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The Actin Family Member Arp6 and the Histone Variant H2A.Z Are Required

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The Actin Family Member Arp6 and the Histone Variant H2A.Z Are Required Short Report 3739 The actin family member Arp6 and the histone variant H2A.Z are required for spatial positioning of chromatin in chicken cell nuclei Eri Ohfuchi Maruyama1,*, Tetsuya Hori2,*, Hideyuki Tanabe3,`, Hiroshi Kitamura1,*, Ryo Matsuda1, Shigenobu Tone4, Pavel Hozak5, Felix A. Habermann6, Johann von Hase7, Christoph Cremer7, Tatsuo Fukagawa2 and Masahiko Harata1,` 1Laboratory of Molecular Biology, Graduate School of Agricultural Science, Tohoku University, Tsutsumidori-Amamiyamachi 1-1, Aoba-ku, Sendai 981-8555, Japan 2Department of Molecular Genetics, National Institute of Genetics and The Graduate University for Advanced Studies, Shizuoka 411-8540, Japan 3Department of Evolutionary Studies of Biosystems, School of Advanced Sciences, The Graduate University for Advanced Studies (Sokendai), Kanagawa 240-0193, Japan 4Department of Biochemistry, Kawasaki Medical School, Kurashiki 701-0192, Japan 5Department of Biology of the Cell Nucleus, Institute of Molecular Genetics, AS CR, v.v.i., Prague 4 14220, Czech Republic 6Ludwig-Maximilians-University, 80539 Munich, Germany 7Institute of Molecular Biology gGmbH (IMB), Ackermannweg 4, 55128 Mainz, Germany *These authors contributed equally to this work `Authors for correspondence ([email protected]; [email protected]) Accepted 3 April 2012 Journal of Cell Science 125, 3739–3744 ß 2012. Published by The Company of Biologists Ltd doi: 10.1242/jcs.103903 Summary The spatial organization of chromatin in the nucleus contributes to genome function and is altered during the differentiation of normal and tumorigenic cells. Although nuclear actin-related proteins (Arps) have roles in the local alteration of chromatin structure, it is unclear whether they are involved in the spatial positioning of chromatin. In the interphase nucleus of vertebrate cells, gene-dense and gene-poor chromosome territories (CTs) are located in the center and periphery, respectively. We analyzed chicken DT40 cells in which Arp6 had been knocked out conditionally, and showed that the radial distribution of CTs was impaired in these knockout cells. Arp6 is an essential component of the SRCAP chromatin remodeling complex, which deposits the histone variant H2A.Z into chromatin. The redistribution of CTs was also observed in H2A.Z-deficient cells for gene-rich microchromosomes, but to lesser extent for gene-poor macrochromosomes. These results indicate that Arp6 and H2A.Z contribute to the radial distribution of CTs through different Journal of Cell Science mechanisms. Microarray analysis suggested that the localization of chromatin to the nuclear periphery per se is insufficient for the repression of most genes. Key words: Actin-related protein, Histone variant, Nuclear organization, Chromosome territory, Gene expression Introduction CTs in the interphase nucleus usually have a radial distribution, in Various chromatin remodeling and histone modification which each CT is part of a polarized arrangement from the center complexes play key roles with respect to the organization of to the periphery of the nucleus (Boyle et al., 2001; Croft et al., chromatin. Members of the actin family, which consists of actin 1999; Sadoni et al., 1999). The position of CTs within this and actin-related proteins (Arps), are essential components of polarized arrangement is correlated with gene density (Bridger and some of these complexes (Chen and Shen, 2007; Dion et al., Bickmore, 1998; Cremer and Cremer, 2001; Gilbert et al., 2005). 2010; Meagher et al., 2009; Ohfuchi et al., 2006; Oma and In chicken cells, the territories of gene-rich microchromosomes Harata, 2011). Arp6 is predominantly localized in the nucleus and gene-poor macrochromosomes are positioned in the center and identified as an essential component of the SWR1/SRCAP and periphery of the nucleus, respectively. The physiological chromatin remodeling complex (Mizuguchi et al., 2004; Wu et al., significance of the radial distribution of CTs is supported by 2005; Yoshida et al., 2010), which catalyzes the replacement of evidence that their arrangement is specific to cell and tissue types, nucleosomal histone H2A with the variant H2A.Z both in yeasts and is altered during development (Meaburn and Misteli, 2007; and vertebrates (Mizuguchi et al., 2004; Ruhl et al., 2006; Wong Meshorer and Misteli, 2006), and in multiple types of cancer cells et al., 2007). (Cremer et al., 2003; Meaburn and Misteli, 2008; Wiech et al., The spatial arrangement of chromatin in the nucleus adds a 2005). further level of organization to the physical structure of the Despite many recent studies of chromatin organization, genome. In vertebrates, functional regions of the genome