The eukaryotic genome is organized in a functional and spatially segregated manner within the interphase nucleus. Nuclear architecture plays a crucial role in gene regulation and defining cellular identity. Early studies led to the classical view of a bipartite chromatin composition in which euchromatin is defined as active chromatin located at the nuclear center while heterochromatin corresponds to the more compact chromatin fraction, generally positioned at the nuclear periphery and surrounding the nucleoli (Cremer and Cremer, 2001; Jost et al., 2012; Solovei et al., 2016). While heterochromatin correlates with late-replicating, low-GC chromatin, euchromatin is characterized by an early replication timing and high-GC content. This differential epigenetic landscape of the interphase nucleus can be also recapitulated by Giemsa bands (G-bands) (Serna-Pujol et al., 2021), which arise from the characteristic banding of metaphase chromosomes.

Chromatin organization involves several hierarchical levels, including chromosome territories (Cremer and Cremer, 2001; Girelli et al., 2020), A (active) and B (inactive) compartments at the megabase level (Lieberman-Aiden et al., 2009), topological associated domains (TADs) (Dixon et al., 2012; Nora et al., 2012; Sexton et al., 2012), and chromatin loops. Moreover, chromatin segregation is facilitated by chromatin tethering to scaffolding structures. This anchorage originates nuclear environments referred as lamina-associated domains (LADs) or nucleolus-associated domains (NADs), which constitute heterochromatic regions anchored to the nuclear lamina and the nucleolus, respectively.

Human cells have 1000–1500 LADs that cover more than one-third of the genome (Guelen et al., 2008). LADs represent a well-known repressive environment, characterized by low gene density, low gene expression, and a great overlap with B compartment. LADs are enriched in repressive histone modifications, including H3K9me2, which is considered a conserved chromatin mark of LADs (Poleshko et al., 2019). While H3K9me2 plays a part in anchoring chromatin to the nuclear lamina, current data indicate that it is probably not a sufficient signal in mammals, as other anchoring mechanisms may exist (Harr et al., 2015; Kind et al., 2013).

The nucleolus is a membraneless structure where ribosome biogenesis and regulation occurs. Nucleoli also act as central chromatin organizers. Genomic regions positioned close to nucleolus are referred as NADs, which were firstly genome-wide identified in human using a biochemical purification of nucleoli (Dillinger et al., 2017; Németh et al., 2010). NADs consist of mainly heterochromatic regions and an important overlap with LADs was found. Accordingly, some LADs have been found to stochastically reshuffled after mitosis and associate with nucleoli (Kind et al., 2013). These observations suggest that the lamina and nucleolus could act as interchangeable scaffolds for heterochromatin positioning. More recently, the inclusion of HiC-based approaches has provided more accurate genome-wide NADs maps (Bersaglieri et al., 2022; Peng et al., 2023).

Histone composition, including histone variants and their modifications, also plays a role in defining chromatin functionality (Martire and Banaszynski, 2020). In particular, linker histone H1 family is evolutionary diverse and human somatic cells may contain up to seven H1 variants (H1.1 to H1.5, H1.0, and H1X). Although H1 has classically been regarded as a general repressor, increasing evidence support H1 variants functional diversity in chromatin regulation (Fyodorov et al., 2018; Millán-Ariño et al., 2016). A compromised H1 content causes chromatin structural defects, evidenced both in human (Serna-Pujol et al., 2022) and mice models (Geeven et al., 2015; Willcockson et al., 2021; Yusufova et al., 2021). Although in these scenarios multiple H1 variants depletion leads to chromatin decompaction, the contribution of individual H1 variants in maintaining chromatin structure has not been studied.

A long-standing enigma concerning H1 is whether its variants have a uniform distribution in different cell types or, conversely, display cell-line-specific binding patterns. The presumption that H1 variants are specifically distributed among different cell lines comes from combining various pieces of evidence from different publications (Cao et al., 2013; Izzo et al., 2013; Li et al., 2012; Millán-Ariño et al., 2014; Torres et al., 2016). Nevertheless, no study has properly addressed the question up to date. Consequently, the absence of existing reports using standardized experimental and analytical workflows may lead to potential misinterpretation of the data. The only studies that performed a systematic analysis of different variants have been performed in a single-cell model and often used overexpression strategies. These include the analysis of H1.1–H1.5 using DamID in IMR-90 cells (Izzo et al., 2013), and a second report in which ChIP-Seq of endogenous H1.2 and H1X and the exogenous H1.0-HA and H1.4-HA was performed in T47D cells (Millán-Ariño et al., 2014). Recently, we performed the first genome-wide analysis of six endogenous H1 variants in human cells, bypassing the everlasting limitation of mapping exogenous proteins (Serna-Pujol et al., 2022 and in preparation for H1.3 data). In T47D cells, H1 variants are distributed in two large groups depending on the local GC content. H1.2, H1.3, H1.5, and H1.0 are enriched at low-GC regions and B compartment while H1.4 and H1X are more abundant within high-GC regions and A compartment. However, whether these distribution profiles are conserved among different cell types remains unknown.

