Advertisement

The nucleosome remodeling and deacetylase complex in development and disease

  • Jeannine Basta
    Affiliations
    Department of Internal Medicine, Saint Louis University, St. Louis, Missouri

    Department of Biochemistry and Molecular Biology, Saint Louis University, St. Louis, Missouri

    John Cochran Division, VA St. Louis Health Care System, St. Louis, Missouri
    Search for articles by this author
  • Michael Rauchman
    Correspondence
    Reprint requests: Michael Rauchman, Department of Internal Medicine, Saint Louis University, Doisy Research Center, 1100 S. Grand Boulevard, St. Louis, MO 63104
    Affiliations
    Department of Internal Medicine, Saint Louis University, St. Louis, Missouri

    Department of Biochemistry and Molecular Biology, Saint Louis University, St. Louis, Missouri

    John Cochran Division, VA St. Louis Health Care System, St. Louis, Missouri
    Search for articles by this author
      The nucleosome remodeling and deacetylase (NuRD) complex is one of the major chromatin remodeling complexes found in cells. It plays an important role in regulating gene transcription, genome integrity, and cell cycle progression. Through its impact on these basic cellular processes, increasing evidence indicates that alterations in the activity of this macromolecular complex can lead to developmental defects, oncogenesis, and accelerated aging. Recent genetic and biochemical studies have elucidated the mechanisms of NuRD action in modifying the chromatin landscape. These advances have the potential to lead to new therapeutic approaches to birth defects and cancer.

      Abbreviations:

      HDAC (histone (protein) deacetylase), Rbbp (Retinoblastoma binding protein), MTA (Metastases-associated protein), MBD (Methyl binding domain), CHD (Chromodomain-helicase-DNA-binding protein), ES cells (Embryonic stem cells)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Translational Research
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Suva M.L.
        • Riggi N.
        • Bernstein B.E.
        Epigenetic reprogramming in cancer.
        Science. 2013; 339: 1567-1570
        • Polo S.E.
        • Kaidi A.
        • Baskcomb L.
        • Galanty Y.
        • Jackson S.P.
        Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4.
        EMBO J. 2010; 29: 3130-3139
        • Zhang Y.
        • LeRoy G.
        • Seelig H.P.
        • Lane W.S.
        • Reinberg D.
        The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities.
        Cell. 1998; 95: 279-289
        • Xue Y.
        • Wong J.
        • Moreno G.T.
        • Young M.K.
        • Cote J.
        • Wang W.
        NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities.
        Mol Cell. 1998; 2: 851-861
        • Wade P.A.
        • Jones P.L.
        • Vermaak D.
        • Wolffe A.P.
        A multiple subunit Mi-2 histone deacetylase from Xenopus laevis cofractionates with an associated Snf2 superfamily ATPase.
        Curr Biol. 1998; 8: 843-846
        • Tong J.K.
        • Hassig C.A.
        • Schnitzler G.R.
        • Kingston R.E.
        • Schreiber S.L.
        Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex.
        Nature. 1998; 395: 917-921
        • Adamo A.
        • Sese B.
        • Boue S.
        • et al.
        LSD1 regulates the balance between self-renewal and differentiation in human embryonic stem cells.
        Nat Cell Biol. 2011; 13: 652-659
        • Wang Y.
        • Zhang H.
        • Chen Y.
        • et al.
        LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer.
        Cell. 2009; 138: 660-662
        • Whyte W.A.
        • Bilodeau S.
        • Orlando D.A.
        • et al.
        Enhancer decommissioning by LSD1 during embryonic stem cell differentiation.
        Nature. 2012; 482: 221-225
        • Smits A.H.
        • Jansen P.W.
        • Poser I.
        • Hyman A.A.
        • Vermeulen M.
        Stoichiometry of chromatin-associated protein complexes revealed by label-free quantitative mass spectrometry-based proteomics.
        Nucleic Acids Res. 2013 7; 41: e28
        • Kim J.J.
        • Khalid O.
        • Vo S.
        • Sun H.H.
        • Wong D.T.
        • Kim Y.
        A novel regulatory factor recruits the nucleosome remodeling complex to wingless integrated (Wnt) signaling gene promoters in mouse embryonic stem cells.
        J Biol Chem. 2012; 287: 41103-41117
        • Spruijt C.G.
        • Bartels S.J.
        • Brinkman A.B.
        • et al.
