Dynamic control of chromatin-associated m6A methylation regulates nascent RNA synthesis

Molecular Cell - Tập 82 - Trang 1156-1168.e7 - 2022
Wenqi Xu1, Chenxi He1, Emily G. Kaye2, Jiahui Li1, Mandi Mu1, Geoffrey M. Nelson2, Li Dong1, Jiahua Wang1, Feizhen Wu1, Yujiang Geno Shi3, Karen Adelman2, Fei Lan1, Yang Shi4, Hongjie Shen1
1Center for Medical Research and Innovation, Shanghai Pudong Hospital, Fudan University Pudong Medical Center, the Shanghai Key Laboratory of Medical Epigenetics, the International Co-laboratory of Medical Epigenetics and Metabolism, Ministry of Science and Technology, Institutes of Biomedical Sciences, Fudan University, Shanghai 201399, China
2Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA
3Division of Endocrinology, Diabetes and Hypertension, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
4Ludwig Institute for Cancer Research, Oxford Branch, Oxford University, Oxford OX3 7DQ, UK

Tài liệu tham khảo

Akhtar, 2021, m6A RNA methylation regulates promoter-proximal pausing of RNA polymerase II, Mol. Cell, 81, 10.1016/j.molcel.2021.06.023 Akichika, 2019, Cap-specific terminal N (6)-methylation of RNA by an RNA polymerase II-associated methyltransferase, Science, 363, 10.1126/science.aav0080 Barbieri, 2017, Promoter-bound METTL3 maintains myeloid leukaemia by m(6)A-dependent translation control, Nature, 552, 126, 10.1038/nature24678 Beckedorff, 2020, The human integrator complex facilitates transcriptional elongation by endonucleolytic cleavage of nascent transcripts, Cell Rep., 32, 107917, 10.1016/j.celrep.2020.107917 Chelmicki, 2021, m(6)A RNA methylation regulates the fate of endogenous retroviruses, Nature, 591, 312, 10.1038/s41586-020-03135-1 Chen, 2018, fastp: an ultra-fast all-in-one FASTQ preprocessor, Bioinformatics, 34, i884, 10.1093/bioinformatics/bty560 Core, 2019, Promoter-proximal pausing of RNA polymerase II: a nexus of gene regulation, Genes Dev., 33, 960, 10.1101/gad.325142.119 Davis, 2018, The encyclopedia of DNA elements (ENCODE): data portal update, Nucleic Acids Res., 46, D794, 10.1093/nar/gkx1081 Dominissini, 2012, Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq, Nature, 485, 201, 10.1038/nature11112 Elrod, 2019, The integrator complex attenuates promoter-proximal transcription at protein-coding genes, Mol. Cell, 76, 10.1016/j.molcel.2019.10.034 2012, An integrated encyclopedia of DNA elements in the human genome, Nature, 489, 57, 10.1038/nature11247 Ezzeddine, 2011, A subset of Drosophila integrator proteins is essential for efficient U7 snRNA and spliceosomal snRNA 3′-end formation, Mol. Cell. Biol., 31, 328, 10.1128/MCB.00943-10 Gaidatzis, 2015, Analysis of intronic and exonic reads in RNA-seq data characterizes transcriptional and post-transcriptional regulation, Nat. Biotechnol., 33, 722, 10.1038/nbt.3269 Gates, 2017, Histone marks in the ‘driver’s seat’: functional roles in steering the transcription cycle, Trends Biochem. Sci., 42, 977, 10.1016/j.tibs.2017.10.004 Heinz, 2010, Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities, Mol. Cell, 38, 576, 10.1016/j.molcel.2010.05.004 Henriques, 2018, Widespread transcriptional pausing and elongation control at enhancers, Genes Dev., 32, 26, 10.1101/gad.309351.117 Jia, 2011, N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO, Nat. Chem. Biol., 7, 885, 10.1038/nchembio.687 Judd, 2021, Pioneer-like factor GAF cooperates with PBAP (SWI/SNF) and NURF (ISWI) to regulate transcription, Genes Dev., 35, 147, 10.1101/gad.341768.120 Kan, 2021, A neural m6A/Ythdf pathway is required for learning and memory in Drosophila, Nat. Commun., 12, 1458, 10.1038/s41467-021-21537-1 Kaya-Okur, 2019, CUT&Tag for efficient epigenomic profiling of small samples and single cells, Nat. Commun., 10, 1930, 10.1038/s41467-019-09982-5 Ke, 2017, m(6)A mRNA modifications are deposited in nascent pre-mRNA and are not required for splicing but do specify cytoplasmic turnover, Genes Dev., 31, 990, 10.1101/gad.301036.117 Knuckles, 2017, RNA fate determination through cotranscriptional adenosine methylation and microprocessor binding, Nat. Struct. Mol. Biol., 24, 561, 10.1038/nsmb.3419 Langmead, 2009, Ultrafast and memory-efficient alignment of short DNA sequences to the human genome, Genome Biol., 10, R25, 10.1186/gb-2009-10-3-r25 Lasman, 2020, Context-dependent