How flagellin and toll-like receptor 5 contribute to enteric infection

Infection and Immunity

Volumn 75, Issue 2, 2007, Pages 545-552

  Steiner, Theodore S ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b NONE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN; TOLL LIKE RECEPTOR 5;

ADAPTIVE IMMUNITY; ANTIGEN RECOGNITION; HUMAN; INFECTION RESISTANCE; INNATE IMMUNITY; INTESTINE INFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SHORT SURVEY;

ANIMALS; BACTERIAL INFECTIONS; BACTERIAL PROTEINS; ENTERITIS; FLAGELLIN; HUMANS; TOLL-LIKE RECEPTOR 5; VIRULENCE FACTORS;

EID: 33846829490     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01506-06     Document Type: Short Survey

References (61)

1. Adamo, R., S. Sokol, G. Soong, M. I. Gomez, and A. Prince. 2004. Pseudomonas aeruginosa flagella activate airway epithelial cells through asialoGM1 and toll-like receptor 2 as well as toll-like receptor 5. Am. J. Respir. Cell Mol. Biol. 30:627-634.
2. + T cells. J. Immunol. 177:3983-3993.
3. Andersen-Nissen, E., K. D. Smith, K. L. Strobe, S. L. Barrett, B. T. Cookson, S. M. Logan, and A. Aderem. 2005. Evasion of Toll-like receptor 5 by flagellated bacteria. Proc. Natl. Acad. Sci. USA. 102:9247-9252.
4. Bambou, J. C., A. Giraud, S. Menard, B. Begue, S. Rakotobe, M. Heyman, F. Taddei, N. Cerf-Bensussan, and V. Gaboriau-Routhiau. 2004. In vitro and ex vivo activation of the TLR5 signaling pathway in intestinal epithelial cells by a commensal Escherichia coli strain. J. Biol. Chem. 279:42984-42992.
5. Barthel, M., S. Hapfelmeier, 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. Darfeuille-Michaud, 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-kappaB and MAP kinase pathways and the upregulated expression of interleukin 8. Cell. Microbiol. 4:635-648.
7. Ciacci-Woolwine, F., I. C. Blomfield, S. H. Richardson, and S. B. Mizel. 1998. Salmonella flagellin induces tumor necrosis factor alpha in a human promonocytic cell line. Infect. Immun. 66:1127-1134.
8. Coburn, B., Y. Li, D. Owen, B. A. Vallance, and B. B. Finlay. 2005. Salmonella enterica serovar Typhimurium pathogenicity island 2 is necessary for complete virulence in a mouse model of infectious enterocolitis. Infect. Immun. 73:3219-3227.
9. Coombes, B. K., B. A. Coburn, A. A. Potter, S. Gomis, K. Mirakhur, Y. Li, and B. B. Finlay. 2005. 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. 73:7161-7169.
10. + T regulatory cells. J. Immunol. 175:8051-8059.
11. Cunningham, A. F., M. Khan, J. Ball, K. M. Toellner, K. Serre, E. Mohr, and I. C. MacLennan. 2004. Responses to the soluble flagellar protein FliC are Th2, while those to FliC on Salmonella are Th1. Eur. J. Immunol. 34:2986-2995.
12. Diez, E., S. H. Lee, S. Gauthier, Z. Yaraghi, M. Tremblay, S. Vidal, and P. Gros. 2003. Bircle is the gene within the Lgn1 locus associated with resistance to Legionella pneumophila. Nat. Genet. 33:55-60.
13. Donnelly, M. A., and T. S. Steiner. 2002. Two nonadjacent regions in enteroaggregative Escherichia coli flagellin are required for activation of toll-like receptor 5. J. Biol. Chem. 277:40456-40461.
14. Eaves-Pyles, T., K. Murthy, L. Liaudet, L. Virag, G. Ross, F. G. Soriano, C. Szabo, and A. L. Salzman. 2001. Flagellin, a novel mediator of Salmonella-induced epithelial activation and systemic inflammation: I kappa B alpha degradation, induction of nitric oxide synthase, induction of proinflammatory mediators, and cardiovascular dysfunction. J. Immunol. 166:1248-1260.