H1 complement (i.e. H1 variants and its proportions present in a specific cell) is dynamic throughout differentiation and cancer and also varies between cell types. Whether these expression fluctuations translate into changes in distribution patterns has not been studied. The best-characterized example is H1.0, which accumulates during differentiation (Terme et al., 2011) and whose expression is associated to a less aggressive phenotype of tumoral cells (Torres et al., 2016). H1.0 has been described as a replacement histone, as it responds to a compromised H1 content. In breast cancer cells, combined depletion of H1.2 and H1.4 leads to H1.0 upregulation, although without significant redistribution alterations (Izquierdo-Bouldstridge et al., 2017; Serna-Pujol et al., 2022).

In this study, we provide novel insights into the differential nuclear distribution of somatic H1 variants in human cells, through an imaging approach. Super-resolution microscopy in T47D cells shows that H1.2, H1.3, H1.5 and, to a lesser extent, H1.0, are enriched at the nuclear periphery and coincide more with more compacted DNA, as supported by super-resolution microscopy. Contrarywise, H1X and H1.4 are distributed throughout the nucleus with a significant H1X enrichment in nucleoli. Differential distribution patterns suggest concrete implications in genome functionality and translate into variant-specific functional consequences upon H1 depletion. Specifically, single or combined H1.2 depletion triggers a general chromatin decompaction, which is not observed when depleting H1.4 or H1X. Furthermore, we conducted the first systematic comparison of six somatic H1 variants in several human cell lines, including ChIP-Seq profiling of H1X in different cell types, which has only been mapped in T47D breast cancer cells up to date. Interestingly, certain H1 variants display universal distribution patterns, despite variations in H1 complement across cell lines. H1.2, H1.3, and H1.5 are consistently enriched at the nuclear periphery while H1X is more abundant at high-GC regions and present at nucleoli in all cell lines evaluated. We identified a recurring concomitant absence of H1.3 and H1.5, and this specific H1 complement is associated with a more peripheral distribution of H1.0 and H1.4 proteins, suggesting potential compensatory mechanisms between variants. Altogether, our study represents a comprehensive attempt to systematically characterize the repertoire of somatic H1 variants, their differential distribution in the human genome and their functional diversity.

Tethering of chromatin to scaffold structures, such as the nuclear lamina or the nucleolus, regulates genome conformation and ultimately, its function. Despite being highly abundant proteins in the nucleus, distribution of histone H1 variants within nuclear domains has not been explored. We have recently reported that H1 variants exhibit differential genomic distributions in T47D breast cancer cells. H1.0, H1.2, H1.3, and H1.5 are enriched at low-GC regions and B compartment while H1.4 and H1X are more abundant within high-GC and A compartment regions (Serna-Pujol et al., 2022). Moreover, a combined depletion of H1.2 and H1.4 leads to chromatin decompaction at the level of TADs (Serna-Pujol et al., 2022), demonstrating that H1 proteins are involved in maintaining genome structure. In this study, we profiled the differential nuclear distribution of six somatic H1 variants in T47D cells and other human cells lines, through imaging techniques, including super-resolution microscopy. We provide here the first systematic comparison of H1 variants distribution in multiple human cell lines.

In T47D cells, H1.2, H1.3, and H1.5 and to a lesser extent H1.0 are enriched toward nuclear periphery. On the other hand, H1X and H1.4 are distributed throughout the nucleus with H1X being highly enriched in nucleoli (Figure 1A). Super-resolution imaging of H1 variants reinforced these differential profiles and revealed that H1.2/H1.3/H1.5/H1.0 coincide more with DNA pattern compared to H1.4 and H1X (Figure 2A), confirming their segregation in two groups denoted by ChIP-Seq data. Both immunofluorescence and ChIP-Seq are performed on fixed cells and H1 are known to be highly mobile proteins. Thus, although our results demonstrate this variant-specific preferential distribution, it is unlikely that H1 variants are unable to dynamically bind other chromatin types.

