Domain Movements of the Enhancer-dependent Sigma Factor Drive DNA Delivery into the RNA Polymerase Active Site: Insights from Single Molecule Studies

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2014 Feb 21

PMID 24553251

Citations 13

Authors

Amit Sharma

Robert N Leach

Christopher Gell

Nan Zhang

Patricia C Burrows

Dale A Shepherd

Sivaramesh Wigneshweraraj

David Alastair Smith

Xiaodong Zhang

Martin Buck

Peter G Stockley

Roman Tuma

Affiliations

Soon will be listed here.

Abstract

Recognition of bacterial promoters is regulated by two distinct classes of sequence-specific sigma factors, σ(70) or σ(54), that differ both in their primary sequence and in the requirement of the latter for activation via enhancer-bound upstream activators. The σ(54) version controls gene expression in response to stress, often mediating pathogenicity. Its activator proteins are members of the AAA+ superfamily and use adenosine triphosphate (ATP) hydrolysis to remodel initially auto-inhibited holoenzyme promoter complexes. We have mapped this remodeling using single-molecule fluorescence spectroscopy. Initial remodeling is nucleotide-independent and driven by binding both ssDNA during promoter melting and activator. However, DNA loading into the RNA polymerase active site depends on co-operative ATP hydrolysis by the activator. Although the coupled promoter recognition and melting steps may be conserved between σ(70) and σ(54), the domain movements of the latter have evolved to require an activator ATPase.

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References

Cannon W, Wigneshweraraj S, Buck M . Interactions of regulated and deregulated forms of the sigma54 holoenzyme with heteroduplex promoter DNA. Nucleic Acids Res. 2002; 30(4):886-93. PMC: 100350. DOI: 10.1093/nar/30.4.886. View

Chaney M, Buck M . The sigma 54 DNA-binding domain includes a determinant of enhancer responsiveness. Mol Microbiol. 1999; 33(6):1200-9. DOI: 10.1046/j.1365-2958.1999.01566.x. View

Callaci S, Heyduk E, Heyduk T . Conformational changes of Escherichia coli RNA polymerase sigma70 factor induced by binding to the core enzyme. J Biol Chem. 1998; 273(49):32995-3001. DOI: 10.1074/jbc.273.49.32995. View

Vogel S, Schulz A, Rippe K . Binding affinity of Escherichia coli RNA polymerase*sigma54 holoenzyme for the glnAp2, nifH and nifL promoters. Nucleic Acids Res. 2002; 30(18):4094-101. PMC: 137104. DOI: 10.1093/nar/gkf519. View

Darst S, Kubalek E, Kornberg R . Three-dimensional structure of Escherichia coli RNA polymerase holoenzyme determined by electron crystallography. Nature. 1989; 340(6236):730-2. DOI: 10.1038/340730a0. View

Kapanidis A, Laurence T, Lee N, Margeat E, Kong X, Weiss S . Alternating-laser excitation of single molecules. Acc Chem Res. 2005; 38(7):523-33. DOI: 10.1021/ar0401348. View

Lisal J, Tuma R . Cooperative mechanism of RNA packaging motor. J Biol Chem. 2005; 280(24):23157-64. DOI: 10.1074/jbc.M502658200. View

Bordes P, Wigneshweraraj S, Chaney M, Dago A, Morett E, Buck M . Communication between Esigma(54) , promoter DNA and the conserved threonine residue in the GAFTGA motif of the PspF sigma-dependent activator during transcription activation. Mol Microbiol. 2004; 54(2):489-506. DOI: 10.1111/j.1365-2958.2004.04280.x. View

Buck M, Gallegos M, Studholme D, Guo Y, Gralla J . The bacterial enhancer-dependent sigma(54) (sigma(N)) transcription factor. J Bacteriol. 2000; 182(15):4129-36. PMC: 101881. DOI: 10.1128/JB.182.15.4129-4136.2000. View

10.

Burrows P, Joly N, Buck M . A prehydrolysis state of an AAA+ ATPase supports transcription activation of an enhancer-dependent RNA polymerase. Proc Natl Acad Sci U S A. 2010; 107(20):9376-81. PMC: 2889110. DOI: 10.1073/pnas.1001188107. View

11.

Kapanidis A, Lee N, Laurence T, Doose S, Margeat E, Weiss S . Fluorescence-aided molecule sorting: analysis of structure and interactions by alternating-laser excitation of single molecules. Proc Natl Acad Sci U S A. 2004; 101(24):8936-41. PMC: 428450. DOI: 10.1073/pnas.0401690101. View

12.

Burrows P, Severinov K, Ishihama A, Buck M, Wigneshweraraj S . Mapping sigma 54-RNA polymerase interactions at the -24 consensus promoter element. J Biol Chem. 2003; 278(32):29728-43. DOI: 10.1074/jbc.M303596200. View

13.

Popham D, Szeto D, Keener J, Kustu S . Function of a bacterial activator protein that binds to transcriptional enhancers. Science. 1989; 243(4891):629-35. DOI: 10.1126/science.2563595. View

14.

Carpousis A, Gralla J . Cycling of ribonucleic acid polymerase to produce oligonucleotides during initiation in vitro at the lac UV5 promoter. Biochemistry. 1980; 19(14):3245-53. DOI: 10.1021/bi00555a023. View

15.

Clegg R . Fluorescence resonance energy transfer and nucleic acids. Methods Enzymol. 1992; 211:353-88. DOI: 10.1016/0076-6879(92)11020-j. View

16.

Borodavka A, Tuma R, Stockley P . Evidence that viral RNAs have evolved for efficient, two-stage packaging. Proc Natl Acad Sci U S A. 2012; 109(39):15769-74. PMC: 3465389. DOI: 10.1073/pnas.1204357109. View

17.

Cannon W, Gallegos M, Buck M . Isomerization of a binary sigma-promoter DNA complex by transcription activators. Nat Struct Biol. 2000; 7(7):594-601. DOI: 10.1038/76830. View

18.

Ha T, Rasnik I, Cheng W, Babcock H, Gauss G, Lohman T . Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase. Nature. 2002; 419(6907):638-41. DOI: 10.1038/nature01083. View

19.

Schuler B, Lipman E, Steinbach P, Kumke M, Eaton W . Polyproline and the "spectroscopic ruler" revisited with single-molecule fluorescence. Proc Natl Acad Sci U S A. 2005; 102(8):2754-9. PMC: 549440. DOI: 10.1073/pnas.0408164102. View

20.

Guo Y, Lew C, Gralla J . Promoter opening by sigma(54) and sigma(70) RNA polymerases: sigma factor-directed alterations in the mechanism and tightness of control. Genes Dev. 2000; 14(17):2242-55. PMC: 316896. DOI: 10.1101/gad.794800. View