Histone variants — ancient wrap artists of the epigenome (original) (raw)
Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F. & Richmond, T. J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature389, 251–260 (1997). ArticleCASPubMed Google Scholar
Zlatanova, J., Bishop, T. C., Victor, J. M., Jackson, V. & van Holde, K. The nucleosome family: dynamic and growing. Structure17, 160–171 (2009). ArticleCASPubMed Google Scholar
Allshire, R. C. & Karpen, G. H. Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nature Rev. Genet.9, 923–937 (2008). ArticleCASPubMed Google Scholar
Malik, H. S. & Henikoff, S. Major evolutionary transitions in centromere complexity. Cell138, 1067–1082 (2009). ArticleCASPubMed Google Scholar
Orsi, G. A., Couble, P. & Loppin, B. Epigenetic and replacement roles of histone variant H3.3 in reproduction and development. Int. J. Dev. Biol.53, 231–243 (2009). ArticleCASPubMed Google Scholar
Altaf, M., Auger, A., Covic, M. & Cote, J. Connection between histone H2A variants and chromatin remodeling complexes. Biochem. Cell Biol.87, 35–50 (2009). ArticleCASPubMed Google Scholar
Ismail, I. H. & Hendzel, M. J. The γH2A.X: is it just a surrogate marker of double-strand breaks or much more? Environ. Mol. Mutagen.49, 73–82 (2008). ArticleCASPubMed Google Scholar
Gonzalez-Romero, R., Mendez, J., Ausio, J. & Eirin-Lopez, J. M. Quickly evolving histones, nucleosome stability and chromatin folding: all about histone H2A.Bbd. Gene413, 1–7 (2008). ArticleCASPubMed Google Scholar
Cairns, B. R. The logic of chromatin architecture and remodelling at promoters. Nature461, 193–198 (2009). ArticleCASPubMed Google Scholar
Arents, G. & Moudrianakis, E. N. The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc. Natl Acad. Sci. USA92, 11170–11174 (1995). ArticleCASPubMedPubMed Central Google Scholar
Sandman, K. & Reeve, J. N. Archaeal histones and the origin of the histone fold. Curr. Opin. Microbiol.9, 520–525 (2006). ArticleCASPubMed Google Scholar
Marc, F., Sandman, K., Lurz, R. & Reeve, J. N. Archaeal histone tetramerization determines DNA affinity and the direction of DNA supercoiling. J. Biol. Chem.277, 30879–30886 (2002). ArticleCASPubMed Google Scholar
Fahrner, R. L., Cascio, D., Lake, J. A. & Slesarev, A. An ancestral nuclear protein assembly: crystal structure of the Methanopyrus kandleri histone. Protein Sci.10, 2002–2007 (2001). ArticleCASPubMedPubMed Central Google Scholar
Li, W. T., Sandman, K., Pereira, S. L. & Reeve, J. N. MJ1647, an open reading frame in the genome of the hyperthermophile Methanococcus jannaschii, encodes a very thermostable archaeal histone with a C-terminal extension. Extremophiles4, 43–51 (2000). CASPubMed Google Scholar
Friedrich-Jahn, U., Aigner, J., Langst, G., Reeve, J. N. & Huber, H. Nanoarchaeal origin of histone H3? J. Bacteriol.191, 1092–1096 (2009). ArticleCASPubMed Google Scholar
Alilat, M., Sivolob, A., Revet, B. & Prunell, A. Nucleosome dynamics. Protein and DNA contributions in the chiral transition of the tetrasome, the histone (H3-H4)2 tetramer-DNA particle. J. Mol. Biol.291, 815–841 (1999). ArticleCASPubMed Google Scholar
Hackett, J. D. et al. Insights into a dinoflagellate genome through expressed sequence tag analysis. BMC Genomics6, 80 (2005). ArticlePubMedPubMed Central Google Scholar
Malik, H. S. & Henikoff, S. Phylogenomics of the nucleosome. Nature Struct. Biol.10, 882–891 (2003). ArticleCASPubMed Google Scholar
