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Published in final edited form as: Curr Opin Struct Biol. 2022 Jul 18;75:102425. doi: 10.1016/j.sbi.2022.102425

Structures and Consequences of Pioneer Factor Binding to Nucleosomes

Edgar Luzete-Monteiro 1,2, Kenneth S Zaret 1
PMCID: PMC9976633  NIHMSID: NIHMS1873035  PMID: 35863165

Abstract

Pioneer transcription factors are able to bind a partially exposed motif on the surface of a nucleosome, enabling the proteins to target sites in silent regions of chromatin that have been compacted by linker histone. The targeting of nucleosomal DNA by pioneer factors has been observed in vitro and in vivo, where binding can promote local nucleosome exposure that allows other transcription factors, nucleosome remodelers, and histone modifiers to engage the chromatin and elicit gene activation or further repression. Pioneer factors thereby establish new gene expression programs during cell fate changes that occur during embryonic development, regeneration, and cancer. Here, we review recent biophysical studies that reveal the structural features and strategies used by pioneer factors to accomplish nucleosome binding and the consequential changes to nucleosomes can lead to DNA accessibility.

Introduction

Changes in gene expression programs are vital for cell fate transitions during development, regeneration, and cancer[1]. Establishing new transcriptional profiles may activate genes antithetical to the biology of the starting cell. Thus, eukaryotic cells have evolved mechanisms to maintain transcriptional silencing[1]. Much of the genome is composed of naïve, silent chromatin that is not enriched with specific histone modifications[2] and whose compaction by core and linker histones makes it refractory to many regulatory factors[3–6]. Inaccessibility to regulators limits the establishment of epigenetic marks and topographies associated with stable gene activation or repression[1].

In this context, pioneer factors can permeate quiescent chromatin [5–7] due to their intrinsic abilities to bind nucleosomes[8–12] and promote local DNA accessibility[5,13–15], which allows binding of downstream factors that establish new transcriptional networks, with continuous pioneer factor expression also observed for cell identity maintenance [16,17]. Here, we review recent developments in structural biology that describe conformational features of pioneer factors that enable nucleosome engagement via alternative binding strategies. We also discuss newly uncovered architectural consequences of pioneer binding on nucleosomes that culminate in local DNA accessibility.

Structural Features that Contribute to Nucleosome Binding

Nucleosomal DNA is wrapped nearly twice around an octamer of four core histones. The presence of histones, DNA curvature, and adjacent DNA gyre poses constraints to nucleosome binding. Therefore, having DNA-binding domains that engage the DNA helix without colliding with nucleosomal components is crucial for nucleosome binding[12,18,19]. Many strong nucleosome binders engage DNA using a single short α-helix that occupies a small surface on the DNA’s outermost surface (Figure 1a) or two α-helices that straddle the helix on both sides perpendicularly to the core, yet do not extend past the DNA circumference (Figure 1b), thus avoiding clashes with histones[19]. Certain factors with longer DNA-recognition α-helices form kinks that shift their trajectory away from the core before reaching histones, allowing nucleosome binding[19] (Figure 1c)[19]. Furthermore, discrete residues in DNA-binding domains can be structurally crucial or hindering to nucleosome binding, as seen for Oct4[20].

Figure 1. Structural features associated with nucleosome-binding ability.

Figure 1.

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As described by Fernandez-Garcia el al. (2019)[19], nucleosome-binding ability is associated with specific DNA-binding domain structures that can engage nucleosomal DNA without clashing with other nucleosomal components such as core histones and the opposing DNA gyrus. (A, B, C) Good nucleosome binders containing DNA-binding domains formed by: (A) short α-helices that engage a small area on a single exposed face of the DNA; (B) scissor-shaped dimers formed by short α-helices able to straddle and engage the DNA bilaterally without extending past its diameter; (C) as in B, but with longer α-helices that adopt kinks, changing their trajectory outwards before reaching the core. (D, E) Poor nucleosome binders formed by: (D) long scissor-like a-helical dimers too rigid to bend away from the core; (E) bulky domains that engage DNA laterally while occupying a large horizontal space, potentially clashing with the opposite DNA gyrus.

