DNA methylation-mediated expression of zinc finger protein 615 affects embryonic development in Bombyx mori

Xu, Guanfeng; Gong, Chengcheng; Tian, Yuan; Fu, Tong-Yu; Lin, Yi-Guang; Liu, Hao; Peng, Yuling; Tong, Chunmei; Feng, Qili; Song, Qisheng; Zheng, Sichun

doi:10.24272/j.issn.2095-8137.2022.4.dwxyj202204007

Cited by 6 publications

(32 citation statements)

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“…In insects, DNA methylation mainly modifies gene bodies to enhance gene expression, including ZnF 615 expression (Xu et al. , 2022b). Although we do not know whether intragenic DNA methylation and transcription factors synergistically regulate ZnF 615 expression, in this study, we demonstrated that ZnF 615 expression was enhanced by high expression of Dnmt1 and Hox A1‐like in ovaries and embryos (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Our previous work showed that DNA methylation enhances ZnF 615 expression in B. mori embryos and ovaries (Xu et al, 2022b). To investigate whether Hox A1-like enhances ZnF 615 expression in embryos and ovaries, similar to DNA methylation, the expression patterns of both genes during embryonic development and in different tissues of pupae were determined.…”

Section: Hox A1-like and Dna Methylation Enhance Znf 615 Gene Expressionmentioning

confidence: 99%

“…Previous work demonstrated that knockout of ZnF 615 suppresses ovarian development and embryogenesis in B. mori (Xu et al, 2022b). To confirm that Hox A1-like can also affect the development of B. mori ovaries and embryos by regulating the expression of ZnF 615, the Hox A1-like gene was knocked out using the CRISPR/Cas9 technique.…”

Section: Knockout Of Hox A1-like Expression Suppresses B Mori Ovarian...mentioning

confidence: 99%

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Homeobox protein A1‐like and DNA methylation regulate embryo‐specific Zinc finger protein 615 gene expression and embryonic development in the silkworm Bombyx mori

Tian

Zhong

et al. 2023

Insect Science

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DNA methylation and transcription factors play roles in gene expression and animal development. In insects, DNA methylation modifies gene bodies, but how DNA methylation and transcription factors regulate gene expression is unclear. In this study, we investigated the mechanism that regulates the expression of Bombyx mori Zinc finger protein 615 (ZnF 615), which is a downstream gene of DNA methyltransferase 1 (Dnmt1), and its effects on the regulation of embryonic development. By progressively truncating the ZnF 615 promoter, it was found that the −223 and −190 nt region, which contains homeobox (Hox) protein cis-regulatory elements (CREs), had the greatest impact on the transcription of ZnF 615. RNA interference (RNAi)-mediated knockdown and overexpression of Hox family genes showed that Hox A1-like can enhance the messenger RNA level of ZnF 615. Further studies showed that Hox A1-like regulates ZnF 615 expression by directly binding to the −223 and −190 nt region of its promoter. Simultaneous RNAimediated knockdown or overexpression of Hox A1-like and Dnmt1 significantly inhibited or enhanced the regulatory effect of either gene alone on ZnF 615 expression, suggesting that both DNA methylation of gene bodies and binding of transcription factors to promoters are essential for gene expression. RNAi-mediated knockdown of Hox A1-like and Dnmt1 showed that the embryonic development was retarded and the hatching rate was decreased. Taken together, these data suggest that Hox A1-like and DNA methylation enhance the expression of ZnF 615, thereby affecting the development of B. mori embryos.

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Section: Discussionmentioning

confidence: 99%

Section: Hox A1-like and Dna Methylation Enhance Znf 615 Gene Expressionmentioning

confidence: 99%

Section: Knockout Of Hox A1-like Expression Suppresses B Mori Ovarian...mentioning

confidence: 99%

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Homeobox protein A1‐like and DNA methylation regulate embryo‐specific Zinc finger protein 615 gene expression and embryonic development in the silkworm Bombyx mori

Tian

Zhong

et al. 2023

Insect Science

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“…Major changes in the rate and distribution of DNA methylation occur at the invertebrate-vertebrate boundary (Bird, 1995;Tweedie et al, 1997). For example, in insects, including Bombyx mori (Xu et al, 2021;2022a), Apis mellifera (Lyko et al, 2010), Tribolium castaneum (Zemach et al, 2010), Schistocerka gregaria (Falckenhayn et al, 2013), Polistes canadensis (Taguchi, 2018), Camponotus floridanus and Harpegnathos saltator (Bonasio et al, 2012), and Nasonia vit-ripennis (Beeler et al, 2014), the methylation rates of CG-associated cytosines range from 0.1% to 3.2%, which could be the reason that various MBD proteins are absent in invertebrates. In insects, there is only 1 MBD family protein, MBD2/3, which is homologous to mammalian MBD2 and MBD3; thus, MBD2/3 is also considered to be the original protein of the vertebrate MBD family (Hendrich & Tweedie, 2003).…”

