Salmonella transiently reside in luminal neutrophils in the inflamed gut

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Loetscher, Yvonne ^a   Wieser, Andreas ^b   Lengefeld, Jette ^a   Kaiser, Patrick ^a   Schubert, Sören ^b   Heikenwalder, Mathias ^c   Hardt, Wolf Dietrich ^a   Stecher, Bärbel ^a,b  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF MUNICH   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD18 ANTIGEN; GENTAMICIN; SIDEROPHORE; BACTERIAL PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; CELL INTERACTION; CELL SURVIVAL; CELL VIABILITY; COLITIS; COMMENSAL; CONTROLLED STUDY; GENE EXPRESSION SYSTEM; HOST PATHOGEN INTERACTION; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN EXPRESSION; SALMONELLA ENTERICA; SEROTYPE; TYPE III SECRETION SYSTEM; UPREGULATION; ANIMAL; CELL MOTION; DISEASE MODEL; DRUG EFFECT; GENETICS; GENOMIC ISLAND; HUMAN; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; NEUTROPHIL; PATHOLOGY; PHAGOCYTOSIS; PHYSIOLOGY; PLASMID; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; TIME LAPSE IMAGING;

SALMONELLA; SALMONELLA ENTERICA;

ANIMALS; BACTERIAL PROTEINS; CELL MOVEMENT; COLITIS; DISEASE MODELS, ANIMAL; GENOMIC ISLANDS; GENTAMICINS; HUMANS; INTESTINAL MUCOSA; MICE; NEUTROPHIL INFILTRATION; NEUTROPHILS; PHAGOCYTOSIS; PLASMIDS; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; TIME-LAPSE IMAGING;

EID: 84859508514     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034812     Document Type: Article

References (40)

