Structural model of an mRNA in complex with the bacterial chaperone Hfq
Abstract
The Sm-like protein Hfq (host factor Q-beta phage) facilitates regulation by bacterial small noncoding RNAs (sRNAs) in response to stress and other environmental signals. In this paper, we present a low-resolution model of Escherichia coli Hfq bound to the rpoS mRNA, a bacterial stress response gene that is targeted by three different sRNAs. Selective 2'-hydroxyl acylation and primer extension, small-angle X-ray scattering, and Monte Carlo molecular dynamics simulations show that the distal face and lateral rim of Hfq interact with three sites in the rpoS leader, folding the RNA into a compact tertiary structure. These interactions are needed for sRNA regulation of rpoS translation and position the sRNA target adjacent to an sRNA binding region on the proximal face of Hfq. Finally, our results show how Hfq specifically distorts the structure of the rpoS mRNA to enable sRNA base pairing and translational control.
- Authors:
-
- Johns Hopkins Univ., Baltimore, MD (United States). Cell, Molecular and Developmental Biology and Biophysics Program
- National Inst. of Standards and Technology (NIST), Gaithersburg, MD (United States). Center for Neutron Research
- National Inst. of Health, Frederick, MD (United States). National Cancer Inst. Center for Cancer Research. Structural Biophysics Lab.
- Johns Hopkins Univ., Baltimore, MD (United States). T. C. Jenkins Dept. of Biophysics
- Publication Date:
- Research Org.:
- Johns Hopkins Univ., Baltimore, MD (United States)
- Sponsoring Org.:
- USDOE; National Inst. of Health (NIH) (United States); National Science Foundation (NSF); Engineering and Physical Sciences Research Council (EPSRC)
- Contributing Org.:
- National Inst. of Standards and Technology (NIST), Gaithersburg, MD (United States); National Inst. of Health, Frederick, MD (United States)
- OSTI Identifier:
- 1168867
- Grant/Contract Number:
- AC02-06CH11357; R01 GM46686; CHE-1265821; EP/K039121/1
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 111; Journal Issue: 48; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences, Washington, DC (United States)
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; small noncoding RNA; RNA–protein interactions; SAXS; Lsm protein; bacterial posttranscriptional control
Citation Formats
Peng, Yi, Curtis, Joseph E., Fang, Xianyang, and Woodson, Sarah A. Structural model of an mRNA in complex with the bacterial chaperone Hfq. United States: N. p., 2014.
Web. doi:10.1073/pnas.1410114111.
Peng, Yi, Curtis, Joseph E., Fang, Xianyang, & Woodson, Sarah A. Structural model of an mRNA in complex with the bacterial chaperone Hfq. United States. https://doi.org/10.1073/pnas.1410114111
Peng, Yi, Curtis, Joseph E., Fang, Xianyang, and Woodson, Sarah A. Mon .
"Structural model of an mRNA in complex with the bacterial chaperone Hfq". United States. https://doi.org/10.1073/pnas.1410114111. https://www.osti.gov/servlets/purl/1168867.
@article{osti_1168867,
title = {Structural model of an mRNA in complex with the bacterial chaperone Hfq},
author = {Peng, Yi and Curtis, Joseph E. and Fang, Xianyang and Woodson, Sarah A.},
abstractNote = {The Sm-like protein Hfq (host factor Q-beta phage) facilitates regulation by bacterial small noncoding RNAs (sRNAs) in response to stress and other environmental signals. In this paper, we present a low-resolution model of Escherichia coli Hfq bound to the rpoS mRNA, a bacterial stress response gene that is targeted by three different sRNAs. Selective 2'-hydroxyl acylation and primer extension, small-angle X-ray scattering, and Monte Carlo molecular dynamics simulations show that the distal face and lateral rim of Hfq interact with three sites in the rpoS leader, folding the RNA into a compact tertiary structure. These interactions are needed for sRNA regulation of rpoS translation and position the sRNA target adjacent to an sRNA binding region on the proximal face of Hfq. Finally, our results show how Hfq specifically distorts the structure of the rpoS mRNA to enable sRNA base pairing and translational control.},
doi = {10.1073/pnas.1410114111},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 48,
volume = 111,
place = {United States},
year = {Mon Nov 17 00:00:00 EST 2014},
month = {Mon Nov 17 00:00:00 EST 2014}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 56 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Small RNA Regulators and the Bacterial Response to Stress
journal, January 2006
- Gottesman, S.; McCULLEN, C. A.; Guillier, M.
