A crystallographic study of the binding of 13 metal ions to two related RNA duplexes

Ennifar, Eric; Walter, P.; Dumas, Philippe

doi:10.1093/nar/gkg350

Cited by 159 publications

(161 citation statements)

References 55 publications

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“…In some cases, the divalent metal ion is directly involved as a cofactor in catalysis, but often requirements for specific ion binding are structural through stabilization of a particular local RNA geometry. X-ray crystallography has revealed important examples of ion binding pockets (Cate and Doudna 1996;Cate et al 1997;Basu et al 1998;Conn et al 2002;Banatao et al 2003;Ennifar et al 2003;Stefan et al 2006). Complementary work using solution probes for selected RNAs has dissected aspects of specific metal ion binding and effects from the nonspecific ion atmosphere (Bukhman and Draper 1997;Horton et al 1998;DeRose 2003;Nakano et al 2003;Das et al 2005b;Travers et al 2007).…”

Section: Introductionmentioning

confidence: 99%

Dissecting electrostatic screening, specific ion binding, and ligand binding in an energetic model for glycine riboswitch folding

Lipfert

Sim

Herschlag

et al. 2010

RNA

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Riboswitches are gene-regulating RNAs that are usually found in the 59-untranslated regions of messenger RNA. As the sugarphosphate backbone of RNA is highly negatively charged, the folding and ligand-binding interactions of riboswitches are strongly dependent on the presence of cations. Using small angle X-ray scattering (SAXS) and hydroxyl radical footprinting, we examined the cation dependence of the different folding stages of the glycine-binding riboswitch from Vibrio cholerae. We found that the partial folding of the tandem aptamer of this riboswitch in the absence of glycine is supported by all tested monoand divalent ions, suggesting that this transition is mediated by nonspecific electrostatic screening. Poisson-Boltzmann calculations using SAXS-derived low-resolution structural models allowed us to perform an energetic dissection of this process. The results showed that a model with a constant favorable contribution to folding that is opposed by an unfavorable electrostatic term that varies with ion concentration and valency provides a reasonable quantitative description of the observed folding behavior. Glycine binding, on the other hand, requires specific divalent ions binding based on the observation that Mg 2+ , Ca 2+ , and Mn 2+ facilitated glycine binding, whereas other divalent cations did not. The results provide a case study of how iondependent electrostatic relaxation, specific ion binding, and ligand binding can be coupled to shape the energetic landscape of a riboswitch and can begin to be quantitatively dissected.

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Section: Introductionmentioning

confidence: 99%

Dissecting electrostatic screening, specific ion binding, and ligand binding in an energetic model for glycine riboswitch folding

Lipfert

Sim

Herschlag

et al. 2010

RNA

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“…For example, metal ion specificity for a catalytic activity can be monitored by maintaining a constant background of one cation that does not support catalytic activity on its own and varying the identity of a second cation that does. Structural approaches, including X-ray crystallography (Cate et al 1997;Basu et al 1998;Ennifar et al 2003), chemical and other footprinting (Celander and2001) have also been used to assess metal ion binding specificity in nucleic acids.…”

Section: Introductionmentioning

confidence: 99%

Low specificity of metal ion binding in the metal ion core of a folded RNA

Travers¹,

Boyd²,

Herschlag³

2007

RNA

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The structure and activity of nucleic acids depend on their interactions with metal ions. Fundamental to these interactions is the degree of specificity observed between the metal ions and nucleic acids, and a complete description of nucleic acid folding requires that we understand the nature of the interactions with metal ions, including specificity. The prior demonstration that high concentrations of monovalent cations prevent nonspecific association of divalent ions with nucleic acids provides a novel and powerful means to examine site-specific metal ion binding isolated from complicating effects of the ion atmosphere. Using these high monovalent cation solution conditions we have monitored the affinity of a series of divalent metal ions for two sitespecific metal ion binding sites in the P4-P6 domain of the Tetrahymena group I intron ribozyme. The metal ion core of this highly structured RNA binds two divalent metal ions under these conditions. Despite multiple metal ion-RNA interactions observed in the X-ray crystallographic structure of P4-P6 RNA at the metal ion binding sites, these sites exhibit low specificity among Mn 2+ , Mg 2+ , Ca 2+ , Ni 2+ , and Zn 2+ . Nevertheless, the largest divalent metal ions tested, Sr 2+ and Ba 2+ , were excluded from binding, exhibiting affinities at least two orders of magnitude weaker than observed for the other metal ions. Thus, a picture emerges of two metal ion binding sites, each with a high tolerance for metal ions with different properties but also with limits to accommodation. These limits presumably arise from steric or electrostatic features of the metal ion binding sites.

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“…The binding of an Au 3+ ion in the center of a G-C base pair has been observed in the crystal structure of an RNA [120].…”

Section: Metallated Nucleic Acids For Nanotechnologymentioning

confidence: 99%

Characterization of Metal Ion-Nucleic Acid Interactions in Solution

Pechlaner

Sigel

2011

Metal Ions in Life Sciences

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Metal ions are inextricably involved with nucleic acids due to their polyanionic nature. In order to understand the structure and function of RNAs and DNAs, one needs to have detailed pictures on the structural, thermodynamic, and kinetic properties of metal ion interactions with these biomacromolecules. In this review we first compile the physicochemical properties of metal ions found and used in combination with nucleic acids in solution. The main part then describes the various methods developed over the past decades to investigate metal ion binding by nucleic acids in solution. This includes for example hydrolytic and radical cleavage experiments, mutational approaches, as well as kinetic isotope effects. In addition, spectroscopic techniques like EPR, lanthanide(III) luminescence, IR and Raman as well as various NMR methods are summarized. Aside from gaining knowledge about the thermodynamic properties on the metal ion-nucleic acid interactions, especially NMR can be used to extract information on the kinetics of ligand exchange rates of the metal ions applied. The final section deals with the influence of anions, buffers, and the solvent permittivity on the binding equilibria between metal ions and nucleic acids. Little is known on some of these aspects, but it is clear that these three factors have a large influence on the interaction between metal ions and nucleic acids.

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A crystallographic study of the binding of 13 metal ions to two related RNA duplexes

Cited by 159 publications

References 55 publications

Dissecting electrostatic screening, specific ion binding, and ligand binding in an energetic model for glycine riboswitch folding

Dissecting electrostatic screening, specific ion binding, and ligand binding in an energetic model for glycine riboswitch folding

Low specificity of metal ion binding in the metal ion core of a folded RNA

Characterization of Metal Ion-Nucleic Acid Interactions in Solution

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