Toll-like receptor 4 contributes to colitis development but not to host defense during Citrobacter rodentium infection in mice

Infection and Immunity

Volumn 74, Issue 5, 2006, Pages 2522-2536

  Khan, Mohammed A ^a   Ma, Caixia ^a   Knodler, Leigh A ^b,d   Valdez, Yanet ^a,b   Rosenberger, Carrie M ^c   Deng, Wanyin ^b   Finlay, B Brett ^b   Vallance, Bruce A ^a  

^a BC CHILDREN S HOSPITAL   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CHEMOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MACROPHAGE INFLAMMATORY PROTEIN 2; MONOCYTE CHEMOTACTIC PROTEIN 1; TOLL LIKE RECEPTOR 4; VIRULENCE FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIUM ADHERENCE; CITROBACTER RODENTIUM; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIARRHEA; DISEASE DURATION; ENTERITIS; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; EPITHELIUM HYPERPLASIA; GASTROINTESTINAL TRACT; GRAM NEGATIVE BACTERIUM; HOST RESISTANCE; INFLAMMATION; INTESTINE EPITHELIUM; MACROPHAGE MIGRATION; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SPECIES DIFFERENCE;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CECUM; CHEMOKINES; CITROBACTER RODENTIUM; COLITIS; COLON; DIARRHEA; ENTEROBACTERIACEAE INFECTIONS; HUMANS; LIPOPOLYSACCHARIDES; LYMPH NODES; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; NF-KAPPA B; PROTEIN TRANSPORT; RNA, MESSENGER; TOLL-LIKE RECEPTOR 4; WEIGHT LOSS;

EID: 33646374141     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.74.5.2522-2536.2006     Document Type: Article

References (58)

