Comprehending the complex connection between PKCβ, TAK1, and IKK in BCR signaling

Immunological Reviews

Volumn 232, Issue 1, 2009, Pages 300-318

  Shinohara, Hisaaki ^a   Kurosaki, Tomohiro ^a,b  

^a RIKEN Center for Integrative Medical Sciences   (Japan)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

Adapter; BCR signal; Fine tuning; IKK; PKC ; TAK1

Indexed keywords

B LYMPHOCYTE RECEPTOR; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; I KAPPA B KINASE GAMMA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 17; INTERLEUKIN 18; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BCL 10; PROTEIN KINASE C BETA; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANTIGEN SPECIFICITY; B CELL LYMPHOMA; CELL DIFFERENTIATION; CELL METABOLISM; CELL PROLIFERATION; CELL STIMULATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; GENETIC TRANSCRIPTION; HUMAN; IMMUNE DEFICIENCY; IMMUNOCOMPETENT CELL; LARGE CELL LYMPHOMA; MAST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; REVIEW; T LYMPHOCYTE; UBIQUITINATION; UPREGULATION;

ANIMALS; B-LYMPHOCYTES; HUMANS; I-KAPPA B KINASE; MAP KINASE KINASE KINASES; NF-KAPPA B; PROTEIN KINASE C; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION;

EID: 70350370720     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2009.00836.x     Document Type: Review

References (262)

1. Goodnow CC. Multistep pathogenesis of autoimmune disease. Cell 2007 130 : 25 35.
2. Vallabhapurapu S, Karin M. Regulation and function of NF-kappaB transcription factors in the immune system. Annu Rev Immunol 2009 27 : 693 733.
3. Hayden MS, Ghosh S. Shared principles in NF-kappaB signaling. Cell 2008 132 : 344 362.
4. Jun JE, Goodnow CC. Scaffolding of antigen receptors for immunogenic versus tolerogenic signaling. Nat Immunol 2003 4 : 1057 1064.
5. Marshak-Rothstein A, Rifkin IR. Immunologically active autoantigens: the role of toll-like receptors in the development of chronic inflammatory disease. Annu Rev Immunol 2007 25 : 419 441.
6. Kovanen PE, Leonard WJ. Cytokines and immunodeficiency diseases: critical roles of the gamma(c)-dependent cytokines interleukins 2, 4, 7, 9, 15, and 21, and their signaling pathways. Immunol Rev 2004 202 : 67 83.
7. Foy TM, Aruffo A, Bajorath J, Buhlmann JE, Noelle RJ. Immune regulation by CD40 and its ligand GP39. Annu Rev Immunol 1996 14 : 591 617.
8. Hacker H, Karin M. Regulation and function of IKK and IKK-related kinases. Sci STKE 2006 2006 : re13.
9. Kurosaki T, Shinohara H, Baba Y. B cell signaling and fate decision. Annu Rev Immunol 2009 doi:.
10. Shinohara H, et al. PKC beta regulates BCR-mediated IKK activation by facilitating the interaction between TAK1 and CARMA1. J Exp Med 2005 202 : 1423 1431.
11. Harwood NE, Batista FD. New insights into the early molecular events underlying B cell activation. Immunity 2008 28 : 609 619.
12. Spitaler M, Cantrell DA. Protein kinase C and beyond. Nat Immunol 2004 5 : 785 790.
13. Leitges M, et al. Immunodeficiency in protein kinase cbeta-deficient mice. Science 1996 273 : 788 791.
14. Saijo K, Mecklenbrauker I, Santana A, Leitger M, Schmedt C, Tarakhovsky A. Protein kinase C beta controls nuclear factor kappaB activation in B cells through selective regulation of the IkappaB kinase alpha. J Exp Med 2002 195 : 1647 1652.
15. Su TT, et al. PKC-beta controls I kappa B kinase lipid raft recruitment and activation in response to BCR signaling. Nat Immunol 2002 3 : 780 786.
16. Hara H, Saito T. CARD9 versus CARMA1 in innate and adaptive immunity. Trends Immunol 2009 30 : 234 242.
17. Thome M. CARMA1, BCL-10 and MALT1 in lymphocyte development and activation. Nat Rev Immunol 2004 4 : 348 359.
18. Rueda D, Thome M. Phosphorylation of CARMA1: the link(er) to NF-kappaB activation. Immunity 2005 23 : 551 553.
19. Sommer K, et al. Phosphorylation of the CARMA1 linker controls NF-kappaB activation. Immunity 2005 23 : 561 574.
20. McCully RR, Pomerantz JL. The protein kinase C-responsive inhibitory domain of CARD11 functions in NF-kappaB activation to regulate the association of multiple signaling cofactors that differentially depend on Bcl10 and MALT1 for association. Mol Cell Biol 2008 28 : 5668 5686.
21. Shinohara H, Maeda S, Watarai H, Kurosaki T. IkappaB kinase beta-induced phosphorylation of CARMA1 contributes to CARMA1 Bcl10 MALT1 complex formation in B cells. J Exp Med 2007 204 : 3285 3293.
22. Ngo VN, et al. A loss-of-function RNA interference screen for molecular targets in cancer. Nature 2006 441 : 106 110.
23. Lenz G, et al. Oncogenic CARD11 mutations in human diffuse large B cell lymphoma. Science 2008 319 : 1676 1679.
24. Compagno M, et al. Mutations of multiple genes cause deregulation of NF-kappaB in diffuse large B-cell lymphoma. Nature 2009 459 : 717 721.
25. Jun JE, et al. Identifying the MAGUK protein Carma-1 as a central regulator of humoral immune responses and atopy by genome-wide mouse mutagenesis. Immunity 2003 18 : 751 762.
26. Bidere N, et al. Casein kinase 1alpha governs antigen-receptor-induced NF-kappaB activation and human lymphoma cell survival. Nature 2009 458 : 92 96.
27. Seet BT, Dikic I, Zhou MM, Pawson T. Reading protein modifications with interaction domains. Nat Rev 2006 7 : 473 483.
28. Uren AG, et al. Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol Cell 2000 6 : 961 967.
29. Lucas PC, et al. Bcl10 and MALT1, independent targets of chromosomal translocation in malt lymphoma, cooperate in a novel NF-kappa B signaling pathway. J Biol Chem 2001 276 : 19012 19019.
30. Rebeaud F, et al. The proteolytic activity of the paracaspase MALT1 is key in T cell activation. Nat Immunol 2008 9 : 272 281.
31. Coornaert B, et al. T cell antigen receptor stimulation induces MALT1 paracaspase-mediated cleavage of the NF-kappaB inhibitor A20. Nat Immunol 2008 9 : 263 271.
32. Ruland J, Duncan GS, Wakeham A, Mak TW. Differential requirement for Malt1 in T and B cell antigen receptor signaling. Immunity 2003 19 : 749 758.
33. Ruefli-Brasse AA, French DM, Dixit VM. Regulation of NF-kappaB-dependent lymphocyte activation and development by paracaspase. Science 2003 302 : 1581 1584.