In contrast, poor nucleosome binders often have scissor-like DNA-binding domains with long α-helices that reach beyond the DNA diameter towards the core, clashing with histones (Figure 1d)[19]. Other poor nucleosome binders include factors with non-α-helical DNA binding domains composed of either short helical twists or unstructured domains[19] (Figure 1e). Although their domains do not extend past the DNA, many occupy a large horizontal area around the helix, potentially colliding with the adjacent DNA gyre wrapped around the octamer. The curved conformation of the DNA around the core can also present an obstacle to nucleosome engagement, although it may be overcome by having flexible DNA-binding domains able to adjust to the nucleosomal topography[18].

Still, a systematic analysis of pioneer factor structures, where DNA-recognition α–helices have been lengthened and shortened, has yet to be performed. Furthermore, analyzing DNA-binding domains alone may blind us to non-DBD regions that affect nucleosome binding due to sterical clashes or additional interaction with nucleosomal components (e.g., opposing DNA gyrus or histones), making the use of full-length factors in future structural studies worthwhile.

Motif Positioning and Binding Location Preferences

Another determinant of nucleosome binding is the rotational positioning of motifs, which determines whether they are accessible or occluded, facing the core. Factors including GATA3, Sox2, Oct4, p53, and Rab1 only bind motifs that face outwards[4,5,21,22], preferring exposed, degenerate motifs over high-affinity binding sites facing the core[20]. Factors with small DNA-binding domains that penetrate single DNA grooves, such as the Homeodomain family, have periodic preference patterns around the nucleosome corresponding to exposed DNA segments[3] (Figure 2a).

Figure 2. Modes and positional preferences of nucleosome engagement.

Figure 2.

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As dissected by Zhu et al. (2018)[3], pioneer factors can present preferences for binding specific nucleosomal positions, including: (A) periodic preference for DNA grooves facing away from the core and thus exposed for binding; (B) DNA’s entry-exit site; (C) dyad; (D) intermediate positions along the nucleosome between the entry-exit site and the dyad; and (E) linker DNA. Pioneer factors can also utilize separate/bipartite DNA-binding domains in alternative ways and engage nucleosomes in different modes such as: (F) one domain engaging a partial DNA motif while another binds core histones; (G) each DNA-binding domain engaging adjacent partial motifs on adjacent DNA gyres; (H) one domain binding a partial motif while the other is entirely disengaged from the nucleosome.

The orientation of asymmetric sequence motifs relative to DNA’s longitudinal axis defines which direction the factors face upon binding and thereby whether specific protein domains would clash with other nucleosomal structures such as histones and the adjacent DNA gyre. As such, many ETS and CREB-bZIP factors[3] and Sox2[4] prefer binding to motifs at specific orientations on nucleosomes.

The translational positioning of motifs along the DNA is also crucial. Aside from determining rotational positioning, it places factors at regions that may pose structural constraints or potential histone interaction sites [23]. Factors like NF-kB[13] and Oct4[4] have no preference for specific motif positions or orientations, possibly due to Oct4’s DNA-binding domain’s flexible modularity, allowing adaption to more varied topographies. Other factors prefer motifs at specific positions to bind or to cause downstream effects such as partial DNA unwrapping[14,24](Figure 2b–e).

DNA entry-exit sites on the nucleosome have larger DNA surfaces that are not occluded by core histones[24] and are preferred by factors that engage large radial (bZIP and bHLH) or lateral (C2H2 ZnF) DNA areas[3] (Figure 2b). TP53[22] and Rap1[5] may prefer such sites because nucleosome breathing transiently presents DNA disengaged from the core at the entry-exit[3,24] or because fewer DNA-histone interactions in the area facilitate active disengagement from the core[24].

