RNA Structure Directs RNA Partitioning and is Actively Disrupted inside Stress Granules to Enable Cellular Recovery
Posted on: 25 September 2025
Preprint posted on 5 June 2025
Shape-Shifting RNAs: Structural Cues Drive Partitioning and Active Remodeling in Stress Granules for Rapid Cellular Recovery
Selected by Mohammed JALLOH
Categories: cell biology, molecular biology
Why I picked this preprint
I chose to highlight this preprint because it resolves a fundamental paradox in stress granule (SG) biology using innovative RNA structure probing techniques. While previous models suggested that promiscuous RNA-RNA interactions drive SG formation through aggregation, this study reveals the opposite: stress granule-enriched RNAs are maintained in a single-stranded state through active unwinding mechanisms. This counterintuitive finding reframes our understanding of how RNA structure controls biomolecular condensate assembly and dissolution, with implications for cellular stress responses and neurodegenerative diseases.
Background
Stress granules (SGs) are cytoplasmic RNA-protein condensates that form when translation initiation is inhibited. They may promote survival by sequestering mRNAs and regulatory factors, but the role of RNA in their assembly remains debated. Some suggest nonspecific RNA-RNA aggregation, while others propose specific mechanisms. Prolonged SGs contribute to neurodegenerative protein aggregation, yet direct measurements of RNA structure within them remain technically challenging.
Main goal
The authors sought to comprehensively map RNA structures and RNA-RNA interactions during SG formation and disassembly, using arsenite-induced oxidative stress as a model system.
Key Findings
RNA structures become more paired globally but remain single-stranded in stress granules
Using in vivo click Selective 2-Hydroxyl Acylation and Profiling Experiment (icSHAPE), the authors mapped RNA structures in HeLa cells before, during, and after sodium arsenite treatment. Globally, ~69% of structure-changing bases became more double-stranded upon stress, particularly in coding regions where ribosomes dissociate (preprint-Figure 1G-H). However, subcellular fractionation revealed a striking paradox: RNAs within stress granules remained significantly more single-stranded than those in the soluble cytoplasm (preprint-Figure 2B-C). This single-strandedness was not simply due to RNA concentration effects, as SGs contain higher RNA densities than the cytosol. The maintenance of single-stranded RNA within SGs challenges models based on promiscuous RNA aggregation.
Single-stranded RNAs are preferentially recruited to stress granules
The authors discovered that stress granule-enriched RNAs exhibit higher single-strandedness even before stress induction (preprint-Figure 2H). To test causality, they transfected synthetic RNAs of identical length and GC content but different structural propensities. The single-stranded RNA showed significantly greater enrichment in SGs compared to the structured RNA (preprint-Figure 2K), directly demonstrating that RNA structure controls partitioning. This recruitment mechanism appears to be independent of other known factors like AU content and transcript length.
Stress granule environment actively maintains RNA single-strandedness
Using a tunable USP10 peptide system to block SG formation, the authors showed that the single-strandedness of stress granule-enriched RNAs depends on the granule environment itself. When stress granules were prevented from forming, these same RNAs became more structured during stress (preprint-Figure 3D-E). Clustering analysis revealed that RNAs requiring stress granules to maintain single-strandedness were the most highly enriched in these structures (preprint-Figure 3F), suggesting active unwinding mechanisms within granules.
Reduced intermolecular RNA-RNA interactions in stress granules
SPLASH (proximity ligation sequencing) analysis revealed that stress granule-enriched RNAs form fewer intra- and intermolecular RNA-RNA interactions compared to depleted RNAs (preprint-Figure 4C-D). Network analysis showed that stress granule-enriched RNAs have simpler interaction patterns with shorter intramolecular pairings (preprint-Figure 4E-F). The authors demonstrated this principle using MRFAP1 and MRFAP1L1 RNAs, which showed decreased intermolecular pairing during stress as they adopted more local secondary structures (preprint-Figure 4H).
SRSF1 mediates single-stranded RNA recruitment to stress granules
Through motif enrichment and eCLIP analysis, the authors identified SRSF1 as a key RNA-binding protein that preferentially binds single-stranded regions and facilitates stress granule recruitment (preprint-Figure 5A-C). SRSF1 targets showed increased single-strandedness and stress granule enrichment, with transcripts containing more SRSF1 binding sites exhibiting greater granule partitioning (preprint-Figure 5H-I). Importantly, SRSF1 knockdown reduced stress granule formation under mild stress conditions (preprint-Figure 5K-L), confirming its functional role in granule assembly.
Conclusion and implications
This study fundamentally reframes the role of RNA in stress granule biology. Rather than forming through promiscuous RNA aggregation, stress granules maintain RNAs in a single-stranded state through coordinated recruitment and unwinding mechanisms. SRSF1 facilitates the initial partitioning of single-stranded RNAs, while DDX3X and other helicases actively maintain this state within granules. This organization enables rapid granule dissolution and cellular recovery when stress is removed, highlighting the importance of RNA structural control in cellular stress responses.
Questions/Future Directions
• How do other RNA helicases contribute to stress granule RNA unwinding, and are there redundant pathways?
• What determines the specificity of SRSF1 for recruiting particular RNAs to stress granules?
• How does this RNA structural control mechanism dysfunction in neurodegenerative diseases with persistent stress granules?
References
1. Anderson, P., Kedersha, N., and Ivanov, P. (2015). Stress granules, P-bodies and cancer. Biochim Biophys Acta 1849, 861-870.
2. Protter, D.S.W., and Parker, R. (2016). Principles and Properties of Stress Granules. Trends Cell Biol 26, 668-679.
3. Jain, S., Wheeler, J.R., Walters, R.W., Agrawal, A., Barsic, A., and Parker, R. (2016). ATPase-Modulated Stress Granules Contain a Diverse Proteome and Substructure. Cell 164, 487-498.
4. Yang, P., Mathieu, C., Kolaitis, R.M., Zhang, P., Messing, J., Yurtsever, U., Yang, Z., Wu, J., Li, Y., Pan, Q., et al. (2020). G3BP1 Is a Tunable Switch that Triggers Phase Separation to Assemble Stress Granules. Cell 181, 325-345.
5. Khong, A., Matheny, T., Jain, S., Mitchell, S.F., Wheeler, J.R., and Parker, R. (2017). The Stress Granule Transcriptome Reveals Principles of mRNA Accumulation in Stress Granules. Mol Cell 68, 808-820.
6. Samir, P., Kesavardhana, S., Patmore, D.M., Gingras, S., Malireddi, R.K.S., Karki, R., Guy, C.S., Briard, B., Place, D.E., Bhattacharya, A., et al. (2019). DDX3X acts as a live-or-die checkpoint in stressed cells by regulating NLRP3 inflammasome. Nature 573, 590-594.
doi: https://doi.org/10.1242/prelights.41459
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