Norepinephrine augments Salmonella enterica-induced enteritis in a manner associated with increased net replication but independent of the putative adrenergic sensor kinases QseC and QseE

Infection and Immunity

Volumn 78, Issue 1, 2010, Pages 372-380

  Pullinger, Gillian D ^a   Carnell, Sonya C ^a   Sharaff, Fathima F ^b   Van Diemen, Pauline M ^a   Dziva, Francis ^a   Morgan, Eirwen ^a   Lyte, Mark ^c   Freestone, Primrose P E ^b   Stevens, Mark P ^a  

^a INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENERGIC RECEPTOR; BACTERIAL PROTEIN; CATECHOLAMINE; FERRIC ION; NORADRENALIN; SENSOR KINASE QSEC; SENSOR KINASE QSEE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIUM MUTANT; CONTROLLED STUDY; COW; ENTERITIS; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC TRANSCRIPTION; IN VITRO STUDY; IN VIVO STUDY; LIGATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; STRESS; TYPHOID FEVER;

ANIMALS; BACTERIAL PROTEINS; CATTLE; CATTLE DISEASES; CELL PROLIFERATION; ENTERITIS; MALE; NOREPINEPHRINE; SALMONELLA ENTERICA; SALMONELLA INFECTIONS, ANIMAL;

EID: 73449114289     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01203-09     Document Type: Article

References (48)

