Bacterial enhancer-binding proteins: unlocking σ54-dependent gene transcription

Bacterial transcription relies on the binding of dissociable sigma (σ) factors to RNA polymerase (RNAP) for promoter specificity. The major variant sigma factor (σ54) forms a stable closed complex with RNAP bound to DNA that rarely spontaneously isomerises to an open complex. ATP hydrolysis by bacterial enhancer-binding proteins is used to remodel the RNAP–σ54–DNA closed complex. Recently, a wealth of structural information on bacterial enhancer-binding proteins has enabled unprecedented insights into their mechanism. These data provide a structural basis for nucleotide binding and hydrolysis, oligomerisation and the conversion of ATPase activity into remodelling events within the RNAP–σ54 closed complex, and represent advances towards a complete understanding of the σ54-dependent transcription activation mechanism.

[1]  P. Stockley,et al.  Mapping ATP-dependent Activation at a σ54 Promoter* , 2006, Journal of Biological Chemistry.

[2]  Sungdae Park,et al.  Two‐component signaling in the AAA+ ATPase DctD: binding Mg2+ and BeF3 selects between alternative dimeric states of the receiver domain , 2002, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[3]  A. Kolb,et al.  Protein‐induced DNA bending clarifies the architectural organization of the σ54‐dependent glnAp2 promoter , 2006, Molecular microbiology.

[4]  L. Joshua-Tor,et al.  Mechanism of DNA translocation in a replicative hexameric helicase , 2006, Nature.

[5]  N. Kunishima,et al.  Crystal structure of the Holliday junction migration motor protein RuvB from Thermus thermophilus HB8. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Hajime Niwa,et al.  Structure of the whole cytosolic region of ATP-dependent protease FtsH. , 2006, Molecular cell.

[7]  A. Wilkinson,et al.  AAA+ superfamily ATPases: common structure–diverse function , 2001, Genes to cells : devoted to molecular & cellular mechanisms.

[8]  David J. Studholme,et al.  DNA Binding Activity of the Escherichia coli Nitric Oxide Sensor NorR Suggests a Conserved Target Sequence in Diverse Proteobacteria , 2004, Journal of bacteriology.

[9]  D. Wemmer,et al.  High-resolution solution structure of the beryllofluoride-activated NtrC receiver domain. , 2003, Biochemistry.

[10]  Hajime Niwa,et al.  Structural basis of the nucleotide driven conformational changes in the AAA+ domain of transcription activator PspF. , 2006, Journal of molecular biology.

[11]  M. Buck,et al.  Functions of the sigma(54) region I in trans and implications for transcription activation. , 1999, The Journal of biological chemistry.

[12]  D. Yan,et al.  A dimeric two‐component receiver domain inhibits the σ54‐dependent ATPase in DctD , 2001 .

[13]  Tania A. Baker,et al.  Rebuilt AAA + motors reveal operating principles for ATP-fuelled machines , 2005, Nature.

[14]  R. Dixon,et al.  Domain Architectures of σ54-Dependent Transcriptional Activators , 2003 .

[15]  M. Buck,et al.  The ATP hydrolyzing transcription activator phage shock protein F of Escherichia coli: Identifying a surface that binds σ54 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[16]  S. Elderkin,et al.  Binding of transcriptional activators to sigma 54 in the presence of the transition state analog ADP-aluminum fluoride: insights into activator mechanochemical action. , 2001, Genes & development.

[17]  M. Buck,et al.  Structures and organisation of AAA+ enhancer binding proteins in transcriptional activation. , 2006, Journal of structural biology.

[18]  J. Berger,et al.  Evolutionary relationships and structural mechanisms of AAA+ proteins. , 2006, Annual review of biophysics and biomolecular structure.

[19]  N. Tucker,et al.  A non-haem iron centre in the transcription factor NorR senses nitric oxide , 2005, Nature.

[20]  David J. Studholme,et al.  The Bacterial Enhancer-Dependent ς54(ςN) Transcription Factor , 2000, Journal of bacteriology.

[21]  P. Hanson,et al.  AAA+ proteins: have engine, will work , 2005, Nature Reviews Molecular Cell Biology.

[22]  P. Tucker,et al.  Crystal structure of the central and C-terminal domain of the σ54-activator ZraR , 2005 .

[23]  C. Robinson,et al.  Structural Insights into the Activity of Enhancer-Binding Proteins , 2005, Science.

[24]  N. Tucker,et al.  DNA binding properties of the Escherichia coli nitric oxide sensor NorR: towards an understanding of the regulation of flavorubredoxin expression. , 2005, Biochemical Society transactions.

[25]  D. Wemmer,et al.  Negative regulation of AAA + ATPase assembly by two component receiver domains: a transcription activation mechanism that is conserved in mesophilic and extremely hyperthermophilic bacteria. , 2005, Journal of molecular biology.

[26]  Seok-Yong Lee,et al.  Regulation of the transcriptional activator NtrC1: structural studies of the regulatory and AAA+ ATPase domains. , 2003, Genes & development.

[27]  R. Finn,et al.  The second paradigm for activation of transcription. , 2005, Progress in nucleic acid research and molecular biology.

[28]  M. Buck,et al.  Mechanochemical ATPases and transcriptional activation , 2002, Molecular microbiology.

[29]  E. Nogales,et al.  The structural basis for regulated assembly and function of the transcriptional activator NtrC. , 2006, Genes & development.

[30]  M. Buck,et al.  Heterogeneous Nucleotide Occupancy Stimulates Functionality of Phage Shock Protein F, an AAA+ Transcriptional Activator* , 2006, Journal of Biological Chemistry.

[31]  R. Ebright,et al.  Transcription activation by catabolite activator protein (CAP). , 1999, Journal of molecular biology.

[32]  A. Ishihama.  Functional modulation of Escherichia coli RNA polymerase. , 2000, Annual review of microbiology.

[33]  Steven Hahn,et al.  Structure and mechanism of the RNA polymerase II transcription machinery , 2004, Nature Structural &Molecular Biology.

[34]  J G Pelton,et al.  Solution structure of the DNA-binding domain of NtrC with three alanine substitutions. , 1999, Journal of molecular biology.

[35]  E V Koonin,et al.  AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. , 1999, Genome research.

[36]  S. Busby,et al.  The regulation of bacterial transcription initiation , 2004, Nature Reviews Microbiology.

[37]  M. Buck,et al.  Functions of the ς54 Region I in Transand Implications for Transcription Activation* , 1999, The Journal of Biological Chemistry.