The role of N6-methyladenosine (m6A) modification in the regulation of circRNAs.

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Abstract

N6-methyladenosine (m6A), the most abundant modification in eukaryotic cells, regulates RNA transcription, processing, splicing, degradation, and translation. Circular RNA (circRNA) is a class of covalently closed RNA molecules characterized by universality, diversity, stability and conservatism of evolution. Accumulating evidence shows that both m6A modification and circRNAs participate in the pathogenesis of multiple diseases, such as cancers, neurological diseases, autoimmune diseases, and infertility. Recently, m6A modification has been identified for its enrichment and vital biological functions in regulating circRNAs. In this review, we summarize the role of m6A modification in the regulation and function of circRNAs. Moreover, we discuss the potential applications and possible future directions in the field.

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Most cited references 43

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Foxo3 circular RNA promotes cardiac senescence by modulating multiple factors associated with stress and senescence responses

William W. Du, Weining Yang, Yu Chen … (2017)

Circular RNAs are a subclass of non-coding RNAs detected within mammalian cells. This study was designed to test the roles of a circular RNA circ-Foxo3 in senescence using in vitro and in vivo approaches.

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m 6 A enhances the phase separation potential of mRNA

Ryan Ries, Sara Zaccara, Pierre Klein … (2019)

N 6-methyladenosine (m6A) is the most prevalent modified nucleotide in mRNA 1,2 , with ~25% of mRNAs containing at least one m6A. Methylation of mRNA to form m6A is required for diverse cellular and physiological processes 3 . Although the presence of m6A in an mRNA can affect its fate in different ways, it is unclear how m6A directs this process and why the effects of m6A can vary in different cellular contexts. Here we show that the cytosolic m6A-binding proteins, YTHDF1–3, undergo liquid-liquid phase separation (LLPS) in vitro and in cells. This LLPS is markedly enhanced by mRNAs that contain multiple, but not single, m6A residues. Polymethylated mRNAs act as a multivalent scaffold for binding YTHDF proteins, juxtaposing their low-complexity domains, leading to phase separation. The resulting mRNA-YTHDF complexes then partition into different endogenous phase-separated compartments, such as P-bodies, stress granules, or neuronal RNA granules. m6A-mRNA is subject to compartment-specific regulation, including reduced mRNA stability and translation. These studies reveal that the number and distribution of m6A sites in cellular mRNAs can regulate and influence the composition of the phase-separated transcriptome. Additionally, these findings indicate that the cellular properties of m6A-modified mRNAs are governed by liquid-liquid phase separation principles.

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Transcriptome-wide discovery of circular RNAs in Archaea

Miri Danan-Gotthold, Schraga Schwartz, Sarit Edelheit … (2011)

Circular RNA forms had been described in all domains of life. Such RNAs were shown to have diverse biological functions, including roles in the life cycle of viral and viroid genomes, and in maturation of permuted tRNA genes. Despite their potentially important biological roles, discovery of circular RNAs has so far been mostly serendipitous. We have developed circRNA-seq, a combined experimental/computational approach that enriches for circular RNAs and allows profiling their prevalence in a whole-genome, unbiased manner. Application of this approach to the archaeon Sulfolobus solfataricus P2 revealed multiple circular transcripts, a subset of which was further validated independently. The identified circular RNAs included expected forms, such as excised tRNA introns and rRNA processing intermediates, but were also enriched with non-coding RNAs, including C/D box RNAs and RNase P, as well as circular RNAs of unknown function. Many of the identified circles were conserved in Sulfolobus acidocaldarius, further supporting their functional significance. Our results suggest that circular RNAs, and particularly circular non-coding RNAs, are more prevalent in archaea than previously recognized, and might have yet unidentified biological roles. Our study establishes a specific and sensitive approach for identification of circular RNAs using RNA-seq, and can readily be applied to other organisms.

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Author and article information

Journal

Journal ID (iso-abbrev): Mol Cancer

Title: Molecular cancer

Publisher: Springer Science and Business Media LLC

ISSN (Electronic): 1476-4598

ISSN (Print): 1476-4598

Publication date (Electronic): June 10 2020

Volume: 19

Issue: 1

Affiliations

[1 ] Department of Colorectal Surgery, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, 450052, Henan, China.

[2 ] Department of Colorectal Surgery, Zhengzhou Central Hospital, Zhengzhou University, Zhengzhou, 450007, Henan, China.

[3 ] Department of Thyroid Surgery, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, 450052, Henan, China.

[4 ] Academy of Medical Sciences, Zhengzhou University, Zhengzhou, 450052, Henan, China.

[5 ] School of Life Sciences, Zhengzhou University, Zhengzhou, 450001, Henan, China.

[6 ] School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, 450002, Henan, China.

[7 ] Department of Thyroid Surgery, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, 450052, Henan, China. detaoyin@zzu.edu.cn.

[8 ] Department of Colorectal Surgery, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, 450052, Henan, China. 1999liujb@163.com.

[9 ] Department of Colorectal Surgery, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, 450052, Henan, China. zqsun82@csu.edu.cn.

[10 ] School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, 450002, Henan, China. zqsun82@csu.edu.cn.

Article

Publisher Item ID: 10.1186/s12943-020-01224-3

DOI: 10.1186/s12943-020-01224-3

PMC ID: 7285594

PubMed ID: 32522202

SO-VID: 30f388ac-ebb3-49b3-bf8d-767088daad98

History

Keywords: CircRNA,Innate immunity,M6A,M6A modified circRNA,Tumour

Data availability:

Keywords: CircRNA, Innate immunity, M6A, M6A modified circRNA, Tumour

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The role of N6-methyladenosine (m6A) modification in the regulation of circRNAs.

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Most cited references 43

Foxo3 circular RNA promotes cardiac senescence by modulating multiple factors associated with stress and senescence responses

m 6 A enhances the phase separation potential of mRNA

Transcriptome-wide discovery of circular RNAs in Archaea

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Cited by 118

Most referenced authors 2,198