functional compensation between Ythdf m(6)A reader proteins, Genes Dev., 34, 1373, 10.1101/gad.340695.120 Lee, 2021, Enhancer RNA m6A methylation facilitates transcriptional condensate formation and gene activation, Mol. Cell, 81, 10.1016/j.molcel.2021.07.024 Li, 2009, The sequence alignment/map format and SAMtools, Bioinformatics, 25, 2078, 10.1093/bioinformatics/btp352 Liu, 2020, N (6)-methyladenosine of chromosome-associated regulatory RNA regulates chromatin state and transcription, Science, 367, 580, 10.1126/science.aay6018 Liu, 2021, The RNA m(6)A reader YTHDC1 silences retrotransposons and guards ES cell identity, Nature, 591, 322, 10.1038/s41586-021-03313-9 Liu, 2017, N6-methyladenosine alters RNA structure to regulate binding of a low-complexity protein, Nucleic Acids Res., 45, 6051, 10.1093/nar/gkx141 Lizio, 2015, Gateways to the FANTOM5 promoter level mammalian expression atlas, Genome Biol., 16, 22, 10.1186/s13059-014-0560-6 Louloupi, 2018, Transient N-6-methyladenosine transcriptome sequencing reveals a regulatory role of m6A in splicing efficiency, Cell Rep., 23, 3429, 10.1016/j.celrep.2018.05.077 Lovén, 2013, Selective inhibition of tumor oncogenes by disruption of super-enhancers, Cell, 153, 320, 10.1016/j.cell.2013.03.036 Lykke-Andersen, 2021, Integrator is a genome-wide attenuator of non-productive transcription, Mol. Cell, 81, 10.1016/j.molcel.2020.12.014 Mahat, 2016, Base-pair-resolution genome-wide mapping of active RNA polymerases using precision nuclear run-on (PRO-seq), Nat. Protoc., 11, 1455, 10.1038/nprot.2016.086 Meyer, 2012, Comprehensive analysis of mRNA methylation reveals enrichment in 3 ′ UTRs and near stop codons, Cell, 149, 1635, 10.1016/j.cell.2012.05.003 Ping, 2014, Mammalian WTAP is a regulatory subunit of the RNA N6-methyladenosine methyltransferase, Cell Res., 24, 177, 10.1038/cr.2014.3 Quinlan, 2010, BEDTools: a flexible suite of utilities for comparing genomic features, Bioinformatics, 26, 841, 10.1093/bioinformatics/btq033 Ramírez, 2016, deepTools2: a next generation web server for deep-sequencing data analysis, Nucleic Acids Re.s, 44, W160, 10.1093/nar/gkw257 Sendinc, 2019, PCIF1 catalyzes m6Am mRNA methylation to regulate gene expression, Mol. Cell, 75, 10.1016/j.molcel.2019.05.030 Shi, 2019, Where, when, and how: context-dependent functions of RNA methylation writers, readers, and erasers, Mol. Cell, 74, 640, 10.1016/j.molcel.2019.04.025 Śledź, 2016, Structural insights into the molecular mechanism of the m(6)A writer complex, eLife, 5, 10.7554/eLife.18434 Trapnell, 2009, TopHat: discovering splice junctions with RNA-Seq, Bioinformatics, 25, 1105, 10.1093/bioinformatics/btp120 Wang, 2016, Structural basis for cooperative function of Mettl3 and Mettl14 methyltransferases, Mol. Cell, 63, 306, 10.1016/j.molcel.2016.05.041 Wang, 2016, Structural basis of N(6)-adenosine methylation by the METTL3-METTL14 complex, Nature, 534, 575, 10.1038/nature18298 Wang, 2014, N6-methyladenosine-dependent regulation of messenger RNA stability, Nature, 505, 117, 10.1038/nature12730 Wang, 2021, Role of Hakai in m6A modification pathway in Drosophila, Nat. Commun., 12, 2159, 10.1038/s41467-021-22424-5 Xiang, 2017, RNA m(6)A methylation regulates the ultraviolet-induced DNA damage response, Nature, 543, 573, 10.1038/nature21671 Xiao, 2019, The RNA N(6)-methyladenosine modification landscape of human fetal tissues, Nat. Cell Biol., 21, 651, 10.1038/s41556-019-0315-4 Xu, 2021, METTL3 regulates heterochromatin in mouse embryonic stem cells, Nature, 591, 317, 10.1038/s41586-021-03210-1 Yu, 2015, ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization, Bioinformatics, 31, 2382, 10.1093/bioinformatics/btv145 Zaccara, 2020, A unified model for the function of YTHDF proteins in regulating m(6)A-modified mRNA, Cell, 181, 10.1016/j.cell.2020.05.012 Zhang, 2008, Model-based analysis of ChIP-Seq (MACS), Genome Biol., 9, R137, 10.1186/gb-2008-9-9-r137 Zhang, 2021, INTS11 regulates hematopoiesis by promoting PRC2 function, Sci. Adv., 7, eabh1684, 10.1126/sciadv.abh1684 Zheng, 2013, ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility, Mol. Cell, 49, 18, 10.1016/j.molcel.2012.10.015 Zhou, 2019, Regulation of co-transcriptional pre-mRNA splicing by m(6)A through the low-complexity protein hnRNPG, Mol. Cell, 76, 10.1016/j.molcel.2019.07.005