Biology of recently discovered cytokines: Discerning the pro- and anti-inflammatory properties of interleukin-27

Arthritis Research and Therapy

Volumn 6, Issue 5, 2004, Pages 225-233

  Villarino, Alejandro V ^a   Hunter, Christopher A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

IL 27; Infection; Th1; Th2; WSX 1

Indexed keywords

AUTOANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 27; INTERLEUKIN 6; INTERLEUKIN RECEPTOR; STAT PROTEIN; TOLL LIKE RECEPTOR;

ANTIINFLAMMATORY ACTIVITY; AUTOIMMUNITY; CELL FUNCTION; CROHN DISEASE; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; EFFECTOR CELL; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HOST; HUMAN; IMMUNE RESPONSE; IMMUNITY; INFECTION RESISTANCE; INFLAMMATION; LEISHMANIA MAJOR; LISTERIA; MOLECULAR BIOLOGY; MOLECULAR MECHANICS; MOUSE; MYCOBACTERIUM; NONHUMAN; PLEIOTROPY; PROTEIN FAMILY; RAT; REVIEW; RHEUMATOID ARTHRITIS; SARCOIDOSIS; STREPTOCOCCUS PYOGENES; TH1 CELL; TH2 CELL; TOXOPLASMA GONDII; TRICHURIS; TRYPANOSOMA CRUZI;

ANIMALS; CYTOKINES; HUMANS; INFLAMMATION; INTERLEUKINS;

EID: 12344288451     PISSN: 14786354     EISSN: None     Source Type: Journal    
DOI: 10.1186/ar1227     Document Type: Review

References (71)

