Interleukin 12 (IL-12) family cytokines: Role in immune pathogenesis and treatment of CNS autoimmune disease

Cytokine

Volumn 75, Issue 2, 2015, Pages 249-255

  Sun, Lin ^a   He, Chang ^a   Nair, Lekha ^a   Yeung, Justine ^a   Egwuagu, Charles E ^a  

^a NATIONAL EYE INSTITUTE   (United States)

Author keywords

Adoptive B cell therapy; Autoimmune disease; Cytokine therapy; IL 12 family cytokines; Regulatory B cells (Bregs and i35 Bregs)

Indexed keywords

AZATHIOPRINE; BENZENESULFONAMIDE DERIVATIVE; CHLORAMBUCIL; CORTICOSTEROID; CYCLOPHOSPHAMIDE; CYCLOSPORIN A; CYTOKINE; DACLIZUMAB; DIGOXIN; ETANERCEPT; INFLIXIMAB; INTERCELLULAR ADHESION MOLECULE 1 ANTIBODY; INTERLEUKIN 12; INTERLEUKIN 12P35; INTERLEUKIN 12P40; INTERLEUKIN 12P40 ANTIBODY; INTERLEUKIN 23; INTERLEUKIN 23P19; INTERLEUKIN 27; INTERLEUKIN 27P28; INTERLEUKIN 35; METHOTREXATE; MONOCLONAL ANTIBODY; RAPAMYCIN; RETINOID RELATED ORPHAN RECEPTOR GAMMA; SR 1001; STAT3 PROTEIN; TACROLIMUS; THALIDOMIDE; UNCLASSIFIED DRUG; UNINDEXED DRUG; IL27 PROTEIN, HUMAN; INTERLEUKIN DERIVATIVE; INTERLEUKIN-35, HUMAN;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ANTIGEN PRESENTATION; AUTOIMMUNE DISEASE; AUTOIMMUNE UVEITIS; B LYMPHOCYTE; CELL FATE; CENTRAL NERVOUS SYSTEM DISEASE; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG TARGETING; EFFECTOR CELL; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOPATHOGENESIS; INNATE IMMUNITY; LYMPHOCYTE DIFFERENTIATION; MULTIPLE SCLEROSIS; NONHUMAN; PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; REVIEW; T LYMPHOCYTE SUBPOPULATION; TH17 CELL; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; IMMUNOLOGY; INFLAMMATION; MOUSE; T LYMPHOCYTE; UVEITIS;

ANIMALS; ANTIGEN PRESENTATION; CELL DIFFERENTIATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; INFLAMMATION; INTERLEUKIN-12; INTERLEUKIN-23; INTERLEUKINS; MICE; MULTIPLE SCLEROSIS; T-LYMPHOCYTES; TH17 CELLS; UVEITIS;

EID: 84939775738     PISSN: 10434666     EISSN: 10960023     Source Type: Journal    
DOI: 10.1016/j.cyto.2015.01.030     Document Type: Review

References (73)

