Linear ubiquitination signals in adaptive immune responses

Immunological Reviews

Volumn 266, Issue 1, 2015, Pages 222-236

  Ikeda, Fumiyo ^a  

^a INSTITUTE OF MOLECULAR BIOTECHNOLOGY   (Austria)

Author keywords

Apoptosis; Linear ubiquitin chain; LUBAC; NEMO; NF B; TNF

Indexed keywords

DEUBIQUITINASE; HOIL 1L INTERACTING PROTEIN; I KAPPA B KINASE GAMMA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; INTERLEUKIN 1 RECEPTOR; LINEAR UBIQUITIN CHAIN ASSEMBLY COMPLEX; MITOGEN ACTIVATED PROTEIN KINASE; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN PROTEIN; PATTERN RECOGNITION RECEPTOR; POLYUBIQUITIN; PROTEIN A20; PROTEIN ABIN 1; PROTEIN OTULIN; PROTEIN SHARPIN; RIG I LIKE RECEPTOR; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN THIOLESTERASE; UNCLASSIFIED DRUG; GUMBY PROTEIN, HUMAN; I KAPPA B KINASE; IKBKG PROTEIN, HUMAN; MULTIPROTEIN COMPLEX; PROTEINASE; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK1 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

ADAPTIVE IMMUNITY; ARTICLE; CELL DEATH; GENE ACTIVATION; HUMAN; IMMUNE RESPONSE; IMMUNITY; INFLAMMATION; LINEAR UBIQUITINATION; MOLECULAR BIOLOGY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROCESSING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; UBIQUITINATION; ANIMAL; METABOLISM; MOUSE;

ADAPTIVE IMMUNITY; ANIMALS; ENDOPEPTIDASES; HUMANS; I-KAPPA B KINASE; MICE; MULTIPROTEIN COMPLEXES; NF-KAPPA B; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84931055813     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12300     Document Type: Article

References (109)

1. Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem 1998;67:425-479.
2. Ozkaynak E, Finley D, Varshavsky A. The yeast ubiquitin gene: head-to-tail repeats encoding a polyubiquitin precursor protein. Nature 1984;312:663-666.
3. Hershko A. Ubiquitin: roles in protein modification and breakdown. Cell 1983;34:11-12.
4. Kulathu Y, Komander D. Atypical ubiquitylation - the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat Rev Mol Cell Biol 2012;13:508-523.
5. Ikeda F, Dikic I. Atypical ubiquitin chains: new molecular signals. 'Protein Modifications: beyond the Usual Suspects' review series. EMBO Rep 2008;9:536-542.
6. Kirisako T, et al. A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J 2006;25:4877-4887.
7. Tokunaga F, et al. SHARPIN is a component of the NF-kappaB-activating linear ubiquitin chain assembly complex. Nature 2011;471:633-636.
8. Ikeda F, et al. SHARPIN forms a linear ubiquitin ligase complex regulating NF-kappaB activity and apoptosis. Nature 2011;471:637-641.
9. Gerlach B, et al. Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 2011;471:591-596.
10. Peng J, et al. A proteomics approach to understanding protein ubiquitination. Nat Biotechnol 2003;21:921-926.
11. Reyes-Turcu FE, Ventii KH, Wilkinson KD. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 2009;78:363-397.
12. Komander D, Clague MJ, Urbe S. Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 2009;10:550-563.
13. Nijman SM, et al. A genomic and functional inventory of deubiquitinating enzymes. Cell 2005;123:773-786.
14. Komander D, Rape M. The ubiquitin code. Annu Rev Biochem 2012;81:203-229.
15. Phu L, et al. Improved quantitative mass spectrometry methods for characterizing complex ubiquitin signals. Mol Cell Proteomics 2011;10:M110 003756.
16. Rahighi S, et al. Specific recognition of linear ubiquitin chains by NEMO is important for NF-kappaB activation. Cell 2009;136:1098-1109.
17. Tokunaga F, et al. Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation. Nat Cell Biol 2009;11:123-132.
18. Haas TL, 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.
19. Verhelst K, Carpentier I, Beyaert R. Regulation of TNF-induced NF-kappaB activation by different cytoplasmic ubiquitination events. Cytokine Growth Factor Rev 2011;22:277-286.
20. Bianchi K, Meier P. A tangled web of ubiquitin chains: breaking news in TNF-R1 signaling. Mol Cell 2009;36:736-742.
21. Li X, Yang Y, Ashwell JD. TNF-RII and c-IAP1 mediate ubiquitination and degradation of TRAF2. Nature 2002;416:345-347.
22. Emmerich CH, Schmukle AC, Walczak H. The emerging role of linear ubiquitination in cell signaling. Sci Signal 2011;4:re5.
23. Varfolomeev E, et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell 2007;131:669-681.
24. Xia ZP, Chen ZJ. TRAF2: a double-edged sword? Sci STKE 2005;2005:pe7.
25. Vucic D, Dixit VM, Wertz IE. Ubiquitylation in apoptosis: a post-translational modification at the edge of life and death. Nat Rev Mol Cell Biol 2011;12:439-452.
26. Dynek JN, et al. c-IAP1 and UbcH5 promote K11-linked polyubiquitination of RIP1 in TNF signalling. EMBO J 2010;29:4198-4209.
27. Xu M, Skaug B, Zeng W, Chen ZJ. A ubiquitin replacement strategy in human cells reveals distinct mechanisms of IKK activation by TNFalpha and IL-1beta. Mol Cell 2009;36:302-314.
28. Chen ZJ. Ubiquitination in signaling to and activation of IKK. Immunol Rev 2012;246:95-106.
29. Kulathu Y, Akutsu M, Bremm A, Hofmann K, Komander D. Two-sided ubiquitin binding explains specificity of the TAB 2 NZF domain. Nat Struct Mol Biol 2009;16:1328-1330.
30. Sato Y, Yoshikawa A, Yamashita M, Yamagata A, Fukai S. Structural basis for specific recognition of Lys 63-linked polyubiquitin chains by NZF domains of TAB 2 and TAB 3. EMBO J 2009;28:3903-3909.
31. Wagner S, et al. Ubiquitin binding mediates the NF-kappaB inhibitory potential of ABIN proteins. Oncogene 2008;27:3739-3745.
32. Lo YC, et al. Structural basis for recognition of diubiquitins by NEMO. Mol Cell 2009;33:602-615.
33. Harhaj EW, Dixit VM. Regulation of NF-kappaB by deubiquitinases. Immunol Rev 2012;246:107-124.
34. Fiil BK, Gyrd-Hansen M. Met1-linked ubiquitination in immune signalling. FEBS J 2014;281:4337-4350.
35. Wertz IE, et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 2004;430:694-699.
36. Catrysse L, Vereecke L, Beyaert R, van Loo G. A20 in inflammation and autoimmunity. Trends Immunol 2014;35:22-31.
37. Verhelst K, et al. A20 inhibits LUBAC-mediated NF-kappaB activation by binding linear polyubiquitin chains via its zinc finger 7. EMBO J 2012;31:3845-3855.
38. Tokunaga F, et al. Specific recognition of linear polyubiquitin by A20 zinc finger 7 is involved in NF-kappaB regulation. EMBO J 2012;31:3856-3870.
39. Komander D, Reyes-Turcu F, Licchesi JD, Odenwaelder P, Wilkinson KD, Barford D. Molecular discrimination of structurally equivalent Lys 63-linked and linear polyubiquitin chains. EMBO Rep 2009;10:466-473.
40. Takiuchi T, et al. Suppression of LUBAC-mediated linear ubiquitination by a specific interaction between LUBAC and the deubiquitinases CYLD and OTULIN. Genes Cells 2014;19:254-272.
41. Rivkin E, et al. The linear ubiquitin-specific deubiquitinase gumby regulates angiogenesis. Nature 2013;498:318-324.
42. Keusekotten K, et al. OTULIN antagonizes LUBAC signaling by specifically hydrolyzing Met1-linked polyubiquitin. Cell 2013;153:1312-1326.
43. Karin M, Gallagher E. TNFR signaling: ubiquitin-conjugated TRAFfic signals control stop-and-go for MAPK signaling complexes. Immunol Rev 2009;228:225-240.
44. Palombella VJ, Rando OJ, Goldberg AL, Maniatis T. The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B. Cell 1994;78:773-785.
45. Yaron A, et al. Identification of the receptor component of the IkappaBalpha-ubiquitin ligase. Nature 1998;396:590-594.
46. Kanarek N, Ben-Neriah Y. Regulation of NF-kappaB by ubiquitination and degradation of the IkappaBs. Immunol Rev 2012;246:77-94.
47. Wang C, Deng L, Hong M, Akkaraju GR, Inoue J, Chen ZJ. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 2001;412:346-351.
48. Kanayama A, et al. TAB 2 and TAB 3 activate the NF-kappaB pathway through binding to polyubiquitin chains. Mol Cell 2004;15:535-548.
49. Andersen PL, et al. Distinct regulation of Ubc13 functions by the two ubiquitin-conjugating enzyme variants Mms2 and Uev1A. J Cell Biol 2005;170:745-755.
50. Zhou H, et al. Bcl10 activates the NF-kappaB pathway through ubiquitination of NEMO. Nature 2004;427:167-171.
51. Yamamoto M, et al. Key function for the Ubc13 E2 ubiquitin-conjugating enzyme in immune receptor signaling. Nat Immunol 2006;7:962-970.
52. Buchberger A. From UBA to UBX: new words in the ubiquitin vocabulary. Trends Cell Biol 2002;12:216-221.
53. Randles L, Walters KJ. Ubiquitin and its binding domains. Front Biosci (Landmark Ed) 2012;17:2140-2157.
54. Dikic I, Wakatsuki S, Walters KJ. Ubiquitin-binding domains - from structures to functions. Nat Rev Mol Cell Biol 2009;10:659-671.
55. Raasi S, Varadan R, Fushman D, Pickart CM. Diverse polyubiquitin interaction properties of ubiquitin-associated domains. Nat Struct Mol Biol 2005;12:708-714.
56. Windheim M, Stafford M, Peggie M, Cohen P. Interleukin-1 (IL-1) induces the Lys63-linked polyubiquitination of IL-1 receptor-associated kinase 1 to facilitate NEMO binding and the activation of IkappaBalpha kinase. Mol Cell Biol 2008;28:1783-1791.
57. Wu CJ, Conze DB, Li T, Srinivasula SM, Ashwell JD. Sensing of Lys 63-linked polyubiquitination by NEMO is a key event in NF-kappaB activation [corrected]. Nat Cell Biol 2006;8:398-406.
58. Ea CK, Deng L, Xia ZP, Pineda G, Chen ZJ. Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol Cell 2006;22:245-257.
59. Heyninck K, Kreike MM, Beyaert R. Structure-function analysis of the A20-binding inhibitor of NF-kappa B activation, ABIN-1. FEBS Lett 2003;536:135-140.
60. Verstrepen L, Carpentier I, Verhelst K, Beyaert R. ABINs: A20 binding inhibitors of NF-kappa B and apoptosis signaling. Biochem Pharmacol 2009;78:105-114.
61. Ikeda F, Rahighi S, Wakatsuki S, Dikic I. Selective binding of linear ubiquitin chