Chapter 6 : Regulatory Networks in Pathogenic Bacteria: Lessons from Cell-Cell Communication in

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Signal transduction and gene regulation show the steepest dependence on the total number of genes among all functional categories of genes in prokaryotic genomes, and this disproportionate increase in the hierarchical complexity of gene regulation with the increase in genome size may ultimately control the maximum achievable genome size. and are motile organisms with comparatively large genomes and complex regulatory systems reflecting their adaptability to diverse environments. Researchers have begun to decipher the underlying transcriptional networks and the role that these networks play in responding to a multitude of environmental conditions. The authors focus on one such regulatory network, quorum sensing, which allows to regulate hundreds of genes, many of which encode virulence factors, in response to population size. The genome-scale studies described in this chapter reveal that quorum sensing is a global regulatory system that affects many different cellular functions. The route of infection of course depends on the predisposing condition (for example, ventilator-associated pneumonia, burns, surgical wounds, and extended-wear contact lenses predispose to acute infection, whereas cystic fibrosis and implanted medical devices predispose to chronic infection) but also represents an important commitment by because acute and chronic routes of infection involve distinctly different virulence factors and bacterial lifestyles. quorum sensing is one of the best-understood cell-cell communication systems in bacteria.

Citation: Schuster M, Greenberg E. 2007. Regulatory Networks in Pathogenic Bacteria: Lessons from Cell-Cell Communication in , p 75-88. In Brogden K, Minion F, Cornick N, Stanton T, Zhang Q, Nolan L, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815851.ch6

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Type III Secretion System
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Signaling complexity is related to genome size. Shown are the numbers of signaling systems (one- and two-component systems) corresponding to 150 sequenced genomes as a function of genome size (raw data were taken from reference ). Black diamonds, pathogenic bacteria emphasized in the text.

Citation: Schuster M, Greenberg E. 2007. Regulatory Networks in Pathogenic Bacteria: Lessons from Cell-Cell Communication in , p 75-88. In Brogden K, Minion F, Cornick N, Stanton T, Zhang Q, Nolan L, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815851.ch6
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Image of FIGURE 2

Quorum-sensing circuitry. The schematic emphasizes the acyl-HSL signals, genes, and corresponding protein components of each quorum-sensing system. Circles denote acyl-HSL signals. Boxes upstream of target genes indicate conserved regulatory elements to which LasR, RhlR, or QscR bind. Some target (tgt) genes within the quorum-sensing regulon are activated by both LasR and RhlR.

Citation: Schuster M, Greenberg E. 2007. Regulatory Networks in Pathogenic Bacteria: Lessons from Cell-Cell Communication in , p 75-88. In Brogden K, Minion F, Cornick N, Stanton T, Zhang Q, Nolan L, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815851.ch6
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Image of FIGURE 3

Interconnection of quorum sensing with other regulatory networks. See the text for a detailed explanation. For enhanced clarity, effects on signal synthase and receptor expression have not been detailed separately. PA1760 is one of several predicted transcriptional regulators that is activated by quorum sensing and appears to mediate quorum-sensing gene expression indirectly. The quorum-sensing regulon is defined as the collection of genes that is activated by LasR–3OC12-HSL or RhlR–C4-HSL, directly or indirectly. The different regulators shown affect the expression of overlapping subsets within the quorum-sensing (QS) regulon. ppGpp, guanosine tetraphosphate.

Citation: Schuster M, Greenberg E. 2007. Regulatory Networks in Pathogenic Bacteria: Lessons from Cell-Cell Communication in , p 75-88. In Brogden K, Minion F, Cornick N, Stanton T, Zhang Q, Nolan L, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815851.ch6
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1. Abdelrahman, Y. M., and, R. J. Belland. 2005. The chlamydial developmental cycle. FEMS Microbiol. Rev. 29:949959.
2. Albus, A. M.,, E. C. Pesci,, L. J. Runyen Janecky,, S. E. West, and, B. H. Iglewski. 1997. Vfr controls quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 179:39283935.
3. Anderson, R. M.,, C. A. Zimprich, and, L. Rust. 1999. A second operator is involved in Pseudomonas aeruginosa elastase (lasB) activation. J. Bacteriol. 181:62646270.
4. Anguige, K.,, J. R. King,, J. P. Ward, and, P. Williams. 2004. Mathematical modelling of therapies targeted at bacterial quorum sensing. Math. Biosci. 192:3983.
