[Cell Cycle 6:17, 2113-2119, 1 September 2007]; ©2007 Landes Bioscience

Perspective

Chromatin Polymorphism and the Nucleosome Superfamily A Genealogy Christophe Lavelle1,* Ariel Prunell2

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Original manuscript submitted: 05/23/07 Revised manuscript submitted: 06/25/07 Manuscript accepted:06/26/07

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*Correspondence to: Christophe Lavelle; Cellular and Molecular Microscopy Group; CNRS - UMR 8126; Institut Gustave Roussy; 39 rue Camille Desmoulins; Villejuif 94805 France; Tel.: 33.6.24.71.44.03; Fax: 33.1.42.11.54.94; Email: [email protected]

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2Chromatin Biochemistry Group; Institut Jacques Monod; Paris, France

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and Molecular Microscopy Group; Institut Gustave Roussy; Villejuif,

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Nucleosomes were discovered more than thirty years ago as the basic repeating units of chromatin. Since then, nucleosomes have progressively revealed their taste to come in many appearances, upon either adjunction of other proteins (e.g., a fifth histone or a nonhistone protein, HMG‑N), histone substitution for isoforms (histone variants), depletion of one or the two H2A‑H2B dimers (sub‑nucleosomes), intimate two‑particle association, or isomeric structural alterations. The resulting entities, some of them are only transient, acquire new properties useful for their specific roles in chromatin function. These structures are presented here in the chronological order of their identification, from the chromatosome to the sub‑nucleosomal hexasome and tetrasome, and from the dinucleosomal altosome and nucleodisome to the nucleosome variants and altered forms: the old lexosome and the most recent reversome.

Previously published online as a Cell Cycle E-publication: http://www.landesbioscience.com/journals/cc/article/4631

The term “chromatin” was introduced more than a century ago by German cytogeneticist W. Flemming (translated from ref. 3: “…the material which thus far I have called the stainable substance of the nucleus […] I shall coin the term chromatin for the time being”), two years before its protein contents received its “histone” name.4 The chromatin subunit, ~160 bp of DNA wrapped into two turns of a left‑handed superhelix around an octameric core of two copies each of histones H2A, H2B, H3 and H4, was identified in 1973/745‑7 and was first called “n‑body”7 (see refs. 8�� ����������������������������������� and 9 for historical perspectives) before receiving its definite name of “nucleosome” in 1975 (quote from ref. 10: “electron microscopic and biochemical studies demonstrate that the fundamental structure of chromatin […] is composed of a flexible chain of spherical particles [nucleosomes]”). Very popular today due to their general property as organizers of the eukaryotic genome and carriers of epigenetic information, nucleosomes are subjected to much effort aiming mainly at revealing their exact role in the controlled access of regulating factors to target DNA sequences. Of particular interest are the studies on histone tails modifications and the so‑called “histone code” hypothesis which occupy most of the epigenetics scene today.11‑14 Despite their common representation as simple cylinders (decorated sometimes with protruding tails), more and more studies suggest that nucleosomes in the cell nucleus spend a significant fraction of their life‑time in various conformations, either structural or replacement isomers, or super‑ or sub‑order structures of the canonical octameric form. The main characteristics of the members of such a nucleosome superfamily are described below. Following the terminology of tetrasome and hexasome for the tetrameric and hexameric sub‑nucleosomal particles (see below), the term “octasome” for the canonical nucleosome would seem more appropriate.15,16 However its appeal may be insufficient to supplant the old nucleosome term crowned with so much historical value.

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chromatin, histone variants, nucleosome, chromatosome, tetrasome, hexasome, lexosome, reversome, altosome, remodeling

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1975: IT All Began with the Nucleosome

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Acknowledgements

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We would like to thank E. Le Cam (Villejuif, France) and N. Conde e Silva (Paris, France) for help related to the figure, and all our coauthors in refs. 1 and 2 for discussion.

