Key Points
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Chromatin-remodelling machines (remodellers) are large, multi-protein complexes that use the energy of ATP hydrolysis to mobilize and restructure nucleosomes. Nucleosomes wrap 146 bp of DNA in ∼1.7 turns around a histone-octamer disk, and the DNA inside the nucleosome is generally inaccessible to DNA-binding factors. Remodellers provide access to the underlying DNA to enable transcription, chromatin assembly, DNA repair and other processes. Central questions in the chromatin field include how remodellers convert the energy of ATP hydrolysis into a mechanical force to mobilize the nucleosome, and how different remodeller complexes select which nucleosome to move and restructure.
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Remodellers are partitioned into five families with specialized biological roles. However, all remodellers contain a subunit with a conserved ATPase domain. As well as the conserved ATPase, each remodeller complex contains unique proteins that specialize each remodeller for these biological roles. However, as all remodellers move nucleosomes, and as all movement is ATP dependent, mobilization is probably a property of the conserved ATPase subunit.
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The ATPase domains of remodellers are similar in sequence and structure to known DNA-translocating proteins in viruses and bacteria. Recent evidence with the SWI/SNF and ISWI remodeller families has revealed that remodeller ATPases are directional DNA translocases that are capable of the directional pumping of DNA. This property is applied to nucleosomes in the following manner: the ATPase seems to bind ∼40 bp inside the nucleosome, from which location it pumps DNA around the histone-octamer surface. This enables the movement of the nucleosome along the DNA, allowing the exposure of DNA to regulatory factors.
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The additional domains and proteins that are attached to the ATPase are important for nucleosome selection, and additionally help to regulate the ATPase activity. These attendant proteins bind to histones and nucleosomal DNA, and their binding to these epitopes is affected by the histone-modification state. Therefore, the modification state of histones helps to determine whether the nucleosome is an appropriate substrate for a remodeller complex.
Abstract
Chromatin remodellers are specialized multi-protein machines that enable access to nucleosomal DNA by altering the structure, composition and positioning of nucleosomes. All remodellers have a catalytic ATPase subunit that is similar to known DNA-translocating motor proteins, suggesting DNA translocation as a unifying aspect of their mechanism. Here, we explore the diversity and specialization of chromatin remodellers, discuss how nucleosome modifications regulate remodeller activity and consider a model for the exposure of nucleosomal DNA that involves the use of directional DNA translocation to pump 'DNA waves' around the nucleosome.
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Glossary
- Kinetochore
-
A large multi-protein complex that assembles onto the centromere of the mitotic chromosome. It links the chromosome to the microtubules of the mitotic spindle to segregate sister chromatids towards the spindle poles.
- Centromere
-
The region of a mitotic chromosome on which the kinetochore assembles.
- Telomere
-
The end of a normal chromosome, which consists of a repeating sequence that is extended by a telomerase to prevent the shortening of DNA that accompanies replication.
- Bromodomain
-
A motif that is common in chromatin factors and that binds to acetylated lysine residues in histone tails and other proteins.
- SANT domain
-
An evolutionarily conserved protein domain so named because it is commonly found in Swi3, Ada2, N-CoR and TFIIIB. It is important for DNA and histone-tail binding.
- SLIDE domain
-
A SANT-like ISWI domain that interacts with DNA.
- Translational position
-
The precise 146-bp region on which the nucleosome resides in a DNA molecule.
- DEAD/H-box ATPase domain
-
An evolutionarily conserved protein domain that is present in DEAD/H-box proteins with ATP-dependent helicase/translocase activity and that contains seven characteristic motifs.
- Helicase
-
A motor protein that uses the energy of ATP hydrolysis to unwind nucleic-acid duplexes.
- Nucleosome dyad
-
The centre of the nucleosome around which there is an overall pseudo two-fold symmetry.
- RecA-like domain
-
A structurally conserved domain that is found in helicases, which probably evolved from the Escherichia coli RecA protein that couples cycles of nucleotide binding and hydrolysis to nucleic-acid translocation.
- One-dimensional diffusion
-
A random walk with one degree of freedom. In this context, it refers to movement of the torsional strain that is imposed on histone?DNA contacts along the length of DNA in the nucleosome.
- B-form of DNA
-
The native form of the right-handed DNA helix with 10.6 base pairs per helical turn.
- Dosage compensation
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The process of equalizing the gene dosage of the X chromosome in males with the two X chromosomes in females.
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Saha, A., Wittmeyer, J. & Cairns, B. Chromatin remodelling: the industrial revolution of DNA around histones. Nat Rev Mol Cell Biol 7, 437–447 (2006). https://doi.org/10.1038/nrm1945
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DOI: https://doi.org/10.1038/nrm1945