Design principles of the bacterial quorum sensing gene networks

Wiley Interdisciplinary Reviews: Systems Biology and Medicine

Volumn 1, Issue 1, 2009, Pages 45-60

  Goryachev, Andrew B ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); PROKARYOTA;

BACTERIAL PHENOMENA AND FUNCTIONS; GENE REGULATORY NETWORK; QUORUM SENSING; REVIEW; SYSTEMS BIOLOGY;

BACTERIAL PHYSIOLOGICAL PHENOMENA; GENE REGULATORY NETWORKS; QUORUM SENSING; SYSTEMS BIOLOGY;

EID: 78651404976     PISSN: 19395094     EISSN: 1939005X     Source Type: Journal    
DOI: 10.1002/wsbm.27     Document Type: Review

References (184)

1. Barnard AM, Bowden SD, Burr T, Coulthurst SJ, Monson RE, et al. Quorum sensing, virulence and secondary metabolite production in plant soft-rotting bacteria. Philos Trans R Soc Lond B Biol Sci 2007, 362:1165-1183.
2. Wei JR, Lai HC. N-acylhomoserine lactonedependent cell-to-cell communication and social behavior in the genus Serratia. Int J Med Microbiol 2006, 296:117-124.
3. McGowan SJ, Holden MT, Bycroft BW, Salmond GP. Molecular genetics of carbapenem antibiotic biosynthesis. Antonie Van Leeuwenhoek 1999, 75:135-141.
4. Minogue TD, Carlier AL, Koutsoudis MD, von Bodman SB. The cell density-dependent expression of stewartan exopolysaccharide in Pantoea stewartii ssp. Stewartii is a function of EsaR-mediated repression of the rcsA gene. Mol Microbiol 2005, 56:189-203.
5. Hilton T, Rosche T, Froelich B, Smith B, Oliver J. Capsular polysaccharide phase variation in Vibrio vulnificus. Appl Environ Microbiol 2006, 72:6986-6993.
6. Koutsoudis MD, Tsaltas D, Minogue TD, von Bodman SB. Quorum-sensing regulation governs bacterial adhesion, biofilm development, and host colonization in Pantoea stewartii subspecies stewartii. Proc Natl Acad Sci U S A 2006, 103:5983-5988.
7. Dunlap PV. Quorum regulation of luminescence in Vibrio fischeri. J Mol Microbiol Biotechnol 1999, 1:5-12.
8. Nyholm SV, McFall-Ngai MJ. The winnowing: establishing the squid-vibrio symbiosis. Nat Rev Microbiol 2004, 2:632-642.
9. Daniels R, Vanderleyden J, Michiels J. Quorum sensing and swarming migration in bacteria. FEMS Microbiol Rev 2004, 28:261-289.
10. Atkinson S, Chang CY, Sockett RE, Camara M, Williams P. Quorum sensing in Yersinia enterocolitica controls swimming and swarming motility. J Appl Bacteriol 2006, 188:1451-1461.
11. Hussain MB, Zhang HB, Xu JL, Liu Q, Jiang Z, et al. The acyl-homoserine lactone-type quorumsensing system modulates cell motility and virulence of Erwinia chrysanthemi pv. zeae. J Appl Bacteriol 2008, 190:1045-1053.
12. Dunny GM, Winans SC. Cell-Cell Signaling in Bacteria. Washington, D.C: ASM Press; 1999.
13. Nealson KH, Platt T, Hastings JW. Cellular control of the synthesis and activity of the bacterial luminescent system. J Appl Bacteriol 1970, 104:313-322.
14. Engebrecht J, Silverman M. Identification of genes and gene products necessary for bacterial bioluminescence. ProcNatl Acad Sci USA 1984, 81:4154-4158.
15. Fuqua WC, Winans SC, Greenberg EP. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Appl Bacteriol 1994, 176:269-275.
16. Fuqua C, Winans SC, Greenberg EP. Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators. Annu Rev Microbiol 1996, 50:727-751.
17. Swift S, Throup JP, Williams P, Salmond GP, Stewart GS. Quorum sensing: a population-density component in the determination of bacterial phenotype. Trends Biochem Sci 1996, 21:214-219.
