Caulobacter crescentus Hfq structure reveals a conserved mechanism of RNA annealing regulation

Andrew Santiago-Frangos; Kathrin S. Fröhlich; Jeliazko R. Jeliazkov; Ewelina M. Małecka; Giada Marino; Jeffrey J. Gray; Ben F. Luisi; Sarah A. Woodson; Steven W. Hardwick

doi:10.1073/pnas.1814428116

Caulobacter crescentus Hfq structure reveals a conserved mechanism of RNA annealing regulation

Andrew Santiago-Frangos, Kathrin S. Fröhlich, Jeliazko R. Jeliazkov, Ewelina M. Małecka, Giada Marino, Jeffrey J. Gray, Ben F. Luisi, Sarah A. Woodson, Steven W. Hardwick

Whiting School of Engineering

Research output: Contribution to journal › Article › peer-review

5 Scopus citations

Abstract

We have solved the X-ray crystal structure of the RNA chaperone protein Hfq from the alpha-proteobacterium Caulobacter crescentus to 2.15-Å resolution, resolving the conserved core of the protein and the entire C-terminal domain (CTD). The structure reveals that the CTD of neighboring hexamers pack in crystal contacts, and that the acidic residues at the C-terminal tip of the protein interact with positive residues on the rim of Hfq, as has been recently proposed for a mechanism of modulating RNA binding. De novo computational models predict a similar docking of the acidic tip residues against the core of Hfq. We also show that C. crescentus Hfq has sRNA binding and RNA annealing activities and is capable of facilitating the annealing of certain Escherichia coli sRNA:mRNA pairs in vivo. Finally, we describe how the Hfq CTD and its acidic tip residues provide a mechanism to modulate annealing activity and substrate specificity in various bacteria.

Original language	English (US)
Pages (from-to)	10978-10987
Number of pages	10
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	166
Issue number	22
DOIs	https://doi.org/10.1073/pnas.1814428116
State	Published - May 28 2019

Keywords

Caulobacter
Hfq
Natively unstructured protein
RNA–protein interaction
SRNA

ASJC Scopus subject areas

General

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10.1073/pnas.1814428116

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Santiago-Frangos, A., Fröhlich, K. S., Jeliazkov, J. R., Małecka, E. M., Marino, G., Gray, J. J., Luisi, B. F., Woodson, S. A., & Hardwick, S. W. (2019). Caulobacter crescentus Hfq structure reveals a conserved mechanism of RNA annealing regulation. Proceedings of the National Academy of Sciences of the United States of America, 166(22), 10978-10987. https://doi.org/10.1073/pnas.1814428116

Caulobacter crescentus Hfq structure reveals a conserved mechanism of RNA annealing regulation. / Santiago-Frangos, Andrew; Fröhlich, Kathrin S.; Jeliazkov, Jeliazko R. et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 166, No. 22, 28.05.2019, p. 10978-10987.

Research output: Contribution to journal › Article › peer-review

Santiago-Frangos, A, Fröhlich, KS, Jeliazkov, JR, Małecka, EM, Marino, G, Gray, JJ, Luisi, BF, Woodson, SA & Hardwick, SW 2019, 'Caulobacter crescentus Hfq structure reveals a conserved mechanism of RNA annealing regulation', Proceedings of the National Academy of Sciences of the United States of America, vol. 166, no. 22, pp. 10978-10987. https://doi.org/10.1073/pnas.1814428116

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title = "Caulobacter crescentus Hfq structure reveals a conserved mechanism of RNA annealing regulation",

abstract = "We have solved the X-ray crystal structure of the RNA chaperone protein Hfq from the alpha-proteobacterium Caulobacter crescentus to 2.15-{\AA} resolution, resolving the conserved core of the protein and the entire C-terminal domain (CTD). The structure reveals that the CTD of neighboring hexamers pack in crystal contacts, and that the acidic residues at the C-terminal tip of the protein interact with positive residues on the rim of Hfq, as has been recently proposed for a mechanism of modulating RNA binding. De novo computational models predict a similar docking of the acidic tip residues against the core of Hfq. We also show that C. crescentus Hfq has sRNA binding and RNA annealing activities and is capable of facilitating the annealing of certain Escherichia coli sRNA:mRNA pairs in vivo. Finally, we describe how the Hfq CTD and its acidic tip residues provide a mechanism to modulate annealing activity and substrate specificity in various bacteria.",

keywords = "Caulobacter, Hfq, Natively unstructured protein, RNA–protein interaction, SRNA",

