Differences in ion-RNA binding modes due to charge density variations explain the stability of RNA in monovalent salts

Henning-Knechtel, Anja; Thirumalai, D.; Kırmızıaltın, Serdal

doi:10.1126/sciadv.abo1190

Cited by 12 publications

(14 citation statements)

References 69 publications

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“…The Li + ion has the highest charge density of the ions studied here. Some studies postulate that increased charge density of ions leads to increased stability of dsRNA . The Li + ion has also been shown to increase the stability of a glycine residue in silico due to an increase in water density around the carboxylate group of the residue and the presence of the first hydration shell of the Li + ion, a feature unique to this ion compared to other alkali metal ions .…”

Section: Discussionmentioning

confidence: 57%

“…These findings were surprising considering Li + has been shown to have a higher affinity for the ion atmosphere compared to Na + . , Both K + and Na + were shown to have relatively the same affinity for the ion atmosphere. These findings were contradictory to recent studies that suggested K + aggregates around the phosphate backbone more so than Na + . One may assume that increased aggregation would lead to increased stability; however, that association may not be the case here.…”

Section: Discussionmentioning

confidence: 99%

“…Most experiments concerned with counting the ions in the ion atmosphere have not considered their impact on the stability of nucleic acids in mixed ion solutions. ,− Many of those studies have shown conflicting results regarding the preferential occupancy of the ion atmosphere. ,,,,, Regardless, these studies have provided benchmarks for electrostatic association calculations of metal ions around nucleic acids. The study presented here has shown measurable differences in Δ G° 37 for nucleic acids that are dependent on the fraction of GC pairs in an RNA duplex, the identity of alkali metal ions in the solution, and the concentration at which those metal chlorides are mixed.…”

Section: Discussionmentioning

confidence: 99%

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Competitive Influence of Alkali Metals in the Ion Atmosphere on Nucleic Acid Duplex Stability

Arteaga,

Dolenz,

Znosko

2023

ACS Omega

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The nonspecific atmosphere around nucleic acids, often termed the ion atmosphere, encompasses a collection of weak ion−nucleic acid interactions. Although nonspecific, the ion atmosphere has been shown to influence nucleic acid folding and structural stability. Studies investigating the composition of the ion atmosphere have shown competitive occupancy of the atmosphere between metal ions in the same solution. Many studies have investigated single ion effects on nucleic acid secondary structure stability; however, no comprehensive studies have investigated how the competitive occupancy of mixed ions in the ion atmosphere influences nucleic acid secondary structure stability. Here, six oligonucleotides were optically melted in buffers containing molar quantities, or mixtures, of either XCl (X = Li, K, Rb, or Cs) or NaCl. A correction factor was developed to better predict RNA duplex stability in solutions containing mixed XCl/NaCl. For solutions containing a 1:1 mixture of XCl/NaCl, one alkali metal chloride contributed more to duplex stability than the other. Overall, there was a 54% improvement in predictive capabilities with the correction factor compared with the standard 1.0 M NaCl nearest-neighbor models. This correction factor can be used in models to better predict RNA secondary structure in solutions containing mixed XCl/NaCl.

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Section: Discussionmentioning

confidence: 57%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Competitive Influence of Alkali Metals in the Ion Atmosphere on Nucleic Acid Duplex Stability

Arteaga,

Dolenz,

Znosko

2023

ACS Omega

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“…Unlike Mg 2+ , the Na + ions have a weaker solvation shell, leading to frequent dehydration events and almost equal Coulombic forces between hexahydrated divalent magnesium cations and dehydrated monovalent sodium cations. The larger size of K + ions leads to a weaker hydration shell compared to Na + . , This property also facilitates the direct binding of K + ions to the DNA surface, causing them to compete with Mg 2+ ions for DNA binding (see Figure S7).…”

Section: Resultsmentioning

confidence: 99%

Sequence-Dependent Orientational Coupling and Electrostatic Attraction in Cation-Mediated DNA–DNA Interactions

