AI-2-mediated signalling in bacteria

FEMS Microbiology Reviews

Volumn 37, Issue 2, 2013, Pages 156-181

  Pereira, Catarina S ^a,b   Thompson, Jessica A ^a,b   Xavier, Karina B ^a,b  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

Autoinducer 2; Bacterial signalling; Interspecies communication; LuxS; Quorum sensing; S adenosylmethionine

Indexed keywords

ADENINE; ADENOSINE; AUTOINDUCER 2 PROTEIN; AUTOINDUCER 2 RECEPTOR; BACTERIAL ENZYME; BACTERIAL PROTEIN; COENZYME A; HOMOCYSTEINE; METHIONINE; METHYLTRANSFERASE; N ACYLHOMOSERINE LACTONE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RECEPTOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; S ADENOSYLMETHIONINE; S RIBOSYLHOMOCYSTEINASE; UNCLASSIFIED DRUG;

ACTINOBACILLUS PLEUROPNEUMONIAE; ACTINOMYCES NAESLUNDII; AGGREGATIBACTER ACTINOMYCETEMCOMITANS; BACILLUS CEREUS; BACTERIAL GENE; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM; BINDING SITE; BORRELIA BURGDORFERI; ECOLOGICAL NICHE; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENZYME ANALYSIS; ENZYME BINDING; ENZYME METABOLISM; ENZYME REGULATION; ENZYME RELEASE; ENZYME SYNTHESIS; ESCHERICHIA COLI; EVOLUTIONARY ADAPTATION; GENE EXPRESSION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HAEMOPHILUS INFLUENZAE; HELICOBACTER PYLORI; MICROBIAL COMMUNITY; MICROFLORA; MORAXELLA CATARRHALIS; MOUTH FLORA; MYCOBACTERIUM AVIUM; NASOPHARYNX; NONHUMAN; OROPHARYNX; PATHOGENESIS; PHENOTYPE; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN TRANSPORT; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; REVIEW; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; SINORHIZOBIUM MELILOTI; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STREPTOCOCCUS ANGINOSUS; STREPTOCOCCUS GORDONII; STREPTOCOCCUS INTERMEDIUS; STREPTOCOCCUS ORALIS; STREPTOCOCCUS PNEUMONIAE; VIBRIO CHOLERAE; VIBRIO HARVEYI;

ADAPTATION, PHYSIOLOGICAL; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; GENE EXPRESSION REGULATION, BACTERIAL; HOMOSERINE; LACTONES; PHENOTYPE; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS);

EID: 84873315902     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/j.1574-6976.2012.00345.x     Document Type: Review

References (193)

1. Ahmed NA, Petersen FC & Scheie AA (2007) AI-2 quorum sensing affects antibiotic susceptibility in Streptococcus anginosus. J Antimicrob Chemother 60: 49-53.
2. Ahmed NA, Petersen FC & Scheie AA (2008) Biofilm formation and autoinducer-2 signaling in Streptococcus intermedius: role of thermal and pH factors. Oral Microbiol Immunol 23: 492-497.
3. Ahmed NA, Petersen FC & Scheie AA (2009) AI-2/LuxS is involved in increased biofilm formation by Streptococcus intermedius in the presence of antibiotics. Antimicrob Agents Chemother 53: 4258-4263.
4. Alfaro JF, Zhang T, Wynn DP, Karschner EL & Zhou ZS (2004) Synthesis of LuxS inhibitors targeting bacterial cell-cell communication. Org Lett 6: 3043-3046.
5. Amara N, Krom BP, Kaufmann GF & Meijler MM (2011) Macromolecular inhibition of quorum sensing: enzymes, antibodies, and beyond. Chem Rev 111: 195-208.
6. Antonova ES & Hammer BK (2011) Quorum-sensing autoinducer molecules produced by members of a multispecies biofilm promote horizontal gene transfer to Vibrio cholerae. FEMS Microbiol Lett 322: 68-76.
7. Armbruster CE, Hong W, Pang B, Dew KE, Juneau RA, Byrd MS, Love CF, Kock ND & Swords WE (2009) LuxS promotes biofilm maturation and persistence of nontypeable haemophilus influenzae in vivo via modulation of lipooligosaccharides on the bacterial surface. Infect Immun 77: 4081-4091.
8. Armbruster CE, Hong W, Pang B, Weimer KE, Juneau RA, Turner J & Swords WE (2010) Indirect pathogenicity of Haemophilus influenzae and Moraxella catarrhalis in polymicrobial otitis media occurs via interspecies quorum signaling. MBio 1: e00102-10.
9. Armbruster CE, Pang B, Murrah K, Juneau RA, Perez AC, Weimer KE & Swords WE (2011) RbsB (NTHI_0632) mediates quorum signal uptake in nontypeable Haemophilus influenzae strain 86-028NP. Mol Microbiol 82: 836-850.
10. Ascenso OS, Marques JC, Santos AR, Xavier KB, Ventura MR & Maycock CD (2011) An efficient synthesis of the precursor of AI-2, the signalling molecule for inter-species quorum sensing. Bioorg Med Chem 19: 1236-1241.
11. Auger S, Krin E, Aymerich S & Gohar M (2006) Autoinducer 2 affects biofilm formation by Bacillus cereus. Appl Environ Microbiol 72: 937-941.
