The inositol phosphatase SHIP-1 inhibits NOD2-induced NF-κB activation by disturbing the interaction of XIAP with RIP2

[en] SHIP-1 is an inositol phosphatase predominantly expressed in hematopoietic cells. Over the ten past years, SHIP-1 has been described as an important regulator of immune functions. Here, we characterize a new inhibitory function for SHIP-1 in NOD2 signaling. NOD2 is a crucial cytoplasmic bacterial sensor that activates proinflammatory and antimicrobial responses upon bacterial invasion. We observed that SHIP-1 decreases NOD2-induced NF-κB activation in macrophages. This negative regulation relies on its interaction with XIAP. Indeed, we observed that XIAP is an essential mediator of the NOD2 signaling pathway that enables proper NF-κB activation in macrophages. Upon NOD2 activation, SHIP-1 C-terminal proline rich domain (PRD) interacts with XIAP, thereby disturbing the interaction between XIAP and RIP2 in order to decrease NF-κB signaling.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Condé, Claude ; Université de Liège - ULiège > GIGA-R : Virologie - Immunologie

Rambout, Xavier ; Université de Liège - ULiège > Chimie et bio-industries > Biologie cell. et moléc.

Lebrun, Marielle ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Virologie et immunologie

Lecat, Aurore ; Université de Liège - ULiège > GIGA-R : Virologie - Immunologie

Di Valentin, Emmanuel ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Virologie et immunologie

Dequiedt, Franck ; Université de Liège - ULiège > GIGA-Research

Piette, Jacques ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Virologie - Immunologie

Gloire, Geoffrey ; Université de Liège - ULiège > Interface Entreprises-Université

Legrand, Sylvie ; Université de Liège - ULiège > GIGA-R : Virologie - Immunologie

Language :

English

Title :

The inositol phosphatase SHIP-1 inhibits NOD2-induced NF-κB activation by disturbing the interaction of XIAP with RIP2

Publication date :

2012

Journal title :

PLoS ONE

eISSN :

1932-6203

Publisher :

Public Library of Science, San Franscisco, United States - California

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 19 June 2012

Statistics

Number of views

131 (19 by ULiège)