1978: The Chromatosome The particle made of the nucleosome plus the linker histone was named chromatosome three years after the nucleosome (quote from ref. 17: “I have prepared chromatin particles from chicken erythrocytes which contain a 160 base pair length of DNA, an octamer of the four smaller histones and a molecule of lysine rich histone […], called chromatosomes for convenience”). In chromatosomes, one copy of the linker histone (H1/H5) seals the two turns of the DNA through interaction of its globular domain, while

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its C‑terminal tail links the two proximal entry/exit DNA regions together into a stem roughly coincident with the particle dyad axis.18 The stem enhances the dynamics of entry/exit DNAs, increasing in particular their ability to cross positively, which generates particles with the interesting property of being almost topologically neutral.19 H1, which may be chaperoned in vivo with ��������������� NAP‑1 or NAP‑2,20 21 22‑25 hinders chromatin repair or transcription, presumably through collective effects, i.e., the capacity of the chromatin fiber to further compact upon linker histone binding.26,27 Several issues related to the linker histone, e.g., its exact binding mode on the nucleosome,28 its role in nucleosome spacing29 or the mechanism of its exchange in vivo30 are still debated (reviewed in ref. 16).�������������������� H1 has competitors for nucleosome binding, in particular HMG‑N.31 HMGs (mainly HMG‑N, HMG‑B and HMG‑A) are generally thought to give chromatin more fluidity and in particular to increase its transcriptional potential, although the mechanisms mediating these effects are not always clear.32

1999: The Tetrasome

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Nucleosome loss of the two H2A‑H2B dimers results in a tetrameric particle the existence of which has been suspected from the early chromatin days, both from nuclease digestion46 and electron microscopy.47 This particle was first named “R‑body”, in reference to arginine (R)‑rich H3 and H4, and to the above “n‑body” appellation of the nucleosome.48 However, it is not clear whether these and subsequent data49 relate to true DNA/tetramer or rather DNA/di‑tetramer complexes. Indeed, ��������������� (H3‑H4)2 tetramers have a propensity to stack on top of each other50 leading to pseudo‑ octamers which wrap DNA very much like normal nucleosomes, as shown by sedimentation,51 low‑angle X‑ray scattering,52 gel electrophoresis,53‑55 site‑directed cleavage with hydroxyl radicals,54 or electron microscopic visualization.53,56 At ������������������������ that time, we coined the single‑tetramer complex as “tetrasome” (quote from ref. 53: “our laboratory has previously reported the ability of the histone (H3‑H4)2 tetramer to form monomeric particles, which for convenience we will call tetrasomes”). “Tetrasome” fibers may also suffer from the 1981: The Nucleodisome tetramer‑stacking problem, as suggested by the ~140‑bp‑wrapped DNase I or II digestions of erythrocyte nuclei were found to result particles obtained upon tetramer ������������������������������������������� assembly on tandem repeats of the in DNA fragments of sizes consistent with a relatively resistant struc- 5S sequence and imaging by atomic force microscopy.15 Our own ture of two nucleosomes33‑35 called nucleodisome (quote from ref. 34: electron micrographs of similar arrays show that true tetrasomes are “the pigeon erythrocyte contains a particular structural unit consisting obtained only at low histone/DNA ratios, i. e. at low particle densities of two nucleosomes. This unit may be called as nucleodisome”). (Fig. 1A), while di‑tetrasome complexes (pseudo‑nucleosomes) form Micrococcal nuclease ability to generate fragments of the usual at larger ratios (Fig. 1B) that resemble regular nucleosomes reconstinucleosome repeat length under the same conditions suggested that tuted on the same DNA (Fig. 1C). Thus, true tetrasomes assembled this double‑nucleosome repeat pattern resulted from a modulation either on long (Fig. 1A) or short DNA (inset in Fig. 1A) have a of cleavage sites accessibility within the histone‑bound DNA, and distinctive hairpin‑like appearance, as opposed to the round‑shaped reflected a particular arrangement of nucleosomes in compact di‑tetrasomes (Fig. 1B). chromatin.35,36 Tetrasomes have the intriguing ability to switch their chirality Nucleodisomes cannot be considered as particles per se (as opposed from a DNA left‑handed wrapping to a right‑handed wrapping, a to compact dinucleosomes or altosomes; see below), and must be process�������������������������������������������������� referred to as the “tetrasome chiral transition”.53,56‑59 This distinguished from dinucleosomes produced by limited cleavage of low‑energy (~2 kT) transition presumably occurs through a rotation linker DNAs in chromatin with micrococcal nuclease.37 Noteworthy, of the two H3‑H4 dimers relative to each other around an axis going these dinucleosomes have sometimes been called disomes, and simi- through the two cysteines 110, as suggested by the observation that larly tetranucleosomes and hexanucleosomes were called tetrasomes their oxidation into a disulfide bridge does not hinder the transition. and hexasomes.38 However, oligonucleosomes have a rare occurrence This scheme also received a theoretical support through Normal in the literature, perhaps explaining that they abandoned their names Mode analysis of tetrasome structural dynamics.60 Interestingly, to sub‑nucleosomal particles (see below). archaeal histones (HMf ) share the capacity to form tetrameric particles which wrap ~50 bp into a superhelix of either chirality.60 1983: The Lexosome The potential functional relevance of the tetrasome chiral transition The lexosome is an altered nucleosome proposed to be a specimen will be discussed below in the reversome section. of a transcription‑poised nucleosome (quote from ref. 39: “the data presented in this paper support the concept of a special type of nucleo- 2002: The Hexasome protein subunit, specifically located on transcribed DNA regions and The hexasome contains the tetramer and only one H2A‑H2B with properties that facilitate transcription. We propose the term dimer (quote from ref. 61: “…the reconstituted histone hexamer “lexosome” for these particles”). The distinctive feature of lexosomes, which allowed them to be purified through affinity chromatography bound to the 254 bp DNA (hexasome) and the novel nucleoproin the first place, is to have their H3 cysteines 110 accessible to thiols tein complex have the same mobility in the native gel…”). Like reagents,40,41 while these residues (located at the H3/H3 interface42) the tetrasome, the hexasome has been observed long ago, usually by incubation in urea or are inaccessible in standard nucleosomes.43 Consistent with this obtained through nucleosome depletion 62,63 Recently, it was observed chemical treatment of amino groups. accessibility, electron spectroscopic imaging of lexosomes showed a with NAP‑1 or RNA lead to hexasomes rather than U‑like shape quite different from that of nucleosomes.44 In vitro tran- that depletions 2,64,65 The same was observed upon transcription of single tetrasomes. 45 scription assays failed, however, to confirm the lexosome transition, nucleosomes with RNA polymerase II,61 in agreement with older ������ emphasizing its elusive nature. studies pointing to hexasomes as facilitating RNA polymerase II transcription through chromatin.61,66,67 In contrast, RNA polymerase I or III and phage RNA polymerases lead, depending on conditions, to the octamer complete removal68 or to its translocation to upstream 2114

