Flagellin/TLR5 signalling activates renal collecting duct cells and facilitates invasion and cellular translocation of uropathogenic Escherichia coli

Cellular Microbiology

Volumn 16, Issue 10, 2014, Pages 1503-1517

  Bens, Marcelle ^a,b   Vimont, Sophie ^c   Mkaddem, Sanae Ben ^a   Chassin, Cécilia ^a,b   Goujon, Jean Michel ^d   Balloy, Viviane ^b,e   Chignard, Michel ^b,e   Werts, Catherine ^e   Vandewalle, Alain ^a,b  

^a CENTRE DE RECHERCHE SUR L INFLAMMATION   (France)

^b INSERM   (France)

^c HÔPITAL TENON   (France)

^d UNIVERSITÉ DE POITIERS   (France)

^e INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; FLAGELLIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; TOLL LIKE RECEPTOR 5; CXCL1 PROTEIN, MOUSE; CXCL2 PROTEIN, MOUSE; LIPOPOLYSACCHARIDE; TLR4 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 4;

ACUTE PYELONEPHRITIS; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; BACTERIUM ADHERENCE; BACTERIUM MUTANT; CELL INVASION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ELECTRIC RESISTANCE; FEMALE; GLOMERULUS; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMAN; INFLAMMATION; INTERNALIZATION; KIDNEY COLLECTING TUBULE; KIDNEY DISTAL TUBULE; KIDNEY MEDULLA; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; MEDIATOR RELEASE; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TIGHT JUNCTION; UROPATHOGENIC ESCHERICHIA COLI; WILD TYPE; ANIMAL; BIOSYNTHESIS; BLADDER; C57BL MOUSE; CYTOLOGY; ESCHERICHIA COLI INFECTION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PYELONEPHRITIS; URINARY TRACT INFECTION;

ANIMALS; BACTERIAL ADHESION; BACTERIAL LOAD; CHEMOKINE CXCL1; CHEMOKINE CXCL2; ESCHERICHIA COLI INFECTIONS; FEMALE; FLAGELLIN; KIDNEY TUBULES, COLLECTING; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; NEUTROPHIL INFILTRATION; NEUTROPHILS; PYELONEPHRITIS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 5; URINARY BLADDER; URINARY TRACT INFECTIONS; UROPATHOGENIC ESCHERICHIA COLI;

EID: 84908052744     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12306     Document Type: Article

References (48)

