Quorum sensing: How bacteria can coordinate activity and synchronize their response to external signals?

Protein Science

Volumn 21, Issue 10, 2012, Pages 1403-1417

  Li, Zhi ^a   Nair, Satish K ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Acyl homoserine lactone; Bacterial signalling; Quorum sensing; Synthase

Indexed keywords

ARGININE; GLUTAMIC ACID; HISTIDINE; LEUCINE; LYSINE; N ACYLHOMOSERINE LACTONE; NITROGEN; PHENYLALANINE; THREONINE; TRANSCRIPTION FACTOR LUXR; TRYPTOPHAN;

ALPHA HELIX; BETA SHEET; BRADYRHIZOBIUM JAPONICUM; CATALYSIS; CHROMOBACTERIUM VIOLACEUM; DIMERIZATION; DNA BINDING; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SYNTHESIS; ESCHERICHIA COLI; HYDROGEN BOND; HYDROPHOBICITY; IN VITRO STUDY; IN VIVO STUDY; LACTONIZATION; LIGAND BINDING; MICROBIAL ACTIVITY; MOLECULAR DOCKING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; REVIEW; RHIZOBIUM LEGUMINOSARUM; RHIZOBIUM RADIOBACTER; SIGNAL TRANSDUCTION; VIBRIO FISCHERI;

ACYL-BUTYROLACTONES; AMINO ACID SEQUENCE; BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIAL PROTEINS; LIGASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; QUORUM SENSING; SEQUENCE ALIGNMENT;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 84866617309     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2132     Document Type: Review

References (128)

1. Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269-275. (Pubitemid 24034041)
2. Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197-222.
3. Schaefer AL, Val DL, Hanzelka BL, Cronan JE, Jr, Greenberg EP (1996) Generation of cell-to-cell signals in quorum sensing: acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. Proc Natl Acad Sci USA 93:9505-9509. (Pubitemid 26296638)
4. Kaplan HB, Greenberg EP (1985) Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system. J Bacteriol 163:1210-1214. (Pubitemid 15229495)
5. Pearson JP, Van Delden C, Iglewski BH (1999) Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals. J Bacteriol 181:1203-1210. (Pubitemid 29119559)
6. Nealson KH (1977) Autoinduction of bacterial luciferase. Occurrence, mechanism and significance. Arch Microbiol 112:73-79.
7. Nealson KH, Platt T, Hastings JW (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol 104:313-322.
8. Eberhard A, Burlingame AL, Eberhard C, Kenyon GL, Nealson KH, Oppenheimer NJ (1981) Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20:2444-2449.
9. Dunlap PV (1999) Quorum regulation of luminescence in Vibrio fischeri. J Mol Microbiol Biotechnol 1:5-12.
10. McFall-Ngai MJ (1990) Crypsis in the Pelagic environment. Am Zool 30:175-188.
11. Visick KL, Foster J, Doino J, McFall-Ngai M, Ruby EG (2000) Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J Bacteriol 182:4578-4586. (Pubitemid 30599822)
12. Bassler BL, Wright M, Showalter RE, Silverman MR (1993) Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol Microbiol 9:773-786. (Pubitemid 23253503)
13. Loh J, Lohar DP, Andersen B, Stacey G (2002) A two-component regulator mediates population-density-dependent expression of the Bradyrhizobium japonicum nodulation genes. J Bacteriol 184:1759-1766. (Pubitemid 34188228)
14. Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, Mekalanos JJ (2002) Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci USA 99:3129-3134. (Pubitemid 34240597)
15. Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N, Kumar N, Schembri MA, Song Z, Kristoffersen P, Manefield M, Costerton JW, Molin S, Eberl L, Steinberg P, Kjelleberg S, Hoiby N, Givskov M (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22:3803-3815. (Pubitemid 36975709)
16. Smith RS, Iglewski BH (2003) P. aeruginosa quorum-sensing systems and virulence. Curr Opin Microbiol 6:56-60. (Pubitemid 36258537)
17. Nadell CD, Xavier JB, Levin SA, Foster KR (2008) The evolution of quorum sensing in bacterial biofilms. PLoS Biol 6:e14.
18. Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295-298. (Pubitemid 28178075)
19. Daniels R, Vanderleyden J, Michiels J (2004) Quorum sensing and swarming migration in bacteria. FEMS Microbiol Rev 28:261-289. (Pubitemid 38721406)
20. Duerkop BA, Varga J, Chandler JR, Peterson SB, Herman JP, Churchill ME, Parsek MR, Nierman WC, Greenberg EP (2009) Quorum-sensing control of antibiotic synthesis in Burkholderia thailandensis. J Bacteriol 191:3909-3918.
21. Yarwood JM, Bartels DJ, Volper EM, Greenberg EP (2004) Quorum sensing in Staphylococcus aureus biofilms. J Bacteriol 186:1838-1850. (Pubitemid 38314529)
22. Bjarnsholt T, Jensen PO, Burmolle M, Hentzer M, Haagensen JA, Hougen HP, Calum H, Madsen KG,Moser C, Molin S, Hoiby N, Givskov M (2005) Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 151:373-383. (Pubitemid 40277742)
23. Alhede M, Bjarnsholt T, Jensen PO, Phipps RK, Moser C, Christophersen L, Christensen LD, van Gennip M, Parsek M, Hoiby N, Rasmussen TB, Givskov M (2009) Pseudomonas aeruginosa recognizes and responds aggressively to the presence of polymorphonuclear leukocytes. Microbiology 155:3500-3508.
24. Jensen PO, Bjarnsholt T, Phipps R, Rasmussen TB, Calum H, Christoffersen L, Moser C, Williams P, Pressler T, Givskov M, Hoiby N (2007) Rapid necrotic killing of polymorphonuclear leukocytes is caused by quorum-sensing-controlled production of rhamnolipid by Pseudomonas aeruginosa. Microbiology 153: 1329-1338. (Pubitemid 46779989)
25. Jensen PO, Givskov M, Bjarnsholt T, Moser C (2010) The immune system vs. Pseudomonas aeruginosa biofilms. FEMS Immunol Med Microbiol 59:292-305.
26. Clatworthy AE, Pierson E, Hung DT (2007) Targeting virulence: a new paradigm for antimicrobial therapy. Nat Chem Biol 3:541-548. (Pubitemid 47294400)
27. Geske GD, O'Neill JC, Miller DM, Mattmann ME, Blackwell HE (2007) Modulation of bacterial quorum sensing with synthetic ligands: systematic evaluation of N-acylated homoserine lactones in multiple species and new insights into their mechanisms of action. J Am Chem Soc 129:13613-13625. (Pubitemid 350071790)
28. Rasmussen TB, Bjarnsholt T, Skindersoe ME, Hentzer M, Kristoffersen P, Kote M, Nielsen J, Eberl L, Givskov M (2005) Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J Bacteriol 187:1799-1814. (Pubitemid 40289382)
29. Khmel IA, Metlitskaia AZ (2006) [Quorum sensing of genes expression - perspective drug target against bacterial pathogenicity]. Mol Biol (Mosk) 40:195-210.
30. Bjarnsholt T, Givskov M (2007) Quorum-sensing blockade as a strategy for enhancing host defences against bacterial pathogens. Philos Trans R Soc Lond B Biol Sci 362:1213-1222. (Pubitemid 47075152)
