Morphologic and Molecular Characterization of Salmonella typhimurium Infection in Neonatal Calves

Veterinary Pathology

Volumn 39, Issue 2, 2002, Pages 200-215

  Santos, R L ^a   Zhang, S ^a   Tsolis, R M ^b   Baumler A J ^b   Adams, L G ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Cattle; chemokine; cytokine; intestine; Peyer's patches; Salmonella typhimurium; salmonellosis; scanning electron microscopy; transmission electron microscopy

Indexed keywords

AUTACOID; BACTERIAL RNA; CYTOKINE;

ANIMAL; ANIMAL DISEASE; ANIMAL SALMONELLOSIS; ARTICLE; CATTLE; CATTLE DISEASE; GENE EXPRESSION; GENETICS; ILEUM; IMMUNOLOGY; MALE; METABOLISM; MICROBIOLOGY; MICROVILLUS; NEUTROPHIL; NEWBORN; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALMONELLA TYPHIMURIUM; SCANNING ELECTRON MICROSCOPY; SCANNING TRANSMISSION ELECTRON MICROSCOPY; TIME; ULTRASTRUCTURE;

ANIMALS; ANIMALS, NEWBORN; CATTLE; CATTLE DISEASES; CYTOKINES; GENE EXPRESSION; ILEUM; INFLAMMATION MEDIATORS; MALE; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, SCANNING TRANSMISSION; MICROVILLI; NEUTROPHILS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, BACTERIAL; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; TIME FACTORS;

EID: 0036490345     PISSN: 03009858     EISSN: 15444221     Source Type: Journal    
DOI: 10.1354/vp.39-2-200     Document Type: Article

References (64)

