Early immune dynamics following infection with Salmonella enterica serovars Enteritidis, Infantis, Pullorum and Gallinarum: Cytokine and chemokine gene expression profile and cellular changes of chicken cecal tonsils

Comparative Immunology, Microbiology and Infectious Diseases

Volumn 35, Issue 5, 2012, Pages 397-410

  Setta, A M ^a,c   Barrow, P A ^a   Kaiser, P ^b   Jones, M A ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c Cairo University   (Egypt)

Author keywords

Caecal tonsils; Chickens; Cytokines; Innate immunity; Salmonella

Indexed keywords

CHEMOKINE; CXCLI1 CHEMOKINE; CXCLI2 CHEMOKINE; CYTOKINE; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 6; LIPOPOLYSACCHARIDE INDUCED TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL STRUCTURES; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BACTERIAL COLONIZATION; BIRD DISEASE; CECAL TONSIL; CHICKEN; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; HATCHING; IMMUNE RESPONSE; MACROPHAGE; NONHUMAN; NUCLEOTIDE SEQUENCE; POULTRY; SALMONELLA ENTERICA; SALMONELLA ENTERITIDIS; SALMONELLA GALLINARUM; SALMONELLA INFANTIS; SALMONELLOSIS; SEROTYPE; STAINING; UPREGULATION;

ANIMALS; B-LYMPHOCYTES; BACTERIAL LOAD; CECUM; CHEMOKINE CXCL1; CHEMOKINE CXCL2; CHICKENS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-10; MACROPHAGES; NITRIC OXIDE SYNTHASE TYPE II; PALATINE TONSIL; POULTRY DISEASES; SALMONELLA ENTERICA; SALMONELLA INFECTIONS, ANIMAL; TRANSCRIPTOME;

ANIMALIA; AVES; GALLUS GALLUS; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERITIDIS;

EID: 84864149127     PISSN: 01479571     EISSN: 18781667     Source Type: Journal    
DOI: 10.1016/j.cimid.2012.03.004     Document Type: Article

References (63)

