Activation of eosinophils by IL-12 family cytokine IL-27: Implications of the pleiotropic roles of IL-27 in allergic responses

Immunobiology

Volumn 216, Issue 1-2, 2011, Pages 54-65

  Hu, Shuiqing ^a,c   Wong, Chun Kwok ^a   Lam, Christopher Wai Kei ^a,b  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b MACAU UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Macao)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Apoptosis; Chemokines; Cytokines; Eosinophils; Signal transduction

Indexed keywords

CXCL1 CHEMOKINE; CYTOKINE RECEPTOR; GLYCOPROTEIN GP 130; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 25; INTERLEUKIN 27; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN WSX 1; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ALLERGY; APOPTOSIS; ARTICLE; CELL STIMULATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME REGULATION; EOSINOPHIL; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; LYMPHOCYTE ACTIVATION; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TH2 CELL;

EID: 78649522921     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imbio.2010.03.004     Document Type: Article

References (46)

1. Amadi-Obi A., Yu C.R., Liu X., Mahdi R.M., Clarke G.L., Nussenblatt R.B., Gery I., Lee Y.S., Egwuagu C.E. TH17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1. Nat. Med. 2007, 13:711-718.
2. Artis D., Villarino A., Silverman M., He W., Thornton E.M., Mu S., Summer S., Covey T.M., Huang E., Yoshida H., Koretzky G., Goldschmidt M., Wu G.D., de Sauvage F., Miller H.R., Saris C.J., Scott P., Hunter C.A. The IL-27 receptor (WSX-1) is an inhibitor of innate and adaptive elements of type 2 immunity. J. Immunol. 2004, 173:5626-5634.
3. Awasthi A., Carrier Y., Peron J.P., Bettelli E., Kamanaka M., Flavell R.A., Kuchroo V.K., Oukka M., Weiner H.L. A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells. Nat. Immunol. 2007, 8:1380-1389.
4. Baldwin A.S. The NF-κB and IκB proteins: new discoveries and insights. Annu. Rev. Immunol. 1996, 14:649-683.
5. Batten M., Ghilardi N. The biology and therapeutic potential of interleukin 27. J. Mol. Med. 2007, 85:661-672.
6. Batten M., Li J., Yi S., Kljavin N.M., Danilenko D.M., Lucas S., Lee J., de Sauvage F.J., Ghilardi N. Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat. Immunol. 2006, 7:929-936.
7. Chae S.C., Li C.S., Kim K.M., Yang J.Y., Zhang Q., Lee Y.C., Yang Y.S., Chung H.T. Identification of polymorphisms in human interleukin-27 and their association with asthma in a Korean population. J. Hum. Genet. 2007, 52:355-361.
8. Chen Q., Ghilardi N., Wang H., Baker T., Xie M.H., Gurney A., Grewal I.S., de Sauvage F.J. Development of Th1-type immune responses requires the type I cytokine receptor TCCR. Nature 2000, 407:916-920.
9. Cheung P.F., Wong C.K., Ip W.K., Lam C.W. IL-25 regulates the expression of adhesion molecules on eosinophils: mechanism of eosinophilia in allergic inflammation. Allergy 2006, 61:878-885.
10. Cheung P.F., Wong C.K., Lam C.W. Molecular mechanisms of cytokine and chemokine release from eosinophils activated by IL-17A, IL-17F, and IL-23: implication for Th17 lymphocytes-mediated allergic inflammation. J. Immunol. 2008, 180:5625-5635.
11. Fitzgerald D.C., Zhang G.X., El-Behi M., Fonseca-Kelly Z., Li H., Yu S., Saris C.J., Gran B., Ciric B., Rostami A. Suppression of autoimmune inflammation of the central nervous system by interleukin 10 secreted by interleukin 27-stimulated T cells. Nat. Immunol. 2007, 8:1372-1379.
12. Fujita H., Teng A., Nozawa R., Takamoto-Matsui Y., Katagiri-Matsumura H., Ikezawa Z., Ishii Y. Production of both IL-27 and IFN-gamma after the treatment with a ligand for invariant NK T cells is responsible for the suppression of Th2 response and allergic inflammation in a mouse experimental asthma model. J. Immunol. 2009, 183:254-260.