are information about the spatial arrangement of chromatin in the located in spatially compartmentalized regions of the nucleus, nucleus remains limited. Although Arps are suggested to be and interphase chromosomes form chromosome territories (CTs) required for higher levels of chromatin organization (Chuang that occupy discrete domains (Cremer et al., 2006; Misteli, 2007). et al., 2006; Hu et al., 2008; Lee et al., 2007; Yoshida et al., 3740 Journal of Cell Science 125 (16) 2010), it is still unclear about their function in the spatial microchromosomes (green) formed a continuous cluster that was positioning of CTs in the nucleus. located in the center of the nucleus in wild-type and control (ARP6-KO without tet) cells (Fig. 1, left panels). In contrast, in Results and Discussion Arp6-deficient cells, the macro- and microchromosome CTs were Impairment of the radial distribution of chromosome dispersed discontinuously and their central and peripheral territories in Arp6-deficient cells distributions had disappeared (Fig. 1, right panels). Although To investigate the cellular function of Arp6, we constructed and less than 10% of the wild-type and control cells had the impaired analyzed conditional knockout (KO) cells for Arp6 using the radial distribution, the percentages increased to 58% and 89% in chicken DT40 B cell line (supplementary material Fig. S1A). In Arp6-deficient cells (Fig. 1). This result indicates that Arp6 is the KO cells, the expression of the ARP6 gene was controlled by required for the radial distribution of CTs. a tetracycline (tet)-repressible promoter. Northern and western The radial distributions of macro- and microchromosomes in the blot analyses showed that the expression of Arp6 in ARP6-KO nuclei were analyzed quantitatively and statistically (Tanabe et al., cells was reduced upon exposure to tet, and Arp6 protein became 2002a; Tanabe et al., 2002b) (Fig. 2). On each graph, the undetectable by 96 hr after the addition of tet (supplementary horizontal axis shows the relative radii of the nuclear shells, and material Fig. S1B,C). Consistently, the ARP6-KO cells treated the positions 0% and 100% correspond to the center and periphery with tet proliferated as well as the cells not treated with tet until of the nucleus, respectively. The vertical axes represent the 96 hr (supplementary material Fig. S1D). FACS analysis revealed normalized relative DNA content of painted CTs in a given area. In that the distribution of Arp6-deficient cells at each stage of the the Arp6-deficient cells (Fig. 2), the macrochromosomes shifted cell cycle was not significantly changed in comparison with wild- inwards whereas the microchromosomes shifted outwards as type cells, and that the number of dead cells did not significantly compared to wild-type cells (Fig. 2). The Mann–Whitney U-test increase until 144 hr after the addition of tet (supplementary showed that these differences were statistically significant material Fig. S2). (P,0.01). Chicken chromosomes are classified on the basis of their size We previously found that the budding yeast Arp6 is required into macrochromosomes and microchromosomes, which are for the spatial arrangement of chromatin in the nucleus (Yoshida composed of gene-poor and gene-rich chromatin, respectively et al., 2010). Therefore, it is suggested that the contribution of (Habermann et al., 2001; Tanabe et al., 2002a; Tanabe et al., Arp6 to the higher order arrangement of chromatin in the nucleus 2002b). We used the three-dimensional fluorescence in situ is evolutionarily conserved. hybridization (3D-FISH) to analyze the spatial distribution of macro- and microchromosome territories. These two types of H2A.Z is also required for the radial distribution of CTs chromosomes were visualized using two pools of probes, one To explain why Arp6-deficient cells impair the radial distribution designed to detect macrochromosomes (chromosomes 1–8 and Z) of CTs, we focused on the histone variant H2A.Z, because we and the other to detect 21 pairs of microchromosomes. The pools recently showed that Arp6 has an essential function in the of probes were hybridized with three-dimensionally preserved SRCAP complex, which is required for the deposition of H2A.Z nuclei. As reported previously (Habermann et al., 2001; Tanabe (Matsuda et al., 2010). Vertebrate H2A.Z has two isoforms Journal of Cell Science et al., 2002a; Tanabe et al., 2002b), the macrochromosomes (red) (H2A.Z-1 and H2A.Z-2) that are encoded by two individual were found predominantly at the periphery of the nucleus, and the genes. In Arp6-deficient cells, the deposition of both H2A.Z Fig. 1. Impairment of the radial distribution of chromosomes in Arp6-deficient cells. (Upper panels) 3D-FISH was performed on structurally preserved cell nuclei using probes for macrochromosomes (red) and for microchromosomes (green). Representative
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