18. Swift S, Stewart GS, Williams P. The innerworkings of a quorum sensing signal generator. Trends Microbiol 1996, 4:463-465.
19. Surette MG, Bassler BL. Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc Natl Acad Sci U S A 1998, 95:7046-7050.
20. Hardman AM, Stewart GS, Williams P. Quorum sensing and the cell-cell communication dependent regulation of gene expression in pathogenic and non-pathogenic bacteria. Antonie Van Leeuwenhoek 1998, 74:199-210.
21. Surette MG, Miller MB, Bassler BL. Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. Proc Natl Acad Sci U S A 1999, 96:1639-1644.
22. Parsek MR, Val DL, Hanzelka BL, Cronan JE Jr, Greenberg EP. Acyl homoserine-lactone quorumsensing signal generation. Proc Natl Acad Sci USA 1999, 96:4360-4365.
23. Eberl L.N-acyl homoserinelactone-mediated gene regulation in gram-negative bacteria. Syst Appl Microbiol 1999, 22:493-506.
24. Williams P, Camara M, Hardman A, Swift S, Milton D, et al. Quorum sensing and the populationdependent control of virulence. Philos Trans R Soc Lond B Biol Sci 2000, 355:667-680.
25. Parsek MR, Greenberg EP. Acyl-homoserine lactone quorum sensing in gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proc Natl Acad Sci U S A 2000, 97:8789-8793.
26. Miller MB, Bassler BL. Quorum sensing in bacteria. Annu Rev Microbiol 2001, 55:165-199.
27. Fuqua C, Parsek MR, Greenberg EP. Regulation of gene expression by cell-to-cell communication: acylhomoserine lactone quorum sensing. Annu Rev Genet 2001, 35:439-468.
28. Bassler BL. Small talk. Cell-to-cell communication in bacteria. Cell 2002, 109:421-424.
29. von Bodman SB, Bauer WD, Coplin DL. Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 2003, 41:455-482.
30. Xavier KB, Bassler BL. LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol 2003, 6:191-197.
31. Taga ME, Bassler BL. Chemical communication among bacteria. Proc Natl Acad Sci U S A 2003, 100(suppl 2):14549-14554.
32. Henke JM, Bassler BL. Bacterial social engagements. Trends Cell Biol 2004, 14:648-656.
33. Waters CM, Bassler BL. Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 2005, 21:319-346.
34. Camilli A, Bassler BL. Bacterial small-molecule signaling pathways. Science 2006, 311:1113-1116.
35. Milton DL.Quorum sensing in vibrios: complexity for diversification. Int J MedMicrobiol 2006, 296:61-71.
36. Williams P, Winzer K, Chan WC, Camara M. Look who's talking: communication and quorum sensing in the bacterial world. Philos Trans R Soc Lond B Biol Sci 2007, 362:1119-1134.
37. Dunny GM. The peptide pheromone-inducible conjugation system of Enterococcus faecalis plasmid pCF10: cell-cell signalling, gene transfer, complexity and evolution. Philos Trans R Soc Lond B Biol Sci 2007, 362:1185-1193.
38. Williams P. Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology 2007, 153:3923-3938.
39. Dunny GM, Brickman TJ, Dworkin M. Multicellular behavior in bacteria: communication, cooperation, competition and cheating. Bioessays 2008, 30:296-298.
40. Hughes DT, Sperandio V. Inter-kingdom signalling: communication between bacteria and their hosts. Nat Rev Microbiol 2008, 6:111-120.
41. West SA, Griffin AS, Gardner A, Diggle SP. Social evolution theory for microorganisms. Nat Rev Microbiol 2006, 4:597-607.
42. Diggle SP, Griffin AS, Campbell GS, West SA. Cooperation and conflict in quorum-sensing bacterial populations. Nature 2007, 450:411-414.
43. Finch RG, Pritchard DI, Bycroft BW, Williams P, Stewart GS. Quorum sensing: a novel target for anti-infective therapy. J Antimicrob Chemother 1998, 42:569-571.
44. Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF, et al. Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 2001, 411:813-817.
45. Zhang LH. Quorum quenching and proactive host defense. Trends Plant Sci 2003, 8:238-244.
46. Rice SA, McDougald D, Kumar N, Kjelleberg S. The use of quorum-sensing blockers as therapeutic agents for the control of biofilm-associated infections. Curr Opin Investig Drugs 2005, 6:178-184.
