Abstract
The interleukin-1 (IL-1) receptor-associated kinase 1 (IRAK1) is a member of the IRAK kinase family that plays a pivotal role in the Toll/IL-1 receptor (TIR) family signaling cascade. We have identified a novel splice variant, IRAK1c, which lacks a region encoded by exon 11 of the IRAK1 gene. IRAK1c expression was confirmed by both RNA and protein detection. Although both IRAK1 and IRAK1c are expressed in most tissues tested, IRAK1c is the predominant form of IRAK1 expressed in the brain. Unlike IRAK1, IRAK1c lacks kinase activity and cannot be phosphorylated by IRAK4. However, IRAK1c retains the ability to strongly interact with IRAK2, MyD88, Tollip, and TRAF6. Overexpression of IRAK1c suppressed NF-kappaB activation and blocked IL-1beta-induced IL-6 as well as lipopolysaccharide- and CpG-induced tumor necrosis factor alpha production in multiple cellular systems. Mechanistically, we provide evidence that IRAK1c functions as a dominant negative by failing to be phosphorylated by IRAK4, thus remaining associated with Tollip and blocking NF-kappaB activation. The presence of a regulated, alternative splice variant of IRAK1 that functions as a kinase-dead, dominant-negative protein adds further complexity to the variety of mechanisms that regulate TIR signaling and the subsequent inflammatory response.
MeSH Terms
Adaptor Proteins, Signal Transducing
Alternative Splicing
Animals
Antigens, Differentiation/metabolism
Brain/enzymology,pathology
Cell Line, Tumor
Cells, Cultured
Humans
Inflammation/genetics,metabolism
Interleukin-1 Receptor-Associated Kinases
Interleukin-6/metabolism
Intracellular Signaling Peptides and Proteins/metabolism
Membrane Glycoproteins/physiology
Mice
Mitogen-Activated Protein Kinases/metabolism
Myeloid Differentiation Factor 88
NF-kappa B/antagonists & inhibitors,metabolism
Phosphorylation
Protein Kinases/genetics,physiology
Receptors, Cell Surface/physiology
Receptors, Immunologic/metabolism
Receptors, Interleukin-1/genetics,metabolism
Signal Transduction/genetics,physiology
TNF Receptor-Associated Factor 6/metabolism
Toll-Like Receptors
Tumor Necrosis Factor-alpha/metabolism
Chemicals
Adaptor Proteins, Signal Transducing
Antigens, Differentiation
Interleukin-6
Intracellular Signaling Peptides and Proteins
MYD88 protein, human
Membrane Glycoproteins
Myd88 protein, mouse
Myeloid Differentiation Factor 88
NF-kappa B
Receptors, Cell Surface
Receptors, Immunologic
Receptors, Interleukin-1
TNF Receptor-Associated Factor 6
TOLLIP protein, human
Toll-Like Receptors
Tollip protein, mouse
Tumor Necrosis Factor-alpha
Protein Kinases
IRAK1 protein, human
IRAK4 protein, human
Interleukin-1 Receptor-Associated Kinases
Irak1 protein, mouse
Mitogen-Activated Protein Kinases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Rao Navin
Johnson and Johnson Pharmaceutical Research and Development, 3210 Merryfield Row, San Diego, CA 92121, USA.
Nguyen Steven
Ngo Karen
Fung-Leung Wai-Ping
References (29)
29 references, click to expand
-
A novel splice variant of mouse interleukin-1-receptor-associated kinase-1 (IRAK-1) activates nuclear factor-kappaB (NF-kappaB) and c-Jun N-terminal kinase (JNK).
Biochem J. 2003 Feb 15;370(Pt 1):159-66
PMID: 12418963
-
IRAK-M is a negative regulator of Toll-like receptor signaling.
Cell. 2002 Jul 26;110(2):191-202
PMID: 12150927
-
Identification and characterization of murine IRAK-2.
Biochem Biophys Res Commun. 2002 Sep 13;297(1):52-8
PMID: 12220507
-
TLRs: differential adapter utilization by toll-like receptors mediates TLR-specific patterns of gene expression.
Mol Interv. 2003 Dec;3(8):466-77
PMID: 14993454
-
CD1-dependent dendritic cell instruction.
