Toll like receptor-5: Protecting the gut from enteric microbes

Seminars in Immunopathology

Volumn 30, Issue 1, 2008, Pages 11-21

  Vijay Kumar, Matam ^a   Aitken, Jesse D ^a   Gewirtz, Andrew T ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN; TOLL LIKE RECEPTOR 5;

ADAPTIVE IMMUNITY; COLITIS; ENTEROBACTERIACEAE; ESCHERICHIA COLI; GENE EXPRESSION; HUMAN; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INFECTION; INTESTINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN POLYMORPHISM; REVIEW; SALMONELLA; SIGNAL TRANSDUCTION;

ANIMALS; COLITIS; FLAGELLIN; GASTROINTESTINAL TRACT; HUMANS; IMMUNITY, NATURAL; POLYMORPHISM, GENETIC; SALMONELLA INFECTIONS, ANIMAL; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 5;

EID: 38749111835     PISSN: 18632297     EISSN: 18632300     Source Type: Journal    
DOI: 10.1007/s00281-007-0100-5     Document Type: Review

References (58)

1. Andersen-Nissen E, Smith KD, Strobe KL, Barrett SL, Cookson BT, Logan SM, Aderem A (2005) Evasion of Toll-like receptor 5 by flagellated bacteria. Proc Natl Acad Sci U S A 102:9247-9252
2. Barthel M, Hapfelmeier S, Quintanilla-Martinez L, Kremer M, Rohde M, Hogardt M, Pfeffer K, Russmann H, Hardt WD (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
3. Cookson BT, Bevan MJ (1997) Identification of a natural T cell epitope presented by Salmonella-infected macrophages and recognized by T cells from orally immunized mice. J Immunol 158:4310-4319
4. Darfeuille-Michaud A (2002) Adherent-invasive Escherichia coli: a putative new E. coli pathotype associated with Crohn's disease. Int J Med Microbiol 292:185-193
5. Didierlaurent A, Ferrero I, Otten LA, Dubois B, Reinhardt M, Carlsen H, Blomhoff R, Akira S, Kraehenbuhl JP, Sirard JC (2004) Flagellin promotes myeloid differentiation factor 88-dependent development of Th2-type response. J Immunol 172:6922-6930
6. Duck LW, Walter MR, Novak J, Kelly D, Tomasi M, Cong Y, Elson CO (2007) Isolation of flagellated bacteria implicated in Crohn's disease. Inflamm Bowel Dis 13:1191-1201
7. Dunstan SJ, Hawn TR, Hue NT, Parry CP, Ho VA, Vinh H, Diep TS, House D, Wain J, Aderem A, Hien TT, Farrar JJ (2005) Host susceptibility and clinical outcomes in toll-like receptor 5-deficient patients with typhoid fever in Vietnam. J Infect Dis 191:1068-1071
8. Feuillet V, Medjane S, Mondor I, Demaria O, Pagni PP, Galan JE, Flavell RA, Alexopoulou L (2006) Involvement of Toll-like receptor 5 in the recognition of flagellated bacteria. Proc Natl Acad Sci U S A 103:12487-12492
9. Franchi L, Amer A, Body-Malapel M, Kanneganti TD, Ozoren N, Jagirdar R, Inohara N, Vandenabeele P, Bertin J, Coyle A, Grant EP, Nunez G (2006) Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat Immunol 7:576-582
10. Franchi L, Kanneganti TD, Dubyak GR, Nunez G (2007) Differential requirement of P2X7 receptor and intracellular K+ for caspase-1 activation induced by intracellular and extracellular bacteria. J Biol Chem 282:18810-18818
11. Geis G, Suerbaum S, Forsthoff B, Leying H, Opferkuch W (1993) Ultrastructure and biochemical studies of the flagellar sheath of Helicobacter pylori. J Med Microbiol 38:371-377
12. Gewirtz AT, Navas TA, Lyons S, Godowski PJ, Madara JL (2001) Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 167:1882-1885
13. Gewirtz AT, Navas TA, Lyons S, Godowski PJ, Madara JL (2001) Cutting edge: bacterial flagellin activates basolaterally expressed tlr5 to induce epithelial proinflammatory gene expression. J Immunol 167:1882-1885
14. Gewirtz AT, Simon PO Jr, Schmitt CK, Taylor LJ, Hagedorn CH, O'Brien AD, Neish AS, Madara JL (2001) Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J Clin Invest 107:99-109
15. Gewirtz AT, Liu Y, Sitaraman SV, Madara JL (2002) Intestinal epithelial pathobiology: past, present and future. Best Pract Res Clin Gastroenterol 16:851-867
16. Gewirtz AT (2003) Intestinal epithelial toll-like receptors: to protect. And serve? Curr Pharm Des 9:1-5
