Mucosal interplay among commensal and pathogenic bacteria: Lessons from flagellin and Toll-like receptor 5

FEBS Letters

Volumn 580, Issue 12, 2006, Pages 2976-2984

  Rumbo, Martin ^a   Nempont, Clément ^b   Kraehenbuhl, Jean Pierre ^c   Sirard, Jean Claude ^b  

^a FACULTAD DE CIENCIAS EXACTAS   (Argentina)

^b INSERM   (France)

^c EuroVacc Foundation   (Switzerland)

Author keywords

Commensal flora; Epithelium; Flagellin; Innate immunity; Pathogenic bacteria; Toll like receptor

Indexed keywords

FLAGELLIN; STRUCTURAL PROTEIN; TOLL LIKE RECEPTOR 5;

BACTERIAL VIRULENCE; BACTERIUM DETECTION; COLITIS; COMMENSALISM; CROHN DISEASE; GENE MUTATION; GENETIC POLYMORPHISM; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOPATHOLOGY; INFECTION SENSITIVITY; INNATE IMMUNITY; INTESTINE MUCOSA; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RECEPTOR UPREGULATION; RESPIRATORY TRACT MUCOSA; SHORT SURVEY; BACTERIAL PHENOMENA AND FUNCTIONS; GENETICS; METABOLISM; MICROBIOLOGY; MUCOSA; PHYSIOLOGY; REVIEW; TRACHEA;

BACTERIAL PHYSIOLOGY; FLAGELLIN; INTESTINAL MUCOSA; MUCOUS MEMBRANE; TOLL-LIKE RECEPTOR 5; TRACHEA;

EID: 33746401619     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2006.04.036     Document Type: Short Survey

References (86)