- Cold Spring Harbor Symposia on Quantitative Biology, Vol. 71, Issue 0
Physiological roles of small RNA molecules
journal, April 2014
- Michaux, C.; Verneuil, N.; Hartke, A.
- Microbiology, Vol. 160, Issue Pt_6
Controlling mRNA stability and translation with small, noncoding RNAs
journal, April 2004
- Storz, Gisela; Opdyke, Jason A.; Zhang, Aixia
- Current Opinion in Microbiology, Vol. 7, Issue 2
Hfq and its constellation of RNA
journal, August 2011
- Vogel, Jörg; Luisi, Ben F.
- Nature Reviews Microbiology, Vol. 9, Issue 8
Archaeal and eukaryotic homologs of Hfq: A structural and evolutionary perspective on Sm function
journal, April 2013
- Mura, Cameron; Randolph, Peter S.; Patterson, Jennifer
- RNA Biology, Vol. 10, Issue 4
Structure and RNA-binding properties of the bacterial LSm protein Hfq
journal, April 2013
- Sauer, Evelyn
- RNA Biology, Vol. 10, Issue 4
Structure of Escherichia coli Hfq bound to polyriboadenylate RNA
journal, November 2009
- Link, T. M.; Valentin-Hansen, P.; Brennan, R. G.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 46
Escherichia coli Hfq has distinct interaction surfaces for DsrA, rpoS and poly(A) RNAs
journal, November 2004
- Mikulecky, Peter J.; Kaw, Meenakshi K.; Brescia, Cristin C.
- Nature Structural & Molecular Biology, Vol. 11, Issue 12
Genomic SELEX for Hfq-binding RNAs identifies genomic aptamers predominantly in antisense transcripts
journal, March 2010
- Lorenz, C.; Gesell, T.; Zimmermann, B.
- Nucleic Acids Research, Vol. 38, Issue 11
Structural basis for RNA 3′-end recognition by Hfq
journal, July 2011
- Sauer, Evelyn; Weichenrieder, Oliver
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 32
Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: a bacterial Sm-like protein
journal, July 2002
- Schumacher, M. A.
- The EMBO Journal, Vol. 21, Issue 13
The functional Hfq-binding module of bacterial sRNAs consists of a double or single hairpin preceded by a U-rich sequence and followed by a 3' poly(U) tail
journal, March 2012
- Ishikawa, H.; Otaka, H.; Maki, K.
- RNA, Vol. 18, Issue 5
PolyU tail of rho-independent terminator of bacterial small RNAs is essential for Hfq action
journal, July 2011
- Otaka, Hironori; Ishikawa, Hirokazu; Morita, Teppei
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 32
Small RNA binding to the lateral surface of Hfq hexamers and structural rearrangements upon mRNA target recognition
journal, May 2012
- Sauer, E.; Schmidt, S.; Weichenrieder, O.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 24
Conserved arginines on the rim of Hfq catalyze base pair formation and exchange
journal, June 2013
- Panja, Subrata; Schu, Daniel J.; Woodson, Sarah A.
- Nucleic Acids Research, Vol. 41, Issue 15
The RpoS-Mediated General Stress Response in Escherichia coli
journal, October 2011
- Battesti, Aurelia; Majdalani, Nadim; Gottesman, Susan
- Annual Review of Microbiology, Vol. 65, Issue 1
Riboregulation in Escherichia coli: DsrA RNA acts by RNA:RNA interactions at multiple loci
journal, October 1998
- Lease, R. A.; Cusick, M. E.; Belfort, M.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 21
DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism, independent of its action as an antisilencer of transcription
journal, October 1998
- Majdalani, N.; Cunning, C.; Sledjeski, D.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 21
Positive regulation by small RNAs and the role of Hfq
journal, May 2010
- Soper, T.; Mandin, P.; Majdalani, N.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 21
The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA
journal, July 2008
- Soper, T. J.; Woodson, S. A.
- RNA, Vol. 14, Issue 9
Cycling of the Sm-like Protein Hfq on the DsrA Small Regulatory RNA
journal, December 2004
- Lease, Richard A.; Woodson, Sarah A.
- Journal of Molecular Biology, Vol. 344, Issue 5
Major role for mRNA binding and restructuring in sRNA recruitment by Hfq
journal, June 2011
- Soper, T. J.; Doxzen, K.; Woodson, S. A.
- RNA, Vol. 17, Issue 8
Effect of Hfq on RprA− rpoS mRNA Pairing: Hfq−RNA Binding and the Influence of the 5′ rpoS mRNA Leader Region †
journal, October 2008
- Updegrove, Taylor; Wilf, Nabil; Sun, Xueguang
- Biochemistry, Vol. 47, Issue 43
Positional Effects of AAN Motifs in rpoS Regulation by sRNAs and Hfq
journal, January 2014
- Peng, Yi; Soper, Toby J.; Woodson, Sarah A.
