Disturbance of calcium homeostasis and myogenesis caused by TET2 deletion in muscle stem cells

Zhang, Haoyuan; Wang, Sheng; Zhou, Qiangwei; Liao, Yinlong; Luo, Wenjing; Peng, Zhelun; Ren, Ruimin; Wang, Heng

doi:10.1038/s41420-022-01041-1

Cited by 15 publications

(9 citation statements)

References 74 publications

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“…Apart from this, several genes related to methylation modification were identified [ 28 , 29 ], among which Tet methylcytosine dioxygenase 2 ( TET2 ) was significantly up-regulated in E14 PGCs of You chicken and Hy-Line chicken. Several studies have shown that TET2 controls meiosis by regulating meiotic gene expression and plays multiple roles during meiosis and oocyte development [ 30 ].…”

Section: Resultsmentioning

confidence: 99%

The Synchronized Progression from Mitosis to Meiosis in Female Primordial Germ Cells between Layers and Broilers

Zhang

et al. 2023

Genes

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Layer and broiler hens show a dramatic difference in the volume and frequency of egg production. However, it is unclear whether the intrinsic competency of oocyte generation is also different between the two types of chicken. All oocytes were derived from the primordial germ cells (PGC) in the developing embryo, and female PGC proliferation (mitosis) and the subsequent differentiation (meiosis) determine the ultimate ovarian pool of germ cells available for future ovulation. In this study, we systematically compared the cellular phenotype and gene expression patterns during PGC mitosis (embryonic day 10, E10) and meiosis (E14) between female layers and broilers to determine whether the early germ cell development is also subjected to the selective breeding of egg production traits. We found that PGCs from E10 showed much higher activity in cell propagation and were enriched in cell proliferation signaling pathways than PGCs from E14 in both types of chicken. A common set of genes, namely insulin-like growth factor 2 (IGF2) and E2F transcription factor 4 (E2F4), were identified as the major regulators of cell proliferation in E10 PGCs of both strains. In addition, we found that E14 PGCs from both strains showed an equal ability to initiate meiosis, which was associated with the upregulation of key genes for meiotic initiation. The intrinsic cellular dynamics during the transition from proliferation to differentiation of female germ cells were conserved between layers and broilers. Hence, we surmise that other non-cell autonomous mechanisms involved in germ-somatic cell interactions would contribute to the divergence of egg production performance between layers and broilers.

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Section: Resultsmentioning

confidence: 99%

The Synchronized Progression from Mitosis to Meiosis in Female Primordial Germ Cells between Layers and Broilers

Zhang

et al. 2023

Genes

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“…To this end, we took advantage of the observation that it is the TET2 and TET3 proteins that mediate the biochemical conversion of methylcytosine to hydroxymethylcytosine, the first step in the demethylation process that takes place during tissue development ( 20 ). While previous experiments employing TET2 deletions had already indicated that demethylation plays a role in muscle formation ( 21 , 22 ), we designed a more targeted approach which enabled us to examine injury-induced regeneration, specifically. 12-wk-old mice homozygous for Tet2/3 fl/fl and carrying an inducible Pax7-Cre construct ( 23 ), as well as the tdTomato gene inserted into the Rosa26 locus, were given tamoxifen 5 d prior to injury in order to activate Cre, leading to the deletion of Tet2/3 , as well as the expression of tdTomato ( SI Appendix , Fig.…”

Section: Resultsmentioning

confidence: 99%

Muscle injury causes long-term changes in stem-cell DNA methylation

Michaeli

Sabag

Fok

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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Injury to muscle brings about the activation of stem cells, which then generate new myocytes to replace damaged tissue. We demonstrate that this activation is accompanied by a dramatic change in the stem-cell methylation pattern that prepares them epigenetically for terminal myocyte differentiation. These de- and de novo methylation events occur at regulatory elements associated with genes involved in myogenesis and are necessary for activation and regeneration. Local injury of one muscle elicits an almost identical epigenetic change in satellite cells from other muscles in the body, in a process mediated by circulating factors. Furthermore, this same methylation state is also generated in muscle stem cells (MuSCs) of female animals following pregnancy, even in the absence of any injury. Unlike the activation-induced expression changes, which are transient, the induced methylation profile is stably maintained in resident MuSCs and thus represents a molecular memory of previous physiological events that is probably programmed to provide a mechanism for long-term adaptation.

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“…DNA methylation-related enzymes such as DNMTs and TETs can regulate DNA methylation and demethylation ( Li and Zhang, 2014 ; Zhang et al, 2022 ). Many reports have shown that exposure to PM 2.5 can generate oxidative stress, which inhibits the function of DNMTs, leading to global hypomethylation and even cancer ( Franco et al, 2008 ).…”

Section: Discussionmentioning

confidence: 99%

Nrf2−/− regulated lung DNA demethylation and CYP2E1 DNA methylation under PM2.5 exposure

Jiang

Ding

et al. 2023

Front. Genet.

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Cytochrome P450 (CYP450) can mediate fine particulate matter (PM2.5) exposure leading to lung injury. Nuclear factor E2-related factor 2 (Nrf2) can regulate CYP450 expression; however, the mechanism by which Nrf2−/− (KO) regulates CYP450 expression via methylation of its promoter after PM2.5 exposure remains unclear. Here, Nrf2−/− (KO) mice and wild-type (WT) were placed in a PM2.5 exposure chamber (PM) or a filtered air chamber (FA) for 12 weeks using the real-ambient exposure system. The CYP2E1 expression trends were opposite between the WT and KO mice following PM2.5 exposure. After exposure to PM2.5,CYP2E1 mRNA and protein levels were increased in WT mice but decreased in KO mice, and CYP1A1 expression was increased after exposure to PM2.5 in both WT and KO mice. CYP2S1 expression decreased after exposure to PM2.5 in both the WT and KO groups. We studied the effect of PM2.5 exposure on CYP450 promoter methylation and global methylation levels in WT and KO mice. In WT and KO mice in the PM2.5 exposure chamber, among the methylation sites examined in the CYP2E1 promoter, the CpG2 methylation level showed an opposite trend with CYP2E1 mRNA expression. The same relationship was evident between CpG3 unit methylation in the CYP1A1 promoter and CYP1A1 mRNA expression, and between CpG1 unit methylation in the CYP2S1 promoter and CYP2S1 mRNA expression. This data suggests that methylation of these CpG units regulates the expression of the corresponding gene. After exposure to PM2.5, the expression of the DNA methylation markers ten-eleven translocation 3 (TET3) and 5-hydroxymethylcytosine (5hmC) was decreased in the WT group but significantly increased in the KO group. In summary, the changes in CYP2E1, CYP1A1, and CYP2S1 expression in the PM2.5 exposure chamber of WT and Nrf2−/− mice might be related to the specific methylation patterns in their promoter CpG units. After exposure to PM2.5, Nrf2 might regulate CYP2E1 expression by affecting CpG2 unit methylation and induce DNA demethylation via TET3 expression. Our study revealed the underlying mechanism for Nrf2 to regulate epigenetics after lung exposure to PM2.5.

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Disturbance of calcium homeostasis and myogenesis caused by TET2 deletion in muscle stem cells

Cited by 15 publications

References 74 publications

The Synchronized Progression from Mitosis to Meiosis in Female Primordial Germ Cells between Layers and Broilers

The Synchronized Progression from Mitosis to Meiosis in Female Primordial Germ Cells between Layers and Broilers

Muscle injury causes long-term changes in stem-cell DNA methylation

Nrf2−/− regulated lung DNA demethylation and CYP2E1 DNA methylation under PM2.5 exposure

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