Defining the functional binding sites of interleukin 12 receptor β1 and interleukin 23 receptor to Janus kinases

Molecular Biology of the Cell

Volumn 27, Issue 14, 2016, Pages 2301-2316

  Floss, Doreen M ^a   Klöcker, Tobias ^a   Schröder, Jutta ^a   Lamertz, Larissa ^a   Mrotzek, Simone ^a   Strobl, Birgit ^b   Hermanns, Heike ^c   Scheller, Jörgen ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^c UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BOX1 PROTEIN; BOX2 PROTEIN; INTERLEUKIN 12 RECEPTOR BETA1; INTERLEUKIN 23 RECEPTOR; JANUS KINASE; PROTEIN; PROTEIN KINASE TYK2; STAT3 PROTEIN; UNCLASSIFIED DRUG; IL12RB1 PROTEIN, HUMAN; IL23A PROTEIN, HUMAN; IL23R PROTEIN, HUMAN; INTERLEUKIN 12; INTERLEUKIN 12 RECEPTOR; INTERLEUKIN 23; INTERLEUKIN 23P19; INTERLEUKIN RECEPTOR; JAK2 PROTEIN, HUMAN; JANUS KINASE 2; PROTEIN BINDING;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL PROLIFERATION; CELL SURFACE; COMPARATIVE STUDY; CONSENSUS SEQUENCE; CONTROLLED STUDY; COS 7 CELL LINE; FIBROSARCOMA CELL; HUMAN; HUMAN CELL; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TH17 CELL; ANIMAL; CHLOROCEBUS AETHIOPS; COS CELL LINE; IMMUNOLOGY; METABOLISM; PHOSPHORYLATION; TUMOR CELL LINE;

AMINO ACID MOTIFS; ANIMALS; BINDING SITES; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; COS CELLS; HUMANS; INTERLEUKIN-12; INTERLEUKIN-23; INTERLEUKIN-23 SUBUNIT P19; JANUS KINASE 2; PHOSPHORYLATION; PROTEIN BINDING; RECEPTORS, INTERLEUKIN; RECEPTORS, INTERLEUKIN-12; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TYK2 KINASE;

EID: 84978633440     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-12-1645     Document Type: Article

References (56)

