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Histone variants at a glance

Paul B. Talbert, Steven Henikoff

Journal of Cell Science · 2021 · Review · CC BY

doi:10.1242/jcs.244749

Abstract

Eukaryotic nucleosomes organize chromatin by wrapping 147 bp of DNA around a histone core particle comprising two molecules each of histone H2A, H2B, H3 and H4. The DNA entering and exiting the particle may be bound by the linker histone H1. Whereas deposition of bulk histones is confined to S-phase, paralogs of the common histones, known as histone variants, are available to carry out functions throughout the cell cycle and accumulate in post-mitotic cells. Histone variants confer different structural properties on nucleosomes by wrapping more or less DNA or by altering nucleosome stability. They carry out specialized functions in DNA repair, chromosome segregation and regulation of transcription initiation, or perform tissue-specific roles. In this Cell Science at a Glance article and the accompanying poster, we briefly examine new insights into histone origins and discuss variants from each of the histone families, focusing on how structural differences may alter their functions.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 20, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

Eukaryotic chromatin is organized by nucleosomes, which package and regulate access to DNA and whose primary role may be to globally repress transcription. Nucleosomes are formed from an octameric core particle of two molecules each of the histones H2A, H2B, H3 and H4, which wraps 147 bp of DNA (see poster). Histone fold domain proteins (HFDs) have a long history in all domains of life (Box 1), but a eukaryotic innovation is their ability to heterodimerize in specific pairs, H3 with H4, and H2A with H2B, which can further associate through four-helix bundles, H3 with H3, and H4 with H2B, to form a central H3–H4 tetramer flanked by two H2A–H2B dimers (see poster). The HFDs have unstructured tails that are the sites of post-translational modifications. A nucleosome may be further stabilized by the H1 ‘linker’ histone, which interacts with the DNA that links adjacent nucleosomes. ‘Bulk’ or ‘replication-coupled’ (RC) histones are primarily deposited during replication. In animals, RC histones are encoded by multiple genes with special mRNAs that lack introns and polyadenylated (polyA) tails, but instead have a 3′ stem-loop structure. A subset of these genes can also form transcripts with polyA tails in differentiated tissues that no longer replicate, and therefore are available to replace evicted histones. Some histone genes, however, encode distinct paralogs that differ in amino acid sequence from their RC counterparts. These histone ‘variants’ are usually encoded by single genes that have both introns and polyA tails, and are typically available for deposition throughout the cell cycle [replication-independent (RI)], replacing evicted RC histones. Histone variants often confer different structural properties on nucleosomes and often have distinct functions in cell division, transcription, DNA repair, differentiation and chromatin remodeling. We have previously reviewed the phylogenomic scope and dynamics of histone variants. In this Cell Science at a Glance article, and the accompanying poster, we instead focus on recent insights into histone origins, and present an overview of variants in each histone class, emphasizing mammalian variants.

+1 nucleosome: the first nucleosome of a gene, immediately downstream of the nucleosome-depleted region at the transcription start site.Azoospermia: absence of motile sperm in the semen. It can be due to an obstruction of the reproductive tract or to the failure to produce sperm.Blastopore: a mouth-like indentation or opening into the developing gastrula. In vertebrates, it becomes the anus.Cohesins: ring-like protein complexes that hold loops of DNA or sister chromatids together.HMfB family: a family of HFD proteins in archaea (named for histone Methanothermus fervidus B) that can wrap DNA but have no significant primary sequence similarity with to eukaryotic histones. They can dimerize, form tetramers or form more extended oligomers.Protamines: small arginine-rich proteins that replace histones in sperm of many vertebrates to further condense the chromatin, presumably to improve sperm motility and DNA protection. Similar proteins are found in many invertebrates.Rapid response genes: genes typically activated within minutes of some stimulus.Sex body: the condensed X and Y chromosomes in mammalian spermatocytes, as the visual manifestation of undergoing meiotic sex chromosome inactivation. Histone fold domain (HFD) proteins are found in all three cellular domains and in some viruses (see poster), although two families of HFD proteins that are found in both bacteria and archaea have unknown functions and DNA-binding abilities. Many archaea additionally have one or more histones of the histone Methanothermus fervidus B (HMfB) family, which bind to DNA and are more similar in structure to eukaryotic histones, although they are not specifically related in sequence and mostly lack the unstructured tails of eukaryotic histones. HMfB family histones fold together, usually in homomeric dimers, which can be further polymerized through four-helix bundles to form tetrameric HFD particles that wrap 60 bp of DNA or to form more extended DNA-wrapping polymers, termed hypernucleosomes (see poster). Some also have tandemly coupled, diverged HFDs that fold together and then dimerize into particles with four HFDs. A similar organization of pairs of tandem HFDs has recently been found in Marseilleviridae, where the tandem HFDs have tails and have distant similarity with H4–H3 and H2B–H2A. Medusavirus, which belongs to the same large clade of nucleo-cytoplasmic large DNA viruses as the Marseilleviridae, encodes individual core histones specifically related to H2A, H2B, H3 and H4. The individual viral histone domains branch in a phylogenetic tree at the base of all eukaryotic histones of the corresponding histone family (see poster), suggesting these viral histones represent an intermediate state in the evolution of histones from archaeal-like HFDs to modern eukaryotic histones. It seems likely that these viruses captured histones at different times in the evolution of proto-eukaryotic histones and adapted them to package their own genomes. Medusavirus also has an H1 linker histone, but it is most closely related (43% identical) to the H1 of its protist host Acanthamoeba castellani, suggesting a more recent derivation than the core histones, which do not show a specific relationship to Acanthamoeba.

+1 nucleosome: the first nucleosome of a gene, immediately downstream of the nucleosome-depleted region at the transcription start site.

Azoospermia: absence of motile sperm in the semen. It can be due to an obstruction of the reproductive tract or to the failure to produce sperm.

Blastopore: a mouth-like indentation or opening into the developing gastrula. In vertebrates, it becomes the anus.

Cohesins: ring-like protein complexes that hold loops of DNA or sister chromatids together.

HMfB family: a family of HFD proteins in archaea (named for histone Methanothermus fervidus B) that can wrap DNA but have no significant primary sequence similarity with to eukaryotic histones. They can dimerize, form tetramers or form more extended oligomers.

Protamines: small arginine-rich proteins that replace histones in sperm of many vertebrates to further condense the chromatin, presumably to improve sperm motility and DNA protection. Similar proteins are found in many invertebrates.

Rapid response genes: genes typically activated within minutes of some stimulus.

Sex body: the condensed X and Y chromosomes in mammalian spermatocytes, as the visual manifestation of undergoing meiotic sex chromosome inactivation.

Histone fold domain (HFD) proteins are found in all three cellular domains and in some viruses (see poster), although two families of HFD proteins that are found in both bacteria and archaea have unknown functions and DNA-binding abilities. Many archaea additionally have one or more histones of the histone Methanothermus fervidus B (HMfB) family, which bind to DNA and are more similar in structure to eukaryotic histones, although they are not specifically related in sequence and mostly lack the unstructured tails of eukaryotic histones. HMfB family histones fold together, usually in homomeric dimers, which can be further polymerized through four-helix bundles to form tetrameric HFD particles that wrap 60 bp of DNA or to form more extended DNA-wrapping polymers, termed hypernucleosomes (see poster). Some also have tandemly coupled, diverged HFDs that fold together and then dimerize into particles with four HFDs. A similar organization of pairs of tandem HFDs has recently been found in Marseilleviridae, where the tandem HFDs have tails and have distant similarity with H4–H3 and H2B–H2A. Medusavirus, which belongs to the same large clade of nucleo-cytoplasmic large DNA viruses as the Marseilleviridae, encodes individual core histones specifically related to H2A, H2B, H3 and H4. The individual viral histone domains branch in a phylogenetic tree at the base of all eukaryotic histones of the corresponding histone family (see poster), suggesting these viral histones represent an intermediate state in the evolution of histones from archaeal-like HFDs to modern eukaryotic histones. It seems likely that these viruses captured histones at different times in the evolution of proto-eukaryotic histones and adapted them to package their own genomes. Medusavirus also has an H1 linker histone, but it is most closely related (43% identical) to the H1 of its protist host Acanthamoeba castellani, suggesting a more recent derivation than the core histones, which do not show a specific relationship to Acanthamoeba.

H3 variants

Most multicellular and some unicellular eukaryotes have separate RC and RI H3 paralogs, although in organisms with only one form of H3, such as yeast, that form is deposited both during and outside of replication and more closely resembles RI variants in sequence. In most animals, the RC and RI H3s correspond to human H3.2 and H3.3, respectively. Human H3.1, which differs in a single amino acid from H3.2, is a mammal-specific RC paralog. Differences between RC and RI H3s in residues 87–90 in the N-terminal end of α-helix 2 (SAVM versus AAIG in animals) specify different modes of chromatin assembly mediated by different chaperones: the chromatin assembly factor 1 (CAF1; CHAF1A, CHAF1B and RBBP4) complex for RC H3.1–H4 dimers, and histone regulator protein A (HIRA), or α-thalassemia mental retardation syndrome X-linked (ATRX) and death domain-associated protein 6 (DAXX) for RI H3.3–H4 dimers (see poster). Whereas CAF1 distributes H3.1 and H3.2 throughout the genome during replication, HIRA replaces nucleosomes lost during transcription with H3.3 nucleosomes, thereby depositing H3.3 in active genes, promoters, enhancers, transcription termination sites and other locations of histone turnover. ATRX and DAXX deposit H3.3 in telomeres, imprinted genes and other heterochromatic loci, where it is modified with the trimethlyated lysine 9 heterochromatic mark (denoted H3K9me3) to maintain heterochromatin at these locations. The difference between deposition pathways for RC H3.1 and RI H3.3 underlies the more-severe effects of pediatric diffuse midline gliomas caused by H3.1K27M mutations than those caused by H3.3K27M mutations, both of which inhibit global formation of H3K7me3, which normally prevents tumorigenesis.

