Insights into IL-23 biology: From structure to function

Cytokine and Growth Factor Reviews

Volumn 26, Issue 5, 2015, Pages 569-578

  Floss, Doreen M ^a   Schröder, Jutta ^a   Franke, Manuel ^a   Scheller, Jürgen ^a  

^a Department of Orthopedic Surgery   (Germany)

Author keywords

IL 12R 1; IL 23 receptor; Interleukin 23; Signal transduction

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR RECEPTOR; COMPLEMENTARY DNA; GAMMA INTERFERON; GLYCOPROTEIN GP 130; INTERLEUKIN 11; INTERLEUKIN 11 RECEPTOR; INTERLEUKIN 12; INTERLEUKIN 12 RECEPTOR; INTERLEUKIN 12 RECEPTOR BETA1; INTERLEUKIN 12P35; INTERLEUKIN 12P40; INTERLEUKIN 17; INTERLEUKIN 23; INTERLEUKIN 23 RECEPTOR; INTERLEUKIN 23P19; INTERLEUKIN 23P40; INTERLEUKIN 27; INTERLEUKIN 27P28; JANUS KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE; NEUTRALIZING ANTIBODY; PHOSPHATIDYLINOSITOL 3 KINASE; STAT1 PROTEIN; STAT2 PROTEIN; STAT3 PROTEIN; STAT4 PROTEIN; STAT5 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG; IL12RB1 PROTEIN, HUMAN; IL23R PROTEIN, HUMAN; INTERLEUKIN RECEPTOR; JANUS KINASE; STAT PROTEIN;

3' UNTRANSLATED REGION; ACUTE MYELOBLASTIC LEUKEMIA; AMINO TERMINAL SEQUENCE; B LYMPHOCYTE; BIOACCUMULATION; BLADDER CANCER; BORRELIA BURGDORFERI; CANCER RISK; CARBOXY TERMINAL SEQUENCE; CROHN DISEASE; CYTOKINE PRODUCTION; DISULFIDE BOND; DNA LIBRARY; ENZYME ACTIVATION; ENZYME INHIBITION; EPSTEIN BARR VIRUS; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; ESOPHAGUS CANCER; EXON; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MULTIPLE SCLEROSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; RHEUMATOID ARTHRITIS; RNA SPLICING; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; STOMACH CANCER; TH17 CELL; ULCERATIVE COLITIS; ANIMAL; AUTOIMMUNE DISEASE; IMMUNOLOGY; PATHOLOGY;

ANIMALS; AUTOIMMUNE DISEASES; HUMANS; INTERLEUKIN-23; JANUS KINASES; MAP KINASE SIGNALING SYSTEM; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTORS, INTERLEUKIN; RECEPTORS, INTERLEUKIN-12; STAT TRANSCRIPTION FACTORS; TH17 CELLS;

EID: 84941943615     PISSN: 13596101     EISSN: 18790305     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2015.07.005     Document Type: Review

References (137)

1. Akdis M., Burgler S., Crameri R., Eiwegger T., Fujita H., Gomez E., et al. Interleukins, from 1 to 37, and interferon-gamma: receptors, functions, and roles in diseases. J. Allergy Clin. Immunol. 2011, 127:701-721.
2. Mosmann T.R., Cherwinski H., Bond M.W., Giedlin M.A., Coffman R.L. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol. 1986, 136:2348-2357.
3. Mosmann T.R., Coffman R.L. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 1989, 7:145-173.
4. Schmitt N., Ueno H. Regulation of human helper T cell subset differentiation by cytokines. Curr. Opin. Immunol. 2015, 34:130-136.
5. Basu R., Hatton R.D., Weaver C.T. The Th17 family: flexibility follows function. Immunol. Rev. 2013, 252:89-103.
6. 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.
7. Vignali D.A., Kuchroo V. IL-12 family cytokines: immunological playmakers. Nat. Immunol. 2012, 13:722-728.
8. 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.
9. Tang C., Chen S., Qian H., Huang W. Interleukin-23: as a drug target for autoimmune inflammatory diseases. Immunology 2011, 135:112-124.
