Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157:H7 chemotaxis, colonization, and gene expression

Infection and Immunity

Volumn 75, Issue 9, 2007, Pages 4597-4607

  Bansal, Tarun ^a   Englert, Derek ^a   Lee, Jintae ^a   Hegde, Manjunath ^a   Wood, Thomas K ^a   Jayaraman, Arul ^a  

^a Texas AandM University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENALIN; INDOLE; NORADRENALIN;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BIOFILM; CELL ADHESION; CHEMOTAXIS; CONTROLLED STUDY; DNA MICROARRAY; ENTEROBACTER INFECTION; ESCHERICHIA COLI O157; GENE EXPRESSION; HORMONAL REGULATION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

CHEMOTAXIS; EPINEPHRINE; ESCHERICHIA COLI O157; GENE EXPRESSION REGULATION, BACTERIAL; HELA CELLS; HUMANS; INDOLES; NOREPINEPHRINE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

EID: 34548500624     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00630-07     Document Type: Article

References (55)

1. Affymetrix. 2004. GeneChip expression: data analysis fundamentals. Affymetrix, Inc., Santa Clara, CA.
2. Ahlman, H., H. N. Bhargava, A. Dahlström, I. Larsson, B. Newson, and G. Pettersson. 1981. On the presence of serotonin in the gut lumen and possible release mechanisms. Acta Physiol. Scand. 112:263-269.
3. Ahlman, H., L. DeMagistris, M. Zinner, and B. M. Jaffe. 1981. Release of immunoreactive serotonin into the lumen of the feline gut in response to vagal nerve stimulation. Science 213:1254-1255.
4. Anyanful, A., J. M. Dolan-Livengood, T. Lewis, S. Sheth, M. N. Dezalia, M. A. Sherman, L. V. Kalman, G. M. Benian, and D. Kalman. 2005. Paralysis and killing of Caenorhabditis elegans by enteropathogenic Escherichia coli requires the bacterial tryptophanase gene. Mol. Microbiol. 57:988-1007.
5. Buckles, E. L., X. Wang, C. V. Lockatell, D. E. Johnson, and M. S. Donnenberg. 2006. PhoU enhances the ability of extraintestinal pathogenic Escherichia coli strain CFT073 to colonize the murine urinary tract. Microbiology 152:153-160.
6. Chen, C., M. Lyte, M. P. Stevens, L. Vulchanova, and D. R. Brown. 2006. Mucosally directed adrenergic nerves and sympathomimetic drugs enhance non-intimate adherence of Escherichia coli O157:H7 to porcine cecum and colon. Eur. J. Pharmacol. 539:116-124.
7. Chen, C., D. R. Brown, Y. Xie, B. T. Green, and M. Lyte. 2003. Catecholamines modulate Escherichia coli O157:H7 adherence to murine cecal mucosa. Shock 20:183-188.
8. 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 103:10420-10425.
9. Clarke, M. B., and V. Sperandio. 2005. Events at the host-microbial interface of the gastrointestinal tract. III. Cell-to-cell signaling among microbial flora, host, and pathogens: there is a whole lot of talking going on. Am. J. Physiol. Gastrointest Liver. 288:G1105-1109.
10. Collier-Hyams, L. S., and A. S. Neish. 2005. Innate immune relationship between commensal flora and the mammalian intestine. Cell Mol. Life Sci. 62:1339-1348.
11. Costa, M., S. J. Brookes, and G. W. Hennig. 2000. Anatomy and physiology of the enteric nervous system. Gut 47:15-19.
12. Daigle, F., J. M. Fairbrother, and J. Harel. 1995. Identification of a mutation in the pst-phoU operon that reduces pathogenicity of an Escherichia coli strain causing septicemia in pigs. Infect. Immun. 63:4924-4927.
13. Domka, J., J. Lee, and T. K. Wood. 2006. YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signaling. Appl. Environ Microbiol. 72:2449-2459.
14. Freestone, P. P., R. D. Haigh, and M. Lyte. 2007. Specificity of catecholamine-induced growth in Escherichia coli O157:H7, Salmonella enterica, and Yersinia enterocolitica. FEMS Microbiol. Lett. 269:221-228.
