Pellino3 ubiquitinates RIP2 and mediates Nod2-induced signaling and protective effects in colitis

Nature Immunology

Volumn 14, Issue 9, 2013, Pages 927-936

  Yang, Shuo ^a   Wang, Bingwei ^a   Humphries, Fiachra ^a   Jackson, Ruaidhri ^a   Healy, Marc E ^a   Bergin, Ronan ^a   Aviello, Gabriella ^b   Hall, Barry ^c   McNamara, Deirdre ^c   Darby, Trevor ^d   Quinlan, Aoife ^d   Shanahan, Fergus ^d   Melgar, Silvia ^d   Fallon, Padraic G ^b,e,f   Moynagh, Paul N ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

^c ADELAIDE AND MEATH HOSPITAL   (Ireland)

^d UNIVERSITY COLLEGE CORK   (Ireland)

^e TRINITY COLLEGE DUBLIN   (Ireland)

^f OUR LADY S CHILDREN S HOSPITAL   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; CYTOKINE; I KAPPA B; MITOGEN ACTIVATED PROTEIN KINASE; PELLINO3; PROTEIN KINASE; RIP2 PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATALYSIS; COLITIS; CONTROLLED STUDY; CROHN DISEASE; DISEASE EXACERBATION; EMBRYO; ENTERITIS; ENZYME ACTIVATION; GENE MUTATION; INTERFERON INDUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; SIGNAL TRANSDUCTION; UBIQUITINATION;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CITROBACTER RODENTIUM; COLITIS; CROHN DISEASE; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; HUMANS; MALE; MICE; MICE, KNOCKOUT; MIDDLE AGED; NOD2 SIGNALING ADAPTOR PROTEIN; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; YOUNG ADULT;

EID: 84883196771     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2669     Document Type: Article

References (50)

