Chapter 27 : Regulation in Response to Host-Derived Signaling Molecules

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Regulation in Response to Host-Derived Signaling Molecules, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818524/9781555816766_Chap27-1.gif /docserver/preview/fulltext/10.1128/9781555818524/9781555816766_Chap27-2.gif


To survive in their environment, bacteria must sense the conditions in which they live and adapt accordingly. The best way to acquire this information is to sense various molecules produced by the host. This interaction, along with the host sensing bacterium-derived molecules, has been termed interkingdom signaling. Hormones, the principal signaling molecules in multicellular organisms, are present in every environment where bacteria interact with the host. Catecholamines are a family of three neuroendocrine hormones that are produced from the amino acid tyrosine. Opioids are neurotransmitters that play multiple roles in host responses such as stress, tissue damage, and regulation of the immune system. Natriuretic peptides are a class of peptide hormones involved in the osmoregulation of blood. The major signaling molecules used by the immune system are cytokines, which makes them a prime target for being eavesdropped on by bacteria. The immune system produces many other molecules aside from cytokines. Among these are cationic antimicrobial peptides (CAMPs). These peptides have a wide array of diversity but share a positive charge and amphipathic regions that allow them to interact with and disrupt the negatively charged bacterial membrane. Gram-positive bacteria also must face the wide array of antimicrobial peptides produced by the host. The ability to sense and respond to host signals has been identified in most major pathogens. The prevalence of this ability suggests that interkingdom signaling may be extremely common and that many more systems will be uncovered in the future.

Citation: Gruber C, Sperandio V. 2013. Regulation in Response to Host-Derived Signaling Molecules, p 545-565. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch27
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Model of interkingdom regulation in EHEC. QseC senses AI-3/epinephrine and NE to increase its autophosphorylation. It then transfers this phosphate to three response regulators: QseB (controls flagellar expression), KdpE (controls LEE gene expression), and QseF (controls pedestal formation). QseBC activate the expression of , where QseE senses Epi, sulfate, and phosphate and transfers its phosphate to QseF. doi:10.1128/9781555818524.ch27f1

Citation: Gruber C, Sperandio V. 2013. Regulation in Response to Host-Derived Signaling Molecules, p 545-565. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch27
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Model of interkingdom signaling in . NE influences the expression of GacA, which in turn influences the expression of , encoding the receptor for the 3-oxo-C12-AHL quorum-sensing signal. LasR controls the expression of that encodes the synthase of the 3-oxo-C12-AHL, forming a positive auto-regulatory loop. LasR also activates expression of the RlhRI quorum-sensing system, which represses expression of the PQS signal. Expression of PQS is positively activated by the presence of PMNs, and through MvfR by dynorphin. IFN-γ through OprF activates the expression of . doi:10.1128/9781555818524.ch27f2

Citation: Gruber C, Sperandio V. 2013. Regulation in Response to Host-Derived Signaling Molecules, p 545-565. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch27
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Model of activation of the serovar Typhimurium PhoQ sensor by CAMPs. doi:10.1128/9781555818524.ch27f3

Citation: Gruber C, Sperandio V. 2013. Regulation in Response to Host-Derived Signaling Molecules, p 545-565. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch27
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

Activation of VirA through interaction with the periplasmic protein ChvE bound to plant-derived monosaccharides. doi:10.1128/9781555818524.ch27f4

Citation: Gruber C, Sperandio V. 2013. Regulation in Response to Host-Derived Signaling Molecules, p 545-565. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch27
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Abachin, E.,, C. Poyart,, E. Pellegrini,, E. Milohanic,, F. Fiedler,, P. Berche,, and P. Trieu-Cuot. 2002. Formation of D-alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes. Mol. Microbiol. 43:114.
2. Abram, M.,, D. Vuckovic,, B. Wraber,, and M. Doric. 2000. Plasma cytokine response in mice with bacterial infection. Mediators Inflamm. 9:229234.
3. Alhede, M.,, T. Bjarnsholt,, P. O. Jensen,, R. K. Phipps,, C. Moser,, L. Christophersen,, L. D. Christensen,, M. van Gennip,, M. Parsek,, N. Hoiby,, T. B. Rasmussen,, and M. Givskov. 2009. Pseudomonas aeruginosa recognizes and responds aggressively to the presence of polymorphonuclear leukocytes. Microbiology 155:35003508.
4. Alpuche Aranda, C. M.,, J. A. Swanson,, W. P. Loomis,, and S. I. Miller. 1992. Salmonella typhimurium activates virulence gene transcription within acidified macrophage phagosomes. Proc. Natl. Acad. Sci. USA 89:1007910083.
5. Alverdy, J.,, C. Holbrook,, F. Rocha,, L. Seiden,, R. L. Wu,, M. Musch,, E. Chang,, D. Ohman,, and S. Suh. 2000. Gut-derived sepsis occurs when the right pathogen with the right virulence genes meets the right host: evidence for in vivo virulence expression in Pseudomonas aeruginosa. Ann. Surg. 232:480489.
6. Anderson, M. T.,, and S. K. Armstrong. 2004. The BfeR regulator mediates enterobactin-inducible expression of Bordetella enterobactin utilization genes. J. Bacteriol. 186:73027311.
7. Anderson, M. T.,, and S. K. Armstrong. 2006. The Bordetella Bfe system: growth and transcriptional response to siderophores, catechols, and neuroendocrine catecholamines. J. Bacteriol. 188:57315740.
8. Anderson, M. T.,, and S. K. Armstrong. 2008. Norepinephrine mediates acquisition of transferrin-iron in Bordetella bronchiseptica. J. Bacteriol. 190:39403947.
9. Aneman, A.,, G. Eisenhofer,, L. Olbe,, J. Dalenback,, P. Nitescu,, L. Fandriks,, and P. Friberg. 1996. Sympathetic discharge to mesenteric organs and the liver. Evidence for substantial mesenteric organ norepinephrine spillover. J. Clin. Investig. 97:16401646.
10. Ankenbauer, R. G.,, and E. W. Nester. 1990. Sugar-mediated induction of Agrobacterium tumefaciens virulence genes: structural specificity and activities of monosaccharides. J. Bacteriol. 172:64426446.
11. Babalola, C. P.,, C. H. Nightingale,, and D. P. Nicolau. 2004. Effect of adjunctive treatment with gamma interferon against Pseudomonas aeruginosa pneumonia in neutropenic and non-neutropenic hosts. Int. J. Antimicrob. Agents 24:219225.
12. Bader, M. W.,, S. Sanowar,, M. E. Daley,, A. R. Schneider,, U. Cho,, W. Xu,, R. E. Klevit,, H. Le Moual,, and S. I. Miller. 2005. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122:461472.
13. Baron, S. S.,, and J. J. Rowe. 1981. Antibiotic action of pyocyanin. Antimicrob. Agents Chemother. 20:814820.
14. Beall, B.,, and G. N. Sanden. 1995. A Bordetella pertussis fepA homologue required for utilization of exogenous ferric enterobactin. Microbiology 141:31933205.
