CYLD Limits Lys63- and Met1-Linked Ubiquitin at Receptor Complexes to Regulate Innate Immune Signaling

Cell Reports

Volumn 14, Issue 12, 2016, Pages 2846-2858

  Hrdinka, Matous ^a   Fiil, Berthe Katrine ^a   Zucca, Mattia ^a   Leske, Derek ^a   Bagola, Katrin ^a   Yabal, Monica ^b   Elliott, Paul R ^c   Damgaard, Rune Busk ^a,c   Komander, David ^c   Jost, Philipp J ^b   Gyrd Hansen, Mads ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; DEUBIQUITINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; LINEAR UBIQUITIN ASSEMBLY COMPLEX; LYSINE; METHIONINE; PROTEIN CYLD; PROTEIN HOIP; PROTEIN KINASE; RECEPTOR INTERACTING PROTEIN KINASE 2; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; CYTOKINE; PROTEINASE; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE 2; RIPK2 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ARTICLE; CATALYSIS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FLOW CYTOMETRY; HCT116 CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INNATE IMMUNITY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; U2OS CELL LINE; UBIQUITINATION; ANTAGONISTS AND INHIBITORS; CHEMISTRY; ENZYME ACTIVE SITE; GENETICS; HEK293 CELL LINE; METABOLISM; RNA INTERFERENCE; SITE DIRECTED MUTAGENESIS; TUMOR CELL LINE;

CATALYTIC DOMAIN; CELL LINE, TUMOR; CYTOKINES; DEUBIQUITINATING ENZYMES; ENDOPEPTIDASES; HEK293 CELLS; HUMANS; IMMUNITY, INNATE; LYSINE; METHIONINE; MUTAGENESIS, SITE-DIRECTED; NF-KAPPA B; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASE 2; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84961225981     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.02.062     Document Type: Article

References (51)

1. 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. 2004, 14:2217-2227.
2. Bauler L.D., Duckett C.S., O'Riordan M.X. XIAP regulates cytosol-specific innate immunity to Listeria infection. PLoS Pathog. 2008, 4:e1000142.
3. Bertrand M.J., Doiron K., Labbé K., Korneluk R.G., Barker P.A., Saleh M. Cellular inhibitors of apoptosis cIAP1 and cIAP2 are required for innate immunity signaling by the pattern recognition receptors NOD1 and NOD2. Immunity 2009, 30:789-801.
4. Bignell G.R., Warren W., Seal S., Takahashi M., Rapley E., Barfoot R., Green H., Brown C., Biggs P.J., Lakhani S.R., et al. Identification of the familial cylindromatosis tumour-suppressor gene. Nat. Genet. 2000, 25:160-165.
5. Boisson B., Laplantine E., Prando C., Giliani S., Israelsson E., Xu Z., Abhyankar A., Israël L., Trevejo-Nunez G., Bogunovic D., et al. Immunodeficiency, autoinflammation and amylopectinosis in humans with inherited HOIL-1 and LUBAC deficiency. Nat. Immunol. 2012, 13:1178-1186.
6. Boisson B., Laplantine E., Dobbs K., Cobat A., Tarantino N., Hazen M., Lidov H.G., Hopkins G., Du L., Belkadi A., et al. Human HOIP and LUBAC deficiency underlies autoinflammation, immunodeficiency, amylopectinosis, and lymphangiectasia. J. Exp. Med. 2015, 212:939-951.
7. Brummelkamp T.R., Nijman S.M., Dirac A.M., Bernards R. Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-kappaB. Nature 2003, 424:797-801.
8. Damgaard R.B., Nachbur U., Yabal M., Wong W.W., Fiil B.K., Kastirr M., Rieser E., Rickard J.A., Bankovacki A., Peschel C., et al. The ubiquitin ligase XIAP recruits LUBAC for NOD2 signaling in inflammation and innate immunity. Mol. Cell 2012, 46:746-758.