1. Andersen-Nissen, E., Smith, K.D., Strobe, K.L., Barrett, S.L., Cookson, B.T., Logan, S.M., and Aderem, A. (2005) Evasion of Toll-like receptor 5 by flagellated bacteria. Proc Natl Acad Sci USA 102: 9247-9252.
2. Andersen-Nissen, E., Hawn, T.R., Smith, K.D., Nachman, A., Lampano, A.E., Uematsu, S., et al. (2007) Cutting edge: Tlr5-/- mice are more susceptible to Escherichia coli urinary tract infection. J Immunol 178: 4717-4720.
3. Backhed, F., Soderhall, M., Ekman, P., Normark, S., and Richter-Dahlfors, A. (2001) Induction of innate immune responses by Escherichia coli and purified lipopolysaccharide correlate with organ- and cell-specific expression of Toll-like receptors within the human urinary tract. Cell Microbiol 3: 153-158.
4. Brown, P., Ki, M., and Foxman, B. (2005) Acute pyelonephritis among adults: cost of illness and considerations for the economic evaluation of therapy. Pharmacoeconomics 23: 1123-1142.
5. Broz, P., and Monack, D.M. (2011) Molecular mechanisms of inflammasome activation during microbial infections. Immunol Rev 243: 174-190.
6. Chassin, C., Goujon, J.M., Darche, S., du Merle, L., Bens, M., Cluzeaud, F., et al. (2006) Renal collecting duct epithelial cells react to pyelonephritis-associated Escherichia coli by activating distinct TLR4-dependent and -independent inflammatory pathways. J Immunol 177: 4773-4784.
7. Chassin, C., Hornef, M.W., Bens, M., Lotz, M., Goujon, J.M., Vimont, S., et al. (2007) Hormonal control of the renal immune response and antibacterial host defense by arginine vasopressin. J Exp Med 204: 2837-2852.
8. Chassin, C., Vimont, S., Cluzeaud, F., Bens, M., Goujon, J.M., Fernandez, B., et al. (2008) TLR4 facilitates translocation of bacteria across renal collecting duct cells. J Am Soc Nephrol 19: 2364-2374.
9. Chaveroche, M.K., Ghigo, J.M., and d'Enfert, C. (2000) A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulans. Nucleic Acids Res 28: E97.
10. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640- 6645.
11. Davies, J.A., and Davey, M.G. (1999) Collecting duct morphogenesis. Pediatr Nephrol 13: 535-541.
12. Duncan, M.J., Li, G., Shin, J.S., Carson, J.L., and Abraham, S.N. (2004) Bacterial penetration of bladder epithelium through lipid rafts. J Biol Chem 279: 18944-18951.
13. Erdem, A.L., Avelino, F., Xicohtencatl-Cortes, J., and Giron, J.A. (2007) Host protein binding and adhesive properties of H6 and H7 flagella of attaching and effacing Escherichia coli. J Bacteriol 189: 7426-7435.
14. Freedman, A.L. (2005) Urologic diseases in North America Project: trends in resource utilization for urinary tract infections in children. J Urol 173: 949-954.
15. Fukuzawa, N., Petro, M., Baldwin, W.M., 3rd, Gudkov, A.V., and Fairchild, R.L. (2011) A TLR5 agonist inhibits acute renal ischemic failure. J Immunol 187: 3831-3839.
16. Gauer, S., Sichler, O., Obermuller, N., Holzmann, Y., Kiss, E., Sobkowiak, E., et al. (2007) IL-18 is expressed in the intercalated cell of human kidney. Kidney Int 72: 1081-1087.
17. Gewirtz, A.T., Navas, T.A., Lyons, S., Godowski, P.J., and Madara, J.L. (2001) Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 167: 1882- 1885.
18. Hang, L., Haraoka, M., Agace, W.W., Leffler, H., Burdick, M., Strieter, R., and Svanborg, C. (1999) Macrophage inflammatory protein-2 is required for neutrophil passage across the epithelial barrier of the infected urinary tract. J Immunol 162: 3037-3044.
19. Hannan, T.J., Mysorekar, I.U., Hung, C.S., Isaacson-Schmid, M.L., and Hultgren, S.J. (2010) Early severe inflammatory responses to uropathogenic E. coli predispose to chronic and recurrent urinary tract infection. PLoS Pathog 6: e1001042.
20. Hawn, T.R., Berrington, W.R., Smith, I.A., Uematsu, S., Akira, S., Aderem, A., et al. (2007) Altered inflammatory responses in TLR5-deficient mice infected with Legionella pneumophila. J Immunol 179: 6981-6987.
21. Hawn, T.R., Scholes, D., Li, S.S., Wang, H., Yang, Y., Roberts, P.L., et al. (2009) Toll-like receptor polymorphisms and susceptibility to urinary tract infections in adult women. PLoS ONE 4: e5990.
22. Hayashi, F., Smith, K.D., Ozinsky, A., Hawn, T.R., Yi, E.C., Goodlett, D.R., et al. (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410: 1099-1103.
23. Im, J., Jeon, J.H., Cho, M.K., Woo, S.S., Kang, S.S., Yun, C.H., et al. (2009) Induction of IL-8 expression by bacterial flagellin is mediated through lipid raft formation and intracellular TLR5 activation in A549 cells. Mol Immunol 47: 614-622.
24. Lane, M.C., Lockatell, V., Monterosso, G., Lamphier, D., Weinert, J., Hebel, J.R., et al. (2005) Role of motility in the colonization of uropathogenic Escherichia coli in the urinary tract. Infect Immun 73: 7644-7656.
25. Lane, M.C., Alteri, C.J., Smith, S.N., and Mobley, H.L. (2007) Expression of flagella is coincident with uropathogenic Escherichia coli ascension to the upper urinary tract. Proc Natl Acad Sci USA 104: 16669-16674.