34. Thome M. Multifunctional roles for MALT1 in T-cell activation. Nat Rev Immunol 2008 8 : 495 500.
35. Ferch U, et al. MALT1 directs B cell receptor-induced canonical nuclear factor-kappaB signaling selectively to the c-Rel subunit. Nat Immunol 2007 8 : 984 991.
36. Castro I, et al. B cell receptor-mediated sustained c-Rel activation facilitates late transitional B cell survival through control of B cell activating factor receptor and NF-kappaB2. J Immunol 2009 182 : 7729 7737.
37. Dierlamm J, et al. The apoptosis inhibitor gene API2 and a novel 18q gene, MLT, are recurrently rearranged in the t(11;18)(q21;q21) associated with mucosa-associated lymphoid tissue lymphomas. Blood 1999 93 : 3601 3609.
38. Zhang Q, et al. Inactivating mutations and overexpression of BCL10, a caspase recruitment domain-containing gene, in MALT lymphoma with t(1;14)(p22;q32). Nat Genet 1999 22 : 63 68.
39. Willis TG, et al. Bcl10 is involved in t(1;14)(p22;q32) of MALT B cell lymphoma and mutated in multiple tumor types. Cell 1999 96 : 35 45.
40. Akagi T, et al. A novel gene, MALT1 at 18q21, is involved in t(11;18) (q21;q21) found in low-grade B-cell lymphoma of mucosa-associated lymphoid tissue. Oncogene 1999 18 : 5785 5794.
41. Morgan JA, et al. Breakpoints of the t(11;18)(q21;q21) in mucosa-associated lymphoid tissue (MALT) lymphoma lie within or near the previously undescribed gene MALT1 in chromosome 18. Cancer Res 1999 59 : 6205 6213.
42. Streubel B, et al. T(14;18)(q32;q21) involving IGH and MALT1 is a frequent chromosomal aberration in MALT lymphoma. Blood 2003 101 : 2335 2339.
43. Wang C, Deng L, Hong M, Akkaraju GR, Inoue J, Chen ZJ. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 2001 412 : 346 351.
44. Yamaguchi K, et al. Identification of a member of the MAPKKK family as a potential mediator of TGF-beta signal transduction. Science 1995 270 : 2008 2011.
45. Sorrentino A, et al. The type I TGF-beta receptor engages TRAF6 to activate TAK1 in a receptor kinase-independent manner. Nat Cell Biol 2008 10 : 1199 1207.
46. Yamashita M, Fatyol K, Jin C, Wang X, Liu Z, Zhang YE. TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-beta. Mol Cell 2008 31 : 918 924.
47. Ishitani T, et al. The TAK1-NLK-MAPK-related pathway antagonizes signalling between beta-catenin and transcription factor TCF. Nature 1999 399 : 798 802.
48. Smit L, Baas A, Kuipers J, Korswagen H, van de Wetering M, Clevers H. Wnt activates the Tak1/Nemo-like kinase pathway. J Biol Chem 2004 279 : 17232 17240.
49. Meneghini MD, et al. MAP kinase and Wnt pathways converge to downregulate an HMG-domain repressor in Caenorhabditis elegans. Nature 1999 399 : 793 797.
50. Ishitani T, et al. The TAK1-NLK mitogen-activated protein kinase cascade functions in the Wnt-5a/Ca(2+) pathway to antagonize Wnt/beta-catenin signaling. Mol Cell Biol 2003 23 : 131 139.
51. Ishitani T, Ninomiya-Tsuji J, Matsumoto K. Regulation of lymphoid enhancer factor 1/T-cell factor by mitogen-activated protein kinase-related Nemo-like kinase-dependent phosphorylation in Wnt/beta-catenin signaling. Mol Cell Biol 2003 23 : 1379 1389.
52. Kanei-Ishii C, et al. Wnt-1 signal induces phosphorylation and degradation of c-Myb protein via TAK1, HIPK2, and NLK. Genes Dev 2004 18 : 816 829.
53. Takada I, Suzawa M, Matsumoto K, Kato S. Suppression of PPAR transactivation switches cell fate of bone marrow stem cells from adipocytes into osteoblasts. Ann NY Acad Sci 2007 1116 : 182 195.
54. Staal FJ, Luis TC, Tiemessen MM. WNT signalling in the immune system: WNT is spreading its wings. Nat Rev Immunol 2008 8 : 581 593.
55. Shibuya H, et al. Role of TAK1 and TAB1 in BMP signaling in early Xenopus development. EMBO J 1998 17 : 1019 1028.
56. Yamaguchi K, et al. XIAP, a cellular member of the inhibitor of apoptosis protein family, links the receptors to TAB1-TAK1 in the BMP signaling pathway. EMBO J 1999 18 : 179 187.
57. Kimura N, Matsuo R, Shibuya H, Nakashima K, Taga T. BMP2-induced apoptosis is mediated by activation of the TAK1-p38 kinase pathway that is negatively regulated by Smad6. J Biol Chem 2000 275 : 17647 17652.
58. Yanagisawa M, et al. Inhibition of BMP2-induced, TAK1 kinase-mediated neurite outgrowth by Smad6 and Smad7. Genes Cells 2001 6 : 1091 1099.
59. Ogihara T, et al. p38 MAPK is involved in activin A- and hepatocyte growth factor-mediated expression of pro-endocrine gene neurogenin 3 in AR42J-B13 cells. J Biol Chem 2003 278 : 21693 21700.
60. Kinugawa K, Jeong MY, Bristow MR, Long CS. Thyroid hormone induces cardiac myocyte hypertrophy in a thyroid hormone receptor alpha1-specific manner that requires TAK1 and p38 mitogen-activated protein kinase. Mol Endocrinol 2005 19 : 1618 1628.
61. Shi-Wen X, et al. Constitutive ALK5-independent c-Jun N-terminal kinase activation contributes to endothelin-1 overexpression in pulmonary fibrosis: evidence of an autocrine endothelin loop operating through the endothelin A and B receptors. Mol Cell Biol 2006 26 : 5518 5527.
62. Xu Z, Lai KO, Zhou HM, Lin SC, Ip NY. Ephrin-B1 reverse signaling activates JNK through a novel mechanism that is independent of tyrosine phosphorylation. J Biol Chem 2003 278 : 24767 24775.
63. Cheung PC, Campbell DG, Nebreda AR, Cohen P. Feedback control of the protein kinase TAK1 by SAPK2a/p38alpha. EMBO J 2003 22 : 5793 5805.
64. Cheung PC, Nebreda AR, Cohen P. TAB3, a new binding partner of the protein kinase TAK1. Biochem J 2004 378 : 27 34.
65. Huangfu WC, Omori E, Akira S, Matsumoto K, Ninomiya-Tsuji J. Osmotic stress activates the TAK1-JNK pathway while blocking TAK1-mediated NF-kappaB activation: TAO2 regulates TAK1 pathways. J Biol Chem 2006 281 : 28802 28810.