Dawson, S. C., Sagolla, M. S. & Cande, W. Z. The CenH3 histone variant defines centromeres in Giardia intestinalis. Chromosoma116, 175–184 (2007). ArticleCASPubMed Google Scholar
Talbert, P. B., Masuelli, R., Tyagi, A. P., Comai, L. & Henikoff, S. Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell14, 1053–1066 (2002). ArticleCASPubMedPubMed Central Google Scholar
Earnshaw, W. C. & Rothfield, N. Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma91, 313–321 (1985). ArticleCASPubMed Google Scholar
Malik, H. S., Vermaak, D. & Henikoff, S. Recurrent evolution of DNA-binding motifs in the Drosophila centromeric histone. Proc. Natl Acad. Sci. USA.99, 1449–1454 (2002). ArticleCASPubMedPubMed Central Google Scholar
Wieland, G., Orthaus, S., Ohndorf, S., Diekmann, S. & Hemmerich, P. Functional complementation of human centromere protein A (CENP-A) by Cse4p from Saccharomyces cerevisiae. Mol. Cell. Biol.24, 6620–6630 (2004). ArticleCASPubMedPubMed Central Google Scholar
Dalal, Y., Wang, H., Lindsay, S. & Henikoff, S. Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells. PLoS Biol.5, e218 (2007). ArticleCASPubMedPubMed Central Google Scholar
Mizuguchi, G., Xiao, H., Wisniewski, J., Smith, M. M. & Wu, C. Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes. Cell129, 1153–1164 (2007). ArticleCASPubMed Google Scholar
Camahort, R. et al. Cse4 is part of an octameric nucleosome in budding yeast. Mol. Cell35, 794–805 (2009). Together with references 30 and 32, this paper proposes mutually exclusive models for the CenH3 histone core; the correct model needs to accommodate the result of reference 31, which shows that CenH3 DNA wraps around the core in a right-handed direction. ArticleCASPubMedPubMed Central Google Scholar
Westermann, S. et al. Architecture of the budding yeast kinetochore reveals a conserved molecular core. J. Cell Biol.163, 215–222 (2003). ArticleCASPubMedPubMed Central Google Scholar
Conde E Silva, N. et al. CENP-A-containing nucleosomes: easier disassembly versus exclusive centromeric localization. J. Mol. Biol.370, 555–573 (2007). ArticleCASPubMed Google Scholar
Dalal, Y., Furuyama, T., Vermaak, D. & Henikoff, S. Structure, dynamics, and evolution of centromeric nucleosomes. Proc. Natl Acad. Sci. USA104, 15974–15981 (2007). ArticlePubMedPubMed Central Google Scholar
Cui, B., Liu, Y. & Gorovsky, M. A. Deposition and function of histone H3 variants in Tetrahymena thermophila. Mol. Cell. Biol.26, 7719–7730 (2006). Mutational analysis of canonical histone H3 and H3.3 shows that H3 is not essential in ciliate development, and H3.3 is not essential for transcription but is required in germline micronuclei. ArticleCASPubMedPubMed Central Google Scholar
Ahmad, K. & Henikoff, S. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell9, 1191–1200 (2002). ArticleCASPubMed Google Scholar
Tagami, H., Ray-Gallet, D., Almouzni, G. & Nakatani, Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell116, 51–61 (2004). ArticleCASPubMed Google Scholar
Polo, S. E., Roche, D. & Almouzni, G. New histone incorporation marks sites of UV repair in human cells. Cell127, 481–493 (2006). ArticleCASPubMed Google Scholar
Mousson, F., Ochsenbein, F. & Mann, C. The histone chaperone Asf1 at the crossroads of chromatin and DNA checkpoint pathways. Chromosoma116, 79–93 (2007). ArticleCASPubMed Google Scholar
Henikoff, S. Nucleosome destabilization in the epigenetic regulation of gene expression. Nature Rev. Genet.9, 15–26 (2008). ArticleCASPubMed Google Scholar