5. Arevalo-Ferro, C.,, M. Hentzer,, G. Reil,, A. Gorg,, S. Kjelleberg,, M. Givskov,, K. Riedel, and, L. Eberl. 2003. Identification of quorum-sensing regulated proteins in the opportunistic pathogen Pseudomonas aeruginosa by proteomics. Environ. Microbiol. 5:13501369.
6. Chugani, S. A.,, M. Whiteley,, K. M. Lee,, D. D. Argenio,, C. Manoil, and, E. P. Greenberg. 2001. QscR, a modulator of quorum-sensing signal synthesis and virulence in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 98:27522757.
7. Costerton, J. W. 2001. Cystic fibrosis pathogenesis and the role of biofilms in persistent infection. Trends Microbiol. 9:5052.
8. Dacheux, D.,, I. Attree, and, B. Toussaint. 2001. Expression of ExsA in trans confers type III secretion system-dependent cytotoxicity on noncytotoxic Pseudomonas aeruginosa cystic fibrosis isolates. Infect. Immun. 69:538542.
9. de Kievit, T.,, P. C. Seed,, J. Nezezon,, L. Passador, and, B. H. Iglewski. 1999. RsaL, a novel repressor of virulence gene expression in Pseudomonas aeruginosa. J. Bacteriol. 181:21752184.
10. Deziel, E.,, S. Gopalan,, A. P. Tampakaki,, F. Lepine,, K. E. Padfield,, M. Saucier,, G. Xiao, and, L. G. Rahme. 2005. The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones. Mol. Microbiol. 55:9981014.
11. Deziel, E.,, F. Lepine,, S. Milot,, J. He,, M. N. Mindrinos,, R. G. Tompkins, and, L. G. Rahme. 2004. Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication. Proc. Natl. Acad. Sci. USA 101:13391344.
12. Diggle, S. P.,, K. Winzer,, S. R. Chhabra,, K. E. Worrall,, M. Camara, and, P. Williams. 2003. The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol. Microbiol. 50:2943.
13. Diggle, S. P.,, K. Winzer,, A. Lazdunski,, P. Williams, and, M. Camara. 2002. Advancing the quorum in Pseudomonas aeruginosa: MvaT and the regulation of N-acylhomoserine lactone production and virulence gene expression. J. Bacteriol. 184:25762586.
14. Dinwiddie, R. 2000. Pathogenesis of lung disease in cystic fibrosis. Respiration 67:38.
15. Fagerlind, M. G.,, P. Nilsson,, M. Harlen,, S. Karlsson,, S. A. Rice, and, S. Kjelleberg. 2005. Modeling the effect of acylated homoserine lactone antagonists in Pseudomonas aeruginosa. Biosystems 80:201213.
16. Fagerlind, M. G.,, S. A. Rice,, P. Nilsson,, M. Harlen,, S. James,, T. Charlton, and, S. Kjelleberg. 2003. The role of regulators in the expression of quorum-sensing signals in Pseudomonas aeruginosa. J. Mol. Microbiol. Biotechnol. 6:88100.
17. Fleischmann, R. D.,, M. D. Adams,, O. White,, R. A. Clayton,, E. F. Kirkness,, A. R. Kerlavage,, C. J. Bult,, J. F. Tomb,, B. A. Dougherty,, J. M. Merrick,, K. McKenney,, G. Sutton,, W. Fitz Hugh,, C. Fields,, J. D. Gocayne,, J. Scott,, R. Shirley,, L. Liu,, A. Glodek,, J. M. Kelley,, J. F. Weidman,, C. A. Phillips,, T. Spriggs,, E. Hedblom,, M. D. Cotton,, T. R. Utterback,, M. C. Hanna,, D. T. Nguyen,, D. M. Saudek,, R. C. Brandon,, L. D. Fine,, J. L. Fritchman,, J. L. Fuhrmann,, N. S. M. Geoghagen,, C. L. Gnehm,, L. A. McDonald,, K. V. Small,, C. M. Fraser,, H. O. Smith, and, V. J. Craig. 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496512.
18. Fraser, C. M.,, J. D. Gocayne,, O. White,, M. D. Adams,, R. A. Clayton,, R. D. Fleischmann,, C. J. Bult,, A. R. Kerlavage,, G. Sutton,, J. M. Kelley,, R. D. Fritchman,, J. F. Weidman,, K. V. Small,, M. Sandusky,, J. Fuhrmann,, D. Nguyen,, T. R. Utterback,, D. M. Saudek,, C. A. Phillips,, J. M. Merrick,, J. F. Tomb,, B. A. Dougherty,, K. F. Bott,, P. C. Hu,, T. S. Lucier,, S. N. Peterson,, H. O. Smith,, C. A. Hutchison III, and, J. C. Venter. 1995. The minimal gene complement of Mycoplasma genitalium. Science 270:397403.
