Activation or suppression of NFκB by HPK1 determines sensitivity to activation-induced cell death

EMBO Journal

Volumn 24, Issue 24, 2005, Pages 4279-4290

  Brenner, Dirk ^a   Golks, Alexander ^a   Kiefer, Friedemann ^b   Krammer, Peter H ^a   Arnold, Rüdiger ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

Author keywords

AICD; Apoptosis; IKK; Signaling; TCR

Indexed keywords

HEMATOPOIETIC CELL KINASE; I KAPPA B; I KAPPA B ALPHA; I KAPPA B BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SMALL INTERFERING RNA; T LYMPHOCYTE RECEPTOR; CHUK PROTEIN, HUMAN; CONCANAVALIN A; FAS ANTIGEN; HEMATOPOIETIC PROGENITOR KINASE 1; I KAPPA B KINASE; IKBKB PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN SERINE THREONINE KINASE;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME REPRESSION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; SENSITIVITY ANALYSIS; SENSITIZATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; ANIMAL; APOPTOSIS; CELL LINE; CELL STRAIN COS1; CERCOPITHECUS; GENETIC TRANSFECTION; IMMUNOPRECIPITATION; LEUKEMIA CELL LINE; METABOLISM; MOUSE; PHENOTYPE; PHOSPHORYLATION; PLASMID; PROTEIN TERTIARY STRUCTURE; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME; TRANSGENIC MOUSE;

ANIMALIA; MUS MUSCULUS;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; CELL DEATH; CELL LINE; CERCOPITHECUS AETHIOPS; CONCANAVALIN A; COS CELLS; GENES, REPORTER; HUMANS; I-KAPPA B KINASE; IMMUNOPRECIPITATION; JURKAT CELLS; MICE; MICE, TRANSGENIC; NF-KAPPA B; PHENOTYPE; PHOSPHORYLATION; PLASMIDS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, ANTIGEN, T-CELL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TIME FACTORS; TRANSFECTION;

EID: 29244440885     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600894     Document Type: Article

References (57)