Schwartz, B. E. & Ahmad, K. Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev.19, 804–814 (2005). ArticleCASPubMedPubMed Central Google Scholar
Hake, S. B. & Allis, C. D. Histone H3 variants and their potential role in indexing mammalian genomes: the “H3 barcode hypothesis”. Proc. Natl Acad. Sci. USA103, 6428–6435 (2006). ArticleCASPubMedPubMed Central Google Scholar
Loyola, A., Bonaldi, T., Roche, D., Imhof, A. & Almouzni, G. PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol. Cell24, 309–316 (2006). ArticleCASPubMed Google Scholar
Ng, R. K. & Gurdon, J. B. Epigenetic memory of an active gene state depends on histone H3.3 incorporation into chromatin in the absence of transcription. Nature Cell Biol.10, 102–109 (2008). Using aXenopus laevisnuclear transplantation assay, the authors show that epigenetic memory of a gene expression state is retained through 12 rounds of cell division without transcription and depends on the presence of wild-type H3.3 but not H3. ArticleCASPubMed Google Scholar
van der Heijden, G. W. et al. Chromosome-wide nucleosome replacement and H3.3 incorporation during mammalian meiotic sex chromosome inactivation. Nature Genet.39, 251–258 (2007). ArticleCASPubMed Google Scholar
Ooi, S. L., Priess, J. R. & Henikoff, S. Histone H3.3 variant dynamics in the germline of Caenorhabditis elegans. PLoS Genet.2, e97 (2006). ArticleCASPubMedPubMed Central Google Scholar
Hodl, M. & Basler, K. Transcription in the absence of histone H3.3. Curr. Biol.19, 1221–1226 (2009). ArticleCASPubMed Google Scholar
Sakai, A., Schwartz, B. E., Goldstein, S. & Ahmad, K. Transcriptional and developmental functions of the H3.3 histone variant in Drosophila. Curr. Biol.19, 1816–1820 (2009). References 51 and 52 show that H3.3 is dispensible for normalDrosophiladevelopment but is essential in the germ line, and reference 52 shows that the germline function does not require methylation of H3.3K4 or phosphorylation of Ser31. ArticleCASPubMedPubMed Central Google Scholar
Schulmeister, A., Schmid, M. & Thompson, E. M. Phosphorylation of the histone H3.3 variant in mitosis and meiosis of the urochordate Oikopleura dioica. Chromosome Res.15, 189–201 (2007). ArticleCASPubMed Google Scholar
Wong, L. H. et al. Histone H3.3 incorporation provides a unique and functionally essential telomeric chromatin in embryonic stem cells. Genome Res.19, 404–414 (2009). ArticleCASPubMedPubMed Central Google Scholar
Adam, M., Robert, F., Larochelle, M. & Gaudreau, L. H2A.Z is required for global chromatin integrity and for recruitment of RNA polymerase II under specific conditions. Mol. Cell. Biol.21, 6270–6279 (2001). ArticleCASPubMedPubMed Central Google Scholar
Hardy, S. et al. The euchromatic and heterochromatic landscapes are shaped by antagonizing effects of transcription on H2A.Z deposition. PLoS Genet.5, e1000687 (2009). ArticleCASPubMedPubMed Central Google Scholar
Zofall, M. et al. Histone H2A.Z cooperates with RNAi and heterochromatin factors to suppress antisense RNAs. Nature461, 419–422 (2009). ArticleCASPubMedPubMed Central Google Scholar
Creyghton, M. P. et al. H2AZ is enriched at polycomb complex target genes in ES cells and is necessary for lineage commitment. Cell135, 649–661 (2008). Reports a striking correlation between H2A.Z and Polycomb group protein locations in mouse embryonic stem cells but not in their differentiated descendants, suggesting that H2A.Z plays a key role in maintaining pluripotency. ArticleCASPubMedPubMed Central Google Scholar