Although Caenorhabditis H3.3 is not required for viability, in H3.3-deficient Drosophila males, chromosomes fail to condense properly for meiosis and undergo segregation defects. In mice with H3.3 knockout mutations, failure to maintain heterochromatin leads to mitotic abnormalities and embryonic lethality. In H3.3-reduced male mice, apoptosis of spermatogonia and spermatocytes occurs, and the transition from histones to protamines (see Glossary) during spermatogenesis is incomplete.

RI H3.3s also typically differ from RC H3s in having a serine or threonine residue in the N-terminal tail (serine 31 in animals), which is phosphorylated in the pericentromere and at telomeres during metaphase by checkpoint kinase 1 (CHK1; also known as CHEK1) and Aurora B kinases. In euchromatin of mouse embryonic stem cells, phosphorylation of H3.3S31 (H3.3S31ph) by CHK1 promotes p300-dependent acetylation at enhancers, which facilitates differentiation of these cells. In Xenopus embryos, H3.3S31ph is necessary for blastopore (see Glossary) closure, and nucleosomes with the phosphomimic H3.3S31D are enriched for H3.3K27 acetylation, which is permissive for gene activation. In addition, in mouse cells, such as macrophages, stimulated to rapid response (see Glossary), H3.3S31 is co-transcriptionally phosphorylated over stimulation-induced gene bodies and interacts directly with the histone lysine N-methyltransferase protein SETD2 to promote H3K36me3 formation in genes and to eject the co-repressor ZMYND11, enhancing transcription.

In Arabidopsis, H3.3T31 inhibits the H3K27 methyltransferases Arabidopsis trithorax-related proteins 5 and 6 (ATXR5 and ATXR6). ATXR5 and ATXR6 themselves recognize H3.1A31 and methylate K27 to assure this heterochromatic mark is inherited through replication while avoiding silencing active chromatin containing H3.3. Similarly, the H3.3-like sperm-specific variant H3.10 is altered near K27 and not recognized by ATXR5 or ATXR6, contributing to the loss of H3K27me3 and the expression of spermatogenesis genes. This suggests that a serine or threonine at residue 31 of H3.3 may be conserved across eukaryotic kingdoms to facilitate nucleosome acetylation and enhanced access for transcriptional machinery and to prevent silencing.

Human H3.Y.1 and H3.Y.2 (H3.X) are H3.3-like variants expressed in early cleavage-stage embryos, where they are induced by brief expression of the double homeobox protein 4 (DUX4) transcription factor. They become incorporated into DUX4-inducible genes and promote perdurance of expression of these genes. Similar to what is found for the H3R42H change in mouse H3.4 (Table 1), the H3R42K change in H3.Y.1 and H3.Y.2 create more flexible DNA ends that bind histone H1 less efficiently in both homotypic H3.Y.1 nucleosomes and heterotypic H3.Y.1-H3.3 nucleosomes. Despite having a chaperone recognition sequence identical to H3.3 in the α2-helix, H3.Y.1 and H3.Y.2 nucleosomes are only deposited by HIRA and not by DAXX, which requires the C-terminus of H3.3.

Other human variants, H3.6, H3.7 and H3.8, are tissue-specific. H3.6 forms nucleosomes that seem to have a deposition pattern similar to H3.3 nucleosomes, but are less stable because of an I62V change that reduces hydrophobic contact with H4. H3.7 does not form nucleosomes in vitro and H3.8 has a very low but detectable expression level in ovary, colon and kidney. Tissue-specific H3 variants are fairly common in ciliates, plants and animals, and are often expressed during animal spermatogenesis, where they may destabilize nucleosomes in the transition from histones to protamines (Table 1).

The most divergent and universal H3 variant is the centromere-specific variant cenH3, known as Cse4 in budding yeast, CENP-A in animals and CENH3 in plants. cenH3 serves as a foundational protein required to build the kinetochore in most eukaryotes, but surprisingly it has been lost in trypanosomes, the fungus Mucor and in four clades of holocentric insects, which comprise thousands of species. The HFDs of cenH3s are generally only ∼50% conserved with those of other H3s and their N-terminal tails and loop 1 are typically longer than H3 tails and cannot be aligned between divergent species. Distinct chaperones exist for cenH3s, which, at least in Drosophila, recognize loop 1 and co-evolve with it. Unlike most other histones, cenH3s in animals and plants evolve rapidly, presumably because competition between centromeres for inclusion in the egg in female meiosis drives rapid evolution of centromeres. This phenomenon, known as centromere drive, can result in the expansion of centromeres (reviewed in; ) and/or in centromeres with a 10 bp periodicity of A/T dinucleotides, which favor stable wrapping of nucleosomes. cenH3s are thought to then evolve to restore equal segregation of unequal centromeres. This conflict highlights the evolutionary tension between genetic (DNA-dependent) and epigenetic (DNA-sequence-independent) pressures on cenH3 evolution.

In summary, from a likely single H3.3-like ancestor, H3 paralogs diversified to specialize for roles in replication, kinetochore formation and spermatogenesis and for differential modification to promote or resist gene silencing. H3 variants can differ in their stability, their modifications, the enzymes or structures that interact with them, or, through their chaperones, differ in where and when they are assembled into nucleosomes.

H4 variants

H4 variants are infrequent, but humans have H4.7 (H4.G), which has a truncated C-terminus and only 85% amino acid identity with RC H4. The H4C7 gene is encoded in the histone 1 gene cluster along with RC histones, but forms a polyadenylated transcript that is expressed at low, but elevated, levels in breast and colon cancer cell lines relative to normal breast tissue. H4.7 localizes to the nucleolus through an interaction of its α3-helix with nucleophosmin 1 and appears to form unstable nucleosome-like structures and less compact chromatin on rDNA, which promotes rRNA transcription.

H2B variants

Whereas H3 and H4 RC genes usually encode only one or a few distinct proteins, RC H2A and H2B genes often encode several different proteins. In Arabidopsis, ten H2Bs differ mostly in the lysine-rich N-terminal tails and in tissue-specific expression. Although most appear to be RC H2Bs, H2B.3 is enriched in mature leaves and in nucleosomes containing H3.3 and/or H2A.Z, consistent with it being a RI variant, and H2B.8 is enriched in dry seed (see poster). A similar heterogeneity of RC H2B and H2A proteins is found in humans, mice and sea urchins. In mice, the mRNA for H2B.21 (H2B.E), which differs in five amino acids from the H2B consensus, is transcribed from the HIST2 gene cluster of RC histones but has a polyA tail, typical of RI variants, and is expressed exclusively in the main olfactory epithelium and the vomeronasal organ. A model of H2B.21 function proposes that increased neuronal activity due to exposure to olfactory stimulants reduces H2B.21 in the corresponding olfactory receptor cells and increases neuronal longevity, whereas stimulant deprivation leads to increased H2B.21 levels and shorter neuronal life span. Other H2B variants are mainly restricted to roles in spermatogenesis (Table 1).

H2A variants

H2A variants occupy the entry and exit positions along the wrap of nucleosomal DNA, making them ideal components to control access to the DNA. Bulk RC H2As in humans differ mostly at their C-termini. The mammalian RI variant H2A.22 (H2A.J) differs from bulk H2As because of an A11V change in the N-terminus and by several residues at its C-terminus, including a potential SQ phosphorylation site, and promotes senescence-associated inflammatory gene expression in cells with persistent DNA damage. Other RI variants also differ at their C-termini, which can alter the extent of DNA wrapping (see poster). They may also differ at the acidic patch, which interacts with chromatin remodelers, and in loop 1, where the two copies of H2A in a nucleosome contact each other to stabilize nucleosomes.

H2A.X – DNA damage and beyond

H2A.X differs from bulk H2As in possessing a C-terminal SQD/EΦ phosphorylation motif (where Φ indicates a hydrophobic residue, often phenylalanine or tyrosine). In response to DNA damage, the serine (S139 in humans) becomes phosphorylated (then known as γH2A.X) and recruits repair enzymes to double-strand breaks (reviewed in ). In single-celled eukaryotes, such as yeast, H2A.X can be the primary form of H2A, whereas in multicellular eukaryotes H2A.X is usually closely related to RC H2As in the same group of multicellular organisms. Because of its conserved function in the DNA damage response, it seems probable that H2A.X is ancestral, and that the various RC H2As are derived from it. In humans, H2A.X differs from other H2A variants in producing mRNAs with either a stem-loop structure typical of RC H2As or a polyadenylated transcript like RI variants. The stem-loop structure may be relevant to deposition of H2A.X during UVC-induced DNA damage repair, where it may serve to augment the amount of H2A.X available to be phosphorylated. Sites prone to DNA damage in cycling cells become enriched with H2A.X, whereas resting cells do not show such enrichment. γH2A.X stimulates the polymerase activity of poly-ADP-ribose polymerase 1 (PARP1), which detects double-strand breaks and recruits additional repair factors.