Emerging evidence from super-resolution microscopy indicates that nucleosomes are grouped in heterogenous nanodomains termed ‘clutches’ (Ricci et al., 2015). Moreover, TADs represent structural chromatin folding units at the sub-megabase scale (Dixon et al., 2012; Nora et al., 2012; Sexton et al., 2012). We have shown that H1 variants form spatially separated nanodomains throughout the nucleus, visualized as a ‘punctuate’ signal by super-resolution imaging, but with the aforementioned differential variant-specific local enrichments. Similarly, super-resolution imaging of core histone H2B also present this clustered pattern in human fibroblasts (Ricci et al., 2015). It is important to mention that nucleosome clutches were originally defined using STORM technique (Ricci et al., 2015), whose resolution is higher than the one achieved by SRRF. For that reason, we favor the idea that nanodomains formed by H1 variants would be more equivalent to TADs or sub-TADs rather than to nucleosome clutches. In fact, shifts on the ChIP-Seq H1 variants distribution tend to coincide with TAD borders and H1 variants are more homogenous within the same TAD than between TADs (Serna-Pujol et al., 2021). This observation also highlights the relationship between H1 distribution and the structural properties of chromatin.

By conventional immunofluorescence, preferential localization of H1.0 with other ‘low-GC’ H1 variants over H1.4/H1X was observed (Figure 2—figure supplement 1). However, this preferential co-localization was not evidenced at the super-resolution level and all H1s co-localized similarly with H1.0 (Figure 2B). This observation may suggest that domains spatially arranged at the 3D level are homogeneously marked by a certain H1 variant and not by random H1 variants. Nevertheless, in a cell population those nanodomains could be marked by different H1 variants. This could explain why at single-cell level we lost preferential co-localization of ‘low-GC’ H1s with H1.0 (compared to H1.4/H1X) while by ChIP-Seq data, mega-base domains of ‘low-GC’ H1 variants coincide. If those nanodomains were homogeneously marked by the same H1 variant in the cell population, we would observe differential enrichments between H1 variants belonging to the same GC cluster, even at the mega-base level. This apparent intra-population ambiguity may be indicating a structural role of ‘low-GC’ H1 variants and emphasizes the existing partial redundancy among certain H1 variants.

H1.2, H1.3, and H1.5 are highly enriched at the nuclear periphery in T47D cells but also in all cell lines analyzed (Figures 1 and 5A, B). Super-resolution microscopy revealed that these H1 variants form an adjacent layer to lamina and highly co-localize with H3K9me2 (Figure 3A–C). H3K9me2 is not only a universal component of LADs, but also it is indispensable for peripheral heterochromatin anchoring to the nuclear lamina (Poleshko et al., 2019). Universal H1.2, H1.3, and H1.5 enrichment at nuclear periphery directly point to these H1 variants as conserved components of LADs, as has been described for H3K9me2. Furthermore, these H1 variants could be postulated as potential orchestrating factors for chromatin tethering to the lamina. Proper chromatin–lamina interactions are crucial to maintain chromatin dynamics (Briand and Collas, 2020; Chandra et al., 2015; Chang et al., 2022; Zheng et al., 2018). LADs detachment through Lamin B1 KO in human cells led to abnormal segregation of chromosome territories and A/B compartments, as well as global chromatin decompaction (Chang et al., 2022). Actually, we have shown that H1.2 depletion in T47D cells also led to a global chromatin decompaction (Figure 4).

Interactions between the nuclear lamina and LADs are disrupted at early stages of mitosis and re-established upon mitotic exit. In general, mitosis involves large structural reorganization of chromatin (Imakaev et al., 2012) that is accompanied by eviction of multiple chromatin factors from DNA (Martínez-Balbás et al., 1995). On the other hand, factors that persist attached to chromatin, including multiple histone variants and histone modifications (Wang and Higgins, 2013), are suggested to act as spatial ‘bookmarks’. This is the case of H3K9me2, which is reported to safeguard positional information of LADs through mitosis, through a phospho-methyl switch (H3K9me2S10p) (Poleshko et al., 2019). Indeed, we have found that interphasic ‘low-GC’ H1 variants persist more attached to chromatin during mitosis, compared to ‘high-GC’ ones (Figure 2E, Figure 2—figure supplements 2 and 3). Moreover, H1.3 and H1.5, which are highly associated to LADs in interphase, persist in the peripheral layer of mitotic chromosomes, showing an analogous profile to the one reported for H3K9me2 (Poleshko et al., 2019). H1.2 attachment to mitotic chromatin is regulated by phosphorylation at early mitotic stages, but interestingly, H1.2 layer re-associates to the forming lamina upon mitotic exit. The strong similarities observed for H1.2, H1.3, and H1.5 with H3K9me2 in both interphase and mitosis suggest that these linker histones may also act as 3D positional ‘bookmarks’ of LADs.

