De novo DNA methylation during monkey pre-implantation embryogenesis

Gao, Fei; Niu, Yuyu; Sun, Yi; Lu, Hanlin; Chen, Yongchang; Li, Siguang; Kang, Yu; Luo, Yuan; Si, Chenyang; Yu, Juehua; Chang, Li; Sun, Nianqin; Si, Wei; Wang, Hong; Ji, Weizhi; Tan, Tao

doi:10.1038/cr.2017.25

Cited by 48 publications

(47 citation statements)

References 32 publications

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“…To validate previously identified maternally methylated imprinted gDMRs (igDMRs) 21–24 , we interrogated DNAme profiles from published whole genome bisulfite sequencing data from gametes, placenta and somatic tissues ( Supplementary Table 1 ) 56 . Specifically, we identified regions that are hypermethylated (> 70% DNAme) in oocytes, hypomethylated (< 30% DNAme) in sperm, retain DNAme (>25%) in the blastocyst, and show 35-65% DNAme in placenta (purified first-trimester cytotrophoblast; CT) or at least one adult somatic tissue 4,5,7,8,18,19,29,40,41,44,47,49,57–69 . We further validated and refined this list by only including gDMRs harboring either reported maternal, monoallelic or bimodal DNAme in the placenta and/or at least one somatic tissue.…”

Section: Methodsmentioning

confidence: 99%

“…To assess the conservation of LITs and DNA methylation of associated gDMRs in macaque oocytes, we analyzed published RNA-sequencing 40 and genome wide DNA methylome data 41 . As expected from the phylogeny of LTR12C elements, no LITs overlapping the region orthologous to the human igDMRs at the ST8SIA1 , SCIN , or COL26A1 loci were detected in macaque oocytes, and their CGIs remain hypomethylated ( Fig.…”

Section: Conservation Of Ltrs Lits and Igdmrs In Apes Versus Old Wormentioning

confidence: 99%

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Evolution of imprinting via lineage-specific insertion of retroviral promoters

Bogutz

Brind’Amour

Kobayashi

et al. 2019

Preprint

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26Imprinted genes are expressed from a single parental allele. In mammals, this unusual mode of 27 transcription generally depends on the epigenetic silencing of one allele by DNA methylation 28 (DNAme) established in the germline. While many species-specific imprinted orthologues have been 29 documented in eutherians, the molecular mechanisms underlying the evolutionary switch from biallelic 30 to imprinted expression are currently unknown. During mouse oogenesis, gametic differentially 31 methylated regions (gDMRs) acquire DNAme in a process guided by transcription. Here we show that 32 transcription initiating in proximal lineage-specific endogenous retroviruses (ERVs) is likely 33 responsible for DNAme established in oocytes at 4/6 mouse-specific and 17/110 human-specific 34 maternal imprinted gDMRs (igDMRs). The latter can be further divided into Catarrhini (Old World 35 monkeys and apes)-or Hominoidea (ape)-specific igDMRs, which are embedded within transcription 36 units initiating in ERVs specific to these primate lineages. Using CRISPR-Cas9 mutagenesis, we 37 deleted the relevant murine-specific ERVs upstream of the maternally methylated genes Impact and 38Slc38a4. Strikingly, imprinting at these genes was lost in the offspring of females harboring these 39 deletions and biallelic expression was observed. Our work reveals a novel evolutionary mechanism 40 whereby maternally silenced genes arise from biallelically expressed progenitors. 41 42 43 During postnatal oocyte growth in mammals, transcribed genomic regions acquire two characteristic 44 epigenetic marks: transcription-coupled trimethylation at lysine 36 of histone H3 (H3K36me3) 1 and 45 DNAme 2-5 . In both human and mouse female germline, the overall levels of CpG methylation increase 46 from less than 5% in post-migratory primordial germ cells (PGCs) to ~40-50% in fully-grown, 47 germinal vesicle oocytes (GVOs) 4,6-8 Kobayashi:2013ia}. In growing murine oocytes, 85-90% of this 48 DNAme is deposited over H3K36me3-marked transcribed regions of the genome 3 . Notably, we 49 recently demonstrated that SETD2-dependent deposition of H3K36me3 is required for de novo 50 3 DNAme of transcribed gene bodies in mouse oocytes 9 . Such transcription-coupled de novo DNAme is 51 also responsible for the establishment of regions of differential DNAme between the mature gametes 52 (gametic differentially methylated regions, gDMRs), a subset of which are maintained throughout 53 preimplantation development. This unique class of gDMRs, the imprinted gDMRs (igDMRs), can 54 direct imprinted paternal allele-specific expression of the gene(s) under their regulation, the imprinted 55 genes 3,10,11 . Importantly, transcription initiating within upstream oocyte-specific promoters has been 56 reported to play a critical role in de novo DNAme at the maternal igDMRs of a number of mouse 57 imprinted genes 3,12-16 , but the evolutionary origin of such promoters remains unexplored. 58 59 Specific families of ERVs, also known as long terminal repeat (LTR) retrotransposons, are 6...