1. Alverdy, J., and E. B. Chang. 2008. The re-emerging role of the intestinal microflora in critical illness and inflammation: why the gut hypothesis of sepsis syndrome will not go away. J. Leukoc. Biol. 83:461-466.
2. 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: 480-489.
3. 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. 44:271-278.
4. Bispham, J., B. N. Tripathi, P. R. Watson, and T. S. Wallis. 2001. Salmonella pathogenicity island 2 influences both systemic salmonellosis and Salmonella-induced enteritis in calves. Infect. Immun. 69:367-377.
5. Bongaerts, R. J., I. Hautefort, J. M. Sidebotham, and J. C. Hinton. 2002. Green fluorescent protein as a marker for conditional gene expression in bacterial cells. Methods Enzymol. 358:43-66.
6. Brown, D. R., and S. M. O'Grady. 1997. Regulation of ion transport in the porcine intestinal tract by enteric neurotransmitters and hormones. Comp. Biochem. Physiol. A Physiol. 118:309-317.
7. Callaway, T. R., J. L. Morrow, T. S. Edrington, K. J. Genovese, S. Dowd, J. Carroll, J. W. Dailey, R. B. Harvey, T. L. Poole, R. C. Anderson, and D. J. Nisbet. 2006. Social stress increases fecal shedding of Salmonella typhimurium by early weaned piglets. Curr. Issues Intest. Microbiol. 7:65-71.
8. 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.
9. r cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158:9-14.
10. 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. U. S. A. 103:10420-10425.
11. Coombes, B. K., B. A. Coburn, A. A. Potter, S. Gomis, K. Mirakhur, Y. Li, and B. B. Finlay. 2005. Analysis of the contribution of Salmonella pathogenicity islands 1 and 2 to enteric disease progression using a novel bovine ileal loop model and a murine model of infectious enterocolitis. Infect. Immun. 73:7161-7169.
12. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
13. Ellermeier, J. R., and J. M. Slauch. 2008. Fur regulates expression of the Salmonella pathogenicity island 1 type III secretion system through HilD. J. Bacteriol. 190:476-486.
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., 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. 182:6091-6098.
17. Freestone, P. P., M. Sandrini, R. D. Haigh, and M. Lyte. 2008. Microbial endocrinology: how stress influences susceptibility to infection. Trends Microbiol. 16:55-64.
18. 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-G1246.
19. - Salmonella typhimurium is enhanced by neutralization of gamma interferon and tumor necrosis factor alpha. Infect. Immun. 65:5191-5197.
20. Hashimoto-Gotoh, T., F. C. Franklin, A. Nordheim, and K. N. Timmis. 1981. Specific-purpose plasmid cloning vectors. I. Low copy number, temperature-sensitive, mobilization defective pSC101-derived containment vectors. Gene 16:227-235.
21. Hautefort, I., M. J. Proença, and J. C. Hinton. 2003. Single-copy green fluorescent protein gene fusions allow accurate measurement of Salmonella gene expression in vitro and during infection of mammalian cells. Appl. Environ. Microbiol. 69:7480-7491.
22. Hoiseth, S. K., and B. A. D. Stocker. 1981. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291:238-239.
23. Hudson, D. L., A. N. Layton, T. R. Field, A. J. Bowen, H. Wolf-Watz, M. Elofsson, M. P. Stevens, and E. E. Galyov. 2007. Inhibition of Type III secretion in Salmonella enterica serovar Typhimurium by small molecule inhibitors. Antimicrob. Agents Chemother. 51:2631-2635.
24. Hughes, D. T., and V. Sperandio. 2008. Inter-kingdom signalling: communication between bacteria and their hosts. Nat. Rev. Microbiol. 6:111-120.
25. Karavolos, M. H., H. Spencer, D. M. Bulmer, A. Thompson, K. Winzer, P. Williams, J. C. D. Hinton, and C. M. A. Khan. 2008. Adrenaline modulates the global transcriptional profile of Salmonella revealing a role in the antimicrobial peptide and oxidative stress resistance responses. BMC Genomics 9:458.
26. Kendrick, M. L., T. Meile, N. J. Zyromski, T. Tanaka, K. D. Libsch, and M. G. Sarr. 2002. Extrinsic denervation causes a transient proabsorptive adrenergic hypersensitivity in the canine proximal colon. Dig. Dis. Sci. 47: 1752-1757.
27. Lee, C. A., M. Silva, A. M. Siber, A. J. Kelly, E. Galyov, and B. A. McCormick. 2000. A secreted Salmonella protein induces a proinflammatory response in epithelial cells, which promotes neutrophil migration. Proc. Natl. Acad. Sci. U. S. A. 97:12283-12288.
28. Lyte, M., B. P. Arulanandam, and C. D. Frank. 1996. Production of Shigalike toxins by Escherichia coli O157:H7 can be influenced by the neuroendocrine hormone norepinephrine. J. Lab. Clin. Med. 128:392-398.
29. Lyte, M., and S. Ernst. 1992. Catecholamine-induced growth of gram-negative bacteria. Life Sci. 50:203-212.
30. Lyte, M., and S. Ernst. 1993. Alpha and beta adrenergic receptor involvement in catecholamine-induced growth of Gram-negative bacteria. Biochem. Biophys. Res. Commun. 190:447-452.
31. 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.
32. Methner, U., W. Rabsch, R. Reissbrodt, and P. H. Williams. 2008. Effect of norepinephrine on colonisation and systemic spread of Salmonella enterica in infected animals: role of catecholate siderophore precursors and degradation products. Int. J. Med. Microbiol. 298:429-439.
33. Morgan, E., J. D. Campbell, S. C. Rowe, J. Bispham, M. P. Stevens, A. J. Bowen, P. A. Barrow, D. J. Maskell, and T. S. Wallis. 2004. Identification of host-specific colonization factors of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 54:994-1010.
34. Paulin, S. M., A. Jagannathan, J. Campbell, T. S. Wallis, and M. P. Stevens. 2007. Net replication of Salmonella enterica serovars Typhimurium and Choleraesuis in porcine intestinal mucosa and nodes is associated with their differential virulence. Infect. Immun. 75:3950-3960.
35. Paulin, S. M., P. R. Watson, A. R. Benmore, M. P. Stevens, P. W. Jones, B. Villarreal-Ramos, and T. S. Wallis. 2002. Analysis of Salmonella enterica serotype-host specificity in calves: Avirulence of S. enterica serotype Gallinarum correlates with bacterial dissemination from mesenteric lymph nodes and persistence in vivo. Infect. Immun. 70:6788-6797.
36. Pullinger, G. D., F. Dziva, B. Charleston, T. S. Wallis, and M. P. Stevens. 2008. Identification of Salmonella enterica serovar Dublin-specific sequences by subtractive hybridization and analysis of their role in intestinal colonization and systemic translocation in cattle. Infect. Immun. 76:5310-5321.
37. Rasko, D. A., C. G. Moreira, D. R. Li, 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 321:1078- 1080.
38. 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. U. S. A. 106:5889-5894.
39. 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. 189:2468-2476.
40. Schmitt, C. K., J. S. Ikeda, S. A. Darnell, P. R. Watson, J. Bispham, T. S. Wallis, D. L. Weinstein, E. S. Metcalf, and A. D. O'Brien. 2001. Absence of all components of the flagellar export and synthesis machinery differentially alters virulence of Salmonella enterica serovar Typhimurium in models of typhoid fever, survival in macrophages, tissue culture invasiveness, and calf enterocolitis. Infect. Immun. 69:5619-5625.
41. 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. U. S. A. 100:8951-8956.
42. 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. 43:809-821.
43. Stevens, M. P. Modulation of the interaction of enteric bacteria with intestinal mucosa by stress-related catecholamines. In M. Lyte and P. Freestone (ed.), Microbial endocrinology, in press. Springer, New York, NY.
44. 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.
45. Wallis, T. S., S. M. Paulin, J. S. Plested, P. R. Watson, and P. W. Jones. 1995. The Salmonella dublin virulence plasmid mediates systemic but not enteric phases of salmonellosis in cattle. Infect. Immun. 63:2755-2761.
46. Watson, P. R., E. E. Galyov, S. M. Paulin, P. W. Jones, and T. S. Wallis. 1998. Mutation of invH, but not stn, reduces Salmonella-induced enteritis in cattle. Infect. Immun. 66:1432-1438.
47. Williams, P. H., W. Rabsch, U. Methner, W. Voigt, H. Tschäpe, and R. Reissbrodt. 2006. Catecholate receptor proteins in Salmonella enterica: role in virulence and implications for vaccine development. Vaccine 24:3840-3844.
48. Winter, S. E., P. Thiennimitr, S. P. Nuccio, T. Haneda, M. G. Winter, R. P. Wilson, J. M. Russell, T. Henry, Q. T. Tran, S. D. Lawhon, G. Gomez, C. L. Bevins, H. Rüssmann, D. M. Monack, L. G. Adams, and A. J. Bäumler. 2009. Contribution of flagellin pattern recognition to intestinal inflammation during Salmonella enterica serotype Typhimurium infection. Infect. Immun. 77:1904-1916.