Zilberman, D., Coleman-Derr, D., Ballinger, T. & Henikoff, S. Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature456, 125–129 (2008). InA. thaliana, H2A.Z and DNA methylation are found to be quantitatively anti-correlated, and mutants in either one result in opposite changes in the other. ArticleCASPubMedPubMed Central Google Scholar
Thakar, A. et al. H2A.Z and H3.3 histone variants affect nucleosome structure: biochemical and biophysical studies. Biochemistry48, 10852–10857 (2009). In contrast to thein vivoresults of reference 68, these authors were unable to detect significant instability of H2A.Z and H3.3 nucleosomesin vitro. ArticleCASPubMed Google Scholar
Goldman, J. A., Garlick, J. D. & Kingston, R. E. Chromatin remodeling by imitation switch (ISWI) class ATP-dependent remodelers is stimulated by histone variant H2A. Z. J. Biol. Chem.285, 4645–4651 (2009). This paper shows that H2A.Z nucleosomes are preferentially associated with nucleosome remodellers, with an enhanced activity of ISWI family remodellers that is dependent on the H2A.Z extended acidic patch. ArticleCASPubMedPubMed Central Google Scholar
Eirin-Lopez, J. M., Gonzalez-Romero, R., Dryhurst, D., Ishibashi, T. & Ausio, J. 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 (2009). ArticleCASPubMedPubMed Central Google Scholar
Faast, R. et al. Histone variant H2A.Z is required for early mammalian development. Curr. Biol.11, 1183–1187 (2001). ArticleCASPubMed Google Scholar
March-Diaz, R. et al. Histone H2A.Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis. Plant J.53, 475–487 (2008). ArticleCASPubMed Google Scholar
Ishibashi, T. et al. Acetylation of vertebrate H2A.Z and its effect on the structure of the nucleosome. Biochemistry48, 5007–5017 (2009). ArticleCASPubMed Google Scholar
Viens, A. et al. Analysis of human histone H2AZ deposition in vivo argues against its direct role in epigenetic templating mechanisms. Mol. Cell. Biol.26, 5325–5335 (2006). ArticleCASPubMedPubMed Central Google Scholar
Zhang, H., Roberts, D. N. & Cairns, B. R. Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell123, 219–231 (2005). ArticleCASPubMedPubMed Central Google Scholar
Jin, C. et al. H3.3/H2A.Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions. Nature Genet.41, 941–945 (2009). Reports that nucleosomes containing both H3.3 and H2A.Z occupy promoters and insulator elementsin vivoand are highly unstable. ArticleCASPubMed Google Scholar
Mavrich, T. N. et al. Nucleosome organization in the Drosophila genome. Nature453, 358–362 (2008). The authors mapped a large collection ofDrosophilaH2Av (H2A.Z) nucleosomes and found that where RNA polymerase II is paused just downstream of the transcriptional start site, the +1 H2A.Z nucleosome is positioned another 10 bp (1 rotational turn) further downstream, suggesting a role for H2A.Z in pausing polymerase. ArticleCASPubMedPubMed Central Google Scholar
Jiang, C. & Pugh, B. F. Nucleosome positioning and gene regulation: advances through genomics. Nature Rev. Genet.10, 161–172 (2009). ArticleCASPubMed Google Scholar
Gevry, N., Chan, H. M., Laflamme, L., Livingston, D. M. & Gaudreau, L. p21 transcription is regulated by differential localization of histone H2A. Z. Genes Dev.21, 1869–1881 (2007). ArticleCASPubMedPubMed Central Google Scholar
Choi, J., Heo, K. & An, W. Cooperative action of TIP48 and TIP49 in H2A.Z exchange catalyzed by acetylation of nucleosomal H2A. Nucleic Acids Res.37, 5993–6007 (2009). ArticleCASPubMedPubMed Central Google Scholar
