The Mi-2/NuRD complex associates with pericentromeric heterochromatin during S phase in rapidly proliferating lymphoid cells

Chromosoma - Tập 118 - Trang 445-457 - 2009
Lisa Helbling Chadwick1, Brian P. Chadwick2,3, David L. Jaye4, Paul A. Wade1
1Laboratory of Molecular Carcinogenesis, National Institute of Environmental Health Sciences, Research Triangle Park, USA
2Institute for Genome Sciences and Policy, Duke University, Durham, USA
3Department of Cell Biology, Duke University, Durham, USA
4Department of Pathology and Laboratory Medicine, Emory University School of Medicine, Atlanta, USA

Tóm tắt

Chromosomal replication results in the duplication not only of DNA sequence but also of the patterns of histone modification, DNA methylation, and nucleoprotein structure that constitute epigenetic information. Pericentromeric heterochromatin in human cells is characterized by unique patterns of histone and DNA modification. Here, we describe association of the Mi-2/NuRD complex with specific segments of pericentromeric heterochromatin consisting of Satellite II/III DNA located on human chromosomes 1, 9, and 16 in some but not all cell types. This association is linked in part to DNA replication and chromatin assembly and may suggest a role in these processes. Mi-2/NuRD accumulation is independent of Polycomb association and is characterized by a unique pattern of histone modification. We propose that Mi-2/NuRD constitutes an enzymatic component of a pathway for assembly and maturation of chromatin utilized by rapidly proliferating lymphoid cells for replication of constitutive heterochromatin.

