Selected SWI/SNF family remodelers from yeast and human.
1. Introduction
Chromatin is the packaged form of the eukaryotic genome in the cell nucleus, presenting the substrate for all DNA dependent processes. The basic packaging unit of chromatin is the nucleosome core, a nucleoprotein structure consisting of 8 histone proteins and 147 bp of DNA. Two of each H2A and H2B, H3 and H4, form an octameric, disc like particle on which 1.65 turns of DNA is wrapped [1]. Nucleosomal cores are separated by a linker DNA, with a varying length of 7 bp to 100 bp, with distinct lengths in different organisms and tissues. Even within one cell type the linker length can vary about 40 bp between the actively transcribed and repressed genes [2].
Binding of the DNA to the histone octamer and the bending of the molecule on the protein surface present a strong barrier to sequence specific recognition of the nucleosomal DNA molecule. That’s why the packaging of DNA into nucleosomes and higher order structures is generally inhibitory to all kind of DNA dependent processes. To overcome DNA sequence accessibility problems, cells have developed mechanisms to open higher order structures of chromatin and to disrupt nucleosomes allowing the binding of sequence specific regulators. In general, two major mechanisms exist which regulate chromatin accessibility: First, histones can be posttranslationally modified and recruit specific effector proteins to chromatin [3]. Second, specific chromatin remodeling enzymes displace the histone octamers from DNA or translocate them on DNA, thereby exposing or protecting underlying DNA sequences to regulatory factors that control the DNA dependent processes [4].
The presence of 53 different chromatin remodeling enzymes in the human cell suggests specialized functions of these enzymes and the associated complexes. Chromatin remodelers are DNA translocases that apply an ATP-dependent torsional strain to DNA, providing the force to reposition nucleosomes; i.e. moving the histone octamer to a different site on the DNA [4,5]. Diverse remodeling enzymes and complexes have distinct nucleosome positioning activities. In other words, the remodelers interpret the DNA sequence/structure information in different ways, establishing target site-specific nucleosome positioning patterns. The exact nucleosome positions at a given site depends on both, the type of the ATPase motor protein and the composition of the multiprotein complex where it is integrated [6]. The specialized functions of remodeling enzymes may result from their different nucleosome positioning behavior and the distinct targeting to genomic sites.
There is plenty of data available on the remodeling mechanism
2. Remodeler families
The catalytic subunit of the remodeling enzymes consists of a conserved ATPase domain and unique flanking domains, used for a simplified separation into four distinct families (Fig. 1). The ATPase domain consists of two tandem RecA-like folds (DExx and HELICc), containing seven conserved helicase-related sequence motifs that classify the enzymes as part of the Superfamily 2 grouping of helicase-like proteins [7,8]. Chromatin remodelers are lacking the ability to separate nucleic acid strands, so they are not bona fide helicases. However, they are DNA translocases that use the energy of ATP to create a necessary force to reposition nucleosomes.
In a qualitative and quantitative study, the Snf2 family members were further subdivided into 24 distinct subfamilies based on similarities within the Snf2-specific motifs. Increased genomic complexity is paralleled by an increasing number of subfamilies and members of a given subfamily: the
2.1. SWI/SNF family
The SWI/SNF complex was first described in
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SWI/SNF | Swi2/Snf2 | Swi1/Adr6, Swi3, Swp73, Snf5, Arp7, Arp9, Swp82, Snf11, Taf14, Snf6, Rtt102 |
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RSC | Sth1 | Sth1, Rsc8/Swh3, Rsc6, SfhI, Arp7, Arp9, Rsc1,2 or 4, Rsc7, Rsc30, Rsc3, Rsc5, Rtt102, Rsc14/Ldb7, Rsc10, Rsc9 | |
BAF | BRM or BRG1 | BAF250, BAF155, BAF170,BAF60(A,B or C), SNF5, BAF57, BAF53(A or B), β-actin, BAF45(A,B,C or D) |
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PBAF | BRG1 | BAF180, BAF200, BRD7, BAF155, BAF45(A,B,C or D), BAF170,BAF60(A, B or C), SNF5, BAF57, BAF53(A or B), β-actin |
2.2. ISWI family
The ISWI (imitation switch) family ATPases harbour a C-terminal SANT domain adjacent to a SLIDE domain (SANT-like ISWI), which together form a nucleosome recognition module that binds to DNA and unmodified H4 tails [4]. The ISWI remodeling enzyme in
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NURF | ISWI | NURF301, NURF55/p55, NURF38 |
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ACF | ACF1 | ||
CHRAC | ACF1, CHRAC 14, CHRAC 16 | ||
ISWI1a | ISWI1 | loc3 |
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ISWI1b | loc2, loc4 | ||
ISWI2 | ISWI2 | Itc1 | |
NURF | Snf2L | BPTF, RbAp46 or RbAP48 |
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ACF | Snf2H | ACF1 | |
CHRAC | ACF1, CHRAC17, CHRAC15 | ||
NoRC | Tip5 | ||
RSF | Rsf1 | ||
WICH | Wstf |
2.3. CHD family
The CHD (Chromodomain-Helicase-DNA binding) family is defined by the presence of two chromodomains, arranged as a tandem, N-terminal of the ATPase domain. Additional structural motifs are used to further divide the CHD family into the subfamilies CHD1, Mi-2 and CHD7 [8,21].
