Impact of Salmonella Typhimurium DT104 virulence factors invC and sseD on the onset, clinical course, colonization patterns and immune response of porcine salmonellosis

Veterinary Microbiology

Volumn 124, Issue 3-4, 2007, Pages 274-285

  Brumme, Steffi ^a,b   Arnold, Thorsten ^a   Sigmarsson, Haukur ^a   Lehmann, Jörg ^c   Scholz, Holger C ^a,d   Hardt, Wolf Dietrich ^e   Hensel, Andreas ^a,f   Truyen, Uwe ^a   Roesler, Uwe ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b Impfstoffwerk Dessau Tornau GmbH   (Germany)

^c FRAUNHOFER INSTITUTE FOR CELL THERAPY AND IMMUNOLOGY   (Germany)

^d Institute for Microbiology of the Armed Force   (Germany)

^e ETH ZURICH   (Switzerland)

^f FEDERAL INSTITUTE FOR RISK ASSESSMENT   (Germany)

Author keywords

Cytokines; ELISA; Immune response; invC; Pig; Real time PCR; Salmonella Typhimurium; Salmonellosis; sseD; Swine

Indexed keywords

COMPLEMENTARY DNA; CYTOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN M ANTIBODY; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 4; MESSENGER RNA; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CYTOKINE PRODUCTION; DISEASE COURSE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE DELETION; IMMUNE RESPONSE; INVC GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SEROLOGY; SSED GENE; SWINE DISEASE;

ANIMALS; ANTIBODY FORMATION; BACTERIAL PROTEINS; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FECES; GENE EXPRESSION REGULATION, BACTERIAL; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; IMMUNITY, CELLULAR; MALE; MEMBRANE PROTEINS; MUTATION; POLYMERASE CHAIN REACTION; PROTON-TRANSLOCATING ATPASES; RANDOM ALLOCATION; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; SWINE; SWINE DISEASES; VIRULENCE FACTORS;

SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM; SUIDAE; SUS;

EID: 34547937697     PISSN: 03781135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetmic.2007.04.032     Document Type: Article

References (36)