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Figure 1. Electron microscopic view of tetrameric, di‑tetrameric and octameric histone/DNA particles. Particles were reconstituted by conventional salt‑ dialysis method147 with (H2A, H2B, H3, H4)2 octamers and (H3, H4)2 tetramers at different histone/DNA weight ratios (r w) on 5S 208‑18 DNA, and observed under the electron microscope (ZEISS 902 in dark field mode; facility provided by E. Le Cam). The lower tetramer/DNA ratio led to standard hairpin‑shaped tetrasomes wrapped with ~75 bp (A), while the higher tetramer/DNA ratio (needed to cover more DNA repeat sequences and begin to build a proper array as in ref. 15) resulted in round‑shaped pseudo‑nucleosomes (B) resembling regular nucleosomes (C), although they are wrapped with slightly less DNA. A tetrasome and a pseudo‑tetrasome similarly assembled on a 199 bp DNA frag‑ ment are shown in insets in (A) and (B) (from ref. 53).

proposed to burry some modified residues on the nucleosome faces, whose exposure following local superstructure disruption upon DNA damage activates repair.78 However, gaping failed to be confirmed by Normal Mode analysis of tetrasome structural dynamics,2 and no direct evidence has so far been brought for its existence.

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DNA sites69 (recently discussed in ref. 70).�������������������� Hexasomes ������������������� can also form in vivo during replication71 or ���������� repair,71,72 and probably also as transient by‑products during the continuous dimer exchange taking place in the nucleus.73 The occurrence of an hexasome intermediate implies that release of the first dimer stabilizes the second dimer, possibly through a still‑to‑be‑characterized allosteric effect within the particle. Interestingly, an hexasome is also the main intermediate in nucleosome assembly with NAP‑1,65 showing that tetrasome incorporation of the first dimer decreases the affinity for the second. In contrast, octamer assembly from the tetramer and the dimers in high salt does not stop at the hexamer step but goes directly to the octamer.74 In the absence of DNA, therefore, the binding of the first dimer instead enhances binding of the second. This discrepancy is consistent with the first dimer forcing the free tetramer into the chirally‑negative conformation suitable for binding of the second.

