Mechanistic insights into c-di-GMP-dependent control of the biofilm regulator FleQ from Pseudomonas aeruginosa

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 2, 2016, Pages E209-E218

  Matsuyama, Bruno Y ^a   Krasteva, Petya V ^b,c   Baraquet, Claudine ^d   Harwood, Caroline S ^d   Sondermann, Holger ^c   Navarro, Marcos V A S ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUT PASTEUR   (France)

^c Department of Molecular Biology and Genetics   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Enhancer binding protein; Flagella; Gene expression; Structure

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; CYCLIC DIGUANOSINE MONOPHOSPHATE; CYCLIC GMP DERIVATIVE; EXOPOLYSACCHARIDE; FLEN PROTEIN; FLEQ PROTEIN; NUCLEIC ACID BINDING PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; BACTERIAL DNA; BIS(3',5')-CYCLIC DIGUANYLIC ACID; CROSS LINKING REAGENT; CYCLIC GMP; FLEQ PROTEIN, PSEUDOMONAS AERUGINOSA; MUTANT PROTEIN; SOLUTION AND SOLUBILITY; TRANSACTIVATOR PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL FLAGELLUM; BIOFILM; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA BINDING MOTIF; ENZYME ACTIVE SITE; GENE EXPRESSION REGULATION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; PSEUDOMONAS AERUGINOSA; SECOND MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; BINDING SITE; CALORIMETRY; CHEMISTRY; CONSERVED SEQUENCE; DRUG EFFECTS; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROMOTER REGION; PROTEIN MOTIF; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS; SOLUTION AND SOLUBILITY; TEMPERATURE; X RAY CRYSTALLOGRAPHY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; BINDING SITES; BIOFILMS; CALORIMETRY; CONSERVED SEQUENCE; CROSS-LINKING REAGENTS; CRYSTALLOGRAPHY, X-RAY; CYCLIC GMP; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA; SEQUENCE ALIGNMENT; SOLUTIONS; TEMPERATURE; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

EID: 84954320667     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1523148113     Document Type: Article

References (62)

1. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: From the natural environment to infectious diseases. Nat Rev Microbiol 2(2):95-108.
2. Solano C, Echeverz M, Lasa I (2014) Biofilm dispersion and quorum sensing. Curr Opin Microbiol 18:96-104.
3. Srivastava D, Waters CM (2012) A tangled web: Regulatory connections between quorum sensing and cyclic Di-GMP. J Bacteriol 194(17):4485-4493.
4. Teschler JK, et al. (2015) Living in the matrix: Assembly and control of Vibrio cholerae biofilms. Nat Rev Microbiol 13(5):255-268.
5. Tolker-Nielsen T (2014) Pseudomonas aeruginosa biofilm infections: From molecular biofilm biology to new treatment possibilities. APMIS Suppl (138):1-51.
6. Furukawa S, Kuchma SL, O'Toole GA (2006) Keeping their options open: Acute versus persistent infections. J Bacteriol 188(4):1211-1217.
7. Mills E, Pultz IS, Kulasekara HD, Miller SI (2011) The bacterial second messenger c-di-GMP: Mechanisms of signalling. Cell Microbiol 13(8):1122-1129.
8. Römling 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):1-52.
9. Sondermann H, Shikuma NJ, Yildiz FH (2012) You've come a long way: c-di-GMP signaling. Curr Opin Microbiol 15(2):140-146.
10. Krasteva PV, Giglio KM, Sondermann H (2012) Sensing the messenger: The diverse ways that bacteria signal through c-di-GMP. Protein Sci 21(7):929-948.
11. Schirmer T, Jenal U (2009) Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol 7(10):724-735.
12. Arora SK, Ritchings BW, Almira EC, Lory S, Ramphal R (1997) A transcriptional activator, FleQ, regulates mucin adhesion and flagellar gene expression in Pseudomonas aeruginosa in a cascade manner. J Bacteriol 179(17):5574-5581.
13. Baraquet C, Murakami K, Parsek MR, Harwood CS (2012) The FleQ protein from Pseudomonas aeruginosa functions as both a repressor and an activator to control gene expression from the pel operon promoter in response to c-di-GMP. Nucleic Acids Res 40(15):7207-7218.
14. Hickman JW, Harwood CS (2008) Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69(2):376-389.
15. Ghosh T, Bose D, Zhang X (2010) Mechanisms for activating bacterial RNA polymerase. FEMS Microbiol Rev 34(5):611-627.
16. Gao R, Mack TR, Stock AM (2007) Bacterial response regulators: Versatile regulatory strategies from common domains. Trends Biochem Sci 32(5):225-234.
17. Gao R, Stock AM (2010) Molecular strategies for phosphorylation-mediated regulation of response regulator activity. Curr Opin Microbiol 13(2):160-167.
18. Bush M, Dixon R (2012) The role of bacterial enhancer binding proteins as specialized activators of σ54-dependent transcription. Microbiol Mol Biol Rev 76(3):497-529.
19. De Carlo S, et al. (2006) The structural basis for regulated assembly and function of the transcriptional activator NtrC. Genes Dev 20(11):1485-1495.
20. Lee SY, et al. (2003) Regulation of the transcriptional activator NtrC1: Structural studies of the regulatory and AAA+ ATPase domains. Genes Dev 17(20):2552-2563.
21. Baraquet C, Harwood CS (2013) Cyclic diguanosine monophosphate represses bacterial flagella synthesis by interacting with the Walker A motif of the enhancer-binding protein FleQ. Proc Natl Acad Sci USA 110(46):18478-18483.
22. Dasgupta N, Ramphal R (2001) Interaction of the antiactivator FleN with the transcriptional activator FleQ regulates flagellar number in Pseudomonas aeruginosa. J Bacteriol 183(22):6636-6644.
23. Jyot J, Dasgupta N, Ramphal R (2002) FleQ, the major flagellar gene regulator in Pseudomonas aeruginosa, binds to enhancer sites located either upstream or atypically downstream of the RpoN binding site. J Bacteriol 184(19):5251-5260.
24. Dasgupta N, et al. (2003) A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol Microbiol 50(3):809-824.
25. Dasgupta N, Arora SK, Ramphal R (2000) fleN, a gene that regulates flagellar number in Pseudomonas aeruginosa. J Bacteriol 182(2):357-364.
26. Srivastava D, Hsieh ML, Khataokar A, Neiditch MB, Waters CM (2013) Cyclic di-GMP inhibits Vibrio cholerae motility by repressing induction of transcription and inducing extracellular polysaccharide production. Mol Microbiol 90(6):1262-1276.
27. Dago AE, Wigneshweraraj SR, Buck M, Morett E (2007) A role for the conserved GAFTGA motif of AAA+ transcription activators in sensing promoter DNA conformation. J Biol Chem 282(2):1087-1097.
28. Wendler P, Ciniawsky S, Kock M, Kube S (2012) Structure and function of the AAA+ nucleotide binding pocket. Biochim Biophys Acta 1823(1):2-14.
29. Rappas M, et al. (2005) Structural insights into the activity of enhancer-binding proteins. Science 307(5717):1972-1975.
30. Zhang N, et al. (2014) Subunit dynamics and nucleotide-dependent asymmetry of an AAA(+) transcription complex. J Mol Biol 426(1):71-83.