47. Rasmussen TB, Givskov M. Quorum sensing inhibitors: a bargain of effects. Microbiology 2006, 152:895-904.
48. Rasmussen TB, Givskov M. Quorum-sensing inhibitors as anti-pathogenic drugs. Int J Med Microbiol 2006, 296:149-161.
49. Chan WC, Coyle BJ, Williams P. Virulence regulation and quorum sensing in staphylococcal infections: competitive AgrC antagonists as quorum sensing inhibitors. J Med Chem 2004, 47:4633-4641.
50. Dong YH, Wang LY, Zhang LH. Quorum-quenching microbial infections: mechanisms and implications. Philos Trans R Soc Lond B Biol Sci 2007, 362:1201-1211.
51. Gottesman S. Bacterial regulation: global regulatory networks. Annu Rev Genet 1984, 18:415-441.
52. VanBogelen RA, Greis KD, Blumenthal RM, Tani TH, Matthews RG. Mapping regulatory networks in microbial cells. Trends Microbiol 1999, 7:320-328.
53. Gilman A, Arkin AP. Genetic "code": representations and dynamical models of genetic components and networks. Annu Rev Genomics Hum Genet 2002, 3:3341-3369.
54. Herrgard MJ, Covert MW, Palsson BO. Reconstruction of microbial transcriptional regulatory networks. Curr Opin Biotechnol 2004, 15:70-77.
55. Fuqua C, Greenberg EP. Self perception in bacteria: quorum sensing with acylated homoserine lactones. Curr Opin Microbiol 1998, 1:183-189.
56. Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP. Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 2001, 25:365-404.
57. Kleerebezem M, Quadri LE, Kuipers OP, de Vos WM. Quorum sensing by peptide pheromones and two-component signal-transduction systems in Grampositive bacteria. Mol Microbiol 1997, 24:895-904.
58. Dunny GM, Leonard BA. Cell-cell communication in gram-positive bacteria. Annu Rev Microbiol 1997, 51:527-564.
59. Lazazzera BA, Grossman AD. The ins and outs of peptide signaling. Trends Microbiol 1998, 6:288-294.
60. Lyon GJ, Novick RP. Peptide signaling in Staphylococcus aureus and other Gram-positive bacteria. Peptides 2004, 25:1389-1403.
61. Podbielski A, Kreikemeyer B. Cell density-dependent regulation: basic principles and effects on the virulence of Gram-positive cocci. Int J Infect Dis 2004, 8:81-95.
62. Pottathil M, Lazazzera BA. The extracellular Phr peptide-Rap phosphatase signaling circuit of Bacillus subtilis. Front Biosci 2003, 8:d32-d45.
63. Leonard BA, Podbielski A, Hedberg PJ, Dunny GM. Enterococcus faecalis pheromone binding protein, PrgZ, recruits a chromosomal oligopeptide permease system to import sex pheromone cCF10 for induction of conjugation. Proc Natl Acad Sci U S A 1996, 93:260-264.
64. Pearson JP, van Delden C, Iglewski BH. Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals. J Appl Bacteriol 1999, 181:1203-1210.
65. Gray KM, Garey JR. The evolution of bacterial LuxI and LuxR quorum sensing regulators. Microbiology 2001, 147:2379-2387.
66. Lerat E, Moran NA. The evolutionary history of quorum-sensing systems in bacteria. Mol Biol Evol 2004, 21:903-913.
67. Gilson L, Kuo A, Dunlap PV. AinS and a new family of autoinducer synthesis proteins. J Appl Bacteriol 1995, 177:6946-6951.
68. Ortori CA, Atkinson S, Chhabra SR, Camara M, Williams P, et al. Comprehensive profiling of Nacylhomoserine lactones produced by Yersinia pseudotuberculosis using liquid chromatography coupled to hybrid quadrupole-linear ion trap mass spectrometry. Anal Bioanal Chem 2007, 387:497-511.
69. Kobayashi H, Kaern M, Araki M, Chung K, Gardner TS, et al. Programmable cells: interfacing natural and engineered gene networks. Proc Natl Acad Sci U S A 2004, 101:8414-8419.