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2005: The Altosome

2003: The Gaped Nucleosome

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Following the model of a DNA superhelix axis curved toward the entry‑exit of the nucleosome in order to explain its DNA sequence‑dependent anomalously large ability to cross positively (the so‑called “ sequence‑dependent nucleosome dynamic polymorphism”),75 a gaped nucleosome was proposed (quote from ref. 76: “we have called “gaping” this kind of hinge opening of the nucleosome because it reminds us of a gaping oyster”). Gaping is viewed to result from a rotation of the two H3‑H4 dimers around their H3/H3 interface in a direction which increases the pitch of the negative superhelix, i.e., opposite to that occurring in the tetrasome chiral transition. By providing a better nucleosome stacking in the fiber superstructure,76 gaped nucleosomes were thought to be of advantage for mitotic chromosomes condensation.77 Forcing �������������������������� a nucleosome into gaping requires a large energy (~20 kT76) supposed to originate from the forces developed during chromatin and chromosome condensation.77 Notably, ����������������������������������������������������������� the resulting tighter nucleosome packing has been www.landesbioscience.com

Human SWI/SNF and yeast RSC acting on mononucleosomes were found to generate altered dinucleosomal structures that were stable in the absence of the factor and which reverted to canonical nucleosomes when reincubated with the remodeler.79,80 At least with SWI/SNF, similar structures, eventually called “altosomes”, occurred when using nucleosome arrays as substrates81,82 (quote from ref. 82: “… this change in supercoiling is due to the conversion of up to one‑half of the nucleosomes on polynucleosomal arrays into asymmetric structures, termed “altosomes”, each composed of two histone octamers…”). In these structures, DNA partially released from one nucleosome is thought to bind to the exposed histone surface on the other and vice versa.83,84 It is not clear, however, whether altosomes contain a full complement of H2A‑H2B dimers, and how they compare with the compact dinucleosomes (~260 bp against ~147 x 2 = 294 bp expected for two abutted core particles) previously obtained upon micrococcal nuclease digestion of chromatin.85

2007: The Reversome Torsional manipulation revealed that single chromatin fibers can accommodate surprisingly large amounts of twist without much change of their length (our recent paper, ref. 1). The model confirmed the access of individual nucleosomes within the array to three conformational states, depending on the crossing status of their entry‑exit DNAs, negative, null, or positive, as originally documented using mononucleosomes on DNA minicircles59,75,86 (reviewed in ref. ��������� 87)� ����.

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In a second paper,2 we showed that fibers submitted to large positive torsions transiently trap approximately one positive turn of DNA topological deformation per nucleosome. Comparison with the torsional response of tetrasome fibers obtained upon depletion of H2A‑H2B dimers (direct reconstitution with tetramers would have led to fibers of pseudo‑nucleosomes; see above and Figure 1B) suggested that the trapping reflected a nucleosome chiral transition to a metastable form built on the right‑handed tetrasome, that we called “reversome” (quote from ref. 2: “ as much as its structure is unique, we propose to call it a reversome—for reverse nucleosome”). The nucleosome‑reversome transition is thought to facilitate transcription elongation by giving the main RNA polymerase a lever to break the docking of the dimers on the tetramer, which otherwise exerts an almost absolute block against transcription in the absence of other factors at physiological ionic strength (see discussion in ref. ��������� ���� 70). Reversomes were proposed to form at a distance under the influence of the positive supercoiling wave pushed in front of the RNA polymerase.88 A model using the energy parameters of the transition suggested that reversomes can be produced in a time‑scale consistent with the polymerase elongation speed, resulting in a “reversome wave” that progresses much faster than the polymerase.2 Once that wave has reached the end of the transcriptional domain, further progression of the polymerase would rely on the relaxing activities of the endogenous topoisomerases.89 Could reversome be another name for the lexosome? Probably not, since the reversome may differ from the lexosome in having the thiols of its H3 cysteines 110 inaccessible. The failure of these cysteines’ oxidation into a disulfide bridge to interfere with the tetrasome chiral transition56 (see above) indeed points to an inaccessibility of the thiols in the right‑handed tetrasome, and thus in the reversome.