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Section: Methodsmentioning

confidence: 99%

Section: Conservation Of Ltrs Lits and Igdmrs In Apes Versus Old Wormentioning

confidence: 99%

Evolution of imprinting via lineage-specific insertion of retroviral promoters

Bogutz

Brind’Amour

Kobayashi

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…It is required in normal developmental processes and when appearing on the gene promoter region, it predominantly functions to repress gene transcription . During the embryonic stage, DNA methylation patterns undergo varying phases through which remethylation and demethylation processes occur . This dynamic process is distinctly coordinated in order to switch on/off genes that may or may not be required for various developmental stages.…”

Section: Epigenetics In Fetal Programmingmentioning

confidence: 99%

In Utero One‐Carbon Metabolism Interplay and Metabolic Syndrome in Cardiovascular Disease Risk Reduction

Mabasa

Samodien

Sangweni

et al. 2019

Molecular Nutrition Food Res

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The maternal obesogenic environment plays a role in programing the susceptibility of the fetus to postnatal non‐alcoholic fatty liver disease (NAFLD), a risk factor for cardiovascular disease (CVD). NAFLD is a multisystem disease that is characterized by hepatic fat accumulation due in part to dysregulated energy metabolism network through epigenetic mechanisms such as DNA methylation. DNA methylation affects fetal programing and disease risk via regulation of gene transcription; it is affected by methyl donor nutrients such as vitamin B12, methionine, folic acid, vitamin B6, and choline. Although several studies have documented the role of several maternal methyl donor nutrients on obesity‐induced NAFLD in offspring, currently, data are lacking on its impact on CVD risk as an endpoint. The aim of this paper is to use current knowledge to construct a postulation for the potential role of a comprehensive gestational methyl donor nutrients supplementary approach on the susceptibility of offspring to developing metabolic‐syndrome‐related cardiovascular complications.

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“…Rhesus macaques are for instance frequently used for the development of vaccines against viral diseases, including Sars-CoV-2, HIV, Influenza and Ebola virus [22][23][24]. They are also widely used in various studies ranging from development and imprinting, to addiction and social cognition [25][26][27][28][29][30]. In parallel, the Chlorocebus genus, among which figure prominently African green monkeys (AGM), have been a gold standard model for the studies and fight against several infectious diseases, such as yellow fever, trypanosoma and plague in the past [31,32].…”

mentioning

confidence: 99%

Analysis and annotation of genome-wide DNA methylation patterns in two nonhuman primate species using the Infinium Human Methylation 450K and EPIC BeadChips

Pichon

Busato

Jochems

et al. 2020

Preprint

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The Infinium Human Methylation450 and Methylation EPIC BeadChips are useful tools for the study of the methylation state of hundreds of thousands of CpG across the human genome at affordable cost. However, in a wide range of experimental settings in particular for studies in infectious or brain-related diseases, human samples cannot be easily obtained. Hence, due to their close developmental, immunological and neurological proximity with humans, nonhuman primates are used in many research fields of human diseases and for preclinical research. Few studies have used DNA methylation microarrays in simian models. Microarrays designed for the analysis of DNA methylation patterns in the human genome could be useful given the genomic proximity between human and nonhuman primates. However, there is currently information lacking about the specificity and usability of each probe for many nonhuman primate species, including rhesus macaques (Macaca mulatta), originating from Asia, and African green monkeys originating from West-Africa (Chlorocebus sabaeus).Rhesus macaques and African green monkeys are among the major nonhuman primate models utilized in biomedical research. Here, we provide a precise evaluation and reannotation of the probes of the two microarrays for the analysis of genome-wide DNA methylation patterns in these two Cercopithecidae species. We demonstrate that up to 162,000 of the 450K and 255,000 probes of the EPIC BeadChip can be reliably used in Macaca mulatta or Chlorocebus sabaeus. The annotation files are provided in a format compatible with a variety of preprocessing, normalization and analytical pipelines designed for data analysis from 450K/EPIC arrays, facilitating high-throughput DNA methylation analyses in Macaca mulatta and Chlorocebus sabaeus. They provide the opportunity to the research community to focus their analysis only on those probes identified as reliable. The described analytical workflow leaves the choice to the user to balance coverage versus specificity and can also be applied to other Cercopithecidae species.

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De novo DNA methylation during monkey pre-implantation embryogenesis

Cited by 48 publications

References 32 publications

Evolution of imprinting via lineage-specific insertion of retroviral promoters

Evolution of imprinting via lineage-specific insertion of retroviral promoters

In Utero One‐Carbon Metabolism Interplay and Metabolic Syndrome in Cardiovascular Disease Risk Reduction

Analysis and annotation of genome-wide DNA methylation patterns in two nonhuman primate species using the Infinium Human Methylation 450K and EPIC BeadChips

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