Fan, J. Y., Gordon, F., Luger, K., Hansen, J. C. & Tremethick, D. J. The essential histone variant H2A.Z regulates the equilibrium between different chromatin conformational states. Nature Struct. Biol.9, 172–176 (2002). ArticleCASPubMed Google Scholar
Deal, R. B., Topp, C. N., McKinney, E. C. & Meagher, R. B. Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A. Z. Plant Cell19, 74–83 (2007). ArticleCASPubMedPubMed Central Google Scholar
Ball, M. P. et al. Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. Nature Biotechnol.27, 361–368 (2009). ArticleCAS Google Scholar
Fan, J. Y., Rangasamy, D., Luger, K. & Tremethick, D. J. H2A.Z alters the nucleosome surface to promote HP1α-mediated chromatin fiber folding. Mol. Cell16, 655–661 (2004). ArticleCASPubMed Google Scholar
Swaminathan, J., Baxter, E. M. & Corces, V. G. The role of histone H2Av variant replacement and histone H4 acetylation in the establishment of Drosophila heterochromatin. Genes Dev.19, 65–76 (2005). ArticleCASPubMedPubMed Central Google Scholar
Hanai, K., Furuhashi, H., Yamamoto, T., Akasaka, K. & Hirose, S. RSF governs silent chromatin formation via histone H2Av replacement. PLoS Genet.4, e1000011 (2008). ArticleCASPubMedPubMed Central Google Scholar
van Attikum, H. & Gasser, S. M. Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol.19, 207–217 (2009). ArticleCASPubMed Google Scholar
Shechter, D. et al. 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. USA106, 749–754 (2009). ArticlePubMedPubMed Central Google Scholar
Xiao, A. et al. WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity. Nature457, 57–62 (2009). ArticleCASPubMed Google Scholar
Fernandez-Capetillo, O. et al. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev. Cell.4, 497–508 (2003). ArticleCASPubMed Google Scholar
Turner, J. M. et al. Silencing of unsynapsed meiotic chromosomes in the mouse. Nature Genet.37, 41–47 (2005). ArticleCASPubMed Google Scholar
Van Doninck, K. et al. Phylogenomics of unusual histone H2A variants in Bdelloid rotifers. PLoS Genet.5, e1000401 (2009). Shows that bdelloid rotifers, which periodically undergo severe dessication resulting in massive DNA breaks, have replaced H2A.X, which recruits DNA repair machinery in other eukaryotes, with novel H2A variants that might have evolved to facilitate DNA repair under dessicating conditions. ArticleCASPubMedPubMed Central Google Scholar
Marzluff, W. F., Gongidi, P., Woods, K. R., Jin, J. & Maltais, L. J. The human and mouse replication-dependent histone genes. Genomics80, 487–498 (2002). ArticleCASPubMed Google Scholar
Marzluff, W. F., Sakallah, S. & Kelkar, H. The sea urchin histone gene complement. Dev. Biol.300, 308–320 (2006). ArticleCASPubMed Google Scholar
Siegel, T. N. et al. Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei. Genes Dev.23, 1063–1076 (2009). Reports that trypanosomes have two versions of each of the four core histones, which form unique combinations at transcription initiation sites and termination sites. This suggests the existence of an ancestral mode of gene regulation based on histone variants and an ancient function for H2A.Z in marking promoters. ArticleCASPubMedPubMed Central Google Scholar
Bernhard, D. & Schlegel, M. Evolution of histone H4 and H3 genes in different ciliate lineages. J. Mol. Evol.46, 344–354 (1998). ArticleCASPubMed Google Scholar
Katz, L. A., Bornstein, J. G., Lasek-Nesselquist, E. & Muse, S. V. Dramatic diversity of ciliate histone H4 genes revealed by comparisons of patterns of substitutions and paralog divergences among eukaryotes. Mol. Biol. Evol.21, 555–562 (2004). ArticleCASPubMed Google Scholar
