The REC domain mediated dimerization is critical for FleQ from Pseudomonas aeruginosa to function as a c-di-GMP receptor and flagella gene regulator

Journal of Structural Biology

Volumn 192, Issue 1, 2015, Pages 1-13

  Su, Tiantian ^a   Liu, Shiheng ^a   Wang, Kang ^a   Chi, Kaikai ^a   Zhu, Deyu ^a   Wei, Tiandi ^a   Huang, Yan ^a   Guo, Liming ^b   Hu, Wei ^a   Xu, Sujuan ^a   Lin, Zong ^c   Gu, Lichuan ^a  

^a SHANDONG UNIVERSITY   (China)

^b Rizhao Meteorological Office   (China)

^c TSINGHUA UNIVERSITY   (China)

Author keywords

Biofilm; Cyclic di GMP; Flagella; Pseudomonas aeruginosa; Structure function; Transcription factor

Indexed keywords

BACTERIAL PROTEIN; BINDING PROTEIN; CYCLIC DIGUANOSINE MONOPHOSPHATE; CYCLIC DIGUANOSINE MONOPHOSPHATE RECEPTOR; CYCLIC NUCLEOTIDE; FLEQ PROTEIN; NTRC1 PROTEIN; REC PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; BIS(3',5')-CYCLIC DIGUANYLIC ACID; CYCLIC GMP; FLEQ PROTEIN, PSEUDOMONAS AERUGINOSA; TRANSACTIVATOR PROTEIN;

ARTICLE; BACTERIAL GENE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; FLAGELLA GENE; FLAGELLUM; GENE EXPRESSION REGULATION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PSEUDOMONAS AERUGINOSA; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANALOGS AND DERIVATIVES; BIOFILM; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BINDING SITES; BIOFILMS; CRYSTALLOGRAPHY, X-RAY; CYCLIC GMP; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PSEUDOMONAS AERUGINOSA; TRANS-ACTIVATORS;

EID: 84952872839     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2015.09.002     Document Type: Article

References (48)