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due to less strict structural requirements. H1° and H5 are among the most divergent.115 Histone variants confer upon nucleosomes new structural and functional properties. Among the most remarkable examples: (1) the partial unwrapping at the edges of H2A.Bbd nucleosomes, which is consistent with H2A.Bbd enrichment in transcriptionally active chromatin;116,117 (2) the easier disassembly of CENP‑A nucleosomes at the levels of both dimers and tetramer, that may help in their exclusive centromeric localization;64 (3) the stabilization of H2A. Z nucleosomes,118 which may prevent spreading of silencing into euchromatin;119 (4) the destabilization of H3.3 nucleosomes,120 which is consistent with their enrichment in active chromatin.121 Interestingly, instability of these nucleosomes appears to be enhanced upon the simultaneous replacement of H2A by H2A.Z,120 consistent with the presence of H2A.Z nucleosomes in active genes of yeast (where H3 is mostly of the H3.3 type122) and chicken;123 and (5) the transcriptional block occurring upon replacement of H1 by the more positively‑charged H5 at some stage in development of the erythroid lineage in avians.124 This block may be mediated by H5 preventing nucleosome opening through a tighter sealing of the two turns of the nucleosomal superhelix. Additionally, core histone variants may directly affect the associative behavior of nucleosomes in chromatin superstructures: for instance, H2A.Z enhances the intramolecular folding of chromatin fibers, while inhibiting their intermolecular association (oligomerization).125 Although free histones suffice to reconstitute nucleosomes in vitro, they usually come with chaperones in vivo. ������������������� Chaperones (unique proteins or large multi‑protein complexes; reviewed in refs. 126 and 127) are in heavy duty, having not only to help canonical histones to be deposited behind the replication fork in S-phase, but also to mediate incorporation of histone variants in a replication‑independent and targeted process to generate specialized chromatin domains 1977–?: The Nucleosome in Disguise: The Variants such as active genes, silent loci or centromeres.94 A list of chaperones Numerous histone nonallelic isoforms (first identified for H2A can only be provisional as new ones are regularly identified. They and H3, ref. 90), called histone variants (or "deviants," refs. 91 and may be regarded, according to ref. 126, as acceptors (nucleoplasmin 92), exhibit primary sequence differences in strategic regions of the for H2A‑H2B;128 N1/N2 for H3‑H4129), donors (Asf1 for H3‑H4, histone fold (reviewed in refs. 91 and 93–97). reviewed in ref. 71; Chz1 for H2A.Z‑H2B130), shuttles (FACT131 H2A. In addition to canonical forms H2A.1 and H2A.2 (the repli- for H2A‑H2B; NAP‑1/2 for all histones16), depositors (CAF‑1 cation type variants, synthesised exclusively during DNA replication, for replication‑dependent deposition of H3.1/H3.2‑H4;132 HIRA ref. 90), H2A variants include H2A.X and H2A.Z (replacement type for transcription‑coupled deposition of H3.3‑H4133), or escorts variants, synthesised throughout the cell cycle;98 noteworthy, H2A.X (RpAb48 (p48) for H3‑H4134,135). represents 2–25% of nuclear H2A in mammals but is the major core Histone chaperones may cooperate with ATP-dependent nucleohistone in yeast99,100), macroH2A (named from its large C‑terminal some remodelers in chromatin assembly136,137 and catalyze active tail of unknown function that makes up two thirds of the protein histone replacement outside of replication. This was found with size and was first isolated from rat liver;101 it has later been renamed H2A.Z both in S. cerevisiae138 or Drosophila139, and may occur with macroH2A.1 since a second macroH2A gene has been identified that other variants as well. In contrast to H2AZ, CENH3s may use a codes for macroH2A.2102), and H2A.Bbd (“Barr‑body deficient”, paossive process to be incorporated in centromeric chromatin. CID characterized by its absence from the inactive X chromosome103). co-purifies with p48 (along with H4) in a preassembly complex134 H2B. H2B variants are all testis specific, as identified so far while Cse4p interacts with Scm3140-142, both simple proteins devoid in human: spH2B (sperm specific, discovered in a telomere- of ATPase activity and without links to active nuclear proccesses. binding complex104), TSH2B (another testis specific variants105) and Intriguingly, Scm3 is able to displace H2A-H2B dimers from the H2BFWT (H2B family, member W, testis specific106). histone octamer, suggesting dimers may be substituted for Scm3 in H3. The H3 family mainly contains H3.1, H3.2 and H3.390 (H3.1 the single nucleosom of the budding yeast point centromere.141 and H3.2 are replication type, while H3.3 is a replacement type deposited in transcriptionally active loci107), and centromere-specific variants Conclusion collectively named CENH3108 (including CENP‑A in humans,109,110 Cse4p in budding yeast111,112 and CID in Drosophila.113 This historical overview clearly shows that nucleosomes can be H4. No variant of that histone has so far been identified. almost anything except “tuna cans” (to share an image introduced H1. The linker histone has diverged substantially more than the core in ref. 143). They acquire specific structural and dynamic properhistones during evolution and shows many variants,114 presumably ties upon interaction with a variety of proteins or protein complexes 2116