31. Sysoeva TA, Chowdhury S, Guo L, Nixon BT (2013) Nucleotide-induced asymmetry within ATPase activator ring drives σ54-RNAP interaction and ATP hydrolysis. Genes Dev 27(22):2500-2511.
32. Su T, et al. (2015) The REC domain mediated dimerization is critical for FleQ from Pseudomonas aeruginosa to function as a c-di-GMP receptor and flagella gene regulator. J Struct Biol 192(1):1-13.
33. Chen C, et al. (2011) Representative proteomes: A stable, scalable and unbiased proteome set for sequence analysis and functional annotation. PLoS One 6(4):e18910.
34. Srivastava D, Harris RC, Waters CM (2011) Integration of cyclic di-GMP and quorum sensing in the control of vpsT and aphA in Vibrio cholerae. J Bacteriol 193(22): 6331-6341.
35. Trampari E, et al. (2015) Bacterial rotary export ATPases are allosterically regulated by the nucleotide second messenger cyclic-di-GMP. J Biol Chem 290(40):24470-24483.
36. Krissinel E (2015) Stock-based detection of protein oligomeric states in jsPISA. Nucleic Acids Res 43(W1):W314-W319.
37. Wigneshweraraj SR, et al. (2005) The second paradigm for activation of transcription. Prog Nucleic Acid Res Mol Biol 79:339-369.
38. Kulasakara H, 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(8):2839-2844.
39. Malone JG, et al. (2010) YfiBNR mediates cyclic di-GMP dependent small colony variant formation and persistence in Pseudomonas aeruginosa. PLoS Pathog 6(3): e1000804.
40. Herrera MC, Krell T, Zhang X, Ramos JL (2009) PhhR binds to target sequences at different distances with respect to RNA polymerase in order to activate transcription. J Mol Biol 394(3):576-586.
41. Pittard J, Camakaris H, Yang J (2005) The TyrR regulon. Mol Microbiol 55(1):16-26.
42. Ueki T, Inouye S (2002) Transcriptional activation of a heat-shock gene, lonD, of Myxococcus xanthus by a two component histidine-aspartate phosphorelay system. J Biol Chem 277(8):6170-6177.
43. Andrews AE, Lawley B, Pittard AJ (1991) Mutational analysis of repression and activation of the tyrP gene in Escherichia coli. J Bacteriol 173(16):5068-5078.
44. Dixon MP, et al. (2002) The central domain of Escherichia coli TyrR is responsible for hexamerization associated with tyrosine-mediated repression of gene expression. J Biol Chem 277(26):23186-23192.
45. Wilson TJ, Maroudas P, Howlett GJ, Davidson BE (1994) Ligand-induced self-association of the Escherichia coli regulatory protein TyrR. J Mol Biol 238(3):309-318.
46. Yang J, et al. (2004) Mode of action of the TyrR protein: Repression and activation of the tyrP promoter of Escherichia coli. Mol Microbiol 52(1):243-256.
47. Kabsch W (2010) XDS. Acta Crystallogr D Biol Crystallogr 66(Pt 2):125-132.
48. Dauter Z, Dauter M, Rajashankar KR (2000) Novel approach to phasing proteins: Derivatization by short cryo-soaking with halides. Acta Crystallogr D Biol Crystallogr 56(Pt 2):232-237.
49. Nagem RA, et al. (2005) Getting the most out of X-ray home sources. Acta Crystallogr D Biol Crystallogr 61(Pt 8):1022-1030.
50. Adams PD, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66(Pt 2):213-221.
51. Sheldrick GM (2008) A short history of SHELX. Acta Crystallogr A 64(Pt 1):112-122.
52. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66(Pt 4):486-501.
53. Mindell JA, Grigorieff N (2003) Accurate determination of local defocus and specimen tilt in electron microscopy. J Struct Biol 142(3):334-347.
54. Shaikh TR, et al. (2008) SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat Protoc 3(12):1941-1974.
55. Tang G, et al. (2007) EMAN2: An extensible image processing suite for electron microscopy. J Struct Biol 157(1):38-46.
56. Webb MR (1992) A continuous spectrophotometric assay for inorganic phosphate and for measuring phosphate release kinetics in biological systems. Proc Natl Acad Sci USA 89(11):4884-4887.
57. 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(3):391-397.
58. Newman JR, Fuqua C (1999) Broad-host-range expression vectors that carry the L-arabinose-inducible Escherichia coli araBAD promoter and the araC regulator. Gene 227(2):197-203.
59. Schuster M, Lostroh CP, Ogi T, Greenberg EP (2003) Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: A transcriptome analysis. J Bacteriol 185(7):2066-2079.
60. Finn RD, et al. (2015) HMMER web server: 2015 update. Nucleic Acids Res 43(W1): W30-W38.
61. Wheeler TJ, Clements J, Finn RD (2014) Skylign: A tool for creating informative, interactive logos representing sequence alignments and profile hidden Markov models. BMC Bioinformatics 15:7.
62. Vidangos N, et al. (2013) Structure, function, and tethering of DNA-binding domains in σ(54) transcriptional activators. Biopolymers 99(12):1082-1096.