Dynamics of DNA methylation during osteogenic differentiation of porcine synovial membrane mesenchymal stem cells from two metabolically distinct breeds

References

• Mochizuki T, Muneta T, Sakaguchi Y, et al. Higher chondrogenic potential of fibrous synovium– and adipose synovium–derived cells compared with subcutaneous fat–derived cells: Distinguishing properties of mesenchymal stem cells in humans. Arthritis Rheum. 2006;54(3):843–15. doi: 10.1002/art.21651
   PubMed Web of Science ®Google Scholar
• Bami M, Sarlikiotis T, Milonaki M, et al. Superiority of synovial membrane mesenchymal stem cells in chondrogenesis, osteogenesis, myogenesis and tenogenesis in a rabbit model. Injury. 2020;51(12):2855–2865. doi: 10.1016/j.injury.2020.03.022
   PubMed Web of Science ®Google Scholar
• Li N, Gao J, Mi L, et al. Synovial membrane mesenchymal stem cells: past life, current situation, and application in bone and joint diseases. Stem Cell Res Ther. 2020;11(1):381. doi: 10.1186/s13287-020-01885-3
   PubMed Web of Science ®Google Scholar
• Li S, Siengdee P, Oster M, et al. Transcriptome changes during osteogenesis of porcine mesenchymal stem cells derived from different types of synovial membranes and genetic background. Sci Rep. 2023;13(1):10048. doi: 10.1038/s41598-023-37260-4
   PubMed Web of Science ®Google Scholar
• Greenberg MVC, Bourc’his D. The diverse roles of DNA methylation in mammalian development and disease. Nat Rev Mol Cell Biol. 2019;20(10):590–607. doi: 10.1038/s41580-019-0159-6
   PubMed Web of Science ®Google Scholar
• Montecino M, Carrasco ME, Nardocci G. Epigenetic control of osteogenic lineage commitment. Front Cell Dev Biol. 2020;8:611197. doi: 10.3389/fcell.2020.611197
   PubMed Web of Science ®Google Scholar
• Wang X, Yu F, Ye L. Epigenetic control of mesenchymal stem cells orchestrates bone regeneration. Front Endocrinol (Lausanne). 2023;14:1126787. doi: 10.3389/fendo.2023.1126787
   PubMed Web of Science ®Google Scholar
• El-Serafi AT, Oreffo RO, Roach HI. Epigenetic modifiers influence lineage commitment of human bone marrow stromal cells: Differential effects of 5-aza-deoxycytidine and trichostatin A. Differentiation. 2011;81(1):35–41. doi: 10.1016/j.diff.2010.09.183
   PubMed Web of Science ®Google Scholar
• Alghfeli L, Parambath D, Tag Eldeen LA, et al. Non-additive effect of the DNA methylation inhibitor, 5-Aza-dC, and glass as a culture surface on osteogenic differentiation. Heliyon. 2022;8(12):e12433. doi: 10.1016/j.heliyon.2022.e12433
   PubMed Web of Science ®Google Scholar
• Yin Y, Morgunova E, Jolma A, et al. Impact of cytosine methylation on DNA binding specificities of human transcription factors. Science. 2017;356(6337):356. doi: 10.1126/science.aaj2239
   PubMed Web of Science ®Google Scholar
• Daniunaite K, Serenaite I, Misgirdaite R, et al. Epigenetic regulation of human adipose-derived stem cells differentiation. Mol Cell Biochem. 2015;410(1–2):111–120. doi: 10.1007/s11010-015-2543-7
   PubMed Web of Science ®Google Scholar
• Marofi F, Hassanzadeh A, Solali S, et al. Epigenetic mechanisms are behind the regulation of the key genes associated with the osteoblastic differentiation of the mesenchymal stem cells: The role of zoledronic acid on tuning the epigenetic changes. J Cell Physiol. 2019;234(9):15108–15122. doi: 10.1002/jcp.28152
   PubMed Web of Science ®Google Scholar
• Wang Z, Wen S, Zhong M, et al. Epigenetics: Novel crucial approach for osteogenesis of mesenchymal stem cells. J Tissue Eng. 2023;14:20417314231175364. doi: 10.1177/20417314231175364
   Web of Science ®Google Scholar
• Luo C, Hajkova P, Ecker JR. Dynamic DNA methylation: In the right place at the right time. Science. 2018;361(6409):1336–1340. doi: 10.1126/science.aat6806
   PubMed Web of Science ®Google Scholar
