Chapter 14 : Quorum Sensing in the Gastrointestinal Tract

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This chapter reviews the published literature concerning quorum sensing (QS) among bacteria of the gastrointestinal (GI) tract, with particular emphasis on pathogenic species that cause infection in the GI tract. Three major QS circuits have been described: one used primarily by gram-negative bacteria, one used primarily by gram-positive bacteria, and one that is universal. The gram-negative bacterial QS system involves the use of acyl homoserine lactones (AHLs) as autoinducers, which then bind to response regulators that affect gene expression. The first evidence that QS could be involved in the regulation of virulence factors of GI pathogens was found with enteropathogenic (EPEC), which causes nonbloody diarrhea primarily in infants in developing countries, and enterohemorrhagic (EHEC), which causes bloody diarrhea and hemolytic-uremic syndrome. The major virulence factors for are cholera toxin (CT) and the toxin-coregulated pilus (TCP), both of which are regulated as part of the ToxR regulon. The discovery of QS in human pathogens has led to considerable interest in developing new therapeutic interventions to interfere with the signaling molecules. There are at least three major strategies for the development of drugs that interrupt bacterial QS: (i) inhibition of QS signal synthesis, (ii) destruction or degradation of the signal, and (iii) inhibition of signal reception. A fundamental property of QS is that the greater the density of bacteria, the greater the density of signaling molecules and the greater the opportunity for cell-to-cell communication.

Citation: Kaper J, Prichett C, Michalski J. 2005. Quorum Sensing in the Gastrointestinal Tract, p 187-198. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch14

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1. Ahmer, B. M. 2004. Cell-to-cell signalling in Escherichia coli and Salmonella enterica. Mol. Microbiol. 52:933945.
2. Ahmer, B. M.,, J. van Reeuwijk,, C. D. Timmers,, P. J. Valentine,, and F. Heffron. 1998. Salmonella typhimurium encodes an SdiA homolog, a putative quorum sensor of the LuxR family, that regulates genes on the virulence plasmid. J. Bacteriol. 180:11851193.
3. Atkinson, S.,, J. P. Throup,, G. S. Stewart,, and P. Williams. 1999. A hierarchical quorum-sensing system in Yersinia pseudotuberculosis is involved in the regulation of motility and clumping. Mol. Microbiol. 33:12671277.
4. Bassler, B. L. 2002. Small talk. Cell-to-cell communication in bacteria. Cell 109:421424.
5. Berg, R. D. 1996. The indigenous gastrointestinal microflora. Trends Microbiol. 4:430435.
6. Borriello, S. P., 2002. The normal flora of the gastrointestinal tract, p. 124. In A. L. Hart,, A. J. Stagg,, H. Graffner,, H. Glise,, P. G. Falk,, and M. A. Kamm (ed.), Gut Ecology. Martin Dunitz, Ltd., London, United Kingdom.
7. Camara, M.,, P. Williams,, and A. Hardman. 2002. Controlling infection by tuning in and turning down the volume of bacterial small-talk. Lancet Infect. Dis. 2:667676.
8. Chen, X.,, S. Schauder,, N. Potier,, A. Van Dorsselaer,, I. Pelczer,, B. L. Bassler,, and F. M. Hughson. 2002. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415:545549.
9. Chun, C. K.,, E. A. Ozer,, M. J. Welsh,, J. Zabner,, and E. P. Greenberg. 2004. Inactivation of a Pseudomonas aeruginosa quorum-sensing signal by human airway epithelia. Proc. Natl. Acad. Sci. USA 101:35873590.
10. Coburn, P. S.,, and M. S. Gilmore. 2003. The Enterococcus faecalis cytolysin: a novel toxin active against eukaryotic and prokaryotic cells. Cell. Microbiol. 5:661669.
11. Day, A. M.,, J. H. Cove,, and M. K. Phillips-Jones. 2003. Cytolysin gene expression in Enterococcus faecalis is regulated in response to aerobiosis conditions. Mol. Genet. Genomics 269:3139.
12. Day, W. A., Jr.,, and A. T. Maurelli. 2001. Shigella flexneri LuxS quorum-sensing system modulates virB expression but is not essential for virulence. Infect. Immun. 69:1523.
13. De Kievit, T. R.,, R. Gillis,, S. Marx,, C. Brown,, and B. H. Iglewski. 2001. Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl. Environ. Microbiol. 67:18651873.
14. Dong, Y. H.,, J. L. Xu,, X. Z. Li,, and L. H. Zhang. 2000. AiiA, an enzyme that inactivates the acylhomoserine lactone quorum- sensing signal and attenuates the virulence of Erwinia carotovora. Proc. Natl. Acad. Sci. USA 97:35263531.