1. Arondel J, Singer M, Matsukawa A, Zychlinsky A, Sansonetti PJ: Increased interleukin-1 (IL-1) and imbalance between IL-1 and IL-1 receptor antagonist during acute inflammation in experimental shigellosis. Infect Immun 67: 6056–6066, 1999
2. Bolton AJ, Osborne MP, Wallis TS, Stephen J: Interaction of Salmonella cholerasuis, Salmonella dublin and Salmonella typhimurium with porcine and bovine terminal ileum in vivo. Microbiology 145: 2431–2441, 1999
3. Brennan MA, Cookson BT: Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 38: 31–40, 2000
4. Caswell JL, Middleton DM, Gordon JR: Production and functional characterization of recombinant bovine interleukin-8 as a specific neutrophil activator and chemoattractant. Vet Immunol Immunopathol 67: 327–340, 1999
5. Chen LM, Kaniga K, Galán JE: Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol 21: 1101–1115, 1996
6. Cirillo DM, Valdivia RH, Monack DM, Falkow S: Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion and its role in intracellular survival. Mol Microbiol 30: 175–188, 1998
7. Clark MA, Jepson MA, Simmons NL, Hirst BH: Preferential interaction of Salmonella typhimurium with mouse Peyer's patch M cells. Res Microbiol 145: 543-552, 1994
8. Collazo CM, Galán JE: The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell. Mol Microbiol 24: 747–756, 1997
9. Darwin KH, Miller VL: Molecular basis of the interaction of Salmonella with the intestinal mucosa. Clin Microbiol Rev 12: 405–428, 1999
10. Dinarello CA: Proinflammatory cytokines. Chest 118: 503–508, 2000
11. Eckmann L, Kagnoff MF, Fierer J: Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect Immun 61: 4569–4574, 1993
12. Eckmann L, Smith JR, Housley MP, Dwinell MB, Kagnoff MF: Analysis by high density cDNA arrays of altered gene expression in human intestinal epithelial cells in response to infection with the invasive enteric bacteria Salmonella. J Biol Chem 275: 14084–14094, 2000
13. Everest P, Allen J, Papakonstantinopoulou A, Mastroeni P, Roberts M, Dougan G: Salmonella typhimurium infections in mice deficient in interleukin-4 production: role of IL-4 in infection-associated pathology. J Immunol 159: 1820–1827, 1997
14. Fields PI, Swanson RV, Haidaris CG, Heffron F: Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci USA 83: 5189–5193, 1986
15. Finlay BB, Falkow S: Salmonella interactions with polarized human intestinal caco-2 epithelial cells. J Infect Dis 162: 1096–1106, 1990
16. Francis CL, Starnbach MN, Falkow S: Morphological and cytoskeletal changes in epithelial cells occur immediately upon interaction with Salmonella typhimurium grown under low-oxygen conditions. Mol Microbiol 6: 3077–3087, 1992
17. Frost AJ, Bland AP, Wallis TS: The early dynamic response of the calf ileal epithelium to Salmonella typhimurium. Vet Pathol 34: 369–386, 1997
18. Galán JE: Interaction of Salmonella with host cells through the centisome 63 type III secretion system. Curr Opin Microbiol 2: 46–50, 1999
19. Galán JE, Curtiss R: Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci USA 86: 6383–6387, 1989
20. Gewirtz AT, Rao AS, Simon PO Jr, Merlin D, Carnes D, Madara JL, Neish AS: Salmonella typhimurium induces epithelial IL-8 expression via Ca2+-mediated activation of the NF-κB pathway. J Clin Invest 105: 79–91, 2000
21. Gewirtz AT, Siber AM, Madara JL, McCormick BA: Orchestration of neutrophil movement by intestinal epithelial cells in response to Salmonella typhimurium can be uncoupled from bacterial internalization. Infect Immun 67: 608–617, 1999
22. Ghayur T, Banerjee S, Hugunin M, Butler D, Herzog L, Carter A, Quintal L, Sekut L, Talanian R, Paskind M, Wong W, Kamen R, Tracey D, Allen H: Caspase-1 processes IFN-gamma-inducing factor and regulates LPSinduced IFN-γ production. Nature 386: 619–623, 1997
23. Gianella RA: Importance of the intestinal inflammatory reaction in Salmonella-mediated intestinal secretion. Infect Immun 23: 140–145, 1979
24. Groisman EA, Ochman H: How Salmonella became a pathogen. Trends Microbiol 5: 343–349, 1997
25. Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, Zychlinsky A: The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci USA 96: 2396–2401, 1999
26. Hobbie S, Chen LM, Davis RJ, Galán JE: Involvement of mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal epithelial cells. J Immunol 159: 5550–5559, 1997
27. Hughes LE, Gibson EA, Roberts HE, Davies ET, Davies G, Sojka WJ: Bovine salmonellosis in England and Wales. Br Vet J 127: 225–38, 1971
28. Jones BD, Ghori N, Falkow S: Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med 180: 15–23, 1994
29. Keane MP, Strieter RM: Chemokine signaling in inflammation. Crit Care Med 28(Suppl):N13–N26, 2000
30. Klimpel GR, Asuncion M, Haithcoat J, Niesel DW: Cholera toxin and Salmonella typhimurium induce different cytokine profiles in the gastrointestinal tract. Infect Immun 63: 1134–1137, 1995
31. Kutukculer N, Cagalayan S: Tumor necrosis factor-α and interleukin-6 in stools of children with bacterial and viral gastroenteritis. J Pediatr Gastroenterol Nutr 25: 556–557, 1997
32. Lee CA, Silva M, Siber AM, Kelly AJ, Galyov E, Mc-Cormick BA: A secreted Salmonella protein induces a proinflammatory response in epithelial cells, which promotes neutrophil migration. Proc Natl Acad Sci USA 97: 12283–12288, 2000
33. Lindgren SW, Stojiljkovic I, Heffron F: Macrophage killing is an essential virulence mechanism of Salmonella typhimurium. Proc Natl Acad Sci USA 93: 4197–4201, 1996