Gladyshev, E. & Meselson, M. Extreme resistance of bdelloid rotifers to ionizing radiation. Proc. Natl Acad. Sci. USA105, 5139–5144 (2008). ArticlePubMedPubMed Central Google Scholar
Pehrson, J. R. & Fuji, R. N. Evolutionary conservation of histone macroH2A subtypes and domains. Nucleic Acids Res.26, 2837–2842 (1998). ArticleCASPubMedPubMed Central Google Scholar
Chadwick, B. P. & Willard, H. F. Histone H2A variants and the inactive X chromosome: identification of a second macroH2A variant. Hum. Mol. Genet.10, 1101–1113 (2001). ArticleCASPubMed Google Scholar
Costanzi, C. & Pehrson, J. R. MACROH2A2, a new member of the MARCOH2A core histone family. J. Biol. Chem.276, 21776–21784 (2001). ArticleCASPubMed Google Scholar
Abbott, D. W., Chadwick, B. P., Thambirajah, A. A. & Ausio, J. Beyond the Xi: macroH2A chromatin distribution and post-translational modification in an avian system. J. Biol. Chem.280, 16437–16445 (2005). ArticleCASPubMed Google Scholar
Doyen, C. M. et al. Mechanism of polymerase II transcription repression by the histone variant macroH2A. Mol. Cell. Biol.26, 1156–1164 (2006). ArticleCASPubMedPubMed Central Google Scholar
Chakravarthy, S. & Luger, K. The histone variant macro-H2A preferentially forms “hybrid nucleosomes”. J. Biol. Chem.281, 25522–25531 (2006). ArticleCASPubMed Google Scholar
Nusinow, D. A. et al. Poly(ADP-ribose) polymerase 1 is inhibited by a histone H2A variant, MacroH2A, and contributes to silencing of the inactive X chromosome. J. Biol. Chem.282, 12851–12859 (2007). ArticleCASPubMed Google Scholar
Timinszky, G. et al. A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nature Struct. Mol. Biol.16, 923–929 (2009). ArticleCAS Google Scholar
Ouararhni, K. et al. The histone variant mH2A1.1 interferes with transcription by down-regulating PARP-1 enzymatic activity. Genes Dev.20, 3324–3336 (2006). ArticleCASPubMedPubMed Central Google Scholar
Buschbeck, M. et al. The histone variant macroH2A is an epigenetic regulator of key developmental genes. Nature Struct. Mol. Biol. (2009). This paper shows that mH2A serves as a repressive mark on autosomes, overlapping with Polycomb repressor complex 2 sites and contributing to regulation of homeobox genes during neuronal differentiation.
Eirin-Lopez, J. M., Ishibashi, T. & Ausio, J. H2A.Bbd: a quickly evolving hypervariable mammalian histone that destabilizes nucleosomes in an acetylation-independent way. FASEB J.22, 316–326 (2008). ArticleCASPubMed Google Scholar
Chadwick, B. P. & Willard, H. F. A novel chromatin protein, distantly related to histone H2A, is largely excluded from the inactive X chromosome. J. Cell Biol.152, 375–384 (2001). ArticleCASPubMedPubMed Central Google Scholar
Okuwaki, M., Kato, K., Shimahara, H., Tate, S. & Nagata, K. Assembly and disassembly of nucleosome core particles containing histone variants by human nucleosome assembly protein I. Mol. Cell. Biol.25, 10639–10651 (2005). ArticleCASPubMedPubMed Central Google Scholar
Zhou, J., Fan, J. Y., Rangasamy, D. & Tremethick, D. J. The nucleosome surface regulates chromatin compaction and couples it with transcriptional repression. Nature Struct. Mol. Biol.14, 1070–1076 (2007). ArticleCAS Google Scholar
Yi, H. et al. Constitutive expression exposes functional redundancy between the Arabidopsis histone H2A gene HTA1 and other H2A gene family members. Plant Cell18, 1575–1589 (2006). ArticleCASPubMedPubMed Central Google Scholar