15. Bearson, B. L.,, and S. M. Bearson. 2008. The role of the QseC quorum-sensing sensor kinase in colonization and norepinephrine-enhanced motility of Salmonella enterica serovar Typhimurium. Microb. Pathog. 44:271278.
16. Bearson, B. L.,, S. M. Bearson,, I. S. Lee,, and B. W. Brunelle. 2010. The Salmonella enterica serovar Typhimurium QseB response regulator negatively regulates bacterial motility and swine colonization in the absence of the QseC sensor kinase. Microb. Pathog. 48:214219.
17. Bodmer, S.,, C. Imark,, and M. Kneubuhl. 1999. Biogenic amines in foods: histamine and food processing. Inflamm. Res. 48:296300.
18. Boontham, P.,, A. Robins,, P. Chandran,, D. Pritchard,, M. Camara,, P. Williams,, S. Chuthapisith,, A. McKechnie,, B. J. Rowlands,, and O. Eremin. 2008. Significant immunomodulatory effects of Pseudomonas aeruginosa quorum-sensing signal molecules: possible link in human sepsis. Clin. Sci. (London) 115:343351.
19. Bordet, J.,, and O. Gengou. 1906. Le microbe de la coqueluche. Ann. Inst. Pasteur (Paris) 20:731741.
20. Brook, I. 2002. Secondary bacterial infections complicating skin lesions. J. Med. Microbiol. 51:808812.
21. Brown, L. M. 2000. Helicobacter pylori: epidemiology and routes of transmission. Epidemiol. Rev. 22:283297.
22. Brubaker, R. R. 1991. Factors promoting acute and chronic diseases caused by yersiniae. Clin. Microbiol. Rev. 4:309324.
23. Burton, C. L.,, S. R. Chhabra,, S. Swift,, T. J. Baldwin,, H. Withers,, S. J. Hill,, and P. Williams. 2002. The growth response of Escherichia coli to neurotransmitters and related catecholamine drugs requires a functional enterobactin biosynthesis and uptake system. Infect. Immun. 70:59135923.
24. Bustamante, V. H.,, F. J. Santana,, E. Calva,, and J. L. Puente. 2001. Transcriptional regulation of type III secretion genes in enteropathogenic Escherichia coli: Ler antagonizes H-NS-dependent repression. Mol. Microbiol. 39:664678.
25. Butzler, J. P. 2004. Campylobacter, from obscurity to celebrity. Clin. Microbiol. Infect. 10:868876.
26. Campellone, K. G.,, D. Robbins,, and J. M. Leong. 2004. EspFU is a translocated EHEC effector that interacts with Tir and N-WASP and promotes Nck-independent actin assembly. Dev. Cell 7:217228.
27. Carlier, A.,, S. Uroz,, B. Smadja,, R. Fray,, X. Latour,, Y. Dessaux,, and D. Faure. 2003. The Ti plasmid of Agrobacterium tumefaciens harbors an attM-paralogous gene, aiiB, also encoding N-acyl homoserine lactonase activity. Appl. Environ. Microbiol. 69:49894993.
28. Casper-Lindley, C.,, and F. H. Yildiz. 2004. VpsT is a transcriptional regulator required for expression of vps biosynthesis genes and the development of rugose colonial morphology in Vibrio cholerae O1 El Tor. J. Bacteriol. 186:15741578.
29. Cheung, A. L.,, A. S. Bayer,, G. Zhang,, H. Gresham,, and Y. Q. Xiong. 2004. Regulation of virulence determinants in vitro and in vivo in Staphylococcus aureus. FEMS Immunol. Med. Microbiol. 40:19.
30. Chevrot, R.,, R. Rosen,, E. Haudecoeur,, A. Cirou,, B. J. Shelp,, E. Ron,, and D. Faure. 2006. GABA controls the level of quorum-sensing signal in Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. USA 103:74607464.
31. Chhabra, S. R.,, C. Harty,, D. S. Hooi,, M. Daykin,, P. Williams,, G. Telford,, D. I. Pritchard,, and B. W. Bycroft. 2003. Synthetic analogues of the bacterial signal (quorum sensing) molecule N-(3-oxododecanoyl)-L-homoserine lactone as immune modulators. J. Med. Chem. 46:97104.
32. Cho, U. S.,, M. W. Bader,, M. F. Amaya,, M. E. Daley,, R. E. Klevit,, S. I. Miller,, and W. Xu. 2006. Metal bridges between the PhoQ sensor domain and the membrane regulate transmembrane signaling. J. Mol. Biol. 356:11931206.
33. Chowers, M. Y.,, N. Keller,, S. Bar-Meir,, and Y. Chowers. 2002. A defined human gastrin sequence stimulates the growth of Helicobacter pylori. FEMS Microbiol. Lett. 217:231236.
34. Chowers, M. Y.,, N. Keller,, R. Tal,, I. Barshack,, R. Lang,, S. Bar-Meir,, and Y. Chowers. 1999. Human gastrin: a Helicobacter pylori-specific growth factor. Gastroenterology 117:11131118.
35. 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.
36. Clarke, M. B.,, D. T. Hughes,, C. Zhu,, E. C. Boedeker,, and V. Sperandio. 2006. The QseC sensor kinase: a bacterial adrenergic receptor. Proc. Natl. Acad. Sci. USA 103:1042010425.
37. Cogan, T. A.,, A. O. Thomas,, L. E. Rees,, A. H. Taylor,, M. A. Jepson,, P. H. Williams,, J. Ketley,, and T. J. Humphrey. 2007. Norepinephrine increases the pathogenic potential of Campylobacter jejuni. Gut 56:10601065.
38. Crane, J. K.,, R. A. Olson,, H. M. Jones,, and M. E. Duffey. 2002. Release of ATP during host cell killing by enteropathogenic E. coli and its role as a secretory mediator. Am. J. Physiol. Gastrointest. Liver Physiol. 283:G74G86.
39. Crane, J. K.,, and I. Shulgina. 2009. Feedback effects of host-derived adenosine on enteropathogenic Escherichia coli. FEMS Immunol. Med. Microbiol. 57:214228.
40. Cravioto, A.,, A. Tello,, A. Navarro,, J. Ruiz,, H. Villafan,, F. Uribe,, and C. Eslava. 1991. Association of Escherichia coli HEp-2 adherence patterns with type and duration of diarrhoea. Lancet 337:262264.
41. Currie, B. 1995. Pseudomonas pseudomallei-insulin interaction. Infect. Immun. 63:3745.
42. Dathe, M.,, and T. Wieprecht. 1999. Structural features of helical antimicrobial peptides: their potential to modulate activity on model membranes and biological cells. Biochim. Biophys. Acta 1462:7187.
43. de Kievit, T. R. 2009. Quorum sensing in Pseudomonas aeruginosa biofilms. Environ. Microbiol. 11:279288.
44. Denis, M.,, D. Campbell,, and E. O. Gregg. 1991. Interleukin-2 and granulocyte-macrophage colony-stimulating factor stimulate growth of a virulent strain of Escherichia coli. Infect. Immun. 59:18531856.