Tài liệu tham khảo

Berger R, Busson-Le Coniat M (1999) Centric and pericentric chromosome rearrangements in hematopoietic malignancies. Leukemia 13:671–678 Blanco-Betancourt CE, Moncla A, Milili M, Jiang YL, Viegas-Pequignot EM, Roquelaure B, Thuret I, Schiff C (2004) Defective B-cell-negative selection and terminal differentiation in the ICF syndrome. Blood 103:2683–2690 Bowen NJ, Fujita N, Kajita M, Wade PA (2004) Mi-2/NuRD: multiple complexes for many purposes. Biochim Biophys Acta 1677:52–57 Brown KE, Guest SS, Smale ST, Hahm K, Merkenschlager M, Fisher AG (1997) Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell 91:845–854 Brown KE, Baxter J, Graf D, Merkenschlager M, Fisher AG (1999) Dynamic repositioning of genes in the nucleus of lymphocytes preparing for cell division. Mol Cell 3:207–217 Busson-Le Coniat M, Salomon-Nguyen F, Dastugue N, Maarek O, Lafage-Pochitaloff M, Mozziconacci MJ, Baranger L, Brizard F, Radford I, Jeanpierre M, Bernard OA, Berger R (1999) Fluorescence in situ hybridization analysis of chromosome 1 abnormalities in hematopoietic disorders: rearrangements of DNA Satellite II and new recurrent translocations. Leukemia 13:1975–1981 Cajal SRy (1903) Un sencillo metodo de coloracion seletiva del reticulo protoplasmatico y sus efectos en los diversos organos nerviosos de vertebrados e invertebrados. Trab Lab Invest Biol 2:129–221 Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science (New York) NY 298:1039–1043 Dimitrova DS, Berezney R (2002) The spatio-temporal organization of DNA replication sites is identical in primary, immortalized and transformed mammalian cells. J Cell Sci 115:4037–4051 Feng Q, Zhang Y (2001) The MeCP1 complex represses transcription through preferential binding, remodeling, and deacetylating methylated nucleosomes. Genes Dev 15:827–832 Fox MH, Arndt-Jovin DJ, Jovin TM, Baumann PH, Robert-Nicoud M (1991) Spatial and temporal distribution of DNA replication sites localized by immunofluorescence and confocal microscopy in mouse fibroblasts. J Cell Sci 99(Pt 2):247–253 Fu XD, Maniatis T (1990) Factor required for mammalian spliceosome assembly is localized to discrete regions in the nucleus. Nature 343:437–441 Fujita N, Takebayashi S, Okumura K, Kudo S, Chiba T, Saya H, Nakao M (1999) Methylation-mediated transcriptional silencing in euchromatin by methyl-CpG binding protein MBD1 isoforms. Mol Cell Biol 19:6415–6426 Fujita N, Jaye DL, Kajita M, Geigerman C, Moreno CS, Wade PA (2003) MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer. Cell 113:207–219 Fujita N, Jaye DL, Geigerman C, Akyildiz A, Mooney MR, Boss JM, Wade PA (2004) MTA3 and the Mi-2/NuRD complex regulate cell fate during B lymphocyte differentiation. Cell 119:75–86 Gazdar AF, Oie HK, Kirsch IR, Hollis GF (1986) Establishment and characterization of a human plasma cell myeloma culture having a rearranged cellular myc proto-oncogene. Blood 67:1542–1549 Guschin D, Wade PA, Kikyo N, Wolffe AP (2000) ATP-dependent histone octamer mobilization and histone deacetylation mediated by the Mi-2 chromatin remodeling complex. Biochemistry 39:5238–5245 Hanna MG Jr (1964) An autoradiographic study of the germinal center in spleen white pulp during early intervals of the immune response. Lab Invest 13:95–104 Hansen RS, Wijmenga C, Luo P, Stanek AM, Canfield TK, Weemaes CM, Gartler SM (1999) The DNMT3B DNA methyltransferase gene is mutated in the ICF immunodeficiency syndrome. Proc Natl Acad Sci USA 96:14412–14417 Hendrich B, Bird A (1998) Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol Cell Biol 18:6538–6547 Houston SI, McManus KJ, Adams MM, Sims JK, Carpenter PB, Hendzel MJ, Rice JC (2008) Catalytic function of the PR-Set7 histone H4 lysine 20 monomethyltransferase is essential for mitotic entry and genomic stability. J Biol Chem 283:19478–19488 Kim J, Sif S, Jones B, Jackson A, Koipally J, Heller E, Winandy S, Viel A, Sawyer A, Ikeda T, Kingston R, Georgopoulos K (1999) Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes. Immunity 10:345–355 Klein G, Giovanella B, Westman A, Stehlin JS, Mumford D (1975) An EBV-genome-negative cell line established from an American Burkitt lymphoma; receptor characteristics. EBV infectibility and permanent conversion into EBV-positive sublines by in vitro infection. Intervirology 5:319–334 Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116–120 Liu YJ, Zhang J, Lane PJ, Chan EY, MacLennan IC (1991) Sites of specific B cell activation in primary and secondary responses to T cell-dependent and T cell-independent antigens. Eur J Immunol 21:2951–2962 Lubit BW, Pham TD, Miller OJ, Erlanger BF (1976) Localization of 5-methylcytosine in human metaphase chromosomes by immunoelectron microscopy. Cell 9:503–509 Maraschio P, Tupler R, Dainotti E, Piantanida