Bergmuller, E., Gehrig, P. M. & Gruissem, W. Characterization of post-translational modifications of histone H2B-variants isolated from Arabidopsis thaliana. J. Proteome Res.6, 3655–3668 (2007). ArticleCASPubMed Google Scholar
Lindsey, G. G., Orgeig, S., Thompson, P., Davies, N. & Maeder, D. L. Extended C-terminal tail of wheat histone H2A interacts with DNA of the “linker” region. J. Mol. Biol.218, 805–813 (1991). ArticleCASPubMed Google Scholar
Green, G. R. Phosphorylation of histone variant regions in chromatin: unlocking the linker? Biochem. Cell Biol.79, 275–287 (2001). ArticleCASPubMed Google Scholar
Eirin-Lopez, J. M. & Ausio, J. Origin and evolution of chromosomal sperm proteins. Bioessays31, 1062–1070 (2009). ArticleCASPubMed Google Scholar
Palmer, D. K., O'Day, K. & Margolis, R. L. The centromere specific histone CENP-A is selectively retained in discrete foci in mammalian sperm nuclei. Chromosoma100, 32–36 (1990). ArticleCASPubMed Google Scholar
Gatewood, J. M., Cook, G. R., Balhorn, R., Schmid, C. W. & Bradbury, E. M. Isolation of four core histones from human sperm chromatin representing a minor subset of somatic histones. J. Biol. Chem.265, 20662–20666 (1990). CASPubMed Google Scholar
Ueda, K. et al. Unusual core histones specifically expressed in male gametic cells of Lilium longiflorum. Chromosoma108, 491–500 (2000). ArticleCASPubMed Google Scholar
Ingouff, M., Hamamura, Y., Gourgues, M., Higashiyama, T. & Berger, F. Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr. Biol.17, 1032–1037 (2007). ArticleCASPubMed Google Scholar
Talbert, P. B. & Henikoff, S. Chromatin-based transcriptional punctuation. Genes Dev.23, 1037–1041 (2009). ArticleCASPubMed Google Scholar
Aggarwal, B. D. & Calvi, B. R. Chromatin regulates origin activity in Drosophila follicle cells. Nature430, 372–376 (2004). ArticleCASPubMed Google Scholar
Miotto, B. & Struhl, K. HBO1 histone acetylase is a coactivator of the replication licensing factor Cdt1. Genes Dev.22, 2633–2638 (2008). ArticleCASPubMedPubMed Central Google Scholar
Ren, Q. & Gorovsky, M. A. Histone H2A.Z acetylation modulates an essential charge patch. Mol. Cell7, 1329–1335 (2001). ArticleCASPubMed Google Scholar
Millar, C. B., Xu, F., Zhang, K. & Grunstein, M. Acetylation of H2AZ Lys 14 is associated with genome-wide gene activity in yeast. Genes Dev.20, 711–722 (2006). ArticleCASPubMedPubMed Central Google Scholar
Tanabe, M. et al. Activation of facultatively silenced Drosophila loci associates with increased acetylation of histone H2AvD. Genes Cells13, 1279–1288 (2008). ArticleCASPubMed Google Scholar
Wan, Y. et al. Role of the histone variant H2A.Z/Htz1p in TBP recruitment, chromatin dynamics, and regulated expression of oleate-responsive genes. Mol. Cell. Biol.29, 2346–2358 (2009). ArticleCASPubMedPubMed Central Google Scholar
de Napoles, M. et al. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev. Cell.7, 663–676 (2004). ArticleCASPubMed Google Scholar
Sarcinella, E., Zuzarte, P. C., Lau, P. N., Draker, R. & Cheung, P. Monoubiquitylation of H2A.Z distinguishes its association with euchromatin or facultative heterochromatin. Mol. Cell. Biol.27, 6457–6468 (2007). ArticleCASPubMedPubMed Central Google Scholar
Stock, J. K. et al. Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nature Cell Biol.9, 1428–1435 (2007). ArticleCASPubMed Google Scholar
Wang, H. et al. Role of histone H2A ubiquitination in Polycomb silencing. Nature431, 873–878 (2004). ArticleCASPubMed Google Scholar