45. 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.
46. DiMango, E.,, H. J. Zar,, R. Bryan,, and A. Prince. 1995. Diverse Pseudomonas aeruginosa gene products stimulate respiratory epithelial cells to produce interleukin-8. J. Clin. Investig. 96:22042210.
47. Engel, J.,, and P. Balachandran. 2009. Role of Pseudomonas aeruginosa type III effectors in disease. Curr. Opin. Microbiol. 12:6166.
48. Fernandez, M.,, B. del Rio,, D. M. Linares,, M. C. Martin,, and M. A. Alvarez. 2006. Real-time polymerase chain reaction for quantitative detection of histamine-producing bacteria: use in cheese production. J. Dairy Sci. 89:37633769.
49. Fields, P. I.,, E. A. Groisman,, and F. Heffron. 1989. A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 243:10591062.
50. Freestone, P. P.,, R. D. Haigh,, and M. Lyte. 2007. Blockade of catecholamine-induced growth by adrenergic and dopaminergic receptor antagonists in Escherichia coli O157:H7, Salmonella enterica and Yersinia enterocolitica. BMC Microbiol. 7:8.
51. Freestone, P. P.,, R. D. Haigh,, P. H. Williams,, and M. Lyte. 1999. Stimulation of bacterial growth by heat-stable, norepinephrine-induced autoinducers. FEMS Microbiol. Lett. 172:5360.
52. Freestone, P. P.,, R. D. Haigh,, P. H. Williams,, and M. Lyte. 2003. Involvement of enterobactin in norepinephrine-mediated iron supply from transferrin to enterohaemorrhagic Escherichia coli. FEMS Microbiol. Lett. 222:3943.
53. Freestone, P. P.,, M. Lyte,, C. P. Neal,, A. F. Maggs,, R. D. Haigh,, and P. H. Williams. 2000. The mammalian neuroendocrine hormone norepinephrine supplies iron for bacterial growth in the presence of transferrin or lactoferrin. J. Bacteriol. 182:60916098.
54. Friedman, D. B.,, D. L. Stauff,, G. Pishchany,, C. W. Whitwell,, V. J. Torres,, and E. P. Skaar. 2006. Staphylococcus aureus redirects central metabolism to increase iron availability. PLoS Pathog. 2:e87.
55. Fuhlbrigge, R. C.,, S. M. Fine,, E. R. Unanue,, and D. D. Chaplin. 1988. Expression of membrane interleukin 1 by fibroblasts transfected with murine pro-interleukin 1 alpha cDNA. Proc. Natl. Acad. Sci. USA 85:56495653.
56. 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.
57. Garmendia, J.,, A. D. Phillips,, M. F. Carlier,, Y. Chong,, S. Schuller,, O. Marches,, S. Dahan,, E. Oswald,, R. K. Shaw,, S. Knutton,, and G. Frankel. 2004. TccP is an enterohaemorrhagic Escherichia coli O157:H7 type III effector protein that couples Tir to the actin-cytoskeleton. Cell. Microbiol. 6:11671183.
58. George, E. A.,, and T. W. Muir. 2007. Molecular mechanisms of agr quorum sensing in virulent staphylococci. Chembiochem 8:847855.
59. Goodnow, R. A. 1980. Biology of Bordetella bronchiseptica. Microbiol. Rev. 44:722738.
60. Gorke, B.,, and J. Vogel. 2008. Noncoding RNA control of the making and breaking of sugars. Genes Dev. 22:29142925.
61. Gottfert, M. 1993. Regulation and function of rhizobial nodulation genes. FEMS Microbiol. Rev. 10:3963.
62. Grant, C. C.,, M. E. Konkel,, W. Cieplak, Jr.,, and L. S. Tompkins. 1993. Role of flagella in adherence, internalization, and translocation of Campylobacter jejuni in nonpolarized and polarized epithelial cell cultures. Infect. Immun. 61:17641771.
63. Gregory, R. A.,, and H. J. Tracy. 1964. The constitution and properties of two gastrins extracted from hog antral mucosa. Gut 5:103114.
64. Guo, L.,, K. B. Lim,, J. S. Gunn,, B. Bainbridge,, R. P. Darveau,, M. Hackett,, and S. I. Miller. 1997. Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ. Science 276:250253.
65. Gupta, S.,, and R. Chowdhury. 1997. Bile affects production of virulence factors and motility of Vibrio cholerae. Infect. Immun. 65:11311134.
66. Hahn, P. Y.,, P. Wang,, S. M. Tait,, Z. F. Ba,, S. S. Reich,, and I. H. Chaudry. 1995. Sustained elevation in circulating catecholamine levels during polymicrobial sepsis. Shock 4:269273.
67. Harmsen, M.,, L. Yang,, S. J. Pamp,, and T. Tolker-Nielsen. 2010. An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunol. Med. Microbiol. 59:253268.
68. Hegde, M.,, T. K. Wood,, and A. Jayaraman. 2009. The neuroendocrine hormone norepinephrine increases Pseudomonas aeruginosa PA14 virulence through the las quorum-sensing pathway. Appl. Microbiol. Biotechnol. 84:763776.
69. Higuchi, T.,, H. Hayashi,, and K. Abe. 1997. Exchange of glutamate and gamma-aminobutyrate in a Lactobacillus strain. J. Bacteriol. 179:33623364.
70. Hofmann, A. F., 1998. Bile secretion and the enterohepatic circulation of bile acids, p. 937948. In M. Feldman,, B. F. Scharschmidt,, and M. H. Sleisenger (ed.), Gastrointestinal and Liver Disease. The W. B. Saunders Co., Philadelphia, PA.
71. Horke, S.,, I. Witte,, S. Altenhofer,, P. Wilgenbus,, M. Goldeck,, U. Forstermann,, J. Xiao,, G. L. Kramer,, D. C. Haines,, P. K. Chowdhary,, R. W. Haley,, and J. F. Teiber. 2010. Paraoxonase 2 is down-regulated by the Pseudomonas aeruginosa quorumsensing signal N-(3-oxododecanoyl)-L-homoserine lactone and attenuates oxidative stress induced by pyocyanin. Biochem. J. 426:7383.
72. Hsu, S. C.,, K. R. Johansson,, and M. J. Donahue. 1986. The bacterial flora of the intestine of Ascaris suum and 5-hydroxytryptamine production. J. Parasitol. 72:545549.
73. Huang, M. L.,, G. A. Cangelosi,, W. Halperin,, and E. W. Nester. 1990. A chromosomal Agrobacterium tumefaciens gene required for effective plant signal transduction. J. Bacteriol. 172:18141822.
74. Hughes, D. T.,, M. B. Clarke,, K. Yamamoto,, D. A. Rasko,, and V. Sperandio. 2009. The QseC adrenergic signaling cascade in Enterohemorrhagic E. coli (EHEC). PLoS Pathog. 5:e1000553.
75. Hung, D. T.,, and J. J. Mekalanos. 2005. Bile acids induce cholera toxin expression in Vibrio cholerae in a ToxT-independent manner. Proc. Natl. Acad. Sci. USA 102:30283033.
