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PMID: 11259596 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Interleukin-1 (IL-1) receptor-associated kinase leads to activation of TAK1 by inducing TAB2 translocation in the IL-1 signaling pathway.

Molecular and cellular biology ·Vol. 21 ·No. 7 ·2001-04-00 ·Pages 2475-84

Takaesu G, Ninomiya-Tsuji J, Kishida S, Li X, Stark GR, Matsumoto K

Abstract

Interleukin-1 (IL-1) is a proinflammatory cytokine that recognizes a surface receptor complex and generates multiple cellular responses. IL-1 stimulation activates the mitogen-activated protein kinase kinase kinase TAK1, which in turn mediates activation of c-Jun N-terminal kinase and NF-kappaB. TAB2 has previously been shown to interact with both TAK1 and TRAF6 and promote their association, thereby triggering subsequent IL-1 signaling events. The serine/threonine kinase IL-1 receptor-associated kinase (IRAK) also plays a role in IL-1 signaling, being recruited to the IL-1 receptor complex early in the signal cascade. In this report, we investigate the role of IRAK in the activation of TAK1. Genetic analysis reveals that IRAK is required for IL-1-induced activation of TAK1. We show that IL-1 stimulation induces the rapid but transient association of IRAK, TRAF6, TAB2, and TAK1. TAB2 is recruited to this complex following translocation from the membrane to the cytosol upon IL-1 stimulation. In IRAK-deficient cells, TAB2 translocation and its association with TRAF6 are abolished. These results suggest that IRAK regulates the redistribution of TAB2 upon IL-1 stimulation and facilitates the formation of a TRAF6-TAB2-TAK1 complex. Formation of this complex is an essential step in the activation of TAK1 in the IL-1 signaling pathway.