10. Ngiow S.F., Teng M.W., Smyth M.J. A balance of Interleukin-12 and -23 in cancer. Trends Immunol. 2013, 34:548-555.
11. Croxford A.L., Mair F., Becher B. IL-23: one cytokine in control of autoimmunity. Eur. J. Immunol. 2012, 42:2263-2273.
12. Croxford A.L., Kulig P., Becher B. IL-12-and IL-23 in health and disease. Cytokine Growth Factor Rev. 2014, 25:415-421.
13. Chiricozzi A., Saraceno R., Chimenti M.S., Guttman-Yassky E., Krueger J.G. Role of IL-23 in the pathogenesis of psoriasis: a novel potential therapeutic target?. Expert Opin. Ther. Targets 2014, 18:513-525.
14. Morrison P.J., Ballantyne S.J., Kullberg M.C. Interleukin-23 and T helper 17-type responses in intestinal inflammation: from cytokines to T-cell plasticity. Immunology 2011, 133:397-408.
15. Duvallet E., Semerano L., Assier E., Falgarone G., Boissier M.C. Interleukin-23: a key cytokine in inflammatory diseases. Ann. Med. 2011, 43:503-511.
16. Levin A.A., Gottlieb A.B. Specific targeting of interleukin-23p19 as effective treatment for psoriasis. J. Am. Acad. Dermatol. 2014, 70:555-561.
17. Garbers C., Hermanns H., Schaper F., Müller-Newen G., Grötzinger J., Rose-John S., et al. Plasticity and cross-talk of interleukin 6-type cytokines. Cytokine Growth Factor Rev. 2012, 23:85-97.
18. Oppmann B., Lesley R., Blom B., Timans J., 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.
19. Lupardus P.J., Garcia K.C. The structure of interleukin-23 reveals the molecular basis of p40 subunit sharing with interleukin-12. J. Mol. Biol. 2008, 382:931-941.
20. Schröder J., Moll J.M., Baran P., Grötzinger J., Scheller J., Floss D.M. Non-canonical interleukin 23 receptor complex assembly: p40 protein recruits interleukin 12 receptor beta1 via site II and induces p19/interleukin 23 receptor interaction via site III. J. Biol. Chem. 2015, 290:359-370.
21. Gubler U., Chua A.O., Schoenhaut D.S., Dwyer C.M., McComas W., Motyka R., et al. Coexpression of two distinct genes is required to generate secreted bioactive cytotoxic lymphocyte maturation factor. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:4143-4147.
22. Schoenhaut D.S., Chua A.O., Wolitzky A.G., Quinn P.M., Dwyer C.M., McComas W., et al. Cloning and expression of murine IL-12. J. Immunol. 1992, 148:3433-3440.
23. Chua A.O., Chizzonite R., Desai B.B., Truitt T.P., Nunes P., Minetti L.J., et al. Expression cloning of a human IL-12 receptor component: a new member of the cytokine receptor superfamily with strong homology to gp130. J. Immunol. 1994, 153:128-136.
24. Chua A., Wilkinson V., Presky D., Gubler U. Cloning and characterization of a mouse IL-12 receptor-beta component. J. Immunol. 1995, 155:4286-4294.
25. Parham C., Chirica M., Timans J., Vaisberg E., Travis M., Cheung J., et al. A receptor for the heterodimeric cytokine IL-23 is composed of IL-12Rbeta1 and a novel cytokine receptor subunit, IL-23R. J. Immunol. 2002, 168:5699-5708.
26. Kobayashi M., Fitz L., Ryan M., Hewick R., Clark S., Chan S., et al. Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J. Exp. Med. 1989, 170:827-845.
27. Bashyam H. Interleukin-12: a master regulator. J. Exp. Med. 2007, 204:969.
28. Stern A.S., Podlaski F.J., Hulmes J.D., Pan Y.C., Quinn P.M., Wolitzky A.G., et al. Purification to homogeneity and partial characterization of cytotoxic lymphocyte maturation factor from human B-lymphoblastoid cells. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:6808-6812.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. Mattner F., Fischer S., Guckes S., Jin S., Kaulen H., Schmitt E., et al. The interleukin-12 subunit p40 specifically inhibits effects of the interleukin-12 heterodimer. Eur. J. Immunol. 1993, 23:2202-2208.
35. 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.