We found that H1 variants may localize to nucleoli. Concretely, H1X and some phosphorylated H1s present different nucleolar distribution patterns (Figure 3F). H1X nucleolar enrichment has already been described in previous works (Mayor et al., 2015; Stoldt et al., 2007). In addition, other histone variants have been found at nucleoli, including testis-restricted H1T linker histone (Tani et al., 2016) or certain core histone variants (Jiang et al., 2021; Long et al., 2019; Pang et al., 2020). Importantly, nucleolar localization of H1X persists after inhibition of RNApol I by ActD (Figure 3—figure supplement 1D), which was also reported previously (Stoldt et al., 2007). These observations might suggest a more structural role of H1X in nucleoli rather than a more functional or regulatory one. On the contrary, H1.2-pT165 and H1.4-pT146 seem to execute a functional role, as the nucleolar distribution of these post-translationally modified H1 variants depends on functional nucleoli, with H1.4-pT146 being presumably associated to RNA pol I active transcription. The nucleolus is a membraneless organelle formed through liquid–liquid phase separation driven by multivalent interactions of its components (Lafontaine et al., 2021). Several molecular features are known drivers for phase separation, including highly intrinsically disordered regions (Shin and Brangwynne, 2017). Indeed, nucleolar proteome and specially proteins localized to the nucleolar rim are extremely disordered (Stenström et al., 2020). We found that nucleolar H1X is enriched, although not limited, at the nucleolar rim, adjacent to the inner side of NPM1 layer (Figure 3E). Histone H1 proteins have a well-known highly disordered structure and have been shown to phase separate in vitro (Gibson et al., 2019; Shakya et al., 2020; Turner et al., 2018). However, the functional relevance of H1 variants as promotors of phase separation in living cells has not been explored.

Proteomic studies in four human cell lines demonstrated that almost 1/3 of the candidate H1.0-binding proteins localized to nucleolus and were related to nucleolar functionality (Kalashnikova et al., 2013). Remarkably, the experiments were performed by pull-down of exogenous, chimeric HaloTag-H1.0 protein. Importantly, direct H1.0 nucleolar localization or rRNA metabolism alterations upon H1.0 depletion were not reported. In contrast, our results show that H1.0 is depleted from nucleoli in all cell lines analyzed (Figure 5A, B). We also checked that H1.0 does not redistribute to nucleoli upon H1X depletion in T47D cells (data not shown). Nevertheless, we cannot discard that H1.0 interacts with nucleolus-related proteins, as it can be enriched at perinucleolar heterochromatin or NADs, as observed in T47D cells.

We have explored how H1 variants depletion affect chromatin structure through super-resolution imaging of DNA (Figure 4). In T47D cells, combined depletion of H1.2 and H1.4 (i.e. multi-H1 KD) caused a global chromatin decompaction. This is in agreement with previously generated ATAC-Seq experiments in these cells, which pointed to a genome-wide gain of chromatin accessibility. Accordingly, Hi-C data analysis in multi-H1 KD cells also showed more de-compacted TAD structures (Serna-Pujol et al., 2022). In mice, multiple H1 variants deficiency has been also associated to chromatin decompaction (Willcockson et al., 2021; Yusufova et al., 2021). However, the differential contribution of individual H1 variants to chromatin structure has not been explored before. Interestingly, analysis of T47D single KDs revealed that single H1.2 depletion also led to chromatin decompaction, but not as pronounced as multi-H1 KD. On the contrary, single depletion of H1.4 or H1X did not cause a significant alteration of chromatin structure. These observations suggest that the structural defects cannot be explained just for the total H1 reduction. Indeed, both H1.2 and H1.4 proteins contribution to total H1 content is the same in T47D, estimated to be 23–24% in each case (Sancho et al., 2008). Thus, H1 variant-specific functionality, related to their differential genomic distribution seems to play a role. These results could support the putative structural function of H1.2 (and maybe also for the rest of ‘low-GC’ variants). In multi-H1 KD cells, total H1 content is reduced ≈30% and chromatin decompaction is more drastic compared to single H1.2 depletion. Due to the fact that H1.2 and H1.4 occupy different genomic regions, the more drastic effects on decompaction in multi-H1 KD cells seem to be due, at least in part, to the additive depletion of two H1 variants with non-redundant functions. In the whole, super-resolution microscopy of DNA enables us to decipher global compaction changes upon several H1 KDs conditions and revealed that H1 variants have specific roles in shaping genome architecture. Moreover, both the total H1 reduction but also the H1 variant repertoire have an impact on the global chromatin compaction homeostasis.

