Structural basis of rotavirus RNA chaperone displacement and RNA annealing

Bravo JPK, Bartnik K, Venditti L, Acker J, Gail EH, Colyer A, Davidovich C, Lamb DC, Tuma R, Calabrese AN, Borodavka A. 2021. Structural basis of rotavirus RNA chaperone displacement and RNA annealing. Proceedings of the National Academy of Sciences. 118(41), e2100198118.

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Author
Bravo, JackISTA ; Bartnik, Kira; Venditti, Luca; Acker, Julia; Gail, Emma H.; Colyer, Alice; Davidovich, Chen; Lamb, Don C.; Tuma, Roman; Calabrese, Antonio N.; Borodavka, Alexander
Abstract
Rotavirus genomes are distributed between 11 distinct RNA molecules, all of which must be selectively copackaged during virus assembly. This likely occurs through sequence-specific RNA interactions facilitated by the RNA chaperone NSP2. Here, we report that NSP2 autoregulates its chaperone activity through its C-terminal region (CTR) that promotes RNA–RNA interactions by limiting its helix-unwinding activity. Unexpectedly, structural proteomics data revealed that the CTR does not directly interact with RNA, while accelerating RNA release from NSP2. Cryo–electron microscopy reconstructions of an NSP2–RNA complex reveal a highly conserved acidic patch on the CTR, which is poised toward the bound RNA. Virus replication was abrogated by charge-disrupting mutations within the acidic patch but completely restored by charge-preserving mutations. Mechanistic similarities between NSP2 and the unrelated bacterial RNA chaperone Hfq suggest that accelerating RNA dissociation while promoting intermolecular RNA interactions may be a widespread strategy of RNA chaperone recycling.
Publishing Year
Date Published
2021-10-06
Journal Title
Proceedings of the National Academy of Sciences
Volume
118
Issue
41
Article Number
e2100198118
ISSN
eISSN
IST-REx-ID

Cite this

Bravo JPK, Bartnik K, Venditti L, et al. Structural basis of rotavirus RNA chaperone displacement and RNA annealing. Proceedings of the National Academy of Sciences. 2021;118(41). doi:10.1073/pnas.2100198118
Bravo, J. P. K., Bartnik, K., Venditti, L., Acker, J., Gail, E. H., Colyer, A., … Borodavka, A. (2021). Structural basis of rotavirus RNA chaperone displacement and RNA annealing. Proceedings of the National Academy of Sciences. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.2100198118
Bravo, Jack Peter Kelly, Kira Bartnik, Luca Venditti, Julia Acker, Emma H. Gail, Alice Colyer, Chen Davidovich, et al. “Structural Basis of Rotavirus RNA Chaperone Displacement and RNA Annealing.” Proceedings of the National Academy of Sciences. Proceedings of the National Academy of Sciences, 2021. https://doi.org/10.1073/pnas.2100198118.
J. P. K. Bravo et al., “Structural basis of rotavirus RNA chaperone displacement and RNA annealing,” Proceedings of the National Academy of Sciences, vol. 118, no. 41. Proceedings of the National Academy of Sciences, 2021.
Bravo JPK, Bartnik K, Venditti L, Acker J, Gail EH, Colyer A, Davidovich C, Lamb DC, Tuma R, Calabrese AN, Borodavka A. 2021. Structural basis of rotavirus RNA chaperone displacement and RNA annealing. Proceedings of the National Academy of Sciences. 118(41), e2100198118.
Bravo, Jack Peter Kelly, et al. “Structural Basis of Rotavirus RNA Chaperone Displacement and RNA Annealing.” Proceedings of the National Academy of Sciences, vol. 118, no. 41, e2100198118, Proceedings of the National Academy of Sciences, 2021, doi:10.1073/pnas.2100198118.
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