70. Wang C, Zhang HB, Wang LH, Zhang LH. Succinic semialdehyde couples stress response to quorumsensing signal decay in Agrobacterium tumefaciens. Mol Microbiol 2006, 62:45-56.
71. Lazazzera BA. The intracellular function of extracellular signaling peptides. Peptides 2001, 22:1519-1527.
72. Perego M, Brannigan JA. Pentapeptide regulation of aspartyl-phosphate phosphatases. Peptides 2001, 22:1541-1547.
73. Schauder S, Shokat K, Surette MG, Bassler BL. The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol Microbiol 2001, 41:463-476.
74. Vendeville A, Winzer K, Heurlier K, Tang CM, Hardie KR. Making 'sense' of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat Rev Microbiol 2005, 3:383-396.
75. Neiditch MB, Federle MJ, Miller ST, Bassler BL, Hughson FM. Regulation of LuxPQ receptor activity by the quorum-sensing signal autoinducer-2. Mol Cell 2005, 18:507-518.
76. Xavier KB, Miller ST, Lu W, Kim JH, Rabinowitz J, et al. Phosphorylation and processing of the quorumsensing molecule autoinducer-2 in enteric bacteria. ACS Chem Biol 2007, 2:128-136.
77. Diggle SP, Cornelis P, Williams P, Camara M. 4-quinolone signalling in Pseudomonas aeruginosa: old molecules, new perspectives. Int J Med Microbiol 2006, 296:83-91.
78. Pesci EC, Milbank JB, Pearson JP, McKnight S, Kende AS, et al. Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 1999, 96:11229-11234.
79. Fouhy Y, Lucey JF, Ryan RP, Dow JM. Cell-cell signaling, cyclic di-GMP turnover and regulation of virulence in Xanthomonas campestris. Res Microbiol 2006, 157:899-904.
80. Van Houdt R, Givskov M, Michiels CW. Quorum sensing in Serratia. FEMS Microbiol Rev 2007, 31:407-424.
81. Higgins DA, Pomianek ME, Kraml CM, Taylor RK, Semmelhack MF, et al. The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature 2007, 450:883-886.
82. Takano E. Gamma-butyrolactones: Streptomyces signalling molecules regulating antibiotic production and differentiation. Curr Opin Microbiol 2006, 9:287-294.
83. Nasser W, Reverchon S. New insights into the regulatory mechanisms of the LuxR family of quorum sensing regulators. Anal Bioanal Chem 2007, 387:381-390.
84. Urbanowski ML, Lostroh CP, Greenberg EP. Reversible acyl-homoserine lactone binding to purified Vibrio fischeri LuxR protein. J Appl Bacteriol 2004, 186:631-637.
85. Zhu J, Winans SC. 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 U S A 1999, 96:4832-4837.
86. Zhu J, Winans SC. The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, protease resistance, and dimerization. Proc Natl Acad Sci U S A 2001, 98:1507-1512.
87. McGowan SJ, Barnard AM, BosgelmezG, SebaihiaM, Simpson NJ, et al. Carbapenem antibiotic biosynthesis in Erwinia carotovora is regulated by physiological and genetic factors modulating the quorum sensingdependent control pathway. Mol Microbiol 2005, 55:526-545.
88. von Bodman SB, Majerczak DR, Coplin DL. A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii. Proc Natl Acad Sci U S A 1998, 95:7687-7692.
89. Andersson RA, Eriksson AR, Heikinheimo R, Mae A, Pirhonen M, et al. Quorum sensing in the plant pathogen Erwinia carotovora subsp. carotovora: the role of expR(Ecc). Mol Plant Microbe Interact 2000, 13:384-393.
90. Minogue TD, Wehland-von Trebra M, Bernhard F, von Bodman SB. The autoregulatory role of EsaR, a quorum-sensing regulator in Pantoea stewartii ssp. stewartii: evidence for a repressor function. Mol Microbiol 2002, 44:1625-1635.
91. Burr T, Barnard AM, Corbett MJ, Pemberton CL, SimpsonNJ, et al. Identification of the central quorum sensing regulator of virulence in the enteric phytopathogen, Erwinia carotovora: the VirR repressor. Mol Microbiol 2006, 59:113-125.