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While alluding to the future (see above), we did not foresee that it was so close. Heterotypic tetrasomes containing one copy each of H2A, H2B, CENH3 and H4 were recently identified in interphasic Drosophila melanogaster centromeres,144 through an approach combining histone cross-linking and nuclease digestion with electron and atomic force microscopies. This comes 30 years after similar particles were first predicted145 and apparently observed in electron micrographs of purified SV40 minichromosomes,146 but never since confirmed. Such half-nucleosomes, that we propose to call “hemisomes,” if unstable relative to nucleosomes, would insure their preferential clearing from the chromosome arms in a contribution to their exclusive centromeric localization,144 providing a striking parallel with our own interpretation of the easier disassembly of human CENP-A nucleosomes.64

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20. Kepert JF, Mazurkiewicz J, Heuvelman GL, Toth KF, Rippe K. NAP1 modulates binding of linker histone H1 to chromatin and induces an extended chromatin fiber conformation. J Biol Chem 2005; 280:34063‑72. 21. Kysela B, Chovanec M, Jeggo PA. Phosphorylation of linker histones by DNA‑dependent protein kinase is required for DNA ligase IV‑dependent ligation in the presence of histone H1. Proc Natl Acad Sci USA 2005; 102:1877‑82. 22. O‘Neill TE, Meersseman G, Pennings S, Bradbury EM. Deposition of histone H1 onto reconstituted nucleosome arrays inhibits both initiation and elongation of transcripts by T7 RNA polymerase. Nucleic Acids Res 1995; 23:1075‑82. 23. Shimamura A, Sapp M, Rodriguez‑Campos A, Worcel A. Histone H1 represses transcription from minichromosomes assembled in vitro. Mol Cell Biol 1989; 9:5573‑84. 24. Wolffe AP. Dominant and specific repression of Xenopus oocyte 5S RNA genes and satellite I DNA by histone H1. Embo J 1989; 8:527‑37. 25. Zlatanova J, Caiafa P, Van Holde K. Linker histone binding and displacement: Versatile mechanism for transcriptional regulation. Faseb J 2000; 14:1697‑704. 26. Bednar J, Horowitz RA, Grigoryev SA, Carruthers LM, Hansen JC, Koster AJ, Woodcock CL. Nucleosomes, linker DNA, and linker histone form a unique structural motif that directs the higher‑order folding and compaction of chromatin. Proc Natl Acad Sci USA 1998; 95:14173‑8. 27. Hannon R, Bateman E, Allan J, Harborne N, Gould H. Control of RNA polymerase binding to chromatin by variations in linker histone composition. J Mol Biol 1984; 180:131‑49. 28. Thomas JO. Histone H1: Location and role. Curr Opin Cell Biol 1999; 11:312‑7. 29. Woodcock CL, Skoultchi AI, Fan Y. Role of linker histone in chromatin structure and function: H1 stoichiometry and nucleosome repeat length. Chromosome Res 2006; 14:17‑25. 30. Misteli T, Gunjan A, Hock R, Bustin M, Brown DT. Dynamic binding of histone H1 to chromatin in living cells. Nature 2000; 408:877‑81. 31. Catez F, Brown DT, Misteli T, Bustin M. Competition between histone H1 and HMGN proteins for chromatin binding sites. EMBO Rep 2002; 3:760‑6. 32. Catez F, Yang H, Tracey KJ, Reeves R, Misteli T, Bustin M. Network of dynamic interactions between histone H1 and high‑mobility‑group proteins in chromatin. Mol Cell Biol 2004; 24:4321‑8. 33. Burgoyne LA, Skinner JD. Chromatin superstructure: The next level of structure above the nucleosome has an alternating character: A two‑nucleosome based series is generated by probes armed with DNAase‑I acting on isolated nuclei. Biochem Biophys Res Commun 1981; 99:893‑9. 34. Khachatrian AT, Pospelov VA, Svetlikova SB, Vorob’ev VI. Nucleodisome ‑ A new repeat unit of chromatin revealed in nuclei of pigeon erythrocytes by DNase I digestion. FEBS Lett 1981; 128:90‑2. 