12. Babb K, von Lackum K, Wattier RL, Riley SP & Stevenson B (2005) Synthesis of autoinducer 2 by the lyme disease spirochete, Borrelia burgdorferi. J Bacteriol 187: 3079-3087.
13. Bansal T, Jesudhasan P, Pillai S, Wood TK & Jayaraman A (2008) Temporal regulation of enterohemorrhagic Escherichia coli virulence mediated by autoinducer-2. Appl Microbiol Biotechnol 78: 811-819.
14. Bassler BL (1999) How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr Opin Microbiol 2: 582-587.
15. Bassler BL & Losick R (2006) Bacterially speaking. Cell 125: 237-246.
16. 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.
17. Bassler BL, Wright M & Silverman MR (1994) Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol Microbiol 13: 273-286.
18. Bassler BL, Greenberg EP & Stevens AM (1997) Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi. J Bacteriol 179: 4043-4045.
19. Beeston AL & Surette MG (2002) pfs-dependent regulation of autoinducer 2 production in Salmonella enterica serovar Typhimurium. J Bacteriol 184: 3450-3456.
20. Blevins JS, Revel AT, Caimano MJ, Yang XF, Richardson JA, Hagman KE & Norgard MV (2004) The luxS gene is not required for Borrelia burgdorferi tick colonization, transmission to a mammalian host, or induction of disease. Infect Immun 72: 4864-4867.
21. Boos W & Lucht JM (1996) Periplasmic binding-protein-dependent ABC transporters. Escherichia coli and Salmonella: Cellular and Molecular Biology, Vol. 1 (Neidhardt FC, Curtiss R, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M & Umbarger HE, eds), pp. 580-599. American Society of Microbiology, Washington, DC.
22. Bordignon E, Grote M & Schneider E (2010) The maltose ATP-binding cassette transporter in the 21st century - towards a structural dynamic perspective on its mode of action. Mol Microbiol 77: 1354-1366.
23. Brackman G, Celen S, Hillaert U, Van Calenbergh S, Cos P, Maes L, Nelis HJ & Coenye T (2011) Structure-activity relationship of cinnamaldehyde analogs as inhibitors of AI-2 based quorum sensing and their effect on virulence of Vibrio spp. PLoS ONE 6: e16084.
24. Casino P, Rubio V & Marina A (2010) The mechanism of signal transduction by two-component systems. Curr Opin Struct Biol 20: 763-771.
25. 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.
26. Choi J, Shin D & Ryu S (2007) Implication of quorum sensing in Salmonella enterica serovar Typhimurium virulence: the luxS gene is necessary for expression of genes in pathogenicity island 1. Infect Immun 75: 4885-4890.
27. Choi J, Shin D, Kim M, Park J, Lim S & Ryu S (2012) LsrR-mediated quorum sensing controls invasiveness of Salmonella typhimurium by regulating SPI-1 and flagella genes. PLoS ONE 7: e37059.
28. Cluzel ME, Zanella-Cleon I, Cozzone AJ, Futterer K, Duclos B & Molle V (2010) The Staphylococcus aureus autoinducer-2 synthase LuxS is regulated by Ser/Thr phosphorylation. J Bacteriol 192: 6295-6301.
29. Cole SP, Harwood J, Lee R, She R & Guiney DG (2004) Characterization of monospecies biofilm formation by Helicobacter pylori. J Bacteriol 186: 3124-3132.
30. Croxatto A, Pride J, Hardman A, Williams P, Camara M & Milton DL (2004) A distinctive dual-channel quorum-sensing system operates in Vibrio anguillarum. Mol Microbiol 52: 1677-1689.
31. De Keersmaecker SC, Varszegi C, van Boxel N, Habel LW, Metzger K, Daniels R, Marchal K, De Vos D & Vanderleyden J (2005) Chemical synthesis of (S)-4, 5-dihydroxy-2, 3-pentanedione, a bacterial signal molecule precursor, and validation of its activity in Salmonella typhimurium. J Biol Chem 280: 19563-19568.
32. De Lay N & Gottesman S (2009) The Crp-activated small noncoding regulatory RNA CyaR (RyeE) links nutritional status to group behavior. J Bacteriol 191: 461-476.
33. DeLisa MP, Wu CF, Wang L, Valdes JJ & Bentley WE (2001) DNA microarray-based identification of genes controlled by autoinducer 2-stimulated quorum sensing in Escherichia coli. J Bacteriol 183: 5239-5247.
34. Derzelle S, Duchaud E, Kunst F, Danchin A & Bertin P (2002) Identification, characterization, and regulation of a cluster of genes involved in carbapenem biosynthesis in Photorhabdus luminescens. Appl Environ Microbiol 68: 3780-3789.
35. Deutscher J, Francke C & Postma PW (2006) How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol Mol Biol Rev 70: 939-1031.
36. Diaz Z, Xavier KB & Miller ST (2009) The crystal structure of the Escherichia coli autoinducer-2 processing protein LsrF. PLoS ONE 4: e6820.
37. Doherty N, Holden MT, Qazi SN, Williams P & Winzer K (2006) Functional analysis of luxS in Staphylococcus aureus reveals a role in metabolism but not quorum sensing. J Bacteriol 188: 2885-2897.