92. Nasser W, Bouillant ML, Salmond G, Reverchon S. Characterization of the Erwinia chrysanthemi expIexpR locus directing the synthesis of two N-acylhomoserine lactone signal molecules. Mol Microbiol 1998, 29:1391-1405.
93. Sjoblom S, Brader G, Koch G, Palva ET. Cooperation of two distinct ExpR regulators controls quorum sensing specificity and virulence in the plant pathogen Erwinia carotovora. Mol Microbiol 2006, 60:1474-1489.
94. Cui Y, Chatterjee A, Hasegawa H, Chatterjee AK. Erwinia carotovora subspecies produce duplicate variants of ExpR, LuxR homologs that activate rsmA transcription but differ in their interactions with Nacylhomoserine lactone signals. J Appl Bacteriol 2006, 188:4715-4726.
95. Shadel GS, Baldwin TO. Positive autoregulation of the Vibrio fischeri luxR gene. LuxR and autoinducer activate cAMP-catabolite gene activator protein complexindependent and -dependent luxR transcription. J Biochem Mol Biol Biophys 1992, 267:7696-7702.
96. Atkinson S, Sockett RE, CamaraM, Williams P. Quorum sensing and the lifestyle of Yersinia. Curr Issues Mol Biol 2006, 8:1-10.
97. Atkinson S, Chang CY, Patrick HL, Buckley CM, Wang Y, et al. Functional interplay between the Yersinia pseudotuberculosis YpsRI and YtbRI quorum sensing systems modulates swimming motility by controlling expression of flhDC and fliA. Mol Microbiol 2008, 69:137-151.
98. White CE, Winans SC. Cell-cell communication in the plant pathogen Agrobacterium tumefaciens. Philos Trans R Soc Lond B Biol Sci 2007, 362:1135-1148.
99. Shadel GS, Baldwin TO. The Vibrio fischeri LuxR protein is capable of bidirectional stimulation of transcription and both positive and negative regulation of the luxR gene. J Appl Bacteriol 1991, 173:568-574.
100. Schuster M, Greenberg EP. A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol 2006, 296:73-81.
101. Showalter RE, Martin MO, Silverman MR. Cloning and nucleotide sequence of luxR, a regulatory gene controlling bioluminescence in Vibrio harveyi. J Appl Bacteriol 1990, 172:2946-2954.
102. JoblingMG, Holmes RK. 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 1997, 26:1023-1034.
103. Hammer BK, Bassler BL. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 2003, 50:101-104.
104. Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, et al. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci U S A 2002, 99:3129-3134.
105. Fidopiastis PM, Miyamoto CM, Jobling MG, Meighen EA, Ruby EG. LitR, a new transcriptional activator in Vibrio fischeri, regulates luminescence and symbiotic light organ colonization. Mol Microbiol 2002, 45:131-143.
106. De Silva RS, Kovacikova G, Lin W, Taylor RK, Skorupski K, et al. Crystal structure of the Vibrio cholerae quorum-sensing regulatory proteinHapR. J Appl Bacteriol 2007, 189:5683-5691.
107. Ramos JL, Martinez-Bueno M, Molina-Henares AJ, TeranW, Watanabe K, et al. The TetR family of transcriptional repressors. Microbiol Mol Biol Rev 2005, 69:326-356.
108. Meibom KL, Blokesch M, Dolganov NA, Wu CY, Schoolnik GK. Chitin induces natural competence in Vibrio cholerae. Science 2005, 310:1824-1827.
109. Lin YH, Miyamoto C, Meighen EA. Purification and characterization of a luxO promoter binding protein LuxT from Vibrio harveyi. Protein Expr Purif 2000, 20:87-94.
110. Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, et al. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 2004, 118:69-82.
111. Henke JM, Bassler BL. Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J Appl Bacteriol 2004, 186:6902-6914.
112. Lenz DH, Miller MB, Zhu J, Kulkarni RV, Bassler BL. CsrA and three redundant small RNAs regulate quorum sensing in Vibrio cholerae. Mol Microbiol 2005, 58:1186-1202.
113. Yarwood JM, Schlievert PM. Quorum sensing in Staphylococcus infections. J Clin Invest 2003, 112:1620-1625.
114. Tyson JJ, Chen KC, Novak B. Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell. Curr Opin Cell Biol 2003, 15:221-231.