15. 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. 172:53-60.
16. Freestone, P. P., P. H. Williams, R. D. Haigh, A. F. Maggs, C. P. Neal, and M. Lyte. 2002. Growth stimulation of intestinal commensal Escherichia coli by catecholamines: a possible contributory factor in trauma-induced sepsis. Shock 18:465-470.
17. Girón, J. A., A. G. Torres, E. Freer, and J. B. Kaper. 2002. The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol. Microbiol. 44:361-379.
18. González Barrios, A. F., R. Zuo, Y. Hashimoto, L. Yang, W. E. Bentley, and T. K. Wood. 2006. Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). J. Bacteriol. 188:305-316.
19. Green, B. T., M. Lyte, C. Chen, Y. Xie, M. A. Casey, A. Kulkarni-Narla, L. Vulchanova, and D. R. Brown. 2004. Adrenergic modulation of Escherichia coli O157:H7 adherence to the colonic mucosa. Am. J. Physiol. Gastrointest. Liver Physiol. 287:G1238-1246.
20. Hansen, M. C., R. J. J. Palmer, C. Udsen, D. C. White, and S. Molin. 2001. Assessment of GFP fluorescence in cells of Streptococcus gordonii under conditions of low pH and low oxygen concentration. Microbiology 147:1383-1391.
21. Herzberg, M., I. K. Kaye, W. Peti, and T. K. Wood. 2006. YdgG (TqsA) controls biofilm formation in Escherichia coli K-12 through autoinducer 2 transport. J. Bacteriol. 188:587-598.
22. Isaacs, H., D. Chao, C. Yanofsky, and M. H. Saier. 1994. Mechanism of catabolite repression of tryptophanase synthesis in Escherichia coli. Microbiology 140:2125-2134.
23. Kaper, J. B., J. P. Nataro, and H. L. T. Mobley. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2:123-139.
24. Kaper, J. B., and V. Sperandio. 2005. Bacterial cell-to-cell signaling in the gastrointestinal tract. Infect. Immun. 73:3197-3209.
25. Karch, H., P. I. Tarr, and M. Bielaszewska. 2005. Enterohaemorrhagic Escherichia coli in human medicine. Int. J. Med. Microbiol. 295:405-418.
26. Kloosterman, T. G., W. T. Hendriksen, J. J. Bijlsma, H. J. Bootsma, S. A. van Hijum, J. Kok, P. W. Hermans, and O. P. Kuipers. 2006. Regulation of glutamine and glutamate metabolism by GlnR and GlnA in Streptococcus pneumoniae. J. Biol. Chem. 281:25097-25109.
27. Lee, J., T. Bansal, A. Jayaraman, W. Bentley, and T. K. Wood. 2007. Enterohemorrhagic Escherichia coli biofilms are inhibited by 7-hydroxyindole and stimulated by isatin. Appl. Environ Microbiol. 73:4100-4109.
28. Lee, J., A. Jayaraman, and T. K. Wood. 2007. Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol. 7:42. doi:10.1186/1471-2180-7-42.
29. Linton, K. J., and C. F. Higgins. 1998. The Escherichia coli ATP-binding cassette (ABC) proteins. Mol. Microbiol. 28:5-13.
30. Lyte, M., B. Arulanandam, K. Nguyen, C. Frank, A. Erickson, and D. Francis. 1997. Norepinephrine induced growth and expression of virulence associated factors in enterotoxigenic and enterohemorrhagic strains of Escherichia coli. Adv. Exp. Med. Biol. 412:331-339.
31. Lyte, M., and M. T. Bailey. 1997. Neuroendocrine-bacterial interactions in a neurotoxin-induced model of trauma. J. Surg. Res. 70:195-201.
32. Lyte, M., A. K. Erickson, B. Arulanandam, C. Frank, M. A. Crawford, and D. Francis. 1997. Norepinephrine-induced expression of the K99 pilus adhesin of enterotoxigenic Escherichia coli. Biochem. Biophys. Res. Commun. 232:682-686.
33. Lyte, M., and S. Ernst. 1992. Catecholamine induced growth of Gram-negative bacteria. Life Sci. 50:203-212.
34. Macfarlane, S., and J. F. Dillon. 2007. Microbial biofilms in the human gastrointestinal tract. J. Appl. Microbiol. 102:1187-1196.
35. Nataro, J. P., and J. B. Kaper. 1998. Diarrhcagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