1. Sansonetti P.J. War and peace at mucosal surfaces. Nat. Rev. Immunol. 4 (2004) 953-964
2. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F., Edberg S., and Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118 (2004) 229-241
3. Hornef M.W., and Bogdan C. The role of epithelial Toll-like receptor expression in host defense and microbial tolerance. J. Endotoxin Res. 11 (2005) 124-128
4. Pull S.L., Doherty J.M., Mills J.C., Gordon J.I., and Stappenbeck T.S. Activated macrophages are an adaptive element of the colonic epithelial progenitor niche necessary for regenerative responses to injury. Proc. Natl. Acad. Sci. USA 102 (2005) 99-104
5. Jiang D., Liang J., Fan J., Yu S., Chen S., Luo Y., Prestwich G.D., Mascarenhas M.M., Garg H.G., Quinn D.A., Homer R.J., Goldstein D.R., Bucala R., Lee P.J., Medzhitov R., and Noble P.W. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat. Med. 11 (2005) 1173-1179
6. Matzinger P. The danger model: a renewed sense of self. Science 296 (2002) 301-305
7. Butler S.M., and Camilli A. Going against the grain: chemotaxis and infection in Vibrio cholerae. Nat. Rev. Microbiol. 3 (2005) 611-620
8. Ramos H.C., Rumbo M., and Sirard J.C. Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol. 12 (2004) 509-517
9. Beatson S.A., Minamino T., and Pallen M.J. Variation in bacterial flagellins: from sequence to structure. Trends Microbiol. (2006)
10. Janeway Jr. C.A., and Medzhitov R. Innate immune recognition. Annu. Rev. Immunol. 20 (2002) 197-216
11. Roach J.C., Glusman G., Rowen L., Kaur A., Purcell M.K., Smith K.D., Hood L.E., and Aderem A. The evolution of vertebrate Toll-like receptors. Proc. Natl. Acad. Sci. USA 102 (2005) 9577-9582
12. Hayashi F., Smith K.D., Ozinsky A., Hawn T.R., Yi E.C., Goodlett D.R., Eng J.K., Akira S., Underhill D.M., and Aderem A. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410 (2001) 1099-1103
13. Gewirtz A.T., Navas T.A., Lyons S., Godowski P.J., and Madara J.L. Bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J. Immunol. 167 (2001) 1882-1885
14. Hajjar A.M., Ernst R.K., Tsai J.H., Wilson C.B., and Miller S.I. Human Toll-like receptor 4 recognizes host-specific LPS modifications. Nat. Immunol. 3 (2002) 354-359
15. Smith K.D., Andersen-Nissen E., Hayashi F., Strobe K., Bergman M.A., Barrett S.L., Cookson B.T., and Aderem A. Toll-like receptor 5 recognizes a conserved site on flagellin protofilament formation and bacterial motility. Nat. Immunol. 4 (2003) 1247-1253
16. Jacchieri S.G., Torquato R., and Brentani R.R. Structural study of binding of flagellin by Toll-like receptor 5. J. Bacteriol. 185 (2003) 4243-4247
17. Andersen-Nissen E., Smith K.D., Strobe K.L., Barrett S.L., Cookson B.T., Logan S.M., and Aderem A. Evasion of Toll-like receptor 5 by flagellated bacteria. Proc. Natl. Acad. Sci. USA 102 (2005) 9247-9252
18. Choe J., Kelker M.S., and Wilson I.A. Crystal structure of human toll-like receptor 3 (TLR3) ectodomain. Science 309 (2005) 581-585
19. Bell J.K., Mullen G.E., Leifer C.A., Mazzoni A., Davies D.R., and Segal D.M. Leucine-rich repeats and pathogen recognition in Toll-like receptors. Trends Immunol. 24 (2003) 528-533
20. Mizel S.B., West A.P., and Hantgan R.R. Identification of a sequence in human toll-like receptor 5 required for the binding of Gram-negative flagellin. J. Biol. Chem. 278 (2003) 23624-23629
21. Hawn T.R., Verbon A., Lettinga K.D., Zhao L.P., Li S.S., Laws R.J., Skerrett S.J., Beutler B., Schroeder L., Nachman A., Ozinsky A., Smith K.D., and Aderem A. A common dominant TLR5 stop codon polymorphism abolishes flagellin signalling and is associated with susceptibility to Legionnaires' disease. J. Exp. Med. 198 (2003) 1563-1572