38. Doherty NC, Shen F, Halliday NM, Barrett DA, Hardie KR, Winzer K & Atherton JC (2010) In Helicobacter pylori, LuxS is a key enzyme in cysteine provision through a reverse transsulfuration pathway. J Bacteriol 192: 1184-1192.
39. Dong YH, Wang LY & Zhang LH (2007) Quorum-quenching microbial infections: mechanisms and implications. Philos Trans R Soc Lond B Biol Sci 362: 1201-1211.
40. Duan K, Dammel C, Stein J, Rabin H & Surette MG (2003) Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol Microbiol 50: 1477-1491.
41. Eicken C, Sharma V, Klabunde T, Lawrenz MB, Hardham JM, Norris SJ & Sacchettini JC (2002) Crystal structure of Lyme disease variable surface antigen VlsE of Borrelia burgdorferi. J Biol Chem 277: 21691-21696.
42. Engebrecht J & Silverman M (1987) Nucleotide sequence of the regulatory locus controlling expression of bacterial genes for bioluminescence. Nucleic Acids Res 15: 10455-10467.
43. Engebrecht J, Nealson K & Silverman M (1983) Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell 32: 773-781.
44. Federle MJ (2009) Autoinducer-2-based chemical communication in bacteria: complexities of interspecies signaling. Contrib Microbiol 16: 18-32.
45. Fernandes R, Roy V, Wu HC & Bentley WE (2010) Engineered biological nanofactories trigger quorum sensing response in targeted bacteria. Nat Nanotechnol 5: 213-217.
46. Fong KP, Chung WO, Lamont RJ & Demuth DR (2001) Intra- and interspecies regulation of gene expression by Actinobacillus actinomycetemcomitans LuxS. Infect Immun 69: 7625-7634.
47. Fong KP, Gao L & Demuth DR (2003) luxS and arcB control aerobic growth of Actinobacillus actinomycetemcomitans under iron limitation. Infect Immun 71: 298-308.
48. Fontecave M, Atta M & Mulliez E (2004) S-adenosylmethionine: nothing goes to waste. Trends Biochem Sci 29: 243-249.
49. Freeman JA & Bassler BL (1999) A genetic analysis of the function of LuxO, a two-component response regulator involved in quorum sensing in Vibrio harveyi. Mol Microbiol 31: 665-677.
50. Frezza M, Soulere L, Queneau Y & Doutheau A (2005) A Baylis-Hillman/ozonolysis route towards (+/-) 4, 5-dihydroxy-2, 3-pentanedione (DPD) and analogues. Tetrahedron Lett 46: 6495-6498.
51. Frezza M, Soulère L, Balestrino D, Gohar M, Deshayes C, Queneau Y, Forestier C & Doutheau A (2007) Ac2-DPD, the bis-(O)-acetylated derivative of 4, 5-dihydroxy-2, 3-pentanedione (DPD) is a convenient stable precursor of bacterial quorum sensing autoinducer AI-2. Bioorg Med Chem Lett 17: 1428-1431.
52. 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.
53. 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.
54. Gambello MJ, Kaye S & Iglewski BH (1993) LasR of Pseudomonas aeruginosa is a transcriptional activator of the alkaline protease gene (apr) and an enhancer of exotoxin A expression. Infect Immun 61: 1180-1184.
55. Gamby S, Roy V, Guo M, Smith JA, Wang J, Stewart JE, Wang X, Bentley WE & Sintim HO (2012) Altering the communication networks of multispecies microbial systems using a diverse toolbox of AI-2 analogs. ACS Chem Biol 7: 1023-1030.
56. Ganin H, Tang X & Meijler MM (2009) Inhibition of Pseudomonas aeruginosa quorum sensing by AI-2 analogs. Bioorg Med Chem Lett 19: 3941-3944.
57. Garner AL, Park J, Zakhari JS, Lowery CA, Struss AK, Sawada D, Kaufmann GF & Janda KD (2011) A multivalent probe for AI-2 quorum-sensing receptors. J Am Chem Soc 133: 15934-15937.
58. Geier H, Mostowy S, Cangelosi GA, Behr MA & Ford TE (2008) Autoinducer-2 triggers the oxidative stress response in Mycobacterium avium, leading to biofilm formation. Appl Environ Microbiol 74: 1798-1804.
59. Giron JA, Torres AG, Freer E & Kaper JB (2002) The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol Microbiol 44: 361-379.
60. Gonzalez Barrios AF, Zuo R, Hashimoto Y, Yang L, Bentley WE & Wood TK (2006) Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). J Bacteriol 188: 305-316.
61. Greenberg EP, Hastings JW & Ulitzur S (1979) Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch Microbiol 120: 87-91.
62. Hammer BK & Bassler BL (2003) Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 50: 101-104.
63. Hammer BK & Bassler BL (2007) Regulatory small RNAs circumvent the conventional quorum sensing pathway in pandemic Vibrio cholerae. P Natl Acad Sci USA 104: 11145-11149.
64. Hardie KR & Heurlier K (2008) Establishing bacterial communities by 'word of mouth': LuxS and autoinducer 2 in biofilm development. Nat Rev Microbiol 6: 635-643.
65. Hardie KR, Cooksley C, Green AD & Winzer K (2003) Autoinducer 2 activity in Escherichia coli culture supernatants can be actively reduced despite maintenance of an active synthase, LuxS. Microbiology 149: 715-728.