Number of downloads

228 (7 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Akira S, Takeda K, (2004) Toll-like receptor signalling. Nat Rev Immunol 4: 499-511.
Wilmanski JM, Petnicki-Ocwieja T, Kobayashi KS, (2008) NLR proteins: integral members of innate immunity and mediators of inflammatory diseases. J Leukoc Biol 83: 13-30.
Inohara N, Ogura Y, Fontalba A, Gutierrez O, Pons F, et al. (2003) Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J Biol Chem 278: 5509-5512.
Girardin SE, Boneca IG, Carneiro LA, Antignac A, Jehanno M, et al. (2003) Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 300: 1584-1587.
Hugot JP, Chamaillard M, Zouali H, Lesage S, Cezard JP, et al. (2001) Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411: 599-603.
Ogura Y, Bonen DK, Inohara N, Nicolae DL, Chen FF, et al. (2001) A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411: 603-606.
Kobayashi KS, Chamaillard M, Ogura Y, Henegariu O, Inohara N, et al. (2005) Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 307: 731-734.
Lecat A, Piette J, Legrand-Poels S, (2010) The protein Nod2: an innate receptor more complex than previously assumed. Biochem Pharmacol 80: 2021-2031.
Bertrand MJ, Doiron K, Labbe K, Korneluk RG, Barker PA, et al. (2009) Cellular inhibitors of apoptosis cIAP1 and cIAP2 are required for innate immunity signaling by the pattern recognition receptors NOD1 and NOD2. Immunity 30: 789-801.
Abbott DW, Wilkins A, Asara JM, Cantley LC, (2004) The Crohn's disease protein, NOD2, requires RIP2 in order to induce ubiquitinylation of a novel site on NEMO. Curr Biol 14: 2217-2227.
Windheim M, Lang C, Peggie M, Plater LA, Cohen P, (2007) Molecular mechanisms involved in the regulation of cytokine production by muramyl dipeptide. Biochem J 404: 179-190.
Yang Y, Yin C, Pandey A, Abbott D, Sassetti C, et al. (2007) NOD2 pathway activation by MDP or Mycobacterium tuberculosis infection involves the stable polyubiquitination of Rip2. J Biol Chem 282: 36223-36229.
Oeckinghaus A, Ghosh S, (2009) The NF-kappaB family of transcription factors and its regulation. Cold Spring Harb Perspect Biol 1: a000034.
Duckett CS, Nava VE, Gedrich RW, Clem RJ, van Dongen JL, et al. (1996) A conserved family of cellular genes related to the baculovirus iap gene and encoding apoptosis inhibitors. EMBO J 15: 2685-2694.
Gyrd-Hansen M, Darding M, Miasari M, Santoro MM, Zender L, et al. (2008) IAPs contain an evolutionarily conserved ubiquitin-binding domain that regulates NF-kappaB as well as cell survival and oncogenesis. Nat Cell Biol 10: 1309-1317.
Gyrd-Hansen M, Meier P, (2010) IAPs: from caspase inhibitors to modulators of NF-kappaB, inflammation and cancer. Nat Rev Cancer 10: 561-574.
Hofer-Warbinek R, Schmid JA, Stehlik C, Binder BR, Lipp J, et al. (2000) Activation of NF-kappa B by XIAP, the X chromosome-linked inhibitor of apoptosis, in endothelial cells involves TAK1. J Biol Chem 275: 22064-22068.
Lu M, Lin SC, Huang Y, Kang YJ, Rich R, et al. (2007) XIAP induces NF-kappaB activation via the BIR1/TAB1 interaction and BIR1 dimerization. Mol Cell 26: 689-702.
Krieg A, Correa RG, Garrison JB, Le Negrate G, Welsh K, et al. (2009) XIAP mediates NOD signaling via interaction with RIP2. Proc Natl Acad Sci U S A 106: 14524-14529.
Bauler LD, Duckett CS, O'Riordan MX, (2008) XIAP regulates cytosol-specific innate immunity to Listeria infection. PLoS Pathog 4: e1000142.
Damen JE, Liu L, Rosten P, Humphries RK, Jefferson AB, et al. (1996) The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3,4,5-triphosphate 5-phosphatase. Proc Natl Acad Sci U S A 93: 1689-1693.
Kavanaugh WM, Pot DA, Chin SM, Deuter-Reinhard M, Jefferson AB, et al. (1996) Multiple forms of an inositol polyphosphate 5-phosphatase form signaling complexes with Shc and Grb2. Curr Biol 6: 438-445.
Lioubin MN, Algate PA, Tsai S, Carlberg K, Aebersold A, et al. (1996) p150Ship, a signal transduction molecule with inositol polyphosphate-5-phosphatase activity. Genes Dev 10: 1084-1095.
Conde C, Gloire G, Piette J, (2011) Enzymatic and non-enzymatic activities of SHIP-1 in signal transduction and cancer. Biochem Pharmacol 82: 1320-1334.
Liu Q, Oliveira-Dos-Santos AJ, Mariathasan S, Bouchard D, Jones J, et al. (1998) The inositol polyphosphate 5-phosphatase ship is a crucial negative regulator of B cell antigen receptor signaling. J Exp Med 188: 1333-1342.
Tridandapani S, Pradhan M, LaDine JR, Garber S, Anderson CL, et al. (1999) Protein interactions of Src homology 2 (SH2) domain-containing inositol phosphatase (SHIP): association with Shc displaces SHIP from FcgammaRIIb in B cells. J Immunol 162: 1408-1414.
Tridandapani S, Phee H, Shivakumar L, Kelley TW, Coggeshall KM, (1998) Role of SHIP in FcgammaRIIb-mediated inhibition of Ras activation in B cells. Mol Immunol 35: 1135-1146.
Bolland S, Pearse RN, Kurosaki T, Ravetch JV, (1998) SHIP modulates immune receptor responses by regulating membrane association of Btk. Immunity 8: 509-516.
Galandrini R, Tassi I, Morrone S, Lanfrancone L, Pelicci P, et al. (2001) The adaptor protein shc is involved in the negative regulation of NK cell-mediated cytotoxicity. Eur J Immunol 31: 2016-2025.