19. Friedman, L., and, R. Kolter. 2004. Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J. Bacteriol. 186:44574465.
20. Gallagher, L. A.,, S. L. McKnight,, M. S. Kuznetsova,, E. C. Pesci, and, C. Manoil. 2002. Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J. Bacteriol. 184:64726480.
21. Gambello, M. J., and, B. H. Iglewski. 1991. Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. J. Bacteriol. 173:30003009.
22. Goodman, A. L.,, B. Kulasekara,, A. Rietsch,, D. Boyd,, R. S. Smith, and, S. Lory. 2004. A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev. Cell 7:745754.
23. Goodman, A. L., and, S. Lory. 2004. Analysis of regulatory networks in Pseudomonas aeruginosa by genomewide transcriptional profiling. Curr. Opin. Microbiol. 7:3944.
24. Heidelberg, J. F.,, J. A. Eisen,, W. C. Nelson,, R. A. Clayton,, M. L. Gwinn,, R. J. Dodson,, D. H. Haft,, E. K. Hickey,, J. D. Peterson,, L. Umayam,, S. R. Gill,, K. E. Nelson,, T. D. Read,, H. Tettelin,, D. Richardson,, M. D. Ermolaeva,, J. Vamathevan,, S. Bass,, H. Qin,, I. Dragoi,, P. Sellers,, L. McDonald,, T. Utterback,, R. D. Fleishmann,, W. C. Nierman,, O. White,, S. L. Salzberg,, H. O. Smith,, R. R. Colwell,, J. J. Mekalanos,, J. C. Venter, and, C. M. Fraser. 2000. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406:477483.
25. Hentzer, M.,, H. Wu,, J. B. Andersen,, K. Riedel,, T. B. Rasmussen,, N. Bagge,, N. Kumar,, M. A. Schembri,, Z. Song,, P. Kristoffersen,, M. Manefield,, J. W. Costerton,, S. Molin,, L. Eberl,, P. Steinberg,, S. Kjelleberg,, N. Hoiby, and, M. Givskov. 2003. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22:38033815.
26. Heurlier, K.,, F. Williams,, S. Heeb,, C. Dormond,, G. Pessi,, D. Singer,, M. Camara,, P. Williams, and, D. Haas. 2004. Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J. Bacteriol. 186:29362945.
27. Hoch, J. A., and, T. J. Silhavy. 1995. Two-Component Signal Transduction. ASM Press, Washington, DC.
28. Jackson, K. D.,, M. Starkey,, S. Kremer,, M. R. Parsek, and, D. J. Wozniak. 2004. Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J. Bacteriol. 186:44664475.
29. Juhas, M.,, L. Wiehlmann,, B. Huber,, D. Jordan,, J. Lauber,, P. Salunkhe,, A. S. Limpert,, F. von Gotz,, I. Steinmetz,, L. Eberl, and, B. Tummler. 2004. Global regulation of quorum sensing and virulence by VqsR in Pseudomonas aeruginosa. Microbiology 150:831841.
30. Kay, E.,, B. Humair,, V. Denervaud,, K. Riedel,, S. Spahr,, L. Eberl,, C. Valverde, and, D. Haas. 2006. Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. J. Bacteriol. 188:60266033.
31. Kiratisin, P.,, K. D. Tucker, and, L. Passador. 2002. LasR, a transcriptional activator of Pseudomonas aeruginosa virulence genes, functions as a multimer. J. Bacteriol. 184:49124919.
32. Konstantinidis, K. T., and, J. M. Tiedje. 2004. Trends between gene content and genome size in prokaryotic species with larger genomes. Proc. Natl. Acad. Sci. USA 101:31603165.
33. Kuroda, M.,, T. Ohta,, I. Uchiyama,, T. Baba,, H. Yuzawa,, I. Kobayashi,, L. Cui,, A. Oguchi,, K. Aoki,, Y. Nagai,, J. Lian,, T. Ito,, M. Kanamori,, H. Matsumaru,, A. Maruyama,, H. Murakami,, A. Hosoyama,, Y. Mizutani-Ui,, N. K. Takahashi,, T. Sawano,, R. Inoue,, C. Kaito,, K. Sekimizu,, H. Hirakawa,, S. Kuhara,, S. Goto,, J. Yabuzaki,, M. Kanehisa,, A. Yamashita,, K. Oshima,, K. Furuya,, C. Yoshino,, T. Shiba,, M. Hattori,, N. Ogasawara,, H. Hayashi, and, K. Hiramatsu. 2001. Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet 357:12251240.
