Structural insights into the regulatory mechanism of the Pseudomonas aeruginosa YfiBNR system

Protein & Cell - Tập 7 Số 6 - Trang 403-416 - 2016
Min Xu1, Xuan Yang2, Xiu‐An Yang1, Lei Zhou1,3, Liu Tie-zheng1,3, Zusen Fan2, Tao Jiang1
1National Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China
2Chinese Academy of Sciences Key Laboratory of Infection and Immunity, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China
3University of Chinese Academy of Sciences, Beijing, 100049, China

Tóm tắt

Từ khóa


Tài liệu tham khảo

Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW et al (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66:213–221

Afonine PV, Grosse-Kunstleve RW, Echols N, Headd JJ, Moriarty NW, Mustyakimov M, Terwilliger TC, Urzhumtsev A, Zwart PH, Adams PD (2012) Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr D Biol Crystallogr 68:352–367

Beaumont HJ, Gallie J, Kost C, Ferguson GC, Rainey PB (2009) Experimental evolution of bet hedging. Nature 462:90–93

Boehm A, Kaiser M, Li H, Spangler C, Kasper CA, Ackermann M, Kaever V, Sourjik V, Roth V, Jenal U (2010) Second messenger-mediated adjustment of bacterial swimming velocity. Cell 141:107–116

Caly DL, Bellini D, Walsh MA, Dow JM, Ryan RP (2015) Targeting cyclic di-GMP signalling: a strategy to control biofilm formation? Curr Pharm Des 21:12–24

Camilli A, Bassler BL (2006) Bacterial small-molecule signaling pathways. Science 311:1113–1116

Choi KH, Kumar A, Schweizer HP (2006) A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbiol Methods 64:391–397

Desmarais SM, Cava F, de Pedro MA, Huang KC (2014) Isolation and preparation of bacterial cell walls for compositional analysis by ultra performance liquid chromatography. J Vis Exp 83:e51183

Duerig A, Abel S, Folcher M, Nicollier M, Schwede T, Amiot N, Giese B, Jenal U (2009) Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev 23:93–104

Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66:486–501

Evans TJ (2015) Small colony variants of Pseudomonas aeruginosa in chronic bacterial infection of the lung in cystic fibrosis. Future Microbiol 10:231–239

Giardina G, Paiardini A, Fernicola S, Franceschini S, Rinaldo S, Stelitano V, Cutruzzola F (2013) Investigating the allosteric regulation of YfiN from Pseudomonas aeruginosa: clues from the structure of the catalytic domain. PLoS One 8:e81324

Giddens SR, Jackson RW, Moon CD, Jacobs MA, Zhang XX, Gehrig SM, Rainey PB (2007) Mutational activation of niche-specific genes provides insight into regulatory networks and bacterial function in a complex environment. Proc Natl Acad Sci USA 104:18247–18252

Govan JR, Deretic V (1996) Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60:539–574

Grubman A, Phillips A, Thibonnier M, Kaparakis-Liaskos M, Johnson C, Thiberge JM, Radcliff FJ, Ecobichon C, Labigne A, de Reuse H. et al (2010) Vitamin B6 is required for full motility and virulence in Helicobacter pylori. MBio 1

Ha DG, O’Toole GA (2015) c-di-GMP and its effects on biofilm formation and dispersion: a Pseudomonas aeruginosa review. Microbiol Spectr 3, MB-0003-2014

Haussler S, Tummler B, Weissbrodt H, Rohde M, Steinmetz I (1999) Small-colony variants of Pseudomonas aeruginosa in cystic fibrosis. Clin Infect Dis 29:621–625

Haussler S, Ziegler I, Lottel A, von Gotz F, Rohde M, Wehmhohner D, Saravanamuthu S, Tummler B, Steinmetz I (2003) Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic fibrosis lung infection. J Med Microbiol 52:295–301

Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7:263–273

Hickman JW, Tifrea DF, Harwood CS (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci USA 102:14422–14427

Hmelo LR, Borlee BR, Almblad H, Love ME, Randall TE, Tseng BS, Lin C, Irie Y, Storek KM, Yang JJ et al (2015) Precision-engineering the Pseudomonas aeruginosa genome with two-step allelic exchange. Nat Protoc 10:1820–1841

Holm L, Rosenstrom P (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38:W545–W549

Huertas MG, Zarate L, Acosta IC, Posada L, Cruz DP, Lozano M, Zambrano MM (2014) Klebsiella pneumoniae yfiRNB operon affects biofilm formation, polysaccharide production and drug susceptibility. Microbiology 160:2595–2606

Hufnagel DA, DePas WH, Chapman MR (2014) The disulfide bonding system suppresses CsgD-independent cellulose production in Escherichia coli. J Bacteriol 196:3690–3699

Jenal U (2004) Cyclic di-guanosine-monophosphate comes of age: a novel secondary messenger involved in modulating cell surface structures in bacteria? Curr Opin Microbiol 7:185–191

Kirillina O, Fetherston JD, Bobrov AG, Abney J, Perry RD (2004) HmsP, a putative phosphodiesterase, and HmsT, a putative diguanylate cyclase, control Hms-dependent biofilm formation in Yersinia pestis. Mol Microbiol 54:75–88

Kirisits MJ, Prost L, Starkey M, Parsek MR (2005) Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 71:4809–4821