66. Singhirunnusorn P, Ueno Y, Matsuo M, Suzuki S, Saiki I, Sakurai H. Transient suppression of ligand-mediated activation of epidermal growth factor receptor by tumor necrosis factor-alpha through the TAK1-p38 signaling pathway. J Biol Chem 2007 282 : 12698 12706.
67. Inagaki M, et al. TAK1-binding protein 1, TAB1, mediates osmotic stress-induced TAK1 activation but is dispensable for TAK1-mediated cytokine signaling. J Biol Chem 2008 283 : 33080 33086.
68. Zetoune FS, et al. A20 inhibits NF-kappa B activation downstream of multiple Map3 kinases and interacts with the I kappa B signalosome. Cytokine 2001 15 : 282 298.
69. Gohda J, et al. HTLV-1 Tax-induced NFkappaB activation is independent of Lys-63-linked-type polyubiquitination. Biochem Biophys Res Commun 2007 357 : 225 230.
70. Suzuki S, et al. Constitutive activation of TAK1 by HTLV-1 tax-dependent overexpression of TAB2 induces activation of JNK-ATF2 but not IKK-NF-kappaB. J Biol Chem 2007 282 : 25177 25181.
71. Wu X, Sun SC. Retroviral oncoprotein Tax deregulates NF-kappaB by activating Tak1 and mediating the physical association of TAK1-IKK. EMBO Rep 2007 8 : 510 515.
72. Yu Q, et al. HTLV-1 Tax-mediated TAK1 activation involves TAB2 adapter protein. Biochem Biophys Res Commun 2008 365 : 189 194.
73. Wan J, et al. Elucidation of the c-Jun N-terminal kinase pathway mediated by Epstein-Barr virus-encoded latent membrane protein 1. Mol Cell Biol 2004 24 : 192 199.
74. Uemura N, et al. TAK1 is a component of the Epstein-Barr virus LMP1 complex and is essential for activation of JNK but not of NF-kappaB. J Biol Chem 2006 281 : 7863 7872.
75. Wan J, et al. BS69, a specific adaptor in the latent membrane protein 1-mediated c-Jun N-terminal kinase pathway. Mol Cell Biol 2006 26 : 448 456.
76. Wu L, Nakano H, Wu Z. The C-terminal activating region 2 of the Epstein-Barr virus-encoded latent membrane protein 1 activates NF-kappaB through TRAF6 and TAK1. J Biol Chem 2006 281 : 2162 2169.
77. Ninomiya-Tsuji J, Kishimoto K, Hiyama A, Inoue J, Cao Z, Matsumoto K. The kinase TAK1 can activate the NIK-I kappaB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 1999 398 : 252 256.
78. Sakurai H, Miyoshi H, Toriumi W, Sugita T. Functional interactions of transforming growth factor beta-activated kinase 1 with IkappaB kinases to stimulate NF-kappaB activation. J Biol Chem 1999 274 : 10641 10648.
79. Chen ZJ, Bhoj V, Seth RB. Ubiquitin, TAK1 and IKK: is there a connection? Cell Death Differ 2006 13 : 687 692.
80. Adhikari A, Xu M, Chen ZJ. Ubiquitin-mediated activation of TAK1 and IKK. Oncogene 2007 26 : 3214 3226.
81. Qian Y, Commane M, Ninomiya-Tsuji J, Matsumoto K, Li X. IRAK-mediated translocation of TRAF6 and TAB2 in the interleukin-1-induced activation of NFkappa B. J Biol Chem 2001 276 : 41661 41667.
82. Takaesu G, Ninomiya-Tsuji J, Kishida S, Li X, Stark GR, Matsumoto K. Interleukin-1 (IL-1) receptor-associated kinase leads to activation of TAK1 by inducing TAB2 translocation in the IL-1 signaling pathway. Mol Cell Biol 2001 21 : 2475 2484.
83. Jiang Z, Ninomiya-Tsuji J, Qian Y, Matsumoto K, Li X. Interleukin-1 (IL-1) receptor-associated kinase-dependent IL-1-induced signaling complexes phosphorylate TAK1 and TAB2 at the plasma membrane and activate TAK1 in the cytosol. Mol Cell Biol 2002 22 : 7158 7167.
84. Kojima H, et al. STAT3 regulates Nemo-like kinase by mediating its interaction with IL-6-stimulated TGFbeta-activated kinase 1 for STAT3 Ser-727 phosphorylation. Proc Natl Acad Sci USA 2005 102 : 4524 4529.
85. Huang F, Kao CY, Wachi S, Thai P, Ryu J, Wu R. Requirement for both JAK-mediated PI3K signaling and ACT1/TRAF6/TAK1-dependent NF-kappaB activation by IL-17A in enhancing cytokine expression in human airway epithelial cells. J Immunol 2007 179 : 6504 6513.
86. Qian Y, et al. The adaptor Act1 is required for interleukin 17-dependent signaling associated with autoimmune and inflammatory disease. Nat Immunol 2007 8 : 247 256.
87. Yang X, et al. Sef interacts with TAK1 and mediates JNK activation and apoptosis. J Biol Chem 2004 279 : 38099 38102.
88. Wald D, Commane M, Stark GR, Li X. IRAK and TAK1 are required for IL-18-mediated signaling. Eur J Immunol 2001 31 : 3747 3754.
89. Takaesu G, Surabhi RM, Park KJ, Ninomiya-Tsuji J, Matsumoto K, Gaynor RB. TAK1 is critical for IkappaB kinase-mediated activation of the NF-kappaB pathway. J Mol Biol 2003 326 : 105 115.
90. Ea CK, Deng L, Xia ZP, Pineda G, Chen ZJ. Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol Cell 2006 22 : 245 257.
91. Li S, Wang L, Dorf ME. PKC phosphorylation of TRAF2 mediates IKKalpha/beta recruitment and K63-linked polyubiquitination. Mol Cell 2009 33 : 30 42.
92. Herrero-Martin G, et al. TAK1 activates AMPK-dependent cytoprotective autophagy in TRAIL-treated epithelial cells. EMBO J 2009 28 : 677 685.
93. Lee SW, Han SI, Kim HH, Lee ZH. TAK1-dependent activation of AP-1 and c-Jun N-terminal kinase by receptor activator of NF-kappaB. J Biochem Mol Biol 2002 35 : 371 376.
94. Mizukami J, et al. Receptor activator of NF-kappaB ligand (RANKL) activates TAK1 mitogen-activated protein kinase kinase kinase through a signaling complex containing RANK, TAB2, and TRAF6. Mol Cell Biol 2002 22 : 992 1000.
95. Kobayashi Y, Mizoguchi T, Take I, Kurihara S, Udagawa N, Takahashi N. Prostaglandin E2 enhances osteoclastic differentiation of precursor cells through protein kinase A-dependent phosphorylation of TAK1. J Biol Chem 2005 280 : 11395 11403.