- Journal of Molecular Biology, Vol. 426, Issue 2
Mapping Local Nucleotide Flexibility by Selective Acylation of 2‘-Amine Substituted RNA
journal, January 2000
- Chamberlin, Stacy I.; Weeks, Kevin M.
- Journal of the American Chemical Society, Vol. 122, Issue 2
Duplex formation between the sRNA DsrA and rpoS mRNA is not sufficient for efficient RpoS synthesis at low temperature
journal, December 2013
- Hämmerle, Hermann; Večerek, Branislav; Resch, Armin
- RNA Biology, Vol. 10, Issue 12
Fingerprinting Noncanonical and Tertiary RNA Structures by Differential SHAPE Reactivity
journal, August 2012
- Steen, Kady-Ann; Rice, Greggory M.; Weeks, Kevin M.
- Journal of the American Chemical Society, Vol. 134, Issue 32
The influence of Escherichia coli Hfq mutations on RNA binding and sRNA•mRNA duplex formation in rpoS riboregulation
journal, October 2011
- Updegrove, Taylor B.; Wartell, Roger M.
- Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1809, Issue 10
Structural insights into the dynamics and function of the C-terminus of the E. coli RNA chaperone Hfq
journal, February 2011
- Beich-Frandsen, Mads; Večerek, Branislav; Konarev, Petr V.
- Nucleic Acids Research, Vol. 39, Issue 11
Hfq binding changes the structure of Escherichia coli small noncoding RNAs OxyS and RprA, which are involved in the riboregulation of rpoS
journal, June 2013
- Henderson, C. A.; Vincent, H. A.; Casamento, A.
- RNA, Vol. 19, Issue 8
NADPH oxidase activator p67phox behaves in solution as a multidomain protein with semi-flexible linkers
journal, January 2010
- Durand, Dominique; Vivès, Corinne; Cannella, Dominique
- Journal of Structural Biology, Vol. 169, Issue 1
Cooperation of Escherichia coli Hfq hexamers in DsrA binding
journal, October 2011
- Wang, W.; Wang, L.; Zou, Y.
- Genes & Development, Vol. 25, Issue 19
SASSIE: A program to study intrinsically disordered biological molecules and macromolecular ensembles using experimental scattering restraints
journal, February 2012
- Curtis, Joseph E.; Raghunandan, Sindhu; Nanda, Hirsh
- Computer Physics Communications, Vol. 183, Issue 2
The MC-Fold and MC-Sym pipeline infers RNA structure from sequence data
journal, March 2008
- Parisien, Marc; Major, François
- Nature, Vol. 452, Issue 7183
Global Rigid Body Modeling of Macromolecular Complexes against Small-Angle Scattering Data
journal, August 2005
- Petoukhov, Maxim V.; Svergun, Dmitri I.
- Biophysical Journal, Vol. 89, Issue 2
An Upstream Hfq Binding Site in the fhlA mRNA Leader Region Facilitates the OxyS-fhlA Interaction
journal, September 2010
- Salim, Nilshad N.; Feig, Andrew L.
- PLoS ONE, Vol. 5, Issue 9
Antagonistic functions between the RNA chaperone Hfq and an sRNA regulate sensitivity to the antibiotic colicin
journal, September 2013
- Salvail, Hubert; Caron, Marie-Pier; Bélanger, Justine
- The EMBO Journal, Vol. 32, Issue 20
Works referencing / citing this record:
Hfq chaperone brings speed dating to bacterial sRNA
journal, April 2018
- Santiago-Frangos, Andrew; Woodson, Sarah A.
- Wiley Interdisciplinary Reviews: RNA, Vol. 9, Issue 4
RNA-based recognition and targeting: sowing the seeds of specificity
journal, February 2017
- Gorski, Stanislaw A.; Vogel, Jörg; Doudna, Jennifer A.
- Nature Reviews Molecular Cell Biology, Vol. 18, Issue 4
RNA-binding proteins in bacteria
journal, July 2018
- Holmqvist, Erik; Vogel, Jörg
- Nature Reviews Microbiology, Vol. 16, Issue 10
Characterization of RNA-binding properties of the archaeal Hfq-like protein from Methanococcus jannaschii
journal, July 2016
- Nikulin, Alexey; Mikhailina, Alisa; Lekontseva, Natalia
- Journal of Biomolecular Structure and Dynamics, Vol. 35, Issue 8
The small RNA, SdsR, acts as a novel type of toxin in Escherichia coli
journal, October 2018
- Choi, Jee Soo; Kim, Wonkyong; Suk, Shinae
- RNA Biology, Vol. 15, Issue 10
Target activation by regulatory RNAs in bacteria
journal, May 2015
- Papenfort, Kai; Vanderpool, Carin K.