1. Arnold R, Liou J, Drexler HCA, Weiss A, Kiefer F (2001) Caspase-mediated cleavage of hematopoietic progenitor kinase 1 (HPK1) converts an activator of NFκB into an inhibitor of NFκB. J Biol Chem 276: 14675-14684
2. Arnold R, Patzak IM, Neuhaus B, Vancauwenbergh S, Veillette A, Van Lint J, Kiefer F (2005) Activation of hematopoietic progenitor kinase 1 involves relocation, autophosphorylation, and transphosphorylation by protein kinase D1. Mol Cell Biol 25: 2364-2383
3. Baumann S, Dostert A, Novac N, Bauer A, Schmid W, Fas SC, Krueger A, Heinzel T, Kirchhoff S, Schutz G, Krammer PH (2005) Glucocorticoids inhibit activation-induced cell death (AICD) via direct DNA-dependent repression of the CD95-ligand gene by a glucocorticoid receptor dimer. Blood 106: 617-625
4. Brunner T, Mogil RJ, LaFace D, Yoo NJ, Mahboubi A, Echeverri F, Martin SJ, Force WR, Lynch DH, Ware CF (1995) Cell-autonomous Fas (CD95)/Fas-ligand interaction mediates activation-induced apoptosis in T-cell hybridomas. Nature 373: 441-444
5. Campbell KJ, Rocha S, Perkins ND (2004) Active repression of antiapoptotic gene expression by ReIA(p65) NF-κB. Mol Cell 13: 853-865
6. Che TJ, You Y, Wang DH, Tanner MJ, Dixit VM, Lin X (2004) MALT1/paracaspase is a signaling component downstream of CARMA1 and mediates T cell receptor-induced NF-κB activation. J Biol Chem 279: 15870-15876
7. Coudronniere N, Villalba M, Englund N, Altman A (2000) NF-κB activation induced by T cell receptor/CD28 costimulation is mediated by protein kinase C-θ. Proc Natl Acad Sci USA 97: 3394-3399
8. Delhase M, Hayakawa M, Chen Y, Karin M (1999) Positive and negative regulation of IκB kinase activity through IKKβ subunit phosphorylation. Science 284: 309-313
9. Dhein J, Walczak H, Baumler C, Debatin KM, Krammer PH (1995) Autocrine T-cell suicide mediated by APO-1/(Fas/CD95). Nature 373: 438-441
10. Gaide O, Favier B, Legler DF, Bonnet D, Brissoni B, Valitutti S, Bron C, Tschopp J, Thome M (2002) CARMA1 is a critical lipid raft-associated regulator of TCR-induced NF-κB activation. Nat Immunol 3: 836-843
11. Ghosh S, Karin M (2002) Missing pieces in the NF-kappa B puzzle. Cell 109: S81-S96
12. Golks A, Brenner D, Fritsch C, Krammer PH, Lavrik IN (2005) c-FLIPR, a new regulator of death receptor-induced apoptosis. J Biol Chem 280: 14507-14513
13. Green DR (2003) Introduction: apoptosis in the development and function of the immune system. Semin Immunol 15: 121-123
14. Hayden MS, Ghosh S (2004) Signaling to NF-κB. Genes Dev 18: 2195-2224
15. Hehner SP, Hofmann TG, Ushmorov A, Dienz O, Leung IWL, Lassam N, Scheidereit C, Droge W, Schmitz ML (2000) Mixed-lineage kinase 3 delivers CD3/CD28-derived signals into the IκB kinase complex. Mol Cell Biol 20: 2556-2568
16. Hildeman DA, Zhu YN, Mitchell TC, Kappler J, Marrack P (2002) Molecular mechanisms of activated T cell death in vivo. Curr Opin Immunol 14: 354-359
17. Kamata H, Honda S, Maeda S, Chang LF, Hirata H, Karin M (2005) Reactive oxygen species promote TNFα-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 120: 649-661
18. Kane LP, Lin J, Weiss A (2002) It's all Rel-ative: NF-κB and CD28 costimulation of T-cell activation. Trends Immunol 23: 413-420
19. Karin M, Lin A (2002) NF-κB at the crossroads of life and death. Nat Immunol 3: 221-227
20. Kerstan A, Hunig T (2004) Cutting edge: distinct TCR- and CD28-derived signals regulate CD95L, Bcl-x(L), and the survival of primary T cells. J Immunol 172: 1341-1345
21. Khoshnan A, Bae D, Tindell CA, Nel AE (2000) The physical association of protein kinase C-θ with a lipid raft-associated inhibitor of κB factor kinase (IKK) complex plays a role in the activation of the NF-κB cascade by TCR and CD28. J Immunol 165: 6933-6940
22. Kiefer F, Tibbles LA, Anafi M, Janssen A, Zanke BW, Lassam N, Pawson T, Woodgett JR, Iscove NN (1996) HPK1, a hematopoietic protein kinase activating the SAPK/JNK pathway. EMBO J 15: 7013-7025
23. Kirchhoff S, Muller WW, Li-Weber M, Krammer PH (2000) Up-regulation of c-FLIPshort and reduction of activation-induced cell death in CD28-costimulated human T cells. Eur J Immunol 30: 2765-2774
24. Krueger A, Fas SC, Baumann S, Krammer PH (2003) The role of CD95 in the regulation of peripheral T-cell apoptosis. Immunol Rev 193: 58-69
25. Le Bras S, Foucault I, Foussat A, Brignone C, Acuto O, Deckert M (2004) Recruitment of the actin-binding protein HIP-55 to the immunological synapse regulates T cell receptor signaling and endocytosis. J Biol Chem 279: 15550-15560
26. Lee K, D'Acquisto F, Hayden M, Shim J, Ghosh S (2005) PDK1 nucleates T cell receptor-induced signaling complex for NF-κB activation. Science 308: 114-118
27. Lin X, O'Mahony A, Mu Y, Geleziunas R, Greene WC (2000) Protein kinase C-θ participates in NF-κB activation induced by CD3-CD28 costimulation through selective activation of IκB kinase beta. Mol Cell Biol 20: 2933-2940
28. Ling L, Cao Z, Goeddel DV (1998) NF-κB-inducing kinase activates IKK-α by phosphorylation of Ser-176. Proc Natl Acad Sci USA 95: 3792-3797
29. Liou J, Kiefer F, Dang A, Hashimoto A, Cobb MH, Kurosaki T, Weiss A (2000) HPK1 is activated by lymphocyte antigen receptors and negatively regulates AP-1. Immunity 12: 399-408