15. Eaves-Pyles, T. D., H. R. Wong, K. Odoms, and R. B. Pyles. 2001. Salmonella flagellin-dependent proinflammatory responses are localized to the conserved amino and carboxyl regions of the protein. J. Immunol. 167:7009-7016.
16. Felix, G., J. D. Duran, S. Volko, and T. Boller. 1999. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18:265-276.
17. Franchi, L., A. Amer, M. Body-Malapel, T. D. Kanneganti, N. Ozoren, R. Jagirdar, N. Inohara, P. Vandenabeele, J. Bertin, A. Coyle, E. P. Grant, and G. Nunez. 2006. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat. Immunol. 7:576-582.
18. Gewirtz, A. T., T. A. Navas, S. Lyons, P. J. Godowski, and J. L. Madara. 2001. Cutting edge: bacterial flagellin activates basolaterally expressed tlr5 to induce epithelial proinflammatory gene expression. J. Immunol. 167:1882-1885.
19. Gewirtz, A. T., P. Simon, Jr., C. K. Schmitt, L. J. Taylor, C. H. Hagedorn, A. D. O'Brien, A. S. Neish, and J. L. Madara. 2001. Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J. Clin. Investig. 107:99-109.
20. Gewirtz, A. T., Y. Yu, U. S. Krishna, D. A. Israel, S. L. Lyons, and R. M. Peek, Jr. 2004. Helicobacter pylori flagellin evades toll-like receptor 5-mediated innate immunity. J. Infect. Dis. 189:1914-1920.
21. Guerry, P., C. P. Ewing, M. Schirm, M. Lorenzo, J. Kelly, D. Pattarini, G. Majam, P. Thibault, and S. Logan. 2006. Changes in flagellin glycosylation affect Campylobacter autoagglutination and virulence. Mol. Microbiol. 60:299-311.
22. 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-dependent and MyD88-independent mechanisms. J. Immunol. 174:1675-1685.
23. Harrington, S. M., M. C. Strauman, C. M. Abe, and J. P. Nataro. 2005. Aggregative adherence fimbriae contribute to the inflammatory response of epithelial cells infected with enteroaggregative Escherichia coli. Cell. Microbiol. 7:1565-1578.
24. Hayashi, F., K. D. Smith, A. Oxinsky, T. R. Hawn, E. C. Yi, D. R. Goodlett, J. K. Eng, S. Akira, D. M. Underhill, and A. Aderem. 2001. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099-1103.
25. Huang, F. C., A. Werne, Q. Li, E. E. Galyov, W. A. Walker, and B. J. Cherayil. 2004. Cooperative interactions between flagellin and SopE2 in the epithelial interleukin-8 response to Salmonella enterica serovar Typhimurium infection. Infect. Immun. 72:5052-5062.
26. Igimi, S., F. Amano, and S. Kumagai. 2000. Inhibition of Salmonella enteritidis binding to human intestinal epithelial cells with anti-flagella antibody, p. 62. Abstr. 100th Gen. Meet. Am. Soc. Microbiol. American Society for Microbiology, Washington, DC.
27. Jacchieri, S. G., R. Torquato, and R. R. Brentani. 2003. Structural study of binding of flagellin by Toll-like receptor 5. J. Bacteriol. 185:4243-4247.
28. Johanesen, P. A., and M. B. Dwinell. 2006. Flagellin-independent regulation of chemokine host defense in Campylobacter jejuni-infected intestinal epithelium. Infect. Immun. 74:3437-3447.
29. Lee, S. E., S. Y. Kim, B. C. Jeong, Y. R. Kim, S. J. Bae, O. S. Ahn, J. J. Lee, H. C. Song, J. M. Kim, H. E. Choy, S. S. Chung, M. N. Kweon, and J. H. Rhee. 2006. A bacterial flagellin, Vibrio vulnificus FlaB, has a strong mucosal adjuvant activity to induce protective immunity. Infect. Immun. 74:694-702.
30. Lee, S. K., A. Stack, E. Katzowitsch, S. I. Aizawa, S. Suerbaum, and C. Josenhans. 2003. Helicobacter pylori flagellins have very low intrinsic activity to stimulate human gastric epithelial cells via TLR5. Microbes Infect. 5:1345-1356.