• Yu F, Shen H, Deng HW. Systemic analysis of osteoblast-specific DNA methylation marks reveals novel epigenetic basis of osteoblast differentiation. Bone Rep. 2017;6:109–119. doi: 10.1016/j.bonr.2017.04.001
   PubMedGoogle Scholar
• Ferreira RS, Assis RIF, Feltran GDS, et al. Genome-wide DNA (hydroxy) methylation reveals the individual epigenetic landscape importance on osteogenic phenotype acquisition in periodontal ligament cells. J Periodontol. 2022;93(3):435–448. doi: 10.1002/JPER.21-0218
   PubMed Web of Science ®Google Scholar
• Gomez R, Barter MJ, Alonso-Perez A, et al. DNA methylation analysis identifies key transcription factors involved in mesenchymal stem cell osteogenic differentiation. Biol Res. 2023;56(1):9. doi: 10.1186/s40659-023-00417-6
   PubMed Web of Science ®Google Scholar
• van Gastel N, Carmeliet G. Metabolic regulation of skeletal cell fate and function in physiology and disease. Nat Metab. 2021;3(1):11–20. doi: 10.1038/s42255-020-00321-3
   PubMedGoogle Scholar
• Frazier TP, Gimble JM, Devay JW, et al. Body mass index affects proliferation and osteogenic differentiation of human subcutaneous adipose tissue-derived stem cells. BMC Cell Biol. 2013;14(1):34. doi: 10.1186/1471-2121-14-34
   PubMedGoogle Scholar
• De Girolamo L, Stanco D, Salvatori L, et al. Stemness and osteogenic and adipogenic potential are differently impaired in subcutaneous and visceral adipose derived stem cells (ASCs) isolated from obese donors. Int J Immunopathol Pharmacol. 2013;26:11–21. doi: 10.1177/03946320130260S103
   PubMed Web of Science ®Google Scholar
• Oliva-Olivera W, Leiva Gea A, Lhamyani S, et al. Differences in the osteogenic differentiation capacity of omental adipose-derived stem cells in obese patients with and without metabolic syndrome. Endocrinology. 2015;156(12):4492–4501. doi: 10.1210/en.2015-1413
   PubMed Web of Science ®Google Scholar
• Strong AL, Hunter RS, Jones RB, et al. Obesity inhibits the osteogenic differentiation of human adipose-derived stem cells. J Transl Med. 2016;14(1):27. doi: 10.1186/s12967-016-0776-1
   PubMedGoogle Scholar
• Luthje FL, Skovgaard K, Jensen HE, et al. Pigs are useful for the molecular study of bone inflammation and regeneration in humans. Lab Anim. 2018;52(6):630–640. doi: 10.1177/0023677218766391
   PubMedGoogle Scholar
• Hotham WE, Henson FMD. The use of large animals to facilitate the process of MSC going from laboratory to patient—‘bench to bedside’. Cell Biol Toxicol. 2020;36(2):103–114. doi: 10.1007/s10565-020-09521-9
   PubMed Web of Science ®Google Scholar
• Afarideh M, Thaler R, Khani F, et al. Global epigenetic alterations of mesenchymal stem cells in obesity: the role of vitamin C reprogramming. Epigenetics. 2021;16(7):705–717. doi: 10.1080/15592294.2020.1819663
   PubMed Web of Science ®Google Scholar
• Glasstetter LM, Oderinde TS, Mirchandani M, et al. Obesity and dyslipidemia are associated with partially reversible modifications to DNA hydroxymethylation of apoptosis- and senescence-related genes in swine adipose-derived mesenchymal stem/stromal cells. Stem Cell Res Ther. 2023;14(1):143. doi: 10.1186/s13287-023-03372-x
   PubMed Web of Science ®Google Scholar
• Rajagopalan KS, Kazeminia S, Glasstetter LM, et al. Metabolic syndrome induces epigenetic alterations in mitochondria-related genes in swine mesenchymal stem cells. Cells. 2023;12(9):12. doi: 10.3390/cells12091274
   Web of Science ®Google Scholar
• Siengdee P, Oster M, Reyer H, et al. Morphological and Molecular Features of Porcine Mesenchymal Stem Cells Derived from Different Types of Synovial Membrane, and Genetic Background of Cell Donors. Front Cell Dev Biol. 2020;8:8. doi: 10.3389/fcell.2020.601212
   PubMed Web of Science ®Google Scholar