22. Ren T., Zamboni D.S., Roy C.R., Dietrich W.F., and Vance R.E. Flagellin-deficient legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog. 2 (2006) e18
23. Didierlaurent A., Ferrero I., Otten L.A., Dubois B., Reinhardt M., Carlsen H., Blomhoff R., Akira S., Kraehenbuhl J.P., and Sirard J.C. Flagellin promotes myeloid differentiation factor 88-dependent development of Th2-type response. J. Immunol. 172 (2004) 6922-6930
24. Zhou X., Giron J.A., Torres A.G., Crawford J.A., Negrete E., Vogel S.N., and Kaper J.B. Flagellin of enteropathogenic Escherichia coli stimulates interleukin-8 production in T84 cells. Infect. Immun. 71 (2003) 2120-2129
25. Berin M.C., Darfeuille-Michaud A., Egan L.J., Miyamoto Y., and Kagnoff M.F. 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 (2002) 635-648
26. Zeng H., Carlson A.Q., Guo Y., Yu Y., Collier-Hyams L.S., Madara J.L., Gewirtz A.T., and Neish A.S. Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella. J. Immunol. 171 (2003) 3668-3674
27. Rhee S.H., Keates A.C., Moyer M.P., and Pothoulakis C. MEK is a key modulator for TLR5-induced interleukin-8 and MIP3alpha gene expression in non-transformed human colonic epithelial cells. J. Biol. Chem. 279 (2004) 25179-25188
28. Hughes E.A., and Galan J.E. Immune response to Salmonella: location, location, location?. Immunity 16 (2002) 325-328
29. Ortega-Cava C.F., Ishihara S., Rumi M.A., Aziz M.M., Kazumori H., Yuki T., Mishima Y., Moriyama I., Kadota C., Oshima N., Amano Y., Kadowaki Y., Ishimura N., and Kinoshita Y. Epithelial toll-like receptor 5 is constitutively localized in the mouse cecum and exhibits distinctive downregulation during experimental colitis. Clin. Vaccine Immunol. 13 (2006) 132-138
30. Bambou J.C., Giraud A., Menard S., Begue B., Rakotobe S., Heyman M., Taddei F., Cerf Bensussan N., and Gaboriau-Routhiau V. In vitro and ex vivo activation of the TLR5 signalling pathway in intestinal epithelial cells by a commensal Escherichia coli strain. J. Biol. Chem. 279 (2004) 42984-42992
31. Rhee S.H., Im E., Riegler M., Kokkotou E., O'Brien M., and Pothoulakis C. Pathophysiological role of Toll-like receptor 5 engagement by bacterial flagellin in colonic inflammation. Proc. Natl. Acad. Sci. USA 102 (2005) 13610-13615
32. Zipfel C., and Felix G. Plants and animals: a different taste for microbes?. Curr. Opin. Plant Biol. 8 (2005) 353-360
33. Backhed F., Ley R.E., Sonnenburg J.L., Peterson D.A., and Gordon J.I. Host-bacterial mutualism in the human intestine. Science 307 (2005) 1915-1920
34. Niedergang F., and Kweon M.N. New trends in antigen uptake in the gut mucosa. Trends Microbiol. 13 (2005) 485-490
35. Ciacci-Woolwine F., Blomfield I.C., Richardson S.H., and Mizel S.B. Salmonella flagellin induces tumor necrosis factor alpha in a human promonocytic cell line. Infect. Immun. 66 (1998) 1127-1134
36. Means T.K., Hayashi F., Smith K.D., Aderem A., and Luster A.D. The Toll-like receptor 5 stimulus bacterial flagellin induces maturation and chemokine production in human dendritic cells. J. Immunol. 170 (2003) 5165-5175
37. Steiner T.S., Nataro J.P., Poteet-Smith C.E., Smith J.A., and Guerrant R.L. Enteroaggregative Escherichia coli expresses a novel flagellin that causes IL-8 release from intestinal epithelial cells. J. Clin. Invest. 105 (2000) 1769-1777
38. Gewirtz A.T., Simon P.O., Schmitt C.K., Taylor L.J., Hagedorn C.H., O'Brien A.D., Neish A.S., and Madara J.L. Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J. Clin. Invest. 107 (2001) 99-109
