Regulation of Toll-like receptor 5 gene expression and function on mucosal dendritic cells

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Feng, Ting ^a,b   Cong, Yingzi ^a,b,c   Alexander, Katie ^a,b   Elson, Charles O ^a,b  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIGAND; RETINOIC ACID; TOLL LIKE RECEPTOR 5; TRANSCRIPTION FACTOR FOXP3; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; EFFECTOR CELL; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; HOST CELL; IMMUNE RESPONSE; LAMINA PROPRIA; MICROFLORA; MODULATION; MOUSE; MUCOSAL DENDRITIC CELL; NONHUMAN; PROTEIN INDUCTION; RECEPTOR DOWN REGULATION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; SPLENIC DENDRITIC CELL; STROMA CELL; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; SPLEEN;

ANIMALS; BONE MARROW CELLS; CELLS, CULTURED; DENDRITIC CELLS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; SPLEEN; T-LYMPHOCYTES, REGULATORY; TOLL-LIKE RECEPTOR 5; TRANSFORMING GROWTH FACTOR ALPHA; TRETINOIN;

EID: 84860173545     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035918     Document Type: Article

References (47)

1. Akira S, Uematsu S, Takeuchi O, (2006) Pathogen recognition and innate immunity. Cell 124: 783-801.
2. 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.
3. Hall JA, Bouladoux N, Sun CM, Wohlfert EA, Blank RB, et al. (2008) Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses. Immunity 29: 637-649.
4. Cario E, (2005) Bacterial interactions with cells of the intestinal mucosa: Toll-like receptors and NOD2. Gut 54: 1182-1193.
5. Cario E, (2010) Toll-like receptors in inflammatory bowel diseases: a decade later. Inflamm Bowel Dis 16: 1583-1597.
6. Santaolalla R, Abreu MT, (2012) Innate immunity in the small intestine. Curr Opin Gastroenterol 28: 124-129.
7. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, et al. (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410: 1099-1103.
8. Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, et al. (2006) Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 7: 569-575.
9. Franchi L, Amer A, Body-Malapel M, Kanneganti TD, Ozoren N, et al. (2006) Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat Immunol 7: 576-582.
10. Smith KD, Andersen-Nissen E, Hayashi F, Strobe K, Bergman MA, 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.
11. Gewirtz AT, (2006) Flag in the crossroads: flagellin modulates innate and adaptive immunity. Curr Opin Gastroenterol 22: 8-12.
12. 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.
13. Uematsu S, Fujimoto K, Jang MH, Yang BG, Jung YJ, et al. (2008) Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat Immunol 9: 769-776.
14. Uematsu S, Jang MH, Chevrier N, Guo Z, Kumagai Y, 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. Zeng H, Carlson AQ, Guo Y, Yu Y, Collier-Hyams LS, et al. (2003) Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella. J Immunol 171: 3668-3674.
16. Kelsall BL, Leon F, (2005) Involvement of intestinal dendritic cells in oral tolerance, immunity to pathogens, and inflammatory bowel disease. Immunol Rev 206: 132-148.
17. Sun CM, Hall JA, Blank RB, Bouladoux N, Oukka M, et al. (2007) Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J Exp Med 204: 1775-1785.
18. Coombes JL, Siddiqui KR, Arancibia-Carcamo CV, Hall J, Sun CM, et al. (2007) A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med 204: 1757-1764.
19. Coombes JL, Powrie F, (2008) Dendritic cells in intestinal immune regulation. Nat Rev Immunol 8: 435-446.
20. Bosshart H, Heinzelmann M, (2007) Targeting bacterial endotoxin: two sides of a coin. Ann N Y Acad Sci 1096: 1-17.
21. Lu YC, Yeh WC, Ohashi PS, (2008) LPS/TLR4 signal transduction pathway. Cytokine 42: 145-151.
22. Fitzgerald KA, Chen ZJ, (2006) Sorting out Toll signals. Cell 125: 834-836.