1. Day DW, Mandal BK, Morson BC, (1978) The rectal biopsy appearances in Salmonella colitis. Histopathology 2: 117-131.
2. McGovern VJ, Slavutin LJ, (1979) Pathology of salmonella colitis. Am J Surg Pathol 3: 483-490.
3. Sachdev HP, Chadha V, Malhotra V, Verghese A, Puri RK, (1993) Rectal histopathology in endemic Shigella and Salmonella diarrhea. J Pediatr Gastroenterol Nutr 16: 33-38.
4. Boyd JF, (1985) Pathology of the alimentary tract in Salmonella typhimurium food poisoning. Gut 26: 935-944.
5. Barthel M, Hapfelmeier S, Quintanilla-Martinez L, Kremer M, Rohde M, et al. (2003) Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun 71: 2839-2858.
6. Hapfelmeier S, Hardt WD, (2005) A mouse model for S. typhimurium-induced enterocolitis. Trends Microbiol.
7. Santos RL, Zhang S, Tsolis RM, Kingsley RA, Adams LG, et al. (2001) Animal models of Salmonella infections: enteritis versus typhoid fever. Microbes Infect 3: 1335-1344.
8. Stecher B, Paesold G, Barthel M, Kremer M, Jantsch J, et al. (2006) Chronic Salmonella enterica Serovar Typhimurium-Induced Colitis and Cholangitis in Streptomycin-Pretreated Nramp1+/+ Mice. Infect Immun 74: 5047-5057.
9. Vijay-Kumar M, Wu H, Jones R, Grant G, Babbin B, et al. (2006) Flagellin suppresses epithelial apoptosis and limits disease during enteric infection. Am J Pathol 169: 1686-1700.
10. Stecher B, Hardt WD, (2008) The role of microbiota in infectious disease. Trends Microbiol 16: 107-114.
11. Santos RL, Raffatellu M, Bevins CL, Adams LG, Tukel C, et al. (2009) Life in the inflamed intestine, Salmonella style. Trends Microbiol 17: 498-506.
12. van der Waaij D, Berghuis-de Vries JM, Lekkerkerk L-V, (1971) Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J Hyg (Lond) 69: 405-411.
13. Stecher B, Hardt WD, (2010) Mechanisms controlling pathogen colonization of the gut. Curr Opin Microbiol.
14. Stecher B, Robbiani R, Walker AW, Westendorf AM, Barthel M, et al. (2007) Salmonella enterica Serovar Typhimurium Exploits Inflammation to Compete with the Intestinal Microbiota. PLoS Biol 5: e244.
15. Barman M, Unold D, Shifley K, Amir E, Hung K, et al. (2008) Enteric salmonellosis disrupts the microbial ecology of the murine gastrointestinal tract. Infect Immun 76: 907-915.
16. Lupp C, Robertson ML, Wickham ME, Sekirov I, Champion OL, et al. (2007) Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of enterobacteriaceae. Cell, host and microbe 2: 119-129.
17. Lawley TD, Clare S, Walker AW, Goulding D, Stabler RA, et al. (2009) Antibiotic treatment of Clostridium difficile carrier mice triggers a supershedder state, spore-mediated transmission, and severe disease in immunocompromised hosts. Infect Immun.
18. Stecher B, Hapfelmeier S, Muller C, Kremer M, Stallmach T, et al. (2004) Flagella and Chemotaxis Are Required for Efficient Induction of Salmonella enterica Serovar Typhimurium Colitis in Streptomycin-Pretreated Mice. Infect Immun 72: 4138-4150.
19. Stecher B, Barthel M, Schlumberger MC, Haberli L, Rabsch W, et al. (2008) Motility allows S. Typhimurium to benefit from the mucosal defence. Cell Microbiol 10: 1166-1180.
20. Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, et al. (2010) Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467: 426-429.
21. Baumler AJ, Tsolis RM, van der Velden AW, Stojiljkovic I, Anic S, et al. (1996) Identification of a new iron regulated locus of Salmonella typhi. Gene 183: 207-213.
22. Raffatellu M, George MD, Akiyama Y, Hornsby MJ, Nuccio SP, et al. (2009) Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 5: 476-486.
23. Stelter C, Kappeli R, Konig C, Krah A, Hardt WD, et al. (2011) Salmonella-Induced Mucosal Lectin RegIIIbeta Kills Competing Gut Microbiota. PLoS ONE 6: e20749.
24. Faust N, Varas F, Kelly LM, Heck S, Graf T, (2000) Insertion of enhanced green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages. Blood 96: 719-726.
25. Hapfelmeier S, Ehrbar K, Stecher B, Barthel M, Kremer M, et al. (2004) Role of the Salmonella Pathogenicity Island 1 Effector Proteins SipA, SopB, SopE, and SopE2 in Salmonella enterica Subspecies 1 Serovar Typhimurium Colitis in Streptomycin-Pretreated Mice. Infect Immun 72: 795-809.
26. Wieser A, Guggenberger C, Pritsch M, Heesemann J, Schubert S, (2011) A novel ex vivo set-up for dynamic long-term characterization of processes on mucosal interfaces by confocal imaging and simultaneous cytokine measurements. Cell Microbiol 13: 742-751.
27. Bongaerts RJ, Hautefort I, Sidebotham JM, Hinton JC, (2002) Green fluorescent protein as a marker for conditional gene expression in bacterial cells. Methods Enzymol 358: 43-66.
28. Hapfelmeier S, Stecher B, Barthel M, Kremer M, Müller A, et al. (2005) The Salmonella Pathogenicity Island (SPI)-1 and SPI-2 Type III Secretion Systems Allow Salmonella Serovar Typhimurium to trigger Colitis via MyD88-Dependent and MyD88-Independent Mechanisms. J Immunol 174: 1675-1685.
29. Rollenhagen C, Bumann D, (2006) Salmonella enterica highly expressed genes are disease specific. Infect Immun 74: 1649-1660.
30. Kjeldsen L, Bainton DF, Sengelov H, Borregaard N, (1994) Identification of neutrophil gelatinase-associated lipocalin as a novel matrix protein of specific granules in human neutrophils. Blood 83: 799-807.
31. Taylor CM, Osman D, Cavet JS, (2009) Differential expression from two iron-responsive promoters in Salmonella enterica serovar Typhimurium reveals the presence of iron in macrophage-phagosomes. Microb Pathog 46: 114-118.
32. Geddes K, Cruz F, Heffron F, (2007) Analysis of cells targeted by Salmonella type III secretion in vivo. PLoS Pathog 3: e196.
33. Pillay J, den Braber I, Vrisekoop N, Kwast LM, de Boer RJ, et al. (2010) In vivo labeling with 2H2O reveals a human neutrophil lifespan of 5.4 days. Blood 116: 625-627.
34. Luo Y, Dorf ME, (1997) Isolation of Mouse Neutrophils. Current Protocols in Immunology pp. 3.20.21-23.20.26.
35. Sekirov I, Gill N, Jogova M, Tam N, Robertson M, et al. (2010) Salmonella SPI-1-mediated neutrophil recruitment during enteric colitis is associated with reduction and alteration in intestinal microbiota. Gut Microbes 1: 30-41.
36. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, et al. (2004) Neutrophil extracellular traps kill bacteria. Science 303: 1532-1535.
37. Segal AW, (2005) How neutrophils kill microbes. Annu Rev Immunol 23: 197-223.
38. Bachman MA, Miller VL, Weiser JN, (2009) Mucosal lipocalin 2 has pro-inflammatory and iron-sequestering effects in response to bacterial enterobactin. PLoS Pathog 5: e1000622.
39. Hoiseth SK, Stocker BA, (1981) Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291: 238-239.
40. Jones PW, Collins P, Aitken MM, (1988) Passive protection of calves against experimental infection with Salmonella typhimurium. Vet Rec 123: 536-541.