6-hydroxydopamine-mediated release of norepinephrine increases faecal excretion of Salmonella enterica serovar Typhimurium in pigs

Veterinary Research

Volumn 41, Issue 5, 2010, Pages

  Pullinger, Gillian D ^a   Van Diemen, Pauline M ^a   Carnell, Sonya C ^a,b   Davies, Holly ^a   Lyte, Mark ^c   Stevens, Mark P ^a  

^a INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

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

Author keywords

Colonisation; Norepinephrine; Salmonella; Stress; Virulence

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM; SUIDAE;

ADRENERGIC RECEPTOR STIMULATING AGENT; NORADRENALIN; OXIDOPAMINE;

ANIMAL; ANIMAL SALMONELLOSIS; ARTICLE; DRUG EFFECT; FECES; METABOLISM; MICROBIOLOGY; NERVE CELL; ORAL DRUG ADMINISTRATION; PHYSIOLOGY; SALMONELLA TYPHIMURIUM; SWINE; SWINE DISEASE;

ADMINISTRATION, ORAL; ADRENERGIC AGENTS; ANIMALS; FECES; NEURONS; NOREPINEPHRINE; OXIDOPAMINE; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; SWINE; SWINE DISEASES;

EID: 77957830239     PISSN: 09284249     EISSN: 12979716     Source Type: Journal    
DOI: 10.1051/vetres/2010040     Document Type: Article

References (46)