36. Shimozato O., Ugai S., Chiyo M., Takenobu H., Nagakawa H., Wada A., et al. The secreted form of the p40 subunit of interleukin (IL)-12 inhibits IL-23 functions and abrogates IL-23-mediated antitumour effects. Immunology 2006, 117:22-28.
37. Ha S.J., Lee C.H., Lee S.B., Kim C.M., Jang K.L., Shin H.S., et al. A novel function of IL-12p40 as a chemotactic molecule for macrophages. J. Immunol. 1999, 163:2902-2908.
38. Russell T.D., Yan Q., Fan G., Khalifah A.P., Bishop D.K., Brody S.L., et al. IL-12 p40 homodimer-dependent macrophage chemotaxis and respiratory viral inflammation are mediated through IL-12 receptor beta 1. J. Immunol. 2003, 171:6866-6874.
39. Abdi K., Singh N.J., Spooner E., Kessler B.M., Radaev S., Lantz L., et al. Free IL-12p40 monomer is a polyfunctional adaptor for generating novel IL-12-like heterodimers extracellularly. J. Immunol. 2014, 192:6028-6036.
40. Prando C., Samarina A., Bustamante J., Boisson-Dupuis S., Cobat A., Picard C., et al. Inherited IL-12p40 deficiency: genetic, immunologic, and clinical features of 49 patients from 30 kindreds. Medicine (Baltimore) 2013, 92:109-122.
41. Sun L., He C., Nair L., Yeung J., Egwuagu C.E. Interleukin 12 (IL-12) family cytokines: role in immune pathogenesis and treatment of CNS autoimmune disease. Cytokine 2015.
42. Ling P., Gately M.K., Gubler U., Stern A.S., Lin P., Hollfelder K., et al. Human IL-12 p40 homodimer binds to the IL-12 receptor but does not mediate biologic activity. J. Immunol. 1995, 154:116-127.
43. Wang X., Wilkinson V.L., Podlaski F.J., Wu C., Stern A.S., Presky D.H., et al. Characterization of mouse interleukin-12 p40 homodimer binding to the interleukin-12 receptor subunits. Eur. J. Immunol. 1999, 29:2007-2013.
44. Robinson R.T. IL12Rbeta1: the cytokine receptor that we used to know. Cytokine 2015, 71:348-359.
45. Presky D., Yang H., Minetti L., Chua A., Nabavi N., Wu C., et al. A functional interleukin 12 receptor complex is composed of two beta-type cytokine receptor subunits. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:14002-14007.
46. Watford W.T., Moriguchi M., Morinobu A., O'Shea J.J. The biology of IL-12: coordinating innate and adaptive immune responses. Cytokine Growth Factor Rev. 2003, 14:361-368.
47. van de Vosse E., Haverkamp M.H., Ramirez-Alejo N., Martinez-Gallo M., Blancas-Galicia L., Metin A., et al. IL-12Rbeta1 deficiency: mutation update and description of the IL12RB1 variation database. Hum. Mutat. 2013, 34:1329-1339.
48. Ford N.R., Miller H.E., Reeme A.E., Waukau J., Bengtson C., Routes J.M., et al. Inflammatory signals direct expression of human IL12RB1 into multiple distinct isoforms. J. Immunol. 2012, 189:4684-4694.
49. Robinson R.T., Khader S.A., Martino C.A., Fountain J.J., Teixeira-Coelho M., Pearl J.E., et al. Mycobacterium tuberculosis infection induces il12rb1 splicing to generate a novel IL-12Rbeta1 isoform that enhances DC migration. J. Exp. Med. 2010, 207:591-605.
50. Ray A.A., Fountain J.J., Miller H.E., Cooper A.M., Robinson R.T. IL12Rbeta1DeltaTM is a secreted product of il12rb1 that promotes control of extrapulmonary tuberculosis. Infect. Immun. 2015, 83:560-571.
51. de Beaucoudrey L., Samarina A., Bustamante J., Cobat A., Boisson-Dupuis S., Feinberg J., et al. Revisiting human IL-12Rbeta1 deficiency: a survey of 141 patients from 30 countries. Medicine (Baltimore) 2010, 89:381-402.
