DHX36结合诱导RNA结构体重塑并通过m6A阅读器YTHDF1调节RNA丰度-动脉网

DHX36 binding induces RNA structurome remodeling and regulates RNA abundance via m6A reader YTHDF1

Nature 等信源发布 2024-11-15 09:51

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AbstractRNA structure constitutes a new layer of gene regulatory mechanisms. RNA binding proteins can modulate RNA secondary structures, thus participating in post-transcriptional regulation. The DEAH-box helicase 36 (DHX36) is known to bind and unwind RNA G-quadruplex (rG4) structure but the transcriptome-wide RNA structure remodeling induced by DHX36 binding and the impact on RNA fate remain poorly understood.

摘要RNA结构构成了一层新的基因调控机制。RNA结合蛋白可以调节RNA二级结构，从而参与转录后调控。已知DEAH盒解旋酶36（DHX36）结合并解开RNA G-四链体（rG4）结构，但DHX36结合诱导的转录组范围的RNA结构重塑以及对RNA命运的影响仍然知之甚少。

Here, we investigate the RNA structurome alteration induced by DHX36 depletion. Our findings reveal that DHX36 binding induces structural remodeling not only at the localized binding sites but also on the entire mRNA transcript most pronounced in 3’UTR regions. DHX36 binding increases structural accessibility at 3’UTRs which is correlated with decreased post-transcriptional mRNA abundance.

在这里，我们研究了DHX36耗竭诱导的RNA结构改变。我们的发现表明，DHX36结合不仅在局部结合位点诱导结构重塑，而且在3'UTR区域最明显的整个mRNA转录本上也诱导结构重塑。DHX36结合增加了3'UTR的结构可及性，这与转录后mRNA丰度降低有关。

Further analyses and experiments uncover that DHX36 binding sites are enriched for N6-methyladenosine (m6A) modification and YTHDF1 binding; and DHX36 induced structural changes may facilitate YTHDF1 binding to m6A sites leading to RNA degradation. Altogether, our findings uncover the structural remodeling effect of DHX36 binding and its impact on RNA abundance through regulating m6A dependent YTHDF1 binding..

进一步的分析和实验发现，DHX36结合位点富含N6-甲基腺苷（m6A）修饰和YTHDF1结合；DHX36诱导的结构变化可能促进YTHDF1与m6A位点的结合，从而导致RNA降解。总之，我们的发现揭示了DHX36结合的结构重塑效应及其通过调节m6A依赖性YTHDF1结合对RNA丰度的影响。。

IntroductionIn recent years, interest in RNA secondary structure has exploded due to its implications in almost all biological functions and its newly appreciated capacity as a therapeutic agent/target1. Examples of secondary structures include long-range interactions, hairpins, R-loops, and G-quadruplexes (G4), and they are formed through interactions of non-adjacent nucleotides.

引言近年来，由于RNA二级结构对几乎所有生物学功能的影响及其作为治疗剂/靶标1的新的被认可的能力，对RNA二级结构的兴趣已经爆发。二级结构的例子包括长程相互作用，发夹，R环和G-四链体（G4），它们是通过非相邻核苷酸的相互作用形成的。

Due to their large size, the structures of mRNAs are challenging to study, but the past decade has seen rapid development in RNA structure-probing methods to capture transcriptome-wide RNA structures (that is, RNA structurome) in many species and across conditions1. For example, structure-seq2 was developed for mapping in vivo RNA structures and interactions by coupling chemical structure probing with deep sequencing.

由于它们的大尺寸，mRNA的结构研究具有挑战性，但在过去的十年中，RNA结构探测方法在许多物种和跨条件下捕获转录组范围的RNA结构（即RNA结构组）方面取得了快速发展1。例如，structure-seq2是通过将化学结构探测与深度测序相结合而开发的，用于绘制体内RNA结构和相互作用。

Chemical modification on the unpaired bases leads to the reverse transcription (RT) stops, which can be read out as a reactivity score and be used to infer RNA structures. It provides quantitative RNA secondary structural information across thousands of transcripts at nucleotide resolution. Several other probing methods have also been developed3,4,5, thus providing tools for systematic interrogation of in vivo RNA structures.The roles of RNA secondary structures in key biological functions can be seen in every type of RNA mainly because of their importance in mediating RNA association with RNA binding proteins (RBPs)6,7,8,9.