1. Brenner F.W., Villar R.G., Angulo F.J., Tauxe R., Swaminathan B. Salmonella nomenclature. J Clin Microbiol 2000, 38(7):2465-2467.
2. Uzzau S., Brown D.J., Wallis T., Rubino S., Leori G., Bernard S., et al. Host adapted serotypes of Salmonella enterica. Epidemiol Infect 2000, 125(2):229-255.
3. Barrow P.A. Salmonella infections: immune and non-immune protection with vaccines. Avian Pathol 2007, 36(1):1-13.
4. Shivaprasad H.L. Fowl typhoid and pullorum disease. Rev Sci Tech 2000, 19(2):405-424.
5. Lister S.A., Barrow P. Enterobacteriaceae. Poultry diseases 2008, Elsevier Ltd. 6th ed. M. Pattison, P. McMullin, J. Bradbury, D. Alexander (Eds.).
6. Shivaprasad H.L., Barrow P.A. Salmonella infections. Diseases of poultry 2008, Blackwell Publishing. Y.M. Saif, A.M. Fadly, J.R. Glisson, L.R. McDougald, L.K. Nolan, D.E. Swayne, Editorial Board for the AAAP (Eds.).
7. Barrow P.A., Simpson J.M., Lovell M.A. Intestinal colonisation in the chicken by food-poisoning Salmonella serotypes: microbial characteristics associated with faecal excretion. Avian Pathol 1988, 17(3):571-588.
8. McPherson M.E., Fielding J.E., Telfer B., Stephens N., Combs B.G., Rice B.A., et al. A multi-jurisdiction outbreak of Salmonella Typhimurium phage type 135 associated with purchasing chicken meat from a supermarket chain. Commun Dis Intell 2006, 30(4):449-455.
9. Noda T., Murakami K., Ishiguro Y., Asai T. Chicken meat is an infection source of Salmonella serovar Infantis for humans in Japan. Foodborne Pathog Dis 2010.
10. EFSA The European Union Summary Report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2009. EFSA J 2011, 9(3):2090.
11. Barrow P.A., Bumstead N., Marston K., Lovell M.A., Wigley P. Faecal shedding and intestinal colonization of Salmonella enterica in in-bred chickens: the effect of host-genetic background. Epidemiol Infect 2004, 132(1):117-126.
12. Barrow P.A., Hassan J.O., Lovell M.A., Berchieri A. Vaccination of chickens with aroA and other mutants of Salmonella typhimurium and S. enteritidis. Res Microbiol 1990, 141(7-8):851-853.
13. Cooper G.L., Venables L.M., Nicholas R.A., Cullen G.A., Hormaeche C.E. Further studies of the application of live Salmonella enteritidis aroA vaccines in chickens. Vet Rec 1993, 133(2):31-36.
14. Hassan J.O., Curtiss R. Efficacy of a live avirulent Salmonella typhimurium vaccine in preventing colonization and invasion of laying hens by Salmonella typhimurium and Salmonella enteritidis. Avian Dis 1997, 41(4):783-791.
15. Smith H.W. The use of live vaccines in experimental Salmonella gallinarum infection in chickens with observations on their interference effect. J Hyg (Lond) 1956, 54(3):419-432.
16. Barrow P.A., Lovell M.A., Berchieri A. The use of two live attenuated vaccines to immunize egg-laying hens against Salmonella enteritidis phage type 4. Avian Pathol 1991, 20(4):681-692.
17. Feberwee A., de Vries T.S., Hartman E.G., de Wit J.J., Elbers A.R., de Jong W.A. Vaccination against Salmonella enteritidis in Dutch commercial layer flocks with a vaccine based on a live Salmonella gallinarum 9R strain: evaluation of efficacy, safety, and performance of serologic Salmonella tests. Avian Dis 2001, 45(1):83-91.
18. Kaiser P. Advances in avian immunology-prospects for disease control: a review. Avian Pathol 2010, 39(5):309-324.
19. Parish C.R., O'Neill E.R. Dependence of the adaptive immune response on innate immunity: some questions answered but new paradoxes emerge. Immunol Cell Biol 1997, 75(6):523-527.
20. Shaughnessy R.G., Meade K.G., Cahalane S., Allan B., Reiman C., Callanan J.J., et al. Innate immune gene expression differentiates the early avian intestinal response between Salmonella and Campylobacter. Vet Immunol Immunopathol 2009, 132(2-4):191-198.
21. Swaggerty C.L., Pevzner I.Y., He H., Genovese K.J., Nisbet D.J., Kaiser P., et al. Selection of broilers with improved innate immune responsiveness to reduce on-farm infection by foodborne pathogens. Foodborne Pathog Dis 2009, 6(7):777-783.
22. Eckmann L., Kagnoff M.F. Cytokines in host defense against Salmonella. Microbes Infect 2001, 3(14-15):1191-1200.
23. Beal R.K., Powers C., Davison T.F., Barrow P.A., Smith A.L. Clearance of enteric Salmonella enterica serovar Typhimurium in chickens is independent of B-cell function. Infect Immun 2006, 74(2):1442-1444.