The functions of H2A.X are not limited to DNA repair. In mouse embryonic stem cells, H2A.X is deposited at rDNA promoters and recruits the nucleolar remodeling complex to repress rDNA transcription and limit cell proliferation, independently of S139 phosphorylation. In Xenopus, a variant of H2A.X (H2A.X-F) is abundant and is phosphorylated in oocytes, eggs and early embryos in the absence of DNA damage, suggesting it has a role in promoting the rapid early divisions or in activating the zygotic genome. H2A.X-knockout mice are viable but show repair defects and genomic instability, and males are infertile, presumably because the X and Y chromosomes in spermatocytes fail to form the sex body (see Glossary) or initiate meiotic sex chromosome inactivation.

H2A.Z – a transcriptional regulator

The RI variant H2A.Z has a prominent and complex role in transcriptional regulation (reviewed in ). It is absent from the early-diverging metamonads Giardia and Trichomonas, but is strongly conserved in nearly all other eukaryotes, where it commonly occurs in the +1 nucleosome position (see Glossary) of genes and appears to poise genes for transcription and promote RNA polymerase II (RNAPII) recruitment. H2A.Z has an extended acidic patch that stimulates ATP-dependent remodelers. The yeast SWR1 complex replaces H2A–H2B dimers with H2A.Z–H2B dimers in the +1 nucleosome of transcribed genes and even in transcribed upstream antisense noncoding RNAs. In vitro, H2A.Z nucleosomes have a lower breaking force in an optical tweezer assay than bulk H2A nucleosomes. This may underlie the ability of H2A.Z to lower the barrier to transcription of the +1 nucleosome in Drosophila cells, which occurs through the loss of an H2A.Z–H2B dimer and its DNA contacts, as well as its lower thermal stability. This presumably facilitates the eviction of H2A.Z without loss of H3 in the thermal response of Arabidopsis. In yeast, eviction of H2A.Z is dependent on the transcription pre-initiation complex and serine-5-phophorylated RNAPII. Apparently contradictory effects of H2A.Z on gene activation or silencing in different contexts are mediated at least in part by acetylation of the N-terminus or monoubiquitylation of the C-terminus, respectively. H2A.Z is also enriched at enhancers, where it is necessary for recruitment of RNAPII and cohesins (see Glossary), which mediate enhancer–promoter interaction, and for the transcription of enhancer RNAs.

Chordates encode two H2A.Z proteins, H2A.Z.1 and H2A.Z.2, which differ by three conserved amino acids (reviewed in ). H2A.Z.1-knockout animals die during early development and H2A.Z.2 is required for melanocyte development in zebrafish. In humans, H2A.Z.1 and H2A.Z.2 have qualitatively similar, but quantitatively different, expression patterns, with a subset of H2A.Z.2-biased enhancers affecting genes that are downregulated in the cranio-facial abnormality disease floating harbor syndrome. In primates, H2A.Z.2 has two splice variants, H2A.Z.2.1 and H2A.Z.2.2. H2A.Z.2.2 destabilizes nucleosomes due to its shorter C-terminus, which resembles short H2As in length (Table 1). Despite the requirements for H2A.Z.1 in embryonic development, and the role of H2A.Z.2 in melanocyte development and cranio-facial formation, a double knockout of these two genes in mouse skeletal muscle has little effect on either basal or induced transcription, calling into question whether H2A.Z plays any necessary part in transcription or simply has a replacement function. The strong conservation of H2A.Z at transcription start sites across diverse eukaryotic kingdoms is hard to rationalize if it has no role in transcription, since other replacement H2As, such as H2A.X are readily available, in most cases. However, if the role of H2A.Z is to help attract RNAPII or reduce the barrier of the +1 nucleosome, there are likely redundant pathways and cofactors for accomplishing this.

H2A.W and macroH2A

Arabidopsis thaliana has four H2A variants – bulk H2A, H2A.X, H2A.Z and the plant-specific H2A.W – all of which form homotypic nucleosomes. With its extended C-terminus (which has a putative minor groove-binding motif KSPKK), H2A.W protects an additional 10–15 bp of linker DNA beyond the 147 bp of most nucleosomes from micrococcal nuclease. H2A.W is found in heterochromatin, where it may serve a silencing function. Like H2A.X, it can be phosphorylated during the DNA damage response. Extended C-terminal tails are also found in H2As of bdelloid rotifers, freshwater microorganisms, which replace conventional H2A, H2A.X and H2A.Z, and are speculated to help protect against DNA damage from desiccation. In animals, the macroH2A variant acts like H2A.W in protecting 10 bp of extranucleosomal DNA and is distinguished from other H2As in that the HFD is connected to a separate macrodomain by a basic protein linker region. Heterotypic macroH2A–H2A nucleosomes form a more stable octamer, and the linker region facilitates condensation. MacroH2A nucleosomes have reduced recruitment of chromatin remodelers, inhibit acetylation by p300 (also known as EP300) and present a barrier to reprogramming cells by stabilizing both active and inactive gene expression patterns.

In contrast to H2A.W and macroH2A, four families of short H2As (H2A.B, H2A.L, H2A.P and H2A.Q), which wrap only 110–130 bp of DNA and have shortened docking domains, reduced DNA-binding capability and smaller acidic patches, are encoded on the X chromosome of placental mammals. All these families have stage-specific expression in testes, where they have roles in splicing and the transition to protamines, and are evolving rapidly (Table 1).

H1 variants

Linker histone H1 lacks a HFD and has a different origin than the other histones. It is absent in the early-diverging metamonads and it is unclear whether it was present in the last eukaryotic common ancestor. In multicellular eukaryotes, H1s have a tripartite structure in which a globular domain with a winged helix motif separates basic N-terminal and C-terminal domains that are variable. The lysine-rich C-terminus, which often contains S/TPKK minor groove-binding motifs, is similar to lysine-rich DNA-binding proteins in bacteria and is necessary for chromatin compaction. The winged helix, which binds at the nucleosome dyad and interacts with the entry and exit linker DNAs (see poster), was either independently acquired in plants, mycetozoans and opisthokonts (animals, fungi and near relatives), or independently lost in kinetoplastids, alveolates and Entamoeba.

Humans and other mammals have 11 H1 paralogs (seven somatic paralogs and four germline paralogs). The genes encoding the somatic paralogs H1.1–H1.5 and the ‘testis-specific’ variant H1.6 (H1t) are part of the histone gene cluster on chromosome VI, whereas RI variants H1.0 and H1.7–H1.10 (H1T2, H1oo, HILS1 and H1X) are encoded elsewhere. In ChIP-seq experiments of endogenous or HA-tagged H1.0, H1.2–H1.5 and H1.10 in a breast cancer cell line, H1s are broadly found on genes, repeats and upstream promoters, but are depleted at transcription start sites. In human lung fibroblasts, H1.5 is enriched over splice sites of exons shorter than the length of a nucleosome and promotes their inclusion, apparently by stalling RNAPII. In mouse embryonic stem cells, H1.2 and H1.3 (H1c and H1d) are enriched in heterochromatic domains marked with H3K9me3, and in vitro H1.0–H1.5 interact directly with H3K9 methyltransferases through their C-termini and promote H3K9 methylation (see poster). Knockout of individual H1s generally has little effect on mouse development, but triple knockout of H1.2, H1.3 and H1.4 (H1e) results in embryonic lethality. In an embryonic cell line derived from the triple knockout, with only 20% of global H1 expression, strong de-repression of transcription of the major satellite and other repeat classes occurs together with loss of H3K9me3 on the affected sequences. Although H1 variants have at least partially redundant functions, they show different effects on nucleosome spacing when introduced to H1-free Xenopus oocytes, with H1.2 and H1.3 increasing nucleosome repeat length by only 5–7 bp, whereas H1.4 and H1.0 from Xenopus and chicken (H5) increase nucleosome repeat length by 13–20 bp. Short repeat length results in greater compaction and silencing.

The somatic RI variants H1.0 and H1.10 are enriched at nucleolus-associated domains and at RNAPII-enriched domains, respectively. H1.0 is conserved in vertebrates and invertebrates, and is found primarily in differentiated tissues. H1.0-binding sites positively correlate with the presence of H3K27me3 (a mediator of developmental silencing), high nucleosome density and GC-rich genes in fibroblasts, and are at low density in AT-rich regions. H1.0 is often heterogeneously expressed in tumor cells, with H1.0 levels correlating with tumor cell differentiation and patient survival, whereas silencing of H1.0 favors self-renewing cells. Similarly, lower levels of H1.10 are an adverse prognosticator for astrocytic gliomas.