1. Akeda Y., and Galan J.E. Genetic analysis of the Salmonella enterica type III secretion-associated ATPase InvC defines discrete functional domains. J. Bacteriol. 186 (2004) 2402-2412
2. Alpuche-Aranda C.M., Berthiaume E.P., Mock B., Swanson J.A., and Miller S.I. Spacious phagosome formation within mouse macrophages correlates with Salmonella serotype pathogenicity and host susceptibility. Infect. Immun. 63 (1995) 4456-4462
3. Bao S., Beagley K.W., France M.P., Shen J., and Husband A.J. Interferon-gamma plays a critical role in intestinal immunity against Salmonella typhimurium infection. Immunology 99 (2000) 464-472
4. Barthel M., Hapfelmeier S., Quintanilla-Martinez L., Kremer M., Rohde M., Hogardt M., Pfeffer K., Russmann H., and Hardt W.D. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun. 71 (2003) 2839-2858
5. Boyen F., Pasmans F., van Immerseel F., Morgan E., Adriaensen C., Hernalsteens J.P., Decostere A., Ducatelle R., and Haesebrouck F. Salmonella Typhimurium SPI-1 genes promote intestinal but not tonsillar colonization in pigs. Microbes Infect. 8 (2006) 2899-2907
6. Bispham J., Tripathi B.N., Watson P.R., and Wallis T.S. Salmonella pathogenicity island 2 influences both systemic salmonellosis and Salmonella-induced enteritis in calves. Infect. Immun. 69 (2001) 367-377
7. Chakravortty D., Hansen-Wester I., and Hensel M. Salmonella pathogenicity island 2 mediates protection of intracellular Salmonella from reactive nitrogen intermediates. J. Exp. Med. 195 (2002) 1155-1166
8. Coombes B.K., Coburn B.A., Potter A.A., Gomis S., Mirakhur K., Li Y., and Finlay B.B. 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 (2005) 7161-7169
9. Eichelberg K., Ginocchio C.C., and Galan J.E. Molecular and functional characterization of the Salmonella typhimurium invasion genes invB and invC: homology of InvC to the F0F1 ATPase family of proteins. J. Bacteriol. 176 (1994) 4501-4510
10. Fedorka-Cray P.J., Kelley L.C., Stabel T.J., Gray J.T., and Laufer J.A. Alternate routes of invasion may affect pathogenesis of Salmonella typhimurium in swine. Infect. Immun. 63 (1995) 2658-2664
11. Fiorentino D.F., Zlotnik A., Mosmann T.R., Howard M., and Ogarra A. IL-10 inhibits cytokine production by activated macrophages. J. Immunol. 147 (1991) 3815-3822
12. Galan J.E. Interaction of Salmonella with host cells through the centisome 63 type III secretion system. Curr. Opin. Microbiol. 2 (1999) 46-50
13. Gallois A., Klein J.R., Allen L.A., Jones B.D., and Nauseef W.M. Salmonella pathogenicity island 2-encoded type III secretion system mediates exclusion of NADPH oxidase assembly from the phagosomal membrane. J. Immunol. 166 (2001) 5741-5748
14. Hapfelmeier S., Stecher B., Barthel M., Kremer M., Müller A.J., Heikenwalder M., Stallmach T., Hensel M., Pfeffer K., Akira S., and Hardt W.D. The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J. Immunol. 174 (2005) 1675-1685
15. Hassan J.O., and Curtiss R.I.I.I. Virulent Salmonella typhimurium-induced lymphocyte depletion and immunosuppression in chickens. Infect. Immun. 62 (1994) 2027-2036
16. Klein J.R., and Jones B.D. Salmonella pathogenicity island 2-encoded proteins SseC and SseD are essential for virulence and are substrates of the type III secretion system. Infect. Immun. 69 (2001) 737-743
17. Lehmann J., Bellmann S., Werner C., Schröder R., Schutze N., and Alber G. IL-12p40-dependent agonistic effects on the development of protective innate and adaptive immunity against Salmonella enteritidis. J. Immunol. 167 (2001) 5304-5315
18. Lehmann J., Springer S., Werner C.E., Lindner T., Bellmann S., Straubinger R.K., Selbitz H.J., and Alber G. Immunity induced with a Salmonella enterica serovar Enteritidis live vaccine is regulated by Th1-cell-dependent cellular and humoral effector mechanisms in susceptible BALB/c mice. Vaccine 24 (2006) 4779-4793
19. Lundberg U., Vinatzer U., Berdnik D., von Gabain A., and Baccarini M. Growth phase-regulated induction of Salmonella-induced macrophage apoptosis correlates with transient expression of SPI-1 genes. J. Bacteriol. 181 (1999) 3433-3437
20. Mastroeni P., Chabalgoity J.A., Dunstan S.J., Maskell D.J., and Dougan G. Salmonella: immune responses and vaccines. Vet. J. 161 (2001) 132-164
21. McGill R.J., Tukey J.W., and Larson W.A. Variations of Box Plots. Am. Statist. 32 (1978) 12-16
22. McSorley S.J., and Jenkins M.K. Antibody is required for protection against virulent but not attenuated Salmonella enterica serovar typhimurium. Infect. Immun. 68 (2000) 3344-3348
23. Medina E., Paglia P., Nikolaus T., Müller A., Hensel M., and Guzman C.A. Pathogenicity island 2 mutants of Salmonella typhimurium are efficient carriers for heterologous antigens and enable modulation of immune responses. Infect. Immun. 67 (1999) 1093-1099
24. Mittrucker H.W., Raupach B., Kohler A., and Kaufmann S.H. Cutting edge: role of B lymphocytes in protective immunity against Salmonella typhimurium infection. J. Immunol. 164 (2000) 1648-1652
25. Monack D.M., Detweiler C.S., and Falkow S. Salmonella pathogenicity island 2-dependent macrophage death is mediated in part by the host cysteine protease caspase-1. Cell Microbiol. 3 (2001) 825-837
26. Nikolaus T., Deiwick J., Rappl C., Freeman J.A., Schröder W., Miller S.I., and Hensel M. SseBCD proteins are secreted by the type III secretion system of Salmonella pathogenicity island 2 and function as a translocon. J. Bacteriol. 183 (2001) 6036-6045
27. Pfaffl M.W. A new mathematical model for relative quantification in real time RT-PCR. Nucleic Acids Res. 29 (2001) e45
28. Rathman M., Barker L.P., and Falkow S. The unique trafficking pattern of Salmonella typhimurium-containing phagosomes in murine macrophages is independent of the mechanism of bacterial entry. Infect. Immun. 65 (1997) 1475-1485
29. Roesler U., Marg H., Schröder I., Mauer S., Arnold T., Lehmann J., Truyen U., and Hensel A. Oral vaccination of pigs with an invasive gyrA-cpxA-rpoB Salmonella Typhimurium mutant. Vaccine 23 (2004) 595-603
30. Sadeyen J.R., Trotereau J., Velge P., Marly J., Beaumont C., Barrow P.A., Bumstead N., and Lalmanach A.C. Salmonella carrier state in chicken: comparison of expression of immune response genes between susceptible and resistant animals. Microbes Infect. 6 (2004) 1278-1286
31. Trebichavsky I., Splichal I., Splichalova A., Muneta Y., and Mori Y. Systemic and local cytokine response of young piglets to oral infection with Salmonella enterica serotype Typhimurium. Folia Microbiol. (Praha) 48 (2003) 403-407
32. Uchiya K., Groisman E.A., and 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. 72 (2004) 1964-1973
33. van der Velden A.W., Lindgren S.W., Worley M.J., and Heffron F. Salmonella pathogenicity island 1-independent induction of apoptosis in infected macrophages by Salmonella enterica serotype typhimurium. Infect. Immun. 68 (2000) 5702-5709
34. Wood R.L., Pospischil A., and Rose R. Distribution of persistent Salmonella typhimurium infection in internal organs of swine. Am. J. Vet. Res. 50 (1989) 1015-1021
35. Wright P.F., Nilson E., Van Rooij E.M.A., Lelenta M., and Jeggo M.H. Standardisation and validation of enzyme-linked-immunosorbent assay techniques for the detection of antibody in infectious disease diagnosis. Rev. Sci. Tech. Off. Int. Epiz. 12 (1993) 435-450
36. Zurawski D.V., and Stein M.A. SseA acts as the chaperone for the SseB component of the Salmonella Pathogenicity Island 2 translocon. Mol. Microbiol. 47 (2003) 1341-1351