52. Zhang X.Y., Zhang H.J., Zhang Y., Fu Y.J., He J., Zhu L.P., et al. Identification and expression analysis of alternatively spliced isoforms of human interleukin-23 receptor gene in normal lymphoid cells and selected tumor cells. Immunogenetics 2006, 57:934-943.
53. Kan S.H., Mancini G., Gallagher G. Identification and characterization of multiple splice forms of the human interleukin-23 receptor alpha chain in mitogen-activated leukocytes. Genes Immun. 2008, 9:631-639.
54. Mancini G., Kan S.H., Gallagher G. A novel insertion variant of the human IL-23 receptor-alpha chain transcript. Genes Immun. 2008, 9:566-569.
55. Zhao J., Liu Y.H., Reichert P., Pflanz S., Pramanik B. Glycosylation analysis of interleukin-23 receptor: elucidation of glycosylation sites and characterization of attached glycan structures. J. Mass Spectrom. 2010, 45:1416-1425.
56. Chognard G., Bellemare L., Pelletier A.N., Dominguez-Punaro M.C., Beauchamp C., Guyon M.J., et al. The dichotomous pattern of IL-12R and IL-23R expression elucidates the role of IL-12 and IL-23 in inflammation. PLOS ONE 2014, 9:e89092.
57. Jones S.A., Scheller J., Rose-John S. Therapeutic strategies for the clinical blockade of IL-6/gp130 signaling. J. Clin. Invest. 2011, 121:3375-3383.
58. Bobby R., Robustelli P., Kralicek A., Mobli M., King G., Grötzinger J., et al. Functional implications of large backbone amplitude motions of the glycoprotein 130-binding epitope of interleukin-6. FEBS J. 2014, 281:2471-2483.
59. Boulanger M.J., Chow D.-C., Brevnova E.E., Garcia K.C. Hexameric structure and assembly of the interleukin-6/IL-6 a receptor/gp130 complex. Science 2003, 300:2101-2104.
60. Jones L., Chaturvedi V., Uyttenhove C., Van Snick J., Vignali D. Distinct subunit pairing criteria within the heterodimeric IL-12 cytokine family. Mol. Immunol. 2012, 51:234-244.
61. Collison L.W., Vignali D.A. Interleukin-35: odd one out or part of the family?. Immunol. Rev. 2008, 226:248-262.
62. Paonessa G., Graziani R., De Serio A., Savino R., Ciapponi L., Lahm A., et al. Two distinct and independent sites on IL-6 trigger gp 130 dimer formation and signalling. EMBO J. 1995, 14:1942-1951.
63. Di Marco A., Gloaguen I., Graziani R., Paonessa G., Saggio I., Hudson K.R., et al. Identification of ciliary neurotrophic factor (CNTF) residues essential for leukemia inhibitory factor receptor binding and generation of CNTF receptor antagonists. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:9247-9252.
64. Plun-Favreau H., Perret D., Diveu C., Froger J., Chevalier S., Lelièvre E., et al. Leukemia inhibitory factor (LIF), cardiotrophin-1, and oncostatin M share structural binding determinants in the immunoglobulin-like domain of LIF receptor. J. Biol. Chem. 2003, 278:27169-27179.
65. Chow D., He X., Snow A.L., Rose-John S., Garcia K.C. Structure of an extracellular gp130 cytokine receptor signaling complex. Science 2001, 291:2150-2155.
66. Floss D., Mrotzek S., Klöcker T., Schröder J., Grötzinger J., Rose-John S., et al. Identification of canonical tyrosine-dependent and non-canonical tyrosine-independent STAT3 activation sites in the intracellular domain of the interleukin 23 receptor. J. Biol. Chem. 2013, 288:19368-19400.
67. Cho M.L., Kang J.W., Moon Y.M., Nam H.J., Jhun J.Y., Heo S.B., et al. STAT3 and NF-kappaB signal pathway is required for IL-23-mediated IL-17 production in spontaneous arthritis animal model IL-1 receptor antagonist-deficient mice. J. Immunol. 2006, 176:5652-5661.
68. Bacon C., Petricoin Er, Ortaldo J., Rees R., Larner A., Johnston J., et al. Interleukin 12 induces tyrosine phosphorylation and activation of STAT4 in human lymphocytes. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:7307-7311.
