Asymmetric Expression of LincGET Biases Cell Fate in Two-Cell Mouse Embryos

Wang, Jiaqiang; Wang, Leyun; Feng, Guihai; Wang, Yukai; Li, Yufei; Li, Xin; Liu, Chao; Jiao, Guanyi; Huang, Cheng; Shi, Junchao; Zhou, Tong; Chen, Qi; Z, Liu; Li, Wei; Zhou, Qi

doi:10.1016/j.cell.2018.11.039

Cited by 116 publications

(118 citation statements)

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“…However, we failed to identify either of these two features at TAD borders in X. tropicalis , which could also be caused by the heterogeneity in the cells we used. Recent work revealed that cells could be different at as early as two- to four-cell stages during mouse embryo development 51 . At s9, at least three lineages of cells already exist in X. tropicalis embryos.…”

Section: Discussionmentioning

confidence: 99%

Systematic Chromatin Architecture Analysis inXenopus tropicalisReveals Conserved Three-Dimensional Folding Principles of Vertebrate Genomes

Niu

Shen

Shi

et al. 2020

Preprint

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23Metazoan genomes are folded into 3D structures in interphase nuclei. 24 However, the molecular mechanism remains unknown. Here, we show that 25 topologically associating domains (TADs) form in two waves during Xenopus 26 tropicalis embryogenesis, first at zygotic genome activation and then as the 27 expression of CTCF and Rad21 is elevated. We also found TAD structures 28 continually change for at least three times during development. Surprisingly, 29 the directionality index is preferentially stronger on one side of TADs where 30 orientation-biased CTCF and Rad21 binding are observed, a conserved 31 pattern that is found in human cells as well. Depletion analysis revealed CTCF, 32 Rad21, and RPB1, a component of RNAPII, are required for the establishment 33 of TADs. Overall, our work shows that Xenopus is a powerful model for 34 chromosome architecture analysis. Furthermore, our findings indicate that 35 cohesin-mediated extrusion may anchor at orientation-biased CTCF binding 36 sites, supporting a CTCF-anchored extrusion model as the mechanism for 37 TAD establishment. 38 39 40 41 42 3 KEYWORDS 43 Hi-C, Topologically associating domain (TAD), CTCF, Orientation-biased 44 binding, Cohesin-mediated extrusion, Directionality, Zygotic genome activation 45 (ZGA), RNAPII, Xenopus tropicalis, Genome assembly 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 Interphase chromosomes are partitioned into topologically associating 65 domains (TADs) 1-4 which segregate into compartments of active or repressive 66 chromatins 5-7 . TAD structures are relatively stable and resilient to 67 environmental perturbations 8,9 . Chromosome architecture at the TAD level is 68 also evolutionarily conserved in eukaryotic species 4,10,11 . Disruption of TAD 69 borders leads to developmental disorders and even tumorigenesis, thus 70 underlining the importance of 3D genome organization in gene regulation 12-15 . 71 The establishment of chromatin architecture during embryogenesis provides 72 an initial spatial frame which may guide proper genome organization, 73 chromatin interaction and gene regulation in following development and 74 differentiation processes 16 . The timing of de novo TADs formation during 75 development has been examined in Drosophila, mouse, zebrafish, and 76 human 17-21 . TAD structures form at zygotic genome activation (ZGA) and 77 continually consolidate during early embryo development in fruit fly, mouse and 78 human 17,19-21 . However, in zebrafish, TADs already exist before ZGA and are 79 lost after ZGA before being reestablished in later developmental stages 18 . This 80 difference raises the question if the process of TAD formation is evolutionarily 81 conserved. 82 Cohesin complex-mediated DNA loop extrusion was recently reported in 83 several in vitro studies 22,23 and proposed as a functional mechanism 84 underlying TAD establishment 24-26 . In cultured cells, the deletion of cohesin 85 5 Rad21 alone is enough to abolish the establishment of TADs 27 . In addition, 86 CTCF, WAPL, and PDS5 proteins p...