Kulasakara H, Lee V, Brencic A, Liberati N, Urbach J, Miyata S, Lee DG, Neely AN, Hyodo M, Hayakawa Y et al (2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proc Natl Acad Sci USA 103:2839–2844

Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283–291

Lebedev AA, Vagin AA, Murshudov GN (2008) Model preparation in MOLREP and examples of model improvement using X-ray data. Acta Crystallogr D Biol Crystallogr 64:33–39

Li S, Li T, Xu Y, Zhang Q, Zhang W, Che S, Liu R, Wang Y, Bartlam M (2015) Structural insights into YfiR sequestering by YfiB in Pseudomonas aeruginosa PAO1. Sci Rep 5:16915

Malone JG (2015) Role of small colony variants in persistence of Pseudomonas aeruginosa infections in cystic fibrosis lungs. Infect Drug Resist 8:237–247

Malone JG, Jaeger T, Spangler C, Ritz D, Spang A, Arrieumerlou C, Kaever V, Landmann R, Jenal U (2010) YfiBNR mediates cyclic di-GMP dependent small colony variant formation and persistence in Pseudomonas aeruginosa. PLoS Pathog 6:e1000804

Malone JG, Jaeger T, Manfredi P, Dotsch A, Blanka A, Bos R, Cornelis GR, Haussler S, Jenal U (2012) The YfiBNR signal transduction mechanism reveals novel targets for the evolution of persistent Pseudomonas aeruginosa in cystic fibrosis airways. PLoS Pathog 8:e1002760

Matias VR, Al-Amoudi A, Dubochet J, Beveridge TJ (2003) Cryo-transmission electron microscopy of frozen-hydrated sections of Escherichia coli and Pseudomonas aeruginosa. J Bacteriol 185:6112–6118

Meroueh SO, Bencze KZ, Hesek D, Lee M, Fisher JF, Stemmler TL, Mobashery S (2006) Three-dimensional structure of the bacterial cell wall peptidoglycan. Proc Natl Acad Sci USA 103:4404–4409

Navarro MV, Newell PD, Krasteva PV, Chatterjee D, Madden DR, O’Toole GA, Sondermann H (2011) Structural basis for c-di-GMP-mediated inside-out signaling controlling periplasmic proteolysis. PLoS Biol 9:e1000588

Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307–326

Parsek MR, Singh PK (2003) Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 57:677–701

Parsons LM, Lin F, Orban J (2006) Peptidoglycan recognition by Pal, an outer membrane lipoprotein. Biochemistry 45:2122–2128

Pesavento C, Hengge R (2009) Bacterial nucleotide-based second messengers. Curr Opin Microbiol 12:170–176

Raterman EL, Shapiro DD, Stevens DJ, Schwartz KJ, Welch RA (2013) Genetic analysis of the role of yfiR in the ability of Escherichia coli CFT073 to control cellular cyclic dimeric GMP levels and to persist in the urinary tract. Infect Immun 81:3089–3098

Reinhardt A, Kohler T, Wood P, Rohner P, Dumas JL, Ricou B, van Delden C (2007) Development and persistence of antimicrobial resistance in Pseudomonas aeruginosa: a longitudinal observation in mechanically ventilated patients. Antimicrob Agents Chemother 51:1341–1350

Ren GX, Yan HQ, Zhu H, Guo XP, Sun YC (2014) HmsC, a periplasmic protein, controls biofilm formation via repression of HmsD, a diguanylate cyclase in Yersinia pestis. Environ Microbiol 16:1202–1216

Romling U, Galperin MY, Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77:1–52

Ross P, Weinhouse H, Aloni Y, Michaeli D, Weinberger-Ohana P, Mayer R, Braun S, de Vroom E, van der Marel GA, van Boom JH et al (1987) Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325:279–281

Ross P, Mayer R, Benziman M (1991) Cellulose biosynthesis and function in bacteria. Microbiol Rev 55:35–58

Sanchez-Torres V, Hu H, Wood TK (2011) GGDEF proteins YeaI, YedQ, and YfiN reduce early biofilm formation and swimming motility in Escherichia coli. Appl Microbiol Biotechnol 90:651–658

Schirmer T, Jenal U (2009) Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol 7:724–735

Schuck P (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J 78:1606–1619

Shimazaki J, Furukawa S, Ogihara H, Morinaga Y (2012) L-Tryptophan prevents Escherichia coli biofilm formation and triggers biofilm degradation. Biochem Biophys Res Commun 419:715–718

Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, D’Argenio DA, Miller SI, Ramsey BW, Speert DP, Moskowitz SM et al (2006) Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 103:8487–8492

Tamayo R, Tischler AD, Camilli A (2005) The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J Biol Chem 280:33324–33330

Ueda A, Wood TK (2009) Connecting quorum sensing, c-di-GMP, pel polysaccharide, and biofilm formation in Pseudomonas aeruginosa through tyrosine phosphatase TpbA (PA3885). PLoS Pathog 5:e1000483

Xu K, Li S, Yang W, Li K, Bai Y, Xu Y, Jin J, Wang Y, Bartlam M (2015) Structural and biochemical analysis of tyrosine phosphatase related to biofilm formation A (TpbA) from the opportunistic pathogen Pseudomonas aeruginosa PAO1. PLoS One 10:e0124330

Yang X, Yang XA, Xu M, Zhou L, Fan Z, Jiang T (2015) Crystal structures of YfiR from Pseudomonas aeruginosa in two redox states. Biochem Biophys Res Commun 461:14–20