PKCθ/β and CYLD Are Antagonistic Partners in the NFκB and NFAT Transactivation Pathways in Primary Mouse CD3+ T Lymphocytes

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Thuille, Nikolaus ^a   Wachowicz, Katarzyna ^a   Hermann Kleiter, Natascha ^a   Kaminski, Sandra ^a   Fresser, Friedrich ^a   Lutz Nicoladoni, Christina ^a   Leitges, Michael ^b   Thome, Margot ^c   Massoumi, Ramin ^d   Baier, Gottfried ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF OSLO   (Norway)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 2; PROTEIN KINASE C; TRANSCRIPTION FACTOR NFAT; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD3+ T LYMPHOCYTE; CYTOKINE PRODUCTION; GEL MOBILITY SHIFT ASSAY; IMMUNOPRECIPITATION; IMMUNOSTIMULATION; LEUKEMIA CELL LINE; LYMPH NODE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; SPLEEN; T LYMPHOCYTE; THYMUS; TRANSACTIVATION;

ANIMALS; ANTIGENS, CD3; CASPASES; CELL LINE; CYSTEINE ENDOPEPTIDASES; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; HUMANS; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MAP KINASE KINASE 4; MAP KINASE KINASE KINASES; MICE; MICE, KNOCKOUT; NEOPLASM PROTEINS; NF-KAPPA B; NFATC TRANSCRIPTION FACTORS; PHENOTYPE; PROTEIN BINDING; PROTEIN KINASE C; PROTEOLYSIS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSCRIPTIONAL ACTIVATION;

MUS;

EID: 84872395016     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053709     Document Type: Article

References (43)