1. Abe, A., U. Heczko, R. G. Hegele, and B. B. Finlay. Two enteropathogenic Escherichia coli type III secreted proteins, EspA and EspB, are virulence factors. J. Exp. Med. 188:1-10.
2. Akashi, S., R. Shimazu, H. Ogata, Y. Nagai, K. Takeda, M. Kimoto, and K. Miyake. 2000. Cutting edge: cell surface expression and lipopolysaccharide signaling via the Toll-like receptor 4-MD-2 complex on mouse peritoneal macrophages. J. Immunol. 164:3471-3475.
3. Barthold, S. W., G. L., Coleman, P. N. Bhatt, G. W. Osbaldiston, and A. M. Jonas. 1976. The etiology of transmissible murine colonic hyperplasia. Lab. Anim. Sci. 26:88-894.
4. Barthold, S. W., G. W. Osbaldiston, and A. M. Jonas. 1977. Dietary, bacterial, and host genetic interactions in the pathogenesis of transmissible murine colonic hyperplasia. Lab. Anim. Sci. 27:938-945.
5. Barthel, M., S. Hapfetmeier, L. Quintanilla-Martinez, M. Kremer, M. Rohde, M. Hogardt, K. Pfeffer, H. Russmann, and W. D. Hardt. 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. Berin, M. C., A. Darfenille-Michand, L. J. Egan, Y. Miyamoto, and M. F. Kagnoff. 2002. Role of EHEC O157:H7 virulence factors in the activation of intestinal epithelial cell NF-κB and MAP kinase pathways and the upregulated expression of interleukin 8. Cell Microbiol. 4:635-648.
7. Bry, L., and M. B. Brenner. 2004. Critical role of T cell-dependent serum antibody, but not the gut-associated lymphoid tissue, for surviving acute mucosal infection with Citrobacter rodentium, an attaching and effacing pathogen. J. Immunol. 172:433-441.
8. Campos, M. A., G. M. Rosinha, I. C. Almeida, X. S. Salgueiro, B. W. Jarvis, G. A. Splitter, N. Qureshi, O. Bruna-Romero, R. T. Gazzinelli, and S. C. Oliveira. 2004. Role of Toll-like receptor 4 in induction of cell-mediated immunity and resistance to Brucella abortus infection in mice. Infect. Immun. 72:176-186.
9. Celli, J., M. Olivier, and B. B. Finlay. 2001. Enteropathogenic Escherichia coli mediates antiphagocytosis through the inhibition of PI 3-kinase-dependent pathways. EMBO J. 20:1245-1258.
10. Clare, S., A. Huett, and G. Dougan. 2002. Host/pathogen interactions at mucosal surfaces: immune consequences. Res. Microbiol. 153:455-459.
11. Daly, C., and B. J. Rollins. 2003. Monocyte chemoattractant protein-1 (CCL2) in inflammatory disease and adaptive immunity: therapeutic opportunities and controversies. Microcirculation 10:247-257.
12. Deng, W., Y. Li, B. A. Vallance, and B. B. Finlay. 2001. Locus of enterocyte effacement from Citrobacter rodentium: sequence analysis and evidence for horizontal transfer among attaching and effacing pathogens. Infect. Immun. 69:6323-6335.
13. Deng, W., J. L. Puente, S. Gruenheid, Y. Li, B. A. Vallance, A. Vazquez, J. Barba, J. A. Ibarra, P. O'Donnell, P. Metalnikov, K. Ashman, S. Lee, D. Goode, T. Pawson, and B. B. Finlay. 2004. Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc. Natl. Acad. Sci. USA 101:3547-3602.
14. Deng, W., B. A. Vallance, Y. Li, J. L. Puente, and B. B. Finlay. 2003. Citrobacter rodentium translocated intimin receptor (Tir) is an essential virulence factor needed for actin condensation, intestinal colonization and colonic hyperplasia in mice. Mol. Microbiol. 48:95-115.
15. Donnenberg, M. S., B. B. Finlay, and J. B. Kaper. 1997. Interactions between enteropathogenic Escherichia coli and host epithelial cells. Trends Microbiol. 5:109-114.
16. Donnenberg, M. S., and T. S. Whittam. 2001. Pathogenesis and evolution of virulence in enteropathogenic and enterohemorrhagic Escherichia coli. J. Clin. Investig. 107:539-548.
17. Eckmann, L. 2004. Innate immunity and mucosal bacterial interactions in the intestine. Curr. Opin. Gastroenterol. 20:82-88.
18. Eskandari, M. K., J. C. Kalff, T. R. Billiar, K. K. Lee, and A. J. Bauer. 1997. Lipopolysaccharide activates the muscularis macrophage network and suppresses circular smooth muscle activity. Am. J. Physiol. 273:G727-G734.
19. Fagundes Neto, U., V. Ferreira, F. R. Patricio, V. L. Mostaco, and L. R. Trabulsi. 1989. Protracted diarrhea: the importance of the enteropathogenic Escherichia coli (EPEC) strains and Salmonella in its genesis. J. Pediatr. Gastroenterol. Nutr. 8:207-211.