He,

Qiu,

Kirmizialtin

2023

J. Chem. Theory Comput.

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Condensation of DNA is vital for its biological functions and controlled nucleic acid assemblies. However, the mechanisms of DNA condensation are not fully understood due to the inability of experiments to access cation distributions and the complex interplay of energetic and entropic forces during assembly. By constructing free energy surfaces using exhaustive sampling and detailed analysis of cation distributions, we elucidate the mechanism of DNA condensation in different salt conditions and with different DNA sequences. We found that DNA condensation is facilitated by the correlated dynamics of the localized cations at the grooves of DNA helices. These dynamics are strongly dependent on the salt conditions and DNA sequences. In the presence of magnesium ions, major groove binding facilitates attraction. In contrast, in the presence of polyvalent cations, minor groove binding serves to create charge patterns, leading to condensation. Our findings present a novel advancement in the field and have broad implications for understanding and controlling nucleic acid complexes in vivo and in vitro.

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“…[30] Regarding the interaction to RNA, several studies reported that Na + condenses more onto the RNA than K + and that this effect induces larger stability of RNA by Na + compared to K + . [7,31,32] Further studies are needed to understand the extent to which monovalent cations affect actual biological processes in living cellular environment.…”

Section: Introductionmentioning

confidence: 99%

Markedly Different Effects of Monovalent Cations on the Efficiency of Gene Expression

et al. 2022

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optimal concentrations of the monovalent cations were ≈80 mm and had maxima with respect to TL efficiencies in the order K + > Rb + > Cs + > Na + ≈ Li + . Regarding the binding/association affinity of monovalent cations for DNA, several studies have reported the order Li + > Cs + > Rb + > K + ≈ Na +[9-11] or a similar ordering, [12,13] although the differences in affinity among the monovalent cations are not significant and depend on the experimental methods used. In contrast, an exactly reverse order of action for the binding affinity of the progesterone receptor to DNA binding was reported, and such reverse order was attributed to the competitive effect of monovalent cations in the receptor-DNA interaction. [14] Except for the unique behavior of Li + , this ordering of the binding potential has been explained, [15,16] as monovalent ions with a smaller size of hydration, corresponding to a larger ionic radius, [17][18][19] may cause a larger Coulombic attractive interaction with negatively charged DNA. On the contrary, it was reported that stronger counter ion condensation, [20] as well as larger contraction of DNA minor groove, [21] is induced by monovalent cation with smaller size; Li + > Na + > K + > Rb + . As a different proposal, Gebala et al. argued [22] that ion atmosphere occupancy around double-strand DNA is insensitive to the cation size across the alkali metal ions Na + , K + , Rb + , Cs + , except for a preference of around 25% for Li + . Based on the hypothesis of counterion condensation, a number of studies have reported the specific manner of interaction of cationic counterions with DNA molecules as highly negative-charged polyelectrolytes, including the effect on higher-order structural changes. [23][24][25] Concerning polymer-and-salt-induced condensation of DNA (Ψ-condensation), Zinchenko et al. [26] performed measurements of single DNA molecules for the transition of higher-order structure from an elongated coil into a compact globule. The observation on the conformational transition was carried out on individual genomesized DNA molecules (T4 GT7 DNA) in a crowded environment with polyethylene glycol, and the researchers found that monovalent ions promote the folding transition with the potentiality:

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Differences in ion-RNA binding modes due to charge density variations explain the stability of RNA in monovalent salts

Cited by 12 publications

References 69 publications

Competitive Influence of Alkali Metals in the Ion Atmosphere on Nucleic Acid Duplex Stability

Competitive Influence of Alkali Metals in the Ion Atmosphere on Nucleic Acid Duplex Stability

Sequence-Dependent Orientational Coupling and Electrostatic Attraction in Cation-Mediated DNA–DNA Interactions

Markedly Different Effects of Monovalent Cations on the Efficiency of Gene Expression

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