66. Hebert CG, Gupta A, Fernandes R, Tsao CY, Valdes JJ & Bentley WE (2010) Biological nanofactories target and activate epithelial cell surfaces for modulating bacterial quorum sensing and interspecies signaling. ACS Nano 4: 6923-6931.
67. Hegde M, Englert DL, Schrock S, Cohn WB, Vogt C, Wood TK, Manson MD & Jayaraman A (2011) Chemotaxis to the quorum-sensing signal AI-2 requires the Tsr chemoreceptor and the periplasmic LsrB AI-2-binding protein. J Bacteriol 193: 768-773.
68. Henke JM & Bassler BL (2004a) Quorum sensing regulates type III secretion in Vibrio harveyi and Vibrio parahaemolyticus. J Bacteriol 186: 3794-3805.
69. Henke JM & Bassler BL (2004b) Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J Bacteriol 186: 6902-6914.
70. Herzberg M, Kaye IK, Peti W & Wood TK (2006) YdgG (TqsA) controls biofilm formation in Escherichia coli K-12 through autoinducer 2 transport. J Bacteriol 188: 587-598.
71. Hilgers MT & Ludwig ML (2001) Crystal structure of the quorum-sensing protein LuxS reveals a catalytic metal site. P Natl Acad Sci USA 98: 11169-11174.
72. Hol C, Van Dijke EE, Verduin CM, Verhoef J & van Dijk H (1994) Experimental evidence for Moraxella-induced penicillin neutralization in pneumococcal pneumonia. J Infect Dis 170: 1613-1616.
73. Hubner A, Revel AT, Nolen DM, Hagman KE & Norgard MV (2003) Expression of a luxS gene is not required for Borrelia burgdorferi infection of mice via needle inoculation. Infect Immun 71: 2892-2896.
74. James D, Shao H, Lamont RJ & Demuth DR (2006) The Actinobacillus actinomycetemcomitans ribose binding protein RbsB interacts with cognate and heterologous autoinducer 2 signals. Infect Immun 74: 4021-4029.
75. Jesudhasan PR, Cepeda ML, Widmer K, Dowd SE, Soni KA, Hume ME, Zhu J & Pillai SD (2010) Transcriptome analysis of genes controlled by luxS/autoinducer-2 in Salmonella enterica serovar Typhimurium. Foodborne Pathog Dis 7: 399-410.
76. Jobling MG & Holmes RK (1997) Characterization of hapR, a positive regulator of the Vibrio cholerae HA/protease gene hap, and its identification as a functional homologue of the Vibrio harveyi luxR gene. Mol Microbiol 26: 1023-1034.
77. Kadirvel M, Stimpson WT, Moumene-Afifi S et al. (2010) Synthesis and bioluminescence-inducing properties of autoinducer (S)-4, 5-dihydroxypentane-2, 3-dione and its enantiomer. Bioorg Med Chem Lett 20: 2625-2628.
78. Kamaraju K, Smith J, Wang J, Roy V, Sintim HO, Bentley WE & Sukharev S (2011) Effects on membrane lateral pressure suggest permeation mechanisms for bacterial quorum signaling molecules. Biochemistry 50: 6983-6993.
79. Karavolos MH, Bulmer DM, Winzer K, Wilson M, Mastroeni P, Williams P & Khan CM (2008) LuxS affects flagellar phase variation independently of quorum sensing in Salmonella enterica serovar typhimurium. J Bacteriol 190: 769-771.
80. Kavanaugh JS, Gakhar L & Horswill AR (2011) The structure of LsrB from Yersinia pestis complexed with autoinducer-2. Acta Crystallogr Sect F Struct Biol Cryst Commun 67: 1501-1505.
81. Keller L & Surette MG (2006) Communication in bacteria: an ecological and evolutionary perspective. Nat Rev Microbiol 4: 249-258.
82. Kint G, Sonck KA, Schoofs G, De Coster D, Vanderleyden J & De Keersmaecker SC (2009) 2D proteome analysis initiates new insights on the Salmonella Typhimurium LuxS protein. BMC Microbiol 9: 198.
83. Krell T, Lacal J, Busch A, Silva-Jimenez H, Guazzaroni ME & Ramos JL (2010) Bacterial sensor kinases: diversity in the recognition of environmental signals. Annu Rev Microbiol 64: 539-559.
84. Krin E, Chakroun N, Turlin E et al. (2006) Pleiotropic role of quorum-sensing autoinducer 2 in Photorhabdus luminescens. Appl Environ Microbiol 72: 6439-6451.
85. Lazazzera BA (2010) The phosphoenolpyruvate phosphotransferase system: as important for biofilm formation by Vibrio cholerae as it is for metabolism in Escherichia coli. J Bacteriol 192: 4083-4085.
86. Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS & Bassler BL (2004) The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118: 69-82.
87. Lewis HA, Furlong EB, Laubert B et al. (2001) A structural genomics approach to the study of quorum sensing: crystal structures of three LuxS orthologs. Structure 9: 527-537.
88. Li J, Wang L, Hashimoto Y, Tsao CY, Wood TK, Valdes JJ, Zafiriou E & Bentley WE (2006) A stochastic model of Escherichia coli AI-2 quorum signal circuit reveals alternative synthesis pathways. Mol Syst Biol 2: 67.