• Ponsuksili S, Trakooljul N, Basavaraj S, et al. Epigenome-wide skeletal muscle DNA methylation profiles at the background of distinct metabolic types and ryanodine receptor variation in pigs. BMC Genomics. 2019;20(1):20. doi: 10.1186/s12864-019-5880-1
   PubMedGoogle Scholar
• Park Y, Wu H. Differential methylation analysis for BS-seq data under general experimental design. Bioinformatics. 2016;32(10):1446–1453. doi: 10.1093/bioinformatics/btw026
   PubMed Web of Science ®Google Scholar
• Law CW, Zeglinski K, Dong X, et al. A guide to creating design matrices for gene expression experiments. F1000Res. 2020;9:1444. doi: 10.12688/f1000research.27893.1
   PubMedGoogle Scholar
• Wang Q, Li M, Wu T, et al. Exploring Epigenomic Datasets by ChIPseeker. Curr Protoc. 2022;2(10):e585. doi: 10.1002/cpz1.585
   PubMedGoogle Scholar
• Gu Z. Complex heatmap visualization. iMeta. 2022;1(3):e43. doi: 10.1002/imt2.43
   PubMedGoogle Scholar
• Ernst J, Bar-Joseph Z. STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics. 2006;7(1):191. doi: 10.1186/1471-2105-7-191
   PubMedGoogle Scholar
• Castro-Mondragon JA, Riudavets-Puig R, Rauluseviciute I, et al. JASPAR 2022: the 9th release of the open-access database of transcription factor binding profiles. Nucleic Acids Res. 2022;50(D1):D165–D73. doi: 10.1093/nar/gkab1113
   PubMed Web of Science ®Google Scholar
• Tan G, Lenhard B. TFBSTools: an R/bioconductor package for transcription factor binding site analysis. Bioinformatics. 2016;32(10):1555–1556. doi: 10.1093/bioinformatics/btw024
   PubMed Web of Science ®Google Scholar
• McLeay RC, Bailey TL. Motif enrichment analysis: a unified framework and an evaluation on ChIP data. BMC Bioinformatics. 2010;11(1):165. doi: 10.1186/1471-2105-11-165
   PubMedGoogle Scholar
• Suelves M, Carrio E, Nunez-Alvarez Y, et al. DNA methylation dynamics in cellular commitment and differentiation. Brief Funct Genomics. 2016;15:443–453. doi: 10.1093/bfgp/elw017
   PubMed Web of Science ®Google Scholar
• Laurent L, Wong E, Li G, et al. Dynamic changes in the human methylome during differentiation. Genome Res. 2010;20(3):320–331. doi: 10.1101/gr.101907.109
   PubMed Web of Science ®Google Scholar
• Farlik M, Halbritter F, Muller F, et al. DNA methylation dynamics of human hematopoietic stem cell differentiation. Cell Stem Cell. 2016;19(6):808–822. doi: 10.1016/j.stem.2016.10.019
   PubMed Web of Science ®Google Scholar
• Zhou GS, Zhang XL, Wu JP, et al. 5-Azacytidine facilitates osteogenic gene expression and differentiation of mesenchymal stem cells by alteration in DNA methylation. Cytotechnology. 2009;60(1–3):11. doi: 10.1007/s10616-009-9203-2
   PubMed Web of Science ®Google Scholar
• Yan X, Ehnert S, Culmes M. 5-azacytidine improves the osteogenic differentiation potential of aged human adipose-derived mesenchymal stem cells by DNA demethylation. PLOS ONE. 2014;9(3):e90846. doi: 10.1371/journal.pone.0090846
   PubMed Web of Science ®Google Scholar
• Liu Z, Chen T, Sun W, et al. DNA demethylation rescues the impaired osteogenic differentiation ability of human periodontal ligament stem cells in high glucose. Sci Rep. 2016;6(1):27447. doi: 10.1038/srep27447
   PubMedGoogle Scholar
• Mansour A, Mezour MA, Badran Z, et al. Extracellular Matrices for Bone Regeneration: A literature review. Tissue Eng Part A. 2017;23(23–24):1436–1451. doi: 10.1089/ten.TEA.2017.0026
   PubMed Web of Science ®Google Scholar
• Lee S, Kim JE, Seo HJ, et al. Design of fibronectin type III domains fused to an elastin-like polypeptide for the osteogenic differentiation of human mesenchymal stem cells. Acta Biochim Biophys Sin (Shanghai). 2019;51(8):856–863. doi: 10.1093/abbs/gmz063
   PubMed Web of Science ®Google Scholar