Members of the CHD1 subfamily contain a C-terminal DNA-binding domain that preferentially binds to AT-rich DNA
The Mi-2 subfamily members contain a pair of PHD domains (plant homeodomain) in their N-terminal part (human Chd3 and Chd4, also known as Mi-2α and Mi-2β in
The CHD7 subfamily members have additional C-terminal domains, like the SANT or BRK domains (Chd5 to Chd9 proteins).
The biological properties of CHD family members are highly heterogenous. Some exist as monomers
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Chd1 | Chd1 |
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Chd2 | Chd2 | ||
NuRD | Mi-2 | MBD2/3, MTA, RPD3, p55, p66/68 | |
Chd1 | Chd1 |
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Chd2 | Chd2 | ||
NuRD | Chd3/Chd4 | MBD3, MTA1/2/3, HDAC1/2, RbAp46/48, p66α/β, DOC-1? | |
Chd5 | Unknown | ||
Chd7 | PARP1, PBAF complex |
2.4. INO80 family
The specific feature of the remodeling enzymes belonging to the INO80 (inositol requiring 80) family is the split ATPase domain. This unique module retains ATPase activity, and acts as a scaffold for the association with the RuvB-like proteins, Rvb1 and Rvb2. RuvB is a bacterial ATP-dependent helicase that forms a double hexamer around Holliday junctions to promote their migration during homologous recombination [30]. Unlike remodelers of other families, the INO80 complex exhibits DNA helicase activity and binds to specialized DNA structures
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INO80 | Ino80 | Rvb1, Rvb2, Arp5, Arp8, Arp4, Act1, Taf14, les1, Ies2, les3, les4, les5, Ies6, Nhp10 |
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SWR1 | Swr1 | Rvb1, Rvb2, Arp6, Arp4, Act1, Yaf9, Swc4/Eaf2, Swc2, Swc3, Swc4, Swc5, Swc6, Yaf9, Bdf1, Swc7, H2AZ, H2B |
3. Translocation mechanism of chromatin remodelers
Chromatin remodelers use the energy of ATP hydrolysis to assemble, reposition or evict histones from DNA. Nucleosome repositioning by remodelers can be described as a 3-step mechanism: 1) initiation step that requires the recognition and specific binding to the substrate, 2) several translocation steps with varying step-lengths and kinetics depending on the particular remodeling enzyme and on the properties of the underlying DNA sequence, 3) release step, which occurs at energetically favourable positions depending on the combination of remodeler and DNA sequence/structure at this site [6,38]. This chapter will focus on the mechanisms of the translocation step.
Proposed models for nucleosome remodeling suggest that only a minor fraction of the 358 direct and indirect histone-DNA interactions are disrupted at a given time of the reaction, as the energy of ATP hydrolysis would not be sufficient to fully disrupt the nucleoprotein structure [39,40]. One of the first mechanisms proposed, is the ’’twist diffusion model’’ describing moving of the DNA over the histone octamer surface in 1 bp intervals. Thus, a single base pair distortion is continuously propagated through the nucleosome, transiently storing one additional basepair in the realm of the nucleoprotein structure. This model is supported by nucleosomal crystal structures exhibiting such a single-basepair “twist defect” [39,41]. However, several studies could not confirm such a translocation model. Experiments using nicked or gapped DNA substrates that uncouple DNA rotation mediated processes still allowed SWI/SNF and ISWI dependent nucleosome remodeling, arguing against a sole twist-diffusion mechanism [42-44].