15. Duan, K.,, C. Dammel,, J. Stein,, H. Rabin,, and M. G. Surette. 2003. Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol. Microbiol. 50:14771491.
16.. Elvers, K. T.,, and S. F. Park. 2002. Quorum sensing in Campylobacter jejuni: detection of a luxS encoded signalling molecule. Microbiology 148:14751481.
17. Erickson, D. L.,, V. L. Nsereko,, D. P. Morgavi,, L. B. Selinger,, L. M. Rode,, and K. A. Beauchemin. 2002. Evidence of quorum sensing in the rumen ecosystem: detection of N-acyl homoserine lactone autoinducers in ruminal contents. Can. J. Microbiol. 48:374378.
18. Falcao, J. P.,, F. Sharp,, and V. Sperandio. 2004. Cell-to-cell signaling in intestinal pathogens. Curr. Issues Intest. Microbiol. 5:917.
19. Fuqua, C.,, and E. P. Greenberg. 2002. Listening in on bacteria: acyl-homoserine lactone signalling. Nat. Rev. Mol. Cell Biol. 3:685695.
20. Fuqua, C.,, M. R. Parsek,, and E. P. Greenberg. 2001. Regulation of gene expression by cell-to-cell communication: acylhomoserine lactone quorum sensing. Annu. Rev. Genet. 35:439468.
21. Haas, W.,, B. D. Shepard,, and M. S. Gilmore. 2002. Twocomponent regulator of Enterococcus faecalis cytolysin responds to quorum-sensing autoinduction. Nature 415:8487.
22. Hammer, B. K.,, and B. L. Bassler. 2003. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol. Microbiol. 50:101104.
23. Henke, J. M.,, and B. L. Bassler. 2004. Quorum sensing regulates type III secretion in Vibrio harveyi and Vibrio parahaemolyticus. J. Bacteriol. 186:37943805.
24. Hentzer, M.,, and M. Givskov. 2003. Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J. Clin. Investig. 112:13001307.
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.EMBOJ. 22:38033815.
26. Jeon, B.,, K. Itoh,, N. Misawa,, and S. Ryu. 2003. Effects of quorum sensing on flaA transcription and autoagglutination in Campylobacter jejuni. Microbiol. Immunol. 47:833839.
27. Kanamaru, K.,, I. Tatsuno,, T. Tobe,, and C. Sasakawa. 2000. SdiA, an Escherichia coli homologue of quorum-sensing regulators, controls the expression of virulence factors in enterohaemorrhagic Escherichia coli O157:H7. Mol. Microbiol. 38:805816.
28. Kaper, J. B.,, and A. D. O’Brien (ed.). 1998. Escherichia coli and Other Shiga-Toxin Producing E. coli Strains. ASM Press, Washington, D.C.
29. Kim, S. Y.,, S. E. Lee,, Y. R. Kim,, C. M. Kim,, P. Y. Ryu,, H. E. Choy,, S. S. Chung,, and J. H. Rhee. 2003. Regulation of Vibrio vulnificus virulence by the LuxS quorum-sensing system. Mol. Microbiol. 48:16471664.
30. Kovacikova, G.,, and K. Skorupski. 2002. Regulation of virulence gene expression in Vibrio cholerae by quorum sensing: HapR functions at the aphA promoter. Mol. Microbiol. 46:11351147.
31. Macfarlane, G. T.,, and S. Macfarlane. 1997. Human colonic microbiota: ecology, physiology and metabolic potential of intestinal bacteria. Scand. J. Gastroenterol. Suppl. 222:39.
32. Manefield, M.,, M. Welch,, M. Givskov,, G. P. Salmond,, and S. Kjelleberg. 2001. Halogenated furanones from the red alga, Delisea pulchra, inhibit carbapenem antibiotic synthesis and exoenzyme virulence factor production in the phytopathogen Erwinia carotovora. FEMS Microbiol. Lett. 205:131138.
33. Manna, A. C.,, and A. L. Cheung. 2003. sarU, a sarA homolog, is repressed by SarT and regulates virulence genes in Staphylococcus aureus. Infect. Immun. 71:343353.
34. Mayville, P.,, G. Ji,, R. Beavis,, H. Yang,, M. Goger,, R. P. Novick,, and T. W. Muir. 1999. Structure-activity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence. Proc. Natl. Acad. Sci. USA 96:12181223.
35. McCracken, V. J.,, and R. G. Lorenz. 2001. The gastrointestinal ecosystem: a precarious alliance among epithelium, immunity and microbiota. Cell. Microbiol. 3:111.
36. McDaniel, T. K.,, K. G. Jarvis,, M. S. Donnenberg,, and J. B. Kaper. 1995. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc. Natl. Acad. Sci. USA 92:16641668.