• Twine NA, Chen L, Pang CN, et al. Identification of differentiation-stage specific markers that define the ex vivo osteoblastic phenotype. Bone. 2014;67:23–32. doi: 10.1016/j.bone.2014.06.027
   PubMed Web of Science ®Google Scholar
• Wu M, Chen G, Li YP. TGF-β and BMP signaling in osteoblast, skeletal development, and bone formation, homeostasis and disease. Bone Res. 2016;4(1):16009. doi: 10.1038/boneres.2016.9
   PubMed Web of Science ®Google Scholar
• Grafe I, Alexander S, Peterson JR, et al. TGF-β Family signaling in mesenchymal differentiation. Cold Spring Harb Perspect Biol. 2018;10(5):10. doi: 10.1101/cshperspect.a022202
   Web of Science ®Google Scholar
• Serpe M, Umulis D, Ralston A, et al. The BMP-binding protein Crossveinless 2 is a short-range, concentration-dependent, biphasic modulator of BMP signaling in Drosophila. Dev Cell. 2008;14(6):940–953. doi: 10.1016/j.devcel.2008.03.023
   PubMed Web of Science ®Google Scholar
• Satomi-Kobayashi S, Kinugasa M, Kobayashi R, et al. Osteoblast-like differentiation of cultured human coronary artery smooth muscle cells by bone morphogenetic protein endothelial cell precursor-derived regulator (BMPER). J Biol Chem. 2012;287(36):30336–30345. doi: 10.1074/jbc.M111.329110
   PubMed Web of Science ®Google Scholar
• He W, Chen L, Huang Y, et al. Synergistic effects of recombinant Lentiviral-mediated BMP2 and TGF-beta3 on the osteogenic differentiation of rat bone marrow mesenchymal stem cells in vitro. Cytokine. 2019;120:1–8. doi: 10.1016/j.cyto.2019.03.020
   PubMed Web of Science ®Google Scholar
• Yan X, Liao H, Cheng M, et al. Smad7 protein interacts with receptor-regulated smads (R-Smads) to inhibit transforming growth factor-β (TGF-β)/Smad signaling. J Biol Chem. 2016;291(1):382–392. doi: 10.1074/jbc.M115.694281
   PubMed Web of Science ®Google Scholar
• Yano M, Inoue Y, Tobimatsu T, et al. Smad7 inhibits differentiation and mineralization of mouse osteoblastic cells. Endocr J. 2012;59(8):653–662. doi: 10.1507/endocrj.ej12-0022
   PubMed Web of Science ®Google Scholar
• Vishal M, Vimalraj S, Ajeetha R, et al. MicroRNA-590-5p Stabilizes Runx2 by Targeting Smad7 During Osteoblast Differentiation. J Cell Physiol. 2017;232(2):371–380. doi: 10.1002/jcp.25434
   PubMed Web of Science ®Google Scholar
• Estrada KD, Wang W, Retting KN, et al. Smad7 regulates terminal maturation of chondrocytes in the growth plate. Dev Biol. 2013;382(2):375–384. doi: 10.1016/j.ydbio.2013.08.021
   PubMed Web of Science ®Google Scholar
• Xiao P, Zhu Z, Du C, et al. Silencing Smad7 potentiates BMP2-induced chondrogenic differentiation and inhibits endochondral ossification in human synovial-derived mesenchymal stromal cells. Stem Cell Res Ther. 2021;12(1):132. doi: 10.1186/s13287-021-02202-2
   PubMed Web of Science ®Google Scholar
• Wegscheid ML, Anastasaki C, Hartigan KA, et al. Patient-derived iPSC-cerebral organoid modeling of the 17q11.2 microdeletion syndrome establishes CRLF3 as a critical regulator of neurogenesis. Cell Rep. 2021;36(1):109315. doi: 10.1016/j.celrep.2021.109315
   PubMed Web of Science ®Google Scholar
• Zhou CC, Xiong QC, Zhu XX, et al. AFF1 and AFF4 differentially regulate the osteogenic differentiation of human MSCs. Bone Res. 2017;5(1):17044. doi: 10.1038/boneres.2017.44
   PubMedGoogle Scholar
• Ambrogini E, Almeida M, Martin-Millan M, et al. FoxO-mediated defense against oxidative stress in osteoblasts is indispensable for skeletal homeostasis in mice. Cell Metab. 2010;11(2):136–146. doi: 10.1016/j.cmet.2009.12.009
   PubMed Web of Science ®Google Scholar
• Moriishi T, Fukuyama R, Miyazaki T, et al. Overexpression of BCLXL in osteoblasts inhibits osteoblast apoptosis and increases bone volume and strength. J Bone Miner Res. 2016;31(7):1366–1380. doi: 10.1002/jbmr.2808
   PubMed Web of Science ®Google Scholar
