Differential Roles of Interleukin-17A and -17F in Host Defense against Mucoepithelial Bacterial Infection and Allergic Responses

Immunity

Volumn 30, Issue 1, 2009, Pages 108-119

  Ishigame, Harumichi ^a   Kakuta, Shigeru ^a   Nagai, Takeshi ^a   Kadoki, Motohiko ^a   Nambu, Aya ^a   Komiyama, Yutaka ^a   Fujikado, Noriyuki ^a   Tanahashi, Yuko ^a   Akitsu, Aoi ^a   Kotaki, Hayato ^a   Sudo, Katsuko ^a   Nakae, Susumu ^a   Sasakawa, Chihiro ^a   Iwakura, Yoichiro ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

CELLIMMUNO; MOLIMMUNO

Indexed keywords

BETA DEFENSIN; INTERLEUKIN 17; INTERLEUKIN 17F;

ALLERGIC ENCEPHALOMYELITIS; ALLERGIC REACTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTHRITIS; ARTICLE; BACTERIAL INFECTION; BAGG ALBINO MOUSE; C57BL 6 MOUSE; CITROBACTER RODENTIUM; CYTOKINE PRODUCTION; EPITHELIUM CELL; HOST RESISTANCE; HYPERSENSITIVITY; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STAPHYLOCOCCUS INFECTION; T LYMPHOCYTE; TRANSGENIC MOUSE;

ANIMALS; ARTHRITIS; BACTERIAL INFECTIONS; CELLS, CULTURED; CYTOKINES; FLOW CYTOMETRY; HYPERSENSITIVITY; INTERLEUKIN-17; MICE; MICE, KNOCKOUT;

EID: 58149231532     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2008.11.009     Document Type: Article

References (50)