39. Anderle P., Rumbo M., Sierro F., Mansourian R., Michetti P., Roberts M.A., and Kraehenbuhl J.P. Novel markers of the human follicle-associated epithelium identified by genomic profiling and microdissection. Gastroenterology 129 (2005) 321-327
40. Jenner R.G., and Young R.A. Insights into host responses against pathogens from transcriptional profiling. Nat. Rev. Microbiol. 3 (2005) 281-294
41. Niedergang F., Didierlaurent A., Kraehenbuhl J.-P., and Sirard J.-C. Dendritic cells: the host Achille's heel for mucosal pathogens?. Trends Microbiol. 12 (2004) 79-88
42. Sierro F., Dubois B., Coste A., Kaiserlian D., Kraehenbuhl J.P., and Sirard J.C. Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc. Natl. Acad. Sci. USA 98 (2001) 13722-13727
43. Iwasaki A., and Kelsall B.L. Localization of distinct Peyer's patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3alpha, MIP-3beta, and secondary lymphoid organ chemokine. J. Exp. Med. 191 (2000) 1381-1394
44. Cook D.N., Prosser D.M., Forster R., Zhang J., Kuklin N.A., Abbondanzo S.J., Niu X.D., Chen S.C., Manfra D.J., Wiekowski M.T., Sullivan L.M., Smith S.R., Greenberg H.B., Narula S.K., Lipp M., and Lira S.A. CCR6 mediates dendritic cell localization, lymphocyte homeostasis, and immune responses in mucosal tissue. Immunity 12 (2000) 495-503
45. Rumbo M., Courjault-Gautier F., Sierro F., Sirard J.C., and Felley-Bosco E. Polarized distribution of inducible nitric oxide synthase regulates activity in intestinal epithelial cells. FEBS J. 272 (2005) 444-453
46. Claud E.C., Lu L., Anton P.M., Savidge T., Walker W.A., and Cherayil B.J. Developmentally regulated IkappaB expression in intestinal epithelium and susceptibility to flagellin-induced inflammation. Proc. Natl. Acad. Sci. USA 101 (2004) 7404-7408
47. Fretin D., Fauconnier A., Kohler S., Halling S., Leonard S., Nijskens C., Ferooz J., Lestrate P., Delrue R.M., Danese I., Vandenhaute J., Tibor A., DeBolle X., and Letesson J.J. The sheathed flagellum of Brucella melitensis is involved in persistence in a murine model of infection. Cell Microbiol. 7 (2005) 687-698
48. Andrade A., Giron J.A., Amhaz J.M., Trabulsi L.R., and Martinez M.B. Expression and characterization of flagella in non-motile enteroinvasive Escherichia coli isolated from diarrhea cases. Infect. Immun. 70 (2002) 5882-5886
49. Gewirtz A.T., Yu Y., Krishna U.S., Israel D.A., Lyons S.L., and Peek Jr. R.M. Helicobacter pylori flagellin evades toll-like receptor 5-mediated innate immunity. J. Infect. Dis. 189 (2004) 1914-1920
50. Lee S.K., Stack A., Katzowitsch E., Aizawa S.I., Suerbaum S., and Josenhans C. Helicobacter pylori flagellins have very low intrinsic activity to stimulate human gastric epithelial cells via TLR5. Microbes Infect. 5 (2003) 1345-1356
51. Guo L., Lim K.B., Gunn J.S., Bainbridge B., Darveau R.P., Hackett M., and Miller S.I. Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ. Science 276 (1997) 250-253
52. Neish A.S., Gewirtz A.T., Zeng H., Young A.N., Hobert M.E., Karmali V., Rao A.S., and Madara J.L. Prokaryotic regulation of epithelial responses by inhibition of I kappa B-alpha ubiquitination. Science 289 (2000) 1560-1563
53. Collier-Hyams L.S., Zeng H., Sun J., Tomlinson A.D., Bao Z.Q., Chen H., Madara J.L., Orth K., and Neish A.S. Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-kappa B pathway. J. Immunol. 169 (2002) 2846-2850
54. Kelly D., Campbell J.I., King T.P., Grant G., Jansson E.A., Coutts A.G., Pettersson S., and Conway S. Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat. Immunol. 5 (2004) 104-112
