Internucleosomal Interactions Mediated by Histone Tails Allow Distant Communication in Chromatin

Kulaeva, Olga I.; Zheng, Guohui; Polikanov, Yury S.; Colasanti, Andrew V.; Clauvelin, Nicolas; Mukhopadhyay, Swagatam; Sengupta, Anirvan M.; Studitsky, Vasily M.; Olson, Wilma K.

doi:10.1074/jbc.m111.333104

Cited by 51 publications

(78 citation statements)

References 61 publications

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“…However, until we obtain a greater collection of experimentally determined structures of nucleosome arrays, our knowledge about chromatin deformability and the associated interactions of nucleosomes must rely upon computer-simulated data. The correspondence between prediction and observation revealed in these studies, such as those that take successful account of communication between proteins at the ends of nucleosome arrays (15)(16)(17), lends credence to the computations and to the molecular insights gleaned from the simulations. On the other hand, the current mesoscale models of chromatin may not necessarily account for new observations and thus will require continued testing and refinement against all available experimental data.…”

supporting

confidence: 54%

“…The approximate representation of local structure and dynamics (at levels ranging from individual to tens of basepairs) has proven useful for interpreting the configurational properties of short proteinmediated DNA loops (10-13) and well-defined chromatin constructs (14)(15)(16)(17)(18), including the long-range communication between different parts of model oligonucleosome chains and the spatial pathways captured with microscopic techniques. Mesoscale studies tend to ignore the influences of DNA sequence other than those associated with certain well-known nucleotide repeating patterns, such as the natural curvature of so-called A-tracts.…”

mentioning

confidence: 99%

“…New measures of the long-range interactions between transcriptional proteins bound to distant sites on welldefined nucleosome arrays offer a fresh perspective on chromatin structure and deformability in solution (15). The level of gene expression induced by the association of an activator protein located at one end of such arrays with RNA polymerase at the other end provides a gauge of the ease with which the two DNA-bound species come into close contact.…”

mentioning

confidence: 99%

“…The level of communication between the proteins, like that between the dyes, depends upon the structure and motions of the intervening chain segments. Recent studies of the interactions between transcriptional proteins attached to regulatory sites at the 5 0 and 3 0 ends of a DNA chain saturated with arrays of precisely positioned 601 nucleosomes show that the positively charged histone tails of the nucleosome are essential for long-range communication, and that the level of interaction falls off with chain length (15). Moreover, the presence of nucleosomes along the DNA facilitates communication between the transcriptional proteins and suggests that the observed enhancement of gene expression over that found on nucleosome-free DNA is more than nucleosome-induced compaction of the double helix.…”

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confidence: 99%

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Contributions of Sequence to the Higher-Order Structures of DNA

Todolli

Perez

Clauvelin

et al. 2017

Biophysical Journal

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One of the critical unanswered questions in genome biophysics is how the primary sequence of DNA bases influences the global properties of very-long-chain molecules. The local sequence-dependent features of DNA found in high-resolution structures introduce irregularities in the disposition of adjacent residues that facilitate the specific binding of proteins and modulate the global folding and interactions of double helices with hundreds of basepairs. These features also determine the positions of nucleosomes on DNA and the lengths of the interspersed DNA linkers. Like the patterns of basepair association within DNA, the arrangements of nucleosomes in chromatin modulate the properties of longer polymers. The intrachromosomal loops detected in genomic studies contain hundreds of nucleosomes, and given that the simulated configurations of chromatin depend on the lengths of linker DNA, the formation of these loops may reflect sequence-dependent information encoded within the positioning of the nucleosomes. With knowledge of the positions of nucleosomes on a given genome, methods are now at hand to estimate the looping propensities of chromatin in terms of the spacing of nucleosomes and to make a direct connection between the DNA base sequence and larger-scale chromatin folding.Despite the astonishing amount of information now known about the sequential makeup and spatial organization of genomic DNA, there is much to learn about how the vast numbers of basepairs in these systems contribute to the three-dimensional architectures and workings of long, spatially constrained, double-helical molecules. New biochemical and imaging methodologies, such as proximity-based ligation and fluorescence in situ hybridization (1-3), have shed light on the large-scale organization of genomic DNA, enabling investigators to pinpoint DNA elements in close spatial proximity and follow the course of these associations during cellular processes. The resulting measurements have motivated the study of long genomes in terms of simple polymer models (4,5), which have in turn illuminated the physical nature of the contacted elements and pointed to mechanisms potentially governing genome architecture and dynamics. Although these models are appropriate for the very large scale of the experimental data, they rest on the assumption that the chemical makeup of DNA does not matter, and thus provide no link between the primary sequence of bases and the tertiary structures and interactions of genomic folds.At the other extreme of chain length, the detailed molecular structures of DNA with only tens of basepairs point to various sequence-dependent spatial and energetic codes underlying the three-dimensional organization of the double helix and its susceptibility to interactions with proteins and other molecules (6). The structural data also include more than 100 crystallographic examples of the tight, superhelical wrapping of~150 DNA basepairs (bp) around the core of the histone proteins in the nucleosome core particle, the fundamental packagi...