115. Ferrell JE Jr. Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability. Curr Opin Cell Biol 2002, 14:140-148.
116. Ozbudak EM, Thattai M, Lim HN, Shraiman BI, Van Oudenaarden A. Multistability in the lactose utilization network of Escherichia coli. Nature 2004, 427:737-740.
117. SantillanM, MackeyMC. Quantitative approaches to the study of bistability in the lac operon of Escherichia coli. J R Soc Interface 2008, 5(suppl 1):S29-S39.
118. Tyson JJ, Chen K, Novak B. Network dynamics and cell physiology. Nat Rev Mol Cell Biol 2001, 2:908-916.
119. Dockery JD, Keener JP. A mathematical model for quorum sensing in Pseudomonas aeruginosa. Bull Math Biol 2001, 63:95-116.
120. James S, Nilsson P, James G, Kjelleberg S, Fagerstrom T. Luminescence control in the marine bacterium Vibrio fischeri: an analysis of the dynamics of lux regulation. J Biochem Mol Biol 2000, 296:1127-1137.
121. Goryachev AB, Toh DJ, Lee T. Systems analysis of a quorum sensing network: design constraints imposed by the functional requirements, network topology and kinetic constants. Biosystems 2006, 83:178-187.
122. Kaufmann BB, Van Oudenaarden A. Stochastic gene expression: from single molecules to the proteome. Curr Opin Genet Dev 2007, 17:107-112.
123. ElowitzMB, Levine AJ, Siggia ED, Swain PS. Stochastic gene expression in a single cell. Science 2002, 297:1183-1186.
124. Welch M, Todd DE, Whitehead NA, McGowan SJ, Bycroft BW, et al. N-acyl homoserine lactone binding to the CarR receptor determines quorum-sensing specificity in Erwinia. EMBO J 2000, 19:631-641.
125. Zhu J, Oger PM, Schrammeijer B, Hooykaas PJ, Farrand SK, et al. The bases of crown gall tumorigenesis. J Appl Bacteriol 2000, 182:3885-3895.
126. Zhang RG, Pappas T, Brace JL, Miller PC, Oulmassov T, et al. Structure of a bacterial quorum-sensing transcription factor complexed with pheromone and DNA. Nature 2002, 417:971-974.
127. Brennan RG, Link TM. Hfq structure, function and ligand binding. Curr Opin Microbiol 2007, 10:125-133.
128. Salazar C, Hofer T. Competition effects shape the response sensitivity and kinetics of phosphorylation cycles in cell signaling. Ann N Y Acad Sci 2006, 109:1517-1530.
129. Neves SR, Iyengar R. Modeling of signaling networks. Bioessays 2002, 24:1110-1117.
130. Vandenesch F, Kornblum J, Novick RP. A temporal signal, independent of agr, is required for hla but not spa transcription in Staphylococcus aureus. J Appl Bacteriol 1991, 173:6313-6320.
131. Majdalani N, Vanderpool CK, Gottesman S. Bacterial small RNA regulators. Crit Rev BiochemMol Biol 2005, 40:93-113.
132. Babitzke P, Romeo T. CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr Opin Microbiol 2007, 10:156-163.
133. Kay E, Dubuis C, Haas D. Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0. Proc Natl Acad Sci U S A 2005, 102:17136-17141.
134. Levine E, Zhang Z, Kuhlman T, Hwa T. Quantitative characteristics of gene regulation by small RNA. PLoS Biol 2007, 5:e229.
135. Aiba H. Mechanism of RNA silencing by Hfqbinding small RNAs. Curr Opin Microbiol 2007, 10:134-139.
136. Shimoni Y, Friedlander G, Hetzroni G, Niv G, Altuvia S, et al. Regulation of gene expression by small noncoding RNAs: a quantitative view. Mol Syst Biol 2007, 3:138.
137. Bejerano-Sagie M, Xavier KB. The role of small RNAs in quorum sensing. Curr Opin Microbiol 2007, 10:189-198.
138. Barnard AM, Salmond GP. Quorum sensing in Erwinia species. Anal Bioanal Chem 2007, 387:415-423.
139. Hwang I, Smyth AJ, Luo ZQ, Farrand SK. Modulating quorum sensing by antiactivation: TraM interacts with TraR to inhibit activation of Ti plasmid conjugal transfer genes. Mol Microbiol 1999, 34:282-294.