36. Nohno, T., T. Saito, and J. S. Hong. 1986. Cloning and complete nucleotide sequence of the Escherichia coli glutamine permease operon (glnHPQ). Mol. Gen. Genet. 205:260-269.
37. Pratt, L. A., and R. Kolter. 1998. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol. Microbiol. 30:285-293.
38. Ren, D., L. A. Bedzyk, R. W. Ye, S. M. Thomas, and T. K. Wood. 2004. Differential gene expression shows natural brominated furanones interfere with the autoinducer-2 bacterial signaling system of Escherichia coli. Biotechnol. Bioeng. 88:630-642.
39. Ren, D., L. A. Bedzyk, R. W. Ye, S. M. Thomas, and T. K. Wood. 2004. Stationary-phase quorum-sensing signals affect autoinducer-2 and gene expression in Escherichia coli. Appl. Environ Microbiol. 70:2038-2043.
40. Ren, D., R. Zuo, A. F. González Barrios, L. A. Bedzyk, G. R. Eldridge, M. E. Pasmore, and T. K. Wood. 2005. Differential gene expression for investigation of Escherichia coli biofilm inhibition by plant extract ursolic acid. Appl. Environ. Microbiol. 71:4022-4034.
41. Sircili, M. P., M. Walters, L. R. Trabulsi, and V. Sperandio. 2004. Modulation of enteropathogenic Escherichia coli virulence by quorum sensing. Infect. Immun. 72:2329-2337.
42. Sperandio, V., C. C. Li, and J. B. Kaper. 2002. Quorum-sensing 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. 70:3085-3093.
43. Sperandio, V., A. G. Torres, J. A. Girón, and J. B. Kaper. 2001. Quorum sensing is a global regulatory mechanism in enterohemorrhagic Escherichia coli O157:H7. J. Bacteriol. 183:5187-5197.
44. 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 100:8951-8956.
45. Taga, M. E., S. T. Miller, and B. L. Bassler. 2003. Lsr-mediated transport and processing of AI-2 in Salmonella typhimurium. Mol. Microbiol. 50:1411-1427.
46. Torres, A. G., and J. B. Kaper. 2003. Multiple elements controlling adherence of enterohemorrhagic Escherichia coli O157:H7 to HeLa cells. Infect. Immun. 71:4985-4995.
47. Torres, A. G., X. Zhou, and J. B. Kaper. 2005. Adherence of diarrheagenic Escherichia coli strains to epithelial cells. Infect. Immun. 73:18-29.
48. Vlisidou, I., M. Lyte, P. M. van Diemen, P. Hawes, P. Monaghan, T. S. Wallis, and M. P. Stevens. 2004. The neuroendocrine stress hormone norepinephrine augments Escherichia coli O157:H7-induced enteritis and adherence in a bovine ligated ileal loop model of infection. Infect. Immun. 72:5446-5451.
49. Walters, M., and V. Sperandio. 2006. Autoinducer 3 and epinephrine signaling in the kinetics of locus of enterocyte effacement gene expression in enterohemorrhagic Escherichia coli. Infect. Immun. 74:5445-5455.
50. Wang, D., X. Ding, and P. N. Rather. 2001. Indole can act as an extracellular signal in Escherichia coli. J. Bacteriol. 183:4210-4216.
51. Wang, L., Y. Hashimoto, C. Y. Tsao, J. J. Valdes, and W. E. Bentley. 2005. Cyclic AMP (cAMP) and cAMP receptor protein influence both synthesis and uptake of extracellular autoinducer 2 in Escherichia coli. J. Bacteriol. 187:2066-2076.
52. Wong, C. S., S. Jelacic, R. L. Habeeb, S. L. Watkins, and P. I. Tarr. 2000. The risk of the hemolytic-uremic syndrome after antibiotic treatment of Escherichia coli O157:H7 infections. N. Engl. J. Med. 342:1930-1936.
53. Wood, T. K., A. F. González Barrios, M. Herzberg, and J. Lee. 2006. Motility influences biofilm architecture in Escherichia coli. Appl. Microbiol. Biotechnol. 72:361-367.
54. Xavier, K. B., and B. L. Bassler. 2005. Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli. J. Bacteriol. 187:238-248.
55. Yu, H. S., and M. Alam. 1997. An agarose-in-plug bridge method to study chemotaxis in the Archaeon Halobacterium salinarum. FEMS Microbiol. Lett. 156:265-269.