The Deubiquitinase OTULIN Is an Essential Negative Regulator of Inflammation and Autoimmunity

Cell

Volumn 166, Issue 5, 2016, Pages 1215-1230.e20

  Damgaard, Rune Busk ^a   Walker, Jennifer A ^a   Marco Casanova, Paola ^a   Morgan, Neil V ^b   Titheradge, Hannah L ^b,c   Elliott, Paul R ^a   McHale, Duncan ^d   Maher, Eamonn R ^e   McKenzie, Andrew N J ^a   Komander, David ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c BIRMINGHAM CHILDREN S HOSPITAL NHS FOUNDATION TRUST   (United Kingdom)

^d UCB PHARMA   (Belgium)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; DEUBIQUITINASE; DEUBIQUITINASE OTULIN; GENOMIC DNA; GRANULOCYTE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; METHIONINE; METHIONINE 1; POLYUBIQUITIN; UNCLASSIFIED DRUG; GUMBY PROTEIN, HUMAN; INFLIXIMAB; NEUTRALIZING ANTIBODY; PROTEINASE; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; AUTOINFLAMMATORY DISEASE; BLOOD SAMPLING; BONE MARROW DERIVED MACROPHAGE; CELL SELECTION; CIRCULAR DICHROISM; COMPARATIVE STUDY; CONTROLLED STUDY; DNA SEQUENCE; DOWN REGULATION; EMBRYO; FLOW CYTOMETRY; GENETIC ANALYSIS; GENETIC LINKAGE; GERMLINE MUTATION; GRANULOPOIESIS; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOCOMPETENT CELL; IN VIVO STUDY; INFLAMMATORY DISEASE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UBIQUITINATION; ANIMAL; ANTAGONISTS AND INHIBITORS; AUTOIMMUNE DISEASES; B LYMPHOCYTE; BONE MARROW CELL; DISEASE MODEL; GENE DELETION; GENETICS; IMMUNOLOGY; INFLAMMATION; METABOLISM; MUTANT MOUSE STRAIN; SYNDROME; T LYMPHOCYTE;

ANIMALS; ANTIBODIES, NEUTRALIZING; AUTOIMMUNE DISEASES; AUTOIMMUNITY; B-LYMPHOCYTES; CYTOKINES; DEUBIQUITINATING ENZYMES; DISEASE MODELS, ANIMAL; ENDOPEPTIDASES; GERM-LINE MUTATION; HUMANS; INFLAMMATION; INFLIXIMAB; METHIONINE; MICE; MICE, MUTANT STRAINS; MYELOID CELLS; POLYUBIQUITIN; SEQUENCE DELETION; SYNDROME; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84981719187     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.07.019     Document Type: Article

References (44)