96. Huang H, et al. Osteoclast differentiation requires TAK1 and MKK6 for NFATc1 induction and NF-kappaB transactivation by RANKL. Cell Death Differ 2006 13 : 1879 1891.
97. Besse A, et al. TAK1-dependent signaling requires functional interaction with TAB2/TAB3. J Biol Chem 2007 282 : 3918 3928.
98. Walsh MC, Kim GK, Maurizio PL, Molnar EE, Choi Y. TRAF6 autoubiquitination-independent activation of the NFkappaB and MAPK pathways in response to IL-1 and RANKL. PLoS ONE 2008 3 : e4064.
99. Hoffmann A, et al. Transforming growth factor-beta-activated kinase-1 (TAK1), a MAP3K, interacts with Smad proteins and interferes with osteogenesis in murine mesenchymal progenitors. J Biol Chem 2005 280 : 27271 27283.
100. Kumar M, Makonchuk DY, Li H, Mittal A, Kumar A. TNF-like weak inducer of apoptosis (TWEAK) activates proinflammatory signaling pathways and gene expression through the activation of TGF-beta-activated kinase 1. J Immunol 2009 182 : 2439 2448.
101. Sato S, et al. Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat Immunol 2005 6 : 1087 1095.
102. Moschonas A, Kouraki M, Knox PG, Thymiakou E, Kardassis D, Eliopoulos AG. CD40 induces antigen transporter and immunoproteasome gene expression in carcinomas via the coordinated action of NF-kappaB and of NF-kappaB-mediated de novo synthesis of IRF-1. Mol Cell Biol 2008 28 : 6208 6222.
103. Chan H, Reed JC. TRAF-dependent association of protein kinase Tpl2/COT1 (MAP3K8) with CD40. Biochem Biophys Res Commun 2005 328 : 198 205.
104. Su WB, Chang YH, Lin WW, Hsieh SL. Differential regulation of interleukin-8 gene transcription by death receptor 3 (DR3) and type I TNF receptor (TNFRI). Exp Cell Res 2006 312 : 266 277.
105. Shuto T, et al. Activation of NF-kappa B by nontypeable Hemophilus influenzae is mediated by toll-like receptor 2-TAK1-dependent NIK-IKK alpha /beta-I kappa B alpha and MKK3/6-p38 MAP kinase signaling pathways in epithelial cells. Proc Natl Acad Sci USA 2001 98 : 8774 8779.
106. Jono H, et al. Transforming growth factor-beta-Smad signaling pathway cooperates with NF-kappa B to mediate nontypeable Haemophilus influenzae-induced MUC2 mucin transcription. J Biol Chem 2002 277 : 45547 45557.
107. Jiang Z, Mak TW, Sen G, Li X. Toll-like receptor 3-mediated activation of NF-kappaB and IRF3 diverges at Toll-IL-1 receptor domain-containing adapter inducing IFN-beta. Proc Natl Acad Sci USA 2004 101 : 3533 3538.
108. Liu X, Yao M, Li N, Wang C, Zheng Y, Cao X. CaMKII promotes TLR-triggered proinflammatory cytokine and type I interferon production by directly binding and activating TAK1 and IRF3 in macrophages. Blood 2008 112 : 4961 4970.
109. Zhang B, et al. The TAK1-JNK cascade is required for IRF3 function in the innate immune response. Cell Res 2009 19 : 412 428.
110. Dong W, et al. The IRAK-1-BCL10-MALT1-TRAF6-TAK1 cascade mediates signaling to NF-[kappa]B from Toll-like receptor 4. J Biol Chem 2006 281 : 26029 26040.
111. Fraczek J, et al. The kinase activity of IL-1 receptor-associated kinase 4 is required for interleukin-1 receptor/toll-like receptor-induced TAK1-dependent NFkappaB activation. J Biol Chem 2008 283 : 31697 31705.
112. Qin J, et al. TLR8-mediated NF-kappaB and JNK activation are TAK1-independent and MEKK3-dependent. J Biol Chem 2006 281 : 21013 21021.
113. Windheim M, Lang C, Peggie M, Plater LA, Cohen P. The kinase activity of IL-1 receptor-associated kinase 4 is required for interleukin-1 receptor/toll-like receptor-induced TAK1-dependent NFkappaB activation. Biochem J 2007 404 : 179 190.
114. Abbott DW, Yang Y, Hutti JE, Madhavarapu S, Kelliher MA, Cantley LC. Coordinated regulation of Toll-like receptor and NOD2 signaling by K63-linked polyubiquitin chains. Mol Cell Biol 2007 27 : 6012 6025.
115. Chen CM, Gong Y, Zhang M, Chen JJ. Reciprocal cross-talk between Nod2 and TAK1 signaling pathways. J Biol Chem 2004 279 : 25876 25882.
116. da Silva Correia J, Miranda Y, Leonard N, Hsu J, Ulevitch RJ. Regulation of Nod1-mediated signaling pathways. Cell Death Differ 2007 14 : 830 839.
117. Hasegawa M, et al. A critical role of RICK/RIP2 polyubiquitination in Nod-induced NF-kappaB activation. EMBO J 2008 27 : 373 383.
118. Yang Y, Yin C, Pandey A, Abbott D, Sassetti C, Kelliher MA. NOD2 pathway activation by MDP or Mycobacterium tuberculosis infection involves the stable polyubiquitination of Rip2. J Biol Chem 2007 282 : 36223 36229.
119. Kim JY, Omori E, Matsumoto K, Nunez G, Ninomiya-Tsuji J. TAK1 is a central mediator of NOD2 signaling in epidermal cells. J Biol Chem 2008 283 : 137 144.
120. Mikkelsen SS, et al. RIG-I-mediated activation of p38 MAPK is essential for viral induction of interferon and activation of dendritic cells: dependence on TRAF2 and TAK1. J Biol Chem 2009 284 : 10774 10782.
121. Momcilovic M, Hong SP, Carlson M. Mammalian TAK1 activates Snf1 protein kinase in yeast and phosphorylates AMP-activated protein kinase in vitro. J Biol Chem 2006 281 : 25336 25343.
122. Xie M, et al. A pivotal role for endogenous TGF-beta-activated kinase-1 in the LKB1/AMP-activated protein kinase energy-sensor pathway. Proc Natl Acad Sci USA 2006 103 : 17378 17383.
123. Nakamura K, et al. Wnt signaling drives WRM-1/beta-catenin asymmetries in early C. elegans embryos. Genes Dev 2005 19 : 1749 1754.
124. Monzen K, et al. Bone morphogenetic proteins induce cardiomyocyte differentiation through the mitogen-activated protein kinase kinase kinase TAK1 and cardiac transcription factors Csx/Nkx-2.5 and GATA-4. Mol Cell Biol 1999 19 : 7096 7105.
125. Rottinger E, Croce J, Lhomond G, Besnardeau L, Gache C, Lepage T. Nemo-like kinase (NLK) acts downstream of Notch/Delta signalling to downregulate TCF during mesoderm induction in the sea urchin embryo. Development 2006 133 : 4341 4353.