24. Kaiser P., Rothwell L., Galyov E.E., Barrow P.A., Burnside J., Wigley P. Differential cytokine expression in avian cells in response to invasion by Salmonella typhimurium, Salmonella enteritidis and Salmonella gallinarum. Microbiology 2000, 146(Pt 12):3217-3226.
25. Kaiser M.G., Cheeseman J.H., Kaiser P., Lamont S.J. Cytokine expression in chicken peripheral blood mononuclear cells after in vitro exposure to Salmonella enterica serovar Enteritidis. Poult Sci 2006, 85(11):1907-1911.
26. Li S., Zhang M.Z., Yan L., Lillehoj H., Pace L.W., Zhang S. Induction of CXC chemokine messenger-RNA expression in chicken oviduct epithelial cells by Salmonella enterica serovar enteritidis via the type three secretion system-1. Avian Dis 2009, 53(3):396-404.
27. Withanage G.S., Kaiser P., Wigley P., Powers C., Mastroeni P., Brooks H., et al. Rapid expression of chemokines and proinflammatory cytokines in newly hatched chickens infected with Salmonella enterica serovar typhimurium. Infect Immun 2004, 72(4):2152-2159.
28. Withanage G.S., Wigley P., Kaiser P., Mastroeni P., Brooks H., Powers C., et al. Cytokine and chemokine responses associated with clearance of a primary Salmonella enterica serovar Typhimurium infection in the chicken and in protective immunity to rechallenge. Infect Immun 2005, 73(8):5173-5182.
29. Berndt A., Wilhelm A., Jugert C., Pieper J., Sachse K., Methner U. Chicken cecum immune response to Salmonella enterica serovars of different levels of invasiveness. Infect Immun 2007, 75(12):5993-6007.
30. Carvajal B.G., Methner U., Pieper J., Berndt A. Effects of Salmonella enterica serovar Enteritidis on cellular recruitment and cytokine gene expression in caecum of vaccinated chickens. Vaccine 2008, 26(42):5423-5433.
31. Jepson M.A., Clark M.A. The role of M cells in Salmonella infection. Microbes Infect 2001, 3(14-15):1183-1190.
32. Barrow P.A., Lovell M.A., Stocker B.A. Protection against experimental fowl typhoid by parenteral administration of live SL5828, an aroA-serC (aromatic dependent) mutant of a wild-type Salmonella Gallinarum strain made lysogenic for P22 sie. Avian Pathol 2000, 29(5):423-431.
33. Thomson N.R., Clayton D.J., Windhorst D., Vernikos G., Davidson S., Churcher C., et al. Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res 2008, 18(10):1624-1637.
34. Berchieri A., Murphy C.K., Marston K., Barrow P.A. Observations on the persistence and vertical transmission of Salmonella enterica serovars Pullorum and Gallinarum in chickens: effect of bacterial and host genetic background. Avian Pathol 2001, 30(3):221-231.
35. Barrow P.A. Further observations on the effect of feeding diets containing avoparcin on the excretion of salmonellas by experimentally infected chickens. Epidemiol Infect 1989, 102(2):239-252.
36. Cheeseman J.H., Levy N.A., Kaiser P., Lillehoj H.S., Lamont S.J. Salmonella Enteritidis-induced alteration of inflammatory CXCL chemokine messenger-RNA expression and histologic changes in the ceca of infected chicks. Avian Dis 2008, 52(2):229-234.
37. Avery S., Rothwell L., Degen W.D., Schijns V.E., Young J., Kaufman J., et al. Characterization of the first nonmammalian T2 cytokine gene cluster: the cluster contains functional single-copy genes for IL-3, IL-4, IL-13, and GM-CSF, a gene for IL-5 that appears to be a pseudogene, and a gene encoding another cytokinelike transcript, KK34. J Interferon Cytokine Res 2004, 24(10):600-610.
38. Pfaffl M.W., Horgan G.W., Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30(9):pe36.
39. Haghighi H.R., Abdul-Careem M.F., Dara R.A., Chambers J.R., Sharif S. Cytokine gene expression in chicken cecal tonsils following treatment with probiotics and Salmonella infection. Vet Microbiol 2008, 126(1-3):225-233.
40. Stern N.J. Salmonella species and Campylobacter jejuni cecal colonization model in broilers. Poult Sci 2008, 87(11):2399-2403.
41. Methner U., Barrow P.A., Berndt A. Induction of a homologous and heterologous invasion-inhibition effect after administration of Salmonella strains to newly hatched chicks. Vaccine 2010, 28(43):6958-6963.
42. Van Immerseel F., De Buck J., De Smet I., Mast J., Haesebrouck F., Ducatelle R. Dynamics of immune cell infiltration in the caecal lamina propria of chickens after neonatal infection with a Salmonella enteritidis strain. Dev Comp Immunol 2002, 26(4):355-364.
43. Van Immerseel F., De Buck J., De Smet I., Mast J., Haesebrouck F., Ducatelle R. The effect of vaccination with a Salmonella enteritidis aroA mutant on early cellular responses in caecal lamina propria of newly-hatched chickens. Vaccine 2002, 20(23-24):3034-3041.