Preference for the dyad (Figure 2c) is seen for GATA3[25], RFX5[3], and Sox factors[3,4,26], possibly because having only one gyrus in the region minimizes potential clashes with the opposite DNA helix[25] and facilitates DNA distortions caused by factors such as Sox2[4]. Binding at or near the dyad could also help displace linker histone in chromatin, helping to expose the underlying nucleosome. Intermediate positions between the dyad and entry-exit sites (Figure 2d) are preferred by Rab1[14]. Finally, linker DNA is enriched with ELF1 and ELF2, possibly due to factor-mediated nucleosome repositioning[3] (Figure 2e). Positional preferences have also been suggested to arise from local interactions with histones[14] (Figure 2f), although such hypothesis remains to be empirically demonstrated.

Strategies for Nucleosome Binding

Pioneer factors can undertake numerous alternative strategies to adapt to the nucleosomal topography. Various factors have multiple DNA-binding domains that independently target partial motifs and are connected by flexible linker regions. This allows domains to adopt variable relative spacings and orientations on the DNA, avoiding grooves occluded by the core to engage non-adjacent exposed motifs[20,27]. By this modality, T-box factors, Rap1, and Oct4 may bind half-motifs at adjacent DNA gyres[3,5,21] (Figure 2g). In Pax7, all DNA-binding domains must engage DNA for nucleosome binding [28]. Still, at times engagement of only some DNA-binding domains is required for nucleosome binding (Figure 2h), as seen for Klf4[18] and Oct4[18,24,27].

Pioneer factors can bind partial or degenerate motifs in the context of nucleosomes[8,12], when part of a motif is hidden facing the core[21], or to circumvent structural constraints[18]. Sox2 and c-Myc have naturally disordered DNA-binding domains (Figure 3a) that only adopt rigid a-helical conformations upon binding DNA (Figure 3b). By binding incomplete motifs, these factors maintain their last DNA-binding segment flexible, lowering (Figure 3c) or eliminating (Figure 3d) clashes with the nucleosome core[18]. In these cases, decreased binding affinity and specificity could be compensated by cooperative binding with other factors[18,24,29].

Figure 3. Recognition of degenerate motifs can allow nucleosome binding.

Figure 3.

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As suggested by Soufi et al. (2015)[18], nucleosome binding can be achieved by factors with DNA-binding domains that are unstructured in solution yet form α-helices upon DNA binding by recognizing degenerate motifs. The figure shows DNA-binding domains that are: (A) not binding DNA and thus unstructured; (B) binding a full consensus motif where the whole domain forms a rigid α-helix incompatible with nucleosome binding due to clashes with the core; (C) binding motifs with one non-conserved base that allow the domain’s terminal segment to remain unbound and flexible, partially eliminating steric clashes and allowing low-affinity nucleosome binding; (D) binding motifs with two degenerate bases, extending the unstructured terminal region to further minimize clashes, allowing higher-affinity nucleosome binding.

Indeed, co-binding of transcriptional regulators seems to be essential for regulatory sites’ uniqueness and specificity[30] and is common among all types of transcription factors[31–37], including pioneer factors[8,38–49]. Co-binding may be required for certain factors to bind nucleosomes[18,20,50] or can be associated with downstream consequences such as recruitment of other factors[10,51–54], nucleosome displacement[32], deposition of histone marks[52,55], chromatin decompaction[9,52,56], phase separation[57], and gene activation[51,52,58]. Cooperativity can either occur through direct protein interaction[58] or independent binding to nearby/overlapping motifs[8,31,50] as described by the dynamic assisted loading model[34–37].

Examples of cooperativity include non-α-helical, poor nucleosome binders, which often interact with pioneer homeodomain factors, suggesting that structural changes triggered by pioneer binding could relieve steric clashes that otherwise limits engagement by non-pioneers[19]. Similarly, c-Myc depends on the pioneering activity of Oct4-Sox2-Klf4 to bind nucleosomes, subsequently enhancing chromatin binding by the trio[59] in a sequential and reciprocal manner. However, hierarchical interactions can also be non-reciprocal: Oct4 binds prior to and affects Sox2’s binding, but not vice-versa[4]. Factors’ interplay can also be affected by motif positioning: Oct4-Sox2 cooperativity is eliminated by reversing Sox2’s motif and is synergistic at the entry-exit but antagonistic at the dyad[4], possibly because DNA unwrapping to stabilize a partners’ binding is easier at the entry-exit[4,23] compared to the dyad, where steric clashes would be more common for co-bound factors[4]

