Dynamic interactions between the RNA chaperone Hfq, small regulatory RNAs, and mRNAs in live bacterial cells
RNA-binding proteins play myriad roles in regulating RNAs and RNA-mediated functions. In bacteria, the RNA chaperone Hfq is an important post-transcriptional gene regulator. Using live-cell super-resolution imaging, we can distinguish Hfq binding to different sizes of cellular RNAs. We demonstrate t...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2021-02-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/64207 |
| _version_ | 1797991905512914944 |
|---|---|
| author | Seongjin Park Karine Prévost Emily M Heideman Marie-Claude Carrier Muhammad S Azam Matthew A Reyer Wei Liu Eric Massé Jingyi Fei |
| author_facet | Seongjin Park Karine Prévost Emily M Heideman Marie-Claude Carrier Muhammad S Azam Matthew A Reyer Wei Liu Eric Massé Jingyi Fei |
| author_sort | Seongjin Park |
| collection | DOAJ |
| description | RNA-binding proteins play myriad roles in regulating RNAs and RNA-mediated functions. In bacteria, the RNA chaperone Hfq is an important post-transcriptional gene regulator. Using live-cell super-resolution imaging, we can distinguish Hfq binding to different sizes of cellular RNAs. We demonstrate that under normal growth conditions, Hfq exhibits widespread mRNA-binding activity, with the distal face of Hfq contributing mostly to the mRNA binding in vivo. In addition, sRNAs can either co-occupy Hfq with the mRNA as a ternary complex, or displace the mRNA from Hfq in a binding face-dependent manner, suggesting mechanisms through which sRNAs rapidly access Hfq to induce sRNA-mediated gene regulation. Finally, our data suggest that binding of Hfq to certain mRNAs through its distal face can recruit RNase E to promote turnover of these mRNAs in a sRNA-independent manner, and such regulatory function of Hfq can be decoyed by sRNA competitors that bind strongly at the distal face. |
| first_indexed | 2024-04-11T08:59:44Z |
| format | Article |
| id | doaj.art-ab2800a10e57478fa40786d8382f020e |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T08:59:44Z |
| publishDate | 2021-02-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-ab2800a10e57478fa40786d8382f020e2022-12-22T04:32:49ZengeLife Sciences Publications LtdeLife2050-084X2021-02-011010.7554/eLife.64207Dynamic interactions between the RNA chaperone Hfq, small regulatory RNAs, and mRNAs in live bacterial cellsSeongjin Park0https://orcid.org/0000-0002-4298-1770Karine Prévost1Emily M Heideman2Marie-Claude Carrier3https://orcid.org/0000-0002-3878-4141Muhammad S Azam4Matthew A Reyer5Wei Liu6Eric Massé7https://orcid.org/0000-0002-5253-1415Jingyi Fei8https://orcid.org/0000-0002-9775-3820Department of Biochemistry and Molecular Biology, The University of Chicago, Chicago, United StatesRNA Group, Department of Biochemistry, University of Sherbrooke, Sherbrooke, CanadaDepartment of Biochemistry and Molecular Biology, The University of Chicago, Chicago, United StatesRNA Group, Department of Biochemistry, University of Sherbrooke, Sherbrooke, CanadaDepartment of Biochemistry and Molecular Biology, The University of Chicago, Chicago, United StatesInstitute for Biophysical Dynamics, The University of Chicago, Chicago, United StatesDepartment of Biochemistry and Molecular Biology, The University of Chicago, Chicago, United StatesRNA Group, Department of Biochemistry, University of Sherbrooke, Sherbrooke, CanadaDepartment of Biochemistry and Molecular Biology, The University of Chicago, Chicago, United States; Institute for Biophysical Dynamics, The University of Chicago, Chicago, United StatesRNA-binding proteins play myriad roles in regulating RNAs and RNA-mediated functions. In bacteria, the RNA chaperone Hfq is an important post-transcriptional gene regulator. Using live-cell super-resolution imaging, we can distinguish Hfq binding to different sizes of cellular RNAs. We demonstrate that under normal growth conditions, Hfq exhibits widespread mRNA-binding activity, with the distal face of Hfq contributing mostly to the mRNA binding in vivo. In addition, sRNAs can either co-occupy Hfq with the mRNA as a ternary complex, or displace the mRNA from Hfq in a binding face-dependent manner, suggesting mechanisms through which sRNAs rapidly access Hfq to induce sRNA-mediated gene regulation. Finally, our data suggest that binding of Hfq to certain mRNAs through its distal face can recruit RNase E to promote turnover of these mRNAs in a sRNA-independent manner, and such regulatory function of Hfq can be decoyed by sRNA competitors that bind strongly at the distal face.https://elifesciences.org/articles/64207hfqsRNAgene regulationsingle-particle trackingsuper-resolution imaging |
| spellingShingle | Seongjin Park Karine Prévost Emily M Heideman Marie-Claude Carrier Muhammad S Azam Matthew A Reyer Wei Liu Eric Massé Jingyi Fei Dynamic interactions between the RNA chaperone Hfq, small regulatory RNAs, and mRNAs in live bacterial cells eLife hfq sRNA gene regulation single-particle tracking super-resolution imaging |
| title | Dynamic interactions between the RNA chaperone Hfq, small regulatory RNAs, and mRNAs in live bacterial cells |
| title_full | Dynamic interactions between the RNA chaperone Hfq, small regulatory RNAs, and mRNAs in live bacterial cells |
| title_fullStr | Dynamic interactions between the RNA chaperone Hfq, small regulatory RNAs, and mRNAs in live bacterial cells |
| title_full_unstemmed | Dynamic interactions between the RNA chaperone Hfq, small regulatory RNAs, and mRNAs in live bacterial cells |
| title_short | Dynamic interactions between the RNA chaperone Hfq, small regulatory RNAs, and mRNAs in live bacterial cells |
| title_sort | dynamic interactions between the rna chaperone hfq small regulatory rnas and mrnas in live bacterial cells |
| topic | hfq sRNA gene regulation single-particle tracking super-resolution imaging |
| url | https://elifesciences.org/articles/64207 |
| work_keys_str_mv | AT seongjinpark dynamicinteractionsbetweenthernachaperonehfqsmallregulatoryrnasandmrnasinlivebacterialcells AT karineprevost dynamicinteractionsbetweenthernachaperonehfqsmallregulatoryrnasandmrnasinlivebacterialcells AT emilymheideman dynamicinteractionsbetweenthernachaperonehfqsmallregulatoryrnasandmrnasinlivebacterialcells AT marieclaudecarrier dynamicinteractionsbetweenthernachaperonehfqsmallregulatoryrnasandmrnasinlivebacterialcells AT muhammadsazam dynamicinteractionsbetweenthernachaperonehfqsmallregulatoryrnasandmrnasinlivebacterialcells AT matthewareyer dynamicinteractionsbetweenthernachaperonehfqsmallregulatoryrnasandmrnasinlivebacterialcells AT weiliu dynamicinteractionsbetweenthernachaperonehfqsmallregulatoryrnasandmrnasinlivebacterialcells AT ericmasse dynamicinteractionsbetweenthernachaperonehfqsmallregulatoryrnasandmrnasinlivebacterialcells AT jingyifei dynamicinteractionsbetweenthernachaperonehfqsmallregulatoryrnasandmrnasinlivebacterialcells |