55. Hasan U.A., Trinchieri G., and Vlach J. Toll-like receptor signaling stimulates cell cycle entry and progression in fibroblasts. J. Biol. Chem. 280 (2005) 20620-20627
56. Collier-Hyams L.S., and Neish A.S. Innate immune relationship between commensal flora and the mammalian intestinal epithelium. Cell. Mol. Life Sci. 62 (2005) 1339-1348
57. Fischer H., Yamamoto M., Akira S., Beutler B., and Svanborg C. Mechanism of pathogen-specific TLR4 activation in the mucosa: fimbriae, recognition receptors and adaptor protein selection. Eur. J. Immunol. 36 (2006) 267-277
58. Brown G.D. Dectin-1: a signalling non-TLR pattern-recognition receptor. Nat. Rev. Immunol. 6 (2006) 33-43
59. Abreu M.T., Vora P., Faure E., Thomas L.S., Arnold E.T., and Arditi M. Decreased expression of Toll-like receptor-4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial lipopolysaccharide. J. Immunol. 167 (2001) 1609-1616
60. Ortega-Cava C.F., Ishihara S., Rumi M.A., Kawashima K., Ishimura N., Kazumori H., Udagawa J., Kadowaki Y., and Kinoshita Y. Strategic compartmentalization of Toll-like receptor 4 in the mouse gut. J. Immunol. 170 (2003) 3977-3985
61. Melmed G., Thomas L.S., Lee N., Tesfay S.Y., Lukasek K., Michelsen K.S., Zhou Y., Hu B., Arditi M., and Abreu M.T. Human intestinal epithelial cells are broadly unresponsive to toll-like receptor 2-dependent bacterial ligands: implications for host-microbial interactions in the gut. J. Immunol. 170 (2003) 1406-1415
62. Ogushi K.I., Wada A., Niidome T., Okuda T., Llanes R., Nakayama M., Nishi Y., Kurazono H., Smith K.D., Aderem A., Moss J., and Hirayama T. Gangliosides act as co-receptors for Salmonella enteritidis FliC and promote FliC-induction of human beta-defensin-2 expression in Caco-2 cells. J. Biol. Chem. 279 (2004) 12213-12219
63. West A.P., Dancho B.A., and Mizel S.B. Gangliosides inhibit flagellin signalling in the absence of an effect on flagellin binding to toll-like receptor 5. J. Biol. Chem. 280 (2005) 9482-9488
64. Tseng J., Do J., Widdicombe J.H., and Machen T.E. Innate immune responses of human tracheal epithelium to P. aeruginosa Flagellin, TNF{alpha} and IL1{beta}. Am. J. Physiol. Cell Physiol. (2005)
65. Zhang Z., Louboutin J.P., Weiner D.J., Goldberg J.B., and Wilson J.M. Human airway epithelial cells sense Pseudomonas aeruginosa infection via recognition of flagellin by Toll-like receptor 5. Infect. Immun. 73 (2005) 7151-7160
66. Liaudet L., Szabo C., Evgenov O.V., Murthy K.G., Pacher P., Virag L., Mabley J.G., Marton A., Soriano F.G., Kirov M.Y., Bjertnaes L.J., and Salzman A.L. Flagellin from Gramnegative bacteria is a potent mediator of acute pulmonary inflammation in sepsis. Shock 19 (2003) 131-137
67. Lopez-Boado Y.S., Wilson C.L., and Parks W.C. Regulation of matrilysin expression in airway epithelial cells by Pseudomonas aeruginosa flagellin. J. Biol. Chem. 276 (2001) 41417-41423
68. Muir A., Soong G., Sokol S., Reddy B., Gomez M., Van Heeckeren A., and Prince A. Toll-like receptors in normal and cystic fibrosis airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 30 (2004) 777-783
69. Cobb L.M., Mychaleckyj J.C., Wozniak D.J., and Lopez-Boado Y.S. Pseudomonas aeruginosa flagellin and alginate elicit very distinct gene expression patterns in airway epithelial cells: implications for cystic fibrosis disease. J. Immunol. 173 (2004) 5659-5670
70. Honko A.N., and Mizel S.B. Mucosal administration of flagellin induces innate immunity in the mouse lung. Infect. Immun. 72 (2004) 6676-6679
71. Lee S.E., Kim S.Y., Jeong B.C., Kim Y.R., Bae S.J., Ahn O.S., Lee J.J., Song H.C., Kim J.M., Choy H.E., Chung S.S., Kweon M.N., and Rhee J.H. A bacterial flagellin, Vibrio vulnificus FlaB, has a strong mucosal adjuvant activity to induce protective immunity. Infect. Immun. 74 (2006) 694-702
