E3 Ubiquitin Ligase Cbl-b Suppresses Proallergic T Cell Development and Allergic Airway Inflammation

Cell Reports

Volumn 6, Issue 4, 2014, Pages 709-723

  Qiao, Guilin ^a,h   Ying, Haiyan ^a   Zhao, Yixia ^a,b,f   Liang, Yanran ^a,b,f   Guo, Hui ^a,b   Shen, Huifeng ^b   Li, Zhenping ^a   Solway, Julian ^a   Tao, Enxiang ^g   Chiang, Y Jeffrey ^c   Lipkowitz, Stanley ^c   Penninger, Josef M ^d   Langdon, Wallace Y ^e   Zhang, Jian ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^e UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^f CENTRAL SOUTH UNIVERSITY   (China)

^g SUN YAT SEN MEMORIAL HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

^h UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CBL B PROTEIN; CBL PROTEIN; GLUTATHIONE TRANSFERASE; INTERLEUKIN 4; STAT5 PROTEIN; STAT6 PROTEIN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR C MAF; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR JUNB; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; CD28 ANTIGEN; E3 UBIQUITIN LIGASE CBL B; GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 5; INTERLEUKIN 9;

ALLERGIC AIRWAY INFLAMMATION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; CELL DIFFERENTIATION; CELL MATURATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; HELPER CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TH2 CELL; TH9 CELL; UBIQUITINATION; CELL COUNT; DISEASE SEVERITY; LYMPHOCYTE DIFFERENTIATION; PROTEIN FUNCTION; TH1 CELL; TH17 CELL;

MUS; PYRONIA TITHONUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGENS, CD28; ASTHMA; CELL DIFFERENTIATION; INTERLEUKIN-4; MICE; MICE, INBRED BALB C; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-CBL; STAT6 TRANSCRIPTION FACTOR; TH2 CELLS; UBIQUITINATION;

EID: 84896711649     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.01.012     Document Type: Article

References (49)

