Solution structure of the c-terminal core domain of human TFIIB: Similarity to cyclin A and interaction with TATA-binding protein

TFIIB is an essential component of the machinery that transcribes protein-coding genes. The three-dimensional structure of the human TFIIB core domain (TFIIBc) has been determined using multidimensional heteronuclear magnetic resonance spectroscopy. The molecule consists of two direct repeats that adopt similar alpha-helical folds, conferring pseudo-twofold symmetry. An extensive, central basic surface including an amphipathic alpha helix is critical to the function of TFIIB as a bridge between the TBP-promoter complex and RNA polymerase II and associated general and regulatory transcription factors. Similarities between the TFIIBc and cyclin A folds indicate that elements of the eukaryotic cell cycle control apparatus evolved from more fundamental transcriptional control components, demonstrating a link between the transcription and cell cycle molecular machineries.

[1]  P. Kraulis.  A program to produce both detailed and schematic plots of protein structures , 1991 .

[2]  Michael Hampsey,et al.  The yeast SUA7 gene encodes a homolog of human transcription factor TFIIB and is required for normal start site selection in vivo , 1992, Cell.

[3]  D. Reinberg,et al.  Multiple functional domains of human transcription factor IIB: distinct interactions with two general transcription factors and RNA polymerase II. , 1993, Genes & development.

[4]  M. Horikoshi,et al.  Isolation and characterization of a cDNA encoding Drosophila transcription factor TFIIB. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[5]  M. Horikoshi,et al.  Functional dissection of TFIIB domains required for TFIIB–TFIID–promoter complex formation and basal transcription activity , 1993, Nature.

[6]  R. Conaway,et al.  General initiation factors for RNA polymerase II. , 1993, Annual review of biochemistry.

[7]  M. Horikoshi,et al.  Transcription factor TFIIB sites important for interaction with promoter-bound TFIID. , 1993, Science.

[8]  S. Harrison,et al.  Delineation of two functional regions of transcription factor TFIIB. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[9]  P. Londei,et al.  Complete nucleotide sequence of an archaeal (Pyrococcus woesei) gene encoding a homolog of eukaryotic transcription factor IIB (TFIIB). , 1993, Nucleic acids research.

[10]  Michael R. Green,et al.  Interaction between an acidic activator and transcription factor TFIIB is required for transcriptional activation , 1993, Nature.

[11]  Kornelia Polyak,et al.  Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex , 1995, Nature.

[12]  M. Swindells,et al.  Intrinsic φ,ψ propensities of amino acids, derived from the coil regions of known structures , 1995, Nature Structural Biology.

[13]  S. Buratowski,et al.  Functional domains of transcription factor TFIIB. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[14]  S. Hahn,et al.  Model for binding of transcription factor TFIIB to the TBP-DNA complex , 1995, Nature.

[15]  J. D. Thompson,et al.  Evidence for a protein domain superfamily shared by the cyclins, TFIIB and RB/p107. , 1994, Nucleic acids research.

[16]  D. Bacon,et al.  A fast algorithm for rendering space-filling molecule pictures , 1988 .

[17]  Yang Li,et al.  A multiprotein mediator of transcriptional activation and its interaction with the C-terminal repeat domain of RNA polymerase II , 1994, Cell.

[18]  A. Hoffmann,et al.  Crystal structure of TFIID TATA-box binding protein , 1992, Nature.

[19]  G J Barton,et al.  ALSCRIPT: a tool to format multiple sequence alignments. , 1993, Protein engineering.

[20]  N. Go,et al.  Common spatial arrangements of backbone fragments in homologous and non-homologous proteins. , 1992, Journal of molecular biology.

[21]  L. Kay,et al.  Enhanced-Sensitivity Triple-Resonance Spectroscopy with Minimal H2O Saturation , 1994 .

[22]  K Wüthrich,et al.  Pseudo-structures for the 20 common amino acids for use in studies of protein conformations by measurements of intramolecular proton-proton distance constraints with nuclear magnetic resonance. , 1983, Journal of molecular biology.

[23]  I. Willis,et al.  PCF4 encodes an RNA polymerase III transcription factor with homology to TFIIB , 1992, Cell.

[24]  S. Inouye,et al.  Unusual helix-containing greek keys in development-specific Ca(2+)-binding protein S. 1H, 15N, and 13C assignments and secondary structure determined with the use of multidimensional double and triple resonance heteronuclear NMR spectroscopy. , 1994, Biochemistry.

[25]  S. Buratowski,et al.  A suppressor of TBP mutations encodes an RNA polymerase III transcription factor with homology to TFIIB , 1992, Cell.

[26]  R. Tjian,et al.  Drosophila TAFII40 interacts with both a VP16 activation domain and the basal transcription factor TFIIB , 1993, Cell.

[27]  R. Tjian,et al.  Functional domains and upstream activation properties of cloned human TATA binding protein. , 1990, Science.

