Systematic characterization of the composition and dynamics of processing body-associated mRNAs

Zhiyuan Sun, Xiaozhen Wen, Yanping Li, Xiaoxin Xie, Peng Dong, Yi Shu, Shuye Tian, Jiao Yang, Yangfan Lin, Mengran Wang, Feifei Jiang, Qionghua Zhu, Huanhuan Cui, Jixian Zhai, Yuhui Hu, Liang Fang () and Wei Chen ()
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Zhiyuan Sun: Southern University of Science and Technology
Xiaozhen Wen: Southern University of Science and Technology
Yanping Li: Southern University of Science and Technology
Xiaoxin Xie: Southern University of Science and Technology
Peng Dong: Southern University of Science and Technology
Yi Shu: Southern University of Science and Technology
Shuye Tian: Southern University of Science and Technology
Jiao Yang: Southern University of Science and Technology
Yangfan Lin: Southern University of Science and Technology
Mengran Wang: Southern University of Science and Technology
Feifei Jiang: Southern University of Science and Technology
Qionghua Zhu: Southern University of Science and Technology
Huanhuan Cui: Southern University of Science and Technology
Jixian Zhai: Southern University of Science and Technology
Yuhui Hu: Southern University of Science and Technology
Liang Fang: Southern University of Science and Technology
Wei Chen: Southern University of Science and Technology

Nature Communications, 2025, vol. 16, issue 1, 1-22

Abstract: Abstract Processing bodies (PBs) are dynamic, membraneless organelles consisting of RNAs and proteins. While PB proteins have been extensively characterized, the methods for systematically profiling PB-associated RNAs are limited. To address this, we developed PB-TRIBE-STAMP, a tool based on two orthogonal RNA editing enzymes. Simultaneously applying APOBEC1-DDX6 and LSM14A-ADAR2dd, PB-TRIBE-STAMP identified 1,639 and 2,577 PB-associated mRNAs in HCT116 and HEK293T cells, respectively. Further biochemical isolation of PBs followed by RNA-seq validated that edited transcripts of these mRNAs were indeed enriched in PBs. Integration of PB-TRIBE-STAMP with long-read sequencing revealed that the PB-associated transcripts possessed shorter poly(A)-tails. Many mRNA 3’ UTR isoforms exhibited isoform-specific PB association patterns. Moreover, we established a TRIBE-ID-based tool to characterize the mRNA-LSM14A/PB association at high temporal resolution and unveiled a higher splicing efficiency of LSM14A-associated XBP1 transcripts during unfolded protein response (UPR). Finally, based on single-cell LSM14A-TRIBE-ID (sc-LSM14A-TRIBE-ID), we demonstrated the dynamic pattern of mRNA-LSM14A/PB association during cell cycle progression.

Date: 2025
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DOI: 10.1038/s41467-025-64848-3

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