The transcription activation domains of Fos and Jun induce DNA bending through electrostatic interactions

Transcription factor‐induced DNA bending is essential for the assembly of active transcription complexes at many promoters. However, most eukaryotic transcription regulatory proteins have modular DNA‐binding and activation domains, which appeared to exclude DNA bending as a mechanism of transcription activation by these proteins. We show that the transcription activation domains of Fos and Jun induce DNA bending. In chimeric proteins, the transcription activation domains induce DNA bending independent of the DNA‐binding domains. DNA bending by the chimeric proteins is directed diametrically away from the transcription activation domains. Therefore, the opposite directions of DNA bending by Fos and Jun are caused, in part, by the opposite locations of the transcription activation domains relative to the DNA‐binding domains in these proteins. DNA bending is reduced in the presence of multivalent cations, indicating that electrostatic interactions contribute to DNA bending by Fos and Jun. Consequently, regions outside the minimal DNA‐binding domain can influence DNA structure, and may thereby contribute to the architectural reorganization of the promoter region required for gene activation.

[1]  T. Kerppola,et al.  DNA bending by Fos–Jun and the orientation of heterodimer binding depend on the sequence of the AP‐1 site , 1997, The EMBO journal.

[2]  T. Kerppola,et al.  Structural basis of DNA bending and oriented heterodimer binding by the basic leucine zipper domains of Fos and Jun. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[3]  T. Curran,et al.  c‐Jun stimulates origin‐dependent DNA unwinding by polyomavirus large Tantigen. , 1996, The EMBO journal.

[4]  T. Kerppola Fos and Jun bend the AP-1 site: effects of probe geometry on the detection of protein-induced DNA bending. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[5]  C. Switzer,et al.  DNA bending by hexamethylene-tethered ammonium ions. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[6]  T. Curran,et al.  Fos-Jun dimerization promotes interaction of the basic region with TFIIE-34 and TFIIF , 1996, Molecular and cellular biology.

[7]  Evaluating Electrostatic Contributions to Binding with the Use of Protein Charge Ladders , 1996, Science.

[8]  R. Tjian,et al.  Contacts in Context: Promoter Specificity and Macromolecular Interactions in Transcription , 1996, Cell.

[9]  Dimitris Thanos,et al.  Reversal of intrinsic DNA bends in the IFNβ gene enhancer by transcription factors and the architectural protein HMG I(Y) , 1995, Cell.

[10]  A. Vershon,et al.  Altered DNA Recognition and Bending by Insertions in the α2 Tail of the Yeast a1/α2 Homeodomain Heterodimer , 1995, Science.

[11]  C. Wolberger,et al.  Crystal Structure of the MATa1/MATα2 Homeodomain Heterodimer Bound to DNA , 1995, Science.

[12]  J. Becker,et al.  DNA loops induced by cooperative binding of transcriptional activator proteins and preinitiation complexes. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[13]  David A. Case,et al.  Structural basis for DNA bending by the architectural transcription factor LEF-1 , 1995, Nature.

[14]  S. Harvey,et al.  Dehydrating agents sharply reduce curvature in DNAs containing A tracts. , 1995, Nucleic acids research.

[15]  R Grosschedl,et al.  Assembly and function of a TCR alpha enhancer complex is dependent on LEF-1-induced DNA bending and multiple protein-protein interactions. , 1995, Genes & development.

[16]  J. Bradner,et al.  DNA-bend modulation in a repressor-to-activator switching mechanism , 1995, Nature.

[17]  Richard J Smeyne,et al.  Regulation of c-fos expression in transgenic mice requires multiple interdependent transcription control elements , 1995, Neuron.

[18]  J. N. Mark Glover,et al.  Crystal structure of the heterodimeric bZIP transcription factor c-Fos–c-Jun bound to DNA , 1995, Nature.

[19]  L. J. Maher,et al.  DNA bending by asymmetric phosphate neutralization. , 1994, Science.

[20]  E. Wagner,et al.  c-Fos: a key regulator of osteoclast-macrophage lineage determination and bone remodeling. , 1994, Science.

[21]  Andrew J. Bannister,et al.  c-Fos-induced activation of a TATA-box-containing promoter involves direct contact with TATA-box-binding protein , 1994, Molecular and cellular biology.

[22]  Barry Honig,et al.  Salt Effects on Protein-DNA Interactions: The λcI Repressor and EcoRI Endonuclease , 1994 .