76. Hung, D. T.,, J. Zhu,, D. Sturtevant,, and J. J. Mekalanos. 2006. Bile acids stimulate biofilm formation in Vibrio cholerae. Mol. Microbiol. 59:193201.
77. Jarvis, K. G.,, J. A. Giron,, A. E. Jerse,, T. K. McDaniel,, M. S. Donnenberg,, and J. B. Kaper. 1995. Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc. Natl. Acad. Sci. USA 92:79968000.
78. Johansson, C.,, O. Wisen,, B. Kollberg,, K. Uvnas-Wallensten,, and S. Efendic. 1978. Effects of intragastrically administered somatostatin on basal and pentagastrin stimulated gastric acid secretion in man. Acta Physiol. Scand. 104:232234.
79. Joseph, I. M.,, and D. Kirschner. 2004. A model for the study of Helicobacter pylori interaction with human gastric acid secretion. J. Theor. Biol. 228:5580.
80. Kalra, P. R.,, J. R. Clague,, A. P. Bolger,, S. D. Anker,, P. A. Poole-Wilson,, A. D. Struthers,, and A. J. Coats. 2003. Myocardial production of C-type natriuretic peptide in chronic heart failure. Circulation 107:571573.
81. Kanai, K.,, E. Kondo,, and T. Kurata. 1996. Affinity and response of Burkholderia pseudomallei and Burkholderia cepacia to insulin. Southeast Asian J. Trop. Med. Public Health 27:584591.
82. Kaper, J. B.,, J. P. Nataro,, and H. L. Mobley. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2:123140.
83. Karlyshev, A. V.,, E. E. Galyov,, O. Smirnov,, A. P. Guzayev,, V. M. Abramov,, and V. P. Zav’yalov. 1992. A new gene of the f1 operon of Y. pestis involved in the capsule biogenesis. FEBS Lett. 297:7780.
84. Kenny, B.,, and B. B. Finlay. 1995. Protein secretion by enteropathogenic Escherichia coli is essential for transducing signals to epithelial cells. Proc. Natl. Acad. Sci. USA 92:79917995.
85. Khansari, D. N.,, A. J. Murgo,, and R. E. Faith. 1990. Effects of stress on the immune system. Immunol. Today 11:170175.
86. Khersonsky, O.,, and D. S. Tawfik. 2005. Structure-reactivity studies of serum paraoxonase PON1 suggest that its native activity is lactonase. Biochemistry 44:63716382.
87. Kostakioti, M.,, M. Hadjifrangiskou,, J. S. Pinkner,, and S. J. Hultgren. 2009. QseC-mediated dephosphorylation of QseB is required for expression of genes associated with virulence in uropathogenic Escherichia coli. Mol. Microbiol. 73:10201031.
88. Kourie, J. I. 1999. Synthetic mammalian C-type natriuretic peptide forms large cation channels. FEBS Lett. 445:5762.
89. Kovacs, M.,, A. Halfmann,, I. Fedtke,, M. Heintz,, A. Peschel,, W. Vollmer,, R. Hakenbeck,, and R. Bruckner. 2006. A functional dlt operon, encoding proteins required for incorporation of D-alanine in teichoic acids in gram-positive bacteria, confers resistance to cationic antimicrobial peptides in Streptococcus pneumoniae. J. Bacteriol. 188:57975805.
90. Krause, A.,, C. Liepke,, M. Meyer,, K. Adermann,, W. G. Forssmann,, and E. Maronde. 2001. Human natriuretic peptides exhibit antimicrobial activity. Eur. J. Med. Res. 6:215218.
91. Kuroda, M.,, K. Kuwahara-Arai,, and K. Hiramatsu. 2000. Identification of the up- and down-regulated genes in vancomycin-resistant Staphylococcus aureus strains Mu3 and Mu50 by cDNA differential hybridization method. Biochem. Biophys. Res. Commun. 269:485490.
92. 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.
93. Lau, G. W.,, D. J. Hassett,, H. Ran,, and F. Kong. 2004. The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol. Med. 10:599606.
94. Laughlin, R. S.,, M. W. Musch,, C. J. Hollbrook,, F. M. Rocha,, E. B. Chang,, and J. C. Alverdy. 2000. The key role of Pseudomonas aeruginosa PA-I lectin on experimental gut-derived sepsis. Ann. Surg. 232:133142.
95. Lee, A.,, J. L. O’Rourke,, P. J. Barrington,, and T. J. Trust. 1986. Mucus colonization as a determinant of pathogenicity in intestinal infection by Campylobacter jejuni: a mouse cecal model. Infect. Immun. 51:536546.
96. Lee, Y. W.,, S. Jin,, W. S. Sim,, and E. W. Nester. 1996. The sensing of plant signal molecules by Agrobacterium: genetic evidence for direct recognition of phenolic inducers by the VirA protein. Gene 179:8388.
97. Li, L.,, D. Hooi,, S. R. Chhabra,, D. Pritchard,, and P. E. Shaw. 2004. Bacterial N-acylhomoserine lactone-induced apoptosis in breast carcinoma cells correlated with down-modulation of STAT3. Oncogene 23:48944902.
98. Li, M.,, Y. Lai,, A. E. Villaruz,, D. J. Cha,, D. E. Sturdevant,, and M. Otto. 2007. Gram-positive three-component antimicrobial peptide-sensing system. Proc. Natl. Acad. Sci. USA 104:94699474.
99. Li, W.,, M. Lyte,, P. P. Freestone,, A. Ajmal,, J. A. Colmer-Hamood,, and A. N. Hamood. 2009. Norepinephrine represses the expression of toxA and the siderophore genes in Pseudomonas aeruginosa. FEMS Microbiol. Lett. 299:100109.
100. Lippa, A. M.,, and M. Goulian. 2009. Feedback inhibition in the PhoQ/PhoP signaling system by a membrane peptide. PLoS Genet. 5:e1000788.
101. Llama-Palacios, A.,, E. Lopez-Solanilla,, C. Poza-Carrion,, F. Garcia-Olmedo,, and P. Rodriguez-Palenzuela. 2003. The Erwinia chrysanthemi phoP-phoQ operon plays an important role in growth at low pH, virulence and bacterial survival in plant tissue. Mol. Microbiol. 49:347357.
102. Luo, G.,, D. W. Niesel,, R. A. Shaban,, E. A. Grimm,, and G. R. Klimpel. 1993. Tumor necrosis factor alpha binding to bacteria: evidence for a high-affinity receptor and alteration of bacterial virulence properties. Infect. Immun. 61:830835.
103. Lyte, M. 1992. The role of catecholamines in gram-negative sepsis. Med. Hypotheses 37:255258.
104. Lyte, M.,, and S. Ernst. 1992. Catecholamine induced growth of gram negative bacteria. Life Sci. 50:203212.
105. Lyte, M.,, C. D. Frank,, and B. T. Green. 1996. Production of an autoinducer of growth by norepinephrine cultured Escherichia coli O157:H7. FEMS Microbiol. Lett. 139:155159.