1. Althoff K, Möllberg J, Aasland D, Voltz N, Kallen K, Grötzinger J, Rose-John S (2001). Recognition sequences and structural elements contribute to shedding susceptibility of membrane proteins. Biochem J 353, 663-672.
2. Aparicio-Siegmund S, Moll JM, Lokau J, Grusdat M, Schröder J, Plöhn S, Rose-John S, Grötzinger J, Lang PA, Scheller J, et al. (2014). Inhibition of protein kinase II (CK2) prevents induced signal transducer and activator of transcription (STAT) 1/3 and constitutive STAT3 activation. Oncotarget 5, 2131-2148.
3. Bacon CM, McVicar DW, Ortaldo JR, Rees RC, OShea JJ, Johnston JA (1995a). Interleukin 12 (IL-12) induces tyrosine phosphorylation of JAK2 and TYK2: differential use of Janus family tyrosine kinases by IL-2 and IL-12. J Exp Med 181, 399-404.
4. Bacon CM, Petricoin EF, Ortaldo JR, Rees RC, Larner AC, Johnston JA, OShea JJ (1995b). Interleukin 12 induces tyrosine phosphorylation and activation of STAT4 in human lymphocytes. Proc Natl Acad Sci USA 92, 7307-7311.
5. Behrmann I, Smyczek T, Heinrich PC, Schmitz-Van de Leur H, Komyod W, Giese B, Muller-Newen G, Haan S, Haan C (2004). Janus kinase (Jak) subcellular localization revisited: The exclusive membrane localization of endogenous Janus kinase 1 by cytokine receptor interaction uncovers the Jak receptor complex to be equivalent to a receptor tyrosine kinase. J Biol Chem 279, 35486-35493.
6. Chua A, Wilkinson V, Presky D, Gubler U (1995). Cloning and characterization of a mouse IL-12 receptor-beta component. J Immunol 155, 4286-4294.
7. Collison L, Vignali DA (2008). Interleukin-35: odd one out or part of the family? Immunol Rev 226, 248-262.
8. Colosi P, Wong K, Leong SR, Wood WI (1993). Mutational analysis of the intracellular domain of the human growth hormone receptor. J Biol Chem 268, 12617-12623.
9. Cosmi L, Maggi L, Santarlasci V, Liotta F, Annunziato F (2014). T helper cells plasticity in inflammation. Cytometry A 85, 36-42.
10. De Paus R, van de Wetering D, van Dissel J, van de Vosse E (2008). IL-23 and IL-12 responses in activated human T cells retrovirally transduced with IL-23 receptor variants. Mol Immunol 45, 3889-3895.
11. Di Cesare A, Di Meglio P, Nestle FO (2009). The IL-23/Th17 axis in the immunopathogenesis of psoriasis. J Invest Dermatol 129, 1339-1350.
12. Di Meglio P, Di Cesare A, Laggner U, Chu C, Napolitano L, Villanova F, Tosi I, Capon F, Trembath RC, Peris K, et al. (2011). The IL23R R381Q gene variant protects against immune-mediated diseases by impairing IL-23-induced Th17 effector response in humans. PLoS One 6, e17160.
13. Di Meglio P, Villanova F, Napolitano L, Tosi I, Terranova Barberio M, Mak RK, Nutland S, Smith CH, Barker JN, Todd JA, Nestle FO (2013). 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 133, 2381-2389.
14. Fischer M, Goldschmitt J, Peschel C, Brakenhoff J, Kallen K, Wollmer A, Grötzinger J, Rose-John S (1997). A bioactive designer cytokine for human hematopoietic progenitor cell expansion. Nat Biotechnol 15, 142-145.
15. Floss DM, Mrotzek S, Klocker T, Schroder J, Grotzinger J, Rose-John S, Scheller J (2013). 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 288, 19386-19400.
16. Floss DM, Schröder J, Franke M, Scheller J (2015). Insights into IL-23 biology. From structure to function. Cytokine Growth Factor Rev 26, 269-578.
17. Fukunaga R, Ishizaka-Ikeda E, Pan CX, Seto Y, Nagata S (1991). Functional domains of the granulocyte colony-stimulating factor receptor. EMBO J 10, 2855-2865.
18. Garbers C, Hermanns H, Schaper F, Möller-Newen G, Grötzinger J, Rose-John S, Scheller J (2012). Plasticity and cross-Talk of interleukin 6-Type cytokines. Plasticity and cross-Talk of interleukin 6-Type cytokines. Cytokine Growth Factor Rev 23, 85-97.
19. Gearing D, Ziegler S, Comeau M, Friend D, Thoma B, Cosman D, Park L, Mosley B (1994). Proliferative responses and binding properties of hematopoietic cells transfected with low-Affinity receptors for leukemia inhibitory factor, oncostatin M, and ciliary neurotrophic factor. Proc Natl Acad Sci USA 91, 1119-1123.