        CDK2AP1/DOC-1 is a bona fide subunit of the Mi-2/NuRD complex.
        Mol Biosyst. 2010; 6: 1700-1706
        • Gururaj A.E.
        • Singh R.R.
        • Rayala S.K.
        • et al.
        MTA1, a transcriptional activator of breast cancer amplified sequence 3.
        Proc Natl Acad Sci U S A. 2006; 103: 6670-6675
        • Bouazoune K.
        • Mitterweger A.
        • Langst G.
        • et al.
        The dMi-2 chromodomains are DNA binding modules important for ATP-dependent nucleosome mobilization.
        EMBO J. 2002; 21: 2430-2440
        • Thompson P.M.
        • Gotoh T.
        • Kok M.
        • White P.S.
        • Brodeur G.M.
        CHD5, a new member of the chromodomain gene family, is preferentially expressed in the nervous system.
        Oncogene. 2003; 22: 1002-1011
        • Zhuang T.
        • Hess R.A.
        • Kolla V.
        • Higashi M.
        • Raabe T.D.
        • Brodeur G.M.
        CHD5 is required for spermiogenesis and chromatin condensation.
        Mech Dev. 2014; 131: 35-46
        • Amaya M.
        • Desai M.
        • Gnanapragasam M.N.
        • et al.
        Mi2beta-mediated silencing of the fetal gamma-globin gene in adult erythroid cells.
        Blood. 2013; 121: 3493-3501
        • Kunert N.
        • Wagner E.
        • Murawska M.
        • Klinker H.
        • Kremmer E.
        • Brehm A.
        dMec: a novel Mi-2 chromatin remodelling complex involved in transcriptional repression.
        EMBO J. 2009; 28: 533-544
        • Williams C.J.
        • Naito T.
        • Arco P.G.
        • et al.
        The chromatin remodeler Mi-2beta is required for CD4 expression and T cell development.
        Immunity. 2004; 20: 719-733
        • Hendrich B.
        • Bird A.
        Identification and characterization of a family of mammalian methyl-CpG binding proteins.
        Mol Cell Biol. 1998; 18: 6538-6547
        • Hashimoto H.
        • Liu Y.
        • Upadhyay A.K.
        • et al.
        Recognition and potential mechanisms for replication and erasure of cytosine hydroxymethylation.
        Nucleic Acids Res. 2012; 40: 4841-4849
        • Hong W.
        • Nakazawa M.
        • Chen Y.Y.
        • et al.
        FOG-1 recruits the NuRD repressor complex to mediate transcriptional repression by GATA-1.
        EMBO J. 2005; 24: 2367-2378
        • Humphrey G.W.
        • Wang Y.
        • Russanova V.R.
        • et al.
        Stable histone deacetylase complexes distinguished by the presence of SANT domain proteins CoREST/kiaa0071 and Mta-L1.
        J Biol Chem. 2001; 276: 6817-6824
        • Roche A.E.
        • Bassett B.J.
        • Samant S.A.
        • Hong W.
        • Blobel G.A.
        • Svensson E.C.
        The zinc finger and C-terminal domains of MTA proteins are required for FOG-2-mediated transcriptional repression via the NuRD complex.
        J Mol Cell Cardiol. 2008; 44: 352-360
        • Murzina N.V.
        • Pei X.Y.
        • Zhang W.
        • et al.
        Structural basis for the recognition of histone H4 by the histone-chaperone RbAp46.
        Structure. 2008; 16: 1077-1085
        • Gnanapragasam M.N.
        • Scarsdale J.N.
        • Amaya M.L.
        • et al.
        p66Alpha-MBD2 coiled-coil interaction and recruitment of Mi-2 are critical for globin gene silencing by the MBD2-NuRD complex.
        Proc Natl Acad Sci U S Am. 2011; 108: 7487-7492
        • Walavalkar N.M.
        • Gordon N.
        • Williams Jr., D.C.
        Unique features of the anti-parallel, heterodimeric coiled-coil interaction between methyl-cytosine binding domain 2 (MBD2) homologues and GATA zinc finger domain containing 2A (GATAD2A/p66alpha).
        J Biol Chem. 2013; 288: 3419-3427
        • Ahringer J.
        NuRD and SIN3 histone deacetylase complexes in development.
        Trends Genet. 2000; 16: 351-356
        • Kelly R.D.
        • Cowley S.M.
        The physiological roles of histone deacetylase (HDAC) 1 and 2: complex co-stars with multiple leading parts.