31. Rasmussen TB, Givskov M (2006) Quorum sensing inhibitors: a bargain of effects. Microbiology 152:895-904.
32. Wu H, Song Z, Hentzer M, Andersen JB, Molin S, Givskov M, Hoiby N (2004) Synthetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. J Antimicrob Chemother 53:1054-1061. (Pubitemid 38807648)
33. Rasmussen TB, Givskov M (2006) Quorum-sensing inhibitors as anti-pathogenic drugs. Int J Med Microbiol 296:149-161. (Pubitemid 43375998)
34. Waters CM, Bassler BL (2005) Quorum sensing: cellto-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319-346. (Pubitemid 41740638)
35. Manefield M, Turner SL (2002) Quorum sensing in context: out of molecular biology and into microbial ecology. Microbiology 148:3762-3764. (Pubitemid 36097437)
36. Mayville P, Ji G, Beavis R, Yang H, Goger M, Novick RP, Muir TW (1999) Structure-activity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence. Proc Natl Acad Sci USA 96:1218-1223. (Pubitemid 29098431)
37. Ansaldi M, Marolt D, Stebe T, Mandic-Mulec I, Dubnau D (2002) Specific activation of the Bacillus quorum-sensing systems by isoprenylated pheromone variants. Mol Microbiol 44:1561-1573. (Pubitemid 34639433)
38. Schauder S, Shokat K, Surette MG, Bassler BL (2001) The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol Microbiol 41:463-476. (Pubitemid 32730544)
39. Taga ME, Semmelhack JL, Bassler BL (2001) The LuxS-dependent autoinducer AI-2 controls the expression of an ABC transporter that functions in AI-2 uptake in Salmonella typhimurium. Mol Microbiol 42:777-793. (Pubitemid 33064486)
40. Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I, Bassler BL, Hughson FM (2002) Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415:545-549. (Pubitemid 34130611)
41. Miller ST, Xavier KB, Campagna SR, Taga ME, Semmelhack MF, Bassler BL, Hughson FM (2004) Salmonella typhimurium recognizes a chemically distinct form of the bacterial quorum-sensing signal AI-2. Mol Cell 15:677-687. (Pubitemid 39194899)
42. Xavier KB, Bassler BL (2003) LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol 6:191-197. (Pubitemid 36628665)
43. Flavier AB, Clough SJ, Schell MA, Denny TP (1997) Identification of 3-hydroxypalmitic acid methyl ester as a novel autoregulator controlling virulence in Ralstonia solanacearum. Mol Microbiol 26:251-259. (Pubitemid 27483675)
44. Holden MT, Ram Chhabra S, de Nys R, Stead P, Bainton NJ, Hill PJ, Manefield M, Kumar N, Labatte M, England D, Rice S, Givskov M, Salmond GP, Stewart GS, Bycroft BW, Kjelleberg S, Williams P (1999) Quorum-sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other gram-negative bacteria. Mol Microbiol 33:1254-1266. (Pubitemid 29433630)
45. Pesci EC, Milbank JB, Pearson JP, McKnight S, Kende AS, Greenberg EP, Iglewski BH (1999) Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 96:11229-11234. (Pubitemid 29487363)
46. Barber CE, Tang JL, Feng JX, Pan MQ, Wilson TJ, Slater H, Dow JM, Williams P, Daniels MJ (1997) A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol Microbiol 24:555-566. (Pubitemid 27241703)
47. Higgins DA, Pomianek ME, Kraml CM, Taylor RK, Semmelhack MF, Bassler BL (2007) The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature 450:883-886. (Pubitemid 350231318)
48. Wei Y, Perez LJ, Ng WL, Semmelhack MF, Bassler BL (2011) Mechanism of Vibrio cholerae autoinducer-1 biosynthesis. ACS Chem Biol 6:356-365.