106. Lyte, M.,, S. G. Nelson,, and M. L. Thompson. 1990. Innate and adaptive immune responses in a social conflict paradigm. Clin. Immunol. Immunopathol. 57:137147.
107. Maciorkowska, E.,, A. Panasiuk,, K. Kondej-Muszynska,, M. Kaczmarski,, and A. Kemona. 2006. Mucosal gastrin cells and serum gastrin levels in children with Helicobacter pylori infection. Adv. Med. Sci. 51:137141.
108. Martin-Orozco, N.,, N. Touret,, M. L. Zaharik,, E. Park,, R. Kopelman,, S. Miller,, B. B. Finlay,, P. Gros,, and S. Grinstein. 2006. Visualization of vacuolar acidification-induced transcription of genes of pathogens inside macrophages. Mol. Biol. Cell 17:498510.
109. Mayer, M. L.,, J. A. Sheridan,, C. J. Blohmke,, S. E. Turvey,, and R. E. Hancock. 2011. The Pseudomonas aeruginosa autoinducer 3O-C12 homoserine lactone provokes hyperinflammatory responses from cystic fibrosis airway epithelial cells. PLoS ONE 6:e16246.
110. 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.
111. McKnight, S. L.,, B. H. Iglewski,, and E. C. Pesci. 2000. The Pseudomonas quinolone signal regulates rhl quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 182:27022708.
112. Meehl, M.,, S. Herbert,, F. Gotz,, and A. Cheung. 2007. Interaction of the GraRS two-component system with the VraFG ABC transporter to support vancomycin-intermediate resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 51:26792689.
113. Mekalanos, J. J.,, E. J. Rubin,, and M. K. Waldor. 1997. Cholera: molecular basis for emergence and pathogenesis. FEMS Immunol. Med. Microbiol. 18:241248.
114. Mellies, J. L.,, S. J. Elliott,, V. Sperandio,, M. S. Donnenberg,, and J. B. Kaper. 1999. The Per regulon of enteropathogenic Escherichia coli: identification of a regulatory cascade and a novel transcriptional activator, the locus of enterocyte effacement (LEE)-encoded regulator (Ler). Mol. Microbiol. 33:296306.
115. Merighi, M.,, A. Carroll-Portillo,, A. N. Septer,, A. Bhatiya,, and J. S. Gunn. 2006. Role of Salmonella enterica serovar Typhimurium two-component system PreA/PreB in modulating PmrA-regulated gene transcription. J. Bacteriol. 188:141149.
116. Merighi, M.,, A. N. Septer,, A. Carroll-Portillo,, A. Bhatiya,, S. Porwollik,, M. McClelland,, and J. S. Gunn. 2009. Genome-wide analysis of the PreA/PreB (QseB/QseC) regulon of Salmonella enterica serovar Typhimurium. BMC Microbiol. 9:42.
117. Minuk, G. Y. 1986. Gamma-aminobutyric acid (GABA) production by eight common bacterial pathogens. Scand. J. Infect. Dis. 18:465467.
118. Moreira, C. G.,, D. Weinshenker,, and V. Sperandio. 2010. QseC mediates Salmonella enterica serovar typhimurium virulence in vitro and in vivo. Infect. Immun. 78:914926.
119. Morera, S.,, V. Gueguen-Chaignon,, A. Raffoux,, and D. Faure. 2008. Cloning, purification, crystallization and preliminary X-ray analysis of a bacterial GABA receptor with a Venus flytrap fold. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 64:11531155.
120. Morici, L. A.,, A. J. Carterson,, V. E. Wagner,, A. Frisk,, J. R. Schurr,, K. Honerzu Bentrup,, D. J. Hassett,, B. H. Iglewski,, K. Sauer,, and M. J. Schurr. 2007. Pseudomonas aeruginosa AlgR represses the Rhl quorum-sensing system in a biofilm-specific manner. J. Bacteriol. 189:77527764.
121. Moss, J. E.,, P. E. Fisher,, B. Vick,, E. A. Groisman,, and A. Zychlinsky. 2000. The regulatory protein PhoP controls susceptibility to the host inflammatory response in Shigella flexneri. Cell. Microbiol. 2:443452.
122. Mountfort, D. O.,, and V. Pybus. 1992. Regulatory influences on the production of gamma-aminobutyric acid by a marine pseudomonad. Appl. Environ. Microbiol. 58:237242.
123. Nakka, S.,, M. Qi,, and Y. Zhao. 2010. The Erwinia amylovora PhoPQ system is involved in resistance to antimicrobial peptide and suppresses gene expression of two novel type III secretion systems. Microbiol. Res. 165:665673.
124. Neoh, H. M.,, L. Cui,, H. Yuzawa,, F. Takeuchi,, M. Matsuo,, and K. Hiramatsu. 2008. Mutated response regulator graR is responsible for phenotypic conversion of Staphylococcus aureus from heterogeneous vancomycin-intermediate resistance to vancomycin-intermediate resistance. Antimicrob. Agents Chemother. 52:4553.
125. Neudeck, B. L.,, J. Loeb,, and J. Buck. 2003. Activation of the kappa-opioid receptor in Caco-2 cells decreases interleukin-8 secretion. Eur. J. Pharmacol. 467:8184.
126. Neudeck, B. L.,, and J. M. Loeb. 2002. Endomorphin-1 alters interleukin-8 secretion in Caco-2 cells via a receptor mediated process. Immunol. Lett. 84:217221.
127. Owens, D. F.,, and A. R. Kriegstein. 2002. Is there more to GABA than synaptic inhibition? Nat. Rev. Neurosci. 3:715727.
128. Oyston, P. C.,, N. Dorrell,, K. Williams,, S. R. Li,, M. Green,, R. W. Titball,, and B. W. Wren. 2000. The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect. Immun. 68:34193425.
129. Pal, U.,, A. M. de Silva,, R. R. Montgomery,, D. Fish,, J. Anguita,, J. F. Anderson,, Y. Lobet,, and E. Fikrig. 2000. Attachment of Borrelia burgdorferi within Ixodes scapularis mediated by outer surface protein A. J. Clin. Investig. 106:561569.
130. Pappas, K. M.,, and S. C. Winans. 2003. A LuxR-type regulator from Agrobacterium tumefaciens elevates Ti plasmid copy number by activating transcription of plasmid replication genes. Mol. Microbiol. 48:10591073.
131. Paris, I.,, P. Martinez-Alvarado,, C. Perez-Pastene,, M. N. Vieira,, C. Olea-Azar,, R. Raisman-Vozari,, S. Cardenas,, R. Graumann,, P. Caviedes,, and J. Segura-Aguilar. 2005. Monoamine transporter inhibitors and norepinephrine reduce dopamine-dependent iron toxicity in cells derived from the substantia nigra. J. Neurochem. 92:10211032.