        Biochem Soc Trans. 2013; 41: 741-749
        • Fujita N.
        • Jaye D.L.
        • Kajita M.
        • Geigerman C.
        • Moreno C.S.
        • Wade P.A.
        MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer.
        Cell. 2003; 113: 207-219
        • Zhang H.
        • Stephens L.C.
        • Kumar R.
        Metastasis tumor antigen family proteins during breast cancer progression and metastasis in a reliable mouse model for human breast cancer.
        Clin Cancer Res. 2006; 12: 1479-1486
        • Le Guezennec X.
        • Vermeulen M.
        • Brinkman A.B.
        • et al.
        MBD2/NuRD and MBD3/NuRD, two distinct complexes with different biochemical and functional properties.
        Mol Cell Biol. 2006; 26: 843-851
        • Fujita N.
        • Jaye D.L.
        • Geigerman C.
        • et al.
        MTA3 and the Mi-2/NuRD complex regulate cell fate during B lymphocyte differentiation.
        Cell. 2004; 119: 75-86
        • Kim J.
        • Sif S.
        • Jones B.
        • et al.
        Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes.
        Immunity. 1999; 10: 345-355
        • Lauberth S.M.
        • Rauchman M.
        A conserved 12-amino acid motif in Sall1 recruits the nucleosome remodeling and deacetylase corepressor complex.
        J Biol Chem. 2006; 281: 23922-23931
        • Nair S.S.
        • Li D.Q.
        • Kumar R.
        A core chromatin remodeling factor instructs global chromatin signaling through multivalent reading of nucleosome codes.
        Mol Cell. 2013; 49: 704-718
        • Matsuoka S.
        • Ballif B.A.
        • Smogorzewska A.
        • et al.
        ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage.
        Science. 2007; 316: 1160-1166
        • Segre C.V.
        • Chiocca S.
        Regulating the regulators: the post-translational code of class I HDAC1 and HDAC2.
        J Biomed Biotechnol. 2011; 2011: 690848
        • Yang T.
        • Jian W.
        • Luo Y.
        • et al.
        Acetylation of histone deacetylase 1 regulates NuRD corepressor complex activity.
        J Biol Chem. 2012; 287: 40279-40291
        • Millard C.J.
        • Watson P.J.
        • Celardo I.
        • et al.
        Class I HDACs share a common mechanism of regulation by inositol phosphates.
        Mol Cell. 2013; 51: 57-67
        • Watson P.J.
        • Fairall L.
        • Santos G.M.
        • Schwabe J.W.
        Structure of HDAC3 bound to co-repressor and inositol tetraphosphate.
        Nature. 2012; 481: 335-340
        • Costa F.C.
        • Fedosyuk H.
        • Chazelle A.M.
        • Neades R.Y.
        • Peterson K.R.
        Mi2beta is required for gamma-globin gene silencing: temporal assembly of a GATA-1-FOG-1-Mi2 repressor complex in beta-YAC transgenic mice.
        PLoS Genet. 2012; 8: e1003155
        • Hendrich B.
        • Guy J.
        • Ramsahoye B.
        • Wilson V.A.
        • Bird A.
        Closely related proteins MBD2 and MBD3 play distinctive but interacting roles in mouse development.
        Genes Dev. 2001; 15: 710-723
        • Kaji K.
        • Caballero I.M.
        • MacLeod R.
        • Nichols J.
        • Wilson V.A.
        • Hendrich B.
        The NuRD component Mbd3 is required for pluripotency of embryonic stem cells.
        Nat Cell Biol. 2006; 8: 285-292
        • Kashiwagi M.
        • Morgan B.A.
        • Georgopoulos K.
        The chromatin remodeler Mi-2beta is required for establishment of the basal epidermis and normal differentiation of its progeny.
        Development. 2007; 134: 1571-1582
        • Baubec T.
        • Ivanek R.
        • Lienert F.
        • Schübeler D.
        Methylation-dependent and -independent genomic targeting principles of the MBD protein family.
        Cell. 2013; 153: 480-492
        • Gunther K.
        • Rust M.
        • Leers J.
        • et al.
        Differential roles for MBD2 and MBD3 at methylated CpG islands, active promoters and binding to exon sequences.
        Nucleic Acids Res. 2013; 41: 3010-3021
        • Shimbo T.
        • Du Y.
        • Grimm S.A.
        • et al.
