK signaling. Int J Mol Sci. https://doi.org/10.3390/ijms21010199

    Article  PubMed  PubMed Central  Google Scholar 

  50. Song Y, Pan Y, Wu M, Sun W, Luo L, Zhao Z, Liu J (2021) METTL3-mediated lncRNA m(6)A modification in the osteogenic differentiation of human adipose-derived stem cells induced by NEL-Like 1 protein. Stem Cell Rev Rep 17:2276–2290. https://doi.org/10.1007/s12015-021-10245-4

    Article  CAS  PubMed  Google Scholar 

  51. He M, Lei H, He X, Liu Y, Wang A, Ren Z, Liu X, Yan G, Wang W, Wang Y, Li G, Wang T, Pu J, Shen Z, Wang Y, Xie J, Du W, Yuan Y, Yang L (2022) METTL14 regulates osteogenesis of bone marrow mesenchymal stem cells via inducing autophagy through m6A/IGF2BPs/Beclin-1 signal axis. Stem Cells Transl Med 11:987–1001. https://doi.org/10.1093/stcltm/szac049

    Article  PubMed  PubMed Central  Google Scholar 

  52. Liu T, Zheng X, Wang C, Wang C, Jiang S, Li B, Chen P, Xu W, Zheng H, Yang R, Huang X, Zhang X, Jiang L (2021) The m(6)A “reader” YTHDF1 promotes osteogenesis of bone marrow mesenchymal stem cells through translational control of ZNF839. Cell Death Dis 12:1078. https://doi.org/10.1038/s41419-021-04312-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Yang W, Li HY, Wu YF, Mi RJ, Liu WZ, Shen X, Lu YX, Jiang YH, Ma MJ, Shen HY (2021) ac4C acetylation of RUNX2 catalyzed by NAT10 spurs osteogenesis of BMSCs and prevents ovariectomy-induced bone loss. Mol Ther Nucleic Acids 26:135–147. https://doi.org/10.1016/j.omtn.2021.06.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Yang R, Chen J, Zhang J, Qin R, Wang R, Qiu Y, Mao Z, Goltzman D, Miao D (2020) 1,25-Dihydroxyvitamin D protects against age-related osteoporosis by a novel VDR-Ezh2-p16 signal axis. Aging Cell 19:e13095. https://doi.org/10.1111/acel.13095

    Article  CAS  PubMed  Google Scholar 

  55. Iyer-Bierhoff A, Krogh N, Tessarz P, Ruppert T, Nielsen H, Grummt I (2018) SIRT7-dependent deacetylation of fibrillarin controls histone H2A methylation and rRNA synthesis during the cell cycle. Cell Rep 25:2946–2954. https://doi.org/10.1016/j.celrep.2018.11.051

    Article  CAS  PubMed  Google Scholar 

  56. Nelson SA, Santora KE, LaRochelle WJ (2000) Isolation and characterization of a novel PDGF-induced human gene. Gene 253:87–93. https://doi.org/10.1016/s0378-1119(00)00232-8

    Article  CAS  PubMed  Google Scholar 

  57. Gaudet P, Livstone MS, Lewis SE, Thomas PD (2011) Phylogenetic-based propagation of functional annotations within the gene ontology consortium. Brief Bioinform 12:449–462. https://doi.org/10.1093/bib/bbr042

    Article  PubMed  PubMed Central  Google Scholar 

  58. Liang X, Zuo MQ, Zhang Y, Li N, Ma C, Dong MQ, Gao N (2020) Structural snapshots of human pre-60S ribosomal particles before and after nuclear export. Nat Commun 11:3542. https://doi.org/10.1038/s41467-020-17237-x

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  59. You F, Sun H, Zhou X, Sun W, Liang S, Zhai Z, Jiang Z (2009) PCBP2 mediates degradation of the adaptor MAVS via the HECT ubiquitin ligase AIP4. Nat Immunol 10:1300–1308. https://doi.org/10.1038/ni.1815

    Article  CAS  PubMed  Google Scholar 

  60. Ito S, Horikawa S, Suzuki T, Kawauchi H, Tanaka Y, Suzuki T, Suzuki T (2014) Human NAT10 is an ATP-dependent RNA acetyltransferase responsible for N4-acetylcytidine formation in 18 S ribosomal RNA (rRNA). J Biol Chem 289:35724–35730. https://doi.org/10.1074/jbc.C114.602698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Finch AJ, Hilcenko C, Basse N, Drynan LF, Goyenechea B, Menne TF, Gonzalez Fernandez A, Simpson P, D’Santos CS, Arends MJ, Donadieu J, Bellanne-Chantelot C, Costanzo M, Boone C, McKenzie AN, Freund SM, Warren AJ (2011) Uncoupling of GTP hydrolysis from eIF6 release on the ribosome causes Shwachman-Diamond syndrome. Genes Dev 25:917–929. https://doi.org/10.1101/gad.623011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Campagne S, de Vries T, Malard F, Afanasyev P, Dorn G, Dedic E, Kohlbrecher J, Boehringer D, Clery A, Allain FH (2021) An in vitro reconstituted U1 snRNP allows the study of the disordered regions of the particle and the interactions with proteins and ligands. Nucleic Acids Res 49:e63. https://doi.org/10.1093/nar/gkab135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Jurica MS, Licklider LJ, Gygi SR, Grigorieff N, Moore MJ (2002) Purification and characterization of native spliceosomes suitable for three-dimensional structural analysis. RNA 8:426–439. https://doi.org/10.1017/s1355838202021088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Bertram K, Agafonov DE, Liu WT, Dybkov O, Will CL, Hartmuth K, Urlaub H, Kastner B, Stark H, Luhrmann R (2017) Cryo-EM structure of a human spliceosome activated for step 2 of splicing. Nature 542:318–323. https://doi.org/10.1038/nature21079

    Article  ADS  CAS  PubMed  Google Scholar 

  65. Foster LJ, Zeemann PA, Li C, Mann M, Jensen ON, Kassem M (2005) Differential expression profiling of membrane proteins by quantitative proteomics in a human mesenchymal stem cell line undergoing osteoblast differentiation. Stem Cells 23:1367–1377. https://doi.org/10.1634/stemcells.2004-0372

    Article  CAS  PubMed  Google Scholar 

  66. Arango D, Sturgill D, Alhusaini N, Dillman AA, Sweet TJ, Hanson G, Hosogane M, Sinclair WR, Nanan KK, Mandler MD, Fox SD, Zengeya TT, Andresson T, Meier JL, Coller J, Oberdoerffer S (2018) Acetylation of cytidine in mRNA promotes translation efficiency. Cell 175:1872–1886. https://doi.org/10.1016/j.cell.2018.10.030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Liu X, Cai S, Zhang C, Liu Z, Luo J, Xing B, Du X (2018) Deacetylation of NAT10 by Sirt1 promotes the transition from rRNA biogenesis to autophagy upon energy stress. Nucleic Acids Res 46:9601–9616. https://doi.org/10.1093/nar/gky777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by supported by the National Natural Science Foundation of China (Grant numbers 82170980 and 81771094), Young Scientist Program of Beijing Stomatological Hospital, Capital Medical University (NO. YSP202207).

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BL: conceived and designed this research, collected and analysed data, and wrote the manuscript. QJ: conceived and designed experiments and revised the manuscript. All authors have read and approved the manuscript.

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Correspondence to Qingsong Jiang.

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Luo, B., Jiang, Q. Effect of RNA-binding proteins on osteogenic differentiation of bone marrow mesenchymal stem cells. Mol Cell Biochem 479, 383–392 (2024). https://doi.org/10.1007/s11010-023-04742-y

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