49. Ruzheinikov SN, Das SK, Sedelnikova SE, Hartley A, Foster SJ, Horsburgh MJ, Cox AG, McCleod CW, Mekhalfia A, Blackburn GM, Rice DW, Baker PJ (2001) The 1.2 A structure of a novel quorum-sensing protein, Bacillus subtilis LuxS. J Mol Biol 313:111-122. (Pubitemid 33001169)
50. Hilgers MT, Ludwig ML (2001) Crystal structure of the quorum-sensing protein LuxS reveals a catalytic metal site. Proc Natl Acad Sci USA 98:11169-11174. (Pubitemid 32928701)
51. Lewis HA, Furlong EB, Laubert B, Eroshkina GA, Batiyenko Y, Adams JM, Bergseid MG, Marsh CD, Peat TS, Sanderson WE, Sauder JM, Buchanan SG (2001) A structural genomics approach to the study of quorum sensing: crystal structures of three LuxS orthologs. Structure 9:527-537. (Pubitemid 32575349)
52. Rajan R, Zhu J, Hu X, Pei D, Bell CE (2005) Crystal structure of S-ribosylhomocysteinase (LuxS) in complex with a catalytic 2-ketone intermediate. Biochemistry 44:3745-3753. (Pubitemid 40358027)
53. Neiditch MB, Federle MJ, Miller ST, Bassler BL, Hughson FM (2005) Regulation of LuxPQ receptoractivity by the quorum-sensing signal autoinducer-2. Mol Cell 18:507-518. (Pubitemid 40726228)
54. Neiditch MB, Federle MJ, Pompeani AJ, Kelly RC, Swem DL, Jeffrey PD, Bassler BL, Hughson FM (2006) Ligand-induced asymmetry in histidine sensor kinase complex regulates quorum sensing. Cell 126:1095-1108. (Pubitemid 44380296)
55. Yu S, Jensen V, Seeliger J, Feldmann I, Weber S, Schleicher E, Haussler S, Blankenfeldt W (2009) Structure elucidation and preliminary assessment of hydrolase activity of PqsE, the Pseudomonas quinolone signal (PQS) response protein. Biochemistry 48:10298-10307.
56. Kelly RC, Bolitho ME, Higgins DA, Lu W, Ng WL, Jeffrey PD, Rabinowitz JD, Semmelhack MF, Hughson FM, Bassler BL (2009) The Vibrio cholerae quorum-sensing autoinducer CAI-1: analysis of the biosynthetic enzyme CqsA. Nat Chem Biol 5:891-895.
57. Ishii S, Yano T, Ebihara A, Okamoto A, Manzoku M, Hayashi H (2010) Crystal structure of the peptidase domain of Streptococcus ComA, a bifunctional ATP-binding cassette transporter involved in the quorumsensing pathway. J Biol Chem 285:10777-10785.
58. Cheng Z, He YW, Lim SC, Qamra R, Walsh MA, Zhang LH, Song H (2010) Structural basis of the sensor-synthase interaction in autoinduction of the quorum sensing signal DSF biosynthesis. Structure 18:1199-1209.
59. Baker MD, Neiditch MB (2011) Structural basis of response regulator inhibition by a bacterial anti-activator protein. PLoS Biol 9:e1001226.
60. Parashar V, Mirouze N, Dubnau DA, Neiditch MB (2011) Structural basis of response regulator dephosphorylation by Rap phosphatases. PLoS Biol 9:e1000589.
61. Engebrecht J, Silverman M (1984) Identification of genes and gene products necessary for bacterial bioluminescence. Proc Natl Acad Sci USA 81:4154-4158. (Pubitemid 14054539)
62. Gambello MJ, Iglewski BH (1991) Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. J Bacteriol 173:3000-3009.
63. Passador L, Cook JM, Gambello MJ, Rust L, Iglewski BH (1993) Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260:1127-1130. (Pubitemid 23186788)
64. Minogue TD, Wehland-von Trebra M, Bernhard F, von Bodman SB (2002) The autoregulatory role of EsaR, a quorum-sensing regulator in Pantoea stewartii ssp. stewartii: evidence for a repressor function. Mol Microbiol 44:1625-1635. (Pubitemid 34639438)
65. Thiel V, Kunze B, Verma P, Wagner-Dobler I, Schulz S (2009) New structural variants of homoserine lactones in bacteria. Chembiochem 10:1861-1868.
66. Pesci EC, Pearson JP, Seed PC, Iglewski BH (1997) Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179:3127-3132. (Pubitemid 27202984)
67. Pearson JP, Passador L, Iglewski BH, Greenberg EP (1995) A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc Natl Acad Sci USA 92:1490-1494.
