USP7 represses lineage differentiation genes in mouse embryonic stem cells by both catalytic and noncatalytic activities

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Abstract

USP7, a ubiquitin-specific peptidase (USP), plays an important role in many cellular processes through its catalytic deubiquitination of various substrates. However, its nuclear function that shapes the transcriptional network in mouse embryonic stem cells (mESCs) remains poorly understood. We report that USP7 maintains mESC identity through both catalytic activity–dependent and –independent repression of lineage differentiation genes. Usp7 depletion attenuates SOX2 levels and derepresses lineage differentiation genes thereby compromising mESC pluripotency. Mechanistically, USP7 deubiquitinates and stabilizes SOX2 to repress mesoendodermal (ME) lineage genes. Moreover, USP7 assembles into RYBP-variant Polycomb repressive complex 1 and contributes to Polycomb chromatin–mediated repression of ME lineage genes in a catalytic activity–dependent manner. USP7 deficiency in its deubiquitination function is able to maintain RYBP binding to chromatin for repressing primitive endoderm–associated genes. Our study demonstrates that USP7 harbors both catalytic and noncatalytic activities to repress different lineage differentiation genes, thereby revealing a previously unrecognized role in controlling gene expression for maintaining mESC identity.

Abstract

Catalytic and non-catalytic functions of USP7 maintain pluripotent stem cells.

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Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2

Michael Love, Wolfgang Huber, Simon Anders (2014)

In comparative high-throughput sequencing assays, a fundamental task is the analysis of count data, such as read counts per gene in RNA-seq, for evidence of systematic changes across experimental conditions. Small replicate numbers, discreteness, large dynamic range and the presence of outliers require a suitable statistical approach. We present DESeq2, a method for differential analysis of count data, using shrinkage estimation for dispersions and fold changes to improve stability and interpretability of estimates. This enables a more quantitative analysis focused on the strength rather than the mere presence of differential expression. The DESeq2 package is available at http://www.bioconductor.org/packages/release/bioc/html/DESeq2.html. Electronic supplementary material The online version of this article (doi:10.1186/s13059-014-0550-8) contains supplementary material, which is available to authorized users.

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Fast gapped-read alignment with Bowtie 2.

Ben Langmead, Steven L Salzberg (2023)

As the rate of sequencing increases, greater throughput is demanded from read aligners. The full-text minute index is often used to make alignment very fast and memory-efficient, but the approach is ill-suited to finding longer, gapped alignments. Bowtie 2 combines the strengths of the full-text minute index with the flexibility and speed of hardware-accelerated dynamic programming algorithms to achieve a combination of high speed, sensitivity and accuracy.

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BEDTools: a flexible suite of utilities for comparing genomic features

Aaron Quinlan, Ira Hall (2010)

Motivation: Testing for correlations between different sets of genomic features is a fundamental task in genomics research. However, searching for overlaps between features with existing web-based methods is complicated by the massive datasets that are routinely produced with current sequencing technologies. Fast and flexible tools are therefore required to ask complex questions of these data in an efficient manner. Results: This article introduces a new software suite for the comparison, manipulation and annotation of genomic features in Browser Extensible Data (BED) and General Feature Format (GFF) format. BEDTools also supports the comparison of sequence alignments in BAM format to both BED and GFF features. The tools are extremely efficient and allow the user to compare large datasets (e.g. next-generation sequencing data) with both public and custom genome annotation tracks. BEDTools can be combined with one another as well as with standard UNIX commands, thus facilitating routine genomics tasks as well as pipelines that can quickly answer intricate questions of large genomic datasets. Availability and implementation: BEDTools was written in C++. Source code and a comprehensive user manual are freely available at http://code.google.com/p/bedtools Contact: aaronquinlan@gmail.com; imh4y@virginia.edu Supplementary information: Supplementary data are available at Bioinformatics online.