34. Mastroeni P, Clare S, Khan S, Harrison JA, Hormaeche CE, Okamura H, Kurimoto M, Dougan G: Interleukin 18 contributes to host resistance and gamma interferon production in mice infected with virulent Salmonella typhimurium. Infect Immun 67: 478–483, 1999
35. McCormick BA, Parkos CA, Colgan SP, Carnes DK, Madara JL: Apical secretion of a pathogen-elicited epithelial chemoattractant activity in response to surface colonization of intestinal epithelia by Salmonella typhimurium. J Immunol 160: 455–466, 1998
36. Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, Griffin PM, Tauxe RV: Food-related illness and death in the United States. Emerg Infect Dis 5: 607–625, 1999
37. Monack DM, Raupach B, Hromockyj AE, Falkow S: Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci USA 93: 9833–9838, 1996
38. Neish AS, Gewirtz AT, Zeng H, Young AN, Hobert ME, Karmali V, Rao AS, Madara JL: Prokaryotic regulation of epithelial responses by inhibition of IkB-alpha ubiquitination. Science 289: 1560–1563, 2000
39. Netea MG, Fantuzzi G, Kullberg BJ, Stuyt RJL, Pulido EJ, McIntyre RC, Joosten LAB, Van der Meer JWM, Dinarello CA: Neutralization of IL-18 reduces neutrophil tissue accumulation and protects mice against lethal Escherichia coli and Salmonella typhimurium endotoxemia. J Immun 164: 2644–2649, 2000
40. Ochman H, Soncini FC, Solomon F, Groisman EA: Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci USA 93: 7800–7804, 1996
41. Opal SM, DePalo VA: Anti-inflammatory cytokines. Chest 117: 1162–1172, 2000.
42. Pace J, Hayman MJ, Galán JE: Signal transduction and invasion of epithelial cells by S. typhimurium. Cell 72: 505–514, 1993
43. Parsons KR, Bland AP, Hall GA: Follicle associated epithelium of the gut associated lymphoid tissue of cattle. Vet Pathol 28: 22–29, 1991
44. Peel JE, Voirol MJ, Kolly C, Gobet D, Martinod S: Induction of circulating tumor necrosis factor cannot be demonstrated during septicemic salmonellosis in calves. Infect Immun 58: 439–442, 1990
45. Petrie L, Selman IE, Grindlay M, Thompson H: Salmonellosis in young calves due to Salmonella enteritidis. Vet Rec 101: 398–402, 1977
46. Richardson A: Outbreaks of bovine salmonellosis caused by serotypes other than S. dublin and S. typhimurium. J Hyg (Lond) 74: 195–203, 1975
47. Rings DM: Salmonellosis in calves. Vet Clin North Am Food Anim Pract 1: 529–539, 1985
48. Ruschkowski S, Rosenshine I, Finlay BB: Salmonella typhimurium induces an inositol phosphate flux in infected epithelial cells. FEMS Microbiol Lett 95: 121–126, 1992
49. Santos RL, Tsolis RM, Bäumler AJ, Smith R III, Adams LG: Salmonella enterica serovar Typhimurium induces cell death in bovine monocyte-derived macrophages by an early sipB-dependent and a delayed sipB-independent mechanism. Infect Immun 69: 2293–2301, 2001
50. Santos RL, Tsolis RM, Zhang S, Ficht TA, Bäumler AJ, Adams LG: Salmonella-induced cell death is not required for enteritis in calves. Infect Immun 69: 4610–4617, 2001
51. Santos RL, Zhang S, Tsolis RM, Kingsley RA, Adams LG, Bäumler AJ: Animal models of Salmonella infections: gastroenteritis vs. typhoid fever. Microbes Infect (in press)
52. Shea JE, Hensel M, Gleeson C, Holden DW: Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc Natl Acad Sci USA 93: 2593–2597, 1996
53. Sojka WJ, Wray C: Incidence of Salmonella infection in animals in England and Wales, 1968-73. Vet Rec 96: 280–284, 1975
54. Stojiljkovic I, Bäumler AJ, Heffron F: Ethanolamine utilization in Salmonella typhimurium: nucleotide sequence, protein expression, and mutational analysis of the cchA cchB eutE eutJ eutG eutH gene cluster. J Bacteriol 177: 1357–1366, 1995
55. Takeuchi A: Electron microscope studies of experimental Salmonella infection. Am J Pathol 50: 109–136, 1966
56. Tsolis RM, Adams LG, Ficht TA, Bäumler AJ: Contribution of Salmonella typhimurium virulence factors to diarrheal disease in calves. Infect Immun 67: 4879–4885, 1999
57. Tsolis RM, Kingsley RA, Townsend SM, Ficht TA, Adams LG, Bäumler AJ: Of mice, calves, and man. Comparison of the mouse typhoid model with other Salmonella infections. Adv Exp Med Biol 473: 261–274, 1999
58. Tsolis RM, Townsend SM, Miao EA, Miller SI, Ficht TA, Adams LG, Bäumler AJ: Identification of a putative Salmonella enterica serotype Typhimurium host range factor with homology to IpaH and YopM by Signaturetagged mutagenesis. Infect Immun 67: 6385–6393, 1999
59. Wallis TS, Galyov EE: Molecular basis of Salmonellainduced enteritis. Mol Microbiol 36: 997–1005, 2000
60. Watson PR, Gautier AV, Paulin SM, Bland AP, Jones PW, Wallis TS: Salmonella enterica serovars Typhimurium and Dublin can lyse macrophages by a mechanism distinct from apoptosis. Infect Immun 68: 3744–3747, 2000
61. Wells S, Fedorka-Cray PJ, Besser T, McDonough P, Smith B: E. coli O157 and Salmonella-Status on U.S. Dairy Operations. National Animal Health Monitoring System, US Department of Agriculture, Washington, DC, 1998
62. Wood MW, Jones MA, Watson PR, Hedges S, Wallis TS, Galyov EE: Identification of a pathogenicity island required for Salmonella enteropathogenicity. Mol Microbiol 29: 883–891, 1998
63. Wray C, Sojka WJ: Experimental Salmonella typhimurium infection in calves. Res Vet Sci 25: 139–143, 1978
64. Yang SK, Eckman L, Panja A, Kagnoff MP: Differential and regulated expression of C-X-C, C-C, and C-chemokines by human colon epithelial cells. Gastroenterology 113: 1214–1223, 1997