N 6-methyladenosine alters RNA structure to regulate binding of a low-complexity protein

Nian Liu, Katherine I. Zhou, Marc Parisien, Qing Dai, Luda Diatchenko, Tao Pan

Nucleic Acids Research · 2017 · 804 citations · 46 references

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TL;DR

N6‑methyladenosine (m6A) is the most abundant internal mRNA modification, influencing all stages of the mRNA life cycle, is recognized by YTH‑domain proteins, and can alter RNA structure to modulate RNA‑protein interactions. The study aims to demonstrate that m6A enhances accessibility of adjacent RNA sequences for binding by heterogeneous nuclear ribonucleoprotein G (HNRNPG). The authors mapped 13,191 transcriptome m6A sites, showing that HNRNPG binds m6A‑modified RNAs via its C‑terminal low‑complexity region that self‑assembles into large particles, thereby influencing target mRNA expression and splicing. The Arg‑Gly‑Gly repeats in HNRNPG’s low‑complexity region are essential for binding to the m6A‑exposed RNA motif, and m6A‑induced structural changes promote direct binding of modified RNAs to low‑complexity regions, affecting expression and splicing of target mRNAs.

Abstract

N6-methyladenosine (m6A) is the most abundant internal modification in eukaryotic messenger RNA (mRNA), and affects almost every stage of the mRNA life cycle. The YTH-domain proteins can specifically recognize m6A modification to control mRNA maturation, translation and decay. m6A can also alter RNA structures to affect RNA-protein interactions in cells. Here, we show that m6A increases the accessibility of its surrounding RNA sequence to bind heterogeneous nuclear ribonucleoprotein G (HNRNPG). Furthermore, HNRNPG binds m6A-methylated RNAs through its C-terminal low-complexity region, which self-assembles into large particles in vitro. The Arg-Gly-Gly repeats within the low-complexity region are required for binding to the RNA motif exposed by m6A methylation. We identified 13,191 m6A sites in the transcriptome that regulate RNA-HNRNPG interaction and thereby alter the expression and alternative splicing pattern of target mRNAs. Low-complexity regions are pervasive among mRNA binding proteins. Our results show that m6A-dependent RNA structural alterations can promote direct binding of m6A-modified RNAs to low-complexity regions in RNA binding proteins.

References

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