89. Li J, Attila C, Wang L, Wood TK, Valdes JJ & Bentley WE (2007) Quorum sensing in Escherichia coli is signaled by AI-2/LsrR: effects on small RNA and biofilm architecture. J Bacteriol 189: 6011-6020.
90. Li M, Villaruz AE, Vadyvaloo V, Sturdevant DE & Otto M (2008) AI-2-dependent gene regulation in Staphylococcus epidermidis. BMC Microbiol 8: 4.
91. Li L, Xu Z, Zhou Y, Li T, Sun L, Chen H & Zhou R (2011) Analysis on Actinobacillus pleuropneumoniae LuxS regulated genes reveals pleiotropic roles of LuxS/AI-2 on biofilm formation, adhesion ability and iron metabolism. Microb Pathog 50: 293-302.
92. Li H, Zhao H, Zhu L, Hong L, Zhang H, Lin F, Xu C, Li S & Zhang Z (2012) Crystallization and preliminary X-ray analysis of S-ribosylhomocysteinase from Streptococcus mutans. Acta Crystallogr Sect F Struct Biol Cryst Commun 68: 199-202.
93. Lilley BN & Bassler BL (2000) Regulation of quorum sensing in Vibrio harveyi by LuxO and sigma-54. Mol Microbiol 36: 940-954.
94. Long T, Tu KC, Wang Y, Mehta P, Ong NP, Bassler BL & Wingreen NS (2009) Quantifying the integration of quorum-sensing signals with single-cell resolution. PLoS Biol 7: e68.
95. Lowery CA, Abe T, Park J, Eubanks LM, Sawada D, Kaufmann GF & Janda KD (2009) Revisiting AI-2 quorum sensing inhibitors: direct comparison of alkyl-DPD analogues and a natural product fimbrolide. J Am Chem Soc 131: 15584-15585.
96. Maddocks JL & May JR (1969) 'Indirect pathogenicity' of penicillinase-producing enterobacteria in chronic bronchial infections. Lancet 1: 793-795.
97. Marques JC, Lamosa P, Russell C, Ventura R, Maycock C, Semmelhack MF, Miller ST & Xavier KB (2011) Processing the interspecies quorum-sensing signal autoinducer-2 (AI-2): characterization of phospho-(S)-4, 5-dihydroxy-2, 3-pentanedione isomerization by LsrG protein. J Biol Chem 286: 18331-18343.
98. McGee DJ, Langford ML, Watson EL, Carter JE, Chen YT & Ottemann KM (2005) Colonization and inflammation deficiencies in Mongolian gerbils infected by Helicobacter pylori chemotaxis mutants. Infect Immun 73: 1820-1827.
99. McNab R, Ford SK, El-Sabaeny A, Barbieri B, Cook GS & Lamont RJ (2003) LuxS-based signaling in Streptococcus gordonii: autoinducer-2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J Bacteriol 185: 274-284.
100. Meijler MM, Hom LG, Kaufmann GF, McKenzie KM, Sun C, Moss JA, Matsushita M & Janda KD (2004) Synthesis and biological validation of a ubiquitous quorum-sensing molecule. Angew Chem Int Ed Engl 43: 2106-2108.
101. Miller CH & Duerre JA (1968) S-ribosylhomocysteine cleavage enzyme from Escherichia coli. J Biol Chem 243: 92-97.
102. Miller MB, Skorupski K, Lenz DH, Taylor RK & Bassler BL (2002) Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110: 303-314.
103. 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.
104. Mok KC, Wingreen NS & Bassler BL (2003) Vibrio harveyi quorum sensing: a coincidence detector for two autoinducers controls gene expression. EMBO J 22: 870-881.
105. Nealson KH, Platt T & Hastings JW (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol 104: 313-322.
106. Neiditch MB, Federle MJ, Miller ST, Bassler BL & Hughson FM (2005) Regulation of LuxPQ receptor activity by the quorum-sensing signal autoinducer-2. Mol Cell 18: 507-518.
107. 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.
108. Ng WL & Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43: 197-222.
109. Niu C, Afre S & Gilbert ES (2006) Subinhibitory concentrations of cinnamaldehyde interfere with quorum sensing. Lett Appl Microbiol 43: 489-494.
110. Njoroge J & Sperandio V (2009) Jamming bacterial communication: new approaches for the treatment of infectious diseases. EMBO Mol Med 1: 201-210.
111. Osaki T, Hanawa T, Manzoku T et al. (2006) Mutation of luxS affects motility and infectivity of Helicobacter pylori in gastric mucosa of a Mongolian gerbil model. J Med Microbiol 55: 1477-1485.
112. Ottemann KM & Lowenthal AC (2002) Helicobacter pylori uses motility for initial colonization and to attain robust infection. Infect Immun 70: 1984-1990.
113. Parveen N & Cornell KA (2011) Methylthioadenosine/S-adenosylhomocysteine nucleosidase, a critical enzyme for bacterial metabolism. Mol Microbiol 79: 7-20.
114. Pecharki D, Petersen FC & Scheie AA (2008) LuxS and expression of virulence factors in Streptococcus intermedius. Oral Microbiol Immunol 23: 79-83.
115. Pereira CS, McAuley JR, Taga ME, Xavier KB & Miller ST (2008) Sinorhizobium meliloti, a bacterium lacking the autoinducer-2 (AI-2) synthase, responds to AI-2 supplied by other bacteria. Mol Microbiol 70: 1223-1235.