1. Alverdy J., Holbrook C., Rocha F., Seiden L., Wu R. L., Musch M., et al., 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. (2000) 232:480-489.
2. Anonymous, Zoonoses Report, United Kingdom 2008, Department for Environment, Food and Rural Affairs Publications, London, 2010.
3. Bailey M. T., Dowd S. E., Parry N. M., Galley J. D., Schauer D. B., Lyte M., Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium, Infect. Immun. (2010) 78:1509-1519.
4. Barthel M., Hapfelmeier S., Quintanilla-Martínez L., Kremer M., Rohde M., Hogardt M., et al., Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host, Infect. Immun. (2003) 71:2839-2858. (Pubitemid 36519898)
5. Bearson B. L., Bearson S. M., The role of the QseC quorum-sensing sensor kinase in colonization and norepinephrine-enhanced motility of Salmonella enterica serovar Typhimurium, Microb. Pathog. (2008) 44:271-278.
6. Bearson B. L., Bearson S. M., Lee I. S., Brunelle B. W., 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. (2010) 48:214-219.
7. Berends B. R., Urlings H. A., Snijders J. M., Van Knapen F., Identification and quantification of risk factors in animal management and transport regarding Salmonella spp. in pigs, Int. J. Food Microbiol. (1996) 30:37-53. (Pubitemid 26258085)
8. Callaway T. R., Morrow J. L., Edrington T. S., Genovese K. J., Dowd S., Carroll J., et al., Social stress increases fecal shedding of Salmonella typhimurium by early weaned piglets, Curr. Issues Intest. Microbiol. (2006) 7:65-71. (Pubitemid 44121996)
9. Clarke M. B., Hughes D. T., Zhu C., Boedeker E. C., Sperandio V., The QseC sensor kinase: a bacterial adrenergic receptor, Proc. Natl. Acad. Sci. USA (2006) 103:10420-10425. (Pubitemid 44051182)
10. Davies R. H., Dalziel R., Gibbens J. C., Wilesmith J. W., Ryan J. M., Evans S. J., et al., National survey for Salmonella in pigs, cattle and sheep at slaughter in Great Britain, (1999-2000), J. Appl. Microbiol. (2004) 96:750-760. (Pubitemid 38437834)
11. de Champlain J., Degeneration and regrowth of adrenergic nerve fibers in the rat peripheral tissues after 6-hydroxydopamine, Can. J. Physiol. Pharmacol. (1971) 4:345-355.
12. Dowd S. E., Callaway T. R., Morrow-Tesch J., Handling may cause increased shedding of Escherichia coli and total coliforms in pigs, Foodborne Pathog. Dis. (2007) 4:99-102. (Pubitemid 46466596)
13. Ellermeier J. R., Slauch J. M., Fur regulates expression of the Salmonella pathogenicity island 1 type III secretion system through HilD, J. Bacteriol. (2008) 190:476-486.
14. Foster N., Lovell M. A., Marston K. L., Hulme S. D., Frost A. J., Bland P., Barrow P. A., Rapid protection of gnotobiotic pigs against experimental salmonellosis following induction of polymorphonuclear leukocytes by avirulent Salmonella enterica, Infect. Immun. (2003) 71:2182-2191. (Pubitemid 36368753)
15. Freestone P. P., Haigh R. D., Lyte M., Specificity of catecholamine-induced growth in Escherichia coli O157:H7, Salmonella enterica and Yersinia enterocolitica, FEMS Microbiol. Lett. (2007) 269:221-228. (Pubitemid 46449724)
16. Freestone P. P., Lyte M., Microbial endocrinology: experimental design issues in the study of interkingdom signalling in infectious disease, Adv. Appl. Microbiol. (2008) 64:75-105. (Pubitemid 351645189)
17. Freestone P. P., Sandrini S. M., Haigh R. D., Lyte M., Microbial endocrinology: how stress influences susceptibility to infection, Trends Microbiol. (2008) 16:55-64.
18. Garner C. D., Antonopoulos D. A., Wagner B., Duhamel G. E., Keresztes I., Ross D. A., et al., Perturbation of the small intestine microbial ecology by streptomycin alters pathology in a Salmonella enterica serovar Typhimurium murine model of infection, Infect. Immun. (2009) 77:2691-2702.
19. Hoiseth S. K., Stocker B. A., Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines, Nature (1981) 291:238-239.
20. Hurd H. S., McKean J. D., Griffith R. W., Wesley I. V., Rostagno M. H., Salmonella enterica infections in market swine with and without transport and holding, Appl. Environ. Microbiol. (2002) 68:2376-2381.
21. Isaacson R. E., Firkins L. D., Weigel R. M., Zuckermann F. A., DiPietro J. A., Effect of transportation and feed withdrawal on shedding of Salmonella typhimurium among experimentally infected pigs, Am. J. Vet. Res. (1999) 60:1155-1158.
22. Jones P. H., Roe J. M., Miller B. G., Effects of stressors on immune parameters and on the faecal shedding of enterotoxigenic Escherichia coli in piglets following experimental inoculation, Res. Vet. Sci. (2001) 70:9-17.
23. Karavolos M. H., Spencer H., Bulmer D. M., Thompson A., Winzer K., Williams P., et al., Adrenaline modulates the global transcriptional profile of Salmonella revealing a role in the antimicrobial peptide and oxidative stress resistance responses, BMC Genomics (2008) 9:458.