        MBD3 localizes at promoters, gene bodies and enhancers of active genes.
        PLoS Genet. 2013; 9: e1004028
        • Zhang J.
        • Jackson A.F.
        • Naito T.
        • et al.
        Harnessing of the nucleosome-remodeling-deacetylase complex controls lymphocyte development and prevents leukemogenesis.
        Nat Immunol. 2012; 13: 86-94
        • Reynolds N.
        • Latos P.
        • Hynes-Allen A.
        • et al.
        NuRD suppresses pluripotency gene expression to promote transcriptional heterogeneity and lineage commitment.
        Cell Stem Cell. 2012; 10: 583-594
        • Margueron R.
        • Reinberg D.
        The Polycomb complex PRC2 and its mark in life.
        Nature. 2011; 469: 343-349
        • Ku M.
        • Koche R.P.
        • Rheinbay E.
        • et al.
        Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains.
        PLoS Genet. 2008; 4: e1000242
        • Mikkelsen T.S.
        • Ku M.
        • Jaffe D.B.
        • et al.
        Genome-wide maps of chromatin state in pluripotent and lineage-committed cells.
        Nature. 2007; 448: 553-560
        • Reynolds N.
        • Salmon-Divon M.
        • Dvinge H.
        • et al.
        NuRD-mediated deacetylation of H3K27 facilitates recruitment of Polycomb Repressive Complex 2 to direct gene repression.
        EMBO J. 2012; 31: 593-605
        • Morey L.
        • Brenner C.
        • Fazi F.
        • et al.
        MBD3, a component of the NuRD complex, facilitates chromatin alteration and deposition of epigenetic marks.
        Mol Cell Biol. 2008; 28: 5912-5923
        • Beyer T.A.
        • Weiss A.
        • Khomchuk Y.
        • et al.
        Switch enhancers interpret TGF-beta and Hippo signaling to control cell fate in human embryonic stem cells.
        Cell Rep. 2013; 5: 1611-1624
        • Rais Y.
        • Zviran A.
        • Geula S.
        • et al.
        Deterministic direct reprogramming of somatic cells to pluripotency.
        Nature. 2013; 502: 65-70
        • Luo M.
        • Ling T.
        • Xie W.
        • et al.
        NuRD blocks reprogramming of mouse somatic cells into pluripotent stem cells.
        Stem cells. 2013; 31: 1278-1286
        • Ng S.Y.
        • Yoshida T.
        • Zhang J.
        • Georgopoulos K.
        Genome-wide lineage-specific transcriptional networks underscore Ikaros-dependent lymphoid priming in hematopoietic stem cells.
        Immunity. 2009; 30: 493-507
        • Yoshida T.
        • Hazan I.
        • Zhang J.
        • et al.
        The role of the chromatin remodeler Mi-2beta in hematopoietic stem cell self-renewal and multilineage differentiation.
        Genes Dev. 2008; 22: 1174-1189
        • Huang H.T.
        • Kathrein K.L.
        • Barton A.
        • et al.
        A network of epigenetic regulators guides developmental haematopoiesis in vivo.
        Nat Cell Biol. 2013; 15: 1516-1525
        • Li X.
        • Jia S.
        • Wang S.
        • Wang Y.
        • Meng A.
        Mta3-NuRD complex is a master regulator for initiation of primitive hematopoiesis in vertebrate embryos.
        Blood. 2009; 114: 5464-5472
        • Miccio A.
        • Blobel G.A.
        Role of the GATA-1/FOG-1/NuRD pathway in the expression of human beta-like globin genes.
        Mol Cell Biol. 2010; 30: 3460-3470
        • Mimoto M.S.
        • Christian J.L.
        Friend of GATA (FOG) interacts with the nucleosome remodeling and deacetylase complex (NuRD) to support primitive erythropoiesis in Xenopus laevis.
        PLoS ONE. 2012; 7: e29882
        • Gregory G.D.
        • Miccio A.
        • Bersenev A.
        • et al.
        FOG1 requires NuRD to promote hematopoiesis and maintain lineage fidelity within the megakaryocytic-erythroid compartment.
        Blood. 2010; 115: 2156-2166
        • Wang Y.
        • Meng R.
        • Hayes V.
        • et al.
        Pleiotropic platelet defects in mice with disrupted FOG1-NuRD interaction.
        Blood. 2011; 118: 6183-6191
        • Basta J.M.
        • Robbins L.
        • Kiefer S.M.
        • Dorsett D.