30. Lissy NA, Davis PK, Irwin M, Kaelin WG, Dowdy SF (2000) A common E2F-1 and p73 pathway mediates cell death induced by TCR activation. Nature 407: 642-645
31. Liu SK, Smith CA, Arnold R, Kiefer F, McGlade CJ (2000) The adaptor protein Gads (Grb2-related adaptor downstream of Shc) is implicated in coupling hemopoietic progenitor kinase-1 to the activated TCR. J Immunol 165: 1417-1426
32. Li-Weber M, Krammer PH (2003) Function and regulation of the CD95 (APO-1/Fas) ligand in the immune system. Semin Immunol 15: 145-157
33. May MJ, Larsen SE, Shim JH, Madge LA, Ghosh S (2004) A novel ubiquitin-like domain in IκB kinaseβ is required for functional activity of the kinase. J Biol Chem 279: 45528-45539
34. Misra RS, Jelley-Gibbs DM, Russell JQ, Huston G, Swain SL, Budd RC (2005) Effector CD4(+) T cells generate intermediate caspase activity and cleavage of caspase-8 substrates. J Immunol 174: 3999-4009
35. Nemoto S, DiDonato JA, Lin AN (1998) Coordinate regulation of IκB kinases by mitogen-activated protein kinase kinase kinase 1 and NF-κB-inducing kinase. Mol Cell Biol 18: 7336-7343
36. Noel PJ, Boise LH, Green JM, Thompson CB (1996) CD28 costimulation prevents cell death during primary T cell activation. J Immunol 157: 636-642
37. Peter ME, Kischkel FC, Scheuerpflug CG, Medema JP, Debatin KM, Krammer PH (1997) Resistance of cultured peripheral T cells towards activation-induced cell death involves a lack of recruitment of FLICE (MACH/caspase 8) to the CD95 death-inducing signaling complex. Eur J Immunol 27: 1207-1212
38. Peter ME, Krammer PH (2003) The CD95(APO-1/Fas) DISC and beyond. Cell Death Differ 10: 26-35
39. Pham CG, Bubici C, Zazzeroni F, Papa S, Jones J, Alvarez K, Jayawardena S, De Smaele E, Cong R, Beaumont C, Torti FM, Torti SV, Franzoso G (2004) Ferritin heavy chain upregulation by NF-κB inhibits TNF alpha-induced apoptosis by suppressing reactive oxygen species. Cell 119: 529-542
40. Quirling M, Page S, Jilg N, Plenagl K, Peus D, Grubmuller C, Weingartner M, Fischer C, Neumeier D, Brand K (2004) Detection of IKKβ-IKKγ subcomplexes in monocytic cells and characterization of associated signaling. J Biol Chem 279: 37452-37460
41. Ruefli-Brasse AA, French DM, Dixit VM (2003) Regulation of NF-κB-dependent lymphocyte activation and development by paracaspase. Science 302: 1581-1584
42. Ruland J, Duncan GS, Elia A, Barrantes ID, Nguyen L, Plyte S, Millar DG, Bouchard D, Wakeham A, Ohashi PS, Mak TW (2001) Bcl10 is a positive regulator of antigen receptor-induced activation of NF-κB and neural tube closure. Cell 104: 33-42
43. Ruland J, Mak TW (2003) From antigen to activation: specific signal transduction pathways linking antigen receptors to NF-κB. Semin Immunol 15: 177-183
44. Scharschmidt E, Wegener E, Heissmeyer V, Rao A, Krappmann D (2004) Degradation of Bcl10 induced by T-cell activation negatively regulates NF-κB signaling. Mol Cell Biol 24: 3860-3873
45. Schmitz ML, Bacher S, Dienz O (2003) NF-κB activation pathways induced by T cell costimulation. FASEB J 17: 2187-2193
46. Schulze-Luehrmann J, Santner-Nanan B, Jha MK, Schimpl A, Avots A, Serfling E (2002) Hematopoietic progenitor kinase 1 supports apoptosis of T lymphocytes. Blood 100: 954-960
47. Shishodia S, Aggarwal BB (2004) Guggulsterone inhibits NF-κB and IκBα kinase activation, suppresses expression of anti-apoptotic gene products, and enhances apoptosis. J Biol Chem 279: 47148-47158
48. Su H, Bidere N, Zheng LX, Cubre A, Sakai K, Dale J, Salmena L, Hakem R, Straus S, Lenardo M (2005) Requirement for caspase-8 in NF-κB activation by antigen receptor. Science 307: 1465-1468
49. Sun LJ, Deng L, Ea CK, Xia ZP, Chen ZJJ (2004) The TRAF6 ubiquitin ligase and TAK1 kinase mediate IKK activation by BCL10 and MALT1 in T lymphocytes. Mol Cell 14: 289-301
50. Tang ED, Inohara N, Wang CY, Nunez G, Guan KL (2003) Roles for homotypic interactions and transautophosphorylation in IκB kinase (IKKβ) activation. J Biol Chem 278: 38566-38570
51. Tegethoff S, Behlke J, Scheidereit C (2003) Tetrameric oligomerization of IκB kinase gamma (IKKγ) is obligatory for IKK complex activity and NF-κB activation. Mol Cell Biol 23: 2029-2041
52. Tsuji S, Okamoto M, Yamada K, Okamoto N, Goitsuka R, Arnold R, Kiefer F, Kitamura D (2001) B cell adaptor containing Src homology 2 domain (BASH) links B cell receptor signaling to the activation of hematopoietic progenitor kinase 1. J Exp Med 194: 529-539
53. Wan YSY, DeGregori J (2003) The survival of antigen-stimulated T cells requires NF-κB-mediated inhibition of p73 expression. Immunity 18: 331-342
54. Wang DH, Matsumoto R, You Y, Che TJ, Lin XY, Gaffen SL, Lin X (2004) CD3/CD28 costimulation-induced NF-κB activation is mediated by recruitment of protein kinase C-θ, Bcl10, and IκB kinase beta to the immunological synapse through CARMA1. Mol Cell Biol 24: 164-171
55. Xiao GT, Sun SC (2000) Negative regulation of the nuclear factor κB-inducing kinase by a cis-acting domain. J Biol Chem 275: 21081-21085
56. Zheng L, Fischer G, Miller RE, Peschon J, Lynch DH, Lenardo MJ (1995) Induction of apoptosis in mature T cells by tumour necrosis factor. Nature 377: 348-351
57. Zhou HL, Wertz I, O'Rourke K, Ultsch M, Seshagiri S, Eby M, Xiao W, Dixit VM (2004) Bcl10 activates the NF-κB pathway through ubiquitination of NEMO. Nature 427: 167-171