Absence of Minor Groove Monovalent Cations in the Crosslinked Dodecamer C-G-C-G-A-A-T-T-C-G-C-G

Chiu, Thang Kien; Kaczor-Grzeskowiak, Maria; Dickerson, Richard E.

doi:10.1006/jmbi.1999.3075

Cited by 134 publications

(130 citation statements)

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“…60,61 In the major groove, the distribution of H-bond donors and acceptors exhibit greater irregularity than in the minor groove, and no regular water superstructure has been identified. 54 Based on the assumption that the water hydrating the minor groove of AT-rich DNA is more ordered than the water hydrating the major groove, its removal is expected to require a greater enthalpy and thereby provide a larger entropy increase than removal of water hydrating the major groove. If water in the AT-rich minor groove is in an "ordered," ice-like state and its removal requires about 6 kJ·mol -1 (the heat of melting ice at 0 °C), the loss of 11 water molecules coordinated in the first and second layers of the 7 bp binding site of an HMG DBD (i.e.…”

Section: Hydration Of the Dna Groovesmentioning

confidence: 99%

What Drives Proteins into the Major or Minor Grooves of DNA?

Privalov

Dragan

Crane‐Robinson

et al. 2007

Journal of Molecular Biology

168

158

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The energetic profiles of a significant number of protein-DNA systems at 20°C reveal that, despite comparable Gibbs free energies, association with the major groove is primarily an enthalpy driven process, whereas binding to the minor groove is characterized by an unfavorable enthalpy that is compensated by favorable entropic contributions. These distinct energetic signatures for major versus minor groove binding are irrespective of the magnitude of DNA bending and/or the extent of binding-induced protein refolding. The primary determinants of their different energetic profiles appear to be the distinct hydration properties of the major and minor grooves, namely that the water in the AT-rich minor groove is in a highly ordered state and its removal results in a substantial positive contribution to the binding entropy. Since the entropic forces driving protein binding into the minor groove are a consequence of displacing water ordered by the regular arrangement of polar contacts, they cannot be regarded as hydrophobic. KeywordsDNA binding; DNA grooves; hydration; thermodynamics; electrostatics Structural and energetic characterizations of protein-nucleic acid complexes are important for a better understanding of the molecular interactions that govern transcriptional regulation. Of particular importance are the energetic profiles of DNA binding domains (DBDs) interacting with their target recognition sites. DBDs are known to interact specifically with either the major or minor grooves of DNA, with binding-induced structural effects ranging from negligible perturbation of the B-DNA conformation to substantial distortions, such as bending and kinking. One can then ask if there are qualitative differences in the forces driving protein binding to the different grooves of DNA. Comparing the association constants of these two types of DBDs does not furnish a satisfactory answer, since both categories contain examples of stronger and weaker binding interactions. An answer to this question therefore requires a detailed analysis of the forces involved in the formation of the specific protein-DNA complexes. This assumes not only measurement of the association constant but also determination of the Gibbs energy and its enthalpic and entropic components over a broad range of conditions, particularly temperature and ionic strength. In this review, we analyze the thermodynamic characteristics of protein binding to DNA published over the last several years. This overall consideration has revealed qualitative differences in the energetic signatures of

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Section: Hydration Of the Dna Groovesmentioning

confidence: 99%

What Drives Proteins into the Major or Minor Grooves of DNA?

Privalov

Dragan

Crane‐Robinson

et al. 2007

Journal of Molecular Biology

168

158

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“…However, a subsequent atomic-resolution (1.1 Å) study of the same duplex (but with a 4-fold higher Mg 2ϩ ͞Na ϩ ratio in the crystallizing solution) did not find any evidence, direct or indirect, for the presence of Na ϩ ions in the minor groove (7). Another study (8) found that the Mg 2ϩ salt of the cross-linked A 2 T 2 duplex (with virtually no monovalent ions present in the crystal) has essentially the same structure (at 1.43-Å resolution) as the Na ϩ salt of the native duplex (at 1.9 Å) (9). This indicates that the crystal structure of the A 2 T 2 duplex is not affected significantly by localized binding of Na ϩ ions (whether they are present in the minor groove or not).…”

mentioning

confidence: 92%

“…This indicates that the crystal structure of the A 2 T 2 duplex is not affected significantly by localized binding of Na ϩ ions (whether they are present in the minor groove or not). The authors of this recent work (8) challenged the earlier arguments in favor of groove-bound Na ϩ ions (5) and also questioned the validity of the procedure used to infer, from crystallographic data, partial occupancy of K ϩ ions at several primary solvation sites in the minor groove of the K ϩ salt of the A 2 T 2 duplex (10). Even if one admits that there exists no unambiguous crystallographic evidence for partial Na ϩ or K ϩ substitution for water molecules in the minor-groove spine of hydration, this does not necessarily mean that such ions are not there.…”

mentioning

confidence: 98%

Sequence-specific binding of counterions toB-DNA

Денисов

Halle

2000

Proc. Natl. Acad. Sci. U.S.A.