1. Hayashi K, Altman A, (2007) Protein kinase C theta (PKCtheta): a key player in T cell life and death. Pharmacol Res 55: 537-544.
2. Marsland BJ, Kopf M, (2008) T-cell fate and function: PKC-theta and beyond. Trends Immunol 29: 179-185.
3. Sedwick CE, Altman A, (2004) Perspectives on PKCtheta in T cell activation. Mol Immunol 41: 675-686.
4. Kong KF, Yokosuka T, Canonigo-Balancio AJ, Isakov N, Saito T, et al. (2011) A motif in the V3 domain of the kinase PKC-theta determines its localization in the immunological synapse and functions in T cells via association with CD28. Nat Immunol 12: 1105-1112.
5. Pfeifhofer C, Kofler K, Gruber T, Tabrizi NG, Lutz C, et al. (2003) Protein kinase C theta affects Ca2+ mobilization and NFAT cell activation in primary mouse T cells. J Exp Med 197: 1525-1535.
6. Sun Z, Arendt CW, Ellmeier W, Schaeffer EM, Sunshine MJ, et al. (2000) PKC-theta is required for TCR-induced NF-kappaB activation in mature but not immature T lymphocytes. Nature 404: 402-407.
7. Marsland BJ, Soos TJ, Spath G, Littman DR, Kopf M, (2004) Protein kinase C theta is critical for the development of in vivo T helper (Th)2 cell but not Th1 cell responses. J Exp Med 200: 181-189.
8. Salek-Ardakani S, So T, Halteman BS, Altman A, Croft M, (2005) Protein kinase Ctheta controls Th1 cells in experimental autoimmune encephalomyelitis. J Immunol 175: 7635-7641.
9. Tan SL, Zhao J, Bi C, Chen XC, Hepburn DL, et al. (2006) Resistance to experimental autoimmune encephalomyelitis and impaired IL-17 production in protein kinase C theta-deficient mice. J Immunol 176: 2872-2879.
10. Giannoni F, Lyon AB, Wareing MD, Dias PB, Sarawar SR, (2005) Protein kinase C theta is not essential for T-cell-mediated clearance of murine gammaherpesvirus 68. J Virol 79: 6808-6813.
11. Bignell GR, Warren W, Seal S, Takahashi M, Rapley E, et al. (2000) Identification of the familial cylindromatosis tumour-suppressor gene. Nat Genet 25: 160-165.
12. Reiley WW, Jin W, Lee AJ, Wright A, Wu X, et al. (2007) Deubiquitinating enzyme CYLD negatively regulates the ubiquitin-dependent kinase Tak1 and prevents abnormal T cell responses. J Exp Med 204: 1475-1485.
13. Zhang J, Stirling B, Temmerman ST, Ma CA, Fuss IJ, et al. (2006) Impaired regulation of NF-kappaB and increased susceptibility to colitis-associated tumorigenesis in CYLD-deficient mice. J Clin Invest 116: 3042-3049.
14. Lim JH, Jono H, Koga T, Woo CH, Ishinaga H, et al. (2007) Tumor suppressor CYLD acts as a negative regulator for non-typeable Haemophilus influenza-induced inflammation in the middle ear and lung of mice. PLoS One 2: e1032.
15. Lim JH, Stirling B, Derry J, Koga T, Jono H, et al. (2007) Tumor suppressor CYLD regulates acute lung injury in lethal Streptococcus pneumoniae infections. Immunity 27: 349-360.
16. Ahmed N, Zeng M, Sinha I, Polin L, Wei WZ, et al. (2011) The E3 ligase Itch and deubiquitinase Cyld act together to regulate Tak1 and inflammation. Nat Immunol 12: 1176-1183.
17. Reiley WW, Zhang M, Jin W, Losiewicz M, Donohue KB, et al. (2006) Regulation of T cell development by the deubiquitinating enzyme CYLD. Nat Immunol 7: 411-417.
18. Staal J, Driege Y, Bekaert T, Demeyer A, Muyllaert D, et al. (2011) T-cell receptor-induced JNK activation requires proteolytic inactivation of CYLD by MALT1. EMBO J 30: 1742-1752.
19. Leitges M, Schmedt C, Guinamard R, Davoust J, Schaal S, et al. (1996) Immunodeficiency in protein kinase cbeta-deficient mice. Science 273: 788-791.
20. Massoumi R, Chmielarska K, Hennecke K, Pfeifer A, Fassler R, (2006) Cyld inhibits tumor cell proliferation by blocking Bcl-3-dependent NF-kappaB signaling. Cell 125: 665-677.
21. Wickstrom SA, Masoumi KC, Khochbin S, Fassler R, Massoumi R, (2010) CYLD negatively regulates cell-cycle progression by inactivating HDAC6 and increasing the levels of acetylated tubulin. EMBO J 29: 131-144.
22. Hermann-Kleiter N, Thuille N, Pfeifhofer C, Gruber T, Schafer M, et al. (2006) PKCtheta and PKA are antagonistic partners in the NF-AT transactivation pathway of primary mouse CD3+ T lymphocytes. Blood 107: 4841-4848.