Perspective

From an ancestral set of five proteins, four of which are among the most conserved proteins known, histone variants continue to diversify and innovate to respond to the necessity of regulating access to DNA in all the contexts in which organisms find themselves. Histone variants greatly expand the roles and dynamics of nucleosomes by wrapping more or less DNA, by having greater or lesser stability, by having unique post-translational modifications or by interacting with other chromatin components. Although ancient variants, such as H2A.Z and H3.3, are well-studied, they continue to raise questions – are their effects on transcription and silencing cellular adaptations to their chromatin maintenance functions in non-dividing cells, when RC histones are unavailable? Similar questions arise in considering the DNA repair-independent functions of H2A.X. More recently evolved variants raise additional questions, such as what is the role of the enigmatic macroH2A domain, the only globular domain fused to a histone, and which is unique to animals. Especially intriguing are the sperm-specific variants in every histone class, which are collectively involved in the process of packaging the genome into protamines, but their individual roles are only starting to become clear. Other challenges include understanding how dysregulation or mutation of histone variants and their chaperones promote tumorigenesis. New profiling and gene editing techniques promise to address these challenges.

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    Aul, R. B. and Oko, R. J. (2002 ). The major subacrosomal occupant of bull spermatozoa is a novel histone H2B variant associated with the forming acrosome during spermiogenesis. Dev. Biol. 242, 376-387.

    Not in our library10.1006/dbio.2002.0575

  9. 9.

    Bagchi, D. N., Battenhouse, A. M., Park, D. and Iyer, V. R. (2020 ). The histone variant H2A.Z in yeast is almost exclusively incorporated into the +1 nucleosome in the direction of transcription. Nucleic Acids Res. 48, 157-170.

    Not in our library10.1093/nar/gkz1075

  10. 10.

    Bao, Y., Konesky, K., Park, Y. J., Rosu, S., Dyer, P. N., Rangasamy, D., Tremethick, D. J., Laybourn, P. J. and Luger, K. (2004 ). Nucleosomes containing the histone variant H2A.Bbd organize only 118 base pairs of DNA. EMBO J. 23, 3314-3324.

    Not in our library10.1038/sj.emboj.7600316

  11. 11.

    Barral, S., Morozumi, Y., Tanaka, H., Montellier, E., Govin, J., de Dieuleveult, M., Charbonnier, G., Coute, Y., Puthier, D., Buchou, T. et al. (2017 ). Histone variant H2A.L.2 guides transition protein-dependent protamine assembly in male germ cells. Mol. Cell 66, 89-101.e8.

    Not in our library10.1016/j.molcel.2017.02.025

  12. 12.

    Bednar, J., Garcia-Saez, I., Boopathi, R., Cutter, A. R., Papai, G., Reymer, A., Syed, S. H., Lone, I. N., Tonchev, O., Crucifix, C. et al. (2017 ). Structure and dynamics of a 197 bp nucleosome in complex with linker histone H1. Mol. Cell 66, 384-397.e8.

    Not in our library10.1016/j.molcel.2017.04.012

  13. 13.

    Beedle, M.-T., Topping, T., Hogarth, C. and Griswold, M. (2019 ). Differential localization of histone variant TH2B during the first round compared with subsequent rounds of spermatogenesis. Dev. Dyn. 248, 488-500.

    Not in our library10.1002/dvdy.33

  14. 14.

    Belotti, E., Lacoste, N., Simonet, T., Papin, C., Padmanabhan, K., Scionti, I., Gangloff, Y. G., Ramos, L., Dalkara, D., Hamiche, A. et al. (2020 ). H2A.Z is dispensable for both basal and activated transcription in post-mitotic mouse muscles. Nucleic Acids Res. 48, 4601-4613.

    Not in our library10.1093/nar/gkaa157

  15. 15.

    Bennett, R. L., Bele, A., Small, E. C., Will, C. M., Nabet, B., Oyer, J. A., Huang, X., Ghosh, R. P., Grzybowski, A. T., Yu, T. et al. (2019 ). A mutation in histone H2B represents a new class of oncogenic driver. Cancer Discov. 9, 1438-1451.

    Not in our library10.1158/2159-8290.cd-19-0393

  16. 16.

    Bergmuller, E., Gehrig, P. M. and Gruissem, W. (2007 ). Characterization of post-translational modifications of histone H2B-variants isolated from Arabidopsis thaliana. J. Proteome Res. 6, 3655-3668.

    Not in our library10.1021/pr0702159

  17. 17.

    Bonisch, C., Schneider, K., Pünzeler, S., Wiedemann, S. M., Bielmeier, C., Bocola, M., Eberl, H. C., Kuegel, W., Neumann, J., Kremmer, E. et al. (2012 ). H2A.Z.2.2 is an alternatively spliced histone H2A.Z variant that causes severe nucleosome destabilization. Nucleic Acids Res. 40, 5951-5964.

    Not in our library10.1093/nar/gks267

  18. 18.

    Borg, M., Jacob, Y., Susaki, D., LeBlanc, C., Buendía, D., Axelsson, E., Kawashima, T., Voigt, P., Boavida, L., Becker, J. et al. (2020 ). Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin. Nat. Cell Biol. 22, 621-629.

    Not in our library10.1038/s41556-020-0515-y

  19. 19.

    Boulard, M., Gautier, T., Mbele, G. O., Gerson, V., Hamiche, A., Angelov, D., Bouvet, P. and Dimitrov, S. (2006 ). The NH2 tail of the novel histone variant H2BFWT exhibits properties distinct from conventional H2B with respect to the assembly of mitotic chromosomes. Mol. Cell. Biol. 26, 1518-1526.

    Not in our library10.1128/mcb.26.4.1518-1526.2006

  20. 20.

    Bowerman, S., Hickok, R. J. and Wereszczynski, J. (2019 ). Unique dynamics in asymmetric macroH2A-H2A hybrid nucleosomes result in increased complex stability. J. Phys. Chem. B 123, 419-427.

    Not in our library10.1021/acs.jpcb.8b10668

  21. 21.

    Brunelle, M., Nordell Markovits, A., Rodrigue, S., Lupien, M., Jacques, P.-E. and Gévry, N. (2015 ). The histone variant H2A.Z is an important regulator of enhancer activity. Nucleic Acids Res. 43, 9742-9756.

    Not in our library10.1093/nar/gkv825

  22. 22.

    Camahort, R., Li, B., Florens, L., Swanson, S. K., Washburn, M. P. and Gerton, J. L. (2007 ). Scm3 is essential to recruit the histone h3 variant cse4 to centromeres and to maintain a functional kinetochore. Mol. Cell 26, 853-865.

    Not in our library10.1016/j.molcel.2007.05.013

  23. 23.

    Celeste, A., Petersen, S., Romanienko, P. J., Fernandez-Capetillo, O., Chen, H. T., Sedelnikova, O. A., Reina-San-Martin, B., Coppola, V., Meffre, E., Difilippantonio, M. J. et al. (2002 ). Genomic instability in mice lacking histone H2AX. Science 296, 922-927.

    Not in our library10.1126/science.1069398

  24. 24.

    Chakravarthy, S., Patel, A. and Bowman, G. D. (2012 ). The basic linker of macroH2A stabilizes DNA at the entry/exit site of the nucleosome. Nucleic Acids Res. 40, 8285-8295.

    Not in our library10.1093/nar/gks645

  25. 25.

    Chang, E. Y., Ferreira, H., Somers, J., Nusinow, D. A., Owen-Hughes, T. and Narlikar, G. J. (2008 ). MacroH2A allows ATP-dependent chromatin remodeling by SWI/SNF and ACF complexes but specifically reduces recruitment of SWI/SNF. Biochemistry 47, 13726-13732.

    Not in our library10.1021/bi8016944

  26. 26.

    Chang, F. T. M., Chan, F. L., McGhie, J. D. R., Udugama, M., Mayne, L., Collas, P., Mann, J. R. and Wong, L. H. (2015 ). CHK1-driven histone H3.3 serine 31 phosphorylation is important for chromatin maintenance and cell survival in human ALT cancer cells. Nucleic Acids Res. 43, 2603-2614.

    Not in our library10.1093/nar/gkv104

  27. 27.

    Cheema, M. S., Good, K. V., Kim, B., Soufari, H., O'Sullivan, C., Freeman, M. E., Stefanelli, G., Casas, C. R., Zengeler, K. E., Kennedy, A. J. et al. (2020 ). Deciphering the enigma of the histone H2A.Z-1/H2A.Z-2 isoforms: novel insights and remaining questions. Cells 9, 1167.

    Not in our library10.3390/cells9051167

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    Chen, C. C., Dechassa, M. L., Bettini, E., Ledoux, M. B., Belisario, C., Heun, P., Luger, K. and Mellone, B. G. (2014 ). CAL1 is the Drosophila CENP-A assembly factor. J. Cell Biol. 204, 313-329.

    Not in our library10.1083/jcb.201305036

  29. 29.

    Churikov, D., Siino, J., Svetlova, M., Zhang, K., Gineitis, A., Morton Bradbury, E. and Zalensky, A. (2004 ). Novel human testis-specific histone H2B encoded by the interrupted gene on the X chromosome. Genomics 84, 745-756.

    Not in our library10.1016/j.ygeno.2004.06.001

  30. 30.
    Histone variant H2A.J accumulates in senescent cells and promotes inflammatory gene expression · 2017
    No notice
  31. 31.

