The Affinity of Nuclear Factor 1 for Its DNA Site Is Drastically Reduced by Nucleosome Organization Irrespective of Its Rotational or Translational Position (*)

A DNA-bending sequence has been used for in vitro reconstitution of nucleosomes in order to direct a nuclear factor 1 (NF-1) binding site into different nucleosome positions. By this strategy nucleosomes were obtained that had one of two rotational positions of the NF-1 binding site, one oriented toward the periphery and the other toward the histone octamer, translationally positioned 50 and 45 base pairs, respectively, from the nucleosome dyad. The affinity of partially purified NF-1 for these nucleosomal targets was compared with its affinity for free DNA by dimethylsulfate methylation protection and DNase I footprinting assays. The binding affinity of NF-1 to all nucleosomal targets was reduced 100-300-fold compared with its affinity for free DNA. The two rotational settings of the NF-1 site showed the same binding affinity for NF-1 as did other nucleosome constructs in which the NF-1 binding site was translationally positioned from 10 to 40 base pairs from the nucleosome dyad. We conclude that the nucleosomal inhibition of NF-1 binding is an inherent characteristic of NF-1 since another transcription factor, the glucocorticoid receptor, is able to bind to its DNA site in a nucleosome.

[1]  Keith R. Yamamoto,et al.  Reversible and persistent changes in chromatin structure accompany activation of a glucocorticoid-dependent enhancer element , 1984, Cell.

[2]  P. Eriksson,et al.  The glucocorticoid receptor acts as an antirepressor in receptor-dependent in vitro transcription. , 1993, European journal of biochemistry.

[3]  H. Bernard,et al.  Nuclear factor I and epithelial cell-specific transcription of human papillomavirus type 16 , 1993, Journal of virology.

[4]  D M Crothers,et al.  Artificial nucleosome positioning sequences. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[5]  G. Hager,et al.  Steroid-dependent interaction of transcription factors with the inducible promoter of mouse mammary tumor virus in vivo , 1987, Cell.

[6]  J. Whitlock,et al.  Transcription-dependent and transcription-independent nucleosome disruption induced by dioxin. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[7]  M. Beato,et al.  Chromatin structure modulates transcription factor binding to the mouse mammary tumor virus (MMTV) promoter , 1993, The Journal of Steroid Biochemistry and Molecular Biology.

[8]  R. Gronostajski,et al.  Analysis of multiple forms of nuclear factor I in human and murine cell lines , 1990, Molecular and cellular biology.

[9]  K. Zaret,et al.  An active tissue-specific enhancer and bound transcription factors existing in a precisely positioned nucleosomal array , 1993, Cell.

[10]  R. Simpson,et al.  Nucleosome positioning: occurrence, mechanisms, and functional consequences. , 1991, Progress in nucleic acid research and molecular biology.

[11]  G. Hager,et al.  Evidence that nucleosomes on the mouse mammary tumor virus promoter adopt specific translational positions. , 1992, Nucleic acids research.

[12]  L. Lutter.  Kinetic analysis of deoxyribonuclease I cleavages in the nucleosome core: evidence for a DNA superhelix. , 1978, Journal of molecular biology.

[13]  Michael R. Green,et al.  Facilitated binding of TATA-binding protein to nucleosomal DNA , 1994, Nature.

[14]  A. E. Sippel,et al.  Identification of a fourth nuclear factor I gene in chicken by cDNA cloning: NFI-X. , 1991, Nucleic acids research.

[15]  R. Tjian,et al.  Purification and analysis of RNA polymerase II transcription factors by using wheat germ agglutinin affinity chromatography. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[16]  A. E. Sippel,et al.  Transcription factor nuclear factor I proteins form stable homo‐ and heterodimers , 1994, FEBS letters.

[17]  H. Richard-Foy,et al.  Sequence‐specific positioning of nucleosomes over the steroid‐inducible MMTV promoter. , 1987, The EMBO journal.

[18]  M. Thompson,et al.  NF1-L Is the DNA-binding Component of the Protein Complex at the Peripherin Negative Regulatory Element (*) , 1995, The Journal of Biological Chemistry.

[19]  E. Winnacker,et al.  Structural and functional organization of a porcine gene coding for nuclear factor I. , 1989, Biochemistry.

[20]  Nicolas Mermod,et al.  A family of human CCAAT-box-binding proteins active in transcription and DNA replication: cloning and expression of multiple cDNAs , 1988, Nature.

[21]  A. E. Sippel,et al.  The TGGCA protein binds to the MMTV-LTR, the adenovirus origin of replication, and the BK virus enhancer. , 1985, Nucleic acids research.