M, Cazzola G, Tiepolo L (1989) Differential expression of the ICF (immunodeficiency, centromeric heterochromatin, facial anomalies) mutation in lymphocytes and fibroblasts. J Med Genet 26:452–456 Minc E, Courvalin JC, Buendia B (2000) HP1gamma associates with euchromatin and heterochromatin in mammalian nuclei and chromosomes. Cytogenet Cell Genet 90:279–284 Monneron A, Bernhard W (1969) Fine structural organization of the interphase nucleus in some mammalian cells. J Ultrastruct Res 27:266–288 Ng HH, Jeppesen P, Bird A (2000) Active repression of methylated genes by the chromosomal protein MBD1. Mol Cell Biol 20:1394–1406 Nicol L, Jeppesen P (1994) Human autoimmune sera recognize a conserved 26 kD protein associated with mammalian heterochromatin that is homologous to heterochromatin protein 1 of Drosophila. Chromosome Res 2:245–253 O'Keefe RT, Henderson SC, Spector DL (1992) Dynamic organization of DNA replication in mammalian cell nuclei: spatially and temporally defined replication of chromosome-specific alpha-satellite DNA sequences. J Cell Biol 116:1095–1110 Polo SE, Almouzni G (2006) Chromatin assembly: a basic recipe with various flavours. Curr Opin Genet Dev 16:104–111 Quivy JP, Roche D, Kirschner D, Tagami H, Nakatani Y, Almouzni G (2004) A CAF-1 dependent pool of HP1 during heterochromatin duplication. Embo J 23:3516–3526 Saurin AJ, Shiels C, Williamson J, Satijn DP, Otte AP, Sheer D, Freemont PS (1998) The human Polycomb group complex associates with pericentromeric heterochromatin to form a novel nuclear domain. J Cell Biol 142:887–898 Sawyer JR, Swanson CM, Koller MA, North PE, Ross SW (1995) Centromeric instability of chromosome 1 resulting in multibranched chromosomes, telomeric fusions, and “jumping translocations” of 1q in a human immunodeficiency virus-related non-Hodgkin's lymphoma. Cancer 76:1238–1244 Sawyer JR, Tricot G, Mattox S, Jagannath S, Barlogie B (1998) Jumping translocations of chromosome 1q in multiple myeloma: evidence for a mechanism involving decondensation of pericentromeric heterochromatin. Blood 91:1732–1741 Sewalt RG, Lachner M, Vargas M, Hamer KM, den Blaauwen JL, Hendrix T, Melcher M, Schweizer D, Jenuwein T, Otte AP (2002) Selective interactions between vertebrate polycomb homologs and the SUV39H1 histone lysine methyltransferase suggest that histone H3–K9 methylation contributes to chromosomal targeting of Polycomb group proteins. Mol Cell Biol 22:5539–5553 Sims JK, Houston SI, Magazinnik T, Rice JC (2006) A trans-tail histone code defined by monomethylated H4 Lys-20 and H3 Lys-9 demarcates distinct regions of silent chromatin. J Biol Chem 281:12760–12766 Sobel RE, Cook RG, Perry CA, Annunziato AT, Allis CD (1995) Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc Natl Acad Sci USA 92:1237–1241 Spector DL, Goldman RD, Leinwand LA (1998) Cells: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY Taddei A, Roche D, Sibarita JB, Turner BM, Almouzni G (1999) Duplication and maintenance of heterochromatin domains. J Cell Biol 147:1153–1166 Voncken JW, Schweizer D, Aagaard L, Sattler L, Jantsch MF, van Lohuizen M (1999) Chromatin-association of the Polycomb group protein BMI1 is cell cycle-regulated and correlates with its phosphorylation status. J Cell Sci 112(Pt 24):4627–4639 Wade PA, Jones PL, Vermaak D, Wolffe AP (1998) A multiple subunit Mi-2 histone deacetylase from Xenopus laevis cofractionates with an associated Snf2 superfamily ATPase. Curr Biol 8:843–846 Wade PA, Gegonne A, Jones PL, Ballestar E, Aubry F, Wolffe AP (1999) Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nat Genet 23:62–66 Weis K, Rambaud S, Lavau C, Jansen J, Carvalho T, Carmo-Fonseca M, Lamond A, Dejean A (1994) Retinoic acid regulates aberrant nuclear localization of PML-RAR alpha in acute promyelocytic leukemia cells. Cell 76:345–356 Wreggett KA, Hill F, James PS, Hutchings A, Butcher GW, Singh PB (1994) A mammalian homologue of Drosophila heterochromatin protein 1 (HP1) is a component of constitutive heterochromatin. Cytogenet Cell Genet 66:99–103 Xu GL, Bestor TH, Bourc'his D, Hsieh CL, Tommerup N, Bugge M, Hulten M, Qu X, Russo JJ, Viegas-Pequignot E (1999) Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402:187–191 Xue Y, Wong J, Moreno GT, Young MK, Cote J, Wang W (1998) NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol Cell 2:851–861 Zhang J, MacLennan IC, Liu YJ, Lane PJ (1988) Is rapid proliferation in B centroblasts linked to somatic mutation in memory B cell clones? Immunol Lett 18:297–299 Zhang Y, LeRoy G, Seelig HP, Lane WS, Reinberg D (1998) The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 95:279–289 Zheng Y, Jung MK, Oakley BR (1991) Gamma-tubulin is present in Drosophila melanogaster and Homo sapiens and is associated with the centrosome. Cell 65:817–823