Nucleosome affinity may also be improved by interactions with histones[20,29,60], potentially contributing to non-specific chromatin scanning[29]. The nucleosome’s acidic patch and its proximal regions are a hotspot for pioneer factor binding[61]. Binding to histone tails is also common, specially H3’s acidic N-terminus – potentially contributing to preferences to entry-exit sites [23]. Histones can be engaged by non-DNA binding residues either outside[29,60] or inside[20] DNA-binding domains. Alternatively, DNA-binding residues themselves could bind histones instead of nucleotides: one of Oct4’s DNA-binding domains is predicted to engage not only an opposite DNA gyrus (Figure 4a), but alternatively the acidic patch[21] (Figure 4b) or H3’s tail[23]. Whether basic DNA-binding domains in general are adept at binding acidic hotspots in histones remains to be studied. Interactions with distinct DNA and histone modifications/variants could also explain certain factors’ preferences for specific chromatin topographies[9,11,62,63] and thereby underlie target specificity, warranting future experiments utilizing non-naïve chromatin.

Figure 4. Recently described structures of pioneer factors bound to nucleosomes.

Figure 4.

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(A&B) molecular dynamics simulations predicting alternative modes of nucleosome engagement by Oct4 (Tan & Takada, 2020)[21]: (A) Oct4 may engage opposite DNA gyre with each of its two DNA-binding domains; (B) one domain can bind DNA while the other binds the core histones’s acidic patch. (C&D) CryoEM structures of Oct4-Sox2-nucleosome complexes showing that motif positioning determines structural effects of binding (Michael et al, 2020)[24]: (C) Sox2 bound close to the entry-exit site bends and thus partially unwraps the DNA (PDB: 6T90); (D) Sox2 bound to an inverted motif closer to the dyad locally peels DNA away from the core (PDB: 6YOV). (E&F) CryoEM structures of Sox2 and Sox11 bound to nucleosomes show local and bilateral terminal DNA detachment from the core (Dodonova et al, 2020) [26]. Due to structural similarities, Sox11 is highlighted: (E) shows a single Sox11 bound laterally (PDB: 6T7A); (F) nucleosomes were also engaged by two Sox11 monomers, promoting bilateral disruption of DNA-histone contacts (PDB: 6T7C).

Structural Consequences of Pioneer Factor Binding

Binding by pioneer factors often affects DNA positioning and structure on the nucleosome. ELF1, ELF2, and RFX5 binding promotes DNA sliding, possibly by stabilizing positions that arise during DNA’s natural thermal-kinetic motion. This can lead to rotational shifts of motifs to more accessible positions[3]. Sliding by Sox2 may also expose or hide distal motifs, thereby affecting binding of other factors such as another Sox2 or Oct4[21]. Although Oct4[24,25] and Rap1[5] do not significantly impact DNA shape (Figure 4a–d), Sox factors bend DNA, promoting partial detachment from the core [18–20]. Effects on nucleosomal structure depend on the direction and positioning of motifs: Oct4-Sox2 binding around entry-exit sites bends DNA away from the core and promotes partial DNA unwrapping[24] (Figure 4c), while binding to a flipped Sox2 motif deeper into the nucleosome creates a DNA curvature facing the core and locally peels DNA from octamers[24] (Figure 4d). Sox11 also causes DNA unwrapping upon binding to the nucleosome superhelical position +2 due to clashes with the DNA terminus on the adjacent gyrus (Figure 4e). DNA detachment also happens on the opposite entry-exit site, possibly due to allosteric effects and stabilized by binding of a second Sox11 at SHL-2 (Figure 4f) [26].