9. Damgaard R.B., Fiil B.K., Speckmann C., Yabal M., zur Stadt U., Bekker-Jensen S., Jost P.J., Ehl S., Mailand N., Gyrd-Hansen M. Disease-causing mutations in the XIAP BIR2 domain impair NOD2-dependent immune signalling. EMBO Mol. Med. 2013, 5:1278-1295.
10. Deng L., Wang C., Spencer E., Yang L., Braun A., You J., Slaughter C., Pickart C., Chen Z.J. Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 2000, 103:351-361.
11. Draber P., Kupka S., Reichert M., Draberova H., Lafont E., de Miguel D., Spilgies L., Surinova S., Taraborrelli L., Hartwig T., et al. LUBAC-recruited CYLD and A20 regulate gene activation and cell death by exerting opposing effects on linear ubiquitin in signaling complexes. Cell Rep. 2015, 13:2258-2272.
12. Elliott P.R., Nielsen S.V., Marco-Casanova P., Fiil B.K., Keusekotten K., Mailand N., Freund S.M., Gyrd-Hansen M., Komander D. Molecular basis and regulation of OTULIN-LUBAC interaction. Mol. Cell 2014, 54:335-348.
13. Emmerich C.H., Ordureau A., Strickson S., Arthur J.S., Pedrioli P.G., Komander D., Cohen P. Activation of the canonical IKK complex by K63/M1-linked hybrid ubiquitin chains. Proc. Natl. Acad. Sci. USA 2013, 110:15247-15252.
14. Fiil B.K., Gyrd-Hansen M. Met1-linked ubiquitination in immune signalling. FEBS J. 2014, 281:4337-4350.
15. Fiil B.K., Damgaard R.B., Wagner S.A., Keusekotten K., Fritsch M., Bekker-Jensen S., Mailand N., Choudhary C., Komander D., Gyrd-Hansen M. OTULIN restricts Met1-linked ubiquitination to control innate immune signaling. Mol. Cell 2013, 50:818-830.
16. Gerlach B., Cordier S.M., Schmukle A.C., Emmerich C.H., Rieser E., Haas T.L., Webb A.I., Rickard J.A., Anderton H., Wong W.W., et al. Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 2011, 471:591-596.
17. Haas T.L., Emmerich C.H., Gerlach B., Schmukle A.C., Cordier S.M., Rieser E., Feltham R., Vince J., Warnken U., Wenger T., 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 2009, 36:831-844.
18. Harhaj E.W., Dixit V.M. Regulation of NF-κB by deubiquitinases. Immunol. Rev. 2012, 246:107-124.
19. Hasegawa M., Fujimoto Y., Lucas P.C., Nakano H., Fukase K., Núñez G., Inohara N. A critical role of RICK/RIP2 polyubiquitination in Nod-induced NF-kappaB activation. EMBO J. 2008, 27:373-383.
20. Hospenthal M.K., Mevissen T.E., Komander D. Deubiquitinase-based analysis of ubiquitin chain architecture using Ubiquitin Chain Restriction (UbiCRest). Nat. Protoc. 2015, 10:349-361.
21. Ikeda F., Deribe Y.L., Skånland S.S., Stieglitz B., Grabbe C., Franz-Wachtel M., van Wijk S.J., Goswami P., Nagy V., Terzic J., et al. SHARPIN forms a linear ubiquitin ligase complex regulating NF-κB activity and apoptosis. Nature 2011, 471:637-641.
22. Jiang X., Chen Z.J. The role of ubiquitylation in immune defence and pathogen evasion. Nat. Rev. Immunol. 2012, 12:35-48.
23. Jono H., Lim J.H., Chen L.F., Xu H., Trompouki E., Pan Z.K., Mosialos G., Li J.D. NF-kappaB is essential for induction of CYLD, the negative regulator of NF-kappaB: evidence for a novel inducible autoregulatory feedback pathway. J. Biol. Chem. 2004, 279:36171-36174.