20. Fine, J. S., A. Rojas-Triana, J. V. Jackson, L. W. Engstrom, G. S. Deno, D. J. Lundell, and L. A. Bober. 2003. Impairment of leukocyte trafficking in a murine pleuritis model by IL-4 and IL-10. Inflammation. 27:161-174.
21. Frankel, G., A. D. Phillips, I. Rosenshine, G. Dougan, J. B. Kaper, and S. Knutton. 1998. Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Mol. Microbiol. 30:911-921.
22. Fukata, M., K. S. Michelsen, R. Eri, L. S. Thomas, B. Hu, K. Lukasek, C. C. Nast, J. Lechago, R. Xu, Y. Naiki, A. Soliman, M. Arditi, and M. T. Abreu. 2005. Toll-like receptor-4 is required for intestinal response to epithelial injury and limiting bacterial translocation in a murine model of acute colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 288:G1055-G1065.
23. Goncalves, N. S., M. Ghaem-Maghami, G. Monteleone, G. Frankel, G. Dougan, D. J. Lewis, C. P. Simmons, and T. T. MacDonald. 2001. Critical role for tumor necrosis factor alpha in controlling the number of lumenal pathogenic bacteria and immunopathology in infectious colitis. Infect. Immun. 69:6651-6659.
24. Hapfelmeier, S., B. Stecher, M. Barthel, M. Kremer, A. J. Muller, M. Heikenwalder, T. Stallmach, M. Hensel, K. Pfeffer, S. Akira, and W. D. Hardt. 2005. The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar Typhimurium to trigger colitis via MyD88-dcpcndent and MyD88-independent mechanisms. J. Immunol. 174:1675-1685.
25. Hausmann, M., S. Kiessling, S. Mestermann, G. Wehb, T. Spottl, T. Andus, J. Scholmerich, H. Herfarth, K. Ray, W. Falk, and G. Rogler. 2002. Toll-like receptors 2 and 4 are up-regulated during intestinal inflammation. Gastroenterology 122:1987-2000.
26. Hecht, G. 2001. Microbes and microbial toxins: paradigms for microbial-mucosal interactions. VII. Enteropathogenic Escherichia coli: physiological alterations from an extracellular position. Am. J. Physiol. Gastrointest. Liver Physiol. 281:G1-G7.
27. Hill, S. M., A. D. Phillips, and J. A. Walker-Smith. 1991. Enteropathogenic Escherichia coli and life threatening chronic diarrhoea. Gut 32:154-158.
28. Kallas, M. R., F. R. Patricio, and U. Fagundes Neto. 1995. Morphometrics of the small intestine in children with diarrhea due to classical enteropathogenic Escherichia coli and to environmental asymptomatic enteropathy. Rev. Assoc. Med. Bras. 41:162-166.
29. Kaper, J. B. 1998. Enterohemorrhagic Escherichia coli. Curr. Opin. Microbiol. 1:103-108.
30. Luperchio, S. A., and D. B. Schauer. 2001. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect. 3:333-340.
31. MacLean, L. L., and M. B. Perry. 2001. Structural studies on the O-polysaccharide of the lipopolysaccharide produced by Citrobacter rodentium (ATCC 51459). Eur. J. Biochem. 268:5740-5746.
32. Mann, P. B., M. J. Kennett, and E. T. Harvill. 2004. Toll-like receptor 4 is critical to innate host defense in a murine model of bordetellosis. J. Infect. Dis. 189:833-836.
33. Marriott, I., D. L. Gray, D. M. Rati, V. G. Fowler, Jr., M. E. Stryjewski, L. S. Levin, M. C. Hudson, and K. L. Bost. 2005. Osteoblasts produce monocyte chemoattractant protein-1 in a murine model of Staphylococcus aureus osteomyelitis and infected human bone tissue. Bone 37:504-512.
34. Miyake, K. 2004. Endotoxin recognition molecules, Toll-like receptor 4-MD-2. Semin. Immunol. 16:11-16.
35. Nataro, J., and J. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
36. O'Brien, A. D., E. S. Metcalf, and D. L. Rosenstreich. 1982. Defect in macrophage effector function confers Salmonella typhimurium susceptibility on C3H/HeJ mice. Cell. Immunol. 67:325-333.
37. Perdomo, O. J., J. M. Cavaillon, M. Huerre, H. Ohayon, P. Gounon, and P. J. Sansonetti. 1994. Acute inflammation causes epithelial invasion and mucosal destruction in experimental shigellosis. J. Exp. Med. 180:1307-1319.
38. Philpott, D. J., S. Yamanka, A. Israel, and P. J. Sansonetti. 2000. Invasive Shigella flexneri activates NF-κB through a lipopolysaccharide- dependent innate intracellular response and leads to IL-8 expression in epithelial cells. J. Immunol. 165:903-914.
39. Poltorak, A., X. He, I. Smirnova, M. Y. Liu, C. Van Huffel, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, M. Freudenberg, P. Ricciardi-Castagnoli, B. Layton, and B. Beutler. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085-2088.
