TLR5-deficient mice lack basal inflammatory and metabolic defects but exhibit impaired CD4 T cell responses to a flagellated pathogen

Journal of Immunology

Volumn 186, Issue 9, 2011, Pages 5406-5412

  Letran, Shirdi E ^a   Lee, Seung Joo ^a   Atif, Shaikh M ^a   Flores Langarica, Adriana ^b   Uematsu, Satoshi ^c,d   Akira, Shizuo ^c,d   Cunningham, Adam F ^b   McSorley, Stephen J ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c OSAKA UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN; TOLL LIKE RECEPTOR 5;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; HOST PATHOGEN INTERACTION; INFECTION RESISTANCE; INFLAMMATION; METABOLIC DISORDER; MOLECULAR CLONING; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN TARGETING; SALMONELLOSIS; TRANSGENIC MOUSE;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; FLAGELLIN; INFLAMMATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SALMONELLA INFECTIONS, ANIMAL; TOLL-LIKE RECEPTOR 5;

EID: 79955527226     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003576     Document Type: Article

References (39)

1. West, A. P., A. A. Koblansky, and S. Ghosh. 2006. Recognition and signaling by toll-like receptors. Annu. Rev. Cell Dev. Biol. 22: 409-437.
2. Mackey, D., and A. J. McFall. 2006. MAMPs and MIMPs: proposed classifications for inducers of innate immunity. Mol. Microbiol. 61: 1365-1371.
3. Rakoff-Nahoum, S., and R. Medzhitov. 2008. Innate immune recognition of the indigenous microbial flora. Mucosal Immunol. 1(Suppl 1): S10-S14.
4. 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. (Pubitemid 38962578)
5. Rakoff-Nahoum, S., L. Hao, and R. Medzhitov. 2006. Role of toll-like receptors in spontaneous commensal-dependent colitis. Immunity 25: 319-329. (Pubitemid 44224143)
6. Honko, A. N., and S. B. Mizel. 2005. Effects of flagellin on innate and adaptive immunity. Immunol. Res. 33: 83-101.
7. Salazar-Gonzalez, R. M., and S. J. McSorley. 2005. Salmonella flagellin, a microbial target of the innate and adaptive immune system. Immunol. Lett. 101: 117-122.
8. Miao, E. A., E. Andersen-Nissen, S. E. Warren, and A. Aderem. 2007. TLR5 and Ipaf: dual sensors of bacterial flagellin in the innate immune system. Semin. Immunopathol. 29: 275-288.
9. Vijay-Kumar, M., and A. T. Gewirtz. 2009. Flagellin: key target of mucosal innate immunity. Mucosal Immunol. 2: 197-205.
10. Uematsu, S., and S. Akira. 2009. Immune responses of TLR5(+) lamina propria dendritic cells in enterobacterial infection. J. Gastroenterol. 44: 803-811.
11. 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.
12. Zeng, H., A. Q. Carlson, Y. Guo, Y. Yu, L. S. Collier-Hyams, J. L. Madara, A. T. Gewirtz, and A. S. Neish. 2003. Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella. J. Immunol. 171: 3668-3674.
13. Franchi, L., J. H. Park, M. H. Shaw, N. Marina-Garcia, G. Chen, Y. G. Kim, and G. Núñez. 2008. Intracellular NOD-like receptors in innate immunity, infection and disease. Cell. Microbiol. 10: 1-8.
14. Uematsu, S., M. H. Jang, N. Chevrier, Z. Guo, Y. Kumagai, M. Yamamoto, H. Kato, N. Sougawa, H. Matsui, H. Kuwata, et al. 2006. Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c+ lamina propria cells. Nat. Immunol. 7: 868-874.
15. Feuillet, V., S. Medjane, I. Mondor, O. Demaria, P. P. Pagni, J. E. Galán, R. A. Flavell, and L. Alexopoulou. 2006. Involvement of Toll-like receptor 5 in the recognition of flagellated bacteria. Proc. Natl. Acad. Sci. USA 103: 12487-12492.
16. Andersen-Nissen, E., T. R. Hawn, K. D. Smith, A. Nachman, A. E. Lampano, S. Uematsu, S. Akira, and A. Aderem. 2007. Cutting edge: Tlr5-/- mice are more susceptible to Escherichia coli urinary tract infection. J. Immunol. 178: 4717-4720. (Pubitemid 46595250)
17. Cookson, B. T., and M. J. Bevan. 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.
18. McSorley, S. J., B. T. Cookson, and M. K. Jenkins. 2000. Characterization of CD4+ T cell responses during natural infection with Salmonella typhimurium. J. Immunol. 164: 986-993.
19. Lodes, M. J., Y. Cong, C. O. Elson, R. Mohamath, C. J. Landers, S. R. Targan, M. Fort, and R. M. Hershberg. 2004. Bacterial flagellin is a dominant antigen in Crohn disease. J. Clin. Invest. 113: 1296-1306.