68. Winson MK, Camara M, Latifi A, Foglino M, Chhabra SR, Daykin M, Bally M, Chapon V, Salmond GP, Bycroft BW, Lazdunski A, Stewart GSAB, Williams P. (1995) Multiple N-acyl-L-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 92:9427-9431.
69. Schripsema J, de Rudder KE, van Vliet TB, Lankhorst PP, de Vroom E, Kijne JW, van Brussel AA (1996) Bacteriocin small of Rhizobium leguminosarum belongs to the class of N-acyl-L-homoserine lactone molecules, known as autoinducers and as quorum sensing co-transcription factors. J Bacteriol 178:366-371.
70. Parsek MR, Schaefer AL, Greenberg EP (1997) Analysis of random and site-directed mutations in rhlI, a Pseudomonas aeruginosa gene encoding an acylhomoserine lactone synthase. Mol Microbiol 26:301-310. (Pubitemid 27483679)
71. Laue BE, Jiang Y, Chhabra SR, Jacob S, Stewart GS, Hardman A, Downie JA, O'Gara F, Williams P (2000) The biocontrol strain Pseudomonas fluorescens F113 produces the Rhizobium small bacteriocin, N-(3-hydroxy-7-cis-tetradecenoyl) homoserine lactone, via HdtS, a putative novel N-acylhomoserine lactone synthase. Microbiology 146:2469-2480.
72. Burton EO, Read HW, Pellitteri MC, Hickey WJ (2005) Identification of acyl-homoserine lactone signal molecules produced by Nitrosomonas europaea strain Schmidt. Appl Environ Microbiol 71:4906-4909. (Pubitemid 41129555)
73. Gilson L, Kuo A, Dunlap PV (1995) AinS and a new family of autoinducer synthesis proteins. J Bacteriol 177:6946-6951.
74. Milton DL, Chalker VJ, Kirke D, Hardman A, Camara M, Williams P (2001) The LuxM homologue VanM from Vibrio anguillarum directs the synthesis of N-(3-hydroxyhexanoyl)homoserine lactone and N-hexanoylhomoserine lactone. J Bacteriol 183:3537-3547. (Pubitemid 32510420)
75. Lerat E, Moran NA (2004) The evolutionary history of quorum-sensing systems in bacteria. Mol Biol Evol 21:903-913. (Pubitemid 38529732)
76. Hanzelka BL, Greenberg EP (1996) Quorum sensing in Vibrio fischeri: evidence that S-adenosylmethionine is the amino acid substrate for autoinducer synthesis. J Bacteriol 178:5291-5294. (Pubitemid 26293091)
77. More MI, Finger LD, Stryker JL, Fuqua C, Eberhard A, Winans SC (1996) Enzymatic synthesis of a quorum-sensing autoinducer through use of defined substrates. Science 272:1655-1658. (Pubitemid 26200025)
78. Parsek MR, Val DL, Hanzelka BL, Cronan JE, Jr, Greenberg EP (1999) Acyl homoserine-lactone quorum-sensing signal generation. Proc Natl Acad Sci USA 96:4360-4365. (Pubitemid 29190341)
79. Val DL, Cronan JE, Jr (1998) In vivo evidence that Sadenosylmethionine and fatty acid synthesis intermediates are the substrates for the LuxI family of autoinducer synthases. J Bacteriol 180:2644-2651. (Pubitemid 28213262)
80. Hanzelka BL, Parsek MR, Val DL, Dunlap PV, Cronan JE, Jr, Greenberg EP (1999) Acylhomoserine lactone synthase activity of the Vibrio fischeri AinS protein. J Bacteriol 181:5766-5770. (Pubitemid 29437149)
81. Schaefer AL, Greenberg EP, Oliver CM, Oda Y, Huang JJ, Bittan-Banin G, Peres CM, Schmidt S, Juhaszova K, Sufrin JR, Harwood CS (2008) A new class of homoserine lactone quorum-sensing signals. Nature 454:595-599.