Alternatively, it was suggested that nucleosomes are repositioned according to the ’’loop recapture model’’, proposing a detachment of a DNA segment from the histone octamer surface at the entry site of the nucleosome. The exposed octamer surface would interact with more distant regions of the DNA molecule, resulting in the formation of a DNA loop on the histone octamer surface. This DNA loop would translocate over the octamer surface in an energy-neutral process, by releasing and rebinding adjacent sequences on the protein surface. DNA loop propagation would change the translational position of the nucleosome, according to the size of the DNA loop [45]. This model is strengthened by biochemical and recent single molecule studies. ACF remodeling complex was shown to cause the unwrapping of DNA, roughly 20 and 40 bp, from the nucleosomal border [46]. ATP dependent translocation of SWI/SNF and RSC on DNA and nucleosomal templates produces DNA loops and nucleosome remodeling by RSC was shown to produce a remodeled intermediate containing internal DNA loops [47].
Nucleosomal translocation and its step-size depend on the size of the DNA loop, a parameter that depends on the nature of the remodeling enzyme. Single molecule studies with the remodeling complex ACF suggested an initial step size of 7 bp and subsequent steps of 3-4 bp [48], whereas RSC was shown to exhibit a step size of 2 bp [49]. Within a strong nucleosomal positioning sequence both recombinant
4. Targeting remodelers: Signals
One of the enigmas is the cellular requirement for 53 types of remodeling enzymes in humans that are capable to form hundreds to thousands of different remodeling complexes [6]. Such high numbers already suggest specialized functions for individual complexes and that remodeling enzymes mobilize nucleosomes in a specific manner. Many chromatin remodelers bind to DNA and nucleosomes in a sequence independent manner
4.1. Direct chromatin targets
4.1.1. DNA and RNA sequence/structure
Mechanistical analysis of the nucleosome remodeling process revealed that binding of a remodeling complex to a mononucleosomal substrate results in a specific and ATP-dependent repositioning of the nucleosome on the DNA [50,51]. An
The remodeling complexes contain DNA-binding motifs that are present in the catalytic or/and in accessory subunits (Fig. 1). For example, catalytic subunit Snf2H contains a SANT-SLIDE domain and in addition the WAC and AT hook motifs in the Acf1 and Tip5 proteins [4,53-57]. These modules allow the specific recognition of DNA sequences and determine the outcome of a remodeling reaction, as it was shown by exchanging such domains between remodeling enzymes [38,58-60]. Nucleosome positioning is most probably affected by the different binding affinities of those motifs to the non-remodeled and remodeled substrates and the sequence dependent flexibility and stability of the particle, impacting the final outcome of the reaction. The role of specific DNA sequences in nucleosome positioning was shown for the ISWI-containing complex ACF, which positions a nucleosome relative to an intrinsically curved DNA sequence element [6].
Not only individual positions, but also internucleosomal distances depend on the DNA binding domains of the enzymes. ACF interacts with linker DNA and is capable to sense its length [61]. This structural element appears to play a key role in the positioning of nucleosomes in regular arrays, as the remodeler-induced mobility of the nucleosome is biased towards the longer flanking DNA [62]. Similarly, the Chd1 remodeler was described to sense the length of linker DNA [63].
Moreover, unusual DNA structures like quadruplexes could represent specific targeting signals. ATRX recognises G-rich repeat sequences, which are prevalent in telomeres [64]. These repeat sequences likely to form G-quadruplex (G4) structures, and ATRX preferentially binds to such a G4 structure
Methylated CpG islands in the DNA were shown to be recognized by MBD (methyl-binding domain) domains, so it can serve as a targeting signal for particular remodelers. For example, MBD2 recruits the NuRD complex to methylated promoters [65]. The related TAM domain (MBD-like) in Tip5, the noncatalytic subunit of the NoRC complex, does not recognise methylated DNA, but binds to the pRNA (promoter RNA). The pRNA is folded into the hairpin-like structure which is bound by NoRC and participates in the recruitment NoRC to the rRNA gene promoter region [56,66-68].