1. Collison L.W., Workman C.J., Kuo T.T., Boyd K., Wang Y., Vignali K.M., et al. The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature 2007, 450:566-569.
2. Wang R.X., Yu C.R., Dambuza I.M., Mahdi R.M., Dolinska M.B., Sergeev Y.V., et al. Interleukin-35 induces regulatory B cells that suppress autoimmune disease. Nat Med 2014, 20:633-641.
3. Shen P., Roch T., Lampropoulou V., O'Connor R.A., Stervbo U., Hilgenberg E., et al. IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature 2014, 507:366-370.
4. Steinman RM. Linking innate to adaptive immunity through dendritic cells. In: Novartis found symp 2006;279:101-9; discussion 9-13, 216-9.
5. Hunter C.A. New IL-12-family members: IL-23 and IL-27, cytokines with divergent functions. Nat Rev 2005, 5:521-531.
6. Trinchieri G., Pflanz S., Kastelein R.A. The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity 2003, 19:641-644.
7. Vignali D.A., Kuchroo V.K. IL-12 family cytokines: immunological playmakers. Nat Immunol 2012, 13:722-728.
8. Wolf S.F., Temple P.A., Kobayashi M., Young D., Dicig M., Lowe L., et al. Cloning of cDNA for natural killer cell stimulatory factor, a heterodimeric cytokine with multiple biologic effects on T and natural killer cells. J Immunol 1991, 146:3074-3081.
9. Oppmann B., Lesley R., Blom B., Timans J.C., Xu Y., Hunte B., et al. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 2000, 13:715-725.
10. Collison L.W., Vignali D.A. Interleukin-35: odd one out or part of the family?. Immunol Rev 2008, 226:248-262.
11. Hunter C.A. New IL-12-family members: IL-23 and IL-27, cytokines with divergent functions. Nat Rev Immunol 2005, 5:521-531.
12. Babik J.M., Adams E., Tone Y., Fairchild P.J., Tone M., Waldmann H. Expression of murine IL-12 is regulated by translational control of the p35 subunit. J Immunol 1999, 162:4069-4078.
13. Levy D.E., Darnell J.E. Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 2002, 3:651-662.
14. Jalah R., Rosati M., Ganneru B., Pilkington G.R., Valentin A., Kulkarni V., et al. The p40 subunit of interleukin (IL)-12 promotes stabilization and export of the p35 subunit: implications for improved IL-12 cytokine production. J Biol Chem 2013, 288:6763-6776.
15. el-Shabrawi Y., Livir-Rallatos C., Christen W., Baltatzis S., Foster C.S. High levels of interleukin-12 in the aqueous humor and vitreous of patients with uveitis. Ophthalmology 1998, 105:1659-1663.
16. Balashov K.E., Smith D.R., Khoury S.J., Hafler D.A., Weiner H.L. Increased interleukin 12 production in progressive multiple sclerosis: induction by activated CD4+ T cells via CD40 ligand. Proc Natl Acad Sci USA 1997, 94:599-603.
17. Comabella M., Balashov K., Issazadeh S., Smith D., Weiner H.L., Khoury S.J. Elevated interleukin-12 in progressive multiple sclerosis correlates with disease activity and is normalized by pulse cyclophosphamide therapy. J Clin Invest 1998, 102:671-678.
18. Pope R.M., Shahrara S. Possible roles of IL-12-family cytokines in rheumatoid arthritis. Nat Rev Rheumatol 2013, 9:252-256.
19. Bright J.J., Musuro B.F., Du C., Sriram S. Expression of IL-12 in CNS and lymphoid organs of mice with experimental allergic encephalitis. J Neuroimmunol 1998, 82:22-30.
20. Tarrant T.K., Silver P.B., Chan C.C., Wiggert B., Caspi R.R. Endogenous IL-12 is required for induction and expression of experimental autoimmune uveitis. J Immunol 1998, 161:122-127. [Baltimore, Md].
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. Gaffen S.L., Jain R., Garg A.V., Cua D.J. The IL-23-IL-17 immune axis: from mechanisms to therapeutic testing. Nat Rev Immunol 2014, 14:585-600.
23. Luger D., Silver P.B., Tang J., Cua D., Chen Z., Iwakura Y., et al. Either a Th17 or a Th1 effector response can drive autoimmunity: conditions of disease induction affect dominant effector category. J Exp Med 2008.
24. Cua D.J., Sherlock J., Chen Y., Murphy C.A., Joyce B., Seymour B., et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003, 421:744-748.
25. Becher B., Durell B.G., Noelle R.J. IL-23 produced by CNS-resident cells controls T cell encephalitogenicity during the effector phase of experimental autoimmune encephalomyelitis. J Clin Invest 2003, 112:1186-1191.
26. Becher B., Durell B.G., Noelle R.J. Experimental autoimmune encephalitis and inflammation in the absence of interleukin-12. J Clin Invest 2002, 110:493-497.