DNA distortions that lead to disruption of DNA-histone interactions [24,26] are also seen with NF-kB[13], Reb1, and Cbf1[14]. Detachment could be accomplished by stabilizing transient DNA disassociation form the core[14], outcompeting histones for DNA binding, or active unwinding[15] and doesn’t necessarily lead to histone eviction[14]. Ablation of DNA-histone interactions also includes displacement of linker histones, which are outcompeted by H1-like domains from FoxA[38,64] and LFY[12] – although Oct4 was seen to be displaced by H1 instead[23].

DNA detachment from the core and displacement of linker histones leads to local DNA accessibility and may result in nucleosome destabilization. Some factors have no effect[5,13] or even stabilize nucleosomal structure[3] and positioning[51]. In fact, DNA unwrapping doesn’t necessarily lead to nucleosome destabilization, as seen for NF-kB[13]. Still, many other factors facilitate partial octamer dissociation from the DNA [3], possibly facilitating subsequent octamer eviction or remodeling. The directionality of effects on nucleosome stability can also depend on the positioning of factors’ binding sites[3]. Accessibility can also be promoted by disruption of nucleosome stacking, as seen for Rab1[5]. Stacking depends on H4’s N-terminal tail engagement of adjacent nucleosomes’ acidic patch. H4’s tail was seen to be repositioned by Sox2, presenting a potential mechanism for disruption of internucleosomal interactions[26] that should be investigated. Still, whether alterations to the nucleosomal structure involve direct interactions between factors and histones themselves remains to be determined.

Ultimately, pioneer factors can promote either the activation of genes [1,9,51,55,65–67] or their repression [1,33,68], depending upon whether they enable activating or repressing secondary factors to enter the chromatin. By recruiting and/or making local DNA accessible to downstream regulators[1,33], they initiate the conversion of naïve chromatin, lacking evident epigenetic marks, into modified chromatin with particular expression states[1]. Regulators include epigenetic factors that modify histones or affect DNA methylation[69], establishing active [1,9,51,55,65–67] or inactive [70] marks. It also includes chromatin remodelers that establish higher-order chromatin accessibility [1,5,10,12,17,33,54,57,65,67,70–72], allowing binding of additional activating/repressive factors [33,70], non-pioneer transcription factors[1,65,73], and/or the transcription machinery[73]. Changes in chromatin architecture such as enhancer-promoter looping[66], formation of super-enhancers[55], and phase separation[57] may also follow, contributing to gene regulation.

Conclusions

Although the consequences of pioneer factor binding have been relatively well-studied, improvements on techniques such as CryoEM allow us to elucidate the crucial first steps of pioneer function, including mechanisms of nucleosome binding and promoting underlying nucleosome and DNA accessibility. At this stage, each detailed structural study of a pioneer factor with a nucleosome is yielding novel insights, suggesting that there is much more to learn as the field moves forward. We note that the use of artificial strong nucleosome-positioning DNA sequences appears not to reflect what happens in situ, where weaker DNA-histone interactions might allow additional structural changes necessary for binding or posterior regulation[1]. Finally, the prevalent use of canonical, non-modified histones still limits our understanding of how factors act on the diverse chromatin landscape found in situ. Going forward, expanding the list of factors studied, adopting endogenous DNA targets more frequently, and diversifying the types of histones utilized in structural studies should allow us to more accurately understand pioneer factors’ function.

Highlights.

  • Pioneer transcription factors can establish new gene expression programs due to their ability to bind compacted nucleosomal DNA and promote local accessibility to other factors.

  • DNA-binding domain structural traits allow certain transcription factors to bind nucleosomes while others possess steric constraints to nucleosome engagement.

  • Pioneer factor binding is affected by DNA motifs’ translational, rotational, and directional positioning on nucleosomes.

  • Pioneer factors can adopt alternative strategies to adapt to nucleosome topography, leading to different modes of binding.

  • Binding by pioneer factors can cause structural changes on nucleosomes, leading to increased DNA accessibility which allows engagement of other factors.

Acknowledgements:

The authors’ work was supported by NIH grant GM36477.

Footnotes

CRediT statement:

- the corresponding author Dr. K. Zaret is responsible for ensuring that all descriptions are accurate and agreed by all authors

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