35. Kukushkin AN, Svetlikova SB, Pospelov VA. A structure of potentially active and inactive genes of chicken erythrocyte chromatin upon decondensation. Nucleic Acids Res 1988; 16:8555‑69. 36. Pospelov VA, Svetlikova SB. Higher order chromatin structure determines double‑nucleosome periodicity of DNA fragmentation. Mol Biol Rep 1982; 8:117‑22. 37. Pospelov VA, Svetlikova SB. On the mechanism of nucleodisome splitting off by nucleases. FEBS Lett 1982; 146:157‑60. 38. Drinkwater RD, Wilson PJ, Skinner JD, Burgoyne LA. Chromatin structures: Dissecting their mixed patterns in nuclease digests. Nucleic Acids Res 1987; 15:8087‑103. 39. Prior CP, Cantor CR, Johnson EM, Littau VC, Allfrey VG. Reversible changes in nucleosome structure and histone H3 accessibility in transcriptionally active and inactive states of rDNA chromatin. Cell 1983; 34:1033‑42. 40. Chen TA, Allfrey VG. Rapid and reversible changes in nucleosome structure accompany the activation, repression, and superinduction of murine fibroblast protooncogenes c‑fos and c‑myc. Proc Natl Acad Sci USA 1987; 84:5252‑6. 41. Johnson EM, Sterner R, Allfrey VG. Altered nucleosomes of active nucleolar chromatin contain accessible histone H3 in its hyperacetylated forms. J Biol Chem 1987; 262:6943‑6. 42. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997; 389:251‑60. 43. Olins DE, Bryan PN, Harrington RE, Hill WE, Olins AL. Conformational states of chromatin nu bodies induced by urea. Nucleic Acids Res 1977; 4:1911‑31. 44. Bazett‑Jones DP, Mendez E, Czarnota GJ, Ottensmeyer FP, Allfrey VG. Visualization and analysis of unfolded nucleosomes associated with transcribing chromatin. Nucleic Acids Res 1996; 24:321‑9. 45. Protacio RU, Widom J. Nucleosome transcription studied in a real‑time synchronous system: Test of the lexosome model and direct measurement of effects due to histone octamer. J Mol Biol 1996; 256:458‑72. 46. Camerini‑Otero RD, Sollner‑Webb B, Felsenfeld G. The organization of histones and DNA in chromatin: Evidence for an arginine‑rich histone kernel. Cell 1976; 8:333‑47. 47. Oudet P, Germond JE, Sures M, Gallwitz D, Bellard M, Chambon P. Nucleosome structure I: All four histones, H2A, H2B, H3, and H4, are required to form a nucleosome, but an H3‑H4 subnucleosomal particle is formed with H3‑H4 alone. Cold Spring Harb Symp Quant Biol 1978; 42(Pt 1):287‑300. 48. Bina‑Stein M. Folding of 140‑base pair length DNA by a core of arginine‑rich histones. J Biol Chem 1978; 253:5213‑9. 49. Read CM, Crane‑Robinson C. The structure of sub‑nucleosomal particles: The octameric (H3/H4)4‑125‑base‑pair‑DNA complex. Eur J Biochem 1985; 152:143‑50. 50. Baxevanis AD, Godfrey JE, Moudrianakis EN. Associative behavior of the histone (H3‑H4)2 tetramer: Dependence on ionic environment. Biochemistry 1991; 30:8817‑23.

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(linker histones, HMGs, transcription factors, histone chaperones etc), and show a great resilience under the transient torques and forces inflicted by endogenous molecular motors (e.g., remodeling factors, polymerases). Histone variants (along with histone post‑translational modifications; not referred to here) introduce a further potential for diversity that has profound consequences at both the individual nucleosome level and the local chromatin superstructure. Even more remarkable, the prospect seems good that nonhistone proteins may, under peculiar circumstances, take the place of true histone components within the structure to bring it to fulfilling new functions. Although already pretty long, this list of members of the nucleosome super‑family together with their variants is unlikely to be complete, as new offspring may come to light in the future. The canonical nucleosome obviously is the head of the family, and some members may be more important than others, but for sure, all are needed.

References

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