23. Northrop JP, Ullman KS, Crabtree GR, (1993) Characterization of the nuclear and cytoplasmic components of the lymphoid-specific nuclear factor of activated T cells (NF-AT) complex. J Biol Chem 268: 2917-2923.
24. Gruber T, Pfeifhofer-Obermair C, Baier G, (2010) PKCtheta is necessary for efficient activation of NFkappaB, NFAT, and AP-1 during positive selection of thymocytes. Immunol Lett 132: 6-11.
25. Morley SC, Weber KS, Kao H, Allen PM, (2008) Protein kinase C-theta is required for efficient positive selection. J Immunol 181: 4696-4708.
26. Reiley W, Zhang M, Sun SC, (2004) Negative regulation of JNK signaling by the tumor suppressor CYLD. J Biol Chem 279: 55161-55167.
27. Koga T, Lim JH, Jono H, Ha UH, Xu H, et al. (2008) Tumor suppressor cylindromatosis acts as a negative regulator for Streptococcus pneumoniae-induced NFAT signaling. J Biol Chem 283: 12546-12554.
28. Coornaert B, Baens M, Heyninck K, Bekaert T, Haegman M, et al. (2008) T cell antigen receptor stimulation induces MALT1 paracaspase-mediated cleavage of the NF-kappaB inhibitor A20. Nat Immunol 9: 263-271.
29. Rebeaud F, Hailfinger S, Posevitz-Fejfar A, Tapernoux M, Moser R, et al. (2008) The proteolytic activity of the paracaspase MALT1 is key in T cell activation. Nat Immunol 9: 272-281.
30. Kingeter LM, Schaefer BC, (2008) Loss of protein kinase C theta, Bcl10, or Malt1 selectively impairs proliferation and NF-kappa B activation in the CD4+ T cell subset. J Immunol 181: 6244-6254.
31. Matsumoto R, Wang D, Blonska M, Li H, Kobayashi M, et al. (2005) Phosphorylation of CARMA1 plays a critical role in T Cell receptor-mediated NF-kappaB activation. Immunity 23: 575-585.
32. Wang D, Matsumoto R, You Y, Che T, Lin XY, et al. (2004) CD3/CD28 costimulation-induced NF-kappaB activation is mediated by recruitment of protein kinase C-theta, Bcl10, and IkappaB kinase beta to the immunological synapse through CARMA1. Mol Cell Biol 24: 164-171.
33. Thuille N, Gruber T, Bock G, Leitges M, Baier G, (2004) Protein kinase C beta is dispensable for TCR-signaling. Mol Immunol 41: 385-390.
34. Volkov Y, Long A, Kelleher D, (1998) Inside the crawling T cell: leukocyte function-associated antigen-1 cross-linking is associated with microtubule-directed translocation of protein kinase C isoenzymes beta(I) and delta. J Immunol 161: 6487-6495.
35. Volkov Y, Long A, McGrath S, Ni Eidhin D, Kelleher D, (2001) Crucial importance of PKC-beta(I) in LFA-1-mediated locomotion of activated T cells. Nat Immunol 2: 508-514.
36. Gruber T, Fresser F, Jenny M, Uberall F, Leitges M, et al. (2008) PKCtheta cooperates with atypical PKCzeta and PKCiota in NF-kappaB transactivation of T lymphocytes. Mol Immunol 45: 117-126.
37. Gruber T, Hermann-Kleiter N, Pfeifhofer-Obermair C, Lutz-Nicoladoni C, Thuille N, et al. (2009) PKC theta cooperates with PKC alpha in alloimmune responses of T cells in vivo. Mol Immunol 46: 2071-2079.
38. Brummelkamp TR, Nijman SM, Dirac AM, Bernards R, (2003) Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-kappaB. Nature 424: 797-801.
39. Kovalenko A, Chable-Bessia C, Cantarella G, Israel A, Wallach D, et al. (2003) The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature 424: 801-805.
40. Trompouki E, Hatzivassiliou E, Tsichritzis T, Farmer H, Ashworth A, et al. (2003) CYLD is a deubiquitinating enzyme that negatively regulates NF-kappaB activation by TNFR family members. Nature 424: 793-796.
41. O'Donnell MA, Perez-Jimenez E, Oberst A, Ng A, Massoumi R, et al. (2011) Caspase 8 inhibits programmed necrosis by processing CYLD. Nat Cell Biol 13: 1437-1442.
42. Reiley W, Zhang M, Wu X, Granger E, Sun SC, (2005) Regulation of the deubiquitinating enzyme CYLD by IkappaB kinase gamma-dependent phosphorylation. Mol Cell Biol 25: 3886-3895.
43. Jono H, Lim JH, Chen LF, Xu H, Trompouki E, et al. (2004) NF-kappaB is essential for induction of CYLD, the negative regulator of NF-kappaB: evidence for a novel inducible autoregulatory feedback pathway. J Biol Chem 279: 36171-36174.