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PMID: 18725521 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Stimulation of Toll-like receptor 3 and 4 induces interleukin-1beta maturation by caspase-8.

The Journal of experimental medicine ·Vol. 205 ·No. 9 ·2008-09-01 ·Pages 1967-73

Maelfait J, Vercammen E, Janssens S, Schotte P, Haegman M, Magez S, Beyaert R

Abstract

The cytokine interleukin (IL)-1beta is a key mediator of the inflammatory response and has been implicated in the pathophysiology of acute and chronic inflammation. IL-1beta is synthesized in response to many stimuli as an inactive pro-IL-1beta precursor protein that is further processed by caspase-1 into mature IL-1beta, which is the secreted biologically active form of the cytokine. Although stimulation of membrane-bound Toll-like receptors (TLRs) up-regulates pro-IL-1beta expression, activation of caspase-1 is believed to be mainly initiated by cytosolic Nod-like receptors. In this study, we show that polyinosinic:polycytidylic acid (poly[I:C]) and lipopolysaccharide stimulation of macrophages induces pro-IL-1beta processing via a Toll/IL-1R domain-containing adaptor-inducing interferon-beta-dependent signaling pathway that is initiated by TLR3 and TLR4, respectively. Ribonucleic acid interference (RNAi)-mediated knockdown of the intracellular receptors NALP3 or MDA5 did not affect poly(I:C)-induced pro-IL-1beta processing. Surprisingly, poly(I:C)- and LPS-induced pro-IL-1beta processing still occurred in caspase-1-deficient cells. In contrast, pro-IL-1beta processing was inhibited by caspase-8 peptide inhibitors, CrmA or vFLIP expression, and caspase-8 knockdown via RNAi, indicating an essential role for caspase-8. Moreover, recombinant caspase-8 was able to cleave pro-IL-1beta in vitro at exactly the same site as caspase-1. These results implicate a novel role for caspase-8 in the production of biologically active IL-1beta in response to TLR3 and TLR4 stimulation.