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supporting

confidence: 54%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Contributions of Sequence to the Higher-Order Structures of DNA

Todolli

Perez

Clauvelin

et al. 2017

Biophysical Journal

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“…We can divide computational approaches of chromatin structure into three basic [156,160], ionic environment [157,161], presence of linker histones [163] and different intra-and inter-chain physical interactions [156,157,[160][161][162][163][164]. In the top-down models the chromatin structure is derived by implementing experimental restraints coming from chromosome conformation capture techniques into a simple model of the chromatin fiber.…”

Section: Mesoscopic Studiesmentioning

confidence: 99%

Multiscale simulation of DNA

Dans¹,

Walther

Gómez

et al. 2016

Current Opinion in Structural Biology

148

131

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DNA is not only among the most important molecules in life, but a meeting point for biology, physics and chemistry, being studied by numerous techniques. Theoretical methods can help in gaining a detailed understanding of DNA structure and function, but their practical use is hampered by the multiscale nature of this molecule. In this regard, the study of DNA covers a broad range of different topics, from sub-Angstrom details of the electronic distributions of nucleobases, to the mechanical properties of millimeter-long chromatin fibers. Some of the biological processes involving DNA occur in femtoseconds, while others require years. In this review, we describe the most recent theoretical methods that have been considered to study DNA, from the electron to the chromosome, enriching our knowledge on this fascinating molecule.

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Mechanisms of Enhancer Action

Nizovtseva

Studitsky

2019

Encyclopedia of Life Sciences

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Genomic studies have revealed a large number of distantly acting regulatory DNA regions (enhancers) activating transcription both in bacteria and in eukaryotes. Enhancers contain multiple specific binding sites for activator proteins that can locally disturb chromatin structure after binding to DNA and activate transcription initiated from enhancer targets (promoters) localised at variable distances from the enhancer. Typically, interactions between enhancer‐ and promoter‐bound proteins involve chromatin looping of intervening stretches of DNA organised in chromatin. These dynamic regulatory chromatin loops of different size and stability operate both in bacteria and in higher organisms where they form extensive and complex three‐dimensional networks that largely define gene expression patterns and identity of eukaryotic cells. Misalignment of these networks results in development of numerous human diseases including cancer. Key Concepts Enhancers are regulatory DNA sequences that regulate transcription both in bacteria and in higher organisms. Enhancers are activated after binding of activator proteins to their specific binding sites localised within the enhancers. Enhancers activate their targets (promoters) over variable distances. An enhancer can work on multiple promoters and a promoter can be activated by multiple enhancers. As a result, there is a dynamic regulatory network formed by regulatory chromatin loops of different size and stability. Promoter activation involves interaction between proteins bound at the enhancers and promoters. Enhancer–promoter interaction is accompanied by looping of intervening chromatin. Gene activation involves a conformational change in promoter‐bound proteins or their covalent modification.

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Internucleosomal Interactions Mediated by Histone Tails Allow Distant Communication in Chromatin

Cited by 51 publications

References 61 publications

Contributions of Sequence to the Higher-Order Structures of DNA

Contributions of Sequence to the Higher-Order Structures of DNA

Multiscale simulation of DNA

Mechanisms of Enhancer Action

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