    Cortijo, S., Charoensawan, V., Brestovitsky, A., Buning, R., Ravarani, C., Rhodes, D., van Noort, J., Jaeger, K. E. and Wigge, P. A. (2017 ). Transcriptional regulation of the ambient temperature response by H2A.Z nucleosomes and HSF1 transcription factors in arabidopsis. Mol. Plant 10, 1258-1273.

    Not in our library10.1016/j.molp.2017.08.014

  32. 32.

    Dai, L., Xie, X. and Zhou, Z. (2018 ). Crystal structure of the histone heterodimer containing histone variant H2A.Bbd. Biochem. Biophys. Res. Commun. 503, 1786-1791.

    Not in our library10.1016/j.bbrc.2018.07.114

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    Dalmasso, M. C., Sullivan, W. J., Jr. and Angel, S. O. (2011 ). Canonical and variant histones of protozoan parasites. Front. Biosci. 16, 2086-2105.

    Not in our library10.2741/3841

  34. 34.

    Dann, G. P., Liszczak, G. P., Bagert, J. D., Muller, M. M., Nguyen, U. T. T., Wojcik, F., Brown, Z. Z., Bos, J., Panchenko, T., Pihl, R. et al. (2017 ). ISWI chromatin remodellers sense nucleosome modifications to determine substrate preference. Nature 548, 607-611.

    Not in our library10.1038/nature23671

  35. 35.

    Dawe, R. K. and Henikoff, S. (2006 ). Centromeres put epigenetics in the driver's seat. Trends Biochem. Sci. 31, 662-669.

    Not in our library10.1016/j.tibs.2006.10.004

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    Delaney, K., Mailler, J., Wenda, J. M., Gabus, C. and Steiner, F. A. (2018 ). Differential expression of histone H3.3 genes and their role in modulating temperature stress response in Caenorhabditis elegans. Genetics 209, 551-565.

    Not in our library10.1534/genetics.118.300909

  37. 37.

    Doyen, C. M., An, W., Angelov, D., Bondarenko, V., Mietton, F., Studitsky, V. M., Hamiche, A., Roeder, R. G., Bouvet, P. and Dimitrov, S. (2006a ). Mechanism of polymerase II transcription repression by the histone variant macroH2A. Mol. Cell. Biol. 26, 1156-1164.

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  38. 38.

    Doyen, C.-M., Montel, F., Gautier, T., Menoni, H., Claudet, C., Delacour-Larose, M., Angelov, D., Hamiche, A., Bednar, J., Faivre-Moskalenko, C. et al. (2006b ). Dissection of the unusual structural and functional properties of the variant H2A.Bbd nucleosome. EMBO J. 25, 4234-4244.

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  39. 39.

    Drane, P., Ouararhni, K., Depaux, A., Shuaib, M. and Hamiche, A. (2010 ). The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev. 24, 1253-1265.

    Not in our library10.1101/gad.566910

  40. 40.
    Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects · 2014
    No notice
  41. 41.

    Dunleavy, E. M., Roche, D., Tagami, H., Lacoste, N., Ray-Gallet, D., Nakamura, Y., Daigo, Y., Nakatani, Y. and Almouzni-Pettinotti, G. (2009 ). HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137, 485-497.

    Not in our library10.1016/j.cell.2009.02.040

  42. 42.

    Eirín-López, J. M., González-Romero, R., Dryhurst, D., Ishibashi, T. and Ausió, J. (2009 ). The evolutionary differentiation of two histone H2A.Z variants in chordates (H2A.Z-1 and H2A.Z-2) is mediated by a stepwise mutation process that affects three amino acid residues. BMC Evol. Biol. 9, 31.

    Not in our library10.1186/1471-2148-9-31

  43. 43.
    NoRC Recruitment by H2A.X Deposition at rRNA Gene Promoter Limits Embryonic Stem Cell Proliferation · 2018
    Not checked
  44. 44.

    Elsässer, S. J., Huang, H., Lewis, P. W., Chin, J. W., Allis, C. D. and Patel, D. J. (2012 ). DAXX envelops a histone H3.3-H4 dimer for H3.3-specific recognition. Nature 491, 560-565.

    Not in our library10.1038/nature11608

  45. 45.

    Elsässer, S. J., Noh, K. M., Diaz, N., Allis, C. D. and Banaszynski, L. A. (2015 ). Histone H3.3 is required for endogenous retroviral element silencing in embryonic stem cells. Nature 522, 240-244.

    Not in our library10.1038/nature14345

  46. 46.
    Phylogenetic analysis of the core histone doublet and DNA topo II genes of Marseilleviridae: evidence of proto-eukaryotic provenance · 2017
    Not checked
  47. 47.

    Faast, R., Thonglairoam, V., Schulz, T. C., Beall, J., Wells, J. R., Taylor, H., Matthaei, K., Rathjen, P. D., Tremethick, D. J. and Lyons, I. (2001 ). Histone variant H2A.Z is required for early mammalian development. Curr. Biol. 11, 1183-1187.

    Not in our library10.1016/s0960-9822(01)00329-3

  48. 48.

    Fan, Y., Nikitina, T., Morin-Kensicki, E. M., Zhao, J., Magnuson, T. R., Woodcock, C. L. and Skoultchi, A. I. (2003 ). H1 linker histones are essential for mouse development and affect nucleosome spacing in vivo. Mol. Cell. Biol. 23, 4559-4572.

    Not in our library10.1128/mcb.23.13.4559-4572.2003

  49. 49.

    Fernandez-Capetillo, O., Mahadevaiah, S. K., Celeste, A., Romanienko, P. J., Camerini-Otero, R. D., Bonner, W. M., Manova, K., Burgoyne, P. and Nussenzweig, A. (2003 ). H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev. Cell 4, 497-508.

    Not in our library10.1016/s1534-5807(03)00093-5

  50. 50.
    The histone variant H2A.Z in gene regulation · 2019
    No notice
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    Gineitis, A. A., Zalenskaya, I. A., Yau, P. M., Bradbury, E. M. and Zalensky, A. O. (2000 ). Human sperm telomere-binding complex involves histone H2B and secures telomere membrane attachment. J. Cell Biol. 151, 1591-1598.

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    Glaich, O., Leader, Y., Lev Maor, G. and Ast, G. (2019 ). Histone H1.5 binds over splice sites in chromatin and regulates alternative splicing. Nucleic Acids Res. 47, 6145-6159.

    Not in our library10.1093/nar/gkz338

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    Goldberg, A. D., Banaszynski, L. A., Noh, K. M., Lewis, P. W., Elsaesser, S. J., Stadler, S., Dewell, S., Law, M., Guo, X., Li, X. et al. (2010 ). Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140, 678-691.

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  54. 54.

    Goldman, J. A., Garlick, J. D. and Kingston, R. E. (2010 ). Chromatin remodeling by imitation switch (ISWI) class ATP-dependent remodelers is stimulated by histone variant H2A.Z. J. Biol. Chem. 285, 4645-4651.

    Not in our library10.1074/jbc.m109.072348

  55. 55.

    González-Romero, R., Ausió, J., Mendez, J. and Eirín-López, J. M. (2009 ). Histone genes of the razor clam Solen marginatus unveil new aspects of linker histone evolution in protostomes. Genome/National Research Council Canada=Genome/Conseil national de recherches Canada 52, 597-607.

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    Greenberg, R. S., Long, H. K., Swigut, T. and Wysocka, J. (2019 ). Single amino acid change underlies distinct Roles of H2A.Z subtypes in human syndrome. Cell 178, 1421-1436.e24.

    Not in our library10.1016/j.cell.2019.08.002

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    Hake, S. B., Garcia, B. A., Kauer, M., Baker, S. P., Shabanowitz, J., Hunt, D. F. and Allis, C. D. (2005 ). Serine 31 phosphorylation of histone variant H3.3 is specific to regions bordering centromeres in metaphase chromosomes. Proc. Natl. Acad. Sci. USA 102, 6344-6349.

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  58. 58.

    Healton, S. E., Pinto, H. D., Mishra, L. N., Hamilton, G. A., Wheat, J. C., Swist-Rosowska, K., Shukeir, N., Dou, Y., Steidl, U., Jenuwein, T. et al. (2020 ). H1 linker histones silence repetitive elements by promoting both histone H3K9 methylation and chromatin compaction. Proc. Natl. Acad. Sci. USA 117, 14251-14258.

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    Henikoff, S., Ahmad, K. and Malik, H. S. (2001 ). The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293, 1098-1102.

    Not in our library10.1126/science.1062939

  60. 60.
    Structure and function of archaeal histones. · 2018
    Not checked
  61. 61.

    Ingouff, M., Hamamura, Y., Gourgues, M., Higashiyama, T. and Berger, F. (2007 ). Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr. Biol. 17, 1032-1037.

    Not in our library10.1016/j.cub.2007.05.019

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    Jacob, Y., Bergamin, E., Donoghue, M. T., Mongeon, V., LeBlanc, C., Voigt, P., Underwood, C. J., Brunzelle, J. S., Michaels, S. D., Reinberg, D. et al. (2014 ). Selective methylation of histone H3 variant H3.1 regulates heterochromatin replication. Science 343, 1249-1253.

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    Jang, C. W., Shibata, Y., Starmer, J., Yee, D. and Magnuson, T. (2015 ). Histone H3.3 maintains genome integrity during mammalian development. Genes Dev. 29, 1377-1392.

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    Jiang, D., Borg, M., Lorković, Z. J., Montgomery, S. A., Osakabe, A., Yelagandula, R., Axelsson, E. and Berger, F. (2020 ). The evolution and functional divergence of the histone H2B family in plants. PLoS Genet. 16, e1008964.

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    Kasinsky, H. E., Lewis, J. D., Dacks, J. B. and Ausió, J. (2001 ). Origin of H1 linker histones. FASEB J. 15, 34-42.

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    Kornberg, R. D. and Lorch, Y. (2020 ). Primary role of the nucleosome. Mol. Cell 79, 371-375.

    Not in our library10.1016/j.molcel.2020.07.020

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    Kujirai, T., Horikoshi, N., Sato, K., Maehara, K., Machida, S., Osakabe, A., Kimura, H., Ohkawa, Y. and Kurumizaka, H. (2016 ). Structure and function of human histone H3.Y nucleosome. Nucleic Acids Res. 44, 6127-6141.

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    Kursel, L. E. and Malik, H. S. (2018 ). The cellular mechanisms and consequences of centromere drive. Curr. Opin. Cell Biol. 52, 58-65.

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    Li, M., Dong, Q. and Zhu, B. (2017 ). Aurora kinase B phosphorylates histone H3.3 at Serine 31 during mitosis in mammalian cells. J. Mol. Biol. 429, 2042-2045.

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  70. 70.

    Long, M., Sun, X., Shi, W., Yanru, A., Leung, S. T. C., Ding, D., Cheema, M. S., MacPherson, N., Nelson, C. J., Ausio, J. et al. (2019 ). A novel histone H4 variant H4G regulates rDNA transcription in breast cancer. Nucleic Acids Res. 47, 8399-8409.

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  71. 71.

    Lorković, Z. J., Park, C., Goiser, M., Jiang, D., Kurzbauer, M. T., Schlögelhofer, P. and Berger, F. (2017 ). Compartmentalization of DNA damage response between heterochromatin and euchromatin is mediated by distinct H2A histone variants. Curr. Biol. 27, 1192-1199.

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  72. 72.

    Lowe, B. R., Maxham, L. A., Hamey, J. J., Wilkins, M. R. and Partridge, J. F. (2019 ). Histone H3 mutations: an updated view of their role in chromatin deregulation and cancer. Cancers (Basel) 11, 660.

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    Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F. and Richmond, T. J. (1997 ). Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 251-260.

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    Lyons, S. M., Cunningham, C. H., Welch, J. D., Groh, B., Guo, A. Y., Wei, B., Whitfield, M. L., Xiong, Y. and Marzluff, W. F. (2016 ). A subset of replication-dependent histone mRNAs are expressed as polyadenylated RNAs in terminally differentiated tissues. Nucleic Acids Res. 44, 9190-9205.

    Not in our library10.1093/nar/gkw620

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    Maehara, K., Harada, A., Sato, Y., Matsumoto, M., Nakayama, K. I., Kimura, H. and Ohkawa, Y. (2015 ). Tissue-specific expression of histone H3 variants diversified after species separation. Epigenet. Chromatin 8, 35.

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  76. 76.

    Mahadevan, I. A., Kumar, S. and Rao, M. R. S. (2020 ). Linker histone variant H1t is closely associated with repressed repeat-element chromatin domains in pachytene spermatocytes. Epigenet. Chromatin 13, 9.

    Not in our library10.1186/s13072-020-00335-x

  77. 77.

    Mannironi, C., Bonner, W. M. and Hatch, C. L. (1989 ). H2A.X. a histone isoprotein with a conserved C-terminal sequence, is encoded by a novel mRNA with both DNA replication type and polyA 3′ processing signals. Nucleic Acids Res. 17, 9113-9126.

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    Martianov, I., Brancorsini, S., Catena, R., Gansmuller, A., Kotaja, N., Parvinen, M., Sassone-Corsi, P. and Davidson, I. (2005 ). Polar nuclear localization of H1T2, a histone H1 variant, required for spermatid elongation and DNA condensation during spermiogenesis. Proc. Natl. Acad. Sci. USA 102, 2808-2813.

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    Martire, S., Gogate, A. A., Whitmill, A., Tafessu, A., Nguyen, J., Teng, Y. C., Tastemel, M. and Banaszynski, L. A. (2019 ). Phosphorylation of histone H3.3 at serine 31 promotes p300 activity and enhancer acetylation. Nat. Genet. 51, 941-946.

    Not in our library10.1038/s41588-019-0428-5

  80. 80.

    Marzluff, W. F. (2005 ). Metazoan replication-dependent histone mRNAs: a distinct set of RNA polymerase II transcripts. Curr. Opin. Cell Biol. 17, 274-280.

    Not in our library10.1016/j.ceb.2005.04.010

  81. 81.

    Marzluff, W. F., Gongidi, P., Woods, K. R., Jin, J. and Maltais, L. J. (2002 ). The human and mouse replication-dependent histone genes. Genomics 80, 487-498.

    Not in our library10.1006/geno.2002.6850

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    Marzluff, W. F., Sakallah, S. and Kelkar, H. (2006 ). The sea urchin histone gene complement. Dev. Biol. 300, 308-320.

    Not in our library10.1016/j.ydbio.2006.08.067

  83. 83.

    Mattiroli, F., Bhattacharyya, S., Dyer, P. N., White, A. E., Sandman, K., Burkhart, B. W., Byrne, K. R., Lee, T., Ahn, N. G., Santangelo, T. J. et al. (2017 ). Structure of histone-based chromatin in Archaea. Science 357, 609-612.

    Not in our library10.1126/science.aaj1849

  84. 84.

    Mayor, R., Izquierdo-Bouldstridge, A., Millán-Ariño, L., Bustillos, A., Sampaio, C., Luque, N. and Jordan, A. (2015 ). Genome distribution of replication-independent histone H1 variants shows H1.0 associated with nucleolar domains and H1X associated with RNA polymerase II-enriched regions. J. Biol. Chem. 290, 7474-7491.

    Not in our library10.1074/jbc.m114.617324

  85. 85.

    Millán-Ariño, L., Islam, A. B., Izquierdo-Bouldstridge, A., Mayor, R., Terme, J. M., Luque, N., Sancho, M., López-Bigas, N. and Jordan, A. (2014 ). Mapping of six somatic linker histone H1 variants in human breast cancer cells uncovers specific features of H1.2. Nucleic Acids Res. 42, 4474-4493.

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    Mishra, L. N., Gupta, N. and Rao, S. M. (2015 ). Mapping of post-translational modifications of spermatid-specific linker histone H1-like protein, HILS1. J. Proteomics 128, 218-230.

    Not in our library10.1016/j.jprot.2015.08.001

  87. 87.

    Mito, Y., Henikoff, J. G. and Henikoff, S. (2005 ). Genome-scale profiling of histone H3.3 replacement patterns. Nat. Genet. 37, 1090-1097.

    Not in our library10.1038/ng1637

  88. 88.

    Mito, Y., Henikoff, J. G. and Henikoff, S. (2007 ). Histone replacement marks the boundaries of cis-regulatory domains. Science 315, 1408-1411.

    Not in our library10.1126/science.1134004

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    Mizuguchi, G., Xiao, H., Wisniewski, J., Smith, M. M. and Wu, C. (2007 ). Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes. Cell 129, 1153-1164.

    Not in our library10.1016/j.cell.2007.04.026

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    Molaro, A., Young, J. M. and Malik, H. S. (2018 ). Evolutionary origins and diversification of testis-specific short histone H2A variants in mammals. Genome Res. 28, 460-473.

    Not in our library10.1101/gr.229799.117

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    Montellier, E., Boussouar, F., Rousseaux, S., Zhang, K., Buchou, T., Fenaille, F., Shiota, H., Debernardi, A., Hery, P., Curtet, S. et al. (2013 ). Chromatin-to-nucleoprotamine transition is controlled by the histone H2B variant TH2B. Genes Dev. 27, 1680-1692.

    Not in our library10.1101/gad.220095.113

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    Moosmann, A., Campsteijn, C., Jansen, P. W., Nasrallah, C., Raasholm, M., Stunnenberg, H. G. and Thompson, E. M. (2011 ). Histone variant innovation in a rapidly evolving chordate lineage. BMC Evol. Biol. 11, 208-2148-11-208.

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    Muthurajan, U. M., McBryant, S. J., Lu, X., Hansen, J. C. and Luger, K. (2011 ). The linker region of macroH2A promotes self-association of nucleosomal arrays. J. Biol. Chem. 286, 23852-23864.

    Not in our library10.1074/jbc.m111.244871

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    Nacev, B. A., Feng, L., Bagert, J. D., Lemiesz, A. E., Gao, J., Soshnev, A. A., Kundra, R., Schultz, N., Muir, T. W. and Allis, C. D. (2019 ). The expanding landscape of ‘oncohistone’ mutations in human cancers. Nature 567, 473-478.

    Not in our library10.1038/s41586-019-1038-1

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    Navarro-Mendoza, M. I., Pérez-Arques, C., Panchal, S., Nicolás, F. E., Mondo, S. J., Ganguly, P., Pangilinan, J., Grigoriev, I. V., Heitman, J., Sanyal, K. et al. (2019 ). Early diverging fungus Mucor circinelloides lacks centromeric histone CENP-A and displays a mosaic of point and regional centromeres. Curr. Biol. 29, 3791-3802.e6.