4.1.2. Histone modifications
The histone code hypothesis suggests that individual covalent modifications of histones or combinations of these modifications are recognized by specific readers which determine downstream events [3]. Chromatin remodeling complexes contain histone code reader domains, allowing the targeting to specifically modified chromatin domains and thereby enabling the establishment of a remodeler dependent nucleosomal positioning landscape.
The SWI/SNF type of remodelers contain bromodomains, interacting specifically with acetylated lysines on the histone tails [69]. Acetylation of the histone H3 N-terminal tail facilitated the recruitment and nucleosome mobilization by SWI/SNF and RSC. Tetra-acetylated H3 tails, but not tetra-acetylated H4 tails, increased the affinity of RSC and SWI/SNF for nucleosomes, which is dependent on the SWI/SNF bromodomain, but is not further enhanced by additional bromodomains present in RSC [70]. By contrast, the SANT domain of the ISWI type of remodelers is known to interact with unmodified histone tails. The H4 tail has been shown to play a decisive role in ISWI remodeling, in that both, the complete removal of the H4 tail [71,72] and its site-specific acetylation suppress the remodeling action of ISWI [73]. Human Chd1 protein interacts with H3K4me2/3 via its double chromodomains, which fold into a functional unit. On the other hand, nucleosomal H3K4 methylation reduces the affinity of the NuRD complex for H3 tail binding. It was shown that the second PHD finger of Chd4 preferentially interacts with unmodified H3K4 and H3K9me3 [74,75]. Full-length NURF301 the large subunit of the ISWI containing NURF complex contains a C-terminal bromodomain and a juxtaposed PHD finger that bind H3K4me3 and H4K16Ac, respectively. However, a NURF301 isoform lacking these C-terminal domains is also detected in cells, suggesting that alternative splicing can change targeting signals and localisation of the complexes within the genome. It was concluded, that the specific recognition of the posttranslational marks by NURF is important for the regulation of primary spermatocyte differentiation in
4.1.3. Histone variants
Non-canonical histone variants differ from the canonical histones at the level of their primary sequence, which can range from a few amino acid changes to large domains. These variants show distinct regulatory mechanisms for their expression and deposition, resulting in the establishment of chromatin domains with specific properties. The exchange of canonical histones for the variant ones is an active process, requiring the activity of remodeling enzymes and the action of RNA and DNA polymerases that actively displace the histones from DNA [77].
Analyzing the dynamic changes in the composition of histone variants in nuclear-transferred embryos revealed that the donor cell-derived histone H3 variants H3.1, H3.2, and H3.3, as well as H2A and H2A.Z, were rapidly eliminated from the chromatin of nuclei transplanted into enucleated oocytes. In parallel to this removal, oocyte-stored histone H3 variants and H2A.X were incorporated into the transplanted nuclei, while the incorporation of H2A and H2A.Z was minimal or not detected. The incorporation of these variant histones was independent of DNA replication suggesting an active process depending on the remodeling complexes [78].
An ATRX (α-thalassemia X-linked mental retardation protein) – Daxx (death domain associated protein) complex can effectively assemble H3.3-containing nucleosomes in murine embryonic stem cells. It was shown that ATRX recruits Daxx to telomeres, and both complex subunits are required for H3.3 deposition at telomeric chromatin [79]. Chd1 in
4.2. Indirect chromatin targets
4.2.1. Sequence specific DNA binding proteins
The DNA-sequence dependent recruitment of remodelers is not necessarily mediated by the remodeling complex subunits themselves but can also occur via transient interactions with other sequence specific DNA binding proteins. For example, the NuRD complex is recruited to the various promoters of the target genes via interaction with several transcription factors and co-regulators such as NAB2, Ikaros, FOG1, BCL11B and several other factors described by Brehm and colleagues [26]. Genome wide expression, genetic and biochemical analysis established that TramTrack69, MEP1, and the
4.2.2. Poly(ADP-ribose) polymer
Several studies demonstrated the targeting of Chd4 to sites of DNA double strand breaks in a PARP dependent manner [87]. The enzyme was shown to bind to the poly(ADP-ribose) polymer
5. Targeting remodelers: Search mechanism
The human genome is packaged into some 30 millions of nuclesosomes that have to be organized into functional chromatin domains with specific local structures. In order to identify target sites or to detect nucleosomes that have to be repositioned, the remodeling complexes have to detect such sites in chromatin very quickly. Potential genome screening mechanisms by the remodelers are discussed in this chapter.