27. Liang D., Zuo A., Shao H., Born W.K., O'Brien R.L., Kaplan H.J., et al. IL-23 receptor expression on gammadelta T cells correlates with their enhancing or suppressive effects on autoreactive T cells in experimental autoimmune uveitis. J Immunol 2013, 191:1118-1125.
28. Yang P., Foster C.S. Interleukin 21, interleukin 23, and transforming growth factor beta1 in HLA-A29-associated birdshot retinochoroidopathy. Am J Ophthalmol 2013, 156:400-406 e2.
29. Segal B.M., Constantinescu C.S., Raychaudhuri A., Kim L., Fidelus-Gort R., Kasper L.H. Repeated subcutaneous injections of IL12/23 p40 neutralising antibody, ustekinumab, in patients with relapsing-remitting multiple sclerosis: a phase II, double-blind, placebo-controlled, randomised, dose-ranging study. Lancet Neurol 2008, 7:796-804.
30. 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.
31. Pflanz S., Timans J.C., Cheung J., Rosales R., Kanzler H., Gilbert J., et al. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells. Immunity 2002, 16:779-790.
32. Villarino A.V., Huang E., Hunter C.A. Understanding the pro- and anti-inflammatory properties of IL-27. J Immunol 2004, 173:715-720. [Baltimore, Md].
33. Owaki T., Asakawa M., Kamiya S., Takeda K., Fukai F., Mizuguchi J., et al. IL-27 suppresses CD28-mediated [correction of medicated] IL-2 production through suppressor of cytokine signaling 3. J Immunol 2006, 176:2773-2780.
34. Villarino A.V., Stumhofer J.S., Saris C.J., Kastelein R.A., de Sauvage F.J., Hunter C.A. IL-27 limits IL-2 production during Th1 differentiation. J Immunol 2006, 176:237-247. [Baltimore, Md].
35. Fitzgerald D.C., Zhang G.X., El-Behi M., Fonseca-Kelly Z., Li H., Yu S., et al. 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.
36. Awasthi A., Carrier Y., Peron J.P., Bettelli E., Kamanaka M., Flavell R.A., et al. A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells. Nat Immunol 2007, 8:1380-1389.
37. Batten M., Li J., Yi S., Kljavin N.M., Danilenko D.M., Lucas S., et al. Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat Immunol 2006, 7:929-936.
38. Amadi-Obi A, Yu CR, Dambuza I, Kim SH, Marrero B, Egwuagu CE. Interleukin 27 induces the expression of complement factor H (CFH) in the retina. PLoS One 7:e45801.
39. Amadi-Obi A., Yu C.R., Liu X., Mahdi R.M., Clarke G.L., Nussenblatt R.B., et al. T(H)17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1. Nat Med 2007, 13:711-718.
40. Lee Y.S., Amadi-Obi A., Yu C.R., Egwuagu C.E. Retinal cells suppress intraocular inflammation (uveitis) through production of interleukin-27 and interleukin-10. Immunology 2011, 132:492-502.
41. Collison L.W., Chaturvedi V., Henderson A.L., Giacomin P.R., Guy C., Bankoti J., et al. IL-35-mediated induction of a potent regulatory T cell population. Nat Immunol 2010, 11:1093-1101.
42. Seyerl M., Kirchberger S., Majdic O., Seipelt J., Jindra C., Schrauf C., et al. Human rhinoviruses induce IL-35-producing Treg via induction of B7-H1 (CD274) and sialoadhesin (CD169) on DC. Eur J Immunol 2010, 40:321-329.
43. Collison L.W., Delgoffe G.M., Guy C.S., Vignali K.M., Chaturvedi V., Fairweather D., et al. The composition and signaling of the IL-35 receptor are unconventional. Nat Immunol 2012, 13:290-299.
44. Shen P., Roch T., Lampropoulou V., O'Connor R.A., Stervbo U., Hilgenberg E., et al. IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature 2014, 507:366-370.
45. Wang R.X., Yu C.R., Dambuza I.M., Mahdi R.M., Dolinska M.B., Sergeev Y.V., et al. Interleukin-35 induces regulatory B cells that suppress autoimmune disease. Nat Med 2014, 20:633-641.
46. Dong C. TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat Rev Immunol 2008, 8:337-348.
47. Harris T.J., Grosso J.F., Yen H.R., Xin H., Kortylewski M., Albesiano E., et al. Cutting edge: an in vivo requirement for STAT3 signaling in TH17 development and TH17-dependent autoimmunity. J Immunol 2007, 179:4313-4317.
48. Liu X., Lee Y.S., Yu C.R., Egwuagu C.E. Loss of STAT3 in CD4+ T cells prevents development of experimental autoimmune diseases. J Immunol 2008, 180:6070-6076.
49. Jakkula E., Leppa V., Sulonen A.M., Varilo T., Kallio S., Kemppinen A., et al. Genome-wide association study in a high-risk isolate for multiple sclerosis reveals associated variants in STAT3 gene. Am J Hum Genet 2010, 86:285-291.
50. Yu C.R., Lee Y.S., Mahdi R.M., Surendran N., Egwuagu C.E. Therapeutic targeting of STAT3 (signal transducers and activators of transcription 3) pathway inhibits experimental autoimmune uveitis. PLoS One 2012, 7:e29742.