140. Swiderska A, Berndtson AK, ChaMR, Li L, Beaudoin GM III, et al. Inhibition of the Agrobacterium tumefaciens TraR quorum-sensing regulator. Interactions with the TraM anti-activator. J Biochem Mol Biol Biophys 2001, 276:49449-49458.
141. Qin Y, Su S, Farrand SK.Molecular basis of transcriptional antiactivation. TraM disrupts the TraR-DNA complex through stepwise interactions. J Biochem Mol Biol Biophys 2007, 282:19979-19991.
142. Goryachev AB, Toh DJ, Wee KB, Lee T, Zhang HB, et al. Transition to quorum sensing in an Agrobacterium population: a stochastic model. PLoS Comput Biol 2005, 1:e37.
143. Withers H, Swift S, Williams P. Quorum sensing as an integral component of gene regulatory networks in Gram-negative bacteria. Curr Opin Microbiol 2001, 4:186-193.
144. Venturi V. Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev 2006, 30:274-291.
145. Juhas M, Eberl L, Tummler B. Quorum sensing: the power of cooperation in the world of Pseudomonas. Environ Microbiol 2005, 7:459-471.
146. Milton DL, Chalker VJ, Kirke D, Hardman A, Camara M, et al. The LuxM homologue VanM from Vibrio anguillarum directs the synthesis of N-(3-hydroxyhexanoyl)homoserine lactone and Nhexanoylhomoserine lactone. J Appl Bacteriol 2001, 183:3537-3547.
147. Miller MB, Skorupski K, Lenz DH, Taylor RK, Bassler BL. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 2002, 110:303-314.
148. Waters CM, Bassler BL. The Vibrio harveyi quorumsensing system uses shared regulatory components to discriminate between multiple autoinducers. Genes Dev 2006, 20:2754-2767.
149. Latifi A, Foglino M, Tanaka K, Williams P, Lazdunski A. A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol 1996, 21:1137-1146.
150. Pesci EC, Pearson JP, Seed PC, Iglewski BH. Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Appl Bacteriol 1997, 179:3127-3132.
151. Lupp C, Urbanowski M, Greenberg EP, Ruby EG. The Vibrio fischeri quorum-sensing systems ain and lux sequentially induce luminescence gene expression and are important for persistence in the squid host. Mol Microbiol 2003, 50:319-331.
152. Lupp C, Ruby EG. Vibrio fischeri uses two quorumsensing systems for the regulation of early and late colonization factors. J Appl Bacteriol 2005, 187:3620-3629.
153. Antunes LC, Schaefer AL, Ferreira RB, QinN, Stevens AM, et al. Transcriptome analysis of the Vibrio fischeri LuxR-LuxI regulon. J Appl Bacteriol 2007, 189:8387-8391.
154. Majdalani N, Gottesman S. The Rcs phosphorelay: a complex signal transduction system. Annu RevMicrobiol 2005, 59:379-405.
155. Wehland M, Kiecker C, Coplin DL, Kelm O, Saenger W, et al. Identification of an RcsA/RcsB recognition motif in the promoters of exopolysaccharide biosynthetic operons from Erwinia amylovora and Pantoea stewartii subsp. stewartii. J Biochem Mol Biol Biophys 1999, 274:3300-3307.
156. Carlier AL, von Bodman SB. The rcsA promoter of Pantoea stewartii subsp. stewartii features a lowlevel constitutive promoter and an EsaR quorumsensing-regulated promoter. J Appl Bacteriol 2006, 188:4581-4584.
157. Romling U, Amikam D. Cyclic di-GMP as a second messenger. Curr Opin Microbiol 2006, 9:218-228.
158. Jenal U, Malone J. Mechanisms of cyclic-di-GMP signaling in bacteria. Annu Rev Genet 2006, 40:385-407.
159. Ryan RP, Fouhy Y, Lucey JF, Dow JM. Cyclic di-GMP signaling in bacteria: recent advances and new puzzles. J Appl Bacteriol 2006, 188:8327-8334.
160. Cotter PA, Stibitz S. c-di-GMP-mediated regulation of virulence and biofilm formation. Curr Opin Microbiol 2007, 10:17-23.