        • Rauchman M.
        Sall1 balances self-renewal and differentiation of renal progenitor cells.
        Development. 2014; 141: 1047-1058
        • Denner D.R.
        • Rauchman M.
        Mi-2/NuRD is required in renal progenitor cells during embryonic kidney development.
        Dev Biol. 2013; 375: 105-116
        • de Ligt J.
        • Willemsen M.H.
        • van Bon B.W.
        • et al.
        Diagnostic exome sequencing in persons with severe intellectual disability.
        N Eng J Med. 2012; 367: 1921-1929
        • Kiefer S.M.
        • Robbins L.
        • Barina A.
        • Zhang Z.
        • Rauchman M.
        SALL1 truncated protein expression in Townes-Brocks syndrome leads to ectopic expression of downstream genes.
        Hum Mutat. 2008; 29: 1133-1140
        • Liu Z L.F.
        • Ruan K.
        • Zhang J.
        • Mej Y.
        • Wu J.
        • Shi Y.
        Structural and functional insights into the human Borjeson-Forssman-Lehmann Syndrome associated protein PHF6.
        J Biol Chem. 2014; 289: 10069-10083
        • Verstappen G.
        • van Grunsven L.A.
        • Michiels C.
        • et al.
        Atypical Mowat-Wilson patient confirms the importance of the novel association between ZFHX1B/SIP1 and NuRD corepressor complex.
        Hum Mol Genet. 2008; 17: 1175-1183
        • Wieczorek D.
        • Bogershausen N.
        • Beleggia F.
        • et al.
        A comprehensive molecular study on Coffin-Siris and Nicolaides-Baraitser syndromes identifies a broad molecular and clinical spectrum converging on altered chromatin remodeling.
        Hum Mol Genet. 2013; 22: 5121-5135
        • Willemsen M.H.
        • Nijhof B.
        • Fenckova M.
        • et al.
        GATAD2B loss-of-function mutations cause a recognisable syndrome with intellectual disability and are associated with learning deficits and synaptic undergrowth in Drosophila.
        J Med Genet. 2013; 50: 507-514
        • Nicolson G.L.
        • Nawa A.
        • Toh Y.
        • Taniguchi S.
        • Nishimori K.
        • Moustafa A.
        Tumor metastasis-associated human MTA1 gene and its MTA1 protein product: role in epithelial cancer cell invasion, proliferation and nuclear regulation.
        Clin Exp Metastasis. 2003; 20: 19-24
        • Mazumdar A.
        • Wang R.A.
        • Mishra S.K.
        • et al.
        Transcriptional repression of oestrogen receptor by metastasis-associated protein 1 corepressor.
        Nat Cell Biol. 2001; 3: 30-37
        • Zhang X.Y.
        • DeSalle L.M.
        • Patel J.H.
        • et al.
        Metastasis-associated protein 1 (MTA1) is an essential downstream effector of the c-MYC oncoprotein.
        Proc Natl Acad Sci U S A. 2005; 102: 13968-13973
        • Zhang H.
        • Singh R.R.
        • Talukder A.H.
        • Kumar R.
        Metastatic tumor antigen 3 is a direct corepressor of the Wnt4 pathway.
        Genes Dev. 2006; 20: 2943-2948
        • Le Gallo M.
        • O'Hara A.J.
        • Rudd M.L.
        • et al.
        Exome sequencing of serous endometrial tumors identifies recurrent somatic mutations in chromatin-remodeling and ubiquitin ligase complex genes.
        Nat Genet. 2012; 44: 1310-1315
        • Zhao S.
        • Choi M.
        • Overton J.D.
        • et al.
        Landscape of somatic single-nucleotide and copy-number mutations in uterine serous carcinoma.
        Proc Natl Acad Sci U S A. 2013; 110: 2916-2921
        • Mansfield R.E.
        • Musselman C.A.
        • Kwan A.H.
        • et al.
        Plant homeodomain (PHD) fingers of CHD4 are histone H3-binding modules with preference for unmodified H3K4 and methylated H3K9.
        J Biol Chem. 2011; 286: 11779-11791
        • Musselman C.A.
        • Ramirez J.
        • Sims J.K.
        • et al.
        Bivalent recognition of nucleosomes by the tandem PHD fingers of the CHD4 ATPase is required for CHD4-mediated repression.
        Proc Natl Acad Sci U S A. 2012; 109: 787-792
        • Watson A.A.
