Structural basis for c-di-GMP-mediated inside-out signaling controlling periplasmic proteolysis

PLoS Biology

Volumn 9, Issue 2, 2011, Pages

  Navarro, Marcos V A S ^a,c   Newell, Peter D ^b   Krasteva, Petya V ^a   Chatterjee, Debashree ^a   Madden, Dean R ^b   O'Toole, George A ^b   Sondermann, Holger ^a  

^a Department of Obstetrics Gynecology   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; MEMBRANE PROTEIN; PROTEIN LAPD; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BIS(3',5') CYCLIC DIGUANYLIC ACID; BIS(3',5')-CYCLIC DIGUANYLIC ACID; DRUG DERIVATIVE; PEPTIDE HYDROLASE; PHOSPHODIESTERASE;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME DEGRADATION; NONHUMAN; OLIGOMERIZATION; POINT MUTATION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS PUTIDA; REGULATORY MECHANISM; BACTERIUM ADHERENCE; BINDING SITE; BIOFILM; CHEMISTRY; CYTOPLASM; DIMERIZATION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

BACTERIA (MICROORGANISMS); PSEUDOMONAS FLUORESCENS;

BACTERIAL ADHESION; BACTERIAL PROTEINS; BINDING SITES; BIOFILMS; CRYSTALLOGRAPHY, X-RAY; CYCLIC GMP; DIMERIZATION; PEPTIDE HYDROLASES; PERIPLASM; PHOSPHORIC DIESTER HYDROLASES; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS FLUORESCENS; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 79952260048     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1000588     Document Type: Article

References (61)

