Survival of Salmonella serovar Typhimurium inside porcine monocytes is associated with complement binding and suppression of the production of reactive oxygen species

Veterinary Microbiology

Volumn 107, Issue 3-4, 2005, Pages 205-214

  Donne E ^a   Pasmans, F ^a   Boyen, F ^a   Van Immerseel, F ^a   Adriaensen, C ^b   Hernalsteens, J P ^b   Ducatelle, R ^a   Haesebrouck, F ^a  

^a GHENT UNIVERSITY   (Belgium)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

Carrier; Monocyte; Pig; Reactive oxygen species; Salmonella Typhimurium

Indexed keywords

BACTERIAL ENZYME; DIPHENYLIODONIUM SALT; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ARTICLE; BACTERIAL IMMUNITY; BACTERIAL INFECTION; BACTERIAL METABOLISM; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; CELL DAMAGE; COMPLEMENT FIXATION; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; MONOCYTE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPSONIZATION; PATHOGENICITY ISLAND; PROTEIN SYNTHESIS; RESPIRATORY BURST; SALMONELLA PATHOGENICITY ISLAND 1; SALMONELLA PATHOGENICITY ISLAND 2; SALMONELLA TYPHIMURIUM; SEROTYPE; SWINE;

BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA TYPHIMURIUM; SUIDAE; SUS SCROFA; TYPHIMURIUM;

EID: 18044399150     PISSN: 03781135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetmic.2005.01.027     Document Type: Article

References (39)