37. Michael, B.,, J. N. Smith,, S. Swift,, F. Heffron,, and B. M. Ahmer. 2001. SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. J. Bacteriol. 183:57335742.
38. Miller, M. B.,, K. Skorupski,, D. H. Lenz,, R. K. Taylor,, and B. L. Bassler. 2002. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110:303314.
39. Mitsumori, M.,, L. Xu,, H. Kajikawa,, M. Kurihara,, K. Tajima,, J. Hai,, and A. Takenaka. 2003. Possible quorum sensing in the rumen microbial community: detection of quorum-sensing signal molecules from rumen bacteria. FEMS Microbiol. Lett. 219:4752.
40. Novick, R. P. 2003. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol. Microbiol. 48:14291449.
41. Ohtani, K.,, H. Hayashi,, and T. Shimizu. 2002. The luxS gene is involved in cell-cell signalling for toxin production in Clostridium perfringens. Mol. Microbiol. 44:171179.
42. Ozaki, E.,, H. Kato,, H. Kita,, T. Karasawa,, T. Maegawa,, Y. Koino,, K. Matsumoto,, T. Takada,, K. Nomoto,, R. Tanaka,, and S. Nakamura. 2004. Clostridium difficile colonization in healthy adults: transient colonization and correlation with enterococcal colonization. J. Med. Microbiol. 53:167172.
43. Parsek, M. R.,, and E. P. Greenberg. 2000. Acyl-homoserine lactone quorum sensing in gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proc. Natl. Acad. Sci. USA 97:87898793.
44. Parsek, M. R.,, D. L. Val,, B. L. Hanzelka,, J. E. Cronan, Jr.,, and E. P. Greenberg. 1999. Acyl homoserine-lactone quorumsensing signal generation. Proc. Natl. Acad. Sci. USA 96:43604365.
45. Qin, X.,, K. V. Singh,, G. M. Weinstock,, and B. E. Murray. 2000. Effects of Enterococcus faecalis fsr genes on production of gelatinase and a serine protease and virulence. Infect. Immun. 68:25792586.
46. Ruiz-Perez, F.,, J. Sheikh,, S. Davis,, E. C. Boedeker,, and J. P. Nataro. 2004. Use of a continuous-flow anaerobic culture to characterize enteric virulence gene expression. Infect. Immun. 72:37933802.
47. Saleh, A.,, C. Figarella,, W. Kammouni,, S. Marchand-Pinatel,, A. Lazdunski,, A. Tubul,, P. Brun,, and M. D. Merten. 1999. Pseudomonas aeruginosa quorum-sensing signal molecule N- (3-oxododecanoyl)-L-homoserine lactone inhibits expression of P2Y receptors in cystic fibrosis tracheal gland cells. Infect. Immun. 67:50765082.
48. Schauder, S.,, and B. L. Bassler. 2001. The languages of bacteria. Genes Dev. 15:14681480.
49. Schauder, S.,, K. Shokat,, M. G. Surette,, and B. L. Bassler. 2001. The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol. Microbiol. 41:463476.
50. Shao, C. P.,, and L. I. Hor. 2001. Regulation of metalloprotease gene expression in Vibrio vulnificus by a Vibrio harveyi LuxR homologue. J. Bacteriol. 183:13691375.
51. Sifri, C. D.,, E. Mylonakis,, K. V. Singh,, X. Qin,, D. A. Garsin,, B. E. Murray,, F. M. Ausubel,, and S. B. Calderwood. 2002. Virulence effect of Enterococcus faecalis protease genes and the quorum-sensing locus fsr in Caenorhabditis elegans and mice. Infect. Immun. 70:56475650.
52. Singh, K. V.,, X. Qin,, G. M. Weinstock,, and B. E. Murray. 1998. Generation and testing of mutants of Enterococcus faecalis in a mouse peritonitis model. J. Infect. Dis. 178:14161420.
53. 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.
54. Smith, R. S.,, E. R. Fedyk,, T. A. Springer,, N. Mukaida,, B. H. Iglewski,, and R. P. Phipps. 2001. IL-8 production in human lung fibroblasts and epithelial cells activated by the Pseudomonas autoinducer N-3-oxododecanoyl homoserine lactone is transcriptionally regulated by NF-kappa B and activator protein-2. J. Immunol. 167:366374.
55. Smith, R. S.,, S. G. Harris,, R. Phipps,, and B. Iglewski. 2002. The Pseudomonas aeruginosa quorum-sensing molecule N-(3- oxododecanoyl)homoserine lactone contributes to virulence and induces inflammation in vivo. J. Bacteriol. 184:11321139.