13. Goriely S., Cavoy R., Goldman M. Interleukin-12 family members and type I interferons in Th17-mediated inflammatory disorders. Allergy 2009, 64:702-709.
14. Hamano S., Himeno K., Miyazaki Y., Ishii K., Yamanaka A., Takeda A., Zhang M., Hisaeda H., Mak T.W., Yoshimura A., Yoshida H. WSX-1 is required for resistance to Trypanosoma cruzi infection by regulation of proinflammatory cytokine production. Immunity 2003, 19:657-667.
15. Ho A.W., Wong C.K., Lam C.W. Tumor necrosis factor-alpha up-regulates the expression of CCL2 and adhesion molecules of human proximal tubular epithelial cells through MAPK signaling pathways. Immunobiology 2008, 213:533-544.
16. Hogan S.P., Rosenberg H.F., Moqbel R., Phipps S., Foster P.S., Lacy P., Kay A.B., Rothenberg M.E. Eosinophils: biological properties and role in health and disease. Clin. Exp. Allergy 2008, 38:709-750.
17. Hölscher C., Hölscher A., Rückerl D., Yoshimoto T., Yoshida H., Mak T., Saris C., Ehlers S. The IL-27 receptor chain WSX-1 differentially regulates antibacterial immunity and survival during experimental tuberculosis. J. Immunol. 2005, 174:3534-3544.
18. Ilarregui J.M., Croci D.O., Bianco G.A., Toscano M.A., Salatino M., Vermeulen M.E., Geffner J.R., Rabinovich G.A. Tolerogenic signals delivered by dendritic cells to T cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10. Nat. Immunol. 2009, 10:981-991.
19. Kalliolias G.D., Ivashkiv L.B. IL-27 activates human monocytes via STAT1 and suppresses IL-10 production but the inflammatory functions of IL-27 are abrogated by TLRs and p38. J. Immunol. 2008, 180:6325-6333.
20. Kanda N., Watanabe T. IL-12, IL-23, and IL-27 enhance human β-defensin-2 production in human keratinocytes. Eur. J. Immunol. 2008, 38:1287-1296.
21. Kastelein R.A., Hunter C.A., Cua D.J. Discovery and biology of IL-23 and IL-27: related but functionally distinct regulators of inflammation. Annu. Rev. Immunol. 2007, 25:221-242.
22. Larousserie F., Charlot P., Bardel E., Froger J., Kastelein R.A., Devergne O. Differential effects of IL-27 on human B cell subsets. J. Immunol. 2006, 176:5890-5897.
23. Miyazaki Y., Inoue H., Matsumura M., Matsumoto K., Nakano T., Tsuda M., Hamano S., Yoshimura A., Yoshida H. Exacerbation of experimental allergic asthma by augmented Th2 responses in WSX-1-deficient mice. J. Immunol. 2005, 175:2401-2407.
24. Murugaiyan G., Mittal A., Lopez-Diego R., Maier L.M., Anderson D.E., Weiner H.L. IL-27 is a key regulator of IL-10 and IL-17 production by human CD4+ T cells. J. Immunol. 2009, 183:2435-2443.
25. Nieuwenhuis E.E., Neurath M.F., Corazza N., Iijima H., Trgovcich J., Wirtz S., Glickman J., Bailey D., Yoshida M., Galle P.R., Kronenberg M., Birkenbach M., Blumberg R.S. Disruption of T helper 2-immune responses in Epstein-Barr virus-induced gene 3-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:16951-16956.
26. Nutku E., Zhuang Q., Soussi-Gounni A., Aris F., Mazer B.D., Hamid Q. Functional expression of IL-12 receptor by human eosinophils: IL-12 promotes eosinophil apoptosis. J. Immunol. 2001, 167:1039-1046.
27. Owaki T., Asakawa M., Kamiya S., Takeda K., Fukai F., Mizuguchi J., Yoshimoto T. IL-27 suppresses CD28-mediated IL-2 production through suppressor of cytokine signaling 3. J. Immunol. 2006, 176:2773-2780.
28. Owaki T., Asakawa M., Morishima N., Hata K., Fukai F., Matsui M., Mizuguchi J., Yoshimoto T. A role for IL-27 in early regulation of Th1 differentiation. J. Immunol. 2005, 175:2191-2200.
29. Pflanz S., Hibbert L., Mattson J., Rosales R., Vaisberg E., Bazan J.F., Phillips J.H., McClanahan T.K., de Waal Malefyt R., Kastelein R.A. WSX-1 and glycoprotein 130 constitute a signal-transducing receptor for IL-27. J. Immunol. 2004, 172:2225-2231.