23. Rakoff-Nahoum S, Medzhitov R, (2008) Innate immune recognition of the indigenous microbial flora. Mucosal Immunol 1 (Suppl 1): S10-14.
24. Sebastiani G, Leveque G, Lariviere L, Laroche L, Skamene E, et al. (2000) 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: 230-240.
25. Jordan T, Schornack S, Lahaye T, (2002) Alternative splicing of transcripts encoding Toll-like plant resistance proteins- what's the functional relevance to innate immunity? Trends Plant Sci 7: 392-398.
26. Feng T, Cong Y, Qin H, Benveniste EN, Elson CO, (2010) Generation of mucosal dendritic cells from bone marrow reveals a critical role of retinoic acid. J Immunol In press.
27. Smythies LE, Sellers M, Clements RH, Mosteller-Barnum M, Meng G, et al. (2005) Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J Clin Invest 115: 66-75.
28. Zhou L, Chong MM, Littman DR, (2009) Plasticity of CD4+ T cell lineage differentiation. Immunity 30: 646-655.
29. Goodman WA, Levine AD, Massari JV, Sugiyama H, McCormick TS, et al. (2009) IL-6 signaling in psoriasis prevents immune suppression by regulatory T cells. J Immunol 183: 3170-3176.
30. Anz D, Koelzer VH, Moder S, Thaler R, Schwerd T, et al. (2010) Immunostimulatory RNA blocks suppression by regulatory T cells. J Immunol 184: 939-946.
31. Cong Y, Feng T, Fujihashi K, Schoeb TR, Elson CO, (2009) A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota. Proc Natl Acad Sci U S A 106: 19256-19261.
32. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI, (2005) Host-bacterial mutualism in the human intestine. Science 307: 1915-1920.
33. Ley RE, Peterson DA, Gordon JI, (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124: 837-848.
34. Strober W, (2009) The multifaceted influence of the mucosal microflora on mucosal dendritic cell responses. Immunity 31: 377-388.
35. Blumberg RS, (2009) Inflammation in the intestinal tract: pathogenesis and treatment. Dig Dis 27: 455-464.
36. Vijay-Kumar M, Aitken JD, Sanders CJ, Frias A, Sloane VM, et al. (2008) Flagellin treatment protects against chemicals, bacteria, viruses, and radiation. J Immunol 180: 8280-8285.
37. Burdelya LG, Krivokrysenko VI, Tallant TC, Strom E, Gleiberman AS, et al. (2008) An agonist of toll-like receptor 5 has radioprotective activity in mouse and primate models. Science 320: 226-230.
38. Van Maele L, Carnoy C, Cayet D, Songhet P, Dumoutier L, et al. (2010) TLR5 signaling stimulates the innate production of IL-17 and IL-22 by CD3(neg)CD127+ immune cells in spleen and mucosa. J Immunol 185: 1177-1185.
39. Lodes MJ, Cong Y, Elson CO, Mohamath R, Landers CJ, et al. (2004) Bacterial flagellin is a dominant antigen in Crohn disease. J Clin Invest 113: 1296-1306.
40. Targan SR, Landers CJ, Yang H, Lodes MJ, Cong Y, et al. (2005) Antibodies to CBir1 flagellin define a unique response that is associated independently with complicated Crohn's disease. Gastroenterology 128: 2020-2028.
41. 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.
42. 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.
43. 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.
44. Bates JT, Uematsu S, Akira S, Mizel SB, (2009) Direct stimulation of tlr5+/+ CD11c+ cells is necessary for the adjuvant activity of flagellin. J Immunol 182: 7539-7547.
45. Qin H, Wang L, Feng T, Elson CO, Niyongere SA, et al. (2009) TGF-beta promotes Th17 cell development through inhibition of SOCS3. J Immunol 183: 97-105.
46. Feng T, Wang L, Schoeb TR, Elson CO, Cong Y, (2010) Microbiota innate stimulation is a prerequisite for T cell spontaneous proliferation and induction of experimental colitis. J Exp Med 207: 1321-1332.
47. Elson CO, Cong Y, Weaver CT, Schoeb TR, McClanahan TK, et al. (2007) Monoclonal anti-interleukin 23 reverses active colitis in a T cell-mediated model in mice. Gastroenterology 132: 2359-2370.