116. Pereira CS, de Regt AK, Brito PH, Miller ST & Xavier KB (2009) Identification of functional LsrB-like autoinducer-2 receptors. J Bacteriol 191: 6975-6987.
117. Pereira CS, Santos AJ, Bejerano-Sagie M, Correia PB, Marques JC & Xavier KB (2012) Phosphoenolpyruvate phosphotransferase system regulates detection and processing of the quorum sensing signal autoinducer-2. Mol Microbiol 84: 93-104.
118. Perrett CA, Karavolos MH, Humphrey S et al. (2009) LuxS-based quorum sensing does not affect the ability of Salmonella enterica serovar Typhimurium to express the SPI-1 type 3 secretion system, induce membrane ruffles, or invade epithelial cells. J Bacteriol 191: 7253-7259.
119. Piper KR, Beck von Bodman S & Farrand SK (1993) Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature 362: 448-450.
120. Pirhonen M, Flego D, Heikinheimo R & Palva ET (1993) A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora. EMBO J 12: 2467-2476.
121. Plummer P, Zhu J, Akiba M, Pei D & Zhang Q (2011) Identification of a key amino acid of LuxS involved in AI-2 production in Campylobacter jejuni. PLoS ONE 6: e15876.
122. Postma PW, Lengeler JW & Jacobson GR (1993) Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 57: 543-594.
123. Prouty AM, Schwesinger WH & Gunn JS (2002) Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp. Infect Immun 70: 2640-2649.
124. Rader BA, Campagna SR, Semmelhack MF, Bassler BL & Guillemin K (2007) The quorum-sensing molecule autoinducer 2 regulates motility and flagellar morphogenesis in Helicobacter pylori. J Bacteriol 189: 6109-6117.
125. Rader BA, Wreden C, Hicks KG, Sweeney EG, Ottemann KM & Guillemin K (2011) Helicobacter pylori perceives the quorum-sensing molecule AI-2 as a chemorepellent via the chemoreceptor TlpB. Microbiology 157: 2445-2455.
126. 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.
127. Ren D, Sims JJ & Wood TK (2001) Inhibition of biofilm formation and swarming of Escherichia coli by (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone. Environ Microbiol 3: 731-736.
128. Ren D, Bedzyk LA, Ye RW, Thomas SM & Wood TK (2004a) Differential gene expression shows natural brominated furanones interfere with the autoinducer-2 bacterial signaling system of Escherichia coli. Biotechnol Bioeng 88: 630-642.
129. Ren D, Bedzyk LA, Ye RW, Thomas SM & Wood TK (2004b) Stationary-phase quorum-sensing signals affect autoinducer-2 and gene expression in Escherichia coli. Appl Environ Microbiol 70: 2038-2043.
130. Rettner RE & Saier MH Jr (2010) The autoinducer-2 exporter superfamily. J Mol Microbiol Biotechnol 18: 195-205.
131. Rezzonico F & Duffy B (2008) Lack of genomic evidence of AI-2 receptors suggests a non-quorum sensing role for luxS in most bacteria. BMC Microbiol 8: 154.
132. Rickard AH, Palmer RJ Jr, Blehert DS, Campagna SR, Semmelhack MF, Egland PG, Bassler BL & Kolenbrander PE (2006) Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol Microbiol 60: 1446-1456.
133. Riley SP, Bykowski T, Babb K, von Lackum K & Stevenson B (2007) Genetic and physiological characterization of the Borrelia burgdorferi ORF BB0374-pfs-metK-luxS operon. Microbiology 153: 2304-2311.
134. Roy V, Fernandes R, Tsao CY & Bentley WE (2010a) Cross species quorum quenching using a native AI-2 processing enzyme. ACS Chem Biol 5: 223-232.
135. Roy V, Smith JA, Wang J, Stewart JE, Bentley WE & Sintim HO (2010b) Synthetic analogs tailor native AI-2 signaling across bacterial species. J Am Chem Soc 132: 11141-11150.
136. Roy V, Adams BL & Bentley WE (2011) Developing next generation antimicrobials by intercepting AI-2 mediated quorum sensing. Enzyme Microb Technol 49: 113-123.
137. Rui F, Marques JC, Miller ST, Maycock CD, Xavier KB & Ventura MR (2012) Stereochemical diversity of AI-2 analogs modulates quorum sensing in Vibrio harveyi and Escherichia coli. Bioorg Med Chem 20: 249-256.
138. Rutherford ST, van Kessel JC, Shao Y & Bassler BL (2011) AphA and LuxR/HapR reciprocally control quorum sensing in vibrios. Genes Dev 25: 397-408.
139. Ruzheinikov SN, Das SK, Sedelnikova SE et al. (2001) The 1.2 A structure of a novel quorum-sensing protein, Bacillus subtilis LuxS. J Mol Biol 313: 111-122.
140. Saenz GC, Rao D, Underwood A, Belapure SA, Campagna SR, Sun Z, Tammariello S & Rickard AH (2012) Autoinducer-2 influences interactions amongst pioneer colonizing streptococci in oral biofilms. Microbiology, in press.
141. Schauder S & Bassler BL (2001) The languages of bacteria. Genes Dev 15: 1468-1480.
142. 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.