1. 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. 13 (2012), 1178–1186.
2. Boisson, B., Laplantine, E., Dobbs, K., Cobat, A., Tarantino, N., Hazen, M., Lidov, H.G.W., Hopkins, G., Du, L., Belkadi, A., et al. Human HOIP and LUBAC deficiency underlies autoinflammation, immunodeficiency, amylopectinosis, and lymphangiectasia. J. Exp. Med. 212 (2015), 939–951.
3. Bonizzi, G., Karin, M., The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 25 (2004), 280–288.
4. Clark, G.R., Sciacovelli, M., Gaude, E., Walsh, D.M., Kirby, G., Simpson, M.A., Trembath, R.C., Berg, J.N., Woodward, E.R., Kinning, E., et al. Germline FH mutations presenting with pheochromocytoma. J. Clin. Endocrinol. Metab. 99 (2014), E2046–E2050.
5. Clausen, B.E., Burkhardt, C., Reith, W., Renkawitz, R., Förster, I., Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8 (1999), 265–277.
6. Damgaard, R.B., Nachbur, U., Yabal, M., Wong, W.W.-L., 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 46 (2012), 746–758.
7. 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. 5 (2013), 1278–1295.
8. 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. 13 (2015), 2258–2272.
9. Elliott, P.R., Nielsen, S.V., Marco-Casanova, P., Fiil, B.K., Keusekotten, K., Mailand, N., Freund, S.M.V., Gyrd-Hansen, M., Komander, D., Molecular basis and regulation of OTULIN-LUBAC interaction. Mol. Cell 54 (2014), 335–348.
10. Emmerich, C.H., Ordureau, A., Strickson, S., Arthur, J.S.C., Pedrioli, P.G.A., Komander, D., Cohen, P., Activation of the canonical IKK complex by K63/M1-linked hybrid ubiquitin chains. Proc. Natl. Acad. Sci. USA 110 (2013), 15247–15252.
11. Fiil, B.K., Gyrd-Hansen, M., Met1-linked ubiquitination in immune signalling. FEBS J. 281 (2014), 4337–4350.
12. 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 50 (2013), 818–830.
13. 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.-L., et al. Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 471 (2011), 591–596.
14. Groom, J.R., Fletcher, C.A., Walters, S.N., Grey, S.T., Watt, S.V., Sweet, M.J., Smyth, M.J., Mackay, C.R., Mackay, F., BAFF and MyD88 signals promote a lupuslike disease independent of T cells. J. Exp. Med. 204 (2007), 1959–1971.
15. Hameyer, D., Loonstra, A., Eshkind, L., Schmitt, S., Antunes, C., Groen, A., Bindels, E., Jonkers, J., Krimpenfort, P., Meuwissen, R., et al. Toxicity of ligand-dependent Cre recombinases and generation of a conditional Cre deleter mouse allowing mosaic recombination in peripheral tissues. Physiol. Genomics 31 (2007), 32–41.
16. Harhaj, E.W., Dixit, V.M., Regulation of NF-κB by deubiquitinases. Immunol. Rev. 246 (2012), 107–124.
17. Hobeika, E., Thiemann, S., Storch, B., Jumaa, H., Nielsen, P.J., Pelanda, R., Reth, M., Testing gene function early in the B cell lineage in mb1-cre mice. Proc. Natl. Acad. Sci. USA 103 (2006), 13789–13794.
18. Hrdinka, M., Fiil, B.K., Zucca, M., Leske, D., Bagola, K., Yabal, M., Elliott, P.R., Damgaard, R.B., Komander, D., Jost, P.J., Gyrd-Hansen, M., CYLD Limits Lys63- and Met1-Linked Ubiquitin at Receptor Complexes to Regulate Innate Immune Signaling. Cell Rep. 14 (2016), 2846–2858.
19. Ikeda, F., Deribe, Y.L., Skånland, S.S., Stieglitz, B., Grabbe, C., Franz-Wachtel, M., van Wijk, S.J.L., Goswami, P., Nagy, V., Terzic, J., et al. SHARPIN forms a linear ubiquitin ligase complex regulating NF-κB activity and apoptosis. Nature 471 (2011), 637–641.
20. Iwai, K., Fujita, H., Sasaki, Y., Linear ubiquitin chains: NF-κB signalling, cell death and beyond. Nat. Rev. Mol. Cell Biol. 15 (2014), 503–508.
21. Jiang, X., Chen, Z.J., The role of ubiquitylation in immune defence and pathogen evasion. Nat. Rev. Immunol. 12 (2012), 35–48.
22. 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 153 (2013), 1312–1326.
23. Komander, D., Rape, M., The ubiquitin code. Annu. Rev. Biochem. 81 (2012), 203–229.