1. Boulay JL, O'Shea JJ, Paul WE: Molecular phylogeny within type I cytokines and their cognate receptors. Immunity 2003, 19:159-163.
2. Villarino AV, Huang E, Hunter CA: Understanding the pro- and anti-inflammatory properties of IL-27. J Immunol 2004, 173: 715-720.
3. + T cells. Immunity 2002, 16: 779-790.
4. Heinrich PC, Behrmann I, Muller-Newen G, Schaper F, Graeve L: Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem J 1998, 334:297-314.
5. Devergne O, Hummel M, Koeppen H, Le Beau MM, Nathanson EC, Kieff E, Birkenbach M: A novel interleukin-12 p40-related protein induced by latent Epstein-Barr virus infection in B lymphocytes. J Virol 1996, 70:1143-1153.
6. Hibbert L, Pflanz S, De Waal Malefyt R, Kastelein RA: IL-27 and IFN-alpha signal via Stat1 and Stat3 and induce T-Bet and IL-12Rbeta2 in naive T cells. J Interferon Cytokine Res 2003, 23:513-522.
7. Larousserie F, Pflanz S, Coulomb-L'Hermine A, Brousse N, Kastelein R, Devergne O: Expression of IL-27 in human Th1-associated granulomatous diseases. J Pathol 2004, 202:164-171.
8. Niedobitek G, Pazolt D, Teichmann M, Devergne O: Frequent expression of the Epstein-Barr virus (EBV)-induced gene, EBI3, an IL-12 p40-related cytokine, in Hodgkin and Read-Sternberg cells. J Pathol 2002, 198:310-316.
9. Devergne O, Cahir McFarland ED, Mosialos G, Izumi KM, Ware CF, Kieff E: Role of the TRAF binding site and NF-kappaB activation in Epstein-Barr virus latent membrane protein 1-induced cell gene expression. J Virol 1998, 72:7900-7908.
10. van Seventer JM, Nagai T, van Seventer GA: Interferon-beta differentially regulates expression of the IL-12 family members p35, p40, p19 and EBI3 in activated human dendritic cells. J Neuroimmunol 2002, 133:60-71.
11. Hashimoto SI, Suzuki T, Nagai S, Yamashita T, Toyoda N, Matsushima K: Identification of genes specifically expressed in human activated and mature dendritic cells through serial analysis of gene expression. Blood 2000, 96:2206-2214.
12. Croy BA, He H, Esadeg S, Wei Q, McCartney D, Zhang J, Borzychowski A, Ashkar AA, Black GP, Evans SS, et al.: Uterine natural killer cells: insights into their cellular and molecular biology from mouse modelling. Reproduction 2003, 126:149-160.
13. Devergne O, Coulomb-L'Hermine A, Capel F, Moussa M, Capron F: Expression of Epstein-Barr virus-induced gene 3, an interleukin-12 p40-related molecule, throughout human pregnancy: involvement of syncytiotrophoblasts and extravillous trophoblasts. Am J Pathol 2001, 159:1763-1776.
14. Christ AD, Stevens AC, Koeppen H, Walsh S, Omata F, Devergne O, Birkenbach M, Blumberg RS: An interleukin 12-related cytokine is up-regulated in ulcerative colitis but not in Crohn's disease. Gastroenterology 1998, 115:307-313.
15. Omata F, Birkenbach M, Matsuzaki S, Christ AD, Blumberg RS: The expression of IL-12 p40 and its homologue, Epstein-Barr virus-induced gene 3, in inflammatory bowel disease. Inflamm Bowel Dis 2001, 7:215-220.
16. Gehlert T, Devergne O, Niedobitek G: Epstein-Barr virus (EBV) infection and expression of the interleukin-12 family member EBV-induced gene 3 (EBI3) in chronic inflammatory bowel disease. J Med Virol 2004, 73:432-438.
17. Nagai T, Devergne O, Mueller TF, Perkins DL, van Seventer JM, van Seventer GA: Timing of IFN-beta exposure during human dendritic cell maturation and naive Th cell stimulation has contrasting effects on Th1 subset generation: a role for IFN-beta-mediated regulation of IL-12 family cytokines and IL-18 in naive Th cell differentiation. J Immunol 2003, 171:5233-5243.
18. Redecke V, Hacker H, Datta SK, Fermin A, Pitha PM, Broide DH, Raz E: Cutting edge: Activation of toll-like receptor 2 induces a Th2 immune response and promotes experimental asthma. J Immunol 2004, 172:2739-2743.
19. Smits HH, Van Beelen AJ, Hessle C, Westland R, De Jong E, Soeteman E, Wold A, Wierenga EA, Kapsenberg ML: Commensal Gram-negative bacteria prime human dendritic cells for enhanced IL-23 and IL-27 expression and enhanced Th1 development. Eur J Immunol 2004, 34:1371-1380.
20. Veckman V, Miettinen M, Pirhonen J, Siren J, Matikainen S, Julkunen I: Streptococcus pyogenes and Lactobacillus rhamnosus differentially induce maturation and production of Th1-type cytokines and chemokines in human monocyte-derived dendritic cells. J Leukoc Biol 2004, 75:764-771.
21. Villarino A, Hibbert L, Lieberman L, Wilson E, Mak T, Yoshida H, Kastelein RA, Saris C, Hunter CA: The IL-27R (WSX-1) is required to suppress T cell hyperactivity during infection. Immunity 2003, 19:645-655.
22. Artis D, Villarino A, Silverman M, He V, Mu S, Summer S, Covey T, Huang E, Yoshida H, Koretzky G, et al.: The IL-27R (WSX-1) inhibits innate and adaptive elements of intestinal helminth-induced T helper 2 responses. J Immunol 2004:in press.
