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m6A Topological Transition Coupled to Developmental Regulation of Gene Expression During Mammalian Tissue Development

N6-methyladenosine (m6A) is the most prevalent internal modification and reversible epitranscriptomic mark in messenger RNAs (mRNAs) and plays essential roles in a variety of biological processes. However, the dynamic distribution patterns of m6A and their significance during mammalian tissue develo...

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Detalles Bibliográficos
Autores principales: Li, Shanshan, Yang, Qing, Jiao, Rui, Xu, Pengfei, Sun, Yazhou, Li, Xin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9294180/
https://www.ncbi.nlm.nih.gov/pubmed/35865625
http://dx.doi.org/10.3389/fcell.2022.916423
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author Li, Shanshan
Yang, Qing
Jiao, Rui
Xu, Pengfei
Sun, Yazhou
Li, Xin
author_facet Li, Shanshan
Yang, Qing
Jiao, Rui
Xu, Pengfei
Sun, Yazhou
Li, Xin
author_sort Li, Shanshan
collection PubMed
description N6-methyladenosine (m6A) is the most prevalent internal modification and reversible epitranscriptomic mark in messenger RNAs (mRNAs) and plays essential roles in a variety of biological processes. However, the dynamic distribution patterns of m6A and their significance during mammalian tissue development are poorly understood. Here, we found that based on m6A distribution patterns, protein-coding genes were classified into five groups with significantly distinct biological features and functions. Strikingly, comparison of the m6A methylomes of multiple mammalian tissues between fetal and adult stages revealed dynamic m6A topological transition during mammalian tissue development, and identified large numbers of genes with significant m6A loss in 5′UTRs or m6A gain around stop codons. The genes with m6A loss in 5′UTRs were highly enriched in developmental stage-specific genes, and their m6A topological transitions were strongly associated with gene expression regulation during tissue development. The genes with m6A gain around the stop codons were associated with tissue-specific functions. Our findings revealed the existence of different m6A topologies among protein-coding genes that were associated with distinct characteristics. More importantly, these genes with m6A topological transitions were crucial for tissue development via regulation of gene expression, suggesting the importance of dynamic m6A topological transitions during mammalian tissue development.
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spelling pubmed-92941802022-07-20 m6A Topological Transition Coupled to Developmental Regulation of Gene Expression During Mammalian Tissue Development Li, Shanshan Yang, Qing Jiao, Rui Xu, Pengfei Sun, Yazhou Li, Xin Front Cell Dev Biol Cell and Developmental Biology N6-methyladenosine (m6A) is the most prevalent internal modification and reversible epitranscriptomic mark in messenger RNAs (mRNAs) and plays essential roles in a variety of biological processes. However, the dynamic distribution patterns of m6A and their significance during mammalian tissue development are poorly understood. Here, we found that based on m6A distribution patterns, protein-coding genes were classified into five groups with significantly distinct biological features and functions. Strikingly, comparison of the m6A methylomes of multiple mammalian tissues between fetal and adult stages revealed dynamic m6A topological transition during mammalian tissue development, and identified large numbers of genes with significant m6A loss in 5′UTRs or m6A gain around stop codons. The genes with m6A loss in 5′UTRs were highly enriched in developmental stage-specific genes, and their m6A topological transitions were strongly associated with gene expression regulation during tissue development. The genes with m6A gain around the stop codons were associated with tissue-specific functions. Our findings revealed the existence of different m6A topologies among protein-coding genes that were associated with distinct characteristics. More importantly, these genes with m6A topological transitions were crucial for tissue development via regulation of gene expression, suggesting the importance of dynamic m6A topological transitions during mammalian tissue development. Frontiers Media S.A. 2022-07-05 /pmc/articles/PMC9294180/ /pubmed/35865625 http://dx.doi.org/10.3389/fcell.2022.916423 Text en Copyright © 2022 Li, Yang, Jiao, Xu, Sun and Li. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Li, Shanshan
Yang, Qing
Jiao, Rui
Xu, Pengfei
Sun, Yazhou
Li, Xin
m6A Topological Transition Coupled to Developmental Regulation of Gene Expression During Mammalian Tissue Development
title m6A Topological Transition Coupled to Developmental Regulation of Gene Expression During Mammalian Tissue Development
title_full m6A Topological Transition Coupled to Developmental Regulation of Gene Expression During Mammalian Tissue Development
title_fullStr m6A Topological Transition Coupled to Developmental Regulation of Gene Expression During Mammalian Tissue Development
title_full_unstemmed m6A Topological Transition Coupled to Developmental Regulation of Gene Expression During Mammalian Tissue Development
title_short m6A Topological Transition Coupled to Developmental Regulation of Gene Expression During Mammalian Tissue Development
title_sort m6a topological transition coupled to developmental regulation of gene expression during mammalian tissue development
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9294180/
https://www.ncbi.nlm.nih.gov/pubmed/35865625
http://dx.doi.org/10.3389/fcell.2022.916423
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