24. Kumari, S., Redouane, Y., López-Mosqueda, J., Shiraishi, R., Romanowska, M., Lutzmayer, S., Kuiper, J., Martinez, C., Dikic, I., Pasparakis, M., Ikeda, F., Sharpin prevents skin inflammation by inhibiting TNFR1-induced keratinocyte apoptosis. eLife, 3, 2014, 3.
25. Lee, P.P., Fitzpatrick, D.R., Beard, C., Jessup, H.K., Lehar, S., Makar, K.W., Pérez-Melgosa, M., Sweetser, M.T., Schlissel, M.S., Nguyen, S., et al. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15 (2001), 763–774.
26. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., 1000 Genome Project Data Processing Subgroup. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25 (2009), 2078–2079.
27. MacDuff, D.A., Reese, T.A., Kimmey, J.M., Weiss, L.A., Song, C., Zhang, X., Kambal, A., Duan, E., Carrero, J.A., Boisson, B., et al. Phenotypic complementation of genetic immunodeficiency by chronic herpesvirus infection. eLife, 4, 2015, 4.
28. Morley, J.E., Thomas, D.R., Wilson, M.-M.G., Cachexia: pathophysiology and clinical relevance. Am. J. Clin. Nutr. 83 (2006), 735–743.
29. Morrison, P.J., Bending, D., Fouser, L.A., Wright, J.F., Stockinger, B., Cooke, A., Kullberg, M.C., Th17-cell plasticity in Helicobacter hepaticus-induced intestinal inflammation. Mucosal Immunol. 6 (2013), 1143–1156.
30. Park, Y., Jin, H.-S., Lopez, J., Lee, J., Liao, L., Elly, C., Liu, Y.-C., SHARPIN controls regulatory T cells by negatively modulating the T cell antigen receptor complex. Nat. Immunol. 17 (2016), 286–296.
31. Peltzer, N., Rieser, E., Taraborrelli, L., Draber, P., Darding, M., Pernaute, B., Shimizu, Y., Sarr, A., Draberova, H., Montinaro, A., et al. HOIP deficiency causes embryonic lethality by aberrant TNFR1-mediated endothelial cell death. Cell Rep. 9 (2014), 153–165.
32. Redecke, V., Chaturvedi, V., Kuriakose, J., Häcker, H., SHARPIN controls the development of regulatory T cells. Immunology 148 (2016), 216–226.
33. Rickard, J.A., Anderton, H., Etemadi, N., Nachbur, U., Darding, M., Peltzer, N., Lalaoui, N., Lawlor, K.E., Vanyai, H., Hall, C., et al. TNFR1-dependent cell death drives inflammation in Sharpin-deficient mice. eLife, 3, 2014, 3.
34. 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 498 (2013), 318–324.
35. Rodríguez, C.I., Buchholz, F., Galloway, J., Sequerra, R., Kasper, J., Ayala, R., Stewart, A.F., Dymecki, S.M., High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat. Genet. 25 (2000), 139–140.
36. Sasaki, Y., Sano, S., Nakahara, M., Murata, S., Kometani, K., Aiba, Y., Sakamoto, S., Watanabe, Y., Tanaka, K., Kurosaki, T., Iwai, K., Defective immune responses in mice lacking LUBAC-mediated linear ubiquitination in B cells. EMBO J. 32 (2013), 2463–2476.
37. Satpathy, S., Wagner, S.A., Beli, P., Gupta, R., Kristiansen, T.A., Malinova, D., Francavilla, C., Tolar, P., Bishop, G.A., Hostager, B.S., Choudhary, C., Systems-wide analysis of BCR signalosomes and downstream phosphorylation and ubiquitylation. Mol. Syst. Biol., 11, 2015, 810.
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 54 (2014), 349–361.
39. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9 (2012), 676–682.
40. Seelow, D., Schuelke, M., Hildebrandt, F., Nürnberg, P., HomozygosityMapper—an interactive approach to homozygosity mapping. Nucleic Acids Res., 37, 2009 W593–W539.
41. Tokunaga, F., Sakata, S., Saeki, Y., Satomi, Y., Kirisako, T., Kamei, K., Nakagawa, T., Kato, M., Murata, S., Yamaoka, S., et al. Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation. Nat. Cell Biol. 11 (2009), 123–132.
42. 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 471 (2011), 633–636.
43. Yang, H., Wang, K., Genomic variant annotation and prioritization with ANNOVAR and wANNOVAR. Nat. Protoc. 10 (2015), 1556–1566.
44. Yang, Y., Kelly, P., Shaffer, A.L. 3rd, Schmitz, R., Yoo, H.M., Liu, X., Huang, W., Webster, D., Young, R.M., Nakagawa, M., et al. Targeting Non-proteolytic Protein Ubiquitination for the Treatment of Diffuse Large B Cell Lymphoma. Cancer Cell 29 (2016), 494–507.