    Not in our library10.1016/j.cub.2019.09.024

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    Öberg, C., Izzo, A., Schneider, R., Wrange, Ö. and Belikov, S. (2012 ). Linker histone subtypes differ in their effect on nucleosomal spacing in vivo. J. Mol. Biol. 419, 183-197.

    Not in our library10.1016/j.jmb.2012.03.007

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    Osakabe, A., Lorković, Z. J., Kobayashi, W., Tachiwana, H., Yelagandula, R., Kurumizaka, H. and Berger, F. (2018 ). Histone H2A variants confer specific properties to nucleosomes and impact on chromatin accessibility. Nucleic Acids Res. 46, 7675-7685.

    Not in our library10.1093/nar/gky540

  98. 98.

    Pang, M. Y. H., Sun, X., Ausió, J. and Ishibashi, T. (2020 ). Histone H4 variant, H4G, drives ribosomal RNA transcription and breast cancer cell proliferation by loosening nucleolar chromatin structure. J. Cell. Physiol. 235, 9601-9608.

    Not in our library10.1002/jcp.29770

  99. 99.

    Piquet, S., Le Parc, F., Bai, S.-K., Chevallier, O., Adam, S. and Polo, S. E. (2018 ). The histone chaperone FACT coordinates H2A.X-dependent signaling and repair of DNA damage. Mol. Cell 72, 888-901.e7.

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  100. 100.

    Pliatska, M., Kapasa, M., Kokkalis, A., Polyzos, A. and Thanos, D. (2018 ). The histone variant MacroH2A blocks cellular reprogramming by inhibiting mesenchymal-to-epithelial transition. Mol. Cell. Biol. 38, e00669-17.

    Not in our library10.1128/mcb.00669-17

  101. 101.

    Postberg, J., Forcob, S., Chang, W.-J. and Lipps, H. J. (2010 ). The evolutionary history of histone H3 suggests a deep eukaryotic root of chromatin modifying mechanisms. BMC Evol. Biol. 10, 259.

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    Raisner, R. M., Hartley, P. D., Meneghini, M. D., Bao, M. Z., Liu, C. L., Schreiber, S. L., Rando, O. J. and Madhani, H. D. (2005 ). Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin. Cell 123, 233-248.

    Not in our library10.1016/j.cell.2005.10.002

  103. 103.

    Raja, D. A., Subramaniam, Y., Aggarwal, A., Gotherwal, V., Babu, A., Tanwar, J., Motiani, R. K., Sivasubbu, S., Gokhale, R. S. and Natarajan, V. T. (2020 ). Histone variant dictates fate biasing of neural crest cells to melanocyte lineage. Development 147, dev182576.

    Not in our library10.1242/dev.182576

  104. 104.

    Ramachandran, S., Ahmad, K. and Henikoff, S. (2017 ). Transcription and remodeling produce asymmetrically unwrapped nucleosomal intermediates. Mol. Cell 68, 1038-1053.e4.

    Not in our library10.1016/j.molcel.2017.11.015

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    Ranjan, A., Mizuguchi, G., FitzGerald, P. C., Wei, D., Wang, F., Huang, Y., Luk, E., Woodcock, C. L. and Wu, C. (2013 ). Nucleosome-free region dominates histone acetylation in targeting SWR1 to promoters for H2A.Z replacement. Cell 154, 1232-1245.

    Not in our library10.1016/j.cell.2013.08.005

  106. 106.

    Resnick, R., Wong, C.-J., Hamm, D. C., Bennett, S. R., Skene, P. J., Hake, S. B., Henikoff, S., van der Maarel, S. M. and Tapscott, S. J. (2019 ). DUX4-induced histone variants H3.X and H3.Y mark DUX4 target genes for expression. Cell Rep. 29, 1812-1820.e5.

    Not in our library10.1016/j.celrep.2019.10.025

  107. 107.

    Rosin, L. and Mellone, B. G. (2016 ). Co-evolving CENP-A and CAL1 domains mediate centromeric CENP-A deposition across Drosophila species. Dev. Cell 37, 136-147.

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    Rosin, L. F. and Mellone, B. G. (2017 ). Centromeres drive a hard bargain. Trends Genet. 33, 101-117.

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    Rudnizky, S., Bavly, A., Malik, O., Pnueli, L., Melamed, P. and Kaplan, A. (2016 ). H2A.Z controls the stability and mobility of nucleosomes to regulate expression of the LH genes. Nat. Commun. 7, 12958.

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    Sakai, A., Schwartz, B. E., Goldstein, S. and Ahmad, K. (2009 ). Transcriptional and developmental functions of the H3.3 histone variant in Drosophila. Curr. Biol. 19, 1816-1820.

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    The activity-dependent histone variant H2BE modulates the life span of olfactory neurons · 2012
    No notice
  112. 112.
    Histone deposition pathways determine the chromatin landscapes of H3.1 and H3.3 K27M oncohistones · 2020
    Not checked
  113. 113.

    Seo, J., Kim, S. C., Lee, H.-S., Kim, J. K., Shon, H. J., Salleh, N. L. M., Desai, K. V., Lee, J. H., Kang, E.-S., Kim, J. S. et al. (2012 ). Genome-wide profiles of H2AX and γ-H2AX differentiate endogenous and exogenous DNA damage hotspots in human cells. Nucleic Acids Res. 40, 5965-5974.

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    Sepsa, A., Levidou, G., Gargalionis, A., Adamopoulos, C., Spyropoulou, A., Dalagiorgou, G., Thymara, I., Boviatsis, E., Themistocleous, M. S., Petraki, K. et al. (2015 ). Emerging role of linker histone variant H1x as a biomarker with prognostic value in astrocytic gliomas. A multivariate analysis including trimethylation of H3K9 and H4K20. PLoS ONE 10, e0115101.

    Not in our library10.1371/journal.pone.0115101

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    Sharma, D., De Falco, L., Padavattan, S., Rao, C., Geifman-Shochat, S., Liu, C.-F. and Davey, C. A. (2019 ). PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome. Nat. Commun. 10, 5751.

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    Shechter, D., Chitta, R. K., Xiao, A., Shabanowitz, J., Hunt, D. F. and Allis, C. D. (2009 ). A distinct H2A.X isoform is enriched in Xenopus laevis eggs and early embryos and is phosphorylated in the absence of a checkpoint. Proc. Natl. Acad. Sci. USA 106, 749-754.

    Not in our library10.1073/pnas.0812207106

  117. 117.

    Shinagawa, T., Takagi, T., Tsukamoto, D., Tomaru, C., Huynh, L. M., Sivaraman, P., Kumarevel, T., Inoue, K., Nakato, R., Katou, Y. et al. (2014 ). Histone variants enriched in oocytes enhance reprogramming to induced pluripotent stem cells. Cell Stem Cell 14, 217-227.

    Not in our library10.1016/j.stem.2013.12.015

  118. 118.

    Shinagawa, T., Huynh, L. M., Takagi, T., Tsukamoto, D., Tomaru, C., Kwak, H.-G., Dohmae, N., Noguchi, J. and Ishii, S. (2015 ). Disruption of Th2a and Th2b genes causes defects in spermatogenesis. Development 142, 1287-1292.

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    Shiraishi, K., Shindo, A., Harada, A., Kurumizaka, H., Kimura, H., Ohkawa, Y. and Matsuyama, H. (2018 ). Roles of histone H3.5 in human spermatogenesis and spermatogenic disorders. Andrology 6, 158-165.

    Not in our library10.1111/andr.12438

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    Sitbon, D., Boyarchuk, E., Dingli, F., Loew, D. and Almouzni, G. (2020 ). Histone variant H3.3 residue S31 is essential for Xenopus gastrulation regardless of the deposition pathway. Nat. Commun. 11, 1256.

    Not in our library10.1038/s41467-020-15084-4

  121. 121.

    Skene, P. J. and Henikoff, S. (2013 ). Histone variants in pluripotency and disease. Development 140, 2513-2524.

    Not in our library10.1242/dev.091439

  122. 122.

    Soboleva, T. A., Parker, B. J., Nekrasov, M., Hart-Smith, G., Tay, Y. J., Tng, W.-Q., Wilkins, M., Ryan, D. and Tremethick, D. J. (2017 ). A new link between transcriptional initiation and pre-mRNA splicing: The RNA binding histone variant H2A.B. PLoS Genet. 13, e1006633.

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  123. 123.

    Stoler, S., Rogers, K., Weitze, S., Morey, L., Fitzgerald-Hayes, M. and Baker, R. E. (2007 ). Scm3, an essential Saccharomyces cerevisiae centromere protein required for G2/M progression and Cse4 localization. Proc. Natl. Acad. Sci. USA 104, 10571-10576.

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  124. 124.

    Tachiwana, H., Osakabe, A., Kimura, H. and Kurumizaka, H. (2008 ). Nucleosome formation with the testis-specific histone H3 variant, H3t, by human nucleosome assembly proteins in vitro. Nucleic Acids Res. 36, 2208-2218.

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    Tagami, H., Ray-Gallet, D., Almouzni, G. and Nakatani, Y. (2004 ). Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116, 51-61.