对不成对碱基的化学修饰会导致逆转录（RT）停止，这可以作为反应性评分读出，并用于推断RNA结构。它以核苷酸分辨率提供了数千个转录本的定量RNA二级结构信息。还开发了其他几种探测方法3,4,5，从而为体内RNA结构的系统询问提供了工具。RNA二级结构在关键生物学功能中的作用可以在每种类型的RNA中看到，主要是因为它们在介导RNA与RNA结合蛋白（RBPs）6,7,8,9的结合中的重要性。

During the mRNA lifecycle, RBPs regulate diverse transcriptional and post-transcriptional stages. They can bind to pre-mRNA molecules in the nucleus and regulate its maturation and transportation to the cytoplasm, where they regulate translation and degradation. Emerging evidence from transcriptome wide profiling of RBP binding such as crosslinking immunoprec.

在mRNA生命周期中，RBP调节不同的转录和转录后阶段。它们可以与细胞核中的前mRNA分子结合，并调节其成熟和向细胞质的运输，从而调节翻译和降解。来自RBP结合的转录组范围分析的新证据，例如交联immunoprec。

(1)

$$\alpha=\min \left(\right. 1,{\sum }_{i}{{{\mathrm{ln}}}}\left(1+{P}_{i}\right)/{\sum }_{i}{{{\mathrm{ln}}}}(1+{M}_{i})$$

$$\ alpha=\ min \ left（\ right.1，{\ sum}{i}{{\ mathrm{ln}}}\ left（1+{P}_{i} \右）/{\ sum}{i}{{\ mathrm{ln}}}（1+{M}_{i} ））$$

(2)

where ${P}_{i}$ and ${M}_{i}$ respectively represent the RT stops of nucleotide i in NAI/DMS-treated and DMSO-treated samples; L represents transcript length; α is a library size correction factor. The raw reactivity was calculated using log-normalized RT stops and then normalized by 2–8% method to generate the final reactivity.

在哪里\({P}_{i} \）和\({M}_{i} \）分别代表NAI/DMS处理和DMSO处理样品中核苷酸i的RT终止；L代表成绩单长度；α是库大小校正因子。使用对数归一化RT停止计算原始反应性，然后通过2-8%方法归一化以产生最终反应性。

In the normalization process, the top 10% of raw reactivities were extracted. Within this subset, the top 2% of raw reactivities were excluded, and the remaining 8% of reactivities were averaged to generate a normalization scale77. Subsequently, the raw reactivities of both WT and KO samples were divided by the WT normalization scale to generate normalized reactivities.

在归一化过程中，提取了前10%的原始反应性。在这个子集中，前2%的原始反应性被排除在外，其余8%的反应性被平均以产生归一化量表77。随后，将WT和KO样品的原始反应性除以WT归一化标度以产生归一化反应性。

Next, the splice_reacts_by_FASTA.py script was used to splice the reactivity profile of the entire transcript by the designated mRNA regions. The average reactivity and the Gini index of SHAPE reactivity of the entire transcript or the designated region were calculated using the react_statistics.py script.

接下来，使用splice\u reacts\u by\u FASTA.py脚本通过指定的mRNA区域剪接整个转录本的反应性谱。使用react\u statistics.py脚本计算整个转录本或指定区域的平均反应性和SHAPE反应性的基尼指数。

RNA structure folding constrained by reactivity score was performed using the Vienna RNA package41. The base-pairing probability of each nucleotide was extracted from the corresponding structure ensemble “.ps” file. The software dStruct40 (parameter: reps_A = 2, reps_B = 2, min_length = 5, batches=T, check_signal_strength = T, check_nucs = T, check_quality = T) was used to identify the significant DRRs within DHX36 binding sites (FDR < 0.25).