[22]  G. Hager,et al.  Transcription factor access is mediated by accurately positioned nucleosomes on the mouse mammary tumor virus promoter , 1991, Molecular and cellular biology.

[23]  R. Tjian,et al.  GC box binding induces phosphorylation of Sp1 by a DNA-dependent protein kinase , 1990, Cell.

[24]  M. M. Bradford.  A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[25]  H. Weintraub,et al.  Nucleosomal DNA is digested to repeats of 10 bases by exonuclease III , 1978, Cell.

[26]  O. Wrange,et al.  Accessibility of a glucocorticoid response element in a nucleosome depends on its rotational positioning , 1995, Molecular and cellular biology.

[27]  M. Beato,et al.  Nucleosome positioning modulates accessibility of regulatory proteins to the mouse mammary tumor virus promoter , 1990, Cell.

[28]  H. Varmus,et al.  Infection of cultured rat hepatoma cells by mouse mammary tumor virus , 1977, Cell.

[29]  H. Bernard,et al.  Cloning and functional analysis of spliced isoforms of human nuclear factor I-X: interference with transcriptional activation by NFI/CTF in a cell-type specific manner. , 1994, Nucleic acids research.

[30]  R. Gronostajski,et al.  Four conserved cysteine residues are required for the DNA binding activity of nuclear factor I. , 1992, The Journal of biological chemistry.

[31]  M. Noll.  Internal structure of the chromatin subunit. , 1974, Nucleic acids research.

[32]  B. Spiegelman,et al.  Identification of a potent adipocyte-specific enhancer: involvement of an NF-1-like factor. , 1991, Genes & development.

[33]  J. Hurwitz,et al.  Specific binding of a cellular DNA replication protein to the origin of replication of adenovirus DNA. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[34]  E. Buetti,et al.  Distinct sequence elements involved in the glucocorticoid regulation of the mouse mammary tumor virus promoter identified by linker scanning mutagenesis. , 1986, Journal of molecular biology.

[35]  P. Eriksson,et al.  Protein-protein contacts in the glucocorticoid receptor homodimer influence its DNA binding properties. , 1990, The Journal of biological chemistry.

[36]  M. Grunstein,et al.  Nucleosome loss activates CUP1 and HIS3 promoters to fully induced levels in the yeast Saccharomyces cerevisiae , 1992, Molecular and cellular biology.

[37]  J. Mymryk,et al.  Dissection of progesterone receptor-mediated chromatin remodeling and transcriptional activation in vivo. , 1995, Genes & development.

[38]  R. Cortese,et al.  Amino‐terminal domain of NF1 binds to DNA as a dimer and activates adenovirus DNA replication. , 1990, The EMBO journal.

[39]  R. Wides,et al.  Structure and function of the adenovirus origin of replication , 1984, Cell.

[40]  O. Wrange,et al.  Translational positioning of a nucleosomal glucocorticoid response element modulates glucocorticoid receptor affinity. , 1993, Genes & development.

[41]  E. A. O'neill,et al.  The proline-rich transcriptional activator of CTF/NF-I is distinct from the replication and DNA binding domain , 1989, Cell.

[42]  M. Beato,et al.  Contacts between hormone receptor and DNA double helix within a glucocorticoid regulatory element of mouse mammary tumor virus. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[43]  F. Claret,et al.  A nuclear factor I-like activity and a liver-specific repressor govern estrogen-regulated in vitro transcription from the Xenopus laevis vitellogenin B1 promoter , 1989, Molecular and cellular biology.

[44]  Stephen K. Burley,et al.  Co-crystal structure of TBP recognizing the minor groove of a TATA element , 1993, Nature.

[45]  K. Yamamoto,et al.  Crystallographic analysis of the interaction of the glucocorticoid receptor with DNA , 2003, Nature.

[46]  T. Osborne,et al.  NF-I proteins from brain interact with the proenkephalin cAMP inducible enhancer. , 1991, Nucleic acids research.

[47]  W. Driel,et al.  Contactpoint analysis of the HeLa nuclear factor I recognition site reveals symmetrical binding at one side of the DNA helix. , 1987 .

[48]  L. Wu,et al.  Mechanism of dioxin action: Ah receptor-mediated increase in promoter accessibility in vivo. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[49]  T. Perlmann,et al.  Specific glucocorticoid receptor binding to DNA reconstituted in a nucleosome. , 1988, The EMBO journal.

[50]  E. Winnacker,et al.  Hydroxyl radical footprints reveal novel structural features around the NF I binding site in adenovirus DNA. , 1989, Nucleic acids research.

[51]  T. Perlmann,et al.  Quantitative analysis of the glucocorticoid receptor-DNA interaction at the mouse mammary tumor virus glucocorticoid response element. , 1990, The Journal of biological chemistry.