24. Keusekotten K., Elliott P.R., Glockner L., Fiil B.K., Damgaard R.B., Kulathu Y., Wauer T., Hospenthal M.K., Gyrd-Hansen M., Krappmann D., et al. OTULIN antagonizes LUBAC signaling by specifically hydrolyzing Met1-linked polyubiquitin. Cell 2013, 153:1312-1326.
25. Kim Y.G., Park J.H., Shaw M.H., Franchi L., Inohara N., Núñez G. The cytosolic sensors Nod1 and Nod2 are critical for bacterial recognition and host defense after exposure to Toll-like receptor ligands. Immunity 2008, 28:246-257.
26. Kirisako T., Kamei K., Murata S., Kato M., Fukumoto H., Kanie M., Sano S., Tokunaga F., Tanaka K., Iwai K. A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J. 2006, 25:4877-4887.
27. Komander D., Reyes-Turcu F., Licchesi J.D., Odenwaelder P., Wilkinson K.D., Barford D. Molecular discrimination of structurally equivalent Lys 63-linked and linear polyubiquitin chains. EMBO Rep. 2009, 10:466-473.
28. Kovalenko A., Chable-Bessia C., Cantarella G., Israël A., Wallach D., Courtois G. The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature 2003, 424:801-805.
29. Lee E.G., Boone D.L., Chai S., Libby S.L., Chien M., Lodolce J.P., Ma A. Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science 2000, 289:2350-2354.
30. Michel M.A., Elliott P.R., Swatek K.N., Simicek M., Pruneda J.N., Wagstaff J.L., Freund S.M., Komander D. Assembly and specific recognition of K29- and K33-linked polyubiquitin. Mol. Cell 2015, 58:95-109.
31. Nishanth G., Deckert M., Wex K., Massoumi R., Schweitzer K., Naumann M., Schlüter D. CYLD enhances severe listeriosis by impairing IL-6/STAT3-dependent fibrin production. PLoS Pathog. 2013, 9:e1003455.
32. Ori D., Kato H., Sanjo H., Tartey S., Mino T., Akira S., Takeuchi O. Essential roles of K63-linked polyubiquitin-binding proteins TAB2 and TAB3 in B cell activation via MAPKs. J. Immunol. 2013, 190:4037-4045.
33. Philpott D.J., Sorbara M.T., Robertson S.J., Croitoru K., Girardin S.E. NOD proteins: regulators of inflammation in health and disease. Nat. Rev. Immunol. 2014, 14:9-23.
34. Rahighi S., Ikeda F., Kawasaki M., Akutsu M., Suzuki N., Kato R., Kensche T., Uejima T., Bloor S., Komander D., et al. Specific recognition of linear ubiquitin chains by NEMO is important for NF-kappaB activation. Cell 2009, 136:1098-1109.
35. Ritorto M.S., Ewan R., Perez-Oliva A.B., Knebel A., Buhrlage S.J., Wightman M., Kelly S.M., Wood N.T., Virdee S., Gray N.S., et al. Screening of DUB activity and specificity by MALDI-TOF mass spectrometry. Nat. Commun. 2014, 5:4763.
36. Rivkin E., Almeida S.M., Ceccarelli D.F., Juang Y.C., MacLean T.A., Srikumar T., Huang H., Dunham W.H., Fukumura R., Xie G., et al. The linear ubiquitin-specific deubiquitinase gumby regulates angiogenesis. Nature 2013, 498:318-324.
37. Sato Y., Goto E., Shibata Y., Kubota Y., Yamagata A., Goto-Ito S., Kubota K., Inoue J., Takekawa M., Tokunaga F., Fukai S. Structures of CYLD USP with Met1- or Lys63-linked diubiquitin reveal mechanisms for dual specificity. Nat. Struct. Mol. Biol. 2015, 22:222-229.
38. Schaeffer V., Akutsu M., Olma M.H., Gomes L.C., Kawasaki M., Dikic I. Binding of OTULIN to the PUB domain of HOIP controls NF-κB signaling. Mol. Cell 2014, 54:349-361.
