The Human SWI-SNF Complex Protein p270 Is an ARID Family Member with Non-Sequence-Specific DNA Binding Activity

ABSTRACT p270 is an integral member of human SWI-SNF complexes, first identified through its shared antigenic specificity with p300 and CREB binding protein. The deduced amino acid sequence of p270 reported here indicates that it is a member of an evolutionarily conserved family of proteins distinguished by the presence of a DNA binding motif termed ARID (AT-rich interactive domain). The ARID consensus and other structural features are common to both p270 and yeast SWI1, suggesting that p270 is a human counterpart of SWI1. The approximately 100-residue ARID sequence is present in a series of proteins strongly implicated in the regulation of cell growth, development, and tissue-specific gene expression. Although about a dozen ARID proteins can be identified from database searches, to date, only Bright (a regulator of B-cell-specific gene expression), dead ringer (a Drosophila melanogastergene product required for normal development), and MRF-2 (which represses expression from the cytomegalovirus enhancer) have been analyzed directly in regard to their DNA binding properties. Each binds preferentially to AT-rich sites. In contrast, p270 shows no sequence preference in its DNA binding activity, thereby demonstrating that AT-rich binding is not an intrinsic property of ARID domains and that ARID family proteins may be involved in a wider range of DNA interactions.

[1]  R. Scheuermann,et al.  Cux/CDP Homeoprotein Is a Component of NF-μNR and Represses the Immunoglobulin Heavy Chain Intronic Enhancer by Antagonizing the Bright Transcription Activator , 1999, Molecular and Cellular Biology.

[2]  Yate-Ching Yuan,et al.  A novel DNA-binding motif shares structural homology to DNA replication and repair nucleases and polymerases , 1998, Nature Structural Biology.

[3]  R. Clubb,et al.  Solution structure of the DNA binding domain from Dead ringer, a sequence‐specific AT‐rich interaction domain (ARID) , 1999, The EMBO journal.

[4]  P. Dallas,et al.  p300/CREB Binding Protein-Related Protein p270 Is a Component of Mammalian SWI/SNF Complexes , 1998, Molecular and Cellular Biology.

[5]  W. Kaelin,et al.  RBP1 Recruits Both Histone Deacetylase-Dependent and -Independent Repression Activities to Retinoblastoma Family Proteins , 1999, Molecular and Cellular Biology.

[6]  S. Altschul,et al.  Issues in searching molecular sequence databases , 1994, Nature Genetics.

[7]  Craig L. Peterson,et al.  DNA-binding properties of the yeast SWI/SNF complex , 1996, Nature.

[8]  Michael R. Green,et al.  Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex , 1994, Nature.

[9]  T. Archer,et al.  Chromatin remodelling by the glucocorticoid receptor requires the BRG1 complex , 1998, Nature.

[10]  O. Wrange,et al.  Glucocorticoid receptor-glucocorticoid response element binding stimulates nucleosome disruption by the SWI/SNF complex , 1997, Molecular and cellular biology.

[11]  R. Kingston,et al.  Repression and activation by multiprotein complexes that alter chromatin structure. , 1996, Genes & development.

[12]  P. Dallas,et al.  Characterization of monoclonal antibodies raised against p300: both p300 and CBP are present in intracellular TBP complexes , 1997, Journal of virology.

[13]  Y. Ohtsuki,et al.  Molecular cloning and expression of a novel human cDNA containing CAG repeats. , 1997, Gene.

[14]  R. Scheuermann,et al.  The immunoglobulin heavy-chain matrix-associating regions are bound by Bright: a B cell-specific trans-activator that describes a new DNA-binding protein family. , 1995, Genes & development.

[15]  A. Agulnik,et al.  Gene sequence and evolutionary conservation of human SMCY , 1996, Nature Genetics.

[16]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[17]  L. Moore,et al.  The trithorax group gene osa encodes an ARID-domain protein that genetically interacts with the brahma chromatin-remodeling factor to regulate transcription. , 1999, Development.

[18]  T. Takeuchi,et al.  Gene trap capture of a novel mouse gene, jumonji, required for neural tube formation. , 1995, Genes & development.

[19]  David M. Heery,et al.  A signature motif in transcriptional co-activators mediates binding to nuclear receptors , 1997, Nature.