Sogin, M. L. & Silberman, J. D. Evolution of the protists and protistan parasites from the perspective of molecular systematics. Int. J. Parasitol.28, 11–20 (1998). ArticleCASPubMed Google Scholar
Martinez-Calvillo, S., Nguyen, D., Stuart, K. & Myler, P. J. Transcription initiation and termination on Leishmania major chromosome 3. Eukaryot. Cell.3, 506–517 (2004). ArticleCASPubMedPubMed Central Google Scholar
Vanacova, S., Liston, D. R., Tachezy, J. & Johnson, P. J. Molecular biology of the amitochondriate parasites, Giardia intestinalis, Entamoeba histolytica and Trichomonas vaginalis. Int. J. Parasitol.33, 235–255 (2003). ArticleCASPubMed Google Scholar
Lowell, J. E. & Cross, G. A. A variant histone H3 is enriched at telomeres in Trypanosoma brucei. J. Cell. Sci.117, 5937–5947 (2004). ArticleCASPubMed Google Scholar
Ghosh, S. & Klobutcher, L. A. A development-specific histone H3 localizes to the developing macronucleus of Euplotes. Genesis26, 179–188 (2000). ArticleCASPubMed Google Scholar
Cui, B. & Gorovsky, M. A. Centromeric histone H3 is essential for vegetative cell division and for DNA elimination during conjugation in Tetrahymena thermophila. Mol. Cell. Biol.26, 4499–4510 (2006). ArticleCASPubMedPubMed Central Google Scholar
Zeitlin, S. G. et al. Double-strand DNA breaks recruit the centromeric histone CENP-A. Proc. Natl Acad. Sci. USA106, 15762–15767 (2009). ArticlePubMedPubMed Central Google Scholar
Cervantes, M. D., Xi, X., Vermaak, D., Yao, M. C. & Malik, H. S. The CNA1 histone of the ciliate Tetrahymena thermophila is essential for chromosome segregation in the germline micronucleus. Mol. Biol. Cell17, 485–497 (2006). ArticleCASPubMedPubMed Central Google Scholar
Iribarren, C., Morin, V., Puchi, M. & Imschenetzky, M. Sperm nucleosomes disassembly is a requirement for histones proteolysis during male pronucleus formation. J. Cell. Biochem.103, 447–455 (2008). ArticleCASPubMed Google Scholar
Govin, J. et al. Pericentric heterochromatin reprogramming by new histone variants during mouse spermiogenesis. J. Cell Biol.176, 283–294 (2007). Describes new H2A variants enriched in pericentric heterochromatin in spermatids that form sub-nucleosomal chromatin particles lacking H3 and H4. ArticleCASPubMedPubMed Central Google Scholar
Tachiwana, H., Osakabe, A., Kimura, H. & Kurumizaka, H. Nucleosome formation with the testis-specific histone H3 variant, H3t, by human nucleosome assembly proteins in vitro. Nucleic Acids Res.36, 2208–2218 (2008). ArticleCASPubMedPubMed Central Google Scholar
Li, A. et al. Characterization of nucleosomes consisting of the human testis/sperm-specific histone H2B variant (hTSH2B). Biochemistry44, 2529–2535 (2005). ArticleCASPubMed Google Scholar
Churikov, D. et al. Novel human testis-specific histone H2B encoded by the interrupted gene on the X chromosome. Genomics84, 745–756 (2004). ArticleCASPubMed Google Scholar
Boulard, M. et al. 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 (2006). ArticleCASPubMedPubMed Central Google Scholar
Aul, R. B. & Oko, R. J. 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 (2002). ArticleCASPubMed Google Scholar
Syed, S. H. et al. The incorporation of the novel histone variant H2AL2 confers unusual structural and functional properties of the nucleosome. Nucleic Acids Res.37, 4684–4695 (2009). ArticleCASPubMedPubMed Central Google Scholar
Gaucher, J. et al. From meiosis to postmeiotic events: the secrets of histone disappearance. FEBS J.277, 509–604 (2009). Google Scholar