Structural basis for ligand binding to the guanidine-II riboswitch
Abstract
The guanidine-II riboswitch, also known as mini-ykkC, is a conserved mRNA element with more than 800 examples in bacteria. It consists of two stem–loops capped by identical, conserved tetraloops that are separated by a linker region of variable length and sequence. Like the guanidine-I riboswitch, it controls the expression of guanidine carboxylases and SugE-like genes. The guanidine-II riboswitch specifically binds free guanidinium cations and functions as a translationally controlled on-switch. Here we report the structure of a P2 stem–loop from the Pseudomonas aeruginosa guanidine-II riboswitch aptamer bound to guanidine at 1.57 Å resolution. The hairpins dimerize via the conserved tetraloop, which also contains the binding pocket. Two guanidinium molecules bind near the dimerization interface, one in each tetraloop. The guanidinium cation is engaged in extensive hydrogen bonding to the RNA. Contacts include the Hoogsteen face of a guanine base and three nonbridging phosphate oxygens. Cation–π interactions and ionic interactions also stabilize ligand binding. Finally, the guanidine-II riboswitch utilizes the same recognition strategies as the guanidine-I riboswitch while adopting an entirely different and much smaller RNA fold.
- Authors:
-
- Yale Univ., New Haven, CT (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Institutes of Health (NIH)
- OSTI Identifier:
- 1430335
- Grant/Contract Number:
- T32GM007223; GM022778
- Resource Type:
- Accepted Manuscript
- Journal Name:
- RNA
- Additional Journal Information:
- Journal Volume: 23; Journal Issue: 9; Journal ID: ISSN 1355-8382
- Publisher:
- Cambridge University Press
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; guanidine; riboswitch; RNA; kissing loop; tetraloop; hairpin
Citation Formats
Reiss, Caroline W., and Strobel, Scott A. Structural basis for ligand binding to the guanidine-II riboswitch. United States: N. p., 2017.
Web. doi:10.1261/rna.061804.117.
Reiss, Caroline W., & Strobel, Scott A. Structural basis for ligand binding to the guanidine-II riboswitch. United States. https://doi.org/10.1261/rna.061804.117
Reiss, Caroline W., and Strobel, Scott A. Fri .
"Structural basis for ligand binding to the guanidine-II riboswitch". United States. https://doi.org/10.1261/rna.061804.117. https://www.osti.gov/servlets/purl/1430335.
@article{osti_1430335,
title = {Structural basis for ligand binding to the guanidine-II riboswitch},
author = {Reiss, Caroline W. and Strobel, Scott A.},
abstractNote = {The guanidine-II riboswitch, also known as mini-ykkC, is a conserved mRNA element with more than 800 examples in bacteria. It consists of two stem–loops capped by identical, conserved tetraloops that are separated by a linker region of variable length and sequence. Like the guanidine-I riboswitch, it controls the expression of guanidine carboxylases and SugE-like genes. The guanidine-II riboswitch specifically binds free guanidinium cations and functions as a translationally controlled on-switch. Here we report the structure of a P2 stem–loop from the Pseudomonas aeruginosa guanidine-II riboswitch aptamer bound to guanidine at 1.57 Å resolution. The hairpins dimerize via the conserved tetraloop, which also contains the binding pocket. Two guanidinium molecules bind near the dimerization interface, one in each tetraloop. The guanidinium cation is engaged in extensive hydrogen bonding to the RNA. Contacts include the Hoogsteen face of a guanine base and three nonbridging phosphate oxygens. Cation–π interactions and ionic interactions also stabilize ligand binding. Finally, the guanidine-II riboswitch utilizes the same recognition strategies as the guanidine-I riboswitch while adopting an entirely different and much smaller RNA fold.},
doi = {10.1261/rna.061804.117},
journal = {RNA},
number = 9,
volume = 23,
place = {United States},
year = {Fri Jun 09 00:00:00 EDT 2017},
month = {Fri Jun 09 00:00:00 EDT 2017}
}
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Works referenced in this record:
Metabolism of Free Guanidine in Bacteria Is Regulated by a Widespread Riboswitch Class
journal, January 2017
- Nelson, James W.; Atilho, Ruben M.; Sherlock, Madeline E.
- Molecular Cell, Vol. 65, Issue 2
Biochemical Validation of a Second Guanidine Riboswitch Class in Bacteria
journal, January 2017
- Sherlock, Madeline E.; Malkowski, Sarah N.; Breaker, Ronald R.
- Biochemistry, Vol. 56, Issue 2
Non-Covalent Interactions: Complexes of Guanidinium with DNA and RNA Nucleobases
journal, September 2013
- Blanco, Fernando; Kelly, Brendan; Sánchez-Sanz, Goar
- The Journal of Physical Chemistry B, Vol. 117, Issue 39
Identification of 22 candidate structured RNAs in bacteria using the CMfinder comparative genomics pipeline
journal, July 2007
- Weinberg, Zasha; Barrick, Jeffrey E.; Yao, Zizhen
- Nucleic Acids Research, Vol. 35, Issue 14
Structural Basis for Ligand Binding to the Guanidine-I Riboswitch
journal, January 2017
- Reiss, Caroline W.; Xiong, Yong; Strobel, Scott A.
- Structure, Vol. 25, Issue 1
Structural basis for guanidine sensing by the ykkC family of riboswitches
journal, January 2017
- Battaglia, Robert A.; Price, Ian R.; Ke, Ailong
- RNA, Vol. 23, Issue 4
Arginine Biosynthesis in Escherichia coli : EXPERIMENTAL PERTURBATION AND MATHEMATICAL MODELING
journal, December 2007
- Caldara, Marina; Dupont, Geneviève; Leroy, Frédéric
- Journal of Biological Chemistry, Vol. 283, Issue 10
The Cation−π Interaction
journal, June 2012
- Dougherty, Dennis A.
- Accounts of Chemical Research, Vol. 46, Issue 4
Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli
journal, June 2009
- Bennett, Bryson D.; Kimball, Elizabeth H.; Gao, Melissa
- Nature Chemical Biology, Vol. 5, Issue 8
Cation-pi interactions at non-redundant protein-RNA interfaces
journal, July 2014
- Zhang, Honggucun; Li, Chunhua; Yang, Feng
- Biochemistry (Moscow), Vol. 79, Issue 7
Distribution of diaminopropane and acetylspermidine in Enterobacteriaceae
journal, February 1996
- Hamana, Koei
- Canadian Journal of Microbiology, Vol. 42, Issue 2
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