        • Mahajan P.
        • Mertens H.D.
        • et al.
        The PHD and chromo domains regulate the ATPase activity of the human chromatin remodeler CHD4.
        J Mol Biol. 2012; 422: 3-17
        • Kong X.
        • Xu X.
        • Yan Y.
        • et al.
        Estrogen regulates the tumour suppressor MiRNA-30c and its target gene, MTA-1, in endometrial cancer.
        PLoS ONE. 2014; 9: e90810
        • Major M.B.
        • Roberts B.S.
        • Berndt J.D.
        • et al.
        New regulators of Wnt/beta-catenin signaling revealed by integrative molecular screening.
        Sci Signal. 2008; 1: ra12
        • Villacorte M.
        • Suzuki K.
        • Hirasawa A.
        • et al.
        beta-Catenin signaling regulates Foxa2 expression during endometrial hyperplasia formation.
        Oncogene. 2013; 32: 3477-3482
        • O'Shaughnessy A.
        • Hendrich B.
        CHD4 in the DNA-damage response and cell cycle progression: not so NuRDy now.
        Biochem Soc Trans. 2013; 41: 777-782
        • Yong K.J.
        • Gao C.
        • Lim J.S.
        • et al.
        Oncofetal gene SALL4 in aggressive hepatocellular carcinoma.
        N Engl J Med. 2013; 368: 2266-2276
        • Gao C.
        • Dimitrov T.
        • Yong K.J.
        • et al.
        Targeting transcription factor SALL4 in acute myeloid leukemia by interrupting its interaction with an epigenetic complex.
        Blood. 2013; 121: 1413-1421
        • Miettinen M.
        • Wang Z.
        • McCue P.A.
        • et al.
        SALL4 expression in germ cell and non-germ cell tumors: a systematic immunohistochemical study of 3215 cases.
        Am J Surg Pathol. 2014; 38: 410-420
        • Li A.
        • Jiao Y.
        • Yong K.J.
        • et al.
        SALL4 is a new target in endometrial cancer.
        Oncogene. 2013; (Epub Dec. 16)
        • Love C.
        • Sun Z.
        • Jima D.
        • et al.
        The genetic landscape of mutations in Burkitt lymphoma.
        Nat Genet. 2012; 44: 1321-1325
        • Wolf J.
        • Muller-Decker K.
        • Flechtenmacher C.
        • et al.
        An in vivo RNAi screen identifies SALL1 as a tumor suppressor in human breast cancer with a role in CDH1 regulation.
        Oncogene. 2013; (Epub Dec. 16)
        • Chudnovsky Y.
        • Kim D.
        • Zheng S.
        • et al.
        ZFHX4 Interacts with the NuRD core member CHD4 and regulates the glioblastoma tumor-initiating cell state.
        Cell Rep. 2014; 6: 313-324
        • Kolla V.
        • Zhuang T.
        • Higashi M.
        • Naraparaju K.
        • Brodeur G.M.
        Role of CHD5 in human cancers: 10 years later.
        Can Res. 2014; 74: 652-658
        • Harrison S.J.
        • Parrish M.
        • Monaghan A.P.
        Sall3 is required for the terminal maturation of olfactory glomerular interneurons.
        J Comp Neurol. 2008; 507: 1780-1794
        • Larsen D.H.
        • Poinsignon C.
        • Gudjonsson T.
        • et al.
        The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage.
        J Cell Biol. 2010; 190: 731-740
        • Sims J.K.
        • Wade P.A.
        Mi-2/NuRD complex function is required for normal S phase progression and assembly of pericentric heterochromatin.
        Mol Biol Cell. 2011; 22: 3094-3102
        • Smeenk G.
        • Wiegant W.W.
        • Vrolijk H.
        • Solari A.P.
        • Pastink A.
        • van Attikum H.
        The NuRD chromatin-remodeling complex regulates signaling and repair of DNA damage.
        J Cell Biol. 2010; 190: 741-749
        • Pegoraro G.
        • Kubben N.
        • Wickert U.
        • Gohler H.
        • Hoffmann K.
        • Misteli T.
        Ageing-related chromatin defects through loss of the NURD complex.
        Nat Cell Biol. 2009; 11: 1261-1267
        • De Vaux V.
        • Pfefferli C.
        • Passannante M.
        • et al.
        The Caenorhabditis elegans LET-418/Mi2 plays a conserved role in lifespan regulation.