30. Pflanz S., Timans J.C., Cheung J., Rosales R., Kanzler H., Gilbert J., Hibbert L., Churakova T., Travis M., Vaisberg E., Blumenschein W.M., Mattson J.D., Wagner J.L., To W., Zurawski S., McClanahan T.K., Gorman D.M., Bazan J.F., de Waal Malefyt R., Rennick D., Kastelein R.A. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells. Immunity 2002, 16:779-790.
31. Plötz S.G., Lentschat A., Behrendt H., Plötz W., Hamann L., Ring J., Rietschel E.T., Flad H.D., Ulmer A.J. The interaction of human peripheral blood eosinophils with bacterial lipopolysaccharide is CD14 dependent. Blood 2001, 97:235-241.
32. Roebuck K.A., Finnegan A. Regulation of intercellular adhesion molecule-1 (CD54) gene expression. J. Leukoc. Biol. 1999, 66:876-888.
33. Shimizu M., Shimamura M., Owaki T., Asakawa M., Fujita K., Kudo M., Iwakura Y., Takeda Y., Luster A.D., Mizuguchi J., Yoshimoto T. Antiangiogenic and antitumor activities of IL-27. J. Immunol. 2006, 176:7317-7324.
34. Simon D., Braathen L.R., Simon H.U. Eosinophils and atopic dermatitis. Allergy 2004, 59:561-570.
35. Spencer L.A., Szela C.T., Perez S.A., Kirchhoffer C.L., Neves J.S., Radke A.L., Weller P.F. Human eosinophils constitutively express multiple Th1, Th2, and immunoregulatory cytokines that are secreted rapidly and differentially. J. Leukoc. Biol. 2009, 85:117-123.
36. Stumhofer J.S., Laurence A., Wilson E.H., Huang E., Tato C.M., Johnson L.M., Villarino A.V., Huang Q., Yoshimura A., Sehy D., Saris C.J., O'Shea J.J., Hennighausen L., Ernst M., Hunter C.A. Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat. Immunol. 2006, 7:937-945.
37. Stumhofer J.S., Silver J.S., Laurence A., Porrett P.M., Harris T.H., Turka L.A., Ernst M., Saris C.J., O'Shea J.J., Hunter C.A. Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10. Nat. Immunol. 2007, 8:1363-1371.
38. Takashi S., Okubo Y., Horie S. Contribution of CD54 to human eosinophil and neutrophil superoxide production. J. Appl. Physiol. 2001, 91:613-622.
39. Takeda A., Hamanom S., Yamanaka A., Hanada T., Ishibashi T., Mak T.W., Yoshimura A., Yoshida H. Cutting edge: role of IL-27/WSX-1 signaling for induction of T-Bet through activation of STAT1 during initial Th1 commitment. J. Immunol. 2003, 170:4886-4890.
40. Villarino A., Hibbert L., Lieberman L., Wilson E., Mak T., Yoshida H., Kastelein R.A., Saris C., Hunter C.A. The IL-27R (WSX-1) is required to suppress T cell hyperactivity during infection. Immunity 2003, 19:645-655.
41. Wong C.K., Cheung P.F., Lam C.W. Leptin-mediated cytokine release and migration of eosinophils: implications for immunopathophysiology of allergic inflammation. Eur. J. Immunol. 2007, 37:2337-2348.
42. Wong C.K., Ip W.K., Lam C.W. Interleukin-3,-5, and granulocyte macrophage colony-stimulating factor-induced adhesion molecule expression on eosinophils by p38 mitogen-activated protein kinase and nuclear factor-κB. Am. J. Respir. Cell Mol. Biol. 2003, 29:133-147.
43. Yamanaka A., Hamano S., Miyazaki Y., Ishii K., Takeda A., Mak T.W., Himeno K., Yoshimura A., Yoshida H. Hyperproduction of proinflammatory cytokines by WSX-1-deficient NKT cells in concanavalin A-induced hepatitis. J. Immunol. 2004, 172:3590-3596.
44. Yang J., Yang M., Htut T.M., Ouyang X., Hanidu A., Li X., Sellati R., Jiang H., Zhang S., Li H., Zhao J., Ting A.T., Mayer L., Unkeless J.C., Labadia M.E., Hodge M., Li J., Xiong H. Epstein-Barr virus-induced gene 3 negatively regulates IL-17, IL-22 and RORgamma t. Eur. J. Immunol. 2008, 38:1204-1214.
45. Yoshida H., Hamano S., Senaldi G., Covey T., Faggioni R., Mu S., Xia M., Wakeham A.C., Nishina H., Potter J., Saris C.J., Mak T.W. WSX-1 is required for the initiation of Th1 responses and resistance to L. major infection. Immunity 2001, 15:569-578.
46. Yoshimoto T., Yoshimoto T., Yasuda K., Mizuguchi J., Nakanishi K. IL-27 suppresses Th2 cell development and Th2 cytokines production from polarized Th2 cells: a novel therapeutic way for Th2-mediated allergic inflammation. J. Immunol. 2007, 179:4415-4423.