author = "Andrew Santiago-Frangos and Fr{\"o}hlich, {Kathrin S.} and Jeliazkov, {Jeliazko R.} and Ma{\l}ecka, {Ewelina M.} and Giada Marino and Gray, {Jeffrey J.} and Luisi, {Ben F.} and Woodson, {Sarah A.} and Hardwick, {Steven W.}",

note = "Funding Information: ACKNOWLEDGMENTS. We thank the staff at Diamond Light Source for their help with collection of X-ray diffraction data and thank Kasia Bandyra, Tom Dendooven, and Kai Papenfort for their critical reading of the manuscript and advice. S.W.H. and B.F.L. are funded by the Wellcome Trust (200873/Z/ 16/Z). K.S.F. receives funding from the mentoring program of the Ludwig Maximilian University Munich Faculty of Biology. This work was also supported by the National Institutes of Health (Grants R01 GM120425, to S.A.W.; F31 GM123616, to J.R.J.; and R01 GM078221, to J.J.G.). Publisher Copyright: {\textcopyright} 2019 National Academy of Sciences. All rights reserved.",

year = "2019",

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doi = "10.1073/pnas.1814428116",

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T1 - Caulobacter crescentus Hfq structure reveals a conserved mechanism of RNA annealing regulation

AU - Santiago-Frangos, Andrew

AU - Fröhlich, Kathrin S.

AU - Jeliazkov, Jeliazko R.

AU - Małecka, Ewelina M.

AU - Marino, Giada

AU - Gray, Jeffrey J.

AU - Luisi, Ben F.

AU - Woodson, Sarah A.

AU - Hardwick, Steven W.

N1 - Funding Information: ACKNOWLEDGMENTS. We thank the staff at Diamond Light Source for their help with collection of X-ray diffraction data and thank Kasia Bandyra, Tom Dendooven, and Kai Papenfort for their critical reading of the manuscript and advice. S.W.H. and B.F.L. are funded by the Wellcome Trust (200873/Z/ 16/Z). K.S.F. receives funding from the mentoring program of the Ludwig Maximilian University Munich Faculty of Biology. This work was also supported by the National Institutes of Health (Grants R01 GM120425, to S.A.W.; F31 GM123616, to J.R.J.; and R01 GM078221, to J.J.G.). Publisher Copyright: © 2019 National Academy of Sciences. All rights reserved.

PY - 2019/5/28

Y1 - 2019/5/28

N2 - We have solved the X-ray crystal structure of the RNA chaperone protein Hfq from the alpha-proteobacterium Caulobacter crescentus to 2.15-Å resolution, resolving the conserved core of the protein and the entire C-terminal domain (CTD). The structure reveals that the CTD of neighboring hexamers pack in crystal contacts, and that the acidic residues at the C-terminal tip of the protein interact with positive residues on the rim of Hfq, as has been recently proposed for a mechanism of modulating RNA binding. De novo computational models predict a similar docking of the acidic tip residues against the core of Hfq. We also show that C. crescentus Hfq has sRNA binding and RNA annealing activities and is capable of facilitating the annealing of certain Escherichia coli sRNA:mRNA pairs in vivo. Finally, we describe how the Hfq CTD and its acidic tip residues provide a mechanism to modulate annealing activity and substrate specificity in various bacteria.

AB - We have solved the X-ray crystal structure of the RNA chaperone protein Hfq from the alpha-proteobacterium Caulobacter crescentus to 2.15-Å resolution, resolving the conserved core of the protein and the entire C-terminal domain (CTD). The structure reveals that the CTD of neighboring hexamers pack in crystal contacts, and that the acidic residues at the C-terminal tip of the protein interact with positive residues on the rim of Hfq, as has been recently proposed for a mechanism of modulating RNA binding. De novo computational models predict a similar docking of the acidic tip residues against the core of Hfq. We also show that C. crescentus Hfq has sRNA binding and RNA annealing activities and is capable of facilitating the annealing of certain Escherichia coli sRNA:mRNA pairs in vivo. Finally, we describe how the Hfq CTD and its acidic tip residues provide a mechanism to modulate annealing activity and substrate specificity in various bacteria.

KW - Caulobacter

KW - Hfq

KW - Natively unstructured protein

KW - RNA–protein interaction

KW - SRNA

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JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

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ER -

Caulobacter crescentus Hfq structure reveals a conserved mechanism of RNA annealing regulation

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