1. Bachmaier K., Krawczyk C., Kozieradzki I., Kong Y.-Y., Sasaki T., Oliveira-dos-Santos A.J., Mariathasan S., Bouchard D., Wakeham A., Itie A., et al. Negative regulation of lymphocyte activation and autoimmunity by the molecular adaptor Cbl-b. Nature 2000, 403:211-216.
2. Bachmaier K., Toya S., Gao X., Triantafillou T., Garrean S., Park G.Y., Frey R.S., Vogel S., Minshall R., Christman J.W., et al. E3 ubiquitin ligase Cblb regulates the acute inflammatory response underlying lung injury. Nat. Med. 2007, 13:920-926.
3. Bettelli E., Oukka M., Kuchroo V.K. T(H)-17 cells in the circle of immunity and autoimmunity. Nat. Immunol. 2007, 8:345-350.
4. Chang H.-C., Sehra S., Goswami R., Yao W., Yu Q., Stritesky G.L., Jabeen R., McKinley C., Ahyi A.-N., Han L., et al. The transcription factor PU.1is required for the development of IL-9-producing Tcells and allergic inflammation. Nat. Immunol. 2010, 11:527-534.
5. Chatila T.A. Interleukin-4 receptor signaling pathways in asthma pathogenesis. Trends Mol. Med. 2004, 10:493-499.
6. Chiang Y.J., Kole H.K., Brown K., Naramura M., Fukuhara S., Hu R.-J., Jang I.K., Gutkind J.S., Shevach E., Gu H. Cbl-b regulates the CD28 dependence of T-cell activation. Nature 2000, 403:216-220.
7. + Foxp3(-) effector Tcells. Nat. Immunol. 2008, 9:1347-1355.
8. Ettenberg S.A., Magnifico A., Cuello M., Nau M.M., Rubinstein Y.R., Yarden Y., Weissman A.M., Lipkowitz S. Cbl-b-dependent coordinated degradation of the epidermal growth factor receptor signaling complex. J.Biol. Chem. 2001, 276:27677-27684.
9. Goswami R., Jabeen R., Yagi R., Pham D., Zhu J., Goenka S., Kaplan M.H. STAT6-dependent regulation of Th9 development. J.Immunol. 2012, 188:968-975.
10. Gruber T., Hermann-Kleiter N., Hinterleitner R., Fresser F., Schneider R., Gastl G., Penninger J.M., Baier G. PKC-theta modulates the strength of Tcell responses by targeting Cbl-b for ubiquitination and degradation. Sci. Signal. 2009, 2:ra30.
11. Guo H., Qiao G., Ying H., Li Z., Zhao Y., Liang Y., Yang L., Lipkowitz S., Penninger J.M., Langdon W.Y., Zhang J. E3 ubiquitin ligase Cbl-b regulates Pten via Nedd4 in Tcells independently of its ubiquitin ligase activity. Cell Rep 2012, 1:472-482.
12. Gustin S.E., Thien C.B., Langdon W.Y. Cbl-b is a negative regulator of inflammatory cytokines produced by IgE-activated mast cells. J.Immunol. 2006, 177:5980-5989.
13. Harada Y., Harada Y., Elly C., Ying G., Paik J.-H., DePinho R.A., Liu Y.-C. Transcription factors Foxo3a and Foxo1 couple the E3 ligase Cbl-b to the induction of Foxp3 expression in induced regulatory Tcells. J.Exp. Med. 2010, 207:1381-1391.
14. Harrington L.E., Mangan P.R., Weaver C.T. Expanding the effector CD4 T-cell repertoire: the Th17 lineage. Curr. Opin. Immunol. 2006, 18:349-356.
15. Heissmeyer V., Macián F., Im S.H., Varma R., Feske S., Venuprasad K., Gu H., Liu Y.C., Dustin M.L., Rao A. Calcineurin imposes Tcell unresponsiveness through targeted proteolysis of signaling proteins. Nat. Immunol. 2004, 5:255-265.
16. Hou J., Schindler U., Henzel W.J., Ho T.C., Brasseur M., McKnight S.L. An interleukin-4-induced transcription factor: IL-4 Stat. Science 1994, 265:1701-1706.
17. Jeon M.S., Atfield A., Venuprasad K., Krawczyk C., Sarao R., Elly C., Yang C., Arya S., Bachmaier K., Su L., et al. Essential role of the E3 ubiquitin ligase Cbl-b in Tcell anergy induction. Immunity 2004, 21:167-177.
18. Kaplan M.H. Th9 cells: differentiation and disease. Immunol. Rev. 2013, 252:104-115.
19. Kaplan M.H., Schindler U., Smiley S.T., Grusby M.J. Stat6 isrequired for mediating responses to IL-4 and for development of Th2 cells. Immunity 1996, 4:313-319.
20. Korn T., Bettelli E., Oukka M., Kuchroo V.K. IL-17 and Th17 Cells. Annu. Rev. Immunol. 2009, 27:485-517.
21. Li D., Gál I., Vermes C., Alegre M.L., Chong A.S., Chen L., Shao Q., Adarichev V., Xu X., Koreny T., et al. Cutting edge: Cbl-b: one of the key molecules tuning CD28- and CTLA-4-mediated Tcell costimulation. J.Immunol. 2004, 173:7135-7139.
22. Matsukura S., Stellato C., Georas S.N., Casolaro V., Plitt J.R., Miura K., Kurosawa S., Schindler U., Schleimer R.P. Interleukin-13 upregulates eotaxin expression in airway epithelial cells by a STAT6-dependent mechanism. Am. J. Respir. Cell Mol. Biol. 2001, 24:755-761.
23. Mikita T., Campbell D., Wu P., Williamson K., Schindler U. Requirements for interleukin-4-induced gene expression and functional characterization of Stat6. Mol. Cell. Biol. 1996, 16:5811-5820.
24. Mikita T., Daniel C., Wu P., Schindler U. Mutational analysis of the STAT6 SH2 domain. J.Biol. Chem. 1998, 273:17634-17642.
25. lo thymocytes invivo. Science 1990, 250:1720-1723.
26. Murphy K.M., Ouyang W., Farrar J.D., Yang J., Ranganath S., Asnagli H., Afkarian M., Murphy T.L. Signaling and transcription in T helper development. Annu. Rev. Immunol. 2000, 18:451-494.