1. Hall-Stoodley L, Costerton J. W, Stoodley P, (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2: 95-108.
2. O'Toole G, Kaplan H. B, Kolter R, (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54: 49-79.
3. Parsek M. R, Singh P. K, (2003) Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 57: 677-701.
4. Hengge R, (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7: 263-273.
5. Weinhouse H, Sapir S, Amikam D, Shilo Y, Volman G, et al. (1997) c-di-GMP-binding protein, a new factor regulating cellulose synthesis in Acetobacter xylinum. FEBS Lett 416: 207-211.
6. Schirmer T, Jenal U, (2009) Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol 7: 724-735.
7. Tal R, Wong H, Calhoon R, Gelfand D, Fear A, et al. (1998) Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes. J Bacteriol 180: 4416-4425.
8. Ryan R. P, Fouhy Y, Lucey J. F, Crossman L. C, Spiro S, et al. (2006) Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci U S A 103: 6712-6717.
9. Simm R, Morr M, Kader A, Nimtz M, Römling U, (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53: 1123-1134.
10. D'Argenio D, Miller S, (2004) Cyclic di-GMP as a bacterial second messenger. Microbiology 150: 2497-2502.
11. Sudarsan N, Lee E. R, Weinberg Z, Moy R. H, Kim J. N, et al. (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321: 411-413.
12. Amikam D, Galperin M. Y, (2006) PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22: 3-6.
13. Ryjenkov D. A, Simm R, Romling U, Gomelsky M, (2006) The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ domain protein YcgR controls motility in enterobacteria. J Biol Chem 281: 30310-30314.
14. Krasteva P. V, Fong J. C, Shikuma N. J, Beyhan S, Navarro M. V, et al. (2010) Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327: 866-868.
15. Hickman J. W, Harwood C. S, (2008) Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69: 376-389.
16. Leduc J. L, Roberts G. P, (2009) Cyclic di-GMP allosterically inhibits the CRP-like protein (Clp) of Xanthomonas axonopodis pv. citri. J Bacteriol 191: 7121-7122.
17. Chan C, Paul R, Samoray D, Amiot N. C, Giese B, et al. (2004) Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci U S A 101: 17084-17089.
18. De N, Pirruccello M, Krasteva P. V, Bae N, Raghavan R. V, et al. (2008) Phosphorylation-independent regulation of the diguanylate cyclase WspR. PLoS Biol 6: e67 doi:10.1371/journal.pbio.0060067.
19. Lee V. T, Matewish J. M, Kessler J. L, Hyodo M, Hayakawa Y, et al. (2007) A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 65: 1474-1484.
20. Beyhan S, Odell L. S, Yildiz F. H, (2008) Identification and characterization of cyclic diguanylate signaling systems controlling rugosity in Vibrio cholerae. J Bacteriol 190: 7392-7405.
21. Galperin M. Y, Nikolskaya A. N, Koonin E. V, (2001) Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203: 11-21.
22. Christen M, Christen B, Folcher M, Schauerte A, Jenal U, (2005) Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J Biol Chem 280: 30829-30837.
23. Kulasakara H, Lee V, Brencic A, Liberati N, Urbach J, 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 U S A 103: 2839-2844.
24. Newell P. D, Monds R. D, O'Toole G. A, (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.
25. Hinsa S. M, Espinosa-Urgel M, Ramos J. L, O'Toole G. A, (2003) Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted protein. Mol Microbiol 49: 905-918.
26. Hinsa S. M, O'Toole G. A, (2006) Biofilm formation by Pseudomonas fluorescens WCS365: a role for LapD. Microbiology 152: 1375-1383.
27. Gjermansen M, Nilsson M, Yang L, Tolker-Nielsen T, (2009) Characterization of starvation-induced dispersion in Pseudomonas putida biofilms: genetic elements and molecular mechanisms. Mol Microbiol 75: 815-826.
28. Monds R. D, Newell P. D, Gross R. H, O'Toole G. A, (2007) Phosphate-dependent 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.
29. Newell P. D, Boyd C. D, Sondermann H, O'Toole G. A, (2011) A C-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage. PLoS Biol 9: e587 doi:10.1371/journal.pbio.1000587.
30. Falke J. J, Hazelbauer G. L, (2001) Transmembrane signaling in bacterial chemoreceptors. Trends Biochem Sci 26: 257-265.
31. Anantharaman V, Balaji S, Aravind L, (2006) The signaling helix: a common functional theme in diverse signaling proteins. Biol Direct 1: 25.
32. Stewart V, Chen L. L, (2010) The S helix mediates signal transmission as a HAMP domain coiled-coil extension in the NarX nitrate sensor from Escherichia coli K-12. J Bacteriol 192: 734-745.
33. Krissinel E, Henrick K, (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797.
34. Barends T. R, Hartmann E, Griese J. J, Beitlich T, Kirienko N. V, et al. (2009) Structure and mechanism of a bacterial light-regulated cyclic nucleotide phosphodiesterase. Nature 459: 1015-1018.