H1 complement is known to be heterogeneous among cell types. We have observed that H1X is expressed in all cell lines tested, as it was previously reported with H1.2 and H1.4 (Millán-Ariño et al., 2016). Interestingly, the simultaneous lack of H1.3 and H1.5 is found recurrently and seems to be mediated by DNA methylation (Figure 5—figure supplements 1 and 2). On the contrary, whether H1 variants are universally distributed or display cell-type-specific patterns is not well understood. H1 variants are thought to be specifically distributed among different cell lines, but this presumption comes from combining various pieces of evidence from different publications (Cao et al., 2013; Izzo et al., 2013; Li et al., 2012; Millán-Ariño et al., 2014; Torres et al., 2016). They mostly address the analysis of a single H1 variant in a particular model or cell line. Moreover, a comparative study of the distribution of a single H1 variant in different cell models has not been performed so far. In the whole, the direct comparison of these studies is biased by the different origin of the data and the varied methodologies used, which in many cases involve the over-expression of H1 variants.

We performed the first systematic analysis of six endogenous variants in different cancer cell lines. Our data unveil, for the first time, universal nuclear patterns exhibited by specific H1 variants. Immunofluorescence experiments revealed that H1.2, H1.3, and H1.5 are universally enriched toward nuclear periphery. H1.0 and H1.4 are distributed throughout the whole nucleus but they show a more peripheral distribution in a subset of cell lines lacking H1.3 and H1.5 (Figure 5). H1X is also distributed throughout the whole nucleus in all cell lines tested with a variable relative nucleolar enrichment. H1.0 and H1.4 re-distribution when H1.3 and H1.5 proteins are absent contrast to the behavior observed in T47D multi-H1 KD. Upon multi-H1 KD, H1 variants distribution is overall robust, with no significant changes at the nuclear level (Serna-Pujol et al., 2022). These represent two different H1-compromised scenarios. In the first one, H1.3 and H1.5 silencing is intrinsically linked to the cell line identity. On the contrary, multi-H1 KD cells represent an inducible H1.2 and H1.4 depletion, abnormal in T47D cells. Our results suggest that compensatory mechanisms between different H1 variants, in terms of distribution, may be limited when perturbing H1 levels but achieved when H1 repertoire is ‘naturally’ compromised. Regarding the functional outcomes of H1-restriction, multi-H1 KD cells are characterized by a robust interferon response, triggered by the expression of repetitive elements (Izquierdo-Bouldstridge et al., 2017). Notably, RT-qPCR experiments indicated that cells lacking H1.3 and H1.5 exhibit a high basal expression of the interferon signature and some repeats (Figure 5—figure supplement 5). Whether the concurrent loss of H1.3 and H1.5 represents an acquired adaptive mechanism in certain cancer cells, as well as the implications of the immune response triggered by H1 loss are interesting subjects for study.

In summary, our findings highlight the differential distribution of H1 variants within nuclear domains and their variant-specific role on chromatin (Figure 6). Moreover, we showed that H1 variants present a potentially more uniform distribution among cell lines than previously anticipated, particularly for certain variants.

Figure 6

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ChIP-Seq data of H1X in five different cancer cell lines have been deposited in NCBI's Gene Expression Omnibus (GEO) and is accessible through GEO Series accession number GSE236678. ChIP-Seq of H1.3 in T47D cells is available through the accession number GSE236878.

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Author details

1. Monica Salinas-Pena

   Molecular Biology Institute of Barcelona (IBMB-CSIC), Barcelona, Spain

   Contribution

   Conceptualization, Data curation, Formal analysis, Validation, Visualization

   Competing interests

   No competing interests declared

2. Elena Rebollo

   Molecular Biology Institute of Barcelona (IBMB-CSIC), Barcelona, Spain

   Contribution

   Data curation, Software, Methodology

   Competing interests

   No competing interests declared

3. Albert Jordan

   Molecular Biology Institute of Barcelona (IBMB-CSIC), Barcelona, Spain

   Contribution

   Conceptualization, Supervision, Funding acquisition, Writing - original draft, Writing - review and editing

   For correspondence

   ajvbmc@ibmb.csic.es

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-3970-8693

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