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Author and article information

Contributors

Chao Liu:

ORCID: https://orcid.org/0000-0001-6789-2443

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Lingang Sun:

ORCID: https://orcid.org/0000-0001-6033-9549

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SoftwareRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Yijun Tan: Role: Validation

Qi Wang:

ORCID: https://orcid.org/0000-0001-7717-084X

Role: Formal analysisRole: Funding acquisitionRole: InvestigationRole: SoftwareRole: Validation

Tao Luo: Role: Formal analysisRole: MethodologyRole: Resources

Chenlu Li: Role: InvestigationRole: SoftwareRole: Validation

Nan Yao:

ORCID: https://orcid.org/0000-0002-2584-3771

Role: Validation

Yuting Xie: Role: Formal analysisRole: Visualization

Xiao Yi: Role: Formal analysisRole: Investigation

Yi Zhu:

ORCID: https://orcid.org/0000-0003-0429-0802

Role: Formal analysisRole: Investigation

Tiannan Guo:

ORCID: https://orcid.org/0000-0003-3869-7651

Role: Formal analysisRole: InvestigationRole: Supervision

Junfeng Ji:

ORCID: https://orcid.org/0000-0001-5040-1863

Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Journal

Journal ID (nlm-ta): Sci Adv

Journal ID (iso-abbrev): Sci Adv

Journal ID (publisher-id): sciadv

Journal ID (hwp): advances

Title: Science Advances

Publisher: American Association for the Advancement of Science

ISSN (Electronic): 2375-2548

Publication date Collection: May 2023

Publication date (Electronic, pub): 17 May 2023

Volume: 9

Issue: 20

Electronic Location Identifier: eade3888

Affiliations

[ ¹ ]Center of Stem Cell and Regenerative Medicine, and Bone Marrow Transplantation Center of the First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou 310058, China.

[ ² ]Zhejiang University-University of Edinburgh Institute, Zhejiang University School of Medicine, Haining 314400, China.

[ ³ ]Westlake Laboratory of Life Sciences and Biomedicine, Key Laboratory of Structural Biology of Zhejiang Province, School of Life Sciences, Westlake University, Hangzhou 310030, China.

[ ⁴ ]Center for Infectious Disease Research, Hangzhou 310030, China.

[ ⁵ ]Institute of Basic Medical Sciences, Westlake Institute for Advanced Study, Hangzhou 310030, China.

[ ⁶ ]Zhejiang Engineering Laboratory for Stem Cell and Immunotherapy, Institute of Hematology, Zhejiang University, Hangzhou 310058, China.

[ ⁷ ]Department of Geriatrics, Affiliated Hangzhou First People’s Hospital, Zhejiang University School of Medicine, Hangzhou 310006, China.

[ ⁸ ]Eye Center, The 2nd Affiliated Hospital, School of Medicine, Zhejiang University, Zhejiang Provincial Key Laboratory of Ophthalmology, Zhejiang Provincial Clinical Research Center for Eye Diseases, Zhejiang Provincial Engineering Institute on Eye Diseases, Hangzhou, Zhejiang 310009, China.

Author notes

[* ]Corresponding author. Email: jijunfeng@ 123456zju.edu.cn

[†]

These authors contributed equally to this work.

Author information

Chao Liu https://orcid.org/0000-0001-6789-2443

Lingang Sun https://orcid.org/0000-0001-6033-9549

Qi Wang https://orcid.org/0000-0001-7717-084X

Nan Yao https://orcid.org/0000-0002-2584-3771

Yi Zhu https://orcid.org/0000-0003-0429-0802

Tiannan Guo https://orcid.org/0000-0003-3869-7651

Junfeng Ji https://orcid.org/0000-0001-5040-1863

Article

Publisher ID: ade3888

DOI: 10.1126/sciadv.ade3888

PMC ID: 10191441

SO-VID: 2e0f288a-da9f-46de-ab58-b91898a7a392

Copyright © Copyright © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.