132. Patel, N. J.,, O. Zaborina,, L. Wu,, Y. Wang,, D. J. Wolfgeher,, V. Valuckaite,, M. J. Ciancio,, J. E. Kohler,, O. Shevchenko,, S. P. Colgan,, E. B. Chang,, J. R. Turner,, and J. C. Alverdy. 2007. Recognition of intestinal epithelial HIF-1alpha activation by Pseudomonas aeruginosa. Am. J. Physiol. Gastrointest. Liver Physiol. 292:G134G142.
133. 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.
134. Peschel, A. 2002. How do bacteria resist human antimicrobial peptides? Trends Microbiol. 10:179186.
135. Peschel, A.,, R. W. Jack,, M. Otto,, L. V. Collins,, P. Staubitz,, G. Nicholson,, H. Kalbacher,, W. F. Nieuwenhuizen,, G. Jung,, A. Tarkowski,, K. P. van Kessel,, and J. A. van Strijp. 2001. Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with L-lysine. J. Exp. Med. 193:10671076.
136. 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.
137. Peterson, M. M.,, J. L. Mack,, P. R. Hall,, A. A. Alsup,, S. M. Alexander,, E. K. Sully,, Y. S. Sawires,, A. L. Cheung,, M. Otto,, and H. D. Gresham. 2008. Apolipoprotein B is an innate barrier against invasive Staphylococcus aureus infection. Cell Host Microbe 4:555566.
138. Peterson, P. K.,, C. C. Chao,, T. Molitor,, M. Murtaugh,, F. Strgar,, and B. M. Sharp. 1991. Stress and pathogenesis of infectious disease. Rev. Infect. Dis. 13:710720.
139. Peterson, P. K.,, T. W. Molitor,, and C. C. Chao. 1998. The opioid-cytokine connection. J. Neuroimmunol. 83:6369.
140. Piper, K. R.,, S. Beck Von Bodman,, and S. K. Farrand. 1993. Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature 362:448450.
141. Piper, K. R.,, S. Beck Von Bodman,, I. Hwang,, and S. K. Farrand. 1999. Hierarchical gene regulatory systems arising from fortuitous gene associations: controlling quorum sensing by the opine regulon in Agrobacterium. Mol. Microbiol. 32:10771089.
142. Porat, R.,, B. D. Clark,, S. M. Wolff,, and C. A. Dinarello. 1991. Enhancement of growth of virulent strains of Escherichia coli by interleukin-1. Science 254:430432.
143. Potter, L. R.,, A. R. Yoder,, D. R. Flora,, L. K. Antos,, and D. M. Dickey. 2009. Natriuretic peptides: their structures, receptors, physiologic functions and therapeutic applications. Handb. Exp. Pharmacol. 2009(191):341366.
144. Prost, L. R.,, M. E. Daley,, M. W. Bader,, R. E. Klevit,, and S. I. Miller. 2008. The PhoQ histidine kinases of Salmonella and Pseudomonas spp. are structurally and functionally different: evidence that pH and antimicrobial peptide sensing contribute to mammalian pathogenesis. Mol. Microbiol. 69:503519.
145. Prost, L. R.,, M. E. Daley,, V. Le Sage,, M. W. Bader,, H. Le Moual,, R. E. Klevit,, and S. I. Miller. 2007. Activation of the bacterial sensor kinase PhoQ by acidic pH. Mol. Cell 26:165174.
146. Provenzano, D.,, D. A. Schuhmacher,, J. L. Barker,, and K. E. Klose. 2000. The virulence regulatory protein ToxR mediates enhanced bile resistance in Vibrio cholerae and other pathogenic Vibrio species. Infect. Immun. 68:14911497.
147. Rashid, M. H.,, C. Rajanna,, D. Zhang,, V. Pasquale,, L. S. Magder,, A. Ali,, S. Dumontet,, and D. K. Karaolis. 2004. Role of exopolysaccharide, the rugose phenotype and VpsR in the pathogenesis of epidemic Vibrio cholerae. FEMS Microbiol. Lett. 230:105113.
148. Rasko, D. A.,, C. G. Moreira,, R. Li de,, N. C. Reading,, J. M. Ritchie,, M. K. Waldor,, N. Williams,, R. Taussig,, S. Wei,, M. Roth,, D. T. Hughes,, J. F. Huntley,, M. W. Fina,, J. R. Falck,, and V. Sperandio. 2008. Targeting QseC signaling and virulence for antibiotic development. Science 321:10781080.
149. Ratledge, C.,, and L. G. Dover. 2000. Iron metabolism in pathogenic bacteria. Annu. Rev. Microbiol. 54:881941.
150. Reading, N. C.,, D. A. Rasko,, A. G. Torres,, and V. Sperandio. 2009. The two-component system QseEF and the membrane protein QseG link adrenergic and stress sensing to bacterial pathogenesis. Proc. Natl. Acad. Sci. USA 106:58895894.
151. Reading, N. C.,, A. G. Torres,, M. M. Kendall,, D. T. Hughes,, K. Yamamoto,, and V. Sperandio. 2007. A novel two-component signaling system that activates transcription of an enterohemorrhagic Escherichia coli effector involved in remodeling of host actin. J. Bacteriol. 189:24682476.
152. Reichenbach, B.,, Y. Gopel,, and B. Gorke. 2009. Dual control by perfectly overlapping sigma 54- and sigma 70- promoters adjusts small RNA GlmY expression to different environmental signals. Mol. Microbiol. 74:10541070.
153. Ritchie, A. J.,, A. Jansson,, J. Stallberg,, P. Nilsson,, P. Lysaght,, and M. A. Cooley. 2005. The Pseudomonas aeruginosa quorum-sensing molecule N-3-(oxododecanoyl)-L-homoserine lactone inhibits T-cell differentiation and cytokine production by a mechanism involving an early step in T-cell activation. Infect. Immun. 73:16481655.
154. Ritchie, A. J.,, A. O. Yam,, K. M. Tanabe,, S. A. Rice,, and M. A. Cooley. 2003. Modification of in vivo and in vitro T- and B-cell-mediated immune responses by the Pseudomonas aeruginosa quorum-sensing molecule N-(3-oxododecanoyl)-L-homoserine lactone. Infect. Immun. 71:44214431.
155. Roberts, M. R. 2007. Does GABA act as a signal in plants– Hints from molecular studies. Plant Signal. Behav. 2:408409.
156. Sansonetti, P. J.,, and C. Egile. 1998. Molecular bases of epithelial cell invasion by Shigella flexneri. Antonie Van Leeuwenhoek 74:191197.
157. Scheckelhoff, M. R.,, S. R. Telford,, M. Wesley,, and L. T. Hu. 2007. Borrelia burgdorferi intercepts host hormonal signals to regulate expression of outer surface protein A. Proc. Natl. Acad. Sci. USA 104:72477252.
158. Schlievert, P. M.,, L. C. Case,, K. A. Nemeth,, C. C. Davis,, Y. Sun,, W. Qin,, F. Wang,, A. J. Brosnahan,, J. A. Mleziva,, M. L. Peterson,, and B. E. Jones. 2007. Alpha and beta chains of hemoglobin inhibit production of Staphylococcus aureus exotoxins. Biochemistry 46:1434914358.