27. Myou S., Leff A.R., Myo S., Boetticher E., Tong J., Meliton A.Y., Liu J., Munoz N.M., Zhu X. Blockade of inflammation and airway hyperresponsiveness in immune-sensitized mice by dominant-negative phosphoinositide 3-kinase-TAT. J.Exp. Med. 2003, 198:1573-1582.
28. Oh S.Y., Park J.-U., Zheng T., Kim Y.-K., Wu F., Cho S.H., Barber D., Penninger J., Zhu Z. Cbl-b regulates airway mucosal tolerance to aeroallergen. Clin. Exp. Allergy 2011, 41:434-442.
29. Oksvold M.P., Dagger S.A., Thien C.B., Langdon W.Y. The Cbl-b RING finger domain has a limited role in regulating inflammatory cytokine production by IgE-activated mast cells. Mol. Immunol. 2008, 45:925-936.
30. Onodera A., Yamashita M., Endo Y., Kuwahara M., Tofukuji S., Hosokawa H., Kanai A., Suzuki Y., Nakayama T. STAT6-mediated displacement of polycomb by trithorax complex establishes long-term maintenance of GATA3 expression in T helper type 2 cells. J.Exp. Med. 2010, 207:2493-2506.
31. Park H., Li Z., Yang X.O., Chang S.H., Nurieva R., Wang Y.H., Wang Y., Hood L., Zhu Z., Tian Q., Dong C. A distinct lineage of CD4Tcellsregulates tissue inflammation by producing interleukin 17. Nat. Immunol. 2005, 6:1133-1141.
32. Perkins C., Yanase N., Smulian G., Gildea L., Orekov T., Potter C., Brombacher F., Aronow B., Wills-Karp M., Finkelman F.D. Selective stimulation of IL-4 receptor on smooth muscle induces airway hyperresponsiveness in mice. J.Exp. Med. 2011, 208:853-867.
33. Pernis A.B., Rothman P.B. JAK-STAT signaling in asthma. J.Clin. Invest. 2002, 109:1279-1283.
34. Qiao G., Lei M., Li Z., Sun Y., Minto A., Fu Y.X., Ying H., Quigg R.J., Zhang J. Negative regulation of CD40-mediated B cell responses by E3 ubiquitin ligase Casitas-B-lineage lymphoma protein-B. J.Immunol. 2007, 179:4473-4479.
35. Qiao G., Li Z., Molinero L., Alegre M.L., Ying H., Sun Z., Penninger J.M., Zhang J. T-cell receptor-induced NF-kappaB activation is negatively regulated by E3 ubiquitin ligase Cbl-b. Mol. Cell. Biol. 2008, 28:2470-2480.
36. Qiao G., Zhao Y., Li Z., Tang P.Q., Langdon W.Y., Yang T., Zhang J. T cell activation threshold regulated by E3 ubiquitin ligase Cbl-b determines fate of inducible regulatory Tcells. J.Immunol. 2013, 191:632-639.
37. Sohn H.W., Gu H., Pierce S.K. Cbl-b negatively regulates B cell antigen receptor signaling in mature B cells through ubiquitination of the tyrosine kinase Syk. J.Exp. Med. 2003, 197:1511-1524.
38. Staudt V., Bothur E., Klein M., Lingnau K., Reuter S., Grebe N., Gerlitzki B., Hoffmann M., Ulges A., Taube C., et al. Interferon-regulatory factor 4 is essential for the developmental program of T helper 9 cells. Immunity 2010, 33:192-202.
39. Szabo S.J., Kim S.T., Costa G.L., Zhang X., Fathman C.G., Glimcher L.H. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 2000, 100:655-669.
40. Takeda K., Tanaka T., Shi W., Matsumoto M., Minami M., Kashiwamura S., Nakanishi K., Yoshida N., Kishimoto T., Akira S. Essential role of Stat6 in IL-4 signalling. Nature 1996, 380:627-630.
41. Thien C.B., Langdon W.Y. c-Cbl and Cbl-b ubiquitin ligases: substrate diversity and the negative regulation of signalling responses. Biochem. J. 2005, 391:153-166.
42. Veldhoen M., Uyttenhove C., van Snick J., Helmby H., Westendorf A., Buer J., Martin B., Wilhelm C., Stockinger B. Transforming growth factor-β 'reprograms' the differentiation of T helper 2 cells and promotes an interleukin 9-producing subset. Nat. Immunol. 2008, 9:1341-1346.
43. Wan Y.Y., Flavell R.A. How diverse-CD4 effector Tcells and their functions. J.Mol. Cell Biol. 2009, 1:20-36.
44. Wurster A.L., Tanaka T., Grusby M.J. The biology of Stat4 and Stat6. Oncogene 2000, 19:2577-2584.
45. Yang X.O., Zhang H., Kim B.-S., Niu X., Peng J., Chen Y., Kerketta R., Lee Y.-H., Chang S.H., Corry D.B., et al. The signaling suppressor CIS controls proallergic Tcell development and allergic airway inflammation. Nat. Immunol. 2013, 14:732-740.
46. Yao W., Zhang Y., Jabeen R., Nguyen E.T., Wilkes D.S., Tepper R.S., Kaplan M.H., Zhou B. Interleukin-9 is required for allergic airway inflammation mediated by the cytokine TSLP. Immunity 2013, 38:360-372.
47. Ying H., Yang L., Qiao G., Li Z., Zhang L., Yin F., Xie D., Zhang J. Cutting edge: CTLA-4-B7 interaction suppresses Th17 cell differentiation. J.Immunol. 2010, 185:1375-1378.
48. Zamorano J., Rivas M.D., Setien F., Perez-G M. Proteolytic regulation of activated STAT6 by calpains. J.Immunol. 2005, 174:2843-2848.
49. Zhang J., Bárdos T., Li D.-D., Gál I., Vermes C., Xu J.-Y., Mikecz K., Finnegan A., Lipkowitz S., Glant T.T. Cutting edge: regulation of Tcell activation threshold by CD28 costimulation through targeting Cbl-b for ubiquitination. J.Immunol. 2002, 169:2236-2240.