Galandrini R, Tassi I, Mattia G, Lenti L, Piccoli M, et al. (2002) SH2-containing inositol phosphatase (SHIP-1) transiently translocates to raft domains and modulates CD16-mediated cytotoxicity in human NK cells. Blood 100: 4581-4589.
Helgason CD, Damen JE, Rosten P, Grewal R, Sorensen P, et al. (1998) Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev 12: 1610-1620.
Kalesnikoff J, Baur N, Leitges M, Hughes MR, Damen JE, et al. (2002) SHIP negatively regulates IgE + antigen-induced IL-6 production in mast cells by inhibiting NF-kappa B activity. J Immunol 168: 4737-4746.
Kalesnikoff J, Lam V, Krystal G, (2002) SHIP represses mast cell activation and reveals that IgE alone triggers signaling pathways which enhance normal mast cell survival. Mol Immunol 38: 1201-1206.
An H, Xu H, Zhang M, Zhou J, Feng T, et al. (2005) Src homology 2 domain-containing inositol-5-phosphatase 1 (SHIP1) negatively regulates TLR4-mediated LPS response primarily through a phosphatase activity- and PI-3K-independent mechanism. Blood 105: 4685-4692.
Gabhann JN, Higgs R, Brennan K, Thomas W, Damen JE, et al. (2010) Absence of SHIP-1 results in constitutive phosphorylation of tank-binding kinase 1 and enhanced TLR3-dependent IFN-beta production. J Immunol 184: 2314-2320.
Dong S, Corre B, Foulon E, Dufour E, Veillette A, et al. (2006) T cell receptor for antigen induces linker for activation of T cell-dependent activation of a negative signaling complex involving Dok-2, SHIP-1, and Grb-2. J Exp Med 203: 2509-2518.
Rual JF, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, et al. (2005) Towards a proteome-scale map of the human protein-protein interaction network. Nature 437: 1173-1178.
Howell BW, Lanier LM, Frank R, Gertler FB, Cooper JA, (1999) The disabled 1 phosphotyrosine-binding domain binds to the internalization signals of transmembrane glycoproteins and to phospholipids. Mol Cell Biol 19: 5179-5188.
Buchse T, Horras N, Lenfert E, Krystal G, Korbel S, et al. (2011) CIN85 interacting proteins in B cells-specific role for SHIP-1. Mol Cell Proteomics 10: M110 006239.
Huang Y, Rich RL, Myszka DG, Wu H, (2003) Requirement of both the second and third BIR domains for the relief of X-linked inhibitor of apoptosis protein (XIAP)-mediated caspase inhibition by Smac. J Biol Chem 278: 49517-49522.
Riedl SJ, Renatus M, Schwarzenbacher R, Zhou Q, Sun C, et al. (2001) Structural basis for the inhibition of caspase-3 by XIAP. Cell 104: 791-800.
Suzuki Y, Nakabayashi Y, Takahashi R, (2001) Ubiquitin-protein ligase activity of X-linked inhibitor of apoptosis protein promotes proteasomal degradation of caspase-3 and enhances its anti-apoptotic effect in Fas-induced cell death. Proc Natl Acad Sci U S A 98: 8662-8667.
Lecine P, Esmiol S, Metais JY, Nicoletti C, Nourry C, et al. (2007) The NOD2-RICK complex signals from the plasma membrane. J Biol Chem 282: 15197-15207.
Kufer TA, Kremmer E, Adam AC, Philpott DJ, Sansonetti PJ, (2008) The pattern-recognition molecule Nod1 is localized at the plasma membrane at sites of bacterial interaction. Cell Microbiol 10: 477-486.
Kerr WG, Park MY, Maubert M, Engelman RW, (2011) SHIP deficiency causes Crohn's disease-like ileitis. Gut 60: 177-188.
McLarren KW, Cole AE, Weisser SB, Voglmaier NS, Conlin VS, et al. (2011) SHIP-deficient mice develop spontaneous intestinal inflammation and arginase-dependent fibrosis. Am J Pathol 179: 180-188.
Netea MG, Ferwerda G, de Jong DJ, Jansen T, Jacobs L, et al. (2005) Nucleotide-binding oligomerization domain-2 modulates specific TLR pathways for the induction of cytokine release. J Immunol 174: 6518-6523.
Wehkamp J, Harder J, Weichenthal M, Schwab M, Schaffeler E, et al. (2004) NOD2 (CARD15) mutations in Crohn's disease are associated with diminished mucosal alpha-defensin expression. Gut 53: 1658-1664.
Prakash H, Albrecht M, Becker D, Kuhlmann T, Rudel T, (2010) Deficiency of XIAP leads to sensitization for Chlamydophila pneumoniae pulmonary infection and dysregulation of innate immune response in mice. J Biol Chem 285: 20291-20302.
Zurek B, Proell M, Wagner RN, Schwarzenbacher R, Kufer TA, (2012) Mutational analysis of human NOD1 and NOD2 NACHT domains reveals different modes of activation. Innate Immun 18: 100-111.
Kufer TA, Kremmer E, Banks DJ, Philpott DJ, (2006) Role for erbin in bacterial activation of Nod2. Infect Immun 74: 3115-3124.
Damen JE, Ware MD, Kalesnikoff J, Hughes MR, Krystal G, (2001) SHIP's C-terminus is essential for its hydrolysis of PIP3 and inhibition of mast cell degranulation. Blood 97: 1343-1351.
Aman MJ, Walk SF, March ME, Su HP, Carver DJ, et al. (2000) Essential role for the C-terminal noncatalytic region of SHIP in FcgammaRIIB1-mediated inhibitory signaling. Mol Cell Biol 20: 3576-3589.
Frecha C, Costa C, Levy C, Negre D, Russell SJ, et al. (2009) Efficient and stable transduction of resting B lymphocytes and primary chronic lymphocyte leukemia cells using measles virus gp displaying lentiviral vectors. Blood 114: 3173-3180.