17. Gewirtz AT, Yu Y, Krishna US, Israel DA, Lyons SL, Peek RM Jr (2004) Helicobacter pylori flagellin evades toll-like receptor 5-mediated innate immunity. J Infect Dis 189:1914-1920
18. Gewirtz AT, Vijay-Kumar M, Brant SR, Duerr RH, Nicolae DL, Cho JH (2006) Dominant-negative TLR5 polymorphism reduces adaptive immune response to flagellin and negatively associates with Crohn's disease. Am J Physiol Gastrointest Liver Physiol 290:G1157-G1163
19. Gewirtz AT (2007) TLRs in the Gut. III. Immune responses to flagellin in Crohn's disease: good, bad, or irrelevant? Am J Physiol Gastrointest Liver Physiol 292:G706-G710
20. Hawn TR, Verbon A, Lettinga KD, Zhao LP, Li SS, Laws RJ, Skerrett SJ, Beutler B, Schroeder L, Nachman A, Ozinsky A, Smith KD, Aderem A (2003) A common dominant TLR5 stop codon polymorphism abolishes flagellin signaling and is associated with susceptibility to legionnaires' disease. J Exp Med 198:1563-1572
21. Hawn TR, Wu H, Grossman JM, Hahn BH, Tsao BP, Aderem A (2005) A stop codon polymorphism of Toll-like receptor 5 is associated with resistance to systemic lupus erythematosus. Proc Natl Acad Sci U S A 102:10593-10597
22. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, Aderem A (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099-1103
23. Hollander D (1992) The intestinal permeability barrier. A hypothesis as to its regulation and involvement in Crohn's disease. Scand J Gastroenterol 27:721-726
24. Konrad A, Cong Y, Duck W, Borlaza R, Elson CO (2006) Tight mucosal compartmentation of the murine immune response to antigens of the enteric microbiota. Gastroenterology 130:2050-2059
25. Lee SK, Stack A, Katzowitsch E, Aizawa SI, Suerbaum S, Josenhans C (2003) Helicobacter pylori flagellins have very low intrinsic activity to stimulate human gastric epithelial cells via TLR5. Microbes Infect 5:1345-1356
26. Ley RE, Knight R, Gordon JI (2007) The human microbiome: eliminating the biomedical/environmental dichotomy in microbial ecology. Environ Microbiol 9:3-4
27. Lodes MJ, Cong Y, Elson CO, Mohamath R, Landers CJ, Targan SR, Fort M, Hershberg RM (2004) Bacterial flagellin is a dominant antigen in Crohn disease. J Clin Invest 113:1296-1306
28. Lu W, Hisatsune A, Koga T, Kato K, Kuwahara I, Lillehoj EP, Chen W, Cross AS, Gendler SJ, Gewirtz AT, Kim KC (2006) Cutting edge: enhanced pulmonary clearance of Pseudomonas aeruginosa by Muc1 knockout mice. J Immunol 176:3890-3894
29. Lyons S, Wang L, Casanova JE, Sitaraman SV, Merlin D, Gewirtz AT (2004) Salmonella typhimurium transcytoses flagellin via an SPI2-mediated vesicular transport pathway. J Cell Sci 117:5771-5780
30. Macnab RM (2003) How bacteria assemble flagella. Annu Rev Microbiol 57:77-100
31. Manson MD, Armitage JP, Hoch JA, Macnab RM (1998) Bacterial locomotion and signal transduction. J Bacteriol 180:1009-1022
32. McDonald WF, Huleatt JW, Foellmer HG, Hewitt D, Tang J, Desai P, Price A, Jacobs A, Takahashi VN, Huang Y, Nakaar V, Alexopoulou L, Fikrig E, Powell TJ (2007) A West Nile virus recombinant protein vaccine that coactivates innate and adaptive immunity. J Infect Dis 195:1607-1617
33. McSorley SJ, Cookson BT, Jenkins MK (2000) Characterization of CD4+ T cell responses during natural infection with Salmonella typhimurium. J Immunol 164:986-993
34. McSorley SJ, Ehst BD, Yu Y, Gewirtz AT (2002) Bacterial flagellin is an effective adjuvant for CD4+ T cells in vivo. J Immunol 169:3914-3919
35. Means TK, Hayashi F, Smith KD, Aderem A, Luster AD (2003) The Toll-like receptor 5 stimulus bacterial flagellin induces maturation and chemokine production in human dendritic cells. J Immunol 170:5165-5175
36. Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, Miller SI, Aderem A (2006) Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 7:569-575
37. Miao EA, Andersen-Nissen E, Warren SE, Aderem A (2007) TLR5 and Ipaf: dual sensors of bacterial flagellin in the innate immune system. Semin Immunopathol (in press)
38. Mizel SB, West AP, Hantgan RR (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