72. Honko A.N., Sriranganathan N., Lees C.J., and Mizel S.B. Flagellin is an effective adjuvant for immunization against lethal respiratory challenge with Yersinia pestis. Infect. Immun. 74 (2006) 1113-1120
73. Pino O., Martin M., and Michalek S.M. Cellular mechanisms of the adjuvant activity of the flagellin component FljB of Salmonella enterica Serovar Typhimurium to potentiate mucosal and systemic responses. Infect. Immun. 73 (2005) 6763-6770
74. Cunningham A.F., Khan M., Ball J., Toellner K.M., Serre K., Mohr E., and Maclennan I.C. Responses to the soluble flagellar protein FliC are Th2, while those to FliC on Salmonella are Th1. Eur. J. Immunol. 34 (2004) 2986-2995
75. Sha Q., Truong-Tran A.Q., Plitt J.R., Beck L.A., and Schleimer R.P. Activation of airway epithelial cells by toll-like receptor agonists. Am. J. Respir. Cell Mol. Biol. 31 (2004) 358-364
76. Thorley A.J., Goldstraw P., Young A., and Tetley T.D. Primary human alveolar type II epithelial cell CCL20 (macrophage inflammatory protein-3alpha)-induced dendritic cell migration. Am. J. Respir. Cell Mol. Biol. 32 (2005) 262-267
77. Sebastiani G., Leveque G., Lariviere L., Laroche L., Skamene E., Gros P., and Malo D. Cloning and characterization of the murine toll-like receptor 5 (Tlr5) gene: sequence and mRNA expression studies in Salmonella-susceptible MOLF/Ei mice. Genomics 64 (2000) 230-240
78. Dunstan S.J., Hawn T.R., Hue N.T., Parry C.P., Ho V.A., Vinh H., Diep T.S., House D., Wain J., Aderem A., Hien T.T., and Farrar J.J. Host susceptibility and clinical outcomes in toll-like receptor 5-deficient patients with typhoid fever in Vietnam. J. Infect. Dis. 191 (2005) 1068-1071
79. Strober W., Murray P.J., Kitani A., and Watanabe T. Signalling pathways and molecular interactions of NOD1 and NOD2. Nat. Rev. Immunol. 6 (2006) 9-20
80. Lodes M.J., Cong Y., Elson C.O., Mohamath R., Landers C.J., Targan S.R., Fort M., and Hershberg R.M. Bacterial flagellin is a dominant antigen in Crohn disease. J. Clin. Invest. 113 (2004) 1296-1306
81. Targan S.R., Landers C.J., Yang H., Lodes M.J., Cong Y., Papadakis K.A., Vasiliauskas E., Elson C.O., and Hershberg R.M. Antibodies to CBir1 flagellin define a unique response that is associated independently with complicated Crohn's disease. Gastroenterology 128 (2005) 2020-2028
82. Sitaraman S.V., Klapproth J.M., Moore III D.A., Landers C., Targan S., Williams I.R., and Gewirtz A.T. Elevated flagellin-specific immunoglobulins in Crohn's disease. Am. J. Physiol. Gastrointest. Liver Physiol. 288 (2005) G403-G406
83. Gewirtz A.T., Vijay-Kumar M., Brant S.R., Duerr R.H., Nicolae D.L., and Cho J.H. Dominant-negative TLR5 polymorphism reduces adaptive immune response to flagellin and negatively associates with Crohn's disease. Am. J. Physiol. Gastrointest. Liver Physiol. (2006)
84. Cario E., and Podolsky D.K. Differential alteration in intestinal epithelial cell expression of Toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect. Immun. 68 (2000) 7010-7017
85. Beckwith J., Cong Y., Sundberg J.P., Elson C.O., and Leiter E.H. Cdcs1, a major colitogenic locus in mice, regulates innate and adaptive immune response to enteric bacterial antigens. Gastroenterology 129 (2005) 1473-1484
86. Hawn T.R., Wu H., Grossman J.M., Hahn B.H., Tsao B.P., and Aderem A. A stop codon polymorphism of Toll-like receptor 5 is associated with resistance to systemic lupus erythematosus. Proc. Natl. Acad. Sci. USA 102 (2005) 10593-10597