56. Smith, R. S.,, and B. H. Iglewski. 2003. Pseudomonas aeruginosa quorum sensing as a potential antimicrobial target. J. Clin. Investig. 112:14601465.
57. Sperandio, V.,, C. C. Li,, and J. B. Kaper. 2002. Quorumsensing Escherichia coli regulator A: a regulator of the LysR family involved in the regulation of the locus of enterocyte effacement pathogenicity island in enterohemorrhagic E. coli. Infect. Immun. 70:30853093.
58. Sperandio, V.,, J. L. Mellies,, W. Nguyen,, S. Shin,, and J. B. Kaper. 1999. Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA 96:1519615201.
59. Sperandio, V.,, A. G. Torres,, J. A. Giron,, and J. B. Kaper. 2001. Quorum sensing is a global regulatory mechanism in enterohemorrhagic Escherichia coli O157:H7. J. Bacteriol. 183:51875197.
60. Sperandio, V.,, A. G. Torres,, B. Jarvis,, J. P. Nataro,, and J. B. Kaper. 2003. Bacteria-host communication: the language of hormones. Proc. Natl. Acad. Sci. USA 100:89518956.
61. Sperandio, V.,, A. G. Torres,, and J. B. Kaper. 2002. Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol. Microbiol. 43:809821.
62. Taga, M. E.,, and B. L. Bassler. 2003. Chemical communication among bacteria. Proc. Natl. Acad. Sci. USA 100 (Suppl. 2):1454914554.
63. Taga, M. E.,, S. T. Miller,, and B. L. Bassler. 2003. Lsr-mediated transport and processing of AI-2 in Salmonella typhimurium. Mol. Microbiol. 50:14111427.
64. Telford, G.,, D. Wheeler,, P. Williams,, P. T. Tomkins,, P. Appleby,, H. Sewell,, G. S. Stewart,, B. W. Bycroft,, and D. I. Pritchard. 1998. The Pseudomonas aeruginosa quorum-sensing signal molecule N-(3-oxododecanoyl)-L-homoserine lactone has immunomodulatory activity. Infect. Immun. 66:3642.
65. Throup, J. P.,, M. Camara,, G. S. Briggs,, M. K. Winson,, S. R. Chhabra,, B. W. Bycroft,, P. Williams,, and G. S. Stewart. 1995. Characterisation of the yenI/yenR locus from Yersinia enterocolitica mediating the synthesis of two N-acylhomoserine lactone signal molecules. Mol. Microbiol. 17:345356.
66. Venter, J. C.,, K. Remington,, J. F. Heidelberg,, A. L. Halpern,, D. Rusch,, J. A. Eisen,, D. Wu,, I. Paulsen,, K. E. Nelson,, W. Nelson,, D. E. Fouts,, S. Levy,, A. H. Knap,, M. W. Lomas,, K. Nealson,, O. White,, J. Peterson,, J. Hoffman,, R. Parsons,, H. Baden- Tillson,, C. Pfannkoch,, Y. H. Rogers,, and H. O. Smith. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:6674.
67. Visick, K. L.,, J. Foster,, J. Doino,, M. McFall-Ngai,, and E. G. Ruby. 2000. Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J. Bacteriol. 182:45784586
68. Wang, X. D.,, P. A. de Boer,, and L. I. Rothfield. 1991. A factor that positively regulates cell division by activating transcription of the major cluster of essential cell division genes of Escherichia coli. EMBO J. 10:33633372.
69. Williams, P. 2002. Quorum sensing: an emerging target for antibacterial chemotherapy? Expert Opin. Ther. Targets 6:257274.
70. Winzer, K.,, K. R. Hardie,, and P. Williams. 2002. Bacterial cellto- cell communication: sorry, can’t talk now—gone to lunch! Curr. Opin. Microbiol. 5:216222.
71. Xavier, K. B.,, and B. L. Bassler. 2003. LuxS quorum sensing: more than just a numbers game. Curr. Opin. Microbiol. 6:191197.
72. Xu, J.,, M. K. Bjursell,, J. Himrod,, S. Deng,, L. K. Carmichael,, H. C. Chiang,, L. V. Hooper,, and J. I. Gordon. 2003. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299:20742076.
73. Yarwood, J. M.,, and P. M. Schlievert. 2003. Quorum sensing in Staphylococcus infections. J. Clin. Investig. 112:16201625.
74. Zhu, J.,, and J. J. Mekalanos. 2003. Quorum sensingdependent biofilms enhance colonization in Vibrio cholerae. Dev. Cell 5:647656.
75. Zhu, J.,, M. B. Miller,, R. E. Vance,, M. Dziejman,, B. L. Bassler,, and J. J. Mekalanos. 2002. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 99:31293134.

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