Ultrasensitive Ribo-seq reveals translational landscapes during mammalian oocyte-to-embryo transition and pre-implantation development

Xiong, Zhuqing; Xu, Kai; Lin, Zili; Kong, Feng; Wang, Qiujun; Quan, Yujun; Sha, Qian‐Qian; Li, Fajin; Zou, Zhuoning; Liu, Ling; Ji, Shu‐Yan; Chen, Yuling; Zhang, Hongmei; Fang, Jau–Shiung; Yu, Guang; Liu, Bofeng; Wang, Limin; Wang, Huili; Deng, Haiteng; Yang, Xuerui; Fan, Heng‐Yu; Li, Lei; Xie, Wei

doi:10.1038/s41556-022-00928-6

Cited by 76 publications

(116 citation statements)

References 93 publications

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“…S2, B and C). The variations between replicates were comparable to the Ribo-seq data in mouse oocytes and early embryos (18,21), as well as mESCs (22) (fig. S2D).…”

Section: Co-profiling Of Translatome and Transcriptome Landscapes Of ...supporting

confidence: 80%

“…S1A). The global patterns of ribosome-protected fragments (RPFs) and mRNAs from R2-lite in 1000 human embryonic kidney 293 (HEK293) cells correlated with those of the conventional Ribo-seq data (20) and the reference Smart-seq2 data (18), respectively (fig. S1B).…”

Section: Co-profiling Of Translatome and Transcriptome Landscapes Of ...mentioning

confidence: 94%

“…High-quality embryos were selected for this study according to morphological criteria (71). R2-lite integrated Ribo-lite (18) and Smart-seq2 (19), as described previously. Briefly, oocytes and embryos were lysed in 20 ml of ice-cold Ribolite lysis buffer.…”

Section: Methods Summarymentioning

confidence: 99%

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Translatome and transcriptome co-profiling reveals a role of TPRXs in human zygotic genome activation

Zou

Zhang

Wang

et al. 2022

Science

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Translational regulation plays a critical role during the oocyte-to-embryo transition (OET) and zygotic genome activation (ZGA). Here, we integrated ultra-low-input Ribo-seq with mRNA-seq to co-profile the translatome and transcriptome in human oocytes and early embryos. Comparison with mouse counterparts identified widespread differentially translated genes functioning in epigenetic reprogramming, transposon defense, and small RNA biogenesis, in part driven by species-specific regulatory elements in 3′ untranslated regions. Moreover, PRD-like homeobox transcription factors, including TPRXL, TPRX1, and TPRX2, are highly translated around ZGA. TPRX1/2/L knockdown leads to defective ZGA and preimplantation development. Ectopically expressed TPRXs bind and activate key ZGA genes in human embryonic stem cells. These data reveal the conservation and divergence of translation landscapes during OET and identify critical regulators of human ZGA.

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“…S2, B and C). The variations between replicates were comparable to the Ribo-seq data in mouse oocytes and early embryos (18,21), as well as mESCs (22) (fig. S2D).…”

Section: Co-profiling Of Translatome and Transcriptome Landscapes Of ...supporting

confidence: 80%

Section: Co-profiling Of Translatome and Transcriptome Landscapes Of ...mentioning

confidence: 94%

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Translatome and transcriptome co-profiling reveals a role of TPRXs in human zygotic genome activation

Zou

Zhang

Wang

et al. 2022

Science

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“…Finally, downregulation of translation machinery components may alter the translation landscape in a cell type-specific manner (89, 90). In the context of new findings regarding the role of translational regulation on cell fate acquisition in murine RGs (89, 90), investigating cell type-specific alterations in protein translation may be possible in the future with current developments for example in single-cell (91) and ultrasensitive (92) Ribo-seq.…”

Section: Discussionmentioning

confidence: 99%

Human brain organoid model of maternal immune activation identifies radial glia cells as selectively vulnerable

Sarieva

Kagermeier

Khakipoor

et al. 2022

Preprint

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Maternal immune activation (MIA) during the critical windows of gestation is correlated with long-term neurodevelopmental deficits in the offspring, including increased risks for autism spectrum disorder (ASD) in humans. Interleukin 6 (IL-6) derived from the gestational parent is one of the major molecular mediators, by which MIA alters the developing brain. In this study, we established a human three-dimensional (3D) in vitro model of MIA by treating induced pluripotent stem cell-derived dorsal forebrain organoids with a constitutively active form of IL-6, Hyper-IL-6. We validated our model by showing that dorsal forebrain organoids express the molecular machinery necessary for responding to Hyper-IL-6 and activate STAT signaling upon Hyper-IL-6 treatment. RNA sequencing analysis revealed the upregulation of major histocompatibility complex class I (MHCI) genes, which have been implicated with ASD. Immunohistochemical analysis as well as single-cell RNA-sequencing revealed a small increase in the proportion of radial glia cells. Single-cell transcriptomic analysis revealed the highest number of differentially expressed genes in radial glia cells with downregulation of genes related to protein translation in line with data from mouse models of MIA. Additionally, we identified differentially expressed genes not found in mouse models of MIA which might drive species-specific responses to MIA. Together, we establish a human 3D model of MIA, which can be used to study the cellular and molecular mechanisms underlying the increased risk for developing disorders such as ASD.

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“…Recently, considerable efforts have been devoted to achieving better understanding of the molecular networks, regulatory programs, and germline-soma or soma-soma communications during gametogenesis and embryogenesis. In particular, the rapid advancement of high-throughput sequencing technologies and ultra-low-input (or even single-cell) omics approaches have accelerated novel discoveries in reproductive development e.g., ( Wang et al, 2018 ; Qiao et al, 2020 ; Xu K. et al, 2021 ; He et al, 2021b ; Tyser et al, 2021 ; Yan et al, 2021 ; Wu et al, 2022 ; Xiong et al, 2022 ). Towards this direction, Qian et al .…”

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confidence: 99%

Editorial: Reproductive genomics

Liu

Yan²,

Shu³

et al. 2022

Front. Genet.

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Ultrasensitive Ribo-seq reveals translational landscapes during mammalian oocyte-to-embryo transition and pre-implantation development

Cited by 76 publications

References 93 publications

Translatome and transcriptome co-profiling reveals a role of TPRXs in human zygotic genome activation

Translatome and transcriptome co-profiling reveals a role of TPRXs in human zygotic genome activation

Human brain organoid model of maternal immune activation identifies radial glia cells as selectively vulnerable

Editorial: Reproductive genomics

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