126. Kitisin K, et al. Tgf-Beta signaling in development. Sci STKE 2007 2007 : cm1.
127. Jackson-Bernitsas DG, et al. Evidence that TNF-TNFR1-TRADD-TRAF2-RIP- TAK1-IKK pathway mediates constitutive NF-kappaB activation and proliferation in human head and neck squamous cell carcinoma. Oncogene 2007 26 : 1385 1397.
128. Nony PA, Kennett SB, Glasgow WC, Olden K, Roberts JD. 15S-Lipoxygenase-2 mediates arachidonic acid-stimulated adhesion of human breast carcinoma cells through the activation of TAK1, MKK6, and p38 MAPK. J Biol Chem 2005 280 : 31413 31419.
129. Lu T, Tian L, Han Y, Vogelbaum M, Stark GR. Dose-dependent cross-talk between the transforming growth factor-beta and interleukin-1 signaling pathways. Proc Natl Acad Sci USA 2007 104 : 4365 4370.
130. Morrison BH, et al. Effect of inositol hexakisphosphate kinase 2 on transforming growth factor beta-activated kinase 1 and NF-kappaB activation. J Biol Chem 2007 282 : 15349 15356.
131. Fujiki T, et al. TAK1 represses transcription of the human telomerase reverse transcriptase gene. Oncogene 2007 26 : 5258 5266.
132. Choo MK, Sakurai H, Koizumi K, Saiki I. TAK1-mediated stress signaling pathways are essential for TNF-alpha-promoted pulmonary metastasis of murine colon cancer cells. Int J Cancer 2006 118 : 2758 2764.
133. Kajino T, Omori E, Ishii S, Matsumoto K, Ninomiya-Tsuji J. TAK1 MAPK kinase kinase mediates transforming growth factor-beta signaling by targeting SnoN oncoprotein for degradation. J Biol Chem 2007 282 : 9475 9481.
134. Raychaudhuri S, et al. Common variants at CD40 and other loci confer risk of rheumatoid arthritis. Nat Genet 2008 40 : 1216 1223.
135. Hammaker DR, Boyle DL, Inoue T, Firestein GS. Regulation of the JNK pathway by TGF-beta activated kinase 1 in rheumatoid arthritis synoviocytes. Arthritis Res Ther 2007 9 : R57.
136. Gregersen PK, et al. REL, encoding a member of the NF-kappaB family of transcription factors, is a newly defined risk locus for rheumatoid arthritis. Nat Genet 2009 41 : 820 823.
137. Vidal S, Khush RS, Leulier F, Tzou P, Nakamura M, Lemaitre B. Mutations in the Drosophila dTAK1 gene reveal a conserved function for MAPKKKs in the control of rel/NF-kappaB-dependent innate immune responses. Genes Dev 2001 15 : 1900 1912.
138. Silverman N, et al. Immune activation of NF-kappaB and JNK requires Drosophila TAK1. J Biol Chem 2003 278 : 48928 48934.
139. Delaney JR, Mlodzik M. TGF-beta activated kinase-1: new insights into the diverse roles of TAK1 in development and immunity. Cell Cycle 2006 5 : 2852 2855.
140. Benus GF, et al. Inhibition of the transforming growth factor beta (TGFbeta) pathway by interleukin-1beta is mediated through TGFbeta-activated kinase 1 phosphorylation of SMAD3. Mol Biol Cell 2005 16 : 3501 3510.
141. Hayashi H, et al. The MAD-related protein Smad7 associates with the TGFbeta receptor and functions as an antagonist of TGFbeta signaling. Cell 1997 89 : 1165 1173.
142. Hong S, et al. Smad7 binds to the adaptors TAB2 and TAB3 to block recruitment of the kinase TAK1 to the adaptor TRAF2. Nat Immunol 2007 8 : 504 513.
143. Morioka S, Omori E, Kajino T, Kajino-Sakamoto R, Matsumoto K, Ninomiya-Tsuji J. TAK1 kinase determines TRAIL sensitivity by modulating reactive oxygen species and cIAP. Oncogene 2009 28 : 2257 2265.
144. Wang C, et al. Melittin, a major component of bee venom, sensitizes human hepatocellular carcinoma cells to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis by activating CaMKII-TAK1-JNK/p38 and inhibiting IkappaBalpha kinase-NFkappaB. J Biol Chem 2009 284 : 3804 3813.
145. Das J, et al. Digital signaling and hysteresis characterize ras activation in lymphoid cells. Cell 2009 136 : 337 351.
146. Kholodenko BN. Cell-signalling dynamics in time and space. Nat Rev 2006 7 : 165 176.
147. Shi L, et al. Heat shock protein 90 (Hsp90) regulates the stability of transforming growth factor beta-activated kinase 1 (TAK1) in interleukin-1beta-induced cell signaling. Mol Immunol 2009 46 : 541 550.
148. Ahmad R, et al. MUC1 oncoprotein activates the IkappaB kinase beta complex and constitutive NF-kappaB signalling. Nat Cell Biol 2007 9 : 1419 1427.
149. Blanco S, Sanz-Garcia M, Santos CR, Lazo PA. Modulation of interleukin-1 transcriptional response by the interaction between VRK2 and the JIP1 scaffold protein. PLoS ONE 2008 3 : e1660.
150. Kishimoto K, Matsumoto K, Ninomiya-Tsuji J. TAK1 mitogen-activated protein kinase kinase kinase is activated by autophosphorylation within its activation loop. J Biol Chem 2000 275 : 7359 7364.
151. Singhirunnusorn P, Suzuki S, Kawasaki N, Saiki I, Sakurai H. Critical roles of threonine 187 phosphorylation in cellular stress-induced rapid and transient activation of transforming growth factor-beta-activated kinase 1 (TAK1) in a signaling complex containing TAK1-binding protein TAB1 and TAB2. J Biol Chem 2005 280 : 7359 7368.
152. Yu Y, et al. Phosphorylation of Thr-178 and Thr-184 in the TAK1 T-loop is required for interleukin (IL)-1-mediated optimal NFkappaB and AP-1 activation as well as IL-6 gene expression. J Biol Chem 2008 283 : 24497 24505.
153. Shibuya H, et al. TAB1: an activator of the TAK1 MAPKKK in TGF-beta signal transduction. Science 1996 272 : 1179 1182.
154. Takaesu G, et al. TAB2, a novel adaptor protein, mediates activation of TAK1 MAPKKK by linking TAK1 to TRAF6 in the IL-1 signal transduction pathway. Mol Cell 2000 5 : 649 658.
155. Ishitani T, Takaesu G, Ninomiya-Tsuji J, Shibuya H, Gaynor RB, Matsumoto K. Role of the TAB2-related protein TAB3 in IL-1 and TNF signaling. EMBO J 2003 22 : 6277 6288.
156. Kanayama A, et al. TAB2 and TAB3 activate the NF-kappaB pathway through binding to polyubiquitin chains. Mol Cell 2004 15 : 535 548.