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Section: Discussionmentioning

confidence: 99%

Systematic Chromatin Architecture Analysis inXenopus tropicalisReveals Conserved Three-Dimensional Folding Principles of Vertebrate Genomes

Niu

Shen

Shi

et al. 2020

Preprint

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“…To further define the transcriptome characteristics of the blastomeres, we performed UHC (19 813 genes) to group the cells from morula. It has been reported that blastomeres with high CARM1 bias the subsequent fate toward ICM, 21,22 revealing that the cells of morula 2 would be segregated into ICM. One group (morula 1; 13/30 cells) showed the expression of genes highly expressed in TE, such as DAB2 and TEAD4, indicating the group of cells has been determined into TE lineage.…”

Section: Icm and Te Precursors In Porcine Morulamentioning

confidence: 99%

Lineage specification and pluripotency revealed by transcriptome analysis from oocyte to blastocyst in pig

Kong

Zhang

et al. 2019

The FASEB Journal

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The inner cell mass (ICM) in blastocyst is the origin of all somatic and germ cells in mammals and pluripotent stem cells (PSCs) in vitro. As the conserved principles between pig and human, here we performed comprehensive single‐cell RNA‐seq for porcine early embryos from oocyte to early blastocyst (EB). We show the specification of the ICM and trophectoderm in morula and the molecular signature of the precursors. We demonstrate the existence of naïve pluripotency signature in morula and ICM of EB, and the specific pluripotent genes and the activity of signalling pathways highlight the characteristics of the naïve pluripotency. We observe the absence of dosage compensation with respect to X‐chromosome (XC) in morula, and incomplete dosage compensation in the EB. However, the dynamics of dosage compensation may be independent of the expression of XIST induced XC inactivation. Our study describes molecular landmarks of embryogenesis in pig that will provide a better strategy for derivation of porcine PSCs and improve research in regenerative medicine.

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“…LncRNAs can be located in the nucleus or cytoplasm, depending on the cell types and detection methods (Derrien et al, 2012; van Heesch et al, 2014). In oocytes or embryos, fluorescence in situ hybridization (FISH) showed that three lncRNAs were in the cytoplasm of bovine GV oocytes (Caballero et al, 2014), and lincGET was in the nucleus of two‐ to four‐cell mouse embryos (J. Wang et al, 2018). In the present study, we failed to position lncRNA2193 in porcine oocytes because the RNA probe synthesized for FISH could not work well.…”

Section: Discussionmentioning

confidence: 99%

Long noncoding RNA 2193 regulates meiosis through global epigenetic modification and cytoskeleton organization in pig oocytes

Yang

Wang

Liu

et al. 2020

Journal Cellular Physiology

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Long noncoding RNAs (lncRNAs) regulate a variety of physiological and pathological processes. However, the biological function of lncRNAs in mammalian germ cells remains largely unexplored. Here we identified one novel lncRNA (lncRNA2193) from single‐cell RNA sequencing performed on porcine oocytes and investigated its function in oocyte meiosis. During in vitro maturation (IVM), from germinal vesicle (GV, 0 hr), GV breakdown (GVBD, 24 hr), to metaphase II stage (MII, 44 hr), the transcriptional abundance of lncRNA2193 remained stable and high. LncRNA2193 interference by small interfering RNA microinjection into porcine GV oocytes could significantly inhibit rates of GVBD and the first polar body extrusion, but enhance the rates of oocytes with a nuclear abnormality. Moreover, lncRNA2193 knockdown disturbed cytoskeletal organization (F‐actin and spindle), and decreased DNA 5‐methylcytosine (5mC) and histone trimethylation (H3K4me3, H3K9me3, H3K27me3, and H3K36me3) levels. The lncRNA2193 downregulation induced a decrease of 5mC level could be partially due to the reduction of DNA methyltransferase 3A and 3B, and the elevation of 5mC‐hydroxylase ten‐11 translocation 2 (TET2). After parthenogenetic activation of MII oocytes, parthenotes exhibited higher fragmentation but lower cleavage rates in the lncRNA2193 downregulated group. However, lncRNA2193 interference performed on mature MII oocytes and parthenotes at 1‐cell stage did not affect the cleavage and blasctocyst rates of pathenotes. Taken together, lncRNA2193 plays an important role in porcine oocyte maturation, providing more insights for relevant investigations on mammalian germ cells.

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Asymmetric Expression of LincGET Biases Cell Fate in Two-Cell Mouse Embryos

Cited by 116 publications

References 40 publications

Systematic Chromatin Architecture Analysis inXenopus tropicalisReveals Conserved Three-Dimensional Folding Principles of Vertebrate Genomes

Systematic Chromatin Architecture Analysis inXenopus tropicalisReveals Conserved Three-Dimensional Folding Principles of Vertebrate Genomes

Lineage specification and pluripotency revealed by transcriptome analysis from oocyte to blastocyst in pig

Long noncoding RNA 2193 regulates meiosis through global epigenetic modification and cytoskeleton organization in pig oocytes

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