A Conserved Structural Module Regulates Transcriptional Responses to Diverse Stress Signals in Bacteria

Overview

Journal Mol Cell

Publisher Cell Press

Specialty Cell Biology

Date 2007 Sep 7

PMID 17803943

Citations 75

Authors

Elizabeth A Campbell

Roger Greenwell

Jennifer R Anthony

Sheng Wang

Lionel Lim

Kalyan Das

Heidi J Sofia

Timothy J Donohue

Seth A Darst

Affiliations

Soon will be listed here.

Abstract

A transcriptional response to singlet oxygen in Rhodobacter sphaeroides is controlled by the group IV sigma factor sigma(E) and its cognate anti-sigma ChrR. Crystal structures of the sigma(E)/ChrR complex reveal a modular, two-domain architecture for ChrR. The ChrR N-terminal anti-sigma domain (ASD) binds a Zn(2+) ion, contacts sigma(E), and is sufficient to inhibit sigma(E)-dependent transcription. The ChrR C-terminal domain adopts a cupin fold, can coordinate an additional Zn(2+), and is required for the transcriptional response to singlet oxygen. Structure-based sequence analyses predict that the ASD defines a common structural fold among predicted group IV anti-sigmas. These ASDs are fused to diverse C-terminal domains that are likely involved in responding to specific environmental signals that control the activity of their cognate sigma factor.

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References

Alberts I, Nadassy K, Wodak S . Analysis of zinc binding sites in protein crystal structures. Protein Sci. 1999; 7(8):1700-16. PMC: 2144076. DOI: 10.1002/pro.5560070805. View

Kang J, Paget M, Seok Y, Hahn M, Bae J, Hahn J . RsrA, an anti-sigma factor regulated by redox change. EMBO J. 1999; 18(15):4292-8. PMC: 1171505. DOI: 10.1093/emboj/18.15.4292. View

Jones D . Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol. 1999; 292(2):195-202. DOI: 10.1006/jmbi.1999.3091. View

Newman J, Falkowski M, Schilke B, Anthony L, Donohue T . The Rhodobacter sphaeroides ECF sigma factor, sigma(E), and the target promoters cycA P3 and rpoE P1. J Mol Biol. 1999; 294(2):307-20. DOI: 10.1006/jmbi.1999.3263. View

Cuff J, Barton G . Application of multiple sequence alignment profiles to improve protein secondary structure prediction. Proteins. 2000; 40(3):502-11. DOI: 10.1002/1097-0134(20000815)40:3<502::aid-prot170>3.0.co;2-q. View

Burger M, Woods R, McCarthy C, Beacham I . Temperature regulation of protease in Pseudomonas fluorescens LS107d2 by an ECF sigma factor and a transmembrane activator. Microbiology (Reading). 2000; 146 Pt 12:3149-3155. DOI: 10.1099/00221287-146-12-3149. View

Cogdell R, Howard T, Bittl R, Schlodder E, Geisenheimer I, Lubitz W . How carotenoids protect bacterial photosynthesis. Philos Trans R Soc Lond B Biol Sci. 2000; 355(1402):1345-9. PMC: 1692869. DOI: 10.1098/rstb.2000.0696. View

KROGH A, Larsson B, von Heijne G, Sonnhammer E . Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001; 305(3):567-80. DOI: 10.1006/jmbi.2000.4315. View

Sofia H, Chen G, Hetzler B, MILLER N . Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucleic Acids Res. 2001; 29(5):1097-106. PMC: 29726. DOI: 10.1093/nar/29.5.1097. View

10.

Harding M . Geometry of metal-ligand interactions in proteins. Acta Crystallogr D Biol Crystallogr. 2001; 57(Pt 3):401-11. DOI: 10.1107/s0907444900019168. View

11.

Paget M, Bae J, Hahn M, Li W, Kleanthous C, Roe J . Mutational analysis of RsrA, a zinc-binding anti-sigma factor with a thiol-disulphide redox switch. Mol Microbiol. 2001; 39(4):1036-47. DOI: 10.1046/j.1365-2958.2001.02298.x. View

12.

Newman J, Anthony J, Donohue T . The importance of zinc-binding to the function of Rhodobacter sphaeroides ChrR as an anti-sigma factor. J Mol Biol. 2001; 313(3):485-99. DOI: 10.1006/jmbi.2001.5069. View

13.

Campbell E, Muzzin O, Chlenov M, Sun J, Olson C, Weinman O . Structure of the bacterial RNA polymerase promoter specificity sigma subunit. Mol Cell. 2002; 9(3):527-39. DOI: 10.1016/s1097-2765(02)00470-7. View

14.

Campbell E, Masuda S, Sun J, Muzzin O, Olson C, Wang S . Crystal structure of the Bacillus stearothermophilus anti-sigma factor SpoIIAB with the sporulation sigma factor sigmaF. Cell. 2002; 108(6):795-807. DOI: 10.1016/s0092-8674(02)00662-1. View

15.

Vassylyev D, Sekine S, Laptenko O, Lee J, Vassylyeva M, Borukhov S . Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 A resolution. Nature. 2002; 417(6890):712-9. DOI: 10.1038/nature752. View

16.

Murakami K, Masuda S, Darst S . Structural basis of transcription initiation: RNA polymerase holoenzyme at 4 A resolution. Science. 2002; 296(5571):1280-4. DOI: 10.1126/science.1069594. View

17.

Helmann J . The extracytoplasmic function (ECF) sigma factors. Adv Microb Physiol. 2002; 46:47-110. DOI: 10.1016/s0065-2911(02)46002-x. View

18.

Li W, Stevenson C, Burton N, Jakimowicz P, Paget M, Buttner M . Identification and structure of the anti-sigma factor-binding domain of the disulphide-stress regulated sigma factor sigma(R) from Streptomyces coelicolor. J Mol Biol. 2002; 323(2):225-36. DOI: 10.1016/s0022-2836(02)00948-8. View

19.

Campbell E, Tupy J, Gruber T, Wang S, Sharp M, Gross C . Crystal structure of Escherichia coli sigmaE with the cytoplasmic domain of its anti-sigma RseA. Mol Cell. 2003; 11(4):1067-78. DOI: 10.1016/s1097-2765(03)00148-5. View

20.

Braun V, Mahren S, Ogierman M . Regulation of the FecI-type ECF sigma factor by transmembrane signalling. Curr Opin Microbiol. 2003; 6(2):173-80. DOI: 10.1016/s1369-5274(03)00022-5. View