143. Semmelhack MF, Campagna SR, Federle MJ & Bassler BL (2005) An expeditious synthesis of DPD and boron binding studies. Org Lett 7: 569-572.
144. Shao H, Lamont RJ & Demuth DR (2007a) Autoinducer 2 is required for biofilm growth of Aggregatibacter (Actinobacillus) actinomycetemcomitans. Infect Immun 75: 4211-4218.
145. Shao H, James D, Lamont RJ & Demuth DR (2007b) Differential interaction of Aggregatibacter (Actinobacillus) actinomycetemcomitans LsrB and RbsB proteins with autoinducer 2. J Bacteriol 189: 5559-5565.
146. Shao CP, Lo HR, Lin JH & Hor LI (2011) Regulation of cytotoxicity by quorum-sensing signaling in Vibrio vulnificus is mediated by SmcR, a repressor of HlyU. J Bacteriol 193: 2557-2565.
147. Shen G, Rajan R, Zhu J, Bell CE & Pei D (2006) Design and synthesis of substrate and intermediate analogue inhibitors of S-ribosylhomocysteinase. J Med Chem 49: 3003-3011.
148. Shen F, Hobley L, Doherty N, Loh JT, Cover TL, Sockett RE, Hardie KR & Atherton JC (2010) In Helicobacter pylori auto-inducer-2, but not LuxS/MccAB catalysed reverse transsulphuration, regulates motility through modulation of flagellar gene transcription. BMC Microbiol 10: 210.
149. Silva AJ, Leitch GJ, Camilli A & Benitez JA (2006) Contribution of hemagglutinin/protease and motility to the pathogenesis of El Tor biotype Cholera. Infect Immun 74: 2072-2079.
150. Smith JA, Wang J, Nguyen-Mau SM, Lee V & Sintim HO (2009) Biological screening of a diverse set of AI-2 analogues in Vibrio harveyi suggests that receptors which are involved in synergistic agonism of AI-2 and analogues are promiscuous. Chem Commun (Camb) 7: 7033-7035.
151. Soni KA, Jesudhasan PR, Cepeda M, Williams B, Hume M, Russell WK, Jayaraman A & Pillai SD (2008) Autoinducer AI-2 is involved in regulating a variety of cellular processes in Salmonella Typhimurium. Foodborne Pathog Dis 5: 147-153.
152. Stevenson B & Babb K (2002) LuxS-mediated quorum sensing in Borrelia burgdorferi, the lyme disease spirochete. Infect Immun 70: 4099-4105.
153. Stevenson B, von Lackum K, Wattier RL, McAlister JD, Miller JC & Babb K (2003) Quorum sensing by the Lyme disease spirochete. Microbes Infect 5: 991-997.
154. Sun J, Daniel R, Wagner-Dobler I & Zeng AP (2004) Is autoinducer-2 a universal signal for interspecies communication: a comparative genomic and phylogenetic analysis of the synthesis and signal transduction pathways. BMC Evol Biol 4: 36.
155. Surette MG, Miller MB & Bassler BL (1999) Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. P Natl Acad Sci USA 96: 1639-1644.
156. Svenningsen SL, Tu KC & Bassler BL (2009) Gene dosage compensation calibrates four regulatory RNAs to control Vibrio cholerae quorum sensing. EMBO J 28: 429-439.
157. 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.
158. Taga ME, Miller ST & Bassler BL (2003) Lsr-mediated transport and processing of AI-2 in Salmonella typhimurium. Mol Microbiol 50: 1411-1427.
159. Tavender TJ, Halliday NM, Hardie KR & Winzer K (2008) LuxS-independent formation of AI-2 from ribulose-5-phosphate. BMC Microbiol 8: 98.
160. Thakker M, Park JS, Carey V & Lee JC (1998) Staphylococcus aureus serotype 5 capsular polysaccharide is antiphagocytic and enhances bacterial virulence in a murine bacteremia model. Infect Immun 66: 5183-5189.
161. Tomasz A & Hotchkiss RD (1964) Regulation of the transformability of pneumococcal cultures by macromolecular cell products. P Natl Acad Sci USA 51: 480-487.
162. Tsuchikama K, Lowery CA & Janda KD (2011) Probing autoinducer-2 based quorum sensing: the biological consequences of molecules unable to traverse equilibrium states. J Org Chem 76: 6981-6989.
163. Tu KC & Bassler BL (2007) Multiple small RNAs act additively to integrate sensory information and control quorum sensing in Vibrio harveyi. Genes Dev 21: 221-233.
164. Tu KC, Waters CM, Svenningsen SL & Bassler BL (2008) A small-RNA-mediated negative feedback loop controls quorum-sensing dynamics in Vibrio harveyi. Mol Microbiol 70: 896-907.
165. Tu KC, Long T, Svenningsen SL, Wingreen NS & Bassler BL (2010) Negative feedback loops involving small regulatory RNAs precisely control the Vibrio harveyi quorum-sensing response. Mol Cell 37: 567-579.
166. Udekwu KI (2010) Transcriptional and post-transcriptional regulation of the Escherichia coli luxS mRNA; involvement of the sRNA MicA. PLoS ONE 5: e13449.
167. Vendeville A, Winzer K, Heurlier K, Tang CM & Hardie KR (2005) Making 'sense' of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat Rev Microbiol 3: 383-396.