159. Schuhmacher, D. A.,, and K. E. Klose. 1999. Environmental signals modulate ToxT-dependent virulence factor expression in Vibrio cholerae. J. Bacteriol. 181:15081514.
160. Schuster, M.,, and E. P. Greenberg. 2006. A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int. J. Med. Microbiol. 296:7381.
161. 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.
162. Shadel, G. S.,, J. H. Devine,, and T. O. Baldwin. 1990. Control of the lux regulon of Vibrio fischeri. J. Biolumin. Chemilumin. 5:99106.
163. Shelp, B. J.,, A. W. Bown,, and M. D. McLean. 1999. Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci. 4:446452.
164. Shiner, E. K.,, D. Terentyev,, A. Bryan,, S. Sennoune,, R. Martinez-Zaguilan,, G. Li,, S. Gyorke,, S. C. Williams,, and K. P. Rumbaugh. 2006. Pseudomonas aeruginosa autoinducer modulates host cell responses through calcium signalling. Cell. Microbiol. 8:16011610.
165. Simpson, A. J.,, and V. Wuthiekanun. 2000. Interaction of insulin with Burkholderia pseudomallei may be caused by a preservative. J. Clin. Pathol. 53:159160.
166. Siraki, A. G.,, J. Smythies,, and P. J. O’Brien. 2000. Superoxide radical scavenging and attenuation of hypoxia-reoxygenation injury by neurotransmitter ferric complexes in isolated rat hepatocytes. Neurosci. Lett. 296:3740.
167. Skaar, E. P.,, M. Humayun,, T. Bae,, K. L. DeBord,, and O. Schneewind. 2004. Iron-source preference of Staphylococcus aureus infections. Science 305:16261628.
168. 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.
169. 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.
170. Smith, R. S.,, and B. H. Iglewski. 2003. P. aeruginosa quorum-sensing systems and virulence. Curr. Opin. Microbiol. 6:5660.
171. Smith, R. S.,, R. Kelly,, B. H. Iglewski,, and R. P. Phipps. 2002. The Pseudomonas autoinducer N-(3-oxododecanoyl) homoserine lactone induces cyclooxygenase-2 and prostaglandin E2 production in human lung fibroblasts: implications for inflammation. J. Immunol. 169:26362642.
172. Smith, R. S.,, M. C. Wolfgang,, and S. Lory. 2004. An adenylate cyclase-controlled signaling network regulates Pseudomonas aeruginosa virulence in a mouse model of acute pneumonia. Infect. Immun. 72:16771684.
173. Sperandio, V. 2004. Striking a balance: inter-kingdom cell-to-cell signaling, friendship or war? Trends Immunol. 25:505507.
174. 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.
175. 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.
176. 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.
177. 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.
178. Stachel, S. E.,, and P. C. Zambryski. 1986. virA and virG control the plant-induced activation of the T-DNA transfer process of A. tumefaciens. Cell 46:325333.
179. Staley, T. E.,, E. W. Jones,, and L. D. Corley. 1969. Attachment and penetration of Escherichia coli into intestinal epithelium of the ileum in newborn pigs. Am. J. Pathol. 56:371392.
180. Sternini, C.,, S. Patierno,, I. S. Selmer,, and A. Kirchgessner. 2004. The opioid system in the gastrointestinal tract. Neurogastroenterol. Motil. 16(Suppl 2):316.
181. Stoltz, D. A.,, E. A. Ozer,, C. J. Ng,, J. M. Yu,, S. T. Reddy,, A. J. Lusis,, N. Bourquard,, M. R. Parsek,, J. Zabner,, and D. M. Shih. 2007. Paraoxonase-2 deficiency enhances Pseudomonas aeruginosa quorum sensing in murine tracheal epithelia. Am. J. Physiol. Lung Cell. Mol. Physiol. 292:L852L860.
182. Tateda, K.,, Y. Ishii,, M. Horikawa,, T. Matsumoto,, S. Miyairi,, J. C. Pechere,, T. J. Standiford,, M. Ishiguro,, and K. Yamaguchi. 2003. The Pseudomonas aeruginosa autoinducer N-3-oxododecanoyl homoserine lactone accelerates apoptosis in macrophages and neutrophils. Infect. Immun. 71:57855793.
183. 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.
184. Thedieck, K.,, T. Hain,, W. Mohamed,, B. J. Tindall,, M. Nimtz,, T. Chakraborty,, J. Wehland,, and L. Jansch. 2006. The MprF protein is required for lysinylation of phospholipids in listerial membranes and confers resistance to cationic antimicrobial peptides (CAMPs) on Listeria monocytogenes. Mol. Microbiol. 62:13251339.
185. Torres, V. J.,, D. L. Stauff,, G. Pishchany,, J. S. Bezbradica,, L. E. Gordy,, J. Iturregui,, K. L. Anderson,, P. M. Dunman,, S. Joyce,, and E. P. Skaar. 2007. A Staphylococcus aureus regulatory system that responds to host heme and modulates virulence. Cell Host Microbe 1:109119.
186. Tsavkelova, E. A.,, I. V. Botvinko,, V. S. Kudrin,, and A. V. Oleskin. 2000. Detection of neurotransmitter amines in microorganisms with the use of high-performance liquid chromatography. Dokl. Biochem. 372:115117.
187. Vallejo, R.,, O. de Leon-Casasola,, and R. Benyamin. 2004. Opioid therapy and immunosuppression: a review. Am. J. Ther. 11:354365.
188. Van Gennip, M.,, L. D. Christensen,, M. Alhede,, R. Phipps,, P. O. Jensen,, L. Christophersen,, S. J. Pamp,, C. Moser,, P. J. Mikkelsen,, A. Y. Koh,, T. Tolker-Nielsen,, G. B. Pier,, N. Hoiby,, M. Givskov,, and T. Bjarnsholt. 2009. Inactivation of the rhlA gene in Pseudomonas aeruginosa prevents rhamnolipid production, disabling the protection against polymorphonuclear leukocytes. APMIS 117:537546.
189. Veron, W.,, O. Lesouhaitier,, X. Pennanec,, K. Rehel,, P. Leroux,, N. Orange,, and M. G. Feuilloley. 2007. Natriuretic peptides affect Pseudomonas aeruginosa and specifically modify lipopolysaccharide biosynthesis. FEBS J. 274:58525864.
190. Volmer, J. B.,, L. F. Thompson,, and M. R. Blackburn. 2006. Ecto-5–-nucleotidase (CD73)-mediated adenosine production is tissue protective in a model of bleomycin-induced lung injury. J. Immunol. 176:44494458.
191. Vuckovic, D.,, M. Abram,, M. Bubonja,, B. Wraber,, and M. Doric. 2006. Host resistance to primary and secondary Campylobacter jejuni infections in C57Bl/6 mice. Microb. Pathog. 40:3539.
192. Vuddhakul, V.,, P. Tharavichitkul,, N. Na-Ngam,, S. Jitsurong,, B. Kunthawa,, P. Noimay,, A. Binla,, and V. Thamlikitkul. 1999. Epidemiology of Burkholderia pseudomallei in Thailand. Am. J. Trop. Med. Hyg. 60:458461.
