Signal Integration by DegS and RseB Governs the σ E-mediated Envelope Stress Response in Escherichia Coli

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2011 Jan 20

PMID 21245315

Citations 43

Authors

Rachna Chaba

Benjamin M Alba

Monica S Guo

Jungsan Sohn

Nidhi Ahuja

Robert T Sauer

Carol A Gross

Affiliations

Soon will be listed here.

Abstract

In Escherichia coli, the σ(E) transcription factor monitors and maintains outer membrane (OM) integrity by activating genes required for assembly of its two key components, outer membrane proteins (OMPs) and lipopolysaccharide (LPS) and by transcribing small RNAs to down-regulate excess unassembled OMPs. σ(E) activity is governed by the rate of degradation of its membrane-spanning anti-σ factor, RseA. Importantly, the DegS protease can initiate RseA cleavage only when activated by binding to unassembled OMPs. The prevalent paradigm has been that the σ(E) response is controlled by the amount of activated DegS. Here we demonstrate that inactivation of a second negative regulator, the periplasmic protein RseB, is also required for σ(E) induction in vivo. Moreover, OMPs, previously known only to activate DegS, also generate a signal to antagonize RseB inhibition. This signal may be lipid related, as RseB is structurally similar to proteins that bind lipids. We propose that the use of an AND gate enables σ(E) to sense and integrate multivariate signals from the envelope.

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References

Sperandeo P, Deho G, Polissi A . The lipopolysaccharide transport system of Gram-negative bacteria. Biochim Biophys Acta. 2009; 1791(7):594-602. DOI: 10.1016/j.bbalip.2009.01.011. View

Sperandeo P, Lau F, Carpentieri A, De Castro C, Molinaro A, Deho G . Functional analysis of the protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. J Bacteriol. 2008; 190(13):4460-9. PMC: 2446812. DOI: 10.1128/JB.00270-08. View

Cezairliyan B, Sauer R . Inhibition of regulated proteolysis by RseB. Proc Natl Acad Sci U S A. 2007; 104(10):3771-6. PMC: 1820659. DOI: 10.1073/pnas.0611567104. View

Wollmann P, Zeth K . The structure of RseB: a sensor in periplasmic stress response of E. coli. J Mol Biol. 2007; 372(4):927-941. DOI: 10.1016/j.jmb.2007.06.039. View

Tam C, Missiakas D . Changes in lipopolysaccharide structure induce the sigma(E)-dependent response of Escherichia coli. Mol Microbiol. 2005; 55(5):1403-12. DOI: 10.1111/j.1365-2958.2005.04497.x. View

Knowles T, Scott-Tucker A, Overduin M, Henderson I . Membrane protein architects: the role of the BAM complex in outer membrane protein assembly. Nat Rev Microbiol. 2009; 7(3):206-14. DOI: 10.1038/nrmicro2069. View

Sohn J, Grant R, Sauer R . OMP peptides activate the DegS stress-sensor protease by a relief of inhibition mechanism. Structure. 2009; 17(10):1411-21. PMC: 2764547. DOI: 10.1016/j.str.2009.07.017. View

Wilken C, Kitzing K, Kurzbauer R, Ehrmann M, Clausen T . Crystal structure of the DegS stress sensor: How a PDZ domain recognizes misfolded protein and activates a protease. Cell. 2004; 117(4):483-94. DOI: 10.1016/s0092-8674(04)00454-4. View

Hasselblatt H, Kurzbauer R, Wilken C, Krojer T, Sawa J, Kurt J . Regulation of the sigmaE stress response by DegS: how the PDZ domain keeps the protease inactive in the resting state and allows integration of different OMP-derived stress signals upon folding stress. Genes Dev. 2007; 21(20):2659-70. PMC: 2000328. DOI: 10.1101/gad.445307. View

10.

Valentin-Hansen P, Johansen J, Rasmussen A . Small RNAs controlling outer membrane porins. Curr Opin Microbiol. 2007; 10(2):152-5. DOI: 10.1016/j.mib.2007.03.001. View

11.

Hagan C, Kim S, Kahne D . Reconstitution of outer membrane protein assembly from purified components. Science. 2010; 328(5980):890-2. PMC: 2873164. DOI: 10.1126/science.1188919. View

12.

Klein G, Lindner B, Brabetz W, Brade H, Raina S . Escherichia coli K-12 Suppressor-free Mutants Lacking Early Glycosyltransferases and Late Acyltransferases: minimal lipopolysaccharide structure and induction of envelope stress response. J Biol Chem. 2009; 284(23):15369-89. PMC: 2708834. DOI: 10.1074/jbc.M900490200. View

13.

Chaba R, Grigorova I, Flynn J, Baker T, Gross C . Design principles of the proteolytic cascade governing the sigmaE-mediated envelope stress response in Escherichia coli: keys to graded, buffered, and rapid signal transduction. Genes Dev. 2007; 21(1):124-36. PMC: 1759897. DOI: 10.1101/gad.1496707. View

14.

De Las Penas A, Connolly L, Gross C . The sigmaE-mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of sigmaE. Mol Microbiol. 1997; 24(2):373-85. DOI: 10.1046/j.1365-2958.1997.3611718.x. View

15.

Ahuja N, Korkin D, Chaba R, Cezairliyan B, Sauer R, Kim K . Analyzing the interaction of RseA and RseB, the two negative regulators of the sigmaE envelope stress response, using a combined bioinformatic and experimental strategy. J Biol Chem. 2008; 284(8):5403-13. PMC: 2643490. DOI: 10.1074/jbc.M806012200. View

16.

Sohn J, Grant R, Sauer R . Allosteric activation of DegS, a stress sensor PDZ protease. Cell. 2007; 131(3):572-83. DOI: 10.1016/j.cell.2007.08.044. View

17.

Silhavy T, Kahne D, Walker S . The bacterial cell envelope. Cold Spring Harb Perspect Biol. 2010; 2(5):a000414. PMC: 2857177. DOI: 10.1101/cshperspect.a000414. View

18.

Ades S, Connolly L, Alba B, Gross C . The Escherichia coli sigma(E)-dependent extracytoplasmic stress response is controlled by the regulated proteolysis of an anti-sigma factor. Genes Dev. 1999; 13(18):2449-61. PMC: 317020. DOI: 10.1101/gad.13.18.2449. View

19.

Wu T, Malinverni J, Ruiz N, Kim S, Silhavy T, Kahne D . Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell. 2005; 121(2):235-45. DOI: 10.1016/j.cell.2005.02.015. View

20.

Kim D, Jin K, Kwon E, Ree M, Kim K . Crystal structure of RseB and a model of its binding mode to RseA. Proc Natl Acad Sci U S A. 2007; 104(21):8779-84. PMC: 1885579. DOI: 10.1073/pnas.0703117104. View

Signal Integration by DegS and RseB Governs the &#963; E-mediated Envelope Stress Response in Escherichia Coli

Signal Integration by DegS and RseB Governs the σ E-mediated Envelope Stress Response in Escherichia Coli