1. Adams P.D., Grosse-Kunstleve R.W., Hung L.W., Ioerger T.R., McCoy A.J., Moriarty N.W., Read R.J., Sacchettini J.C., Sauter N.K., Terwilliger T.C. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 2002, 58:1948-1954.
2. Arora S.K., Ritchings B.W., Almira E.C., Lory S., Ramphal R. A transcriptional activator, FleQ, regulates mucin adhesion and flagellar gene expression in Pseudomonas aeruginosa in a cascade manner. J. Bacteriol. 1997, 179:5574-5581.
3. Bailey T.L., Elkan C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 1994, 2:28-36.
4. Baraquet C., Harwood C.S. Cyclic diguanosine monophosphate represses bacterial flagella synthesis by interacting with the Walker A motif of the enhancer-binding protein FleQ. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:18478-18483.
5. Baraquet C., Murakami K., Parsek M.R., Harwood C.S. 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. 2012, 40:7207-7218.
6. Batchelor J.D., Doucleff M., Lee C.J., Matsubara K., De Carlo S., Heideker J., Lamers M.H., Pelton J.G., Wemmer D.E. Structure and regulatory mechanism of Aquifex aeolicus NtrC4: variability and evolution in bacterial transcriptional regulation. J. Mol. Biol. 2008, 384:1058-1075.
7. Bush M., Dixon R. The role of bacterial enhancer binding proteins as specialized activators of sigma54-dependent transcription. Microbiol. Mol. Biol. Rev. 2012, 76:497-529.
8. Choi K.H., Schweizer H.P. An improved method for rapid generation of unmarked Pseudomonas aeruginosa deletion mutants. BMC Microbiol. 2005, 5:30.
9. Dasgupta N., Ramphal R. Interaction of the antiactivator FleN with the transcriptional activator FleQ regulates flagellar number in Pseudomonas aeruginosa. J. Bacteriol. 2001, 183:6636-6644.
10. Dasgupta N., Arora S.K., Ramphal R. FleN, a gene that regulates flagellar number in Pseudomonas aeruginosa. J. Bacteriol. 2000, 182:357-364.
11. Dasgupta N., Wolfgang M.C., Goodman A.L., Arora S.K., Jyot J., Lory S., Ramphal R. A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol. Microbiol. 2003, 50:809-824.
12. De N., Navarro M.V.A.S., Raghavan R.V., Sondermann H. Determinants for the activation and autoinhibition of the diguanylate cyclase response regulator WspR. J. Mol. Biol. 2009, 393:619-633.
13. Doucleff M., Chen B.Y., Maris A.E., Wemmer D.E., Kondrashkina E., Nixon B.T. Negative regulation of AAA+ ATPase assembly by two component receiver domains: a transcription activation mechanism that is conserved in mesophilic and extremely hyperthermophilic bacteria. J. Mol. Biol. 2005, 353:242-255.
14. Dutton R.J., Xu Z., Gober J.W. Linking structural assembly to gene expression: a novel mechanism for regulating the activity of a sigma54 transcription factor. Mol. Microbiol. 2005, 58:743-757.
15. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
16. Gouet P., Courcelle E., Stuart D.I., Metoz F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 1999, 15:305-308.
17. Hickman J.W., Harwood C.S. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol. Microbiol. 2008, 69:376-389.
18. Hoang T.T., Karkhoff-Schweizer R.R., Kutchma A.J., Schweizer H.P. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 1998, 212:77-86.
19. Holm L., Rosenstrom P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 2010, 38:W545-W549.
20. Jain R., Kazmierczak B.I. A conservative amino acid mutation in the master regulator FleQ renders Pseudomonas aeruginosa aflagellate. PLoS ONE 2014, 9:e97439.
21. Jyot J., Dasgupta N., Ramphal R. 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. 2002, 184:5251-5260.
22. Kim Y.K., McCarter L.L. Analysis of the polar flagellar gene system of Vibrio parahaemolyticus. J. Bacteriol. 2000, 182:3693-3704.
23. Klose K.E., Mekalanos J.J. Distinct roles of an alternative sigma factor during both free-swimming and colonizing phases of the Vibrio cholerae pathogenic cycle. Mol. Microbiol. 1998, 28:501-520.
24. Krissinel E., Henrick K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 2007, 372:774-797.
25. Lee S.Y., De La Torre A., Yan D., Kustu S., Nixon B.T., Wemmer D.E. Regulation of the transcriptional activator NtrC1: structural studies of the regulatory and AAA+ ATPase domains. Genes Dev. 2003, 17:2552-2563.
26. )) method. Methods 2001, 25:402-408.
27. McCarter L.L. Regulation of flagella. Curr. Opin. Microbiol. 2006, 9:180-186.
28. McCoy A.J., Grosse-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., Read R.J. Phaser crystallographic software. J. Appl. Crystallogr. 2007, 40:658-674.
29. Milani M., Leoni L., Rampioni G., Zennaro E., Ascenzi P., Bolognesi M. An active-like structure in the unphosphorylated StyR response regulator suggests a phosphorylation-dependent allosteric activation mechanism. Structure 2005, 13:1289-1297.
30. Moens S., Vanderleyden J. Functions of bacterial flagella. Crit. Rev. Microbiol. 1996, 22:67-100.
31. Muir R.E., Gober J.W. Mutations in FlbD that relieve the dependency on flagellum assembly alter the temporal and spatial pattern of developmental transcription in Caulobacter crescentus. Mol. Microbiol. 2002, 43:597-615.
32. Muir R.E., Gober J.W. Regulation of FlbD activity by flagellum assembly is accomplished through direct interaction with the trans-acting factor, FliX. Mol. Microbiol. 2004, 54:715-730.
33. Muir R.E., O'Brien T.M., Gober J.W. The Caulobacter crescentus flagellar gene, fliX, encodes a novel trans-acting factor that couples flagellar assembly to transcription. Mol. Microbiol. 2001, 39:1623-1637.
34. Notredame C., Higgins D.G., Heringa J. T-coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 2000, 302:205-217.
35. O'Toole G.A., Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 1998, 30:295-304.
36. O'Toole G.A., Kolter R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 1998, 28:449-461.
37. O'Toole G.A., Pratt L.A., Watnick P.I., Newman D.K., Weaver V.B., Kolter R. Genetic approaches to study of biofilms. Methods Enzymol. 1999, 310:91-109.
38. Ottemann K.M., Miller J.F. Roles for motility in bacterial-host interactions. Mol. Microbiol. 1997, 24:1109-1117.
39. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 276:307-326.
40. Prouty M.G., Correa N.E., Klose K.E. The novel sigma54- and sigma28-dependent flagellar gene transcription hierarchy of Vibrio cholerae. Mol. Microbiol. 2001, 39:1595-1609.
41. Ramakrishnan G., Newton A. FlbD of Caulobacter crescentus is a homologue of the NtrC (NRI) protein and activates sigma 54-dependent flagellar gene promoters. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:2369-2373.
42. Schweizer H.P., Hoang T.T. An improved system for gene replacement and xylE fusion analysis in Pseudomonas aeruginosa. Gene 1995, 158:15-22.
43. Srivastava D., Hsieh M.L., Khataokar A., Neiditch M.B., Waters C.M. Cyclic di-GMP inhibits Vibrio cholerae motility by repressing induction of transcription and inducing extracellular polysaccharide production. Mol. Microbiol. 2013, 90:1262-1276.
44. Stivala A., Wybrow M., Wirth A., Whisstock J.C., Stuckey P.J. Automatic generation of protein structure cartoons with pro-origami. Bioinformatics 2011, 27:3315-3316.
45. Wang C., Ye F., Kumar V., Gao Y.G., Zhang L.H. BswR controls bacterial motility and biofilm formation in Pseudomonas aeruginosa through modulation of the small RNA rsmZ. Nucleic Acids Res. 2014, 42:4563-4576.
46. Windgassen M., Urban A., Jaeger K.E. Rapid gene inactivation in Pseudomonas aeruginosa. FEMS Microbiol. Lett. 2000, 193:201-205.
47. Winn M.D., Ballard C.C., Cowtan K.D., Dodson E.J., Emsley P., Evans P.R., Keegan R.M., Krissinel E.B., Leslie A.G., McCoy A., McNicholas S.J., Murshudov G.N., Pannu N.S., Potterton E.A., Powell H.R., Read R.J., Vagin A., Wilson K.S. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 2011, 67:235-242.
48. Yang J.G., Shih M.S., Kuo W.T., Chin K.H., Shen G.H., Chou S.H. Crystallization of the N-terminal regulatory domain of the enhancer-binding protein FleQ from Stenotrophomonas maltophilia. Acta Crystallogr. F Struct. Biol. Commun. 2014, 70:326-330.