193. Vuopio-Varkila, J.,, and G. K. Schoolnik. 1991. Localized adherence by enteropathogenic Escherichia coli is an inducible phenotype associated with the expression of new outer membrane proteins. J. Exp. Med. 174:11671177.
194. Wade, D. S.,, M. W. Calfee,, E. R. Rocha,, E. A. Ling,, E. Engstrom,, J. P. Coleman,, and E. C. Pesci. 2005. Regulation of Pseudomonas quinolone signal synthesis in Pseudomonas aeruginosa. J. Bacteriol. 187:43724380.
195. Watnick, P. I.,, and R. Kolter. 1999. Steps in the development of a Vibrio cholerae El Tor biofilm. Mol. Microbiol. 34:586595.
196. Weiss, D. S.,, A. Brotcke,, T. Henry,, J. J. Margolis,, K. Chan,, and D. M. Monack. 2007. In vivo negative selection screen identifies genes required for Francisella virulence. Proc. Natl. Acad. Sci. USA 104:60376042.
197. Wertheim, H. F.,, M. C. Vos,, A. Ott,, A. van Belkum,, A. Voss,, J. A. Kluytmans,, P. H. van Keulen,, C. M. Vandenbroucke-Grauls,, M. H. Meester,, and H. A. Verbrugh. 2004. Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet 364:703705.
198. Woods, D. E.,, A. L. Jones,, and P. J. Hill. 1993. Interaction of insulin with Pseudomonas pseudomallei. Infect. Immun. 61:40454050.
199. Wretlind, B.,, A. Bjorklind,, and O. R. Pavlovskis. 1987. Role of exotoxin A and elastase in the pathogenicity of Pseudomonas aeruginosa strain PAO experimental mouse burn infection. Microb. Pathog. 2:397404.
200. Wu, L.,, O. Estrada,, O. Zaborina,, M. Bains,, L. Shen,, J. E. Kohler,, N. Patel,, M. W. Musch,, E. B. Chang,, Y. X. Fu,, M. A. Jacobs,, M. I. Nishimura,, R. E. Hancock,, J. R. Turner,, and J. C. Alverdy. 2005. Recognition of host immune activation by Pseudomonas aeruginosa. Science 309:774777.
201. Wu, L.,, C. Holbrook,, O. Zaborina,, E. Ploplys,, F. Rocha,, D. Pelham,, E. Chang,, M. Musch,, and J. Alverdy. 2003. Pseudomonas aeruginosa expresses a lethal virulence determinant, the PA-I lectin/adhesin, in the intestinal tract of a stressed host: the role of epithelia cell contact and molecules of the quorum sensing signaling system. Ann. Surg. 238:754764.
202. Wu, L. R.,, O. Zaborina,, A. Zaborin,, E. B. Chang,, M. Musch,, C. Holbrook,, J. R. Turner,, and J. C. Alverdy. 2005. Surgical injury and metabolic stress enhance the virulence of the human opportunistic pathogen Pseudomonas aeruginosa. Surg. Infect. (Larchmt) 6:185195.
203. Yamamoto, K.,, K. Hirao,, T. Oshima,, H. Aiba,, R. Utsumi,, and A. Ishihama. 2005. Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J. Biol. Chem. 280:14481456.
204. Yamashita, K.,, H. Kaneko,, S. Yamamoto,, T. Konagaya,, K. Kusugami,, and T. Mitsuma. 1998. Inhibitory effect of somatostatin on Helicobacter pylori proliferation in vitro. Gastroenterology 115:11231130.
205. Yang, F.,, L. H. Wang,, J. Wang,, Y. H. Dong,, J. Y. Hu,, and L. H. Zhang. 2005. Quorum quenching enzyme activity is widely conserved in the sera of mammalian species. FEBS Lett. 579:37133717.
206. Yang, X. F.,, U. Pal,, S. M. Alani,, E. Fikrig,, and M. V. Norgard. 2004. Essential role for OspA/B in the life cycle of the Lyme disease spirochete. J. Exp. Med. 199:641648.
207. Yarwood, J. M.,, J. K. McCormick,, M. L. Paustian,, V. Kapur,, and P. M. Schlievert. 2002. Repression of the Staphylococcus aureus accessory gene regulator in serum and in vivo. J. Bacteriol. 184:10951101.
208. Yarwood, J. M.,, J. K. McCormick,, and P. M. Schlievert. 2001. Identification of a novel two-component regulatory system that acts in global regulation of virulence factors of Staphylococcus aureus. J. Bacteriol. 183:11131123.
209. Yildiz, F. H.,, N. A. Dolganov,, and G. K. Schoolnik. 2001. VpsR, a member of the response regulators of the two-component regulatory systems, is required for expression of vps biosynthesis genes and EPS(ETr)-associated phenotypes in Vibrio cholerae O1 El Tor. J. Bacteriol. 183:17161726.
210. Zaborina, O.,, F. Lepine,, G. Xiao,, V. Valuckaite,, Y. Chen,, T. Li,, M. Ciancio,, A. Zaborin,, E. O. Petrof,, J. R. Turner,, L. G. Rahme,, E. Chang,, and J. C. Alverdy. 2007. Dynorphin activates quorum sensing quinolone signaling in Pseudomonas aeruginosa. PLoS Pathog. 3:e35.
211. Zav’yalov, V. P.,, T. V. Chernovskaya,, E. V. Navolotskaya,, A. V. Karlyshev,, S. MacIntyre,, A. M. Vasiliev,, and V. M. Abramov. 1995. Specific high affinity binding of human interleukin 1 beta by Caf1A usher protein of Yersinia pestis. FEBS Lett. 371:6568.
212. Zhang, H. B.,, L. H. Wang,, and L. H. Zhang. 2002. Genetic control of quorum-sensing signal turnover in Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. USA 99:46384643.
213. Zhang, L.,, P. J. Murphy,, A. Kerr,, and M. E. Tate. 1993. Agrobacterium conjugation and gene regulation by N-acyl-L-homoserine lactones. Nature 362:446448.
214. Zhou, Y.,, A. Mohsenin,, E. Morschl,, H. W. Young,, J. G. Molina,, W. Ma,, C. X. Sun,, H. Martinez-Valdez,, and M. R. Blackburn. 2009. Enhanced airway inflammation and remodeling in adenosine deaminase-deficient mice lacking the A2B adenosine receptor. J. Immunol. 182:80378046.
215. Zimmermann, S.,, C. Wagner,, W. Muller,, G. Brenner-Weiss,, F. Hug,, B. Prior,, U. Obst,, and G. M. Hansch. 2006. Induction of neutrophil chemotaxis by the quorum-sensing molecule N-(3-oxododecanoyl)-L-homoserine lactone. Infect. Immun. 74:56875692.


Generic image for table
Table 1

Summary of interkingdom signaling systems

Citation: Gruber C, Sperandio V. 2013. Regulation in Response to Host-Derived Signaling Molecules, p 545-565. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch27

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error