69. Thierfelder W., van Deursen J., Yamamoto K., Tripp R., Sarawar S., Carson R., et al. Requirement for STAT4 in Interleukin 12-mediated responses of natural killer and T cells. Nature 1996, 382:171-174.
70. Stahl N., Farruggella T.J., Boulton T.G., Zhong Z., Darnell J.E., Yancopoulos G.D. Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors. Science 1995, 267:1349-1353.
71. Demoulin J., Uyttenhove C., Van Roost E., DeLestré B., Donckers D., Van Snick J., et al. A single tyrosine of the interleukin-9 (IL-9) receptor is required for STAT activation, antiapoptotic activity, and growth regulation by IL-9. Mol. Cell. Biol. 1996, 16:4710-4716.
72. Case R., Piccione E., Wolf G., Benett A., Lechleider R., Neel B., et al. SH-PTP2/Syp SH2 domain binding specificity is defined by direct interactions with platelet-derived growth factor beta-receptor, epidermal growth factor receptor, and insulin receptor substrate-1-derived phosphopeptides. J. Biol. Chem. 1994, 269:10467-10474.
73. Naeger L., McKinney J., Salvekar A., Hoey T. Identification of a STAT4 binding site in the interleukin-12 receptor required for signaling. J. Biol. Chem. 1999, 274:1875-1878.
74. Yao B., Niu P., Surowy C., Faltynek C. Direct interaction of STAT4 with the IL-12 receptor. Arch. Biochem. Biophys. 1999, 368:147-155.
75. Heinrich P.C., 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.
76. Wiederkehr-Adam M., Ernst P., Müller K., Bieck E., Gombert F., Ottl J., et al. Characterization of phosphopeptide motifs specific for the Src homology 2 domains of signal transducer and activator of transcription 1 (STAT1) and STAT3. J. Biol. Chem. 2003, 278:16117-16128.
77. Ward A., Hermans M., Smith L., van Aesch Y., Schelen A., Antonissen C., et al. Tyrosine-dependent and -independent mechanisms of STAT3 activation by the human granulocyte colony-stimulating factor (G-CSF) receptor are differentially utilized depending on G-CSF concentration. Can. J. Vet. Res. 1999, 93:113-124.
78. Dumoutier L., de Meester C., Tavernier J., Renauld J. New activation modus of STAT3: a tyrosine-less region of the interleukin-22 receptor recruits STAT3 by interacting with its coiled-coil domain. J. Biol. Chem. 2009, 284:26377-26384.
79. Li X., Leung S., Kerr I., Stark G. Functional subdomains of STAT2 required for preassociation with the alpha interferon receptor and for signaling. Mol. Cell. Biol. 1997, 17:2048-2056.
80. White C., Nicola N. SOCS3: an essential physiological inhibitor of signaling by interleukin-6 and G-CSF family cytokines. JAKSTAT 2013, 2:e25045.
81. de Paus R.A., van de Wetering D., van Dissel J.T., van de Vosse E. IL-23 and IL-12 responses in activated human T cells retrovirally transduced with IL-23 receptor variants. Mol. Immunol. 2008, 45:3889-3895.
82. Chen Z., Laurence A., Kanno Y., Pacher-Zavisin M., Zhu B., Tato C., et al. Selective regulatory function of Socs3 in the formation of IL-17-secreting T cells. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:8137-8142.
83. Wang X., Tomso D.J., Liu X., Bell D.A. Single nucleotide polymorphism in transcriptional regulatory regions and expression of environmentally responsive genes. Toxicol. Appl. Pharmacol. 2005, 207:84-90.
84. Yates C.M., Sternberg M.J. Proteins and domains vary in their tolerance of non-synonymous single nucleotide polymorphisms (nsSNPs). J. Mol. Biol. 2013, 425:1274-1286.
85. Ferrer-Costa C., Orozco M., de la Cruz X. Characterization of disease-associated single amino acid polymorphisms in terms of sequence and structure properties. J. Mol. Biol. 2002, 315:771-786.
86. Fareed M., Afzal M. Single nucleotide polymorphism in genome-wide association of human population: a tool for broad spectrum service. Egypt. J. Med. Hum. Genet. 2013, 14:123-134.
87. Duerr R.H., Taylor K.D., Brant S.R., Rioux J.D., Silverberg M.S., Daly M.J., et al. A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 2006, 314:1461-1463.