26. Lien, E., Means, T.K., Heine, H., Yoshimura, A., Kusumoto, S., Fukase, K., et al. (2000) Toll-like receptor 4 imparts ligand-specific recognition of bacterial lipopolysaccharide. J Clin Invest 105: 497-504.
27. Martinez, J.J., Mulvey, M.A., Schilling, J.D., Pinkner, J.S., and Hultgren, S.J. (2000) Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J 19: 2803- 2812.
28. Miao, E.A., Alpuche-Aranda, C.M., Dors, M., Clark, A.E., Bader, M.W., Miller, S.I., and Aderem, A. (2006) Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 7: 569-575.
29. Miyazaki, J., Ba-Thein, W., Kumao, T., Akaza, H., and Hayashi, H. (2002) Identification of a type III secretion system in uropathogenic Escherichia coli. FEMS Microbiol Lett 212: 221-228.
30. Molofsky, A.B., Byrne, B.G., Whitfield, N.N., Madigan, C.A., Fuse, E.T., Tateda, K., and Swanson, M.S. (2006) Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J Exp Med 203: 1093-1104.
31. Morris, A.E., Liggitt, H.D., Hawn, T.R., and Skerrett, S.J. (2009) Role of Toll-like receptor 5 in the innate immune response to acute P. aeruginosa pneumonia. Am J Physiol Lung Cell Mol Physiol 297: L1112-L1119.
32. Patole, P.S., Schubert, S., Hildinger, K., Khandoga, S., Khandoga, A., Segerer, S., et al. (2005) Toll-like receptor-4: renal cells and bone marrow cells signal for neutrophil recruitment during pyelonephritis. Kidney Int 68: 2582-2587.
33. Pichon, C., Hechard, C., du Merle, L., Chaudray, C., Bonne, I., Guadagnini, S., et al. (2009) Uropathogenic Escherichia coli AL511 requires flagellum to enter renal collecting duct cells. Cell Microbiol 11: 616-628.
34. Ren, T., Zamboni, D.S., Roy, C.R., Dietrich, W.F., and Vance, R.E. (2006) Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog 2: e18.
35. Rogers, T.J., Thorpe, C.M., Paton, A.W., and Paton, J.C. (2012) Role of lipid rafts and flagellin in invasion of colonic epithelial cells by Shiga-toxigenic Escherichia coli O113:H21. Infect Immun 80: 2858-2867.
36. Sampaio, S.C., Gomes, T.A., Pichon, C., du Merle, L., Guadagnini, S., Abe, C.M., et al. (2009) The flagella of an atypical enteropathogenic Escherichia coli strain are required for efficient interaction with and stimulation of interleukin-8 production by enterocytes in vitro. Infect Immun 77: 4406-4413.
37. Schilling, J.D., Martin, S.M., Hung, C.S., Lorenz, R.G., and Hultgren, S.J. (2003a) Toll-like receptor 4 on stromal and hematopoietic cells mediates innate resistance to uropathogenic Escherichia coli. Proc Natl Acad Sci USA 100: 4203-4208.
38. Schilling, J.D., Martin, S.M., Hunstad, D.A., Patel, K.P., Mulvey, M.A., Justice, S.S., et al. (2003b) CD14- and Tolllike receptor-dependent activation of bladder epithelial cells by lipopolysaccharide and type 1 piliated Escherichia coli. Infect Immun 71: 1470-1480.
39. Smith, K.D., Andersen-Nissen, E., Hayashi, F., Strobe, K., Bergman, M.A., Barrett, S.L., et al. (2003) Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat Immunol 4: 1247-1253.
40. Song, J., and Abraham, S.N. (2008) Innate and adaptive immune responses in the urinary tract. Eur J Clin Invest 38 (Suppl. 2): 21-28.
41. Takeuchi, O., and Akira, S. (2010) Pattern recognition receptors and inflammation. Cell 140: 805-820.
42. Tourneur, E., Ben Mkaddem, S., Chassin, C., Bens, M., Goujon, J.M., Charles, N., et al. (2013) Cyclosporine a impairs nucleotide binding oligomerization domain (nod1)-mediated innate antibacterial renal defenses in mice and human transplant recipients. PLoS Pathog 9: e1003152.
43. Tsuboi, N., Yoshikai, Y., Matsuo, S., Kikuchi, T., Iwami, K., Nagai, Y., et al. (2002) Roles of toll-like receptors in C-C chemokine production by renal tubular epithelial cells. J Immunol 169: 2026-2033.
44. Uematsu, S., Jang, M.H., Chevrier, N., Guo, Z., Kumagai, Y., Yamamoto, M., et al. (2006) Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c+ lamina propria cells. Nat Immunol 7: 868-874.
45. Van Asten, F.J., Hendriks, H.G., Koninkx, J.F., Van der Zeijst, B.A., and Gaastra, W. (2000) Inactivation of the flagellin gene of Salmonella enterica serotype enteritidis strongly reduces invasion into differentiated Caco-2 cells. FEMS Microbiol Lett 185: 175-179.
46. Wright, K.J., Seed, P.C., and Hultgren, S.J. (2005) Uropathogenic Escherichia coli flagella aid in efficient urinary tract colonization. Infect Immun 73: 7657-7668.
47. Zhang, D., Zhang, G., Hayden, M.S., Greenblatt, M.B., Bussey, C., Flavell, R.A., and Ghosh, S. (2004) A Toll-like receptor that prevents infection by uropathogenic bacteria. Science 303: 1522-1526.
48. Zhang, Z., Louboutin, J.P., Weiner, D.J., Goldberg, J.B., and Wilson, J.M. (2005) Human airway epithelial cells sense Pseudomonas aeruginosa infection via recognition of flagellin by Toll-like receptor 5. Infect Immun 73: 7151-7160.