Section: Introductionmentioning

confidence: 99%

Methyl‐CpG binding domain (MBD)2/3 specifically recognizes and binds to the genomic mCpG site with a β‐sheet in the MBD to affect embryonic development in Bombyx mori

Tian

et al. 2023

Insect Science

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Methyl‐CpG (mCpG) binding domain (MBD) proteins especially bind with methylated DNA, and are involved in many important biological processes; however, the binding mechanism between insect MBD2/3 and mCpG remains unclear. In this study, we identified 2 isoforms of the MBD2/3 gene in Bombyx mori, MBD2/3‐S and MBD2/3‐L. Binding analysis of MBD2/3‐L, MBD2/3‐S, and 7 mutant MBD2/3‐L proteins deficient in β1−β6 or α1 in the MBD showed that β2−β3‐turns in the β‐sheet of the MBD are necessary for the formation of the MBD2/3–mCpG complex; furthermore, other secondary structures, namely, β4−β6 and an α‐helix, play a role in stabilizing the β‐sheet structure to ensure that the MBD is able to bind mCpG. In addition, sequence alignment and binding analyses of different insect MBD2/3s indicated that insect MBD2/3s have an intact and conserved MBD that binds to the mCpG of target genes. Furthermore, MBD2/3 RNA interference results showed that MBD2/3‐L plays a role in regulating B. mori embryonic development, similar to that of DNA methylation; however, MBD2/3‐S without β4−β6 and α‐helix does not alter embryonic development. These results suggest that MBD2/3‐L recognizes and binds to mCpG through the intact β‐sheet structure in its MBD, thus ensuring silkworm embryonic development.

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“…The silkworm is a good model for studying the relationship between m6A methylation and embryonic development, including insect diapause. Previous studies have suggested that DNA methylation plays an important role in diapause initiation and termination during silkworm embryonic development (Li et al, 2019a) and ensure ovarian and embryonic development (Xu et al, 2022). However, the mechanism of m6A methylation in RNA during silkworm embryonic development is not clear.…”

Section: Introductionmentioning

confidence: 99%

RNA methyltransferase BmMettl3 and BmMettl14 in silkworm (Bombyx mori) and the regulation of silkworm embryonic development

Huang

et al. 2023

Arch Insect Biochem Physiol

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N6-methyladenosine (m6A) is a ubiquitous reversible epigenetic RNA modification that plays an important role in regulating many biological processes, especially embryonic development. However, regulation of m6A methylation during silkworm embryonic development and diapause remains to be investigated. In this study, we analyzed the phylogeny of subunits of methyltransferases BmMettl3 and BmMettl14, and detected the expression patterns of BmMettl3 and BmMettl14 in different tissues and at different developmental stages in silkworm. To investigate the function of m6A on the development of silkworm embryo, we analyzed the m6A/A ratio in diapause and diapause termination eggs. The results showed that BmMettl3 and BmMettl14 were highly expressed in gonads and eggs. Moreover, the expression of BmMettl3 and BmMettl14 and the m6A/A ratio were significantly increased in diapause termination eggs compared with diapause eggs in the early stage of silkworm embryonic development. Furthermore, in BmN cell cycle experiments, the percentage of cells in the S phase increased when lacking BmMettl3 or BmMettl14. This work contributes to understanding the role of m6A methylation during insect embryogenesis and gametogenesis. It also provides a research

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DNA methylation-mediated expression of zinc finger protein 615 affects embryonic development in Bombyx mori

Cited by 6 publications

References 0 publications

Homeobox protein A1‐like and DNA methylation regulate embryo‐specific Zinc finger protein 615 gene expression and embryonic development in the silkworm Bombyx mori

Homeobox protein A1‐like and DNA methylation regulate embryo‐specific Zinc finger protein 615 gene expression and embryonic development in the silkworm Bombyx mori

Methyl‐CpG binding domain (MBD)2/3 specifically recognizes and binds to the genomic mCpG site with a β‐sheet in the MBD to affect embryonic development in Bombyx mori

RNA methyltransferase BmMettl3 and BmMettl14 in silkworm (Bombyx mori) and the regulation of silkworm embryonic development

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