[28]  H. Jäckle,et al.  Control of transcription by Krüppel through interactions with TFIIB and TFIIEβ , 1995, Nature.

[29]  R. Roeder,et al.  Potential RNA polymerase II-induced interactions of transcription factor TFIIB , 1993, Molecular and cellular biology.

[30]  R. Young,et al.  Association of Cdk-activating kinase subunits with transcription factor TFIIH , 1995, Nature.

[31]  J. Hoeijmakers,et al.  The MO15 cell cycle kinase is associated with the TFIIH transcription-DNA repair factor , 1994, Cell.

[32]  R. Tjian,et al.  Cloning and expression of human TAFII250: a TBP-associated factor implicated in cell-cycle regulation , 1993, Nature.

[33]  D. Reinberg,et al.  Initiation of transcription by RNA polymerase II: a multi-step process. , 1993, Progress in nucleic acid research and molecular biology.

[34]  A. Gronenborn,et al.  Three-dimensional structure of potato carboxypeptidase inhibitor in solution. A study using nuclear magnetic resonance, distance geometry, and restrained molecular dynamics. , 1987, Biochemistry.

[35]  K. Sharp,et al.  Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons , 1991, Proteins.

[36]  Chris Sander,et al.  TFIIB, an evolutionary link between the transcription machineries of archaebacteria and eukaryotes , 1992, Cell.

[37]  M. Horikoshi,et al.  The p250 subunit of native TATA box-binding factor TFIID is the cell-cycle regulatory protein CCG1 , 1993, Nature.

[38]  J. Manley,et al.  A direct interaction between a glutamine-rich activator and the N terminus of TFIIB can mediate transcriptional activation in vivo , 1995, Molecular and cellular biology.

[39]  M. Nilges,et al.  Sampling Properties of Simulated Annealing and Distance Geometry , 1991 .

[40]  J. Manley,et al.  Interaction between a transcriptional activator and transcription factor IIB in vivo , 1993, Nature.

[41]  L. Kay,et al.  Simultaneous Acquisition of 15N- and 13C-Edited NOE Spectra of Proteins Dissolved in H2O , 1994 .

[42]  Jeffrey C. Hoch,et al.  Computational Aspects of the Study of Biological Macromolecules by Nuclear Magnetic Resonance Spectroscopy , 1991, NATO ASI Series.

[43]  D. Reinberg,et al.  Cloning of a human gene encoding the general transcription initiation factor IIB , 1991, Nature.

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

[45]  M. Haussler,et al.  Transcription factor TFIIB and the vitamin D receptor cooperatively activate ligand-dependent transcription. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Michael R. Green,et al.  Eukaryotic activators function during multiple steps of preinitiation complex assembly , 1993, Nature.

[47]  Timothy F. Havel,et al.  Protein structures in solution by nuclear magnetic resonance and distance geometry. The polypeptide fold of the basic pancreatic trypsin inhibitor determined using two different algorithms, DISGEO and DISMAN. , 1987, Journal of molecular biology.

[48]  R. Kornberg,et al.  RNA polymerase II initiation factor interactions and transcription start site selection. , 1994, Science.

[49]  P. Sharp,et al.  Five intermediate complexes in transcription initiation by RNA polymerase II , 1989, Cell.

[50]  S. Inouye,et al.  NMR-derived three-dimensional solution structure of protein S complexed with calcium. , 1994, Structure.

[51]  Richard A. Young,et al.  An RNA polymerase II holoenzyme responsive to activators , 1994, Nature.

[52]  M. Horikoshi,et al.  Sequence of general transcription factor TFIIB and relationships to other initiation factors. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

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

[54]  Masami Horikoshi,et al.  Highly conserved core domain and unique N terminus with presumptive regulatory motifs in a human TATA factor (TFIID) , 1990, Nature.

[55]  L. Kay,et al.  Backbone 1H and 15N resonance assignments of the N-terminal SH3 domain of drk in folded and unfolded states using enhanced-sensitivity pulsed field gradient NMR techniques , 1994, Journal of biomolecular NMR.

[56]  R. J. Kelleher,et al.  Effects of activation-defective TBP mutations on transcription initiation in yeast , 1994, Nature.

[57]  S. Hahn,et al.  A yeast TFIIB-related factor involved in RNA polymerase III transcription. , 1992, Genes & development.

[58]  Paul C. Driscoll,et al.  Practical aspects of proton-carbon-carbon-proton three-dimensional correlation spectroscopy of 13C-labeled proteins , 1990 .

[59]  L. Kay,et al.  Gradient-Enhanced Triple-Resonance Three-Dimensional NMR Experiments with Improved Sensitivity , 1994 .

[60]  D. Wishart,et al.  The 13C Chemical-Shift Index: A simple method for the identification of protein secondary structure using 13C chemical-shift data , 1994, Journal of biomolecular NMR.