82. Ahlgren NA, Harwood CS, Schaefer AL, Giraud E, Greenberg EP (2011) Aryl-homoserine lactone quorum sensing in stem-nodulating photosynthetic bradyrhizobia. Proc Natl Acad Sci USA 108:7183-7188.
83. Lindemann A, Pessi G, Schaefer AL, Mattmann ME, Christensen QH, Kessler A, Hennecke H, Blackwell HE, Greenberg EP, Harwood CS (2011) Isovalerylhomoserine lactone, an unusual branched-chain quorum-sensing signal from the soybean symbiont Bradyrhizobium japonicum. Proc Natl Acad Sci USA 108:16765-16770.
84. Hanzelka BL, Stevens AM, Parsek MR, Crone TJ, Greenberg EP (1997) Mutational analysis of theVibrio fischeri LuxI polypeptide: critical regions of an autoinducer synthase. J Bacteriol 179:4882-4887. (Pubitemid 27339736)
85. Watson WT, Minogue TD, Val DL, von Bodman SB, Churchill ME (2002) Structural basis and specificity of acyl-homoserine lactone signal production in bacterial quorum sensing. Mol Cell 9:685-694. (Pubitemid 34273797)
86. Gould TA, Schweizer HP, Churchill ME (2004) Structure of the Pseudomonas aeruginosa acyl-homoserinelactone synthase LasI. Mol Microbiol 53:1135-1146. (Pubitemid 39120435)
87. Chung J, Goo E, Yu S, Choi O, Lee J, Kim J, Kim H, Igarashi J, Suga H, Moon JS, Hwang I, Rhee S (2011) Small-molecule inhibitor binding to an N-acyl-homoserine lactone synthase. Proc Natl Acad Sci USA 108:12089-12094.
88. Holm L, Rosenstrom P (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38:W545-W549.
89. Watson WT, Murphy FVT, Gould TA, Jambeck P, Val DL, Cronan JE, Jr, Beck von Bodman S, Churchill ME (2001) Crystallization and rhenium MAD phasing of the acyl-homoserinelactone synthase EsaI. Acta Crystallogr D Biol Crystallogr 57:1945-1949. (Pubitemid 33145629)
90. Parris KD, Lin L, Tam A, Mathew R, Hixon J, Stahl M, Fritz CC, Seehra J, Somers WS (2000) Crystal structures of substrate binding to Bacillus subtilis holo-(acyl carrier protein) synthase reveal a novel trimeric arrangement of molecules resulting in three active sites. Structure 8:883-895.
91. Huang CC, Smith CV, Glickman MS, Jacobs WR, Jr, Sacchettini JC (2002) Crystal structures of mycolic acid cyclopropane synthases from Mycobacterium tuberculosis. J Biol Chem 277:11559-11569. (Pubitemid 34952927)
92. Raychaudhuri A, Jerga A, Tipton PA (2005) Chemical mechanism and substrate specificity of RhlI, an acylhomoserine lactone synthase from Pseudomonas aeruginosa. Biochemistry 44:2974-2981. (Pubitemid 40297911)
93. Hickman AB, Namboodiri MA, Klein DC, Dyda F (1999) The structural basis of ordered substrate binding by serotonin N-acetyltransferase: enzyme complex at 1.8 A resolution with a bisubstrate analog. Cell 97:361-369.
94. Tanner KG, Trievel RC, Kuo MH, Howard RM, Berger SL, Allis CD, Marmorstein R, Denu JM (1999) Catalytic mechanism and function of invariant glutamic acid 173 from the histone acetyltransferase GCN5 transcriptional coactivator. J Biol Chem 274:18157-18160.
95. Raychaudhuri A, Tullock A, Tipton PA (2008) Reactivity and reaction order in acylhomoserine lactone formation by Pseudomonas aeruginosa RhlI. Biochemistry 47:2893-2898. (Pubitemid 351328841)
96. Choi SH, Greenberg EP (1991) The C-terminal region of the Vibrio fischeri LuxR protein contains an inducer-independent lux gene activating domain. Proc Natl Acad Sci USA 88:11115-11119. (Pubitemid 21915990)
97. Hanzelka BL, Greenberg EP (1995) Evidence that the N-terminal region of the Vibrio fischeri LuxR protein constitutes an autoinducer-binding domain. J Bacteriol 177:815-817.