34. Latifi, A.,, M. Foglino,, K. Tanaka,, P. Williams, and, A. Lazdunski. 1996. 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. 21:11371146.
35. Ledgham, F.,, I. Ventre,, C. Soscia,, M. Foglino,, J. N. Sturgis, and, A. Lazdunski. 2003. Interactions of the quorum sensing regulator QscR: interaction with itself and the other regulators of Pseudomonas aeruginosa LasR and RhlR. Mol. Microbiol. 48:199210.
36. Lee, J. H.,, Y. Lequette, and, E. P. Greenberg. 2006. Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum-sensing transcription factor. Mol. Microbiol. 59:602609.
37. Lenz, D. H.,, K. C. Mok,, B. N. Lilley,, R. V. Kulkarni,, N. S. Wingreen, and, B. L. Bassler. 2004. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118:6982.
38. Lequette, Y.,, J. H. Lee,, F. Ledgham,, A. Lazdunski, and, E. P. Greenberg. 2006. A distinct QscR regulon in the Pseudomonas aeruginosa quorum-sensing circuit. J. Bacteriol. 188:33653370.
39. Lerat, E., and, N. A. Moran. 2004. The evolutionary history of quorum-sensing systems in bacteria. Mol. Biol. Evol. 21:903913.
40. Lindsay, J. A., and, M. T. Holden. 2004. Staphylococcus aureus: superbug, super genome? Trends Microbiol. 12:378385.
41. Lyczak, J. B.,, C. L. Cannon, and, G. B. Pier. 2000. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect. 2:10511060.
42. Marrs, C. F.,, G. P. Krasan,, K. W. McCrea,, D. L. Clemans, and, J. R. Gilsdorf. 2001. Haemophilus influenzae; human specific bacteria. Front. Biosci. 6:E41E60.
43. Mashburn, L. M., and, M. Whiteley. 2005. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437:422425.
44. Matsukawa, M., and, E. P. Greenberg. 2004. Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development. J. Bacteriol. 186:44494456.
45. Munch, R.,, K. Hiller,, H. Barg,, D. Heldt,, S. Linz,, E. Wingender, and, D. Jahn. 2003. PRO-DORIC: prokaryotic database of gene regulation. Nucleic Acids Res. 31:266269.
46. Nouwens, A. S.,, S. A. Beatson,, C. B. Whitchurch,, B. J. Walsh,, H. P. Schweizer,, J. S. Mattick, and, S. J. Cordwell. 2003. Proteome analysis of extracellular proteins regulated by the las and rhl quorum sensing systems in Pseudomonas aeruginosa PAO1. Microbiology 149:13111322.
47. Ochsner, U. A.,, A. K. Koch,, A. Fiechter, and, J. Reiser. 1994. Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. J. Bacteriol. 176:20442054.
48. Ochsner, U. A., and, J. Reiser. 1995. Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 92:64246428.
49. Passador, L.,, J. M. Cook,, M. J. Gambello,, L. Rust, and, B. H. Iglewski. 1993. Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260:11271130.
50. Pearson, J. P.,, M. Feldman,, B. H. Iglewski, and, A. Prince. 2000. Pseudomonas aeruginosa cell-to-cell signaling is required for virulence in a model of acute pulmonary infection. Infect. Immun. 68:43314334.
51. Pearson, J. P.,, K. M. Gray,, L. Passador,, K. D. Tucker,, A. Eberhard,, B. H. Iglewski, and, E. P. Greenberg. 1994. Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc. Natl. Acad. Sci. USA 91:197201.
52. Pearson, J. P.,, L. Passador,, B. H. Iglewski, and, E. P. Greenberg. 1995. A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 92:14901494.
53. Pesci, E. C.,, J. B. Milbank,, J. P. Pearson,, S. McKnight,, A. S. Kende,, E. P. Greenberg, and, B. H. Iglewski. 1999. Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 96:1122911234.
54. Pesci, E. C.,, J. P. Pearson,, P. C. Seed, and, B. H. Iglewski. 1997. Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 179:31273132.