157. Brown K, Vial SC, Dedi N, Long JM, Dunster NJ, Cheetham GM. Structural basis for the interaction of TAK1 kinase with its activating protein TAB1. J Mol Biol 2005 354 : 1013 1020.
158. Ono K, et al. An evolutionarily conserved motif in the TAB1 C-terminal region is necessary for interaction with and activation of TAK1 MAPKKK. J Biol Chem 2001 276 : 24396 24400.
159. Conner SH, et al. TAK1-binding protein 1 is a pseudophosphatase. Biochem J 2006 399 : 427 434.
160. Ge B, et al. TAB1beta (transforming growth factor-beta-activated protein kinase 1-binding protein 1beta), a novel splicing variant of TAB1 that interacts with p38alpha but not TAK1. J Biol Chem 2003 278 : 2286 2293.
161. Hanada M, et al. Regulation of the TAK1 signaling pathway by protein phosphatase 2C. J Biol Chem 2001 276 : 5753 5759. (Pubitemid 37385728)
162. Li MG, et al. Regulation of the interleukin-1-induced signaling pathways by a novel member of the protein phosphatase 2C family (PP2Cepsilon). J Biol Chem 2003 278 : 12013 12021.
163. Kajino T, et al. Protein phosphatase 6 down-regulates TAK1 kinase activation in the IL-1 signaling pathway. J Biol Chem 2006 281 : 39891 39896.
164. Kim SI, Kwak JH, Wang L, Choi ME. Protein phosphatase 2A is a negative regulator of transforming growth factor-beta1-induced TAK1 activation in mesangial cells. J Biol Chem 2008 283 : 10753 10763.
165. Baril C, Sahmi M, Ashton-Beaucage D, Stronach B, Therrien M. The PP2C Alphabet is a negative regulator of stress-activated protein kinase signaling in Drosophila. Genetics 2009 181 : 567 579.
166. Lu M, et al. XIAP induces NF-kappaB activation via the BIR1/TAB1 interaction and BIR1 dimerization. Mol Cell 2007 26 : 689 702.
167. Komatsu Y, et al. Targeted disruption of the Tab1 gene causes embryonic lethality and defects in cardiovascular and lung morphogenesis. Mech Dev 2002 119 : 239 249.
168. Shim JH, et al. TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev 2005 19 : 2668 2681.
169. Ge B, et al. MAPKK-independent activation of p38alpha mediated by TAB1-dependent autophosphorylation of p38alpha. Science 2002 295 : 1291 1294.
170. Jin G, et al. Identification of a human NF-kappaB-activating protein, TAB3. Proc Natl Acad Sci USA 2004 101 : 2028 2033.
171. Jiang Z, Zamanian-Daryoush M, Nie H, Silva AM, Williams BR, Li X. Poly(I-C)-induced Toll-like receptor 3 (TLR3)-mediated activation of NFkappa B and MAP kinase is through an interleukin-1 receptor-associated kinase (IRAK)-independent pathway employing the signaling components TLR3-TRAF6-TAK1-TAB2-PKR. J Biol Chem 2003 278 : 16713 16719.
172. Morlon A, Munnich A, Smahi A. TAB2, TRAF6 and TAK1 are involved in NF-kappaB activation induced by the TNF-receptor, Edar and its adaptator Edaradd. Hum Mol Genet 2005 14 : 3751 3757.
173. Geuking P, Narasimamurthy R, Basler K. A genetic screen targeting the tumor necrosis factor/Eiger signaling pathway: identification of Drosophila TAB2 as a functionally conserved component. Genetics 2005 171 : 1683 1694.
174. Kleino A, et al. Inhibitor of apoptosis 2 and TAK1-binding protein are components of the Drosophila Imd pathway. EMBO J 2005 24 : 3423 3434.
175. Zhuang ZH, et al. Drosophila TAB2 is required for the immune activation of JNK and NF-kappaB. Cell Signal 2006 18 : 964 970.
176. Sanjo H, Takeda K, Tsujimura T, Ninomiya-Tsuji J, Matsumoto K, Akira S. TAB2 is essential for prevention of apoptosis in fetal liver but not for interleukin-1 signaling. Mol Cell Biol 2003 23 : 1231 1238.
177. Lee KY, D'Acquisto F, Hayden MS, Shim JH, Ghosh S. PDK1 nucleates T cell receptor-induced signaling complex for NF-kappaB activation. Science 2005 308 : 114 118.
178. Kishida S, Sanjo H, Akira S, Matsumoto K, Ninomiya-Tsuji J. TAK1-binding protein 2 facilitates ubiquitination of TRAF6 and assembly of TRAF6 with IKK in the IL-1 signaling pathway. Genes Cells 2005 10 : 447 454.
179. Liu Q, Busby JC, Molkentin JD. Interaction between TAK1-TAB1-TAB2 and RCAN1-calcineurin defines a signalling nodal control point. Nat Cell Biol 2009 11 : 154 161.
180. Prickett TD, et al. TAB4 stimulates TAK1-TAB1 phosphorylation and binds polyubiquitin to direct signaling to NF-kappaB. J Biol Chem 2008 283 : 19245 19254.
181. Ma Q, Zhou L, Shi H, Huo K. NUMBL interacts with TAB2 and inhibits TNFalpha and IL-1beta-induced NF-kappaB activation. Cell Signal 2008 20 : 1044 1051.
182. Shi M, et al. TRIM30 alpha negatively regulates TLR-mediated NF-kappa B activation by targeting TAB2 and TAB3 for degradation. Nat Immunol 2008 9 : 369 377.
183. Skaug B, Jiang X, Chen ZJ. The role of ubiquitin in NF-kappaB regulatory pathways. Annu Rev Biochem 2009 78 : 769 796.
184. Komander D, Reyes-Turcu F, Licchesi JD, Odenwaelder P, Wilkinson KD, Barford D. Molecular discrimination of structurally equivalent Lys 63-linked and linear polyubiquitin chains. EMBO Rep 2009 10 : 466 473.
185. Chen ZJ, Sun LJ. Nonproteolytic functions of ubiquitin in cell signaling. Mol Cell 2009 33 : 275 286.
186. Kang RS, et al. Solution structure of a CUE-ubiquitin complex reveals a conserved mode of ubiquitin binding. Cell 2003 113 : 621 630.
187. Bhoj VG, Chen ZJ. Ubiquitylation in innate and adaptive immunity. Nature 2009 458 : 430 437.
188. Sun L, Deng L, Ea CK, Xia ZP, Chen ZJ. The TRAF6 ubiquitin ligase and TAK1 kinase mediate IKK activation by BCL10 and MALT1 in T lymphocytes. Mol Cell 2004 14 : 289 301.
189. Noels H. A Novel TRAF6 binding site in MALT1 defines distinct mechanisms of NF-kB activation by API2-MALT1 fusions. J Biol Chem 2007 282 : 10180 10189.
