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Dynamic Recruitment of Single RNAs to Processing Bodies Depends on RNA Functionality
Sethuramasundaram Pitchiaya1, Marcio D A Mourao2, Ameya P Jalihal3
1Single Molecule Analysis Group, Department of Chemistry, University of Michigan, Ann Arbor, MI 48109-1055, USA; Michigan Center for Translational Pathology, University of Michigan Medical School, Ann Arbor, MI 48109-1055, USA; Department of Pathology, University of Michigan, Ann Arbor, MI 48109, USA; Comprehensive Cancer Center, University of Michigan, Ann Arbor, MI 48109, USA.
Molecular Cell
|April 7, 2019
Summary
Cellular RNA granules called processing bodies (PBs) sequester unused microRNAs (miRNAs) for surveillance. This study reveals dynamic RNA localization within PBs, impacting gene silencing and turnover.
Area of Science:
- Molecular Biology
- Cell Biology
- RNA Biology
Background:
- Cellular RNAs, including microRNAs (miRNAs), messenger RNAs (mRNAs), and long non-coding RNAs (lncRNAs), are frequently found in cytoplasmic ribonucleoprotein (RNP) granules known as processing bodies (PBs).
- Processing bodies are membrane-less organelles involved in RNA processing, storage, and decay, but the dynamic behavior of individual RNA species within them remains incompletely understood.
Purpose of the Study:
- To investigate the dynamic localization patterns of individual miRNAs, mRNAs, and lncRNAs within processing bodies.
- To elucidate the relationship between RNA localization within PBs and gene silencing mechanisms.
- To understand the role of PBs in RNA metabolism and the regulation of RNA fate.
Main Methods:
- Intracellular single-molecule fluorescence microscopy was employed to track the real-time localization of individual RNA molecules (miRNAs, mRNAs, lncRNAs) within living cells.
- Computational modeling was utilized to analyze the dynamics of RNA localization and its impact on gene silencing.
- Supporting experimental approaches were used to validate findings related to RNA partitioning and phase separation within PBs.
Main Results:
- Unused miRNAs exhibit stable binding to processing bodies, suggesting a role in miRNA sequestration and surveillance.
- Functional miRNAs, repressed mRNAs, and lncRNAs show both transient and stable localization within PB cores and peripheries, with varying degrees.
- mRNA localization dynamics within PBs are significantly influenced by translation potential and the position of miRNA target sites.
- RNA partitioning within the PB phase was found to attenuate mRNA silencing, indicating that active mRNA turnover primarily occurs outside PBs.
Conclusions:
- Processing bodies primarily function in sequestering unused miRNAs for cellular surveillance rather than active mRNA decay.
- The dynamic localization of various RNA species within PBs is a key factor influencing gene silencing efficacy.
- This study provides a single-molecule resolution framework for understanding the assembly and function of RNP granules via phase separation.
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