[20]  K. Helin,et al.  Characterization of the retinoblastoma binding proteins RBP1 and RBP2. , 1993, Oncogene.

[21]  I. Herskowitz,et al.  Characterization of the yeast SWI1, SWI2, and SWI3 genes, which encode a global activator of transcription , 1992, Cell.

[22]  J. T. Kadonaga.  Eukaryotic Transcription: An Interlaced Network of Transcription Factors and Chromatin-Modifying Machines , 1998, Cell.

[23]  P. Branton,et al.  RBP1 induces growth arrest by repression of E2F-dependent transcription , 1999, Oncogene.

[24]  M. Yaniv,et al.  Purification and biochemical heterogeneity of the mammalian SWI‐SNF complex. , 1996, The EMBO journal.

[25]  G. Crabtree,et al.  Architectural DNA binding by a high-mobility-group/kinesin-like subunit in mammalian SWI/SNF-related complexes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[26]  G M Rubin,et al.  eyelid antagonizes wingless signaling during Drosophila development and has homology to the Bright family of DNA-binding proteins. , 1997, Genes & development.

[27]  A. Courey,et al.  Dorsal-Mediated Repression Requires the Formation of a Multiprotein Repression Complex at the Ventral Silencer , 1998, Molecular and Cellular Biology.

[28]  G. Crabtree,et al.  Diversity and specialization of mammalian SWI/SNF complexes. , 1996, Genes & development.

[29]  C. Peterson,et al.  The SWI-SNF complex: a chromatin remodeling machine? , 1995, Trends in biochemical sciences.

[30]  W. Schaffner,et al.  Different activation domains stimulate transcription from remote (‘enhancer’) and proximal (‘promoter’) positions. , 1992, The EMBO journal.

[31]  C. Sardet,et al.  A human protein with homology to Saccharomyces cerevisiae SNF5 interacts with the potential helicase hbrm. , 1995, Nucleic acids research.

[32]  R. Saint,et al.  Characterization of the dead ringer gene identifies a novel, highly conserved family of sequence-specific DNA-binding proteins , 1996, Molecular and cellular biology.

[33]  K. Itakura,et al.  The novel Mrf-2 DNA-binding domain recognizes a five-base core sequence through major and minor-groove contacts. , 1999, Biochemical and biophysical research communications.

[34]  I. Herskowitz,et al.  Roles of SWI1, SWI2, and SWI3 proteins for transcriptional enhancement by steroid receptors. , 1992, Science.

[35]  M. Stinski,et al.  Regulation of a human cytomegalovirus immediate-early gene (US3) by a silencer-enhancer combination , 1996, Journal of virology.

[36]  R. Kingston,et al.  Human SWI/SNF Interconverts a Nucleosome between Its Base State and a Stable Remodeled State , 1998, Cell.

[37]  E. Young,et al.  The yeast ADR6 gene encodes homopolymeric amino acid sequences and a potential metal-binding domain. , 1988, Nucleic acids research.

[38]  K. Itakura,et al.  Repression by a differentiation-specific factor of the human cytomegalovirus enhancer. , 1996, Nucleic acids research.

[39]  R. Durbin,et al.  2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans , 1994, Nature.

[40]  H. Chiba,et al.  Two human homologues of Saccharomyces cerevisiae SWI2/SNF2 and Drosophila brahma are transcriptional coactivators cooperating with the estrogen receptor and the retinoic acid receptor. , 1994, Nucleic acids research.

[41]  R. Saint,et al.  The Drosophila dead ringer gene is required for early embryonic patterning through regulation of argos and buttonhead expression. , 1999, Development.

[42]  R. Saint,et al.  The human dead ringer/bright homolog, DRIL1: cDNA cloning, gene structure, and mapping to D19S886, a marker on 19p13.3 that is strictly linked to the Peutz-Jeghers syndrome. , 1998, Genomics.

[43]  R. Kingston,et al.  ATP-dependent remodeling and acetylation as regulators of chromatin fluidity. , 1999, Genes & development.

[44]  R. Saint,et al.  ARID proteins come in from the desert. , 2000, Trends in biochemical sciences.

[45]  M. Yaniv,et al.  A human homologue of Saccharomyces cerevisiae SNF2/SWI2 and Drosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor. , 1993, The EMBO journal.