23. Bancroft AJ, Humphreys NE, Worthington JJ, Yoshida H, Grencis RK: WSX-1: a key role in induction of chronic intestinal nematode infection. J Immunol 2004, 172:7635-7641.
24. Trinchieri G, Pflanz S, Kastelein RA: The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity 2003, 19:641-644.
25. Trinchieri G: Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 2003, 3: 33-146.
26. Cua DJ, Sherlock J, Chen Y, Murphy CA, Joyce B, Seymour B, Lucian L, To W, Kwan S, Churakova T, Zurawski S, Wiekowski M, Lira SA, Gorman D, Kastelein RA, Sedgwick JD: Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003, 421:744-748.
27. Oppmann B, Lesley R, Blom B, Timans JC, Xu Y, Hunte B, Vega F, Yu N, Wang J, Singh K, et al.: Novel p19 protein engages IL-12p4O to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 2000, 13:715-725.
28. Lieberman LA, Cardillo F, Cua D, Rennick D, Kastelein R, Hunter CA: IL-23 provides a limited mechanism of resistance to acute toxoplasmosis in the absence of IL-12. J Immunol 2004:in press.
29. Devergne O, Birkenbach M, Kieff E: Epstein-Barr virus-induced gene 3 and the p35 subunit of interleukin 12 form a novel heterodimeric hematopoietin. Proc Natl Acad Sci USA 1997, 94: 12041-12046.
30. de Jong R, Altare F, Haagen IA, Elferink DG, Boer T, van Breda Vriesman PJ, Kabel PJ, Draaisma JM, van Dissel JT, Kroon FP, et al.: Severe mycobacterial and Salmonella infections in interleukin-12 receptor-deficient patients. Science 1998, 280: 1435-1438.
31. Altare F, Durandy A, Lammas D, Emile JF, Lamhamedi S, Le Deist F, Drysdale P, Jouanguy E, Doffinger R, Bernaudin F, et al.: Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science 1998, 280:1432-1435.
32. Taga T, Kishimoto T: Gp130 and the interleukin-6 family of cytokines. Annu Rev Immunol 1997, 15:797-819.
33. Yoshida K, Taga T, Saito M, Suematsu S, Kumanogoh A, Tanaka T, Fujiwara H, Hirata M, Yamagami T, Nakahata T, et al.: Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders. Proc Natl Acad Sci USA 1996, 93: 407-411.
34. Pflanz S, Hibbert L, Mattson J, Rosales R, Vaisberg E, Bazan JF, Phillips JH, McClanahan TK, De Waal Malefyt R, Kastelein RA: WSX-1 and glycoprotein 130 constitute a signal-transducing receptor for IL-27. J Immunol 2004, 172:2225-2231.
35. Sprecher CA, Grant FJ, Baumgartner JW, Presnell SR, Schrader SK, Yamagiwa T, Whitmore TE, O'Hara PJ, Foster DF: Cloning and characterization of a novel class I cytokine receptor. Biochem Biophys Res Commun 1998, 246:82-90.
36. Chen Q, Ghilardi N, Wang H, Baker T, Xie MH, Gurney A, Grewal IS, de Sauvage FJ: Development of Th1-type immune responses requires the type I cytokine receptor TCCR. Nature 2000, 407: 16-920.
37. Yoshida H, Hamano S, Senaldi G, Covey T, Faggioni R, Mu S, Xia M, Wakeham AC, Nishina H, Potter J, et al.: WSX-1 is required for the initiation of Th1 responses and resistance to L major infection. Immunity 2001, 15:569-578.
38. O'Shea JJ, Gadina M, Schreiber RD: Cytokine signaling in 2002: new surprises in the Jak/Stat pathway. Cell 2002, Suppl: S121-S131.
39. Takeda A, Hamano S, Yamanaka A, Hanada T, Ishibashi T, Mak TW, 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. Lucas S, Ghilardi N, Li J, de Sauvage FJ: IL-27 regulates IL-12 responsiveness of naive CD4+ T cells through Stat1-dependent and -independent mechanisms. Proc Natl Acad Sci USA 2003, 100: 5047-15052.
41. Szabo SJ, Sullivan BM, Peng SL, Glimcher LH: Molecular mechanisms regulating Th1 immune responses. Annu Rev Immunol 2003, 21:713-758.
42. Murphy KM, Reiner SL: The lineage decisions of helper T cells. Nat Rev Immunol 2002, 2:933-944.
43. Scott P, Hunter CA: Dendritic cells and immunity to leishmaniasis and toxoplasmosis. Curr Opin Immunol 2002, 14: 66-470.
44. Artis D, Johnson LM, Joyce K, Saris C, Villarino A, Hunter CA, Scott P: Cutting edge: early IL-4 production governs the requirement for IL-27-WSX-1 signaling in the development of protective Th1 cytokine responses following Leishmania major infection. J Immunol 2004, 172:4672-4675.
45. Hisada M, Kamiya S, Fujita K, Belladonna ML, Aoki T, Koyanagi Y, Mizuguchi J, Yoshimoto T: Potent antitumor activity of interleukin-27. Cancer Res 2004, 64:1152-1156.
46. Robinson DS, O'Garra A: Further checkpoints in Th1 development. Immunity 2002, 16:755-758.
47. Agnello D, Lankford CS, Bream J, Morinobu A, Gadina M, O'Shea JJ, Frucht DM: Cytokines and transcription factors that regulate T helper cell differentiation: new players and new insights. J Clin Immunol 2003, 23:147-161.
48. Brombacher F, Kastelein RA, Alber G: Novel IL-12 family members shed light on the orchestration of Th1 responses. Trends Immunol 2003, 24:207-212.
