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

Mesenchymal stem cells (MSCs), with the ability to differentiate into osteoblasts, adipocytes, or chondrocytes, show evidence that the donor cell’s metabolic type influences the osteogenic process. Limited knowledge exists on DNA methylation changes during osteogenic differentiation and the impact o...

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Main Authors: Shuaichen Li, Puntita Siengdee, Frieder Hadlich, Nares Trakooljul, Michael Oster, Henry Reyer, Klaus Wimmers, Siriluck Ponsuksili
Format: Article
Language:English
Published: Taylor & Francis Group 2024-12-01
Series:Epigenetics
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Online Access:https://www.tandfonline.com/doi/10.1080/15592294.2024.2375011
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author Shuaichen Li
Puntita Siengdee
Frieder Hadlich
Nares Trakooljul
Michael Oster
Henry Reyer
Klaus Wimmers
Siriluck Ponsuksili
author_facet Shuaichen Li
Puntita Siengdee
Frieder Hadlich
Nares Trakooljul
Michael Oster
Henry Reyer
Klaus Wimmers
Siriluck Ponsuksili
author_sort Shuaichen Li
collection DOAJ
description Mesenchymal stem cells (MSCs), with the ability to differentiate into osteoblasts, adipocytes, or chondrocytes, show evidence that the donor cell’s metabolic type influences the osteogenic process. Limited knowledge exists on DNA methylation changes during osteogenic differentiation and the impact of diverse donor genetic backgrounds on MSC differentiation. In this study, synovial membrane mesenchymal stem cells (SMSCs) from two pig breeds (Angeln Saddleback, AS; German Landrace, DL) with distinct metabolic phenotypes were isolated, and the methylation pattern of SMSCs during osteogenic induction was investigated. Results showed that most differentially methylated regions (DMRs) were hypomethylated in osteogenic-induced SMSC group. These DMRs were enriched with genes of different osteogenic signalling pathways at different time points including Wnt, ECM, TGFB and BMP signalling pathways. AS pigs consistently exhibited a higher number of hypermethylated DMRs than DL pigs, particularly during the peak of osteogenesis (day 21). Predicting transcription factor motifs in regions of DMRs linked to osteogenic processes and donor breeds revealed influential motifs, including KLF1, NFATC3, ZNF148, ASCL1, FOXI1, and KLF5. These findings contribute to understanding the pattern of methylation changes promoting osteogenic differentiation, emphasizing the substantial role of donor the metabolic type and epigenetic memory of different donors on SMSC differentiation.
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spelling doaj-art-88e9d7aa83b84518abb8fcba29664ea02025-08-20T02:20:49ZengTaylor & Francis GroupEpigenetics1559-22941559-23082024-12-0119110.1080/15592294.2024.2375011Dynamics of DNA methylation during osteogenic differentiation of porcine synovial membrane mesenchymal stem cells from two metabolically distinct breedsShuaichen Li0Puntita Siengdee1Frieder Hadlich2Nares Trakooljul3Michael Oster4Henry Reyer5Klaus Wimmers6Siriluck Ponsuksili7Institute of Genome Biology, Research Institute for Farm Animal Biology (FBN), Dummerstorf, GermanyInstitute of Genome Biology, Research Institute for Farm Animal Biology (FBN), Dummerstorf, GermanyInstitute of Genome Biology, Research Institute for Farm Animal Biology (FBN), Dummerstorf, GermanyInstitute of Genome Biology, Research Institute for Farm Animal Biology (FBN), Dummerstorf, GermanyInstitute of Genome Biology, Research Institute for Farm Animal Biology (FBN), Dummerstorf, GermanyInstitute of Genome Biology, Research Institute for Farm Animal Biology (FBN), Dummerstorf, GermanyInstitute of Genome Biology, Research Institute for Farm Animal Biology (FBN), Dummerstorf, GermanyInstitute of Genome Biology, Research Institute for Farm Animal Biology (FBN), Dummerstorf, GermanyMesenchymal stem cells (MSCs), with the ability to differentiate into osteoblasts, adipocytes, or chondrocytes, show evidence that the donor cell’s metabolic type influences the osteogenic process. Limited knowledge exists on DNA methylation changes during osteogenic differentiation and the impact of diverse donor genetic backgrounds on MSC differentiation. In this study, synovial membrane mesenchymal stem cells (SMSCs) from two pig breeds (Angeln Saddleback, AS; German Landrace, DL) with distinct metabolic phenotypes were isolated, and the methylation pattern of SMSCs during osteogenic induction was investigated. Results showed that most differentially methylated regions (DMRs) were hypomethylated in osteogenic-induced SMSC group. These DMRs were enriched with genes of different osteogenic signalling pathways at different time points including Wnt, ECM, TGFB and BMP signalling pathways. AS pigs consistently exhibited a higher number of hypermethylated DMRs than DL pigs, particularly during the peak of osteogenesis (day 21). Predicting transcription factor motifs in regions of DMRs linked to osteogenic processes and donor breeds revealed influential motifs, including KLF1, NFATC3, ZNF148, ASCL1, FOXI1, and KLF5. These findings contribute to understanding the pattern of methylation changes promoting osteogenic differentiation, emphasizing the substantial role of donor the metabolic type and epigenetic memory of different donors on SMSC differentiation.https://www.tandfonline.com/doi/10.1080/15592294.2024.2375011DNA methylationMesenchymal stem cellsOsteogenic differentiationPig breedsEpigenetic pattern
spellingShingle Shuaichen Li
Puntita Siengdee
Frieder Hadlich
Nares Trakooljul
Michael Oster
Henry Reyer
Klaus Wimmers
Siriluck Ponsuksili
Dynamics of DNA methylation during osteogenic differentiation of porcine synovial membrane mesenchymal stem cells from two metabolically distinct breeds
Epigenetics
DNA methylation
Mesenchymal stem cells
Osteogenic differentiation
Pig breeds
Epigenetic pattern
title Dynamics of DNA methylation during osteogenic differentiation of porcine synovial membrane mesenchymal stem cells from two metabolically distinct breeds
title_full Dynamics of DNA methylation during osteogenic differentiation of porcine synovial membrane mesenchymal stem cells from two metabolically distinct breeds
title_fullStr Dynamics of DNA methylation during osteogenic differentiation of porcine synovial membrane mesenchymal stem cells from two metabolically distinct breeds
title_full_unstemmed Dynamics of DNA methylation during osteogenic differentiation of porcine synovial membrane mesenchymal stem cells from two metabolically distinct breeds
title_short Dynamics of DNA methylation during osteogenic differentiation of porcine synovial membrane mesenchymal stem cells from two metabolically distinct breeds
title_sort dynamics of dna methylation during osteogenic differentiation of porcine synovial membrane mesenchymal stem cells from two metabolically distinct breeds
topic DNA methylation
Mesenchymal stem cells
Osteogenic differentiation
Pig breeds
Epigenetic pattern
url https://www.tandfonline.com/doi/10.1080/15592294.2024.2375011
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