使用维也纳RNA包装41进行受反应性评分约束的RNA结构折叠。从相应的结构集合“.ps”文件中提取每个核苷酸的碱基配对概率。使用软件dStruct40（参数：reps\u A = 2，reps\u B = 2，min\u length = 5，Batch=T，check\u signal\u strength=T，check\u nucs=T，check\u quality=T）来识别DHX36结合位点内的重要DRR（FDR<0.25）。

VARNA78 was used to visualize the selected RNA secondary structures (Figs. 3H, 6B).For 18S rRNA benchmarking, we respectively aligned the reads in HEK293T or C2C12 cells to human and mouse 18S rRNA reference (human: NR_145820.1; mouse: NR_003278.3). The RT stops and reactivity scores were calculated based on the same w.

VARNA78用于可视化所选的RNA二级结构（图3H，6B）。对于18S rRNA基准测试，我们分别将HEK293T或C2C12细胞中的读数与人和小鼠18S rRNA参考（人：NR\u 145820.1；小鼠：NR\u 003278.3）进行比对。RT停止和反应性评分是基于相同的w计算的。

Data availability

数据可用性

The data supporting the findings of this study are available from the corresponding authors upon request. Structure-seq and RBNS data used in this study have been deposited in Gene Expression Omnibus (GEO) database under the accession codes GSE237160 (WT and DHX36/Dhx36 Structure-seq), GSE237161 (RBNS), GSE264498 (YTHDF1 CLIP-seq), and GSE264642 (Control and m6A-inhibited Structure-seq).

支持本研究结果的数据可应要求从通讯作者处获得。本研究中使用的Structure-seq和RBNS数据已保存在Gene Expression Omnibus（GEO）数据库中，登录号为GSE237160（WT和DHX36/DHX36 Structure-seq），GSE237161（RBNS），GSE264498（YTHDF1 CLIP-seq）和GSE264642（对照和m6A抑制的Structure-seq）。

Source data for the figures and Supplementary Figs. are provided as a Source Data file. Source data are provided with this paper..

图和补充图的源数据作为源数据文件提供。本文提供了源数据。。

Code availability

代码可用性

The code used in this study is available at Zenodo97 and the GitHub repository (https://github.com/zhangyw0713/Scripts_for_DHX36_paper).

这项研究中使用的代码可以在Zenodo97和GitHub存储库中找到(https://github.com/zhangyw0713/Scripts_for_DHX36_paper)。

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Yuwei, Z. et al. DHX36 binding induces RNA structurome remodeling and regulates RNA abundance via m6A/YTHDF1. https://doi.org/10.5281/zenodo.13852598 (2024).Download referencesAcknowledgementsThis work was supported by National Key R&D Program of China to H.W. (2022YFA0806003); the National Natural Science Foundation of China (NSFC) (grant no.

Yuwei，Z。等人。DHX36结合诱导RNA结构体重塑并通过m6A/YTHDF1调节RNA丰度。https://doi.org/10.5281/zenodo.13852598（2024年）。下载参考文献致谢这项工作得到了中国国家重点研发计划对H.W.（2022YFA0806003）的支持；国家自然科学基金（NSFC）（批准号：。

82172436 to H.W.; 32300703 to X.C.; 32270587 to Y.Z.; 32471343 to C.K.K); National Natural Science Foundation of China (NSFC) Excellent Young Scientists Fund (Hong Kong and Macau) Project (32222089) to C.K.K.; Natural Science Foundation of Guangdong Province, China to X.C. (2024A1515030291); General Research Funds (GRF) from the Research Grants Council (RGC) of the Hong Kong Special Administrative Region (14115319, 14100620, 14106521, and 14105823 to H.W.; 14120420, 14103522, and 14105123 to H.S.; RFS2425-1S02, CityU 11100123, CityU 11100222, and CityU 11100421 to C.K.K.); the research funds from Health@InnoHK program launched by Innovation Technology Commission, the Government of the Hong Kong SAR, China to H.W.; Collaborative Research Fund (CRF) from RGC to H.W.