98. Vannini A, Volpari C, Gargioli C, Muraglia E, Cortese R, De Francesco R, Neddermann P, Marco SD (2002) The crystal structure of the quorum sensing protein TraR bound to its autoinducer and target DNA. EMBO J 21:4393-4401. (Pubitemid 34984326)
99. Zhang RG, Pappas KM, Brace JL, Miller PC, Oulmassov T, Molyneaux JM, Anderson JC, Bashkin JK, Winans SC, Joachimiak A (2002) Structure of a bacterial quorum-sensing transcription factor complexed with pheromone and DNA. Nature 417:971-974. (Pubitemid 34716876)
100. Chen G, Jeffrey PD, Fuqua C, Shi Y, Chen L (2007) Structural basis for antiactivation in bacterial quorum sensing. Proc Natl Acad Sci USA 104:16474-16479. (Pubitemid 350211043)
101. Bottomley MJ, Muraglia E, Bazzo R, Carfi A (2007) Molecular insights into quorum sensing in the human pathogen Pseudomonas aeruginosa from the structure of the virulence regulator LasR bound to its autoinducer. J Biol Chem 282:13592-13600. (Pubitemid 47100513)
102. Lintz MJ, Oinuma K, Wysoczynski CL, Greenberg EP, Churchill ME (2011) Crystal structure of QscR, a Pseudomonas aeruginosa quorum sensing signal receptor. Proc Natl Acad Sci USA 108:15763-15768.
103. Chen G, Swem LR, Swem DL, Stauff DL, O'Loughlin CT, Jeffrey PD, Bassler BL, Hughson FM (2011) A strategy for antagonizing quorum sensing. Mol Cell 42:199-209.
104. Yao Y, Martinez-Yamout MA, Dickerson TJ, Brogan AP, Wright PE, Dyson HJ (2006) Structure of the Escherichia coli quorum sensing protein SdiA: activation of the folding switch by acyl homoserine lactones. J Mol Biol 355:262-273. (Pubitemid 41774130)
105. Zhu J, Winans SC (1999) Autoinducer binding by the quorum-sensing regulator TraR increases affinity for target promoters in vitro and decreases TraR turnover rates in whole cells. Proc Natl Acad Sci USA 96:4832-4837. (Pubitemid 29214497)
106. Aravind L, Ponting CP (1997) The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem Sci 22:458-459. (Pubitemid 27515909)
107. Ducros VM, Lewis RJ, Verma CS, Dodson EJ, Leonard G, Turkenburg JP, Murshudov GN, Wilkinson AJ, Brannigan JA (2001) Crystal structure of GerE, the ultimate transcriptional regulator of spore formation in Bacillus subtilis. J Mol Biol 306:759-771. (Pubitemid 33027698)
108. Kahn D, Ditta G (1991) Modular structure of FixJ: homology of the transcriptional activator domain with the -35 binding domain of sigma factors. Mol Microbiol 5:987-997. (Pubitemid 21896124)
109. Fuqua C, Parsek MR, Greenberg EP (2001) Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35:439-468. (Pubitemid 34032983)
110. Kiratisin P, Tucker KD, Passador L (2002) LasR, a transcriptional activator of Pseudomonas aeruginosa virulence genes, functions as a multimer. J Bacteriol 184:4912-4919.