1. Newton, K. & Dixit, V.M. Signaling in innate immunity and inflammation. Cold Spring Harb. Perspect. Biol. 4, 1-19 (2012).
2. Kawai, T. & Akira, S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34, 637-650 (2011).
3. Rubino, S.J., Selvanantham, T., Girardin, S.E. & Philpott, D.J. Nod-like receptors in the control of intestinal inflammation. Curr. Opin. Immunol. 24, 398-404 (2012).
4. Hugot, J.P. et al. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411, 599-603 (2001).
5. Ogura, Y. et al. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411, 603-606 (2001).
6. Hampe, J. et al. Association between insertion mutation in NOD2 gene and Crohn's disease in German and British populations. Lancet 357, 1925-1928 (2001).
7. Miceli-Richard, C. et al. CARD15 mutations in Blau syndrome. Nat. Genet. 29, 19-20 (2001).
8. Kanazawa, N. et al. Early-onset sarcoidosis and CARD15 mutations with constitutive nuclear factor-kappaB activation: common genetic etiology with Blau syndrome. Blood 105, 1195-1197 (2005).
9. Inohara, N. et al. Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J. Biol. Chem. 278, 5509-5512 (2003).
10. Girardin, S.E. et al. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem. 278, 8869-8872 (2003).
11. Tanabe, T. et al. Regulatory regions and critical residues of NOD2 involved in muramyl dipeptide recognition. EMBO J. 23, 1587-1597 (2004).
12. Abbott, D.W., Wilkins, A., Asara, J.M. & Cantley, L.C. The Crohn's disease protein, NOD2, requires RIP2 in order to induce ubiquitinylation of a novel site on NEMO. Curr. Biol. 14, 2217-2227 (2004).
13. Ogura, Y. et al. Nod2, a Nod1/Apaf-1 family member that is restricted to monocytes and activates NF-B. J. Biol. Chem. 276, 4812-4818 (2001).
14. Abbott, D.W. et al. Coordinated regulation of Toll-like receptor and NOD2 signaling by K63-linked polyubiquitin chains. Mol. Cell Biol. 27, 6012-6025 (2007).
15. Yang, Y. et al. NOD2 pathway activation by MDP or Mycobacterium tuberculosis infection involves the stable polyubiquitination of Rip2. J. Biol. Chem. 282, 36223-36229 (2007).
16. Hasegawa, M. et al. A critical role of RICK/RIP2 polyubiquitination in Nod-induced NF-B activation. EMBO J. 27, 373-383 (2008).
17. McCarthy, J.V., Ni, J. & Dixit, V.M. RIP2 is a novel NF-B-activating and cell death-inducing kinase. J. Biol. Chem. 273, 16968-16975 (1998).
18. Windheim, M., Lang, C., Peggie, M., Plater, L.A. & Cohen, P. Molecular mechanisms involved in the regulation of cytokine production by muramyl dipeptide. Biochem. J. 404, 179-190 (2007).
19. Kanayama, A. et al. TAB2 and TAB3 activate the NF-B pathway through binding to polyubiquitin chains. Mol. Cell 15, 535-548 (2004).
20. Moynagh, P.N. TLR signalling and activation of IRFs: revisiting old friends from the NF-kappaB pathway. Trends Immunol. 26, 469-476 (2005).
21. Traenckner, E.B. et al. Phosphorylation of human IB-on serines 32 and 36 controls IB-proteolysis and NF-B activation in response to diverse stimuli. EMBO J. 14, 2876-2883 (1995).
22. Moynagh, P.N. The NF-B pathway. J. Cell Sci. 118, 4589-4592 (2005).
23. Damgaard, R.B. et al. The ubiquitin ligase XIAP recruits LUBAC for NOD2 signaling in inflammation and innate immunity. Mol. Cell 46, 746-758 (2012).
24. Bertrand, M.J. et al. 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 (2009).
25. Tao, M. et al. ITCH K63-ubiquitinates the NOD2 binding protein, RIP2, to influence inflammatory signaling pathways. Curr. Biol. 19, 1255-1263 (2009).
26. Moynagh, P.N. The Pellino family: IRAK E3 ligases with emerging roles in innate immune signalling. Trends Immunol. 30, 33-42 (2009).
27. Schauvliege, R., Janssens, S. & Beyaert, R. Pellino proteins: novel players in TLR and IL-1R signalling. J. Cell Mol. Med. 11, 453-461 (2007).
28. Lin, C.C., Huoh, Y.S., Schmitz, K.R., Jensen, L.E. & Ferguson, K.M. Pellino proteins contain a cryptic FHA domain that mediates interaction with phosphorylated IRAK1. Structure 16, 1806-1816 (2008).
29. Schauvliege, R., Janssens, S. & Beyaert, R. Pellino proteins are more than scaffold proteins in TLR/IL-1R signalling: a role as novel RING E3-ubiquitin-ligases. FEBS Lett. 580, 4697-4702 (2006).
30. Butler, M.P., Hanly, J.A. & Moynagh, P.N. Kinase-active interleukin-1 receptor-associated kinases promote polyubiquitination and degradation of the Pellino family: direct evidence for PELLINO proteins being ubiquitin-protein isopeptide ligases. J. Biol. Chem. 282, 29729-29737 (2007).
31. Ordureau, A. et al. The IRAK-catalysed activation of the E3 ligase function of Pellino isoforms induces the Lys63-linked polyubiquitination of IRAK1. Biochem. J. 409, 43-52 (2008).
32. Smith, H. et al. Identification of the phosphorylation sites on the E3 ubiquitin ligase Pellino that are critical for activation by IRAK1 and IRAK4. Proc. Natl. Acad. Sci. USA 106, 4584-4590 (2009).
33. Smith, H. et al. The role of TBK1 and IKK in the expression and activation of Pellino 1. Biochem. J. 434, 537-548 (2011).
34. Goh, E.T. et al. Identification of the protein kinases that activate the E3 ubiquitin ligase Pellino 1 in the innate immune system. Biochem. J. 441, 339-346 (2012).
35. Strelow, A., Kollewe, C. & Wesche, H. Characterization of Pellino2, a substrate of IRAK1 and IRAK4. FEBS Lett. 547, 157-161 (2003).
36. Chang, M., Jin, W. & Sun, S.C. Peli1 facilitates TRIF-dependent Toll-like receptor signaling and proinflammatory cytokine production. Nat. Immunol. 10, 1089-1095 (2009).
37. Chang, M. et al. The ubiquitin ligase Peli1 negatively regulates T cell activation and prevents autoimmunity. Nat. Immunol. 12, 1002-1009 (2011).
38. Moynagh, P.N. Peli1 (rel)ieves autoimmunity. Nat. Immunol. 12, 927-929 (2011).
39. Siednienko, J. et al. Pellino3 targets the IRF7 pathway and facilitates autoregulation of TLR3-and viral-induced expression of type I interferons. Nat. Immunol. 13, 1055-1062 (2012).
40. Kim, Y.G. et al. The Nod2 sensor promotes intestinal pathogen eradication via the chemokine CCL2-dependent recruitment of inflammatory monocytes. Immunity 34, 769-780 (2011).
41. Murphy, C.T. et al. The sphingosine-1-phosphate analogue FTY720 impairs mucosal immunity and clearance of the enteric pathogen Citrobacter rodentium. Infect. Immun. 80, 2712-2723 (2012).
42. Watanabe, T. et al. Muramyl dipeptide activation of nucleotide-binding oligomerization domain 2 protects mice from experimental colitis. J. Clin. Invest. 118, 545-559 (2008).
43. Hitotsumatsu, O. et al. The ubiquitin-editing enzyme A20 restricts nucleotide-binding oligomerization domain containing 2-triggered signals. Immunity 28, 381-390 (2008).
44. Inohara, N., del Peso, L., Koseki, T., Chen, S. & Nunez, G. RICK, a novel protein kinase containing a caspase recruitment domain, interacts with CLARP and regulates CD95-mediated apoptosis. J. Biol. Chem. 273, 12296-12300 (1998).
45. Bertrand, M.J. et al. cIAP1/2 are direct E3 ligases conjugating diverse types of ubiquitin chains to receptor interacting proteins kinases 1 to 4 (RIP1-4). PLoS ONE 6, e22356 (2011).
46. Haas, T.L. et al. Recruitment of the linear ubiquitin chain assembly complex stabilizes the TNF-R1 signaling complex and is required for TNF-mediated gene induction. Mol. Cell 36, 831-844 (2009).
47. Geddes, K. et al. Identification of an innate T helper type 17 response to intestinal bacterial pathogens. Nat. Med. 17, 837-844 (2011).
48. Smith, P. et al. Infection with a helminth parasite prevents experimental colitis via a macrophage-mediated mechanism. J. Immunol. 178, 4557-4566 (2007).
49. Wirtz, S., Neufert, C., Weigmann, B. & Neurath, M.F. Chemically induced mouse models of intestinal inflammation. Nat. Protoc. 2, 541-546 (2007).
50. Hall, L.J. et al. Natural killer cells protect mice from DSS-induced colitis by regulating neutrophil function via the NKG2A receptor. Mucosal Immunol. advance online publication, doi:10.1038/mi.2012.140 (23 January 2013).