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    Taguchi, H., Xie, Y., Horikoshi, N., Maehara, K., Harada, A., Nogami, J., Sato, K., Arimura, Y., Osakabe, A., Kujirai, T. et al. (2017 ). Crystal structure and characterization of novel human histone H3 variants, H3.6, H3.7, and H3.8. Biochemistry 56, 2184-2196.

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    Talbert, P. B. and Henikoff, S. (2010 ). Histone variants—ancient wrap artists of the epigenome. Nat. Rev. Mol. Cell Biol. 11, 264-275.

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    Talbert, P. B. and Henikoff, S. (2014 ). Environmental responses mediated by histone variants. Trends Cell Biol. 24, 642-650.

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    Talbert, P. B. and Henikoff, S. (2017 ). Histone variants on the move: substrates for chromatin dynamics. Nat. Rev. Mol. Cell Biol. 18, 115-126.

    Not in our library10.1038/nrm.2016.148

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    Talbert, P. B. and Henikoff, S. (2020 ). What makes a centromere? Exp. Cell Res. 389, 111895.

    Not in our library10.1016/j.yexcr.2020.111895

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    Talbert, P. B., Bayes, J. J. and Henikoff, S. (2008 ). The evolution of centromeres and kinetochores: a two-part fugue. In The Kinetochore: From Molecular Discoveries to Cancer Therapy, Vol. 1 (ed. P. De Wulf and W. C. Earnshaw ), pp. 193-230: Springer.

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    Tanaka, M., Hennebold, J. D., Macfarlane, J. and Adashi, E. Y. (2001 ). A mammalian oocyte-specific linker histone gene H1oo: homology with the genes for the oocyte-specific cleavage stage histone (cs-H1) of sea urchin and the B4/H1M histone of the frog. Development 128, 655-664.

    Not in our library10.1242/dev.128.5.655

  133. 133.

    Tanaka, H., Iguchi, N., Isotani, A., Kitamura, K., Toyama, Y., Matsuoka, Y., Onishi, M., Masai, K., Maekawa, M., Toshimori, K. et al. (2005 ). HANP1/H1T2, a novel histone H1-like protein involved in nuclear formation and sperm fertility. Mol. Cell. Biol. 25, 7107-7119.

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    Tani, R., Hayakawa, K., Tanaka, S. and Shiota, K. (2016 ). Linker histone variant H1T targets rDNA repeats. Epigenetics 11, 288-302.

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    Teimouri, M., Najaran, H., Hosseinzadeh, A. and Mazoochi, T. (2018 ). Association between two common transitions of H2BFWT gene and male infertility: a case-control, meta, and structural analysis. Andrology 6, 306-316.

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    Torres, C. M., Biran, A., Burney, M. J., Patel, H., Henser-Brownhill, T., Cohen, A. S., Li, Y., Ben-Hamo, R., Nye, E., Spencer-Dene, B. et al. (2016 ). The linker histone H1.0 generates epigenetic and functional intratumor heterogeneity. Science 353, aaf1644.

    Not in our library10.1126/science.aaf1644

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    Tramantano, M., Sun, L., Au, C., Labuz, D., Liu, Z., Chou, M., Shen, C. and Luk, E. (2016 ). Constitutive turnover of histone H2A.Z at yeast promoters requires the preinitiation complex. eLife 5, e14243

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    Tran, M. H., Aul, R. B., Xu, W., van der Hoorn, F. and Oko, R. (2011 ). Involvement of Classical Bipartite/Karyopherin nuclear import pathway components in acrosomal trafficking and assembly during bovine and murid spermiogenesis. Biol. Reprod. 86, 1-11.

    Not in our library10.1095/biolreprod.111.096842

  139. 139.

    Ueda, J., Harada, A., Urahama, T., Machida, S., Maehara, K., Hada, M., Makino, Y., Nogami, J., Horikoshi, N., Osakabe, A. et al. (2017 ). Testis-specific histone variant H3t gene is essential for entry into spermatogenesis. Cell Rep. 18, 593-600.

    Not in our library10.1016/j.celrep.2016.12.065

  140. 140.

    Urahama, T., Harada, A., Maehara, K., Horikoshi, N., Sato, K., Sato, Y., Shiraishi, K., Sugino, N., Osakabe, A., Tachiwana, H. et al. (2016 ). Histone H3.5 forms an unstable nucleosome and accumulates around transcription start sites in human testis. Epigenet. Chromatin 9, 2.

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    Van Doninck, K., Mandigo, M. L., Hur, J. H., Wang, P., Guglielmini, J., Milinkovitch, M. C., Lane, W. S. and Meselson, M. (2009 ). Phylogenomics of unusual histone H2A Variants in Bdelloid rotifers. PLoS Genet. 5, e1000401.

    Not in our library10.1371/journal.pgen.1000401

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    ATRX Plays a Key Role in Maintaining Silencing at Interstitial Heterochromatic Loci and Imprinted Genes · 2015
    No notice
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    Wang, J., Youkharibache, P., Zhang, D., Lanczycki, C. J., Geer, R. C., Madej, T., Phan, L., Ward, M., Lu, S., Marchler, G. H. et al. (2020 ). iCn3D, a web-based 3D viewer for sharing 1D/2D/3D representations of biomolecular structures. Bioinformatics 36, 131-135.

    Not in our library10.1093/bioinformatics/btz502

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    Waterborg, J. H. (2012 ). Evolution of histone H3: emergence of variants and conservation of post-translational modification sites. Biochem. Cell Biol. Biochim. Biol. Cell. 90, 79-95.

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    Waterborg, J. H. and Robertson, A. J. (1996 ). Common features of analogous replacement histone H3 genes in animals and plants. J. Mol. Evol. 43, 194-206.

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    Weber, C. M., Ramachandran, S. and Henikoff, S. (2014 ). Nucleosomes are context-specific, H2A.Z-modulated barriers to RNA polymerase. Mol. Cell 53, 819-830.

    Not in our library10.1016/j.molcel.2014.02.014

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    Wirbelauer, C., Bell, O. and Schubeler, D. (2005 ). Variant histone H3.3 is deposited at sites of nucleosomal displacement throughout transcribed genes while active histone modifications show a promoter-proximal bias. Genes Dev. 19, 1761-1766.

    Not in our library10.1101/gad.347705

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    Wong, L. H., Ren, H., Williams, E., McGhie, J., Ahn, S., Sim, M., Tam, A., Earle, E., Anderson, M. A., Mann, J. et al. (2009 ). Histone H3.3 incorporation provides a unique and functionally essential telomeric chromatin in embryonic stem cells. Genome Res. 19, 404-414.

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    Wong, L. H., McGhie, J. D., Sim, M., Anderson, M. A., Ahn, S., Hannan, R. D., George, A. J., Morgan, K. A., Mann, J. R. and Choo, K. H. A. (2010 ). ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res. 20, 351-360.

    Not in our library10.1101/gr.101477.109

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    Wu, W.-H., Wu, C.-H., Ladurner, A., Mizuguchi, G., Wei, D., Xiao, H., Luk, E., Ranjan, A. and Wu, C. (2009 ). N terminus of Swr1 binds to histone H2AZ and provides a platform for subunit assembly in the chromatin remodeling complex. J. Biol. Chem. 284, 6200-6207.

    Not in our library10.1074/jbc.m808830200

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    Wu, B. J., Dong, F. L., Ma, X. S., Wang, X. G., Lin, F. and Liu, H. L. (2014 ). Localization and expression of histone H2A variants during mouse oogenesis and preimplantation embryo development. Genet. Mol. Res. 13, 5929-5939.

    Not in our library10.4238/2014.august.7.8

  152. 152.

    Yan, W., Ma, L., Burns, K. H. and Matzuk, M. M. (2003 ). HILS1 is a spermatid-specific linker histone H1-like protein implicated in chromatin remodeling during mammalian spermiogenesis. Proc. Natl. Acad. Sci. USA 100, 10546-10551.

    Not in our library10.1073/pnas.1837812100

  153. 153.

    Yelagandula, R., Stroud, H., Holec, S., Zhou, K., Feng, S., Zhong, X., Muthurajan, U. M., Nie, X., Kawashima, T., Groth, M. et al. (2014 ). The histone variant H2A.W defines heterochromatin and promotes chromatin condensation in Arabidopsis. Cell 158, 98-109.

    Not in our library10.1016/j.cell.2014.06.006

  154. 154.
    Medusavirus, a Novel Large DNA Virus Discovered from Hot Spring Water · 2019
    No notice
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    Yuen, B. T. K., Bush, K. M., Barrilleaux, B. L., Cotterman, R. and Knoepfler, P. S. (2014 ). Histone H3.3 regulates dynamic chromatin states during spermatogenesis. Development 141, 3483-3494.

    Not in our library10.1242/dev.106450

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    Zink, L.-M., Delbarre, E., Eberl, H. C., Keilhauer, E. C., Bönisch, C., Pünzeler, S., Bartkuhn, M., Collas, P., Mann, M. and Hake, S. B. (2017 ). H3.Y discriminates between HIRA and DAXX chaperone complexes and reveals unexpected insights into human DAXX-H3.3-H4 binding and deposition requirements. Nucleic Acids Res. 45, 5691-5706.

    Not in our library10.1093/nar/gkx131

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