190. Lamothe B, Besse A, Campos AD, Webster WK, Wu H, Darnay BG. Site-specific Lys-63-linked tumor necrosis factor receptor-associated factor 6 auto-ubiquitination is a critical determinant of I kappa B kinase activation. J Biol Chem 2007 282 : 4102 4112.
191. Lamothe B, Webster WK, Gopinathan A, Besse A, Campos AD, Darnay BG. TRAF6 ubiquitin ligase is essential for RANKL signaling and osteoclast differentiation. Biochem Biophys Res Commun 2007 359 : 1044 1049.
192. Wu CJ, Ashwell JD. NEMO recognition of ubiquitinated Bcl10 is required for T cell receptor-mediated NF-kappaB activation. Proc Natl Acad Sci USA 2008 105 : 3023 3028.
193. Oeckinghaus A, et al. Malt1 ubiquitination triggers NF-kappaB signaling upon T-cell activation. EMBO J 2007 26 : 4634 4645.
194. Rahighi S, et al. Specific recognition of linear ubiquitin chains by NEMO is important for NF-kappaB activation. Cell 2009 136 : 1098 1109.
195. Tokunaga F, et al. Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation. Nat Cell Biol 2009 11 : 123 132.
196. Zhou H, et al. Bcl10 activates the NF-kB pathway through ubiquitination of NEMO. Nature 2004 427 : 167 171.
197. Yin Q, et al. E2 interaction and dimerization in the crystal structure of TRAF6. Nature Struct Mol Biol 2009 16 : 658 666.
198. Hofer-Warbinek R, Schmid JA, Stehlik C, Binder BR, Lipp J, de Martin R. Activation of NF-kappa B by XIAP, the X chromosome-linked inhibitor of apoptosis, in endothelial cells involves TAK1. J Biol Chem 2000 275 : 22064 22068.
199. Jin HS, Lee DH, Kim DH, Chung JH, Lee SJ, Lee TH. cIAP1, cIAP2, and XIAP act cooperatively via nonredundant pathways to regulate genotoxic stress-induced nuclear factor-kappaB activation. Cancer Res 2009 69 : 1782 1791.
200. Leulier F, Lhocine N, Lemaitre B, Meier P. The Drosophila inhibitor of apoptosis protein DIAP2 functions in innate immunity and is essential to resist gram-negative bacterial infection. Mol Cell Biol 2006 26 : 7821 7831.
201. Dubrez-Daloz L, Dupoux A, Cartier J. IAPs: more than just inhibitors of apoptosis proteins. Cell Cycle 2008 7 : 1036 1046.
202. Kobayashi T, et al. TRAF6 is required for generation of the B-1a B cell compartment as well as T cell-dependent and -independent humoral immune responses. PLoS ONE 2009 4 : e4736.
203. King CG, et al. TRAF6 is a T cell-intrinsic negative regulator required for the maintenance of immune homeostasis. Nat Med 2006 12 : 1088 1092.
204. Yamamoto M. Key function for the Ubc13 E2 ubiquitin-conjugating enzyme in immune receptor signaling. Nat Immunol 2006 7 : 962 970.
205. Yamamoto M, et al. Cutting edge: pivotal function of Ubc13 in thymocyte TCR signaling. J Immunol 2006 177 : 7520 7524.
206. Liu HH, Xie M, Schneider MD, Chen ZJ. Essential role of TAK1 in thymocyte development and activation. Proc Natl Acad Sci USA 2006 103 : 11677 11682.
207. Wan YY, Chi H, Xie M, Schneider MD, Flavell RA. The kinase TAK1 integrates antigen and cytokine receptor signaling for T cell development, survival and function. Nat Immunol 2006 7 : 851 858.
208. Sato S. TAK1 is indispensable for development of T cells and prevention of colitis by the generation of regulatory T cells. Int Immunol 2006 18 : 1405 1411.
209. Schuman J, et al. A critical role of TAK1 in B-cell receptor-mediated nuclear factor kappaB activation. Blood 2009 113 : 4566 4574.
210. Hobeika E, et al. Testing gene function early in the B cell lineage in mb1-cre mice. Proc Natl Acad Sci USA 2006 103 : 13789 13794.
211. Thome M, Weil R. Post-translational modifications regulate distinct functions of CARMA1 and BCL10. Trends Immunol 2007 28 : 281 288.
212. Rueda D, et al. Bcl10 controls TCR- and FcgammaR-induced actin polymerization. J Immunol 2007 178 : 4373 4384.
213. Schaefer BC, Kappler JW, Kupfer A, Marrack P. Complex and dynamic redistribution of NF-kappaB signaling intermediates in response to T cell receptor stimulation. Proc Natl Acad Sci USA 2004 101 : 1004 1009.
214. Lobry C, Lopez T, Israel A, Weil R. Negative feedback loop in T cell activation through IkappaB kinase-induced phosphorylation and degradation of Bcl10. Proc Natl Acad Sci USA 2007 104 : 908 913.
215. Wegener E, et al. Essential role for IkappaB kinase beta in remodeling Carma1-Bcl10-Malt1 complexes upon T cell activation. Mol Cell 2006 23 : 13 23.
216. Renner F, Schmitz ML. Autoregulatory feedback loops terminating the NF-kappaB response. Trends Biochem Sci 2009 34 : 128 135.
217. Cheong R, Hoffmann A, Levchenko A. Understanding NF-kappaB signaling via mathematical modeling. Mol Syst Biol 2008 4 : 192.
218. Cheong R, Levchenko A. Wires in the soup: quantitative models of cell signaling. Trends Cell Biol 2008 18 : 112 118.
219. Kearns JD, Hoffmann A. Integrating computational and biochemical studies to explore mechanisms in NF-kB signaling. J Biol Chem 2009 284 : 5439 5443.
220. Hoffmann A, Baltimore D. Circuitry of nuclear factor kappaB signaling. Immunol Rev 2006 210 : 171 186.
221. Coornaert B, Carpentier I, Beyaert R. A20: central gatekeeper in inflammation and immunity. J Biol Chem 2009 284 : 8217 8221.
222. Lin SC, et al. Molecular basis for the unique deubiquitinating activity of the NF-kappaB inhibitor A20. J Mol Biol 2008 376 : 526 540.
223. Schmitz R, et al. TNFAIP3 (A20) is a tumor suppressor gene in Hodgkin lymphoma and primary mediastinal B cell lymphoma. J Exp Med 2009 206 : 981 989.
224. Kato M, et al. Frequent inactivation of A20 in B-cell lymphomas. Nature 2009 459 : 712 716.
225. Sarma V, et al. Activation of the B-cell surface receptor CD40 induces A20, a novel zinc finger protein that inhibits apoptosis. J Biol Chem 1995 270 : 12343 12346.
226. Ikeda F, Dikic I. CYLD in ubiquitin signaling and tumor pathogenesis. Cell 2006 125 : 643 645.
227. Sun SC. Deubiquitylation and regulation of the immune response. Nat Rev Immunol 2008 8 : 501 511.
228. Simonson SJ, Wu ZH, Miyamoto S. CYLD: a DUB with many talents. Dev Cell 2007 13 : 601 603.
229. Bignell GR, et al. Identification of the familial cylindromatosis tumour-suppressor gene. Nat Genet 2000 25 : 160 165.
