The inhibitory site of a diguanylate cyclase is a necessary element for interaction and signaling with an effector protein

Journal of Bacteriology

Volumn 198, Issue 11, 2016, Pages 1595-1603

  Dahlstrom, Kurt M ^a   Giglio, Krista M ^b   Sondermann, Holger ^b   O'Toolea, George A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; BACTERIAL PROTEIN; CYCLIC DIGUANYLATE; CYCLIC NUCLEOTIDE; DIGUANYLATE CYCLASE; PROTEIN GCBC; PROTEIN LAPD; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; LYASE;

ARTICLE; AUTOINHIBITORY SITE; BACTERIUM ISOLATE; BIOFILM; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME STRUCTURE; ESCHERICHIA COLI; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PSEUDOMONAS FLUORESCENS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION;

BACTERIAL PROTEINS; BIOFILMS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MUTATION; PHOSPHORUS-OXYGEN LYASES; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS FLUORESCENS; SIGNAL TRANSDUCTION;

EID: 84971572630     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00090-16     Document Type: Article

References (27)

1. Galperin MY, Nikolskaya AN, Koonin EV. 2001. Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203:11-21. http://dx.doi.org/10.1111/j.1574-6968.2001.tb10814.x.
2. Ha DG, Richman ME, O'Toole GA. 2014. Deletion mutant library for investigation of functional outputs of cyclic diguanylate metabolism in Pseudomonas aeruginosa PA14. Appl Environ Microbiol 80:3384-3393. http://dx.doi.org/10.1128/AEM.00299-14.
3. Kulasakara H, Lee V, Brencic A, Liberati N, Urbach J, Miyata S, Lee DG, Neely AN, Hyodo M, Hayakawa Y, Ausubel FM, Lory S. 2006. Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3=-5=)-cyclic-GMP in virulence. Proc Natl Acad Sci U S A 103:2839-2844. http://dx.doi.org/10.1073/pnas .0511090103.
4. Lindenberg S, Klauck G, Pesavento C, Klauck E, Hengge R. 2013. The EAL domain protein YciR acts as a trigger enzyme in a c-di-GMP signalling cascade in E. coli biofilm control. EMBO J 32:2001-2014. http://dx .doi.org/10.1038/emboj.2013.120.
5. Merritt JH, Ha DG, Cowles KN, Lu W, Morales DK, Rabinowitz J, Gitai Z, O'Toole GA. 2010. Specific control of Pseudomonas aeruginosa surfaceassociated behaviors by two c-di-GMP diguanylate cyclases. mBio 1:e00183-10. http://dx.doi.org/10.1128/mBio.00183-10.
6. Newell PD, Yoshioka S, Hvorecny KL, Monds RD, O'Toole GA. 2011. Systematic analysis of diguanylate cyclases that promote biofilm formation by Pseudomonas fluorescens Pf0-1. J Bacteriol 193:4685-4698. http: //dx.doi.org/10.1128/JB.05483-11.
7. Christen B, Christen M, Paul R, Schmid F, Folcher M, Jenoe P, Meuwly M, Jenal U. 2006. Allosteric control of cyclic di-GMP signaling. J Biol Chem 281:32015-32024. http://dx.doi.org/10.1074/jbc.M603589200.
8. Hunter JL, Severin GB, Koestler BJ, Waters CM. 2014. The Vibrio cholerae diguanylate cyclase VCA0965 has an AGDEF active site and synthesizes cyclic di-GMP. BMC Microbiol 14:22. http://dx.doi.org/10.1186/1471-2180-14-22.
9. Pultz IS, Christen M, Kulasekara HD, Kennard A, Kulasekara B, Miller SI. 2012. The response threshold of Salmonella PilZ domain proteins is determined by their binding affinities for c-di-GMP. Mol Microbiol 86: 1424-1440. http://dx.doi.org/10.1111/mmi.12066.
10. Abel S, Bucher T, Nicollier M, Hug I, Kaever V, Abel Zur Wiesch P, Jenal U. 2013. Bi-modal distribution of the second messenger c-di-GMP controls cell fate and asymmetry during the Caulobacter cell cycle. PLoS Genet 9:e1003744. http://dx.doi.org/10.1371/journal.pgen.1003744.
11. Dahlstrom KM, Giglio KM, Collins AJ, Sondermann H, O'Toole GA. 2015. Contribution of physical interactions to signaling specificity between a diguanylate cyclase and its effector. mBio 6:e01978-15. http://dx .doi.org/10.1128/mBio.01978-15.