49. Holscher C: The power of combinatorial immunology: IL-12 and IL-12-related dimeric cytokines in infectious diseases. Med Microbiol Immunol (Berl) 2003, 193:1-17.
50. Watford WT, Moriguchi M, Morinobu A, O'Shea JJ: The biology of IL-12: coordinating innate and adaptive immune responses. Cytokine Growth Factor Rev 2003, 14:361-368.
51. Ishihara K, Hirano T: IL-6 in autoimmune disease and chronic inflammatory proliferative disease. Cytokine Growth Factor Rev 2002, 13:357-368.
52. Nieuwenhuis EE, Neurath MF, Corazza N, Iijima H, Trgovcich J, Wirtz S, Glickman J, Bailey D, Yoshida M, Galle PR, et al.: Disruption of T helper 2-immune responses in Epstein-Barr virus-induced gene 3-deficient mice. Proc Natl Acad Sci USA 2002, 99: 6951-16956.
53. Hamano S, Himeno K, Miyazaki Y, Ishii K, Yamanaka A, Takeda A, Zhang M, Hisaeda H, Mak TW, Yoshimura A, et al.: WSX-1 is required for resistance to Trypanosoma cruzi infection by regulation of proinflammatory cytokine production. Immunity 2003, 19:657-667.
54. Yamanaka A, Hamano S, Miyazaki Y, Ishii K, Takeda A, Mak TW, 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.
55. Nguyen KB, Cousens LP, Doughty LA, Pien GC, Durbin JE, Biron CA: Interferon alpha/beta-mediated inhibition and promotion of interferon gamma: STAT1 resolves a paradox. Nat Immunol 2000, 1:70-76.
56. Lee CK, Smith E, Gimeno R, Gertner R, Levy DE: STAT1 affects lymphocyte survival and proliferation partially independent of its role downstream of IFN-gamma. J Immunol 2000, 164: 1286-1292.
57. Lieberman LA, Banica M, Reiner SL, Hunter CA: STAT1 plays a critical role in the regulation of antimicrobial effector mechanisms, but not in the development of Th1-type responses during toxoplasmosis. J Immunol 2004, 172:457-463.
58. Diehl S, Anguita J, Hoffmeyer A, Zapton T, Ihle JN, Fikrig E, Rincon M: Inhibition of Th1 differentiation by IL-6 is mediated by SOCS1. Immunity 2000, 13:805-815.
59. Gazzinelli RT, Wysocka M, Hieny S, Scharton-Kersten T, Cheever A, Kuhn R, Muller W, Trinchieri G, Sher A: In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-gamma and TNF-alpha. J Immunol 1996, 157:798-805.
60. Finkelman FD, Shea-Donohue T, Goldhill J, Sullivan CA, Morris SC, Madden KB, Gause WC, Urban JF Jr: Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu Rev Immunol 1997, 15: 05-533.
61. Artis D, Grencia RK: T helper cell cytokine responses during intestinal nematode infection: induction, regulation and effector function. In Parasitic Nematodes: Molecular Biology, Biochemsitry and Immunology. Edited by Harnett W. New York: CABI Publishing; 2001:331-371.
62. Bird JJ, Brown DR, Mullen AC, Moskowitz NH, Mahowald MA, Sider JR, Gajewski TF, Wang CR, Reiner SL: Helper T cell differentiation is controlled by the cell cycle. Immunity 1998, 9:229-237.
63. Takeda K, Clausen BE, Kaisho T, Tsujimura T, Terada N, Forster I, Akira S: Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 1999, 10:39-49.
64. Feldmann M, Brennan FM, Maini RN: Role of cytokines in rheumatoid arthritis. Annu Rev Immunol 1996, 14:397-440.
65. van de Loo FA, Kuiper S, van Enckevort FH, Arntz OJ, van den Berg WB: Interleukin-6 reduces cartilage destruction during experimental arthritis. A study in interieukin-6-deficient mice. Am J Pathol 1997, 151:177-191.
66. Germann T, Szeliga J, Hess H, Storkel S, Podlaski FJ, Gately MK, Schmitt E, Rude E: Administration of interleukin 12 in combination with type II collagen induces severe arthritis in DBA/1 mice. Proc Natl Acad Sci USA 1995, 92:4823-4827.
67. Leung BP, McInnes IB, Esfandiari E, Wei XQ, Liew FY: Combined effects of IL-12 and IL-18 on the induction of collagen-induced arthritis. J Immunol 2000, 164:6495-6502.
68. Murphy CA, Langrish CL, Chen Y, Blumenschein W, McClanahan T, Kastelein RA, Sedgwick JD, Cua DJ: Divergent pro- and anti-inflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 2003, 198:1951-1957.
69. Goldberg R, Wildbaum G, Zohar Y, Maor G, Karin N: Suppression of ongoing adjuvant-induced arthritis by neutralizing the function of the p28 subunit of IL-27. J Immunol 2004, 173: 1171-1178.
70. de Hooge AS, van de Loo FA, Koenders MI, Bennink MB, Arntz OJ, Kolbe T, van den Berg WB: Local activation of STAT-1 and STAT-3 in the inflamed synovium during zymosan-induced arthritis: exacerbation of joint inflammation in STAT-1 gene-knockout mice. Arthritis Rheum 2004, 50:2014-2023.
71. Ernst M, Inglese M, Waring P, Campbell IK, Bao S, Clay FJ, Alexander WS, Wicks IP, Tarlinton DM, Novak U, et al.: Defective gp130-mediated signal transducer and activator of transcription (STAT) signaling results in degenerative joint disease, gastrointestinal ulceration, and failure of uterine implantation. J Exp Med 2001, 194:189-203.