35. Minasov G, Padavattan S, Shuvalova L, Brunzelle J. S, Miller D. J, et al. (2009) Crystal structures of YkuI and its complex with second messenger c-di-GMP suggests catalytic mechanism of phosphodiester bond cleavage by EAL domains. J Biol Chem 284: 13174-13184.
36. Navarro M. V, De N, Bae N, Wang Q, Sondermann H, (2009) Structural analysis of the GGDEF-EAL domain-containing c-di-GMP receptor FimX. Structure 17: 1104-1116.
37. Tchigvintsev A, Xu X, Singer A, Chang C, Brown G, et al. (2010) Structural insight into the mechanism of cyclic di-GMP hydrolysis by EAL domain phosphodiesterases. J Mol Biol 402: 524-538.
38. Wassmann P, Chan C, Paul R, Beck A, Heerklotz H, et al. (2007) Structure of BeF3--modified response regulator PleD: implications for diguanylate cyclase activation, catalysis, and feedback inhibition. Structure 15: 915-927.
39. Rao F, Yang Y, Qi Y, Liang Z. X, (2008) Catalytic mechanism of cyclic di-GMP-specific phosphodiesterase: a study of the EAL domain-containing RocR from Pseudomonas aeruginosa. J Bacteriol 190: 3622-3631.
40. Rao F, Qi Y, Chong H. S, Kotaka M, Li B, et al. (2009) The functional role of a conserved loop in EAL domain-based cyclic di-GMP-specific phosphodiesterase. J Bacteriol 191: 4722-4731.
41. De N, Navarro M. V, Raghavan R. V, Sondermann H, (2009) Determinants for the activation and autoinhibition of the diguanylate cyclase response regulator WspR. J Mol Biol 393: 619-633.
42. De N, Navarro M. V, Wang Q, Krasteva P. V, Sondermann H, (2010) Biophysical assays for protein interactions in the Wsp sensory system and biofilm formation. Methods Enzymol 471: 161-184.
43. Holm L, Kaariainen S, Rosenstrom P, Schenkel A, (2008) Searching protein structure databases with DaliLite v.3. Bioinformatics 24: 2780-2781.
44. Reinelt S, Hofmann E, Gerharz T, Bott M, Madden D. R, (2003) The structure of the periplasmic ligand-binding domain of the sensor kinase CitA reveals the first extracellular PAS domain. J Biol Chem 278: 39189-39196.
45. Moglich A, Ayers R. A, Moffat K, (2009) Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 17: 1282-1294.
46. Chang C, Tesar C, Gu M, Babnigg G, Joachimiak A, et al. (2010) Extracytoplasmic PAS-like domains are common in signal transduction proteins. J Bacteriol 192: 1156-1159.
47. Cheung J, Bingman C. A, Reyngold M, Hendrickson W. A, Waldburger C. D, (2008) Crystal structure of a functional dimer of the PhoQ sensor domain. J Biol Chem 283: 13762-13770.
48. Sevvana M, Vijayan V, Zweckstetter M, Reinelt S, Madden D. R, et al. (2008) A ligand-induced switch in the periplasmic domain of sensor histidine kinase CitA. J Mol Biol 377: 512-523.
49. Hulko M, Berndt F, Gruber M, Linder J. U, Truffault V, et al. (2006) The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126: 929-940.
50. Airola M. V, Watts K. J, Bilwes A. M, Crane B. R, (2010) Structure of concatenated HAMP domains provides a mechanism for signal transduction. Structure 18: 436-448.
51. Beyhan S, Bilecen K, Salama S. R, Casper-Lindley C, Yildiz F. H, (2007) Regulation of rugosity and biofilm formation in Vibrio cholerae: comparison of VpsT and VpsR regulons and epistasis analysis of vpsT, vpsR, and hapR. J Bacteriol 189: 388-402.
52. Suzuki K, Babitzke P, Kushner S. R, Romeo T, (2006) Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E. Genes Dev 20: 2605-2617.
53. Benach J, Swaminathan S. S, Tamayo R, Handelman S. K, Folta-Stogniew E, et al. (2007) The structural basis of cyclic diguanylate signal transduction by PilZ domains. EMBO J 26: 5153-5166.
54. Ko J, Ryu K. S, Kim H, Shin J. S, Lee J. O, et al. (2010) Structure of PP4397 reveals the molecular basis for different c-di-GMP binding modes by Pilz domain proteins. J Mol Biol 398: 97-110.
55. Guzzo C. R, Salinas R. K, Andrade M. O, Farah C. S, (2009) PILZ protein structure and interactions with PILB and the FIMX EAL domain: implications for control of type IV pilus biogenesis. J Mol Biol 393: 848-866.
56. Laue T. M, Shah B. D, Ridgeway T. M, Pelletier S. L, (1992) Computer-aided interpretation of analytical sedimentation data for proteins. In: Harding S. E, Rowe A. J, Horton J. C, editors. Analytical ultracentrifugation in biochemistry and polymer science Cambridge Royal Society of Chemistry pp. 90-125.
57. Stafford W. F, Sherwood P. J, (2004) Analysis of heterologous interacting systems by sedimentation velocity: curve fitting algorithms for estimation of sedimentation coefficients, equilibrium and kinetic constants. Biophys Chem 108: 231-243.
58. Choi K. H, Kumar A, Schweizer H. P, (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.
59. Monds R. D, Newell P. D, Schwartzman J. A, O'Toole G. A, (2006) Conservation of the Pho regulon in Pseudomonas fluorescens Pf0-1. Appl Environ Microbiol 72: 1910-1924.
60. Larkin M. A, Blackshields G, Brown N. P, Chenna R, McGettigan P. A, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
61. Gouet P, Courcelle E, Stuart D. I, Metoz F, (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15: 305-308.