• Pasumarthy KK, Doni Jayavelu N, Kilpinen L, et al. Methylome analysis of human bone marrow MSCs reveals extensive age- and culture-induced changes at distal regulatory elements. Stem Cell Reports. 2017;9(3):999–1015. doi: 10.1016/j.stemcr.2017.07.018
   PubMed Web of Science ®Google Scholar
• Xie S, Choudhari S, Wu CL, et al. Aging and obesity prime the methylome and transcriptome of adipose stem cells for disease and dysfunction. Faseb J. 2023;37(3):e22785. doi: 10.1096/fj.202201413R
   PubMed Web of Science ®Google Scholar
• Yang Y, Zhou R, Mu Y, et al. Genome-wide analysis of DNA methylation in obese, lean, and miniature pig breeds. Sci Rep. 2016;6(1):30160. doi: 10.1038/srep30160
   PubMedGoogle Scholar
• Yi G, Liu L, Yao Y, et al. Multi-omics analysis reveals signatures of selection and loci associated with complex traits in pigs. bioRxiv. doi: 10.1101/2023.09.19.558553
   Google Scholar
• Pan JX, Xiong L, Zhao K, et al. YAP promotes osteogenesis and suppresses adipogenic differentiation by regulating β-catenin signaling. Bone Res. 2018;6(1):18. doi: 10.1038/s41413-018-0018-7
   PubMedGoogle Scholar
• Shah R, Spektor TM, Weisenberger DJ, et al. Reversal of dual epigenetic repression of non-canonical Wnt-5a normalises diabetic corneal epithelial wound healing and stem cells. Diabetologia. 2023;66(10):1943–1958. doi: 10.1007/s00125-023-05960-1
   PubMed Web of Science ®Google Scholar
• Hattersley AT. Prime suspect: the TCF7L2 gene and type 2 diabetes risk. J Clin Invest. 2007;117(8):2077–2079. doi: 10.1172/JCI33077
   PubMed Web of Science ®Google Scholar
• Du ZQ, Fan B, Zhao X, et al. Association analyses between type 2 diabetes genes and obesity traits in pigs. Obesity (Silver Spring). 2009;17(2):323–329. doi: 10.1038/oby.2008.557
   PubMed Web of Science ®Google Scholar
• Maeda K, Kobayashi Y, Udagawa N, et al. Wnt5a-Ror2 signaling between osteoblast-lineage cells and osteoclast precursors enhances osteoclastogenesis. Nat Med. 2012;18(3):405–412. doi: 10.1038/nm.2653
   PubMed Web of Science ®Google Scholar
• Mohan S, Kesavan C. T-cell factor 7L2 is a novel regulator of osteoblast functions that acts in part by modulation of hypoxia signaling. Am J Physiol Endocrinol Metab. 2022;322(6):E528–E39. doi: 10.1152/ajpendo.00035.2022
   PubMed Web of Science ®Google Scholar
• Kaluscha S, Domcke S, Wirbelauer C, et al. Evidence that direct inhibition of transcription factor binding is the prevailing mode of gene and repeat repression by DNA methylation. Nat Genet. 2022;54(12):1895–1906. doi: 10.1038/s41588-022-01241-6
   PubMed Web of Science ®Google Scholar
• Abe M, Saeki N, Ikeda Y, et al. Kruppel-like Factors in Skeletal Physiology and Pathologies. Int J Mol Sci. 2022;23(23):15174. doi: 10.3390/ijms232315174
   PubMed Web of Science ®Google Scholar
• Zakeri S, Aminian H, Sadeghi S, et al. Kruppel-like factors in bone biology. Cell Signal. 2022;93:110308. doi: 10.1016/j.cellsig.2022.110308
   PubMed Web of Science ®Google Scholar
• Shinoda Y, Ogata N, Higashikawa A, et al. Krüppel-like factor 5 causes cartilage degradation through transactivation of matrix metalloproteinase 9. J Biol Chem. 2008;283(36):24682–24689. doi: 10.1074/jbc.M709857200
   PubMed Web of Science ®Google Scholar
• Wangzhou K, Lai Z, Lu Z, et al. MiR-143-3p Inhibits osteogenic differentiation of human periodontal ligament cells by targeting KLF5 and inactivating the Wnt/beta-catenin pathway. Front Physiol. 2020;11:606967. doi: 10.3389/fphys.2020.606967
   PubMed Web of Science ®Google Scholar
• Lee HL, Bae OY, Baek KH, et al. High extracellular calcium-induced NFATc3 regulates the expression of receptor activator of NF-κB ligand in osteoblasts. Bone. 2011;49(2):242–249. doi: 10.1016/j.bone.2011.04.006
   PubMed Web of Science ®Google Scholar