111. Luo ZQ, Smyth AJ, Gao P, Qin Y, Farrand SK (2003) Mutational analysis of TraR. Correlating function with molecular structure of a quorum-sensing transcriptional activator. J Biol Chem 278:13173-13182. (Pubitemid 36800086)
112. Lamb JR, Patel H, Montminy T, Wagner VE, Iglewski BH (2003) Functional domains of the RhlR transcriptional regulator of Pseudomonas aeruginosa. J Bacteriol 185:7129-7139. (Pubitemid 37509828)
113. Chai Y, Zhu J, Winans SC (2001) TrlR, a defective TraR-like protein of Agrobacterium tumefaciens, blocks TraR function in vitro by forming inactive TrlR:TraR dimers. Mol Microbiol 40:414-421. (Pubitemid 32391635)
114. Luo ZQ, Farrand SK (1999) Signal-dependent DNA binding and functional domains of the quorum-sensing activator TraR as identified by repressor activity. Proc Natl Acad Sci USA 96:9009-9014.
115. Devine JH, Shadel GS, Baldwin TO (1989) Identification of the operator of the lux regulon from the Vibrio fischeri strain ATCC7744. Proc Natl Acad Sci USA 86:5688-5692. (Pubitemid 19218864)
116. Egland KA, Greenberg EP (1999) Quorum sensing in Vibrio fischeri: elements of the luxl promoter. Mol Microbiol 31:1197-1204. (Pubitemid 29082248)
117. Farrand SK, Hwang I, Cook DM (1996) The tra region of the nopaline-type Ti plasmid is a chimera with elements related to the transfer systems of RSF1010, RP4, and F. J Bacteriol 178:4233-4247. (Pubitemid 26240906)
118. Fuqua C, Winans SC (1996) Conserved cis-acting promoter elements are required for density-dependent transcription of Agrobacterium tumefaciens conjugal transfer genes. J Bacteriol 178:435-440. (Pubitemid 26030596)
119. Finney AH, Blick RJ, Murakami K, Ishihama A, Stevens AM (2002) Role of the C-terminal domain of the alpha subunit of RNA polymerase in LuxR-dependent transcriptional activation of the lux operon during quorum sensing. J Bacteriol 184:4520-4528. (Pubitemid 34832580)
120. Johnson DC, Ishihama A, Stevens AM (2003) Involvement of region 4 of the sigma70 subunit of RNA polymerase in transcriptional activation of the lux operon during quorum sensing. FEMS Microbiol Lett 228:193-201. (Pubitemid 37456844)
121. Carlier AL, von Bodman SB (2006) The rcsA promoter of Pantoea stewartii subsp. stewartii features a lowlevel constitutive promoter and an EsaR quorum-sensing-regulated promoter. J Bacteriol 188:4581-4584. (Pubitemid 43865779)
122. White CE, Winans SC (2007) The quorum-sensing transcription factor TraR decodes its DNA binding site by direct contacts with DNA bases and by detection of DNA flexibility. Mol Microbiol 64:245-256. (Pubitemid 46435040)
123. Hentzer M, Givskov M (2003) Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J Clin Invest 112:1300-1307. (Pubitemid 38057681)
124. Ni N, Li M, Wang J, Wang B (2009) Inhibitors and antagonists of bacterial quorum sensing. Med Res Rev 29:65-124.
125. Njoroge J, Sperandio V (2009) Jamming bacterial communication: new approaches for the treatment of infectious diseases. EMBO Mol Med 1:201-210.
126. Muh U, SchusterM, Heim R, Singh A, Olson ER, Greenberg EP (2006) Novel Pseudomonas aeruginosa quorumsensing inhibitors identified in an ultra-high-throughput screen. Antimicrob Agents Chemother 50:3674-3679. (Pubitemid 44684880)
127. Muh U, Hare BJ, Duerkop BA, Schuster M, Hanzelka BL, Heim R, Olson ER, Greenberg EP (2006) A structurally unrelated mimic of a Pseudomonas aeruginosa acyl-homoserine lactone quorum-sensing signal. Proc Natl Acad Sci USA 103:16948-16952. (Pubitemid 44737358)
128. Zou Y, Nair SK (2009) Molecular basis for the recognition of structurally distinct autoinducer mimics by the Pseudomonas aeruginosa LasR quorum-sensing signaling receptor. Chem Biol 16:961-970.