MeSH Terms
Adaptor Proteins, Signal Transducing Carrier Proteins/physiology Cell Line Enzyme Activation Humans Interleukin-1/physiology MAP Kinase Kinase Kinases/physiology MAP Kinase Signaling System Receptors, Interleukin-1/physiology Signal Transduction
Chemicals
Adaptor Proteins, Signal Transducing Carrier Proteins Interleukin-1 Receptors, Interleukin-1 TAB2 protein, human MAP Kinase Kinase Kinases MAP kinase kinase kinase 7
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Takaesu G
Department of Molecular Biology, Graduate School of Science, Nagoya University, Nagoya 464-8602, Japan.
Ninomiya-Tsuji J
Kishida S
Li X
Stark G R
Matsumoto K
References (47)
47 references, click to expand
  1. Impaired cytokine signaling in mice lacking the IL-1 receptor-associated kinase.
    J Immunol. 1999 Jul 15;163(2):978-84 PMID: 10395695
  2. Biologic basis for interleukin-1 in disease.
    Blood. 1996 Mar 15;87(6):2095-147 PMID: 8630372
  3. The beginning of the end: IkappaB kinase (IKK) and NF-kappaB activation.
    J Biol Chem. 1999 Sep 24;274(39):27339-42 PMID: 10488062
  4. TAK1 mitogen-activated protein kinase kinase kinase is activated by autophosphorylation within its activation loop.
    J Biol Chem. 2000 Mar 10;275(10):7359-64 PMID: 10702308
  5. TAB1: an activator of the TAK1 MAPKKK in TGF-beta signal transduction.
    Science. 1996 May 24;272(5265):1179-82 PMID: 8638164
  6. TRAF6 is a signal transducer for interleukin-1.
    Nature. 1996 Oct 3;383(6599):443-6 PMID: 8837778
  7. NF-kappa B: ten years after.
    Cell. 1996 Oct 4;87(1):13-20 PMID: 8858144
  8. Activation of the IkappaB alpha kinase complex by MEKK1, a kinase of the JNK pathway.
    Cell. 1997 Jan 24;88(2):213-22 PMID: 9008162
  9. MAP3K-related kinase involved in NF-kappaB induction by TNF, CD95 and IL-1.
    Nature. 1997 Feb 6;385(6616):540-4 PMID: 9020361
  10. The interleukin-1 receptor accessory protein (IL-1RAcP) is essential for IL-1-induced activation of interleukin-1 receptor-associated kinase (IRAK) and stress-activated protein kinases (SAP kinases).
    J Biol Chem. 1997 Mar 21;272(12):7727-31 PMID: 9065432
  11. Identification and characterization of an IkappaB kinase.
    Cell. 1997 Jul 25;90(2):373-83 PMID: 9244310
  12. A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB.
    Nature. 1997 Aug 7;388(6642):548-54 PMID: 9252186
  13. The interleukin-1 receptor-associated kinase is degraded by proteasomes following its phosphorylation.
    J Biol Chem. 1997 Aug 22;272(34):21540-7 PMID: 9261174
  14. The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation.
    Cell. 1997 Oct 17;91(2):243-52 PMID: 9346241
  15. IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation.
    Science. 1997 Oct 31;278(5339):860-6 PMID: 9346484
  16. IkappaB kinase-beta: NF-kappaB activation and complex formation with IkappaB kinase-alpha and NIK.
    Science. 1997 Oct 31;278(5339):866-9 PMID: 9346485
  17. IRAK (Pelle) family member IRAK-2 and MyD88 as proximal mediators of IL-1 signaling.
    Science. 1997 Nov 28;278(5343):1612-5 PMID: 9374458
  18. Recruitment of IRAK to the interleukin 1 receptor complex requires interleukin 1 receptor accessory protein.
    Proc Natl Acad Sci U S A. 1997 Nov 25;94(24):12829-32 PMID: 9371760
  19. MyD88: an adapter that recruits IRAK to the IL-1 receptor complex.
    Immunity. 1997 Dec;7(6):837-47 PMID: 9430229
  20. NF-kappaB-inducing kinase activates IKK-alpha by phosphorylation of Ser-176.
    Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3792-7 PMID: 9520446
  21. MyD88, an adapter protein involved in interleukin-1 signaling.
    J Biol Chem. 1998 May 15;273(20):12203-9 PMID: 9575168
  22. Interleukin (IL)-1 receptor-associated kinase (IRAK) requirement for optimal induction of multiple IL-1 signaling pathways and IL-6 production.
    J Exp Med. 1998 Jun 15;187(12):2073-9 PMID: 9625767
  23. Complementation cloning of NEMO, a component of the IkappaB kinase complex essential for NF-kappaB activation.
    Cell. 1998 Jun 26;93(7):1231-40 PMID: 9657155
  24. MEKK1 activates both IkappaB kinase alpha and IkappaB kinase beta.
    Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9319-24 PMID: 9689078
  25. IKK-gamma is an essential regulatory subunit of the IkappaB kinase complex.
    Nature. 1998 Sep 17;395(6699):297-300 PMID: 9751060
  26. Activation of IkappaB kinase beta by protein kinase C isoforms.
    Mol Cell Biol. 1999 Mar;19(3):2180-8 PMID: 10022904
  27. A Drosophila TNF-receptor-associated factor (TRAF) binds the ste20 kinase Misshapen and activates Jun kinase.
    Curr Biol. 1999 Jan 28;9(2):101-4 PMID: 10021364
  28. The kinase TAK1 can activate the NIK-I kappaB as well as the MAP kinase cascade in the IL-1 signalling pathway.
    Nature. 1999 Mar 18;398(6724):252-6 PMID: 10094049
  29. Overexpression of an enzymically inactive interleukin-1-receptor-associated kinase activates nuclear factor-kappaB.
    Biochem J. 1999 Apr 15;339 ( Pt 2):227-31 PMID: 10191251
  30. Effects of IL-1 receptor-associated kinase (IRAK) expression on IL-1 signaling are independent of its kinase activity.
    FEBS Lett. 1999 Apr 1;448(1):81-5 PMID: 10217414
  31. TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling.
    Genes Dev. 1999 Apr 15;13(8):1015-24 PMID: 10215628
  32. Oligomerisation of Tube and Pelle leads to nuclear localisation of dorsal.
    Mech Dev. 1999 Mar;81(1-2):127-38 PMID: 10330490
  33. Phylogenetic perspectives in innate immunity.
    Science. 1999 May 21;284(5418):1313-8 PMID: 10334979
  34. Mutant cells that do not respond to interleukin-1 (IL-1) reveal a novel role for IL-1 receptor-associated kinase.
    Mol Cell Biol. 1999 Jul;19(7):4643-52 PMID: 10373513
  35. IRAK-M is a novel member of the Pelle/interleukin-1 receptor-associated kinase (IRAK) family.
    J Biol Chem. 1999 Jul 2;274(27):19403-10 PMID: 10383454
  36. The atypical PKC-interacting protein p62 channels NF-kappaB activation by the IL-1-TRAF6 pathway.
    EMBO J. 2000 Apr 3;19(7):1576-86 PMID: 10747026
  37. 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 Apr;5(4):649-58 PMID: 10882101
  38. pelle encodes a protein kinase required to establish dorsoventral polarity in the Drosophila embryo.
    Cell. 1993 Feb 26;72(4):515-25 PMID: 8440018
  39. Domain mapping of tube, a protein essential for dorsoventral patterning of the Drosophila embryo.
    EMBO J. 1993 Sep;12(9):3449-58 PMID: 8253071
  40. Activation of the kinase Pelle by Tube in the dorsoventral signal transduction pathway of Drosophila embryo.
    Nature. 1994 Dec 8;372(6506):563-6 PMID: 7527496
  41. NF-kappa B: a lesson in family values.
    Cell. 1995 Feb 24;80(4):529-32 PMID: 7867060
  42. Molecular cloning and characterization of a second subunit of the interleukin 1 receptor complex.
    J Biol Chem. 1995 Jun 9;270(23):13757-65 PMID: 7775431
  43. Interaction of the pelle kinase with the membrane-associated protein tube is required for transduction of the dorsoventral signal in Drosophila embryos.
    Development. 1995 Jul;121(7):2209-18 PMID: 7635064
  44. Rel/NF-kappa B/I kappa B family: intimate tales of association and dissociation.
    Genes Dev. 1995 Nov 15;9(22):2723-35 PMID: 7590248
  45. Identification of a member of the MAPKKK family as a potential mediator of TGF-beta signal transduction.
    Science. 1995 Dec 22;270(5244):2008-11 PMID: 8533096
  46. IRAK: a kinase associated with the interleukin-1 receptor.
    Science. 1996 Feb 23;271(5252):1128-31 PMID: 8599092
  47. ECSIT is an evolutionarily conserved intermediate in the Toll/IL-1 signal transduction pathway.
    Genes Dev. 1999 Aug 15;13(16):2059-71 PMID: 10465784
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2001-04-00
Pages
2475-84
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC86880
Subset
IM
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