55. Pessi, G., and, D. Haas. 2000. Transcriptional control of the hydrogen cyanide biosynthetic genes hcnABC by the anaerobic regulator ANR and the quorum-sensing regulators LasR and RhlR in Pseudomonas aeruginosa. J. Bacteriol. 182:69406949.
56. Pessi, G.,, F. Williams,, Z. Hindle,, K. Heurlier,, M. T. Holden,, M. Camara,, D. Haas, and, P. Williams. 2001. The global posttranscriptional regulator RsmA modulates production of virulence determinants and N-acylhomoserine lactones in Pseudomonas aeruginosa. J. Bacteriol. 183:66766683.
57. Rampioni, G.,, I. Bertani,, E. Zennaro,, F. Polticelli,, V. Venturi, and, L. Leoni. 2006. The quorum-sensing negative regulator RsaL of Pseudomonas aeruginosa binds to the lasI promoter. J. Bacteriol. 188:815819.
58. Reidl, J., and, K. E. Klose. 2002. Vibrio cholerae and cholera: out of the water and into the host. FEMS Microbiol. Rev. 26:125139.
59. Reimmann, C.,, M. Beyeler,, A. Latifi,, H. Winteler,, M. Foglino,, A. Lazdunski, and, D. Haas. 1997. The global activator GacA of Pseudomonas aeruginosa PAO positively controls the production of the autoinducer N-butyrylhomoserine lactone and the formation of the virulence factors pyocyanin, cyanide, and lipase. Mol. Microbiol. 24:309319.
60. Rosengarten, R.,, C. Citti,, M. Glew,, A. Lischewski,, M. Droesse,, P. Much,, F. Winner,, M. Brank, and, J. Spergser. 2000. Host-pathogen interactions in mycoplasma pathogenesis: virulence and survival strategies of minimalist prokaryotes. Int. J. Med. Microbiol. 290:1525.
61. Roy-Burman, A.,, R. H. Savel,, S. Racine,, B. L. Swanson,, N. S. Revadigar,, J. Fujimoto,, T. Sawa,, D. W. Frank, and, J. P. Wiener Kronish. 2001. Type III protein secretion is associated with death in lower respiratory and systemic Pseudomonas aeruginosa infections. J. Infect. Dis. 183:17671774.
62. Rumbaugh, K. P.,, J. A. Griswold, and, A. N. Hamood. 2000. The role of quorum sensing in the in vivo virulence of Pseudomonas aeruginosa. Microbes Infect. 2:17211731.
63. Rumbaugh, K. P.,, J. A. Griswold,, B. H. Iglewski, and, A. N. Hamood. 1999. Contribution of quorum sensing to the virulence of Pseudomonas aeruginosa in burn wound infections. Infect. Immun. 67:58545862.
64. Rust, L.,, E. C. Pesci, and, B. H. Iglewski. 1996. Analysis of the Pseudomonas aeruginosa elastase (lasB) regulatory region. J. Bacteriol. 178:11341140.
65. Schuster, M., and, E. P. Greenberg. 2006. A network of networks: quorum sensing gene regulation in Pseudomonas aeruginosa. Int. J. Med. Microbiol. 296:7381.
66. Schuster, M.,, A. C. Hawkins,, C. S. Harwood, and, E. P. Greenberg. 2004. The Pseudomonas aeruginosa RpoS regulon and its relationship to quorum sensing. Mol. Microbiol. 51:973985.
67. Schuster, M.,, C. P. Lohstroh,, T. Ogi, and, E. P. Greenberg. 2003. Identification, timing and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J. Bacteriol. 185:20662079.
68. Schuster, M.,, M. L. Urbanowski, and, E. P. Greenberg. 2004. Promoter specificity in Pseudomonas aeruginosa quorum sensing revealed by DNA binding of purified LasR. Proc. Natl. Acad. Sci. USA 101:1583315839.
69. Seed, P. C.,, L. Passador, and, B. H. Iglewski. 1995. Activation of the Pseudomonas aeruginosa lasI gene by LasR and the Pseudomonas autoinducer PAI: an autoinduction regulatory hierarchy. J. Bacteriol. 177:654659.
70. Shen-Orr, S. S.,, R. Milo,, S. Mangan, and, U. Alon. 2002. Network motifs in the transcriptional regulation network of Escherichia coli. Nat. Genet. 31:6468.
71. Singh, P. K.,, A. L. Schaefer,, M. R. Parsek,, T. O. Moninger,, M. J. Welsh, and, E. P. Greenberg. 2000. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407:762764.