Nat Immunol. 2002 Dec;3(12):1163-8
PMID: 12415264
-
Tollip, a new component of the IL-1RI pathway, links IRAK to the IL-1 receptor.
Nat Cell Biol. 2000 Jun;2(6):346-51
PMID: 10854325
-
IL-1-induced NFkappa B and c-Jun N-terminal kinase (JNK) activation diverge at IL-1 receptor-associated kinase (IRAK).
Proc Natl Acad Sci U S A. 2001 Apr 10;98(8):4461-5
PMID: 11287640
-
Functional diversity and regulation of different interleukin-1 receptor-associated kinase (IRAK) family members.
Mol Cell. 2003 Feb;11(2):293-302
PMID: 12620219
-
CpG DNA induces self and cross-hyporesponsiveness of RAW264.7 cells in response to CpG DNA and lipopolysaccharide: alterations in IL-1 receptor-associated kinase expression.
J Immunol. 2003 Jan 15;170(2):1052-61
PMID: 12517973
-
Severe impairment of interleukin-1 and Toll-like receptor signalling in mice lacking IRAK-4.
Nature. 2002 Apr 18;416(6882):750-6
PMID: 11923871
-
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 Oct;22(20):7158-67
PMID: 12242293
-
TRAF6 is a signal transducer for interleukin-1.
Nature. 1996 Oct 3;383(6599):443-6
PMID: 8837778
-
The role of interleukin 1 receptor-associated kinase-4 (IRAK-4) kinase activity in IRAK-4-mediated signaling.
J Biol Chem. 2004 Sep 24;279(39):40653-8
PMID: 15292196
-
Regulation of interleukin-1- and lipopolysaccharide-induced NF-kappaB activation by alternative splicing of MyD88.
Curr Biol. 2002 Mar 19;12(6):467-71
PMID: 11909531
-
IRAK-4: a novel member of the IRAK family with the properties of an IRAK-kinase.
Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):5567-72
PMID: 11960013
-
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
-
Inhibition of interleukin 1 receptor/Toll-like receptor signaling through the alternatively spliced, short form of MyD88 is due to its failure to recruit IRAK-4.
J Exp Med. 2003 Jan 20;197(2):263-8
PMID: 12538665
-
Toll-like receptor signalling.
Nat Rev Immunol. 2004 Jul;4(7):499-511
PMID: 15229469
-
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
-
Of mice and not men: differences between mouse and human immunology.
J Immunol. 2004 Mar 1;172(5):2731-8
PMID: 14978070
-
Exip, a splicing variant of p38alpha, participates in interleukin-1 receptor proximal complex and downregulates NF-kappaB pathway.
FEBS Lett. 2004 Sep 24;575(1-3):136-40
PMID: 15388348
-
Defective interleukin (IL)-18-mediated natural killer and T helper cell type 1 responses in IL-1 receptor-associated kinase (IRAK)-deficient mice.
J Exp Med. 1999 Apr 5;189(7):1129-38
PMID: 10190904
-
MyD88S, a splice variant of MyD88, differentially modulates NF-kappaB- and AP-1-dependent gene expression.
FEBS Lett. 2003 Jul 31;548(1-3):103-7
PMID: 12885415
-
Sequential autophosphorylation steps in the interleukin-1 receptor-associated kinase-1 regulate its availability as an adapter in interleukin-1 signaling.
J Biol Chem. 2004 Feb 13;279(7):5227-36
PMID: 14625308
-
An essential role of ubiquitination in Cbl-mediated negative regulation of the Src-family kinase Fyn.
Signal Transduct. 2002 Nov 7;2(1-2):29-39
PMID: 19966925
-
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
-
Pyogenic bacterial infections in humans with IRAK-4 deficiency.
Science. 2003 Mar 28;299(5615):2076-9
PMID: 12637671
-
The murine IRAK2 gene encodes four alternatively spliced isoforms, two of which are inhibitory.
J Biol Chem. 2004 Jun 25;279(26):27699-708
PMID: 15082713
-
IRAK1b, a novel alternative splice variant of interleukin-1 receptor-associated kinase (IRAK), mediates interleukin-1 signaling and has prolonged stability.
J Biol Chem. 2001 Aug 3;276(31):29037-44
PMID: 11397809