88. Zheng J., Jiang L., Zhang L., Yang L., Deng J., You Y., et al. Functional genetic variations in the IL-23 receptor gene are associated with risk of breast, lung and nasopharyngeal cancer in Chinese populations. Carcinogenesis 2012, 33:2409-2416.
89. Cummings J.R., Ahmad T., Geremia A., Beckly J., Cooney R., Hancock L., et al. Contribution of the novel inflammatory bowel disease gene IL23R to disease susceptibility and phenotype. Inflamm. Bowel Dis. 2007, 13:1063-1068.
90. Serbati N., Senhaji N., Diakite B., Badre W., Nadifi S. IL23R and ATG16L1 variants in Moroccan patients with inflammatory bowel disease. BMC Res. Notes 2014, 7:570.
91. Liu M., Zhu W., Wang J., Zhang J., Guo X., Song J., et al. Interleukin-23 receptor genetic polymorphisms and ulcerative colitis susceptibility: a meta-analysis. Clin. Res. Hepatol. Gastroenterol. 2014.
92. Mihaljevic S., Kibel A., Stefanic M., Glavas-Obrovac L., Takac B., Krznaric Z., et al. Polymorphisms of interleukin-23 receptor in patients with inflammatory bowel disease in a Croatian tertiary center. Coll. Antropol. 2013, 37:1171-1177.
93. Huber A.K., Jacobson E.M., Jazdzewski K., Concepcion E.S., Tomer Y. Interleukin (IL)-23 receptor is a major susceptibility gene for Graves' ophthalmopathy: the IL-23/T-helper 17 axis extends to thyroid autoimmunity. J. Clin. Endocrinol. Metab. 2008, 93:1077-1081.
94. Cargill M., Schrodi S.J., Chang M., Garcia V.E., Brandon R., Callis K.P., et al. A large-scale genetic association study confirms IL12B and leads to the identification of IL23R as psoriasis-risk genes. Am. J. Hum. Genet. 2007, 80:273-290.
95. Capon F., Di Meglio P., Szaub J., Prescott N.J., Dunster C., Baumber L., et al. Sequence variants in the genes for the interleukin-23 receptor (IL23R) and its ligand (IL12B) confer protection against psoriasis. Hum. Genet. 2007, 122:201-206.
96. Nair R.P., Ruether A., Stuart P.E., Jenisch S., Tejasvi T., Hiremagalore R., et al. Polymorphisms of the IL12B and IL23R genes are associated with psoriasis. J. Invest. Dermatol. 2008, 128:1653-1661.
97. Nair R.P., Duffin K.C., Helms C., Ding J., Stuart P.E., Goldgar D., et al. Genome-wide scan reveals association of psoriasis with IL-23 and NF-kappaB pathways. Nat. Genet. 2009, 41:199-204.
98. Oka A., Mabuchi T., Ikeda S., Terui T., Haida Y., Ozawa A., et al. IL12B and IL23R gene SNPs in Japanese psoriasis. Immunogenetics 2013, 65:823-828.
99. Hollis-Moffatt J.E., Merriman M.E., Rodger R.A., Rowley K.A., Chapman P.T., Dalbeth N., et al. Evidence for association of an interleukin 23 receptor variant independent of the R381Q variant with rheumatoid arthritis. Ann. Rheum. Dis. 2009, 68:1340-1344.
100. Hamdy G., Darweesh H., Khattab E.A., Fawzy S., Fawzy E., Sheta M. Evidence of association of interleukin-23 receptor gene polymorphisms with Egyptian rheumatoid arthritis patients. Hum. Immunol. 2015.
101. Yalcin B., Atakan N., Dogan S. Association of interleukin-23 receptor gene polymorphism with Behcet disease. Clin. Exp. Dermatol. 2014, 39:881-887.
102. Dong H., Li Q., Zhang Y., Tan W., Jiang Z. IL23R gene confers susceptibility to ankylosing spondylitis concomitant with uveitis in a Han Chinese population. PLoS ONE 2013, 8:e67505.
103. Xu B., Ma J.X., Ma X.L., Jia H.B., Feng R., Xu L.Y. Association between rs7517847 and rs2201841 polymorphisms in IL-23 receptor gene and risk of ankylosing spondylitis: a meta-analysis. PeerJ 2015, 3:e910.