161. Waters CM, Lu W, Rabinowitz JD, Bassler BL. Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic di-GMP levels and repression of vpsT. J Appl Bacteriol 2008, 190:2527-2536.
162. Rahman M, Simm R, Kader A, Basseres E, Romling U, et al. The role of c-di-GMP signaling in an Aeromonas veronii biovar sobria strain. FEMS Microbiol Lett 2007, 273:172-179.
163. Heermann R, Fuchs TM. Comparative analysis of the Photorhabdus luminescens and the Yersinia enterocolitica genomes: uncovering candidate genes involved in insect pathogenicity. BMC Genomics 2008, 9:40.
164. Williamson NR, Fineran PC, OgawaW, Woodley LR, Salmond GP. Integrated regulation involving quorum sensing, a two-component system, a GGDEF/EAL domain protein and a post-transcriptional regulator controls swarming and RhlA-dependent surfactant biosynthesis in Serratia. Environ Microbiol 2008, 10:1202-1217.
165. Koerber AJ, King JR, Williams P. Deterministic and stochastic modelling of endosome escape by Staphylococcus aureus: "quorum" sensing by a single bacterium. J Math Biol 2005, 50:440-488.
166. Redfield RJ. Is quorum sensing a side effect of diffusion sensing? Trends Microbiol 2002, 10:365-370.
167. McLean RJ, WhiteleyM, Stickler DJ, Fuqua WC. Evidence of autoinducer activity in naturally occurring biofilms. FEMS Microbiol Lett 1997, 154:259-263.
168. Stickler DJ, MorrisNS, McLean RJ, Fuqua C. Biofilms on indwelling urethral catheters produce quorumsensing signal molecules in situ and in vitro. Appl Environ Microbiol 1998, 64:3486-3490.
169. Parsek MR, Greenberg EP. Quorum sensing signals in development of Pseudomonas aeruginosa biofilms. Methods Enzymol 1999, 310:43-55.
170. Singh PK, Schaefer AL, Parsek MR, Moninger TO, Welsh MJ, et al. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 2000, 407:762-764.
171. Schembri MA, Givskov M, Klemm P. An attractive surface: gram-negative bacterial biofilms. Sci STKE 2002, 132:RE6.
172. Chopp DL, Kirisits MJ, Moran B, Parsek MR. A mathematical model of quorum sensing in a growing bacterial biofilm. J Ind Microbiol Biotechnol 2002, 29:339-346.
173. Ward JP, King JR, Koerber AJ, Croft JM, Sockett RE, et al. Early development and quorum sensing in bacterial biofilms. J Math Biol 2003, 47:23-55.
174. Lenz AP, Williamson K, Pitts B, Stewart PS, Franklin MJ. Localized gene expression in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 2008, 74:4463-4471.
175. Wagner VE, Iglewski BH. P. aeruginosa biofilms in CF infection. Clin Rev Allergy Immunol 2008, 35:124-134.
176. Boles BR, Horswill AR. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 2008, 4:e1000052.
177. Nadell CD, Xavier JB, Levin SA, Foster KR. The evolution of quorum sensing in bacterial biofilms. PLoS Biol 2008, 6:e14.
178. Losick R, Kaiser D. Why and how bacteria communicate. Sci Am 1997, 276:68-73.
179. Dworkin M. Shape, polarity, and multicellular morphogenesis. Curr Opin Microbiol 2007, 10:588-590.
180. Aguilar C, Vlamakis H, Losick R, Kolter R. Thinking about Bacillus subtilis as a multicellular organism. Curr Opin Microbiol 2007, 10:638-643.
181. Kaiser D. Coupling cell movement to multicellular development in myxobacteria. Nat Rev Microbiol 2003, 1:45-54.
182. Kholodenko BN. Cell-signalling dynamics in time and space. Nat Rev Mol Cell Biol 2006, 7:165-176.
183. Viretta AU, Fussenegger M. Modeling the quorum sensing regulatory network of human-pathogenic Pseudomonas aeruginosa. Biotechnol Prog 2004, 20:670-678.
184. Ward JP, King JR, Koerber AJ, Williams P, Croft JM, et al. Mathematical modelling of quorum sensing in bacteria. IMA J Math Appl Med Biol 2001, 18:263-292.