44. Berndt A., Methner U. B cell and macrophage response in chicks after oral administration of Salmonella typhimurium strains. Comp Immunol Microbiol Infect Dis 2004, 27(4):235-246.
45. Sasai K., Aita M., Lillehoj H.S., Miyamoto T., Fukata T., Baba E. Dynamics of lymphocyte subpopulation changes in the cecal tonsils of chickens infected with Salmonella enteritidis. Vet Microbiol 2000, 74(4):345-351.
46. Chappell L., Kaiser P., Barrow P., Jones M.A., Johnston C., Wigley P. The immunobiology of avian systemic salmonellosis. Vet Immunol Immunopathol 2009, 128(1-3):53-59.
47. Fasina Y.O., Holt P.S., Moran E.T., Moore R.W., Conner D.E., McKee S.R. Intestinal cytokine response of commercial source broiler chicks to Salmonella typhimurium infection. Poult Sci 2008, 87(7):1335-1346.
48. Hong Y.H., Lillehoj H.S., Dalloul R.A., Min W., Miska K.B., Tuo W., et al. Molecular cloning and characterization of chicken lipopolysaccharide-induced TNF-alpha factor (LITAF). Dev Comp Immunol 2006, 30(10):919-929.
49. Nauciel C., Espinasse-Maes F. Role of gamma interferon and tumor necrosis factor alpha in resistance to Salmonella typhimurium infection. Infect Immun 1992, 60(2):450-454.
50. Morrissey P.J., Charrier K., Vogel S.N. Exogenous tumor necrosis factor alpha and interleukin-1 alpha increase resistance to Salmonella typhimurium: efficacy is influenced by the Ity and Lps loci. Infect Immun 1995, 63(8):3196-3198.
51. Gulig P.A., Doyle T.J., Clare-Salzler M.J., Maiese R.L., Matsui H. Systemic infection of mice by wild-type but not Spv- Salmonella typhimurium is enhanced by neutralization of gamma interferon and tumor necrosis factor alpha. Infect Immun 1997, 65(12):5191-5197.
52. Royle M.C., Tötemeyer S., Alldridge L.C., Maskell D.J., Bryant C.E. Stimulation of Toll-like receptor 4 by lipopolysaccharide during cellular invasion by live Salmonella typhimurium is a critical but not exclusive event leading to macrophage responses. J Immunol 2003, 170(11):5445-5454.
53. Talbot S., Tötemeyer S., Yamamoto M., Akira S., Hughes K., Gray D., et al. Toll-like receptor 4 signalling through MyD88 is essential to control Salmonella enterica serovar typhimurium infection, but not for the initiation of bacterial clearance. Immunology 2009, 128(4):472-483.
54. Ma J., Zhang Y.G., Xia Y., Sun J. The inflammatory cytokine tumor necrosis factor modulates the expression of Salmonella typhimurium effector proteins. J Inflamm (Lond) 2010, 7:42.
55. Jones R.M., Wu H., Wentworth C., Luo L., Collier-Hyams L., Neish A.S. Salmonella AvrA coordinates suppression of host immune and apoptotic defenses via JNK pathway blockade. Cell Host Microbe 2008, 3(4):233-244.
56. Collier-Hyams L.S., Zeng H., Sun J., Tomlinson A.D., Bao Z.Q., Chen H., et al. Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-kappa B pathway. J Immunol 2002, 169(6):2846-2850.
57. Ye Z., Petrof E.O., Boone D., Claud E.C., Sun J. Salmonella effector AvrA regulation of colonic epithelial cell inflammation by deubiquitination. Am J Pathol 2007, 171(3):882-892.
58. Lu R., Wu S., Liu X., Xia Y., Zhang Y.G., Sun J. Chronic effects of a Salmonella type III secretion effector protein AvrA in vivo. PLoS One 2010, 5(5):pe10505.
59. Rosenberger C.M., Finlay B.B. Macrophages inhibit Salmonella typhimurium replication through MEK/ERK kinase and phagocyte NADPH oxidase activities. J Biol Chem 2002, 277(21):18753-18762.
60. Uchiya K., Groisman E.A., Nikai T. Involvement of Salmonella pathogenicity island 2 in the up-regulation of interleukin-10 expression in macrophages: role of protein kinase A signal pathway. Infect Immun 2004, 72(4):1964-1973.
61. Powell F.L., Rothwell L., Clarkson M.J., Kaiser P. The turkey, compared to the chicken, fails to mount an effective early immune response to Histomonas meleagridis in the gut. Parasite Immunol 2009, 31(6):312-327.
62. Beal R.K., Powers C., Wigley P., Barrow P.A., Smith A.L. Temporal dynamics of the cellular, humoral and cytokine responses in chickens during primary and secondary infection with Salmonella enterica serovar Typhimurium. Avian Pathol 2004, 33(1):25-33.
63. Eisenstein T.K. Implications of Salmonella-induced nitric oxide (NO) for host defense and vaccines: NO, an antimicrobial, antitumor, immunosuppressive and immunoregulatory molecule. Microbes Infect 2001, 3(14-15):1223-1231.