39. Sims J.J., Scavone F., Cooper E.M., Kane L.A., Youle R.J., Boeke J.D., Cohen R.E. Polyubiquitin-sensor proteins reveal localization and linkage-type dependence of cellular ubiquitin signaling. Nat. Methods 2012, 9:303-309.
40. Takiuchi T., Nakagawa T., Tamiya H., Fujita H., Sasaki Y., Saeki Y., Takeda H., Sawasaki T., Buchberger A., Kimura T., et al. Suppression of LUBAC-mediated linear ubiquitination by a specific interaction between LUBAC and the deubiquitinases CYLD and OTULIN. Genes to Cells 2014, 19:254-272.
41. Tang J., Qu L.K., Zhang J., Wang W., Michaelson J.S., Degenhardt Y.Y., El-Deiry W.S., Yang X. Critical role for Daxx in regulating Mdm2. Nat. Cell Biol. 2006, 8:855-862.
42. Tao M., Scacheri P.C., Marinis J.M., Harhaj E.W., Matesic L.E., Abbott D.W. ITCH K63-ubiquitinates the NOD2 binding protein, RIP2, to influence inflammatory signaling pathways. Curr. Biol. 2009, 19:1255-1263.
43. Thorslund T., Ripplinger A., Hoffmann S., Wild T., Uckelmann M., Villumsen B., Narita T., Sixma T.K., Choudhary C., Bekker-Jensen S., Mailand N. Histone H1 couples initiation and amplification of ubiquitin signalling after DNA damage. Nature 2015, 527:389-393.
44. Tokunaga F., Nakagawa T., Nakahara M., Saeki Y., Taniguchi M., Sakata S., Tanaka K., Nakano H., Iwai K. SHARPIN is a component of the NF-κB-activating linear ubiquitin chain assembly complex. Nature 2011, 471:633-636.
45. Trompouki E., Hatzivassiliou E., Tsichritzis T., Farmer H., Ashworth A., Mosialos G. CYLD is a deubiquitinating enzyme that negatively regulates NF-kappaB activation by TNFR family members. Nature 2003, 424:793-796.
46. van Wijk S.J., Fiskin E., Putyrski M., Pampaloni F., Hou J., Wild P., Kensche T., Grecco H.E., Bastiaens P., Dikic I. Fluorescence-based sensors to monitor localization and functions of linear and K63-linked ubiquitin chains in cells. Mol. Cell 2012, 47:797-809.
47. Warner N., Burberry A., Franchi L., Kim Y.G., McDonald C., Sartor M.A., Núñez G. A genome-wide siRNA screen reveals positive and negative regulators of the NOD2 and NF-κB signaling pathways. Sci. Signal. 2013, 6:rs3.
48. Watanabe T., Asano N., Meng G., Yamashita K., Arai Y., Sakurai T., Kudo M., Fuss I.J., Kitani A., Shimosegawa T., et al. NOD2 downregulates colonic inflammation by IRF4-mediated inhibition of K63-linked polyubiquitination of RICK and TRAF6. Mucosal Immunol. 2014, 7:1312-1325.
49. Wertz I.E., O'Rourke K.M., Zhou H., Eby M., Aravind L., Seshagiri S., Wu P., Wiesmann C., Baker R., Boone D.L., et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 2004, 430:694-699.
50. Xu M., Skaug B., Zeng W., Chen Z.J. A ubiquitin replacement strategy in human cells reveals distinct mechanisms of IKK activation by TNFalpha and IL-1beta. Mol. Cell 2009, 36:302-314.
51. Yang S., Wang B., Humphries F., Jackson R., Healy M.E., Bergin R., Aviello G., Hall B., McNamara D., Darby T., et al. Pellino3 ubiquitinates RIP2 and mediates Nod2-induced signaling and protective effects in colitis. Nat. Immunol. 2013, 14:927-936.