104. Liu Y., Yu J.T., Zhang W., Zong Y., Lu R.C., Zhou J., et al. Interleukin-23 receptor polymorphisms are associated with Alzheimer's disease in Han Chinese. J. Neuroimmunol. 2014, 271:43-48.
105. Zhang M., Cai Z.R., Zhang B., Cai X., Li W., Guo Z., et al. Functional polymorphisms in interleukin-23 receptor and susceptibility to coronary artery disease. DNA Cell Biol. 2014, 33:891-897.
106. Hu D., Hu G., Zhu J., Shen Y., Kang H., Hong S. Association between polymorphisms of the IL-23R gene and allergic rhinitis in a Chinese Han population. PLoS ONE 2013, 8:e63858.
107. Cocco C., Canale S., Frasson C., Di Carlo E., Ognio E., Ribatti D., et al. Interleukin-23 acts as antitumor agent on childhood B-acute lymphoblastic leukemia cells. Blood 2010, 116:3887-3898.
108. Cocco C., Morandi F., Airoldi I. Interleukin-27 and interleukin-23 modulate human plasmacell functions. J. Leukoc. Biol. 2011, 89:729-734.
109. Langowski J.L., Zhang X., Wu L., Mattson J.D., Chen T., Smith K., et al. IL-23 promotes tumour incidence and growth. Nature 2006, 442:461-465.
110. Chen J., Lu Y., Zhang H., Ding Y., Ren C., Hua Z., et al. A nonsynonymous polymorphism in IL23R gene is associated with risk of gastric cancer in a Chinese population. Mol. Carcinog. 2010, 49:862-868.
111. Chu H., Cao W., Chen W., Pan S., Xiao Y., Liu Y., et al. Potentially functional polymorphisms in IL-23 receptor and risk of esophageal cancer in a Chinese population. Int. J. Cancer 2012, 130:1093-1097.
112. Yao J., Liu L., Yang M. Interleukin-23 receptor genetic variants contribute to susceptibility of multiple cancers. Gene 2014, 533:21-25.
113. Tang T., Xue H., Cui S., Gong Z., Fei Z., Cheng S., et al. Association of interleukin-23 receptor gene polymorphisms with risk of bladder cancer in Chinese. Fam. Cancer 2014, 13:619-623.
114. Ni B., Chen S., Xie H., Ma H. Functional polymorphisms in interleukin-23 receptor and susceptibility to esophageal squamous cell carcinoma in Chinese population. PLOS ONE 2014, 9:e89111.
115. Zhou S., Ruan Y., Yu H., Chen Y., Yao Y., Ma Y., et al. Functional IL-23R rs10889677 genetic polymorphism and risk of multiple solid tumors: a meta-analysis. PLoS ONE 2013, 8:e80627.
116. Qian X., Cao S., Yang G., Pan Y., Yin C., Chen X., et al. Potentially functional polymorphism in IL-23 receptor and risk of acute myeloid leukemia in a Chinese population. PLoS ONE 2013, 8:e55473.
117. Di Meglio P., Villanova F., Napolitano L., Tosi I., Terranova Barberio M., Mak R.K., et al. The IL23R A/Gln381 allele promotes IL-23 unresponsiveness in human memory T-helper 17 cells and impairs Th17 responses in psoriasis patients. J. Invest. Dermatol. 2013, 133:2381-2389.
118. Lin Z., Poritz L., Franke A., Li T.Y., Ruether A., Byrnes K.A., et al. Genetic association of nonsynonymous variants of the IL23R with familial and sporadic inflammatory bowel disease in women. Dig. Dis. Sci. 2010, 55:739-746.
119. Sarin R., Wu X., Abraham C. Inflammatory disease protective R381Q IL23 receptor polymorphism results in decreased primary CD4+ and CD8+ human T-cell functional responses. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:9560-9565.
120. Di Meglio P., Di Cesare A., Laggner U., Chu C.C., Napolitano L., Villanova F., et al. The IL23R R381Q gene variant protects against immune-mediated diseases by impairing IL-23-induced Th17 effector response in humans. PLoS ONE 2011, 6:e17160.