40. Pugin, J., C. C. Schurer-Maly, D. Leturcq, A. Moriarty, R. J. Ulevitch, and P. S. Tobias. 1993. Lipopolysaccharide activation of human endothelial and epithelial cells is mediated by lipopolysaccharide-binding protein and soluble CD14. Proc. Natl. Acad. Sci. USA 90:2744-2748.
41. Rakoff-Nahoum, S., J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov. 2004. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 118:229-241.
42. Rescigno, M., M. Urbano, M. Rimoldi, B. Valzasina, G. Rotta, F. Granucci, and P. Ricciardi-Castagnoli. 2002. Toll-like receptor 4 is not required for the full maturation of dendritic cells or for the degradation of gram-negative bacteria. Eur. J. Immunol. 32:2800-2806.
43. Ritchie, J. M., C. M. Thorpe, A. B. Rogers, and M. K. Waldor. 2003. Critical roles for stx2, eae, and tir in enterohemorrhagic Escherichia coli-induced diarrhea and intestinal inflammation in infant rabbits. Infect. Immun. 71:7129-7139.
44. Sansonetti, P. J. 2001. Microbes and microbial toxins: paradigms for microbial-mucosal interactions. III. Shigellosis: from symptoms to molecular pathogenesis. Am. J. Physiol. Gastrointest. Liver Physiol. 280:G319-G323.
45. Sansonetti, P. J. 2001. Rupture, invasion and inflammatory destruction of the intestinal barrier by Shigella, making sense of prokaryote-eukaryote cross-talks. FEMS Microbiol. Rev. 25:3-14.
46. Schauer, D. B., and S. Falkow. 1993. The eae gene of Citrobacter freundii biotype 4280 is necessary for colonization in transmissible murine colonic hyperplasia. Infect. Immun. 61:4654-4661.
47. Schilling, J. D., S. M. Martin, C. S. Hung, R. G. Lorenz, and S. J. Hultgren. 2003. Toll-like receptor 4 on stromal and hematopoietic cells mediates innate resistance to uropathogcnic Escherichia coli. Proc. Natl. Acad. Sci. USA 100:4203-4208.
48. + T cells in immunity to infection by the attaching and effacing pathogen Citrobacter rodentium. Infect. Immun. 71:5077-5086.
49. Simmons, C. P., N. S. Goncalves, M. Ghaem-Maghami, M. Bajaj-Elliott, S. Clare, B. Neves, G. Frankel, G. Dougan, and T. T. MacDonald. 2002. Impaired resistance and enhanced pathology during infection with a noninvasive, attaching-effacing enteric bacterial pathogen, Citrobacter rodentium, in mice lacking IL-12 or IFN-gamma. J. Immunol. 168:1804-1812.
50. Standiford, T. J., S. L. Kunkel, and R. M. Strieter. 1997. Role of chemokines in antibacterial host defense. Methods Enzymol. 288:220-241.
51. Takeda, K., and S. Akira. 2005. Toll-like receptors in innate immunity. Int. Immunol. 17:1-14.
52. Tomson, F. L., V. K. Viswanathan, K. J. Kanack, R. P. Kanteti, K. V. Straub, M. Menet, J. B. Kaper, and G. Hecht. 2005. Enteropathogenic Escherichia coli EspG disrupts microtubules and in conjunction with Orf3 enhances perturbation of the tight junction barrier. Mol. Microbiol. 56:447-464.
53. Vallance, B. A., W. Deng, M. De Grado, C. Chan, K. Jacobson, and B. B. Finlay. 2002. Modulation of inducible nitric oxide synthase expression by the attaching and effacing bacterial pathogen Citrobacter rodentium in infected mice. Infect. Immun. 70:6424-6435.
54. Vallance, B. A., W. Deng, K. Jacobson, and B. B. Finlay. 2003. Host susceptibility to the attaching and effacing bacterial pathogen Citrobacter rodentium. Infect. Immun. 71:3443-3453.
55. Vallance, B. A., W. Deng, L. A. Knodler, and B. B. Finlay. 2002. Mice lacking T and B lymphocytes develop transient colitis and crypt hyperplasia yet suffer impaired bacterial clearance during Citrobacter rodentium infection. Infect. Immun. 70:2070-2081.
56. Vallance, B. A., and B. B. Finlay. 2000. Exploitation of host cells by enteropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA 97:8799-8806.
57. Vazquez-Torres, A., B. A. Vallance, M. A. Bergman, B. B. Finlay, B. T. Cookson, J. Jones-Carson, and F. C. Fang. 2004. Toll-like receptor 4 dependence of innate and adaptive immunity to Salmonella: importance of the Kupffer cell network. J. Immunol. 172:6202-6208.
58. Wiles, S., S. Clare, J. Harker, A. Huett, D. Young, G. Dougan, and G. Frankel. 2004. Organ specificity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen Citrobacter rodentium. Cell Microbiol. 6:963-972.