82172436给H.W。；32300703给X.C。；32270587至Y.Z。；；国家自然科学基金（NSFC）优秀青年科学家基金（港澳）项目（32222089）授予C.K.K。；广东省自然科学基金（2024A1515030291）；香港特别行政区研究资助委员会（RGC）的一般研究基金（GRF）（H.W.的14115319、14100620、14106521和14105823；H.S.的14120420、14103522和14105123；C.K.的RFS2425-1S02、城大11100123、城大11100222和城大11100421）；研究经费来自Health@InnoHK由中国香港特别行政区政府创新科技委员会向H.W.发起的计划。；RGC与H.W.的合作研究基金（CRF）。

(C6018-19GF); Theme-based Research Scheme (TRS) from RGC (project number: T13-602/21-N); Area of Excellence Scheme (AoE) from RGC (project number: AoE/M-402/20); Health and Medical Research Fund (HMRF) from Health Bureau of the Hong Kong Special Administrative Region, China (project Code: 10210906 and 08190626 to H.W.); Croucher Foundation Project (9509003) to C.K.K.; State Key Laboratory of Marine Pollution Seed Collaborative Research Fund (SCRF/0037, SCRF/0040, SCRF0070) to C.K.K.; City University of Hong Kong projects (7030001, 9678302 and 6000827) to C.K.K.; the Hong Kong Institute for Advanced Study, City University of Hong Kong [9360157] to C.K.K.Au.

（C6018-19GF）；RGC基于主题的研究计划（TRS）（项目编号：T13-602/21-N）；RGC的卓越领域计划（AoE）（项目编号：AoE/M-402/20）；中国香港特别行政区卫生局健康与医学研究基金（HMRF）（项目代码：10210906和08190626至H.W.）；克劳奇基金会项目（9509003）给C.K.K。；海洋污染种子合作研究基金国家重点实验室（SCRF/0037，SCRF/0040，SCRF0070）至C.K.K。；香港城市大学项目（70300019678302和6000827）给C.K.K。；香港城市大学香港高级研究院〔9360157〕致C.K.K.Au。

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PubMed Google ScholarContributionsY.W.Z., X.C., and H.W. conceived the research. Y.W.Z. designed and performed all computational analyses. K.L. constructed the DHX36-KO cell line. J.Z. constructed Structure-seq library, RBNS library, and performed experimental validation assisted by X.C.

PubMed谷歌学术贡献。W、 Z.，X.C。和H.W.构思了这项研究。Y、 W.Z.设计并执行了所有计算分析。K、 L.构建了DHX36-KO细胞系。J、 Z.构建了Structure-seq库，RBNS库，并在X.C.的协助下进行了实验验证。

Y.Q. conducted m6A inhibition and quantification. J.K. and Y.Z. constructed YTHDF1 CLIP-seq libraries. F.Y. analyzed the YTHDF1 CLIP-seq data. X.G. conducted the reporter assay assisted by X.C. H.S. supervised computational analyses. Y.D. and C.K.K. supervised RNA Structure-seq and RBNS experiments and analyses.

Y、 Q.进行m6A抑制和定量。J、 K.和Y.Z.构建了YTHDF1 CLIP-seq库。F、 Y.分析了YTHDF1 CLIP-seq数据。十、 G.在X.C.H.S.监督的计算分析的帮助下进行了报告分析。Y、 D.和C.K.K.监督RNA Structure-seq和RBNS实验和分析。

C.K.K. and H.W. supervised experimental validation. Y.W.Z., J.Z., X.C., C.K.K., and H.W. wrote the manuscript with input from all authors.Corresponding authorsCorrespondence to.

C、 K.K.和H.W.监督实验验证。Y、 W.Z.，J.Z.，X.C.，C.K.K。和H.W.在所有作者的意见下撰写了手稿。通讯作者通讯。

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Reprints and permissionsAbout this articleCite this articleZhang, Y., Zhao, J., Chen, X. et al. DHX36 binding induces RNA structurome remodeling and regulates RNA abundance via m6A reader YTHDF1.

转载和许可本文引用本文Zhang，Y.，Zhao，J.，Chen，X。等人。DHX36结合诱导RNA结构体重塑并通过m6A读取器YTHDF1调节RNA丰度。

Nat Commun 15, 9890 (2024). https://doi.org/10.1038/s41467-024-54000-yDownload citationReceived: 15 September 2023Accepted: 28 October 2024Published: 15 November 2024DOI: https://doi.org/10.1038/s41467-024-54000-yShare this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard.

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