121. Pidasheva S., Trifari S., Phillips A., Hackney J.A., Ma Y., Smith A., et al. Functional studies on the IBD susceptibility gene IL23R implicate reduced receptor function in the protective genetic variant R381Q. PLoS ONE 2011, 6:e25038.
122. Oosting M., ter Hofstede H., van de Veerdonk F.L., Sturm P., Kullberg B.J., van der Meer J.W., et al. Role of interleukin-23 (IL-23) receptor signaling for IL-17 responses in human Lyme disease. Infect. Immun. 2011, 79:4681-4687.
123. Hazlett J., Stamp L.K., Merriman T., Highton J., Hessian P.A. IL-23R rs11209026 polymorphism modulates IL-17A expression in patients with rheumatoid arthritis. Genes Immun. 2012, 13:282-287.
124. Yu R.Y., Brazaitis J., Gallagher G. The human IL-23 receptor rs11209026 A allele promotes the expression of a soluble IL-23R-encoding mRNA species. J. Immunol. 2015, 194:1062-1068.
125. Belladonna M.L., Grohmann U. Bioengineering heterodimeric cytokines: turning promiscuous proteins into therapeutic agents. Biotechnol. Genet. Eng. Rev. 2013, 29:149-174.
126. Skrombolas D., Wylie I., Maharaj S., Frelinger J.G. Characterization of an IL-12 p40/p35 truncated fusion protein that can inhibit the action of IL-12. J. Interferon Cytokine Res. 2015, 10.1089/jir.2014.0176.
127. Benson J.M., Sachs C.W., Treacy G., Zhou H., Pendley C.E., Brodmerkel C.M., et al. Therapeutic targeting of the IL-12/23 pathways: generation and characterization of ustekinumab. Nat. Biotechnol. 2011, 29:615-624.
128. Lima X.T., Abuabara K., Kimball A.B., Lima H.C. Briakinumab. Expert Opin. Biol. Ther. 2009, 9:1107-1113.
129. Ramamurthy V., Krystek S.R., Bush A., Wei A., Emanuel S.L., Das Gupta R., et al. Structures of adnectin/protein complexes reveal an expanded binding footprint. Structure 2012, 20:259-269.
130. Yu R.Y., Gallagher G. A naturally occurring, soluble antagonist of human IL-23 inhibits the development and in vitro function of human Th17 cells. J. Immunol. 2010, 185:7302-7308.
131. Guo W., Luo C., Wang C., Zhu Y., Wang X., Gao X., et al. Protection against Th17 cells differentiation by an interleukin-23 receptor cytokine-binding homology region. PLoS ONE 2012, 7:e45625.
132. Guo W., Luo C., Wang C., Wang Y.H., Wang X., Gao X.D., et al. Suppression of human and mouse Th17 differentiation and autoimmunity by an endogenous Interleukin 23 receptor cytokine-binding homology region. Int. J. Biochem. Cell Biol. 2014, 55:304-310.
133. Economides A.N., Carpenter L.R., Rudge J.S., Wong V., Koehler-Stec E.M., Hartnett C., et al. Cytokine traps: multi-component, high-affinity blockers of cytokine action. Nat. Med. 2003, 9:47-52.
134. Ancey C., Kuster A., Haan S., Herrmann A., Heinrich P.C., Muller-Newen G. A fusion protein of the gp130 and interleukin-6Ralpha ligand-binding domains acts as a potent interleukin-6 inhibitor. J. Biol. Chem. 2003, 278:16968-16972.
135. Metz S., Wiesinger M., Vogt M., Lauks H., Schmalzing G., Heinrich P.C., et al. Characterization of the Interleukin (IL)-6 Inhibitor IL-6-RFP: fused receptor domains act as high affinity cytokine-binding proteins. J. Biol. Chem. 2007, 282:1238-1248.
136. Metz S., Naeth G., Heinrich P.C., Muller-Newen G. Novel inhibitors for murine and human leukemia inhibitory factor based on fused soluble receptors. J. Biol. Chem. 2008, 283:5985-5995.
137. Wada Y., Cardinale I., Khatcherian A., Chu J., Kantor A.B., Gottlieb A.B., et al. Apilimod inhibits the production of IL-12 and IL-23 and reduces dendritic cell infiltration in psoriasis. PLoS ONE 2012, 7:e35069.