20. Guschin D, Rogers N, Briscoe J, Witthuhn B, Watling D, Horn F, Pellegrini S, Yasukawa K, Heinrich P, Stark GR, et al. (1995). A major role for the protein tyrosine kinase JAK1 in the JAK/STAT signal transduction pathway in response to interleukin-6. EMBO J 14, 1421-1429.
21. Ha SJ, Lee CH, Lee SB, Kim CM, Jang KL, Shin HS, Sung YC (1999). A novel function of IL-12p40 as a chemotactic molecule for macrophages. J Immunol 163, 2902-2908.
22. Haan C, Haan S (2013). Co-immunoprecipitation protocol to investigate cytokine receptor-Associated proteins, e.g., Janus kinases or other associated signaling proteins. Methods Mol Biol 967, 21-38.
23. Ihle JN, Kerr IM (1995). Jaks and Stats in signaling by the cytokine receptor superfamily. Trends Genet 11, 69-74.
24. Jacobson NG, Szabo SJ, Weber-Nordt RM, Zhong Z, Schreiber RD, Darnell JE Jr, Murphy KM (1995). Interleukin 12 signaling in T helper type 1 (Th1) cells involves tyrosine phosphorylation of signal transducer and activator of transcription (Stat)3 and Stat4. J Exp Med 181, 1755-1762.
25. Karaghiosoff M, Neubauer H, Lassnig C, Kovarik P, Schindler H, Pircher H, McCoy B, Bogdan C, Decker T, Brem G, et al. (2000). Partial impairment of cytokine responses in Tyk2-deficient mice. Immunity 13, 549-560.
26. Ketteler R, Glaser S, Sandra O, Martens U, Klingmöller U (2002). Enhanced transgene expression in primitive hematopoietic progenitor cells and embryonic stem cells efficiently transduced by optimized retroviral hybrid vectors. Gene Ther 9, 477-487.
27. Korn T, Bettelli E, Oukka M, Kuchroo VK (2009). IL-17 and Th17 cells. Annu Rev Immunol 27, 485-517.
28. Kotenko SV, Izotova LS, Pollack BP, Muthukumaran G, Paukku K, Silvennoinen O, Ihle JN, Pestka S (1996). Other kinases can substitute for Jak2 in signal transduction by interferon-gamma. J Biol Chem 271, 17174-17182.
29. Minegishi Y, Saito M, Morio T, Watanabe K, Agematsu K, Tsuchiya S, Takada H, Hara T, Kawamura N, Ariga T, et al. (2006). Human tyrosine kinase 2 deficiency reveals its requisite roles in multiple cytokine signals involved in innate and acquired immunity. Immunity 25, 745-755.
30. Murakami M, Narazaki M, Hibi M, Yawata H, Yasukawa K, Hamaguchi M, Taga T, Kishimoto T (1991). Critical cytoplasmic region of the interleukin 6 signal transducer gp130 is conserved in the cytokine receptor family. Proc Natl Acad Sci USA 88, 11349-11353.
31. Naeger L, McKinney J, Salvekar A, Hoey T (1999). Identification of a STAT4 binding site in the interleukin-12 receptor required for signaling. J Biol Chem 274, 1875-1878.
32. Neubauer H, Cumano A, Muller M, Wu H, Huffstadt U, Pfeffer K (1998). Jak2 deficiency defines an essential developmental checkpoint in definitive hematopoiesis. Cell 93, 397-409.
33. Nishikomori R, Usui T, Wu CY, Morinobu A, OShea JJ, Strober W (2002). Activated STAT4 has an essential role in Th1 differentiation and proliferation that is independent of its role in the maintenance of IL-12R beta 2 chain expression and signaling. J Immunol 169, 4388-4398.
34. Ouyang W, Kolls JK, Zheng Y (2008). The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28, 454-467.
35. Parganas E, Wang D, Stravopodis D, Topham DJ, Marine JC, Teglund S, Vanin EF, Bodner S, Colamonici OR, van Deursen JM, et al. (1998). Jak2 is essential for signaling through a variety of cytokine receptors. Cell 93, 385-395.
36. Parham C, Chirica M, Timans J, Vaisberg E, Travis M, Cheung J, Pflanz S, Zhang R, Singh KP, Vega F, et al. (2002). A receptor for the heterodimeric cytokine IL-23 is composed of IL-12Rbeta1 and a novel cytokine receptor subunit, IL-23R. J Immunol 168, 5699-5708.
37. Park H, Li Z, Yang XO, Hee Chang S, Nurieva R, Wang Y, Wang Y, Hood L, Zhu Z, Tian Q, et al. (2005). A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 6, 1133-1141.