MeSH Terms
Animals Caspase 8/metabolism Cell Line Gene Expression Regulation Humans Inflammation Interleukin-1beta/metabolism Mice Models, Biological RNA Interference Signal Transduction Toll-Like Receptor 3/metabolism Toll-Like Receptor 4/metabolism
Chemicals
Interleukin-1beta TLR3 protein, human TLR3 protein, mouse TLR4 protein, human Tlr4 protein, mouse Toll-Like Receptor 3 Toll-Like Receptor 4 Caspase 8
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Maelfait Jonathan
Unit of Molecular Signal Transduction in Inflammation, Department for Molecular Biomedical Research, VIB, B-9052 Ghent, Belgium.
Vercammen Elisabeth
Janssens Sophie
Schotte Peter
Haegman Mira
Magez Stefan
Beyaert Rudi
References (30)
30 references, click to expand
  1. Caspase-8 serves both apoptotic and nonapoptotic roles.
    J Immunol. 2004 Sep 1;173(5):2976-84 PMID: 15322156
  2. TLRs, NLRs and RLRs: a trinity of pathogen sensors that co-operate in innate immunity.
    Trends Immunol. 2006 Aug;27(8):352-7 PMID: 16807108
  3. Apoptotic cell removal.
    Curr Biol. 2001 Oct 2;11(19):R795-805 PMID: 11591341
  4. Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1.
    Immunity. 2006 Mar;24(3):317-27 PMID: 16546100
  5. Identification of bacterial muramyl dipeptide as activator of the NALP3/cryopyrin inflammasome.
    Curr Biol. 2004 Nov 9;14(21):1929-34 PMID: 15530394
  6. Processing of precursor interleukin 1 beta and inflammatory disease.
    J Biol Chem. 1990 Apr 15;265(11):6318-22 PMID: 2156847
  7. Mechanisms of the TRIF-induced interferon-stimulated response element and NF-kappaB activation and apoptosis pathways.
    J Biol Chem. 2004 Apr 9;279(15):15652-61 PMID: 14739303
  8. Toll/IL-1 receptor domain-containing adaptor inducing IFN-beta (TRIF) associates with TNF receptor-associated factor 6 and TANK-binding kinase 1, and activates two distinct transcription factors, NF-kappa B and IFN-regulatory factor-3, in the Toll-like receptor signaling.
    J Immunol. 2003 Oct 15;171(8):4304-10 PMID: 14530355
  9. Response to local inflammation of IL-1 beta-converting enzyme- deficient mice.
    J Immunol. 1997 Feb 15;158(4):1818-24 PMID: 9029121
  10. Development of a simple, sensitive and specific bioassay for interleukin-1 based on the proliferation of RPMI 1788 cells. Comparison with other bioassays for IL-1.
    J Immunol Methods. 1990 Dec 31;135(1-2):25-32 PMID: 2273259
  11. Pannexin-1-mediated recognition of bacterial molecules activates the cryopyrin inflammasome independent of Toll-like receptor signaling.
    Immunity. 2007 Apr;26(4):433-43 PMID: 17433728
  12. TLR signaling.
    Semin Immunol. 2007 Feb;19(1):24-32 PMID: 17275323
  13. Targeting Rac1 by the Yersinia effector protein YopE inhibits caspase-1-mediated maturation and release of interleukin-1beta.
    J Biol Chem. 2004 Jun 11;279(24):25134-42 PMID: 15060067
  14. RIP1 is an essential mediator of Toll-like receptor 3-induced NF-kappa B activation.
    Nat Immunol. 2004 May;5(5):503-7 PMID: 15064760
  15. The interleukin-1 receptor/Toll-like receptor superfamily: signal transduction during inflammation and host defense.
    Sci STKE. 2003 Feb 25;2003(171):re3 PMID: 12606705
  16. ASC is essential for LPS-induced activation of procaspase-1 independently of TLR-associated signal adaptor molecules.
    Genes Cells. 2004 Nov;9(11):1055-67 PMID: 15507117
  17. Caspase 1-independent IL-1beta release and inflammation induced by the apoptosis inducer Fas ligand.
    Nat Med. 1998 Nov;4(11):1287-92 PMID: 9809553
  18. Caspases in cell survival, proliferation and differentiation.
    Cell Death Differ. 2007 Jan;14(1):44-55 PMID: 17053807
  19. Apoptosis induced by the toll-like receptor adaptor TRIF is dependent on its receptor interacting protein homotypic interaction motif.
    J Immunol. 2005 Apr 15;174(8):4942-52 PMID: 15814722
  20. Cryopyrin activates the inflammasome in response to toxins and ATP.
    Nature. 2006 Mar 9;440(7081):228-32 PMID: 16407890
  21. Inflammatory caspases and inflammasomes: master switches of inflammation.
    Cell Death Differ. 2007 Jan;14(1):10-22 PMID: 16977329
  22. Caspase inhibitors: viral, cellular and chemical.
    Cell Death Differ. 2007 Jan;14(1):73-8 PMID: 16946729
  23. IL-1-converting enzyme requires aspartic acid residues for processing of the IL-1 beta precursor at two distinct sites and does not cleave 31-kDa IL-1 alpha.
    J Immunol. 1991 Nov 1;147(9):2964-9 PMID: 1919001
  24. Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock.
    Cell. 1995 Feb 10;80(3):401-11 PMID: 7859282
  25. MDP-induced interleukin-1beta processing requires Nod2 and CIAS1/NALP3.
    J Leukoc Biol. 2007 Jul;82(1):177-83 PMID: 17403772
  26. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo.
    Nat Biotechnol. 1997 Sep;15(9):871-5 PMID: 9306402
  27. Critical role for Cryopyrin/Nalp3 in activation of caspase-1 in response to viral infection and double-stranded RNA.
    J Biol Chem. 2006 Dec 1;281(48):36560-8 PMID: 17008311
  28. Cleavage of PITSLRE kinases by ICE/CASP-1 and CPP32/CASP-3 during apoptosis induced by tumor necrosis factor.
    J Biol Chem. 1997 May 2;272(18):11694-7 PMID: 9115219
  29. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses.
    Nature. 2006 May 4;441(7089):101-5 PMID: 16625202
  30. 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
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
1540-9538
Published
2008-09-01
Epub
2008-00-25
Pages
1967-73
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2526192
Subset
IM
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