72. Smith, E. E.,, D. G. Buckley,, Z. Wu,, C. Saenphimmachak,, L. R. Hoffman,, D. A. D’Argenio,, S. I. Miller,, B. W. Ramsey,, D. P. Speert,, S. M. Moskowitz,, J. L. Burns,, R. Kaul, and, M. V. Olson. 2006. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc. Natl. Acad. Sci. USA 103:84878492.
73. Stephens, R. S.,, S. Kalman,, C. Lammel,, J. Fan,, R. Marathe,, L. Aravind,, W. Mitchell,, L. Olinger,, R. L. Tatusov,, Q. Zhao,, E. V. Koonin, and, R. W. Davis. 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282:754759.
74. Stover, C. K.,, X. Q. Pham,, A. L. Erwin,, S. D. Mizoguchi,, P. Warrener,, M. J. Hickey,, F. S. Brinkman,, W. O. Hufnagle,, D. J. Kowalik,, M. Lagrou,, R. L. Garber,, L. Goltry,, E. Tolentino,, S. Westbrock-Wadman,, Y. Yuan,, L. L. Brody,, S. N. Coulter,, K. R. Folger,, A. Kas,, K. Larbig,, R. Lim,, K. Smith,, D. Spencer,, G. K. Wong,, Z. Wu, and, I. T. Paulsen. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:947948.
75. Ulrich, L. E.,, E. V. Koonin, and, I. B. Zhulin. 2005. One-component systems dominate signal transduction in prokaryotes. Trends Microbiol. 13:5256.
76. van Delden, C.,, R. Comte, and, A. M. Bally. 2001. Stringent response activates quorum sensing and modulates cell density-dependent gene expression in Pseudomonas aeruginosa. J. Bacteriol. 183:53765384.
77. Vannini, A.,, C. Volpari,, C. Gargioli,, E. Muraglia,, R. Cortese,, R. De Francesco,, P. Neddermann, and, S. D. Marco. 2002. The crystal structure of the quorum sensing protein TraR bound to its autoinducer and target DNA. EMBO J. 21:43934401.
78. Ventre, I.,, A. L. Goodman,, I. Vallet-Gely,, P. Vasseur,, C. Soscia,, S. Molin,, S. Bleves,, A. Lazdunski,, S. Lory, and, A. Filloux. 2006. Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc. Natl. Acad. Sci. USA 103:171176.
79. Ventre, I.,, F. Ledgham,, V. Prima,, A. Lazdunski,, M. Foglino, and, J. N. Sturgis. 2003. Dimerization of the quorum sensing regulator RhlR: development of a method using EGFP fluorescence anisotropy. Mol. Microbiol. 48:187198.
80. Viretta, A. U., and, M. Fussenegger. 2004. Modeling the quorum sensing regulatory network of human-pathogenic Pseudomonas aeruginosa. Biotechnol. Prog. 20:670678.
81. Wagner, V. E.,, D. Bushnell,, L. Passador,, A. I. Brooks, and, B. H. Iglewski. 2003. Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J. Bacteriol. 185:20802095.
82. Ward, J. P.,, J. R. King,, A. J. Koerber,, J. M. Croft,, R. E. Sockett, and, P. Williams. 2004. Cell-signalling repression in bacterial quorum sensing. Math. Med. Biol. 21:169204.
83. Whiteley, M., and, E. P. Greenberg. 2001. Promoter specificity elements in Pseudomonas aeruginosa quorum-sensing-controlled genes. J. Bacteriol. 183:55295534.
84. Whiteley, M.,, K. M. Lee, and, E. P. Greenberg. 1999. Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 96:1390413909.
85. Whiteley, M.,, M. R. Parsek, and, E. P. Greenberg. 2000. Regulation of quorum sensing by RpoS in Pseudomonas aeruginosa. J. Bacteriol. 182:43564360.
86. Winzer, K.,, C. Falconer,, N. C. Garber,, S. P. Diggle,, M. Camara, and, P. Williams. 2000. The Pseudomonas aeruginosa lectins PA-IL and PA-IIL are controlled by quorum sensing and by RpoS. J. Bacteriol. 182:64016411.
87. Wolfgang, M. C.,, V. T. Lee,, M. E. Gilmore, and, S. Lory. 2003. Coordinate regulation of bacterial virulence genes by a novel adenylate cyclase-dependent signaling pathway. Dev. Cell 4:253263.

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