1. Antonysamy M.A., Fanslow W.C., Fu F., Li W., Qian S., Troutt A.B., and Thomson A.W. Evidence for a role of IL-17 in organ allograft rejection: IL-17 promotes the functional differentiation of dendritic cell progenitors. J. Immunol. 162 (1999) 577-584
2. H17 and regulatory T cells. Nature 441 (2006) 235-238
3. Bry L., and Brenner M.B. Critical role of T cell-dependent serum antibody, but not the gut-associated lymphoid tissue, for surviving acute mucosal infection with Citrobacter rodentium, an attaching and effacing pathogen. J. Immunol. 172 (2004) 433-441
4. Coury F., Annels N., Rivollier A., Olsson S., Santoro A., Speziani C., Azocar O., Flacher M., Djebali S., Tebib J., et al. Langerhans cell histiocytosis reveals a new IL-17A-dependent pathway of dendritic cell fusion. Nat. Med. 14 (2008) 81-87
5. Da Silva C.A., Hartl D., Liu W., Lee C.G., and Elias J.A. TLR-2 and IL-17A in chitin-induced macrophage activation and acute inflammation. J. Immunol. 181 (2008) 4279-4286
6. Happel K.I., Dubin P.J., Zheng M., Ghilardi N., Lockhart C., Quinton L.J., Odden A.R., Shellito J.E., Bagby G.J., Nelson S., and Kolls J.K. Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 202 (2005) 761-769
7. Horai R., Nakajima A., Habiro K., Kotani M., Nakae S., Matsuki T., Nambu A., Saijo S., Kotaki H., Sudo K., et al. TNF-α is crucial for the development of autoimmune arthritis in IL-1 receptor antagonist-deficient mice. J. Clin. Invest. 114 (2004) 1603-1611
8. Hue S., Ahern P., Buonocore S., Kullberg M.C., Cua D.J., McKenzie B.S., Powrie F., and Maloy K.J. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J. Exp. Med. 203 (2006) 2473-2483
9. Hurst S.D., Muchamuel T., Gorman D.M., Gilbert J.M., Clifford T., Kwan S., Menon S., Seymour B., Jackson C., Kung T.T., et al. New IL-17 family members promote Th1 or Th2 responses in the lung: In vivo function of the novel cytokine IL-25. J. Immunol. 169 (2002) 443-453
10. Hymowitz S.G., Filvaroff E.H., Yin J.P., Lee J., Cai L., Risser P., Maruoka M., Mao W., Foster J., Kelley R.F., et al. IL-17s adopt a cystine knot fold: Structure and activity of a novel cytokine, IL-17F, and implications for receptor binding. EMBO J. 20 (2001) 5332-5341
11. + T helper cells. Cell 126 (2006) 1121-1133
12. Jovanovic D.V., Di Battista J.A., Martel-Pelletier J., Jolicoeur F.C., He Y., Zhang M., Mineau F., and Pelletier J.P. IL-17 stimulates the production and expression of proinflammatory cytokines, IL-β and TNF-α, by human macrophages. J. Immunol. 160 (1998) 3513-3521
13. Kao C.Y., Chen Y., Thai P., Wachi S., Huang F., Kim C., Harper R.W., and Wu R. IL-17 markedly up-regulates β-defensin-2 expression in human airway epithelium via JAK and NF-κB signaling pathways. J. Immunol. 173 (2004) 3482-3491
14. Kawaguchi M., Adachi M., Oda N., Kokubu F., and Huang S.K. IL-17 cytokine family. J. Allergy Clin. Immunol. 114 (2004) 1265-1273
15. Kolls J.K., and Linden A. Interleukin-17 family members and inflammation. Immunity 21 (2004) 467-476
16. Komiyama Y., Nakae S., Matsuki T., Nambu A., Ishigame H., Kakuta S., Sudo K., and Iwakura Y. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J. Immunol. 177 (2006) 566-573
17. H17 cells. Nature 448 (2007) 484-487
18. Kramer J.M., Yi L., Shen F., Maitra A., Jiao X., Jin T., and Gaffen S.L. Evidence for ligand-independent multimerization of the IL-17 receptor. J. Immunol. 176 (2006) 711-715
19. Kuestner R.E., Taft D.W., Haran A., Brandt C.S., Brender T., Lum K., Harder B., Okada S., Ostrander C.D., Kreindler J.L., et al. Identification of the IL-17 receptor related molecule IL-17RC as the receptor for IL-17F. J. Immunol. 179 (2007) 5462-5473
20. LeBlanc P.M., Yeretssian G., Rutherford N., Doiron K., Nadiri A., Zhu L., Green D.R., Gruenheid S., and Saleh M. Caspase-12 modulates NOD signaling and regulates antimicrobial peptide production and mucosal immunity. Cell Host Microbe 3 (2008) 146-157
21. LeibundGut-Landmann S., Gross O., Robinson M.J., Osorio F., Slack E.C., Tsoni S.V., Schweighoffer E., Tybulewicz V., Brown G.D., Ruland J., and Reis e Sousa C. Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat. Immunol. 8 (2007) 630-638
22. Liang S.C., Tan X.Y., Luxenberg D.P., Karim R., Dunussi-Joannopoulos K., Collins M., and Fouser L.A. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J. Exp. Med. 203 (2006) 2271-2279
23. H17 lineage. Nature 441 (2006) 231-234
24. McGeachy M.J., and Cua D.J. Th17 cell differentiation: The long and winding road. Immunity 28 (2008) 445-453
25. H17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature 452 (2008) 773-776
26. Mundy R., MacDonald T.T., Dougan G., Frankel G., and Wiles S. Citrobacter rodentium of mice and man. Cell. Microbiol. 7 (2005) 1697-1706