38. Pidasheva S, Trifari S, Phillips A, Hackney JA, Ma Y, Smith A, Sohn SJ, Spits H, Little RD, Behrens TW, et al. (2011). Functional studies on the IBD susceptibility gene IL23R implicate reduced receptor function in the protective genetic variant R381Q. PLoS One 6, e25038.
39. Prchal-Murphy M, Semper C, Lassnig C, Wallner B, Gausterer C, Teppner-Klymiuk I, Kobolak J, Möller S, Kolbe T, Karaghiosoff M, et al. (2012). TYK2 kinase activity is required for functional type I interferon responses in vivo. PLoS One 7, e39141.
40. Presky D, Yang H, Minetti L, Chua A, Nabavi N, Wu C, Gately M, Gubler U (1996). A functional interleukin 12 receptor complex is composed of two beta-Type cytokine receptor subunits. Proc Natl Acad Sci USA 93, 14002-14007.
41. Russell TD, Yan Q, Fan G, Khalifah AP, Bishop DK, Brody SL, Walter MJ (2003). IL-12 p40 homodimer-dependent macrophage chemotaxis and respiratory viral inflammation are mediated through IL-12 receptor beta 1. J Immunol 171, 6866-6874.
42. Sakamaki K, Miyajima I, Kitamura T, Miyajima A (1992). Critical cytoplasmic domains of the common beta subunit of the human GM-CSF, IL-3 and IL-5 receptors for growth signal transduction and tyrosine phosphorylation. EMBO J 11, 3541-3549.
43. Sarin R, Wu X, Abraham C (2011). Inflammatory disease protective R381Q IL23 receptor polymorphism results in decreased primary CD4+ and CD8+ human T-cell functional responses. Proc Natl Acad Sci USA 108, 9560-9565.
44. Shimoda K, Kato K, Aoki K, Matsuda T, Miyamoto A, Shibamori M, Yamashita M, Numata A, Takase K, Kobayashi S, et al. (2000). Tyk2 plays a restricted role in IFN alpha signaling, although it is required for IL-12-mediated T cell function. Immunity 13, 561-571.
45. Suthaus J, Tillmann A, Lorenzen I, Bulanova E, Rose-John S, Scheller J (2010). Forced homo-And heterodimerization of all gp130-Type receptor complexes leads to constitutive ligand-independent signaling and cytokine-independent growth. Mol Biol Cell 21, 2797-2807.
46. Tanner JW, Chen W, Young RL, Longmore GD, Shaw AS (1995). The conserved box 1 motif of cytokine receptors is required for association with JAK kinases. J Biol Chem 270, 6523-6530.
47. Thierfelder WE, van Deursen JM, Yamamoto K, Tripp RA, Sarawar SR, Carson RT, Sangster MY, Vignali DAA, Doherty PC, Grosveld GC, et al. (1996). Requirement for Stat4 in interleukin-12-mediated responses of natural killer and T cells. Nature 382, 171-174.
48. Trinchieri G, Pflanz S, Kastelein RA (2003). The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity 19, 641-644.
49. Usacheva A, Sandoval R, Domanski P, Kotenko SV, Nelms K, Goldsmith MA, Colamonici OR (2002). Contribution of the Box 1 and Box 2 motifs of cytokine receptors to Jak1 association and activation. J Biol Chem 277, 48220-48226.
50. Vignali DA, Kuchroo V (2012). IL-12 family cytokines: Immunological playmakers. Nat Immunol 13, 722-728.
51. Wallweber HJ, Tam C, Franke Y, Starovasnik MA, Lupardus PJ (2014). Structural basis of recognition of interferon-Alpha receptor by tyrosine kinase 2. Nat Struct Mol Biol 21, 443-448.
52. Watford WT, Hissong BD, Bream JH, Kanno Y, Muul L, OShea JJ (2004). Signaling by IL-12 and IL-23 and the immunoregulatory roles of STAT4. Immunol Rev 202, 139-156.
53. Watford WT, Moriguchi M, Morinobu A, OShea JJ (2003). The biology of IL-12: Coordinating innate and adaptive immune responses. Cytokine Growth Factor Rev 14, 361-368.
54. Wu C, Wang X, Gadina M, OShea J, Presky D, Magram J (2000). IL-12 receptor beta 2 (IL-12R beta 2)-deficient mice are defective in IL-12-mediated signaling despite the presence of high affinity IL-12 binding sites. J Immunol 165, 6221-6228.
55. Yamamoto K, Yamaguchi M, Miyasaka N, Miura O (2003). SOCS-3 inhibits IL-12-induced STAT4 activation by binding through its SH2 domain to the STAT4 docking site in the IL-12 receptor beta2 subunit. Biochem Biophys Res Commun 310, 1188-1193.
56. Zou J, Presky DH, Wu CY, Gubler U (1997). Differential associations between the cytoplasmic regions of the interleukin-12 receptor subunits beta1 and beta2 and JAK kinases. J Biol Chem 272, 6073-6077.