51. Egwuagu C.E. STAT3 in CD4+ T helper cell differentiation and inflammatory diseases. Cytokine 2009, 47:149-156.
52. Egwuagu C.E., Yu C.R., Zhang M., Mahdi R.M., Kim S.J., Gery I. Suppressors of cytokine signaling proteins are differentially expressed in Th1 and Th2 cells: implications for Th cell lineage commitment and maintenance. J Immunol 2002, 168:3181-3187.
53. Egwuagu C.E., Larkin J. Therapeutic targeting of STAT pathways in CNS autoimmune diseases. JAKSTAT 2013, 2:e24134.
54. Jo D., Liu D., Yao S., Collins R.D., Hawiger J. Intracellular protein therapy with SOCS3 inhibits inflammation and apoptosis. Nat Med 2005, 11:892-898.
55. Yu C.R., Hayashi K., Lee Y.S., Mahdi R.M., Shen D.F., Chan C.C., et al. Suppressor of cytokine signaling 1 (SOCS1) mitigates anterior uveitis and confers protection against ocular HSV-1 infection. Inflammation 2015, 38:555-565.
56. Storek J., Dawson M.A., Lim L.C., Burman B.E., Stevens-Ayers T., Viganego F., et al. Efficacy of donor vaccination before hematopoietic cell transplantation and recipient vaccination both before and early after transplantation. Bone Marrow Transplant 2004, 33:337-346.
57. Waiboci L.W., Ahmed C.M., Mujtaba M.G., Flowers L.O., Martin J.P., Haider M.I., et al. Both the suppressor of cytokine signaling 1 (SOCS-1) kinase inhibitory region and SOCS-1 mimetic bind to JAK2 autophosphorylation site: implications for the development of a SOCS-1 antagonist. J Immunol 2007, 178:5058-5068.
58. Eberl G., Littman D.R. The role of the nuclear hormone receptor RORgammat in the development of lymph nodes and Peyer's patches. Immunol Rev 2003, 195:81-90.
59. Ivanov I.I., Zhou L., Littman D.R. Transcriptional regulation of Th17 cell differentiation. Semin Immunol 2007, 19:409-417.
60. Solt L.A., Kumar N., Nuhant P., Wang Y., Lauer J.L., Liu J., et al. Suppression of TH17 differentiation and autoimmunity by a synthetic ROR ligand. Nature 2011, 472:491-494.
61. Huh J.R., Leung M.W., Huang P., Ryan D.A., Krout M.R., Malapaka R.R., et al. Digoxin and its derivatives suppress TH17 cell differentiation by antagonizing RORgammat activity. Nature 2011, 472:486-490.
62. Wang R.X., Yu C.R., Mahdi R.M., Egwuagu C.E. Novel IL27p28/IL12p40 cytokine suppressed experimental autoimmune uveitis by inhibiting autoreactive Th1/Th17 cells and promoting expansion of regulatory T cells. J Biol Chem 2012, 287:36012-36021.
63. Stumhofer J.S., Tait E.D., Quinn W.J., Hosken N., Spudy B., Goenka R., et al. A role for IL-27p28 as an antagonist of gp130-mediated signaling. Nat Immunol 2010, 11:1119-1126.
64. Brahmachari S., Pahan K. Role of cytokine p40 family in multiple sclerosis. Minerva Med 2008, 99:105-118.
65. Heinzel F.P., Hujer A.M., Ahmed F.N., Rerko R.M. In vivo production and function of IL-12 p40 homodimers. J Immunol 1997, 158:4381-4388.
66. Shigehara K., Shijubo N., Ohmichi M., Kamiguchi K., Takahashi R., Morita-Ichimura S., et al. Increased circulating interleukin-12 (IL-12) p40 in pulmonary sarcoidosis. Clin Exp Immunol 2003, 132:152-157.
67. van Boxel-Dezaire A.H., Hoff S.C., van Oosten B.W., Verweij C.L., Drager A.M., Ader H.J., et al. Decreased interleukin-10 and increased interleukin-12p40 mRNA are associated with disease activity and characterize different disease stages in multiple sclerosis. Ann Neurol 1999, 45:695-703.
68. Fassbender K., Ragoschke A., Rossol S., Schwartz A., Mielke O., Paulig A., et al. Increased release of interleukin-12p40 in MS: association with intracerebral inflammation. Neurology 1998, 51:753-758.
69. Liu J.Q., Liu Z., Zhang X., Shi Y., Talebian F., Carl J.W., et al. Increased Th17 and regulatory T cell responses in EBV-induced gene 3-deficient mice lead to marginally enhanced development of autoimmune encephalomyelitis. J Immunol 2012, 188:3099-3106.
70. Egwuagu C.E., Charukamnoetkanok P., Gery I. Thymic expression of autoantigens correlates with resistance to autoimmune disease. J Immunol 1997, 159:3109-3112.
71. Stumhofer J.S., Tait E.D., Quinn W.J., Hosken N., Spudy B., Goenka R., et al. A role for IL-27p28 as an antagonist of gp130-mediated signaling. Nat Immunol 2010, 11:1119-1126.
72. Gillessen S., Carvajal D., Ling P., Podlaski F.J., Stremlo D.L., Familletti P.C., et al. Mouse interleukin-12 (IL-12) p40 homodimer: a potent IL-12 antagonist. Eur J Immunol 1995, 25:200-206.
73. Nagai H., Oniki S., Fujiwara S., Xu M., Mizoguchi I., Yoshimoto T., et al. Antitumor activities of interleukin-27 on melanoma. Endocr Metab Immune Disord Drug Targets 2010, 10:41-46.