5.1. Release/termination model
In the seventies, JJ Hopfield introduced the kinetic proofreading mechanism for reducing errors in biological systems. He used Michaelis Menten kinetics to explain how enzymes discriminate between different substrates [89]. A similar kinetic proofreading mechanism can be used to describe the action of remodelers, where “good” substrates are characterized by a high affinity of the remodeler for the nucleosome substrate (low value of Michaelis-Menten constant
5.2. The continuous sampling mechanism
Many proteins in the nucleus, including several remodelers are highly mobile as revealed by fluorescence recovery after photobleaching (FRAP) experiments. For proteins that do not interact with any cellular structures, FRAP kinetics are a direct reflection of their translational motion properties. In contrast, proteins that bind to immobile structures such as chromatin, exhibit a slower overall mobility. The mobility of ISWI family remodelers Snf2H, Snf2L and Snf2L+13 (an ATPase inactive variant of the Snf2L) was studied in living U2OS cells. During G1/2 phase only 1-4% of the enzymes were immobilized [90], whereas the rest could be fitted by the free-diffusion model, suggesting only transient binding events. Additionally, chip-seq experiments with remodeling enzymes support the transient binding events. These experiments revealed that the localization pattern of wild-type Isw2p did not correlate with known sites of Isw2 function
5.3. Immobilization
In parallel with the continuous sampling mechanism, remodeling complexes are engaged by specific recruitment or immobilization at specific target sites. The respective mechanisms are described in chapter 4. For example, when cells were treated with dexamethasone, BRG1 and BRM were concentrated in a single spot in the nucleus, as revealed by immunofluorescence. The site coincided with the multimerized MMTV DNA and RNA FISH signals, showing that the enzymes are recruited to the MMTV array in a hormone-dependent manner. In this case the recruitment of the SWI/SNF machine results in the maintenance of an active chromatin structure that is compatible with transcription [93]. In other cases, like the nucleolar remodeling complex NoRC recruitment to the rRNA genes, continuous targeting results in gene repression via changes of the promoter nucleosome positioning that are incompatible with transcription initiation factor binding and further leads to the heterochromatin formation [20,94].
5.4. Nuclear dynamics of chromatin remodeling enzymes
Cells express a plethora of different remodeling complexes that act simultaneously on the cellular chromatin. The remodeler complexes diffuse freely through the nucleus, searching for “good” nucleosomes. “Good” nucleosomal substrates for the one machine may represent “bad” substrates for the other machine, suggesting that an active, free diffusing pool of remodeling complexes continuously changes the local chromatin structure. Upon specific signals individual machines are recruited to the specific sites to establish local chromatin structures correlating with a persistent activation or repression of certain DNA dependent processes. We hypothesize that the mixture of remodeling complexes in the cell, with their complex-specific remodeling patterns would continuously changes local chromatin structures, depending on complex that is currently recruited to such sites. Overall the action of the diverse remodeling complexes suggests that chromatin is continuously switching local nucleosome positions according to the levels, activity and set of remodeling complexes in a given cell [95].
6. Regulation of remodeler activity
As mentioned above, the individual accessory proteins of the remodeling complexes contain a diverse set of histones, DNA and nucleosome recognition motifs and these proteins change the outcome of nucleosome remodeling reactions. Accordingly, these proteins significantly determine the targeting to genomic regions and the qualitative outcome of a remodeling reaction. In this chapter, we want to focus on the regulation of the overall activity of remodeling enzymes by metabolites and modifications. Subunits of chromatin remodeling complexes often contain domains capable of recognizing specific posttranslational modifications on histone tails. However, significantly less is known about the functions of posttranslational modifications on remodeling complexes themselves and our understanding of its role is only beginning to emerge.
7. Conclusion
Global chromatin structure is a result of the combination of chromatin remodelers present in the cell. The ability to form various complexes with different activities and the concentration of the remodelers influences the nucleosomal positions genome-wide. Much data have been accumulated from
Acknowledgments
We apologize to all colleagues whose work could not be cited due to space limitations. Work in the G.L. laboratory is funded by the DFG, EraSysBio+ and Baygene. Funding for open access charge: Regensburg University Library.References
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