24. Laughlin R. S., Musch M. W., Hollbrook C. J., Rocha F. M., Chang E. B., Alverdy J. C., The key role of Pseudomonas aeruginosa PA-I lectin on experimental gut-derived sepsis, Ann. Surg. (2000) 232:133-142.
25. Lyte M., Bailey M. T., Neuroendocrine-bacterial interactions in a neurotoxin-induced model of trauma, J. Surg. Res. (1997) 70:195-201. (Pubitemid 27315206)
26. McCuddin Z. P., Carlson S. A., Sharma V. K., Experimental reproduction of bovine Salmonella encephalopathy using a norepinephrine-based stress model, Vet. J. (2008) 175:82-88.
27. Methner U., Rabsch W., Reissbrodt R., Williams P. H., 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. (2008) 298:429-439. (Pubitemid 351734795)
28. Moreira C. G., Weinshenker D., Sperandio V., QseC mediates Salmonella enteria serovar Typhimurium virulence in vitro and in vivo, Infect. Immun. (2010) 78:914-926.
29. Morgan I. R., Krautil F. L., Craven J. A., Effect of time in lairage on caecal and carcass Salmonella contamination of slaughter pigs, Epidemiol. Infect. (1987) 98:323-330.
30. Paulin S. M., Jagannathan A., Campbell J., Wallis T. S., Stevens M. P., Net replication of Salmonella enterica serovars Typhimurium and Choleraesuis in porcine intestinal mucosa and nodes is associated with their differential virulence, Infect. Immun. (2007) 75:3950-3960. (Pubitemid 47206293)
31. Pullinger G. D., Carnell S. C., Sharaff F. F., van Diemen P. M., Dziva F., Morgan E., et al., 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, Infect. Immun. (2010) 78:372-380.
32. Rasko D. A., Moreira C. G., Li de R., Reading N. C., Ritchie J. M., Waldor M. K., et al., Targeting QseC signaling and virulence for antibiotic development, Science (2008) 321:1078-1080.
33. Rasko D. A., Sperandio V., Anti-virulence strategies to combat bacteria-mediated disease, Nat. Rev. Drug Discov. (2010) 9:117-128.
34. Reading N. C., Rasko D. A., Torres A. G., Sperandio V., The two-component system QseEF and the membrane protein QseG link adrenergic and stress sensing to bacterial pathogenesis, Proc. Natl. Acad. Sci. USA (2009) 106:5889-5894.
35. Reissbrodt R., Rienaecker I., Romanova J. M., Freestone P. P., Haigh R. D., Lyte M., et al., Resuscitation of Salmonella enterica serovar Typhimurium and enterohemorrhagic Escherichia coli from the viable but nonculturable state by heat-stable enterobacterial autoinducer, Appl. Environ. Microbiol. (2002) 68:4788-4794. (Pubitemid 35154782)
36. Sandrini S. M., Shergill R., Woodward J., Muralikuttan R., Haigh R. D., Lyte M., Freestone P. P., Elucidation of the mechanism by which catecholamine stress hormones liberate iron from the innate immune defense proteins transferrin and lactoferrin, J. Bacteriol. (2010) 192:587-594.
37. Sekirov I., Tam N. M., Jogova M., Robertson M. L., Li Y., Lupp C., Finlay B. B., Antibiotic-induced perturbations of the intestinal microbiota alter host susceptibility to enteric infection, Infect. Immun. (2008) 76:4726-4736.
38. Spencer H., Karavolos M. H., Bulmer D. M., Aldridge P., Chhabra S. R., Winzer K., et al., Genome-wide transposon mutagenesis identifies a role for host neuroendocrine stress hormones in regulating the expression of virulence genes in Salmonella, J. Bacteriol. (2010) 192:714-724.
39. Stabel T. J., Evaluation of 2-deoxy-D-glucose for induction of a stress response in pigs, Am. J. Vet. Res. (1999) 60:708-713. (Pubitemid 129543845)
40. Stabel T. J., Fedorka-Cray P. J., Effect of 2-deoxy-D-glucose induced stress on Salmonella choleraesuis shedding and persistence in swine, Res. Vet. Sci. (2004) 76:187-194.
41. Stevens M. P., Modulation of the interaction of enteric bacteria with intestinal mucosa by stressrelated catecholamines, in: Lyte M., Freestone P. (Eds.), Microbial Endocrinology, Springer Press, London, 2010, pp. 111-134.
42. Thomas G. D., O'Hagan K. P., Zambraski E. J., Effects of 6-hydroxydopamine in hypertensive adult miniature swine, Clin. Exp. Hypertens. A (1990) 12:647-661.
43. Toscano M. J., Stabel T. J., Bearson S. M. D., Bearson B. L., Lay D. C., Cultivation of Salmonella enterica serovar Typhimurium in a norepinephrinecontaining medium alters in vivo tissue prevalence in swine, J. Exp. Anim. Sci. (2007) 43:329-338.
44. Vlisidou I., Lyte M., van Diemen P. M., Hawes P., Monaghan P., Wallis T. S., Stevens M. P., 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. (2004) 72:5446-5451. (Pubitemid 39223433)
45. Watson P. R., Paulin S. M., Jones P. W., Wallis T. S., Interaction of Salmonella serotypes with porcine macrophages in vitro does not correlate with virulence, Microbiology (2000) 146:1639-1649.
46. Williams P. H., Rabsch W., Methner U., Voigt W., Tschäpe H., Reissbrodt R., Catecholate receptor proteins in Salmonella enterica: role in virulence and implications for vaccine development, Vaccine (2006) 24:3840-3844.