31. Lyons, S., L. Wang, J. E. Casanova, S. V. Sitaraman, B. Merlin, and A. T. Gewirtz. 2004. Salmonella typhimurium transcytoses flagellin via an SPI2-mediated vesicular transport pathway. J. Cell Sci. 117:5771-5780.
32. Maaser, C., J. Heidemann, C. von Eiff, A. Lugering, T. W. Spahn, D. G. Binion, W. Domschke, N. Lugering, and T. Kucharzik. 2004. Human intestinal microvascular endothelial cells express Toll-like receptor 5: a binding partner for bacterial flagellin. J. Immunol. 172:5056-5062.
33. McDermott, P. F., F. Ciacci-Woolwine, J. A. Snipes, and S. B. Mizel. 2000. High-affinity interaction between gram-negative flagellin and a cell surface polypeptide results in human monocyte activation. Infect. Immun. 68:5525-5529.
34. Miao, E. A., C. M. Alpuche-Aranda, M. Dors, A. E. Clark, M. W. Bader, S. I. Miller, and A. Aderem. 2006. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat. Immunol. 7:569-575.
35. Mizel, S. B., A. N. Honko, M. A. Moors, P. S. Smith, and A. P. West. 2003. Induction of macrophage nitric oxide production by gram-negative flagellin involves signaling via heteromeric toll-like receptor 5/toll-like receptor 4 complexes. J. Immunol. 170:6217-6223.
36. Mizel, S. B., A. P. West, and R. R. Hantgan. 2003. Identification of a sequence in human toll-like receptor 5 required for the binding of Gram-negative flagellin. J. Biol. Chem. 278:23624-23629.
37. Molofsky, A. B., B. G. Byrne, N. N. Whitfield, C. A. Madigan, E. T. Fuse, K. Tateda, and M. S. Swanson. 2006. Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J. Exp. Med. 203:1093-1104.
38. Murthy, K. G., A. Deb, S. Goonesekera, C. Szabo, and A. L. Salzman. 2004. Identification of conserved domains in Salmonella muenchen flagellin that are essential for its ability to activate TLR5 and to induce an inflammatory response in vitro. J. Biol. Chem. 279:5667-5675.
39. Pietila, T. E., V. Veckman, P. Kyllonen, K. Lahteenmaki, T. K. Korhonen, and I. Julkunen. 2005. Activation, cytokine production, and intracellular survival of bacteria in Salmonella-infected human monocyte-derived macrophages and dendritic cells. J. Leukoc. Biol. 78:909-920.
40. Ren, T., D. S. Zamboni, C. R. Roy, W. F. Dietrich, and R. E. Vance. 17 March 2006, posting date. Flagellin-deficient Legionella mutants evade caspase-1-and Naip5-mediated macrophage immunity. PLoS Pathog. 2:e18. [Epub ahead of print.]
41. Rhee, S. H., E. Im, M. Riegler, E. Kokkotou, M. O'Brien, and C. Pothoulakis. 2005. Pathophysiological role of Toll-like receptor 5 engagement by bacterial flagellin in colonie inflammation. Proc. Natl. Acad. Sci. USA. 102:13610-13615.
42. Samatey, F. A., K. Imada, S. Nagashima, F. Vonderviszt, T. Kumasaka, M. Yamamoto, and K. Namba. 2001. Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 410:331-337.
43. Schmitt, C. K., S. C. Darnell, and A. D. O'Brien. 1996. The attenuated phenotype of a Salmonella typhimurium flgM mutant is related to expression of FliC flagellin. J. Bacteriol. 178:2911-2915.
44. Schmitt, C. K., J. S. Ikeda, S. C. Darnell, P. R. Watson, J. Bispham, T. S. Wallis, D. L. Weinstein, E. S. Metcalf, and A. D. O'Brien. 2001. Absence of all components of the flagellar export and synthesis machinery differentially alters virulence of Salmonella enterica serovar Typhimurium in models of typhoid fever, survival in macrophages, tissue culture invasiveness, and calf enterocolitis. Infect. Immun. 69:5619-5625.
45. Smith, K. D., E. Andersen-Nissen, F. Hayashi, K. Strobe, M. A. Bergman, S. L. Barrett, B. T. Cookson, and A. Aderem. 2003. Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat. Immunol. 4:1247-1253.