        Aging Cell. 2013; 12: 1012-1020
        • Lagger G.
        • O'Carroll D.
        • Rembold M.
        • et al.
        Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression.
        EMBO J. 2002; 21: 2672-2681
        • Dovey O.M.
        • Foster C.T.
        • Conte N.
        • et al.
        Histone deacetylase 1 and 2 are essential for normal T-cell development and genomic stability in mice.
        Blood. 2013; 121: 1335-1344
        • Montgomery R.L.
        • Davis C.A.
        • Potthoff M.J.
        • et al.
        Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility.
        Genes Dev. 2007; 21: 1790-1802
        • Montgomery R.L.
        • Hsieh J.
        • Barbosa A.C.
        • Richardson J.A.
        • Olson E.N.
        Histone deacetylases 1 and 2 control the progression of neural precursors to neurons during brain development.
        Proc Natl Acad Sci U S A. 2009; 106: 7876-7881
        • Lejon S.
        • Thong S.Y.
        • Murthy A.
        • et al.
        Insights into association of the NuRD complex with FOG-1 from the crystal structure of an RbAp48.FOG-1 complex.
        J Biol Chem. 2011; 286: 1196-1203
        • Manavathi B.
        • Peng S.
        • Rayala S.K.
        • et al.
        Repression of Six3 by a corepressor regulates rhodopsin expression.
        Proc Natl Acad Sci U S A. 2007; 104: 13128-13133
        • Lu X.
        • Kovalev G.I.
        • Chang H.
        • et al.
        Inactivation of NuRD component Mta2 causes abnormal T cell activation and lupus-like autoimmune disease in mice.
        J Biol Chem. 2008; 283: 13825-13833
        • Charles M.A.
        • Saunders T.L.
        • Wood W.M.
        • et al.
        Pituitary-specific Gata2 knockout: effects on gonadotrope and thyrotrope function.
        Mol Endocrinol. 2006; 20: 1366-1377
        • Trivedi C.M.
        • Luo Y.
        • Yin Z.
        • et al.
        Hdac2 regulates the cardiac hypertrophic response by modulating Gsk3 beta activity.
        Nat Med. 2007; 13: 324-331
        • Cianciolo Cosentino C.
        • Skrypnyk N.I.
        • Brilli L.L.
        • et al.
        Histone deacetylase inhibitor enhances recovery after AKI.
        J Am Soc Nephrol. 2013; 24: 943-953
        • Novitskaya T.
        • McDermott L.
        • Zhang K.X.
        • et al.
        A PTBA small molecule enhances recovery and reduces postinjury fibrosis after aristolochic acid-induced kidney injury.
        Am J Physiol Renal Physiol. 2014; 306: F496-F504
        • Brilli L.L.
        • Swanhart L.M.
        • de Caestecker M.P.
        • Hukriede N.A.
        HDAC inhibitors in kidney development and disease.
        Pediatr Nephrol. 2013; 28: 1909-1921
        • Slingerland M.
        • Guchelaar H.J.
        • Gelderblom H.
        Histone deacetylase inhibitors: an overview of the clinical studies in solid tumors.
        Anticancer Drugs. 2014; 25: 140-149
        • Chaurasia P.
        • Gajzer D.C.
        • Schaniel C.
        • D'Souza S.
        • Hoffman R.
        Epigenetic reprogramming induces the expansion of cord blood stem cells.
        J Clin Invest. 2014; 124: 2378-2395
        • Allen H.F.
        • Daze K.D.
        • Shimbo T.
        • et al.
        Inhibition of histone binding by supramolecular hosts.
        Biochem J. 2014; 459: 505-512
        • Sansom O.J.
        • Berger J.
        • Bishop S.M.
        • Hendrich B.
        • Bird A.
        • Clarke A.R.
        Deficiency of Mbd2 suppresses intestinal tumorigenesis.
        Nat Genet. 2003; 34: 145-147
        • Li D.Q.
        • Pakala S.B.
        • Nair S.S.
        • Eswaran J.
        • Kumar R.
        Metastasis-associated protein 1/nucleosome remodeling and histone deacetylase complex in cancer.
        Cancer Res. 2012; 72: 387-394
        • Aury-Landas J.
        • Bougeard G.
        • Castel H.
        • et al.
        Germline copy number variation of genes involved in chromatin remodelling in families suggestive of Li-Fraumeni syndrome with brain tumours.
        Eur J Hum Genet. 2013; 21: 1369-1376