Thermodynamic Signature of GCN4-bZIP Binding to DNA Indicates the Role of Water in Discriminating Between the AP-1 and ATF/CREB Sites

Dragan, Anatoly I.; Frank, Leslie C.; Liu, Yingyun; Makeyeva, Elena N.; Crane‐Robinson, Colyn; Privalov, Peter L.

doi:10.1016/j.jmb.2004.08.101

Cited by 40 publications

(47 citation statements)

References 53 publications

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“…Complexes of yAP-1 protein with the YRE-O DNA sequence have been associated with an increase in incorporated water molecules (Dragan et al 2004a) leading to a decrease in DNA flexibility (Kim and Struhl 1995) compared with yAP-1/YRE-A complexes. A previous report has suggested that changes in DNA flexibility play a key role in determining half-site spacing preference and are responsible for differences between in vivo and in vitro measurements (Suckow and Hollenberg 1998).…”

Section: Org Downloaded Frommentioning

confidence: 99%

Coevolution within a transcriptional network by compensatory trans and cis mutations

Kuo¹,

Licon²,

Bandyopadhyay³

et al. 2010

Genome Res.

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Transcriptional networks have been shown to evolve very rapidly, prompting questions as to how such changes arise and are tolerated. Recent comparisons of transcriptional networks across species have implicated variations in the cis-acting DNA sequences near genes as the main cause of divergence. What is less clear is how these changes interact with trans-acting changes occurring elsewhere in the genetic circuit. Here, we report the discovery of a system of compensatory trans and cis mutations in the yeast AP-1 transcriptional network that allows for conserved transcriptional regulation despite continued genetic change. We pinpoint a single species, the fungal pathogen Candida glabrata, in which a trans mutation has occurred very recently in a single AP-1 family member, distinguishing it from its Saccharomyces ortholog. Comparison of chromatin immunoprecipitation profiles between Candida and Saccharomyces shows that, despite their different DNA-binding domains, the AP-1 orthologs regulate a conserved block of genes. This conservation is enabled by concomitant changes in the cisregulatory motifs upstream of each gene. Thus, both trans and cis mutations have perturbed the yeast AP-1 regulatory system in such a way as to compensate for one another. This demonstrates an example of ''coevolution'' between a DNAbinding transcription factor and its cis-regulatory site, reminiscent of the coevolution of protein binding partners.

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Section: Org Downloaded Frommentioning

confidence: 99%

Coevolution within a transcriptional network by compensatory trans and cis mutations

Kuo¹,

Licon²,

Bandyopadhyay³

et al. 2010

Genome Res.

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“…[2][3][4][5][6][15][16][17][18][19][20][21][22][23][24][25][26][27][28][29][30] For the present analysis, we have selected data obtained under similar conditions (20°C, near neutral pH, 100 mM NaCl) and analyzed by the same approach, namely correcting for refolding effects and resolving the electrostatic and non-electrostatic components of the binding characteristics, as outlined in Figures 1 and 2. All these data are illustrated in Figure 3 and summarized in Table 1 in Supplementary Materials.…”

Section: Thermodynamic Parameters Of Protein-dna Interactionsmentioning

confidence: 99%

“…The only cases among those considered for which water ordering seems to occur upon complex formation are the bZIP/AP-1 and IRF1 complexes which proceed with a large negative enthalpy and entropy (Figure 3 b and c). 5,45 In the case of the minor groove, judging from the predominance of AT sequences among its DBD binding sites and bearing in mind the absence of the 2-amino group in adenosine (relative to guanosine), it is argued that this groove is more apolar than the major groove. Furthermore, it is known that apolar groups promote water ordering.…”

Section: Components Of the Binding Entropymentioning

confidence: 99%

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

Privalov

Dragan

Crane‐Robinson

et al. 2007

Journal of Molecular Biology

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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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“…For example, the leucine zipper dimerization domain and the N-terminal basic region of the DBD of the activator Gcn4 permit the recognition of palindromic and pseudopalindromic sites on DNA. [8] In addition, DBDs contribute to overall potency through cooperative DNA binding that can increase the number of activators bound proximal to a gene. [9,10] In contrast, the AD typically contributes little to the specificity of a transcriptional activator but rather dictates the levels of gene up-regulation through binding interactions with transcriptional machinery proteins.…”

Section: Introductionmentioning

confidence: 99%