1. C.M. Alpuche-Aranda, E.L. Racoosin, J.A. Swanson, and S.I. Miller Salmonella stimulate macrophage macropinocytosis and persist within spacious phagosomes J. Exp. Med. 179 1994 601 608
2. B. Alvarez, C. Sanchez, R. Bullido, A. Marina, J. Lunney, F. Alonso, A. Ezquerra, and J. Dominguez A porcine cell surface receptor identified by monoclonal antibodies to SWC3 is a member of the signal regulatory protein family and associates with protein-tyrosine phosphatase SHP-1 Tissue Antigens 55 2000 342 351
3. P.A. Barrow, M.B. Huggins, and M.A. Lovell Host specificity of Salmonella infection in chickens and mice is expressed in vivo primarily at the level of the reticuloendothelial system Infect. Immun. 62 1994 4602 4610
4. M.A. Brennan, and B.T. Cookson Salmonella induces macrophage death by caspase-1-dependent necrosis Mol. Microbiol. 38 2000 31 40
5. N.A. Buchmeier, and F. Heffron Intracellular survival of wild-type Salmonella Typhimurium and macrophage-sensitive mutants in diverse populations of macrophages Infect. Immun. 57 1989 1 7
6. N.A. Buchmeier, C.J. Lipps, M.Y. So, and F. Heffron Recombination- deficient mutants of Salmonella Typhimurium are avirulent and sensitive to the oxidative burst of macrophages Mol. Microbiol. 7 1993 933 936
7. J. Canvin, P.R. Langford, K.E. Wilks, and J.S. Kroll Identification of sodC encoding periplasmic (Cu,Zn)-superoxide dismutase in Salmonella FEMS Microbiol. Lett. 136 1996 215 220
8. L.M. Chen, K. Kaniga, and J.E. Galan Salmonella spp. are cytotoxic for cultured macrophages Mol. Microbiol. 21 1996 1101 1115
9. K.A. Datsenko, and B.L. Wanner One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products Proc. Natl. Acad. Sci. U.S.A. 97 2000 6640 6645
10. M.A. De Groote, U.A. Ochsner, M.U. Shiloh, C. Nathan, J.M. McCord, M.C. Dinauer, S.J. Libby, A. Vazquez-Torres, Y. Xu, and F.C. Fang Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase Proc. Natl. Acad. Sci. U.S.A. 94 1997 13997 14001
11. Ducoffre, G., January 2003. Surveillance of infectious diseases by a network of laboratory of microbiology 2001. Epidemiologic Trends 1983-2000, Scientific Institute of Public Health, Epidemiology Unit, available online: http://www.iph.fgov.be/epidemio/epien/index0000.htm.
12. N.E. Dunlap Jr., W.H. Benjamin Jr., R.D. McCall, A.B. Tilden, and D.E. Briles A 'safe-site' for Salmonella Typhimurium is within splenic cells during the early phase of infection in mice Microb. Pathog. 10 1991 297 310
13. P.I. Fields, R.V. Swanson, C.G. Haidaris, and F. Heffron Mutants of Salmonella Typhimurium that cannot survive within the macrophage are avirulent Proc. Natl. Acad. Sci. U.S.A. 83 1986 5189 5193
14. B.B. Finlay, and S. Falkow Salmonella as an intracellular parasite Mol. Microbiol. 3 1989 1833 1841
15. J.E. Galán Salmonella interactions with host cells: type III secretion at work Annu. Rev. Cell. Dev. Biol. 17 2001 53 86
16. E.A. Groisman, C. Parralopez, M. Salcedo, C.J. Lipps, and F. Heffron Resistance to host antimicrobial peptides is necessary for Salmonella virulence Proc. Natl. Acad. Sci. U.S.A. 89 1992 11939 11943
17. M. Hensel Salmonella pathogenicity island 2 Mol. Microbiol. 36 2000 1015 1023
18. Y. Ishibashi, and T. Arai A possible mechanism for host-specific pathogenesis of Salmonella serovars Microb. Pathog. 21 1996 435 446
19. L.A. Knodler, and O. Steele-Mortimer Taking possession: biogenesis of the Salmonella-containing vacuole Traffic 4 2003 587 599
20. K.Y. Leung, and B.B. Finlay Intracellular replication is essential for the virulence of Salmonella Typhimurium Proc. Natl. Acad. Sci. U.S.A. 88 1991 11470 11474
21. Y. Li, and M.A. Trush Diphenyleneiodonium, an NAD(P)H oxidase inhibitor, also potently inhibits mitochondrial reactive oxygen species production Biochem. Biophys. Res. Commun. 253 1998 295 299
22. S.W. Lindgren, I. Stojiljkovic, and F. Heffron Macrophage killing is an essential virulence mechanism of Salmonella Typhimurium Proc. Natl. Acad. Sci. U.S.A. 93 1996 4197 4201
23. B.E. Lundberg, R.E. Wolf, M.C. Dinauer, Y.S. Xu, and F.C. Fang Glucose 6-phosphate dehydrogenase is required for Salmonella Typhimurium virulence and resistance to reactive oxygen and nitrogen intermediates Infect. Immun. 67 1999 436 438
24. P. Mastroeni, A. Vazquez-Torres, F.C. Fang, Y. Xu, S. Khan, C.E. Hormaeche, and G. Dougan Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. Part II: effects on microbial proliferation and host survival in vivo J. Exp. Med. 192 2000 237 248
25. M.S. Pampusch, A.M. Bennaars, S. Harsch, and M.P. Murtaugh Inducible nitric oxide synthase expression in porcine immune cells Vet. Immunol. Immunopathol. 61 1998 279 289
26. M.D. Pescovitz, J.K. Lunney, and D.H. Sachs Preparation and characterization of monoclonal antibodies reactive with porcine PBL J. Immunol. 133 1984 368 375
27. U. Riber, and P. Lind Interaction between Salmonella Typhimurium and phagocytic cells in pigs: phagocytosis, oxidative burst and killing in polymorphonuclear leukocytes and monocytes Vet. Immunol. Immunopathol. 67 1999 259 270
28. H. Schmieger, and H. Backhaus Altered cotransduction frequencies exhibited by HT-mutants of Salmonella-phage P22 Mol. Gen. Genet. 143 1976 307 309
29. A.S. Tan, and M.V. Berridge Superoxide produced by activated neutrophils efficiently reduces the tetrazolium salt, WST-1 to produce a soluble formazan: a simple colorimetric assay for measuring respiratory burst activation and for screening anti-inflammatory agents J. Immunol. Methods 238 2000 59 68
30. E. Thacker, A. Summerfield, K. McCullough, A. Ezquerra, J. Dominguez, F. Alonso, J. Lunney, J. Sinkora, and K. Haverson Summary of workshop findings for porcine myelomonocytic markers Vet. Immunol. Immunopathol. 80 2001 93 109
31. A.W.M. Van der Velden, S.W. Lindgren, M.J. Worley, and F. Heffron Salmonella pathogenicity island 1-independent induction of apoptosis in infected macrophages by Salmonella enterica serotype Typhimurium Infect. Immun. 68 2000 5702 5709
32. A. Vazquez-Torres, and F.C. Fang Oxygen-dependent anti-Salmonella activity of macrophages Trends Microbiol. 9 2001 29 33
33. A. Vazquez-Torres, J. Jones-Carson, P. Mastroeni, H. Ischiropoulos, and F.C. Fang Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. Part I: effects on microbial killing by activated peritoneal macrophages in vitro J. Exp. Med. 192 2000 227 236
34. A. Vazquez-Torres, Y.S. Xu, C.J. Jones, D.W. Holden, S.M. Lucia, M.C. Dinauer, P. Mastroeni, and F.C. Fang Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase Science 287 2000 1655 1658
35. I.R. Vladoianu, H.R. Chang, and J.C. Pechere Expression of host resistance to Salmonella typhi and Salmonella Typhimurium: bacterial survival within macrophages of murine and human origin Microb. Pathog. 8 1990 83 90
36. P.R. Watson, A.V. Gautier, S.M. Paulin, A.P. Bland, P.W. Jones, and T.S. Wallis Salmonella enterica serovars Typhimurium and Dublin can lyse macrophages by a mechanism distinct from apoptosis Infect. Immun. 68 2000 3744 3747
37. R.L. Wood, A. Pospischil, and R. Rose Distribution of persistent Salmonella Typhimurium infection in internal organs of swine Am. J. Vet. Res. 50 1989 1015 1021
38. X. Zhou, N. Mantis, X.R. Zhang, D.A. Potoka, S.C. Watkins, and H.R. Ford Salmonella Typhimurium induces apoptosis in human monocyte-derived macrophages Microbiol. Immunol. 44 2000 987 998
39. A. Zychlinsky, C. Fitting, J.M. Cavaillon, and P.J. Sansonetti Interleukin 1 is released by murine macrophages during apoptosis induced by Shigella flexneri J. Clin. Invest. 94 1994 1328 1332