20. Sanders, C. J., L. Franchi, F. Yarovinsky, S. Uematsu, S. Akira, G. Núñez, and A. T. Gewirtz. 2009. Induction of adaptive immunity by flagellin does not require robust activation of innate immunity. Eur. J. Immunol. 39: 359-371.
21. Sandoval, D. A., and R. J. Seeley. 2010. Medicine. The microbes made me eat it. Science 328: 179-180.
22. Vijay-Kumar, M., C. J. Sanders, R. T. Taylor, A. Kumar, J. D. Aitken, S. V. Sitaraman, A. S. Neish, S. Uematsu, S. Akira, I. R. Williams, and A. T. Gewirtz. 2007. Deletion of TLR5 results in spontaneous colitis in mice. J. Clin. Invest. 117: 3909-3921.
23. Vijay-Kumar, M., J. D. Aitken, A. Kumar, A. S. Neish, S. Uematsu, S. Akira, and A. T. Gewirtz. 2008. Toll-like receptor 5-deficient mice have dysregulated intestinal gene expression and nonspecific resistance to Salmonella-induced typhoidlike disease. Infect. Immun. 76: 1276-1281.
24. Vijay-Kumar, M., J. D. Aitken, F. A. Carvalho, T. C. Cullender, S. Mwangi, S. Srinivasan, S. V. Sitaraman, R. Knight, R. E. Ley, and A. T. Gewirtz. 2010. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 328: 228-231.
25. McSorley, S. J., S. Asch, M. Costalonga, R. L. Reinhardt, and M. K. Jenkins. 2002. Tracking salmonella-specific CD4 T cells in vivo reveals a local mucosal response to a disseminated infection. Immunity 16: 365-377.
26. Srinivasan, A., J. Foley, R. Ravindran, and S. J. McSorley. 2004. Low-dose Salmonella infection evades activation of flagellin-specific CD4 T cells. J. Immunol. 173: 4091-4099.
27. Barnden, M. J., J. Allison, W. R. Heath, and F. R. Carbone. 1998. Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and betachain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 76: 34-40.
28. Srinivasan, A., and S. J. McSorley. 2007. Pivotal advance: exposure to LPS suppresses CD4+ T cell cytokine production in Salmonella-infected mice and exacerbates murine typhoid. J. Leukoc. Biol. 81: 403-411.
29. Ibrahim, G. F., G. H. Fleet, M. J. Lyons, and R. A. Walker. 1985. Method for the isolation of highly purified Salmonella flagellins. J. Clin. Microbiol. 22: 1040-1044.
30. Salazar-Gonzalez, R. M., A. Srinivasan, A. Griffin, G. Muralimohan, J. M. Ertelt, R. Ravindran, A. T. Vella, and S. J. McSorley. 2007. Salmonella flagellin induces bystander activation of splenic dendritic cells and hinders bacterial replication in vivo. J. Immunol. 179: 6169-6175.
31. Cookson, B. T., L. A. Cummings, and S. L. Rassoulian Barrett. 2001. Bacterial antigens elicit T cell responses via adaptive and transitional immune recognition. Curr. Opin. Microbiol. 4: 267-273.
32. Targan, S. R., C. J. Landers, H. Yang, M. J. Lodes, Y. Cong, K. A. Papadakis, E. Vasiliauskas, C. O. Elson, and R. M. Hershberg. 2005. Antibodies to CBir1 flagellin define a unique response that is associated independently with complicated Crohn's disease. Gastroenterology 128: 2020-2028.
33. Dubinsky, M. C., Y. C. Lin, D. Dutridge, Y. Picornell, C. J. Landers, S. Farrior, I. Wrobel, A. Quiros, E. A. Vasiliauskas, B. Grill, et al; Western Regional Pediatric IBD Research Alliance. 2006. Serum immune responses predict rapid disease progression among children with Crohn's disease: immune responses predict disease progression. Am. J. Gastroenterol. 101: 360-367.
34. Letran, S. E., S. J. Lee, S. M. Atif, S. Uematsu, S. Akira, and S. J. McSorley. 2011. TLR5 functions as an endocytic receptor to enhance flagellin-specific adaptive immunity. Eur. J. Immunol. 41: 29-38.
35. Griffin, A. J., and S. J. McSorley. 2011. Development of protective immunity to Salmonella, a mucosal pathogen with a systemic agenda. Mucosal Immunol. DOI: 10.1038/mi.2011.2.
36. Salazar-Gonzalez, R. M., J. H. Niess, D. J. Zammit, R. Ravindran, A. Srinivasan, J. R. Maxwell, T. Stoklasek, R. Yadav, I. R. Williams, X. Gu, et al. 2006. CCR6- mediated dendritic cell activation of pathogen-specific T cells in Peyer's patches. Immunity 24: 623-632. (Pubitemid 43744358)
37. Sierro, F., B. Dubois, A. Coste, D. Kaiserlian, J. P. Kraehenbuhl, and J. C. Sirard. 2001. Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc. Natl. Acad. Sci. USA 98: 13722-13727.
38. Williams, I. R. 2006. CCR6 and CCL20: partners in intestinal immunity and lymphorganogenesis. Ann. N. Y. Acad. Sci. 1072: 52-61.
39. +/+ CD11c+ cells is necessary for the adjuvant activity of flagellin. J. Immunol. 182: 7539-7547.