27. Nagai T., Abe A., and Sasakawa C. Targeting of enteropathogenic Escherichia coli EspF to host mitochondria is essential for bacterial pathogenesis: Critical role of the 16th leucine residue in EspF. J. Biol. Chem. 280 (2005) 2998-3011
28. Nakae S., Komiyama Y., Nambu A., Sudo K., Iwase M., Homma I., Sekikawa K., Asano M., and Iwakura Y. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17 (2002) 375-387
29. Nakae S., Nambu A., Sudo K., and Iwakura Y. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J. Immunol. 171 (2003) 6173-6177
30. Nakae S., Saijo S., Horai R., Sudo K., Mori S., and Iwakura Y. IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc. Natl. Acad. Sci. USA 100 (2003) 5986-5990
31. Nakae S., Suto H., Berry G.J., and Galli S.J. Mast cell-derived TNF can promote Th17 cell-dependent neutrophil recruitment in ovalbumin-challenged OTII mice. Blood 109 (2007) 3640-3648
32. Nakane A., Okamoto M., Asano M., Kohanawa M., and Minagawa T. Endogenous γ interferon, tumor necrosis factor, and interleukin-6 in Staphylococcus aureus infection in mice. Infect. Immun. 63 (1995) 1165-1172
33. Nurieva R., Yang X.O., Martinez G., Zhang Y., Panopoulos A.D., Ma L., Schluns K., Tian Q., Watowich S.S., Jetten A.M., and Dong C. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 448 (2007) 480-483
34. Oboki K., Ohno T., Saito H., and Nakae S. Th17 and Allergy. Allergol. Int. 57 (2008) 121-134
35. Oda N., Canelos P.B., Essayan D.M., Plunkett B.A., Myers A.C., and Huang S.K. Interleukin-17F induces pulmonary neutrophilia and amplifies antigen-induced allergic response. Am. J. Respir. Crit. Care Med. 171 (2005) 12-18
36. Ouyang W., Kolls J.K., and Zheng Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28 (2008) 454-467
37. Park H., Li Z., Yang X.O., Chang S.H., Nurieva R., Wang Y.H., Wang Y., Hood L., Zhu Z., Tian Q., and Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6 (2005) 1133-1141
38. Rickel E.A., Siegel L.A., Yoon B.R., Rottman J.B., Kugler D.G., Swart D.A., Anders P.M., Tocker J.E., Comeau M.R., and Budelsky A.L. Identification of functional roles for both IL-17RB and IL-17RA in mediating IL-25-induced activities. J. Immunol. 181 (2008) 4299-4310
39. Schwarzenberger P., and Kolls J.K. Interleukin 17: An example for gene therapy as a tool to study cytokine mediated regulation of hematopoiesis. J. Cell. Biochem. Suppl. 38 (2002) 88-95
40. Simmons C.P., Goncalves N.S., Ghaem-Maghami M., Bajaj-Elliott M., Clare S., Neves B., Frankel G., Dougan G., and MacDonald T.T. Impaired resistance and enhanced pathology during infection with a noninvasive, attaching-effacing enteric bacterial pathogen, Citrobacter rodentium, in mice lacking IL-12 or IFN-γ. J. Immunol. 168 (2002) 1804-1812
41. Suzuki S., Kokubu F., Kawaguchi M., Homma T., Odaka M., Watanabe S., Ieki K., Matsukura S., Kurokawa M., Takeuchi H., et al. Expression of interleukin-17F in a mouse model of allergic asthma. Int. Arch. Allergy Immunol. 143 Suppl 1 (2007) 89-94
42. Toy D., Kugler D., Wolfson M., Vanden Bos T., Gurgel J., Derry J., Tocker J., and Peschon J. Cutting edge: Interleukin 17 signals through a heteromeric receptor complex. J. Immunol. 177 (2006) 36-39
43. van Beelen A.J., Zelinkova Z., Taanman-Kueter E.W., Muller F.J., Hommes D.W., Zaat S.A., Kapsenberg M.L., and de Jong E.C. Stimulation of the intracellular bacterial sensor NOD2 programs dendritic cells to promote interleukin-17 production in human memory T cells. Immunity 27 (2007) 660-669
44. Veldhoen M., Hocking R.J., Atkins C.J., Locksley R.M., and Stockinger B. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24 (2006) 179-189
45. Veldhoen M., Hocking R.J., Flavell R.A., and Stockinger B. Signals mediated by transforming growth factor-β initiate autoimmune encephalomyelitis, but chronic inflammation is needed to sustain disease. Nat. Immunol. 7 (2006) 1151-1156
46. Weaver C.T., Hatton R.D., Mangan P.R., and Harrington L.E. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol. 25 (2007) 821-852
47. Wright J.F., Bennett F., Li B., Brooks J., Luxenberg D.P., Whitters M.J., Tomkinson K.N., Fitz L.J., Wolfman N.M., Collins M., et al. The human IL-17F/IL-17A heterodimeric cytokine signals through the IL-17RA/IL-17RC receptor complex. J. Immunol. 181 (2008) 2799-2805
48. Yang X.O., Chang S.H., Park H., Nurieva R., Shah B., Acero L., Wang Y.H., Schluns K.S., Broaddus R.R., Zhu Z., and Dong C. Regulation of inflammatory responses by IL-17F. J. Exp. Med. 205 (2008) 1063-1075
49. Zheng Y., Valdez P.A., Danilenko D.M., Hu Y., Sa S.M., Gong Q., Abbas A.R., Modrusan Z., Ghilardi N., de Sauvage F.J., and Ouyang W. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14 (2008) 282-289
50. H-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat. Immunol. 8 (2007) 967-974