39. Molofsky AB, Byrne BG, Whitfield NN, Madigan CA, Fuse ET, Tateda K, Swanson MS (2006) Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J Exp Med 203:1093-1104
40. Ozinsky A, Underhill DM, Fontenot JD, Hajjar AM, Smith KD, Wilson CB, Schroeder L, Aderem A (2000) The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proc Natl Acad Sci U S A 97:13766-13771
41. Reed KA, Hobert ME, Kolenda CE, Sands KA, Rathman M, O'Connor M, Lyons S, Gewirtz AT, Sansonetti PJ, Madara JL (2002) The Salmonella typhimurium flagellar basal body protein FliE is required for flagellin production and to induce a proinflammatory response in epithelial cells. J Biol Chem 277:13346-13353
42. Ren T, Zamboni DS, Roy CR, Dietrich WF, Vance RE (2006) Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog 2:e18
43. Rhee SH, Im E, Riegler M, Kokkotou E, O'Brien M, Pothoulakis C (2005) Pathophysiological role of Toll-like receptor 5 engagement by bacterial flagellin in colonic inflammation. Proc Natl Acad Sci U S A 102:13610-13615
44. Sanders CJ, Yu Y, Moore DA 3rd, Williams IR, Gewirtz AT (2006) Humoral immune response to flagellin requires T cells and activation of innate immunity. J Immunol 177:2810-2818
45. Sitaraman SV, Klapproth JM, Moore DA 3rd, Landers C, Targan S, Williams IR, Gewirtz AT (2005) Elevated flagellin-specific immunoglobulins in Crohn's disease. Am J Physiol Gastrointest Liver Physiol 288:G403-G406
46. Smith KD, Andersen-Nissen E, Hayashi F, Strobe K, Bergman MA, Barrett SL, Cookson BT, Aderem A (2003) Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat Immunol 4:1247-1253
47. Strober W, Fuss I, Mannon P (2007) The fundamental basis of inflammatory bowel disease. J Clin Invest 117:514-521
48. Subramanian N, Qadri A (2006) Lysophospholipid sensing triggers secretion of flagellin from pathogenic Salmonella. Nat Immunol 7:583-589
49. Swidsinski A, Ladhoff A, Pernthaler A, Swidsinski S, Loening-Baucke V, Ortner M, Weber J, Hoffmann U, Schreiber S, Dietel M, Lochs H (2002) Mucosal flora in inflammatory bowel disease. Gastroenterology 122:44-54
50. Uematsu S, Jang MH, Chevrier N, Guo Z, Kumagai Y, Yamamoto M, Kato H, Sougawa N, Matsui H, Kuwata H, Hemmi H, Coban C, Kawai T, Ishii KJ, Takeuchi O, Miyasaka M, Takeda K, Akira S (2006) Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c+ lamina propria cells. Nat Immunol 7:868-874
51. Vijay-Kumar M, Wu H, Jones R, Grant G, Babbin B, King TP, Kelly D, Gewirtz AT, Neish AS (2006) Flagellin suppresses epithelial apoptosis and limits disease during enteric infection. Am J Pathol 169:1686-1700
52. Vijay-Kumar M, Sanders CJ, Akira S, Neish AS, Williams IR, Uematsu S, Gewirtz AT (2007) Mice lacking TLR5 develop spontaneous colitis. J Clin Invest (in press)
53. Watson RO, Galan JE (2005) Signal transduction in Campylobacter jejuni-induced cytokine production. Cell Microbiol 7:655-665
54. Yu Y, Zeng H, Lyons S, Carlson A, Merlin D, Neish AS, Gewirtz AT (2003) TLR5-mediated activation of p38 MAPK regulates epithelial IL-8 expression via posttranscriptional mechanism. Am J Physiol Gastrointest Liver Physiol 285:G282-G290
55. Yu Y, Zeng H, Vijay-Kumar M, Neish AS, Merlin D, Sitaraman SV, Gewirtz AT (2004) STAT signaling underlies difference between flagellin-induced and tumor necrosis factor-alpha-induced epithelial gene expression. J Biol Chem 279:35210-35218
56. Yu Y, Nagai S, Wu H, Neish AS, Koyasu S, Gewirtz AT (2006) TLR5-mediated phosphoinositide 3-kinase activation negatively regulates flagellin-induced proinflammatory gene expression. J Immunol 176:6194-6201
57. Zeng H, Carlson AQ, Guo Y, Yu Y, Collier-Hyams LS, Madara JL, Gewirtz AT, Neish AS (2003) Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella. J Immunol 171:3668-3674
58. Zeng H, Wu H, Sloane V, Jones R, Yu Y, Lin P, Gewirtz AT, Neish AS (2006) Flagellin/TLR5 responses in epithelia reveal intertwined activation of inflammatory and apoptotic pathways. Am J Physiol Gastrointest Liver Physiol 290:G96-G108