- FEMS Microbiology Reviews, Vol. 39, Issue 3
An RNA-dependent mechanism for transient expression of bacterial translocation filaments
journal, February 2018
- Wang, Dai; McAteer, Sean P.; Wawszczyk, Agata B.
- Nucleic Acids Research, Vol. 46, Issue 7
A metastable rRNA junction essential for bacterial 30S biogenesis
journal, February 2018
- Sharma, Indra Mani; Rappé, Mollie C.; Addepalli, Balasubrahmanyam
- Nucleic Acids Research, Vol. 46, Issue 10
Dynamic interactions between the RNA chaperone Hfq, small regulatory RNAs and mRNAs in live bacterial cells
journal, January 2020
- Park, Seongjin; Prévost, Karine; Heideman, Emily M.
- eLife
Stability of local secondary structure determines selectivity of viral RNA chaperones
journal, May 2018
- Bravo, Jack P. K.; Borodavka, Alexander; Barth, Anders
- Nucleic Acids Research
Hfq Globally Binds and Destabilizes sRNAs and mRNAs in Yersinia pestis
journal, July 2019
- Han, Yanping; Chen, Dong; Yan, Yanfeng
- mSystems, Vol. 4, Issue 4
Mechanism to control the cell lysis and the cell survival strategy in stationary phase under heat stress
journal, October 2015
- Noor, Rashed
- SpringerPlus, Vol. 4, Issue 1
Conformation and mechanical property of rpoS mRNA inhibitory stem studied by optical tweezers and X-ray scattering
journal, September 2019
- Hu, Xinyao; Li, Xuanling; Yang, Lingna
- PLOS ONE, Vol. 14, Issue 9
Hfq‐dependent mRNA unfolding promotes sRNA ‐based inhibition of translation
journal, February 2019
- Hoekzema, Mirthe; Romilly, Cédric; Holmqvist, Erik
- The EMBO Journal, Vol. 38, Issue 7
Recognition of the small regulatory RNA RydC by the bacterial Hfq protein
journal, December 2014
- Dimastrogiovanni, Daniela; Fröhlich, Kathrin S.; Bandyra, Katarzyna J.
- eLife, Vol. 3
Stability of local secondary structure determines selectivity of viral RNA chaperones
journal, May 2018
- Bravo, Jack P. K.; Borodavka, Alexander; Barth, Anders
- Nucleic Acids Research, Vol. 46, Issue 15
Characterization of RNA-binding properties of the archaeal Hfq-like protein from Methanococcus jannaschii
text, January 2016
- Nikulin, Alexey; Mikhailina, Alisa; Lekontseva, Natalia
- Taylor & Francis
Characterization of RNA-binding properties of the archaeal Hfq-like protein from Methanococcus jannaschii
text, January 2016
- Nikulin, Alexey; Mikhailina, Alisa; Lekontseva, Natalia
- Taylor & Francis
Nucleoid and cytoplasmic localization of small RNAs inEscherichia coli
journal, January 2017
- Sheng, Huanjie; Stauffer, Weston T.; Hussein, Razika
- Nucleic Acids Research
The important conformational plasticity of DsrA sRNA for adapting multiple target regulation
journal, June 2017
- Wu, Pengzhi; Liu, Xiaodan; Yang, Lingna
- Nucleic Acids Research, Vol. 45, Issue 16
Stability of local secondary structure determines selectivity of viral RNA chaperones
journal, May 2018
- Bravo, Jack P. K.; Borodavka, Alexander; Barth, Anders
- Nucleic Acids Research, Vol. 46, Issue 15
Hfq Globally Binds and Destabilizes sRNAs and mRNAs in Yersinia pestis
journal, July 2019
- Han, Yanping; Chen, Dong; Yan, Yanfeng
- mSystems, Vol. 4, Issue 4
Genome-wide analyses of small non-coding RNAs in streptococci
journal, May 2015
- Patenge, Nadja; Pappesch, Roberto; Khani, Afsaneh
- Frontiers in Genetics, Vol. 06
Recognition of the small regulatory RNA RydC by the bacterial Hfq protein
journal, December 2014
- Dimastrogiovanni, Daniela; Fröhlich, Kathrin S.; Bandyra, Katarzyna J.
- eLife, Vol. 3