170

154

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Recent studies by x-ray crystallography, NMR, and molecular simulations have suggested that monovalent counterions can penetrate deeply into the minor groove of B form DNA. Such groovebound ions potentially could play an important role in AT-tract bending and groove narrowing, thereby modulating DNA function in vivo. To address this issue, we report here 23 Na magnetic relaxation dispersion measurements on oligonucleotides, including difference experiments with the groove-binding drug netropsin. The exquisite sensitivity of this method to ions in long-lived and intimate association with DNA allows us to detect sequencespecific sodium ion binding in the minor groove AT tract of three B-DNA dodecamers. The sodium ion occupancy is only a few percent, however, and therefore is not likely to contribute importantly to the ensemble of B-DNA structures. We also report results of ion competition experiments, indicating that potassium, rubidium, and cesium ions bind to the minor groove with similarly weak affinity as sodium ions, whereas ammonium ion binding is somewhat stronger. The present findings are discussed in the light of previous NMR and diffraction studies of sequence-specific counterion binding to DNA.

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“…Monovalent cations are generally less strongly solvated than divalent cations and therefore tend to interact with DNA purely electrostatically without making hydrogen bonds from metal-coordinated water molecules (5). As a consequence, DNA-associated monovalent cations are generally not clearly identified in x-ray crystallographic studies of duplex DNA (9). Although monovalent cations have been found in a few cases to be localized at preferred sites with low occupancies, the stable and specific solvation geometries adopted by divalent cations endow them with the ability to strongly and selectively bind DNA (10,11).…”

mentioning

confidence: 99%

DNA-dependent divalent cation binding in the nucleosome core particle

Davey¹,

Richmond²

2002

Proc. Natl. Acad. Sci. U.S.A.

107

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Sequence-specific binding of divalent cations to nucleosomal DNA can potentially influence nucleosome position and mobility, as well as modulate interactions with nuclear factors. We define the bonding and specificity of divalent cation interaction with nucleosomal DNA by characterizing Mn 2؉ binding in the x-ray structure of the nucleosome core particle at 1.9-Å resolution. Manganese ions are found ligated with high occupancy in the major groove to 12 of 22 GG and GC base pair steps. The specific location and mode of metal binding is the consequence of unambiguous conformational differences between dinucleotide sites, owing to their sequence context and orientation in the nucleosome core. D ivalent cations serve critical functions across a multitude of biochemical processes (1, 2). They generally play one of two roles: (i) bond activation in cleavage or rearrangement reactions of enzymes, or (ii) structural stabilization in macromolecules. The importance of divalent cations in the three-dimensional structure of DNA and RNA has been demonstrated in recent studies (3-6). A striking example is the induction of the B-to Z-form transition in poly[d(G-C)] by transition metal cations (7). In many crystal structures of nucleotides and oligonucleotides, divalent cations are observed to bind in a context or site-specific manner, interacting variably with base, phosphate, and sugar moieties depending on the nature of the metal ion. The recent crystal structures of two B-form DNA decamers at 1-Å resolution revealed up to 22 divalent cations per duplex, providing a detailed view of cation association to naked DNA and indicating that major groove binding of Mg 2ϩ and Ca 2ϩ can stabilize bending into the major groove (5).The affinity of a cation for a specific site on a polynucleotide is a general function of its charge, hydration-free energy, coordination geometry, and coordinate bond-forming capacity (2, 8). The hydration-free energy is particularly important in distinguishing monovalent from divalent cation binding. Monovalent cations are generally less strongly solvated than divalent cations and therefore tend to interact with DNA purely electrostatically without making hydrogen bonds from metal-coordinated water molecules (5). As a consequence, DNA-associated monovalent cations are generally not clearly identified in x-ray crystallographic studies of duplex DNA (9). Although monovalent cations have been found in a few cases to be localized at preferred sites with low occupancies, the stable and specific solvation geometries adopted by divalent cations endow them with the ability to strongly and selectively bind DNA (10, 11).Mg 2ϩ is the most prevalent intracellular divalent cation, occurring in millimolar quantity (Ϸ40 mM) (12). However, others, such as Mn 2ϩ (Ϸ0.5 M) and Ca 2ϩ

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Absence of Minor Groove Monovalent Cations in the Crosslinked Dodecamer C-G-C-G-A-A-T-T-C-G-C-G

Cited by 134 publications

References 50 publications

What Drives Proteins into the Major or Minor Grooves of DNA?

What Drives Proteins into the Major or Minor Grooves of DNA?

Sequence-specific binding of counterions toB-DNA

DNA-dependent divalent cation binding in the nucleosome core particle

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