[23]  D. Goodsell,et al.  "...the tyranny of the lattice...". , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[24]  S. Phillips,et al.  Electrostatic activation of Escherichia coli methionine repressor. , 1994, Structure.

[25]  K. Sharp,et al.  Salt effects on protein-DNA interactions. The lambda cI repressor and EcoRI endonuclease. , 1994, Journal of molecular biology.

[26]  M. Gilman,et al.  DNA bending and orientation-dependent function of YY1 in the c-fos promoter. , 1993, Genes & development.

[27]  S. Lippard,et al.  High-mobility-group 1 protein mediates DNA bending as determined by ring closures. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

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

[29]  Steven Hahn,et al.  Crystal structure of a yeast TBP/TATA-box complex , 1993, Nature.

[30]  E. Wagner,et al.  c-Jun is essential for normal mouse development and hepatogenesis , 1993, Nature.

[31]  T. Richmond,et al.  The X-ray structure of the GCN4-bZIP bound to ATF/CREB site DNA shows the complex depends on DNA flexibility. , 1993, Journal of molecular biology.

[32]  J. Pérez-Martín,et al.  Protein-induced bending as a transcriptional switch. , 1993, Science.

[33]  J A McCammon,et al.  Poisson-Boltzmann analysis of the lambda repressor-operator interaction. , 1992, Biophysical journal.

[34]  Andrew J. Bannister,et al.  Conserved motifs in Fos and Jun define a new class of activation domain. , 1992, Genes & development.

[35]  D M Crothers,et al.  Protein-induced bending and DNA cyclization. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[36]  D M Crothers,et al.  Global features of DNA structure by comparative gel electrophoresis. , 1992, Methods in enzymology.

[37]  T. Curran,et al.  DNA bending by Fos and Jun: the flexible hinge model. , 1991, Science.

[38]  P. S. Kim,et al.  X-ray structure of the GCN4 leucine zipper, a two-stranded, parallel coiled coil. , 1991, Science.

[39]  T. Steitz,et al.  Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees , 1991, Science.

[40]  T. Curran,et al.  Fos-Jun heterodimers and jun homodimers bend DNA in opposite orientations: Implications for transcription factor cooperativity , 1991, Cell.

[41]  D. Luk,et al.  Transcriptional regulation by Fos and Jun in vitro: interaction among multiple activator and regulatory domains , 1991, Molecular and cellular biology.

[42]  R F Schleif,et al.  DNA looping and unlooping by AraC protein , 1990, Science.

[43]  S. Kustu,et al.  The integration host factor stimulates interaction of RNA polymerase with NIFA, the transcriptional activator for nitrogen fixation operons , 1990, Cell.

[44]  B. Matthews,et al.  Protein-DNA conformational changes in the crystal structure of a lambda Cro-operator complex. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[45]  W. DeGrado,et al.  Design of DNA-binding peptides based on the leucine zipper motif. , 1990, Science.

[46]  P. S. Kim,et al.  Sequence-specific DNA binding by a short peptide dimer. , 1990, Science.

[47]  P. Dervan,et al.  Structural motif of the GCN4 DNA binding domain characterized by affinity cleaving. , 1990, Science.

[48]  D M Crothers,et al.  Intrinsically bent DNA. , 1990, The Journal of biological chemistry.

[49]  H. Echols,et al.  DNA looping in cellular repression of transcription of the galactose operon. , 1990, Genes & development.

[50]  T. Steitz,et al.  Crystal lattice packing is important in determining the bend of a DNA dodecamer containing an adenine tract. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[51]  J. F. Thompson,et al.  Empirical estimation of protein-induced DNA bending angles: applications to lambda site-specific recombination complexes. , 1988, Nucleic acids research.

[52]  D. Crothers,et al.  DNA bend direction by phase sensitive detection , 1987, Nature.

[53]  Alan R. Fersht,et al.  Tailoring the pH dependence of enzyme catalysis using protein engineering , 1985, Nature.

[54]  A. Rich,et al.  Asymmetric lateral distribution of unshielded phosphate groups in nucleosomal DNA and its role in DNA bending. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[55]  G. S. Manning The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides , 1978, Quarterly Reviews of Biophysics.

[56]  W. Wooster,et al.  Crystal structure of , 2005 .