230. Trompouki E, Hatzivassiliou E, Tsichritzis T, Farmer H, Ashworth A, Mosialos G. CYLD is a deubiquitinating enzyme that negatively regulates NF-kappaB activation by TNFR family members. Nature 2003 424 : 793 796.
231. Brummelkamp TR, Nijman SM, Dirac AM, Bernards R. Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-kappaB. Nature 2003 424 : 797 801.
232. Kovalenko A, Chable-Bessia C, Cantarella G, Israel A, Wallach D, Courtois G. The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature 2003 424 : 801 805.
233. Jin W, et al. Deubiquitinating enzyme CYLD regulates the peripheral development and naive phenotype maintenance of B cells. J Biol Chem 2007 282 : 15884 15893.
234. Hovelmeyer N, et al. Regulation of B cell homeostasis and activation by the tumor suppressor gene CYLD. J Exp Med 2007 204 : 2615 2627.
235. Hutti JE, et al. Phosphorylation of the tumor suppressor CYLD by the breast cancer oncogene IKKepsilon promotes cell transformation. Mol Cell 2009 34 : 461 472.
236. Mizuno T, Rothstein TL. B cell receptor (BCR) cross-talk: CD40 engagement creates an alternate pathway for BCR signaling that activates IkB Kinase/IkBa/NF-kB without the need for PI3K and phospholipase Cg. J Immunol 2005 174 : 6062 6070.
237. Richards S, Watanabe C, Santos L, Craxton A, Clark EA. Regulation of B-cell entry into the cell cycle. Immunol Rev 2008 224 : 183 200.
238. Conley ME, et al. Primary B cell immunodeficiencies: comparisons and contrasts. Annu Rev Immunol 2009 27 : 199 227.
239. Stadanlick JE, et al. Tonic B cell antigen receptor signals supply an NF-kB substrate for prosurvival BLyS signaling. Nat Immunol 2008 9 : 1379 1387.
240. Rifkin IR, Leadbetter EA, Busconi L, Viglianti G, Marshak-Rothstein A. Toll-like receptors, endogenous ligands, and systemic autoimmune disease. Immunol Rev 2005 204 : 27 42.
241. Wardemann H, Yurasov S, Schaefer A, Young JW, Meffre E, Nussenzweig MC. Predominant autoantibody production by early human B cell precursors. Science 2003 301 : 1374 1377.
242. Claudio E, Brown K, Siebenlist U. NF-kappaB guides the survival and differentiation of developing lymphocytes. Cell Death Differ 2006 13 : 697 701.
243. Verkoczy L, et al. A role for nuclear factor kappa B/rel transcription factors in the regulation of the recombinase activator genes. Immunity 2005 22 : 519 531.
244. Nemazee D. Receptor editing in lymphocyte development and central tolerance. Nat Rev Immunol 2006 6 : 728 740.
245. Derudder E, et al. Development of immunoglobulin lambda-chain-positive B cells, but not editing of immunoglobulin kappa-chain, depends on NF-kappaB signals. Nat Immunol 2009 10 : 647 654.
246. Mackay F, Schneider P. Cracking the BAFF code. Nat Rev Immunol 2009 9 : 491 502.
247. Cancro MP, D'Cruz DP, Khamashta MA. The role of B lymphocyte stimulator (BLyS) in systemic lupus erythematosus. J Clin Invest 2009 119 : 1066 1073.
248. Basak S, et al. A fourth IkappaB protein within the NF-kappaB signaling module. Cell 2007 128 : 369 381.
249. Jiang Z, Johnson HJ, Nie H, Qin J, Bird TA, Li X. Pellino 1 is required for interleukin-1 (IL-1)-mediated signaling through its interaction with the IL-1 receptor-associated kinase 4 (IRAK4)-IRAK-tumor necrosis factor receptor-associated factor 6 (TRAF6) complex. J Biol Chem 2003 278 : 10952 10956.
250. Xiao H, et al. Pellino 3b negatively regulates interleukin-1-induced TAK1-dependent NF kappaB activation. J Biol Chem 2008 283 : 14654 14664.
251. Jensen LE, Whitehead AS. Pellino2 activates the mitogen activated protein kinase pathway. FEBS Lett 2003 545 : 199 202.
252. Ohkawara B, et al. Role of the TAK1-NLK-STAT3 pathway in TGF-beta-mediated mesoderm induction. Genes Dev 2004 18 : 381 386.
253. Di Y, Li S, Wang L, Zhang Y, Dorf ME. Homeostatic interactions between MEKK3 and TAK1 involved in NF-kappaB signaling. Cell Signal 2008 20 : 705 713.
254. Blonska M, et al. TAK1 is recruited to the tumor necrosis factor-alpha (TNF-alpha) receptor 1 complex in a receptor-interacting protein (RIP)-dependent manner and cooperates with MEKK3 leading to NF-kappaB activation. J Biol Chem 2005 280 : 43056 43063.
255. Yao J, et al. Interleukin-1 (IL-1)-induced TAK1-dependent Versus MEKK3-dependent NFkappaB activation pathways bifurcate at IL-1 receptor-associated kinase modification. J Biol Chem 2007 282 : 6075 6089.
256. Minoda Y, Sakurai H, Kobayashi T, Yoshimura A, Takaesu G. An F-box protein, FBXW5, negatively regulates TAK1 MAP3K in the IL-1beta signaling pathway. Biochem Biophys Res Commun 2009 381 : 412 417.
257. Mochida Y, et al. ASK1 inhibits interleukin-1-induced NF-kappa B activity through disruption of TRAF6-TAK1 interaction. J Biol Chem 2000 275 : 32747 32752.
258. Frobose H, et al. Suppressor of cytokine signaling-3 inhibits interleukin-1 signaling by targeting the TRAF-6/TAK1 complex. Mol Endocrinol 2006 20 : 1587 1596.
259. Thiefes A, et al. The Yersinia enterocolitica effector YopP inhibits host cell signalling by inactivating the protein kinase TAK1 in the IL-1 signalling pathway. EMBO Rep 2006 7 : 838 844.
260. Haase R, Richter K, Pfaffinger G, Courtois G, Ruckdeschel K. Yersinia outer protein P suppresses TGF-beta-activated kinase-1 activity to impair innate immune signaling in Yersinia enterocolitica-infected cells. J Immunol 2005 175 : 8209 8217.
261. Madhavan S, Anghelina M, Sjostrom D, Dossumbekova A, Guttridge DC, Agarwal S. Biomechanical signals suppress TAK1 activation to inhibit NF-kappaB transcriptional activation in fibrochondrocytes. J Immunol 2007 179 : 6246 6254.
262. Hirata Y, et al. MyD88 and TNF receptor-associated factor 6 are critical signal transducers in Helicobacter pylori-infected human epithelial cells. J Immunol 2006 176 : 3796 3803.