168. Vidal JE, Ludewick HP, Kunkel RM, Zahner D & Klugman KP (2011) The LuxS-dependent quorum-sensing system regulates early biofilm formation by Streptococcus pneumoniae strain D39. Infect Immun 79: 4050-4060.
169. von Lackum K, Babb K, Riley SP, Wattier RL, Bykowski T & Stevenson B (2006) Functionality of Borrelia burgdorferi LuxS: the Lyme disease spirochete produces and responds to the pheromone autoinducer-2 and lacks a complete activated-methyl cycle. Int J Med Microbiol 296(suppl 40): 92-102.
170. Voyich JM, Braughton KR, Sturdevant DE et al. (2005) Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J Immunol 175: 3907-3919.
171. Wang L, Hashimoto Y, Tsao CY, Valdes JJ & Bentley WE (2005a) Cyclic AMP (cAMP) and cAMP receptor protein influence both synthesis and uptake of extracellular autoinducer 2 in Escherichia coli. J Bacteriol 187: 2066-2076.
172. Wang L, Li J, March JC, Valdes JJ & Bentley WE (2005b) luxS-dependent gene regulation in Escherichia coli K-12 revealed by genomic expression profiling. J Bacteriol 187: 8350-8360.
173. Waters CM & Bassler BL (2006) The Vibrio harveyi quorum-sensing system uses shared regulatory components to discriminate between multiple autoinducers. Genes Dev 20: 2754-2767.
174. Winans SC (2002) Bacterial esperanto. Nat Struct Biol 9: 83-84.
175. Winzer K, Hardie KR & Williams P (2002a) Bacterial cell-to-cell communication: sorry, can't talk now - gone to lunch! Curr Opin Microbiol 5: 216-222.
176. Winzer K, Hardie KR, Burgess N et al. (2002b) LuxS: its role in central metabolism and the in vitro synthesis of 4-hydroxy-5-methyl-3(2H)-furanone. Microbiology 148: 909-922.
177. Winzer K, Hardie KR & Williams P (2003) LuxS and autoinducer-2: their contribution to quorum sensing and metabolism in bacteria. Adv Appl Microbiol 53: 291-396.
178. Wnuk SF, Robert J, Sobczak AJ, Meyers BP, Malladi VL, Zhu J, Gopishetty B & Pei D (2009) Inhibition of S-ribosylhomocysteinase (LuxS) by substrate analogues modified at the ribosyl C-3 position. Bioorg Med Chem 17: 6699-6706.
179. Xavier KB & Bassler BL (2003) LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol 6: 191-197.
180. Xavier KB & Bassler BL (2005a) Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli. J Bacteriol 187: 238-248.
181. Xavier KB & Bassler BL (2005b) Interference with AI-2-mediated bacterial cell-cell communication. Nature 437: 750-753.
182. Xavier KB, Miller ST, Lu W, Kim JH, Rabinowitz J, Pelczer I, Semmelhack MF & Bassler BL (2007) Phosphorylation and processing of the quorum-sensing molecule autoinducer-2 in enteric bacteria. ACS Chem Biol 2: 128-136.
183. Xue T, Zhao L, Sun H, Zhou X & Sun B (2009) LsrR-binding site recognition and regulatory characteristics in Escherichia coli AI-2 quorum sensing. Cell Res 19: 1258-1268.
184. Yajima A (2011) Synthesis of microbial signaling molecules and their stereochemistry-activity relationships. Biosci Biotechnol Biochem 75: 1418-1429.
185. Yildiz FH & Visick KL (2009) Vibrio biofilms: so much the same yet so different. Trends Microbiol 17: 109-118.
186. Yuan J, Wang B, Sun Z et al. (2008) Analysis of host-inducing proteome changes in Bifidobacterium longum NCC2705 grown in vivo. J Proteome Res 7: 375-385.
187. Zhang L, Murphy PJ, Kerr A & Tate ME (1993) Agrobacterium conjugation and gene regulation by N-acyl-L-homoserine lactones. Nature 362: 446-448.
188. Zhang Y, Gardina PJ, Kuebler AS, Kang HS, Christopher JA & Manson MD (1999) Model of maltose-binding protein/chemoreceptor complex supports intrasubunit signaling mechanism. P Natl Acad Sci USA 96: 939-944.
189. Zhao L, Xue T, Shang F, Sun H & Sun B (2010) Staphylococcus aureus AI-2 quorum sensing associates with the KdpDE two-component system to regulate capsular polysaccharide synthesis and virulence. Infect Immun 78: 3506-3515.
190. Zhu P & Li M (2012) Recent progresses on AI-2 bacterial quorum sensing inhibitors. Curr Med Chem 19: 174-186.
191. Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL & Mekalanos JJ (2002) Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. P Natl Acad Sci USA 99: 3129-3134.
192. Zhu J, Dizin E, Hu X, Wavreille AS, Park J & Pei D (2003) S-Ribosylhomocysteinase (LuxS) is a mononuclear iron protein. Biochemistry 42: 4717-4726.
193. Zhu C, Feng S, Sperandio V, Yang Z, Thate TE, Kaper JB & Boedeker EC (2007) The possible influence of LuxS in the in vivo virulence of rabbit enteropathogenic Escherichia coli. Vet Microbiol 125: 313-322.