12. Chatterjee D, Cooley RB, Boyd CD, Mehl RA, O'Toole GA, Sondermann H. 2014. Mechanistic insight into the conserved allosteric regulation of periplasmic proteolysis by the signaling molecule cyclic-di-GMP. eLife 3:e03650. http://dx.doi.org/10.7554/eLife.03650.
13. Newell PD, Boyd CD, Sondermann H, O'Toole GA. 2011. A c-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage. PLoS Biol 9:e1000587. http://dx.doi.org/10.1371/journal .pbio.1000587.
14. Newell PD, Monds RD, O'Toole GA. 2009. LapD is a bis-(3=,5=)-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0-1. Proc Natl Acad Sci U S A 106:3461-3466. http: //dx.doi.org/10.1073/pnas.0808933106.
15. Simon R, Priefer U, Puhler A. 1983. A broad host range mobilization system for in vivo genetic engineering-transposon mutagenesis in gramnegative bacteria. Nat Biotechnol 1:784-791. http://dx.doi.org/10.1038/nbt1183-784.
16. Karimova G, Pidoux J, Ullmann A, Ladant D. 1998. A bacterial twohybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci U S A 95:5752-5756. http://dx.doi.org/10.1073/pnas.95.10.5752.
17. O'Toole GA, Kolter R. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28:449-461. http://dx.doi.org /10.1046/j.1365-2958.1998.00797.x.
18. Monds RD, Newell PD, Wagner JC, Schwartzman JA, Lu W, Rabinowitz JD, O'Toole GA. 2010. Di-adenosine tetraphosphate (Ap4A) metabolism impacts biofilm formation by Pseudomonas fluorescens via modulation of c-di-GMP-dependent pathways. J Bacteriol 192:3011-3023. http: //dx.doi.org/10.1128/JB.01571-09.
19. Chan C, Paul R, Samoray D, Amiot NC, Giese B, Jenal U, Schirmer T. 2004. Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci U S A 101:17084-17089. http://dx.doi.org/10.1073/pnas.0406134101.
20. De N, Navarro MV, Raghavan RV, Sondermann H. 2009. Determinants for the activation and autoinhibition of the diguanylate cyclase response regulator WspR. J Mol Biol 393:619-633. http://dx.doi.org/10.1016/j.jmb .2009.08.030.
21. De N, Pirruccello M, Krasteva PV, Bae N, Raghavan RV, Sondermann H. 2008. Phosphorylation-independent regulation of the diguanylate cyclase WspR. PLoS Biol 6:e67. http://dx.doi.org/10.1371/journal.pbio .0060067.
22. Deepthi A, Liew CW, Liang ZX, Swaminathan K, Lescar J. 2014. Structure of a diguanylate cyclase from Thermotoga maritima: insights into activation, feedback inhibition and thermostability. PLoS One 9:e110912. http://dx.doi.org/10.1371/journal.pone.0110912.
23. Schirmer T, Jenal U. 2009. Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol 7:724-735. http://dx.doi.org/10.1038/nrmicro2203.
24. Bobrov AG, Kirillina O, Forman S, Mack D, Perry RD. 2008. Insights into Yersinia pestis biofilm development: topology and co-interaction of Hms inner membrane proteins involved in exopolysaccharide production. Environ Microbiol 10:1419-1432. http://dx.doi.org/10.1111/j.1462-2920.2007.01554.x.
25. Navarro MV, Newell PD, Krasteva PV, Chatterjee D, Madden DR, O'Toole GA, Sondermann H. 2011. Structural basis for c-di-GMPmediated inside-out signaling controlling periplasmic proteolysis. PLoS Biol 9:e1000588. http://dx.doi.org/10.1371/journal.pbio.1000588.
26. Monds RD, Newell PD, Gross RH, O'Toole GA. 2007. Phosphatedependent modulation of c-di-GMP levels regulates Pseudomonas fluorescens Pf0-1 biofilm formation by controlling secretion of the adhesin LapA. Mol Microbiol 63:656-679.
27. Yang CY, Chin KH, Chuah ML, Liang ZX, Wang AH, Chou SH. 2011. The structure and inhibition of a GGDEF diguanylate cyclase complexed with (c-di-GMP)(2) at the active site. Acta Crystallogr D Biol Crystallogr 67:997-1008. http://dx.doi.org/10.1107/S090744491104039X.