46. Smith, K. D., and A. Ozinsky. 2002. Toll-like receptor-5 and the innate immune response to bacterial flagellin. Curr. Top. Microbiol. Immunol. 270:93-108.
47. Smith, M. F., Jr, A. Mitchell, G. Li, S. Ding, A. M. Fitzmaurice, K. Ryan, S. Crowe, and J. B. Goldberg. 2003. Toll-like receptor (TLR) 2 and TLR5, but not TLR4, are required for Helicobacter pylori-induced NF-kappa B activation and chemokine expression by epithelial cells. J. Biol. Chem. 278: 32552-32560.
48. Stecher, B., S. Hapfelmeier, C. Muller, M. Kremer, T. Stallmach, and W. D. Hardt. 2004. Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin-pretreated mice. Infect. Immun. 72:4138-4150.
49. Steiner, T. S., A. A. Lima, J. P. Nataro, and R. L. Guerrant. 1998. Entero-aggregative Escherichia coli produce intestinal inflammation and growth impairment and cause interleukin-8 release from intestinal epithelial cells. J. Infect. Dis. 177:88-96.
50. Steiner, T. S., J. P. Nataro, C. E. Poteet-Smith, J. A. Smith, and R. L. Guerrant. 2000. Enteroaggregative Escherichia coli expresses a novel flagellin that causes IL-8 release from intestinal epithelial cells. J. Clin. Investig. 105:1769-1777.
51. Tallant, T., A. Deb, N. Kar, J. Lupica, M. J. de Veer, and J. A. DiDonato. 2004. Flagellin acting via TLR5 is the major activator of key signaling pathways leading to NF-kappa B and proinflammatory gene program activation in intestinal epithelial cells. BMC Microbiol. 4:33.
52. Torok, A. M., A. H. Bouton, and J. B. Goldberg. 2005. Helicobacter pylori induces interleukin-8 secretion by Toll-like receptor 2- and Toll-like receptor 5-dependent and -independent pathways. Infect. Immun. 73:1523-1531.
53. Tsujita, T., A. Ishii, H. Tsukada, M. Matsumoto, F. S. Che, and T. Seya. 2006. Fish soluble Toll-like receptor (TLR)5 amplifies human TLR5 response via physical binding to flagellin. Vaccine 24:2193-2199.
54. + lamina propria cells. Nat. Immunol. 7:868-874.
55. Verma, A., S. K. Arora, S. K. Kuravi, and R. Ramphal. 2005. Roles of specific amino acids in the N terminus of Pseudomonas aeruginosa flagellin and of flagellin glycosylation in the innate immune response. Infect. Immun. 73:8237-8246.
56. Weinstein, D. L., M. Carsiotis, C. R. Lissner, and A. D. O'Brien. 1984. Flagella help Salmonella typhimurium survive within murine macrophages. Infect. Immun. 46:819-825.
57. West, A. P., B. A. Dancho, and S. B. Mizel. 2005. Gangliosides inhibit flagellin signaling in the absence of an effect on flagellin binding to toll-like receptor 5. J. Biol. Chem. 280:9482-9488.
58. Wright, E. K., S. A. Goodart, J. D. Growney, V. Hadinoto, M. G. Endrizzi, E. M. Long, K. Sadigh, A. L. Abney, I. Bernstein-Hanley, and W. F. Dietrich. 2003. Naip5 affects host susceptibility to the intracellular pathogen Legionella pneumophila. Curr. Biol. 13:27-36.
59. Wyant, T. L., M. K. Tanner, and M. B. Sztein. 1999. Potent immunoregulatory effects of Salmonella typhi flagella on antigenic stimulation of human peripheral blood mononuclear cells. Infect. Immun. 67:1338-1346.
60. Wyant, T. L., M. K. Tanner, and M. B. Sztein. 1999. Salmonella typhi flagella are potent inducers of proinflammatory cytokine. Infect. Immun. 67:3619-3624.
61. Zhou, X., J. A. Giron, A. G. Torres, J. A. Crawford, E. Negrete, S. N. Vogel, and J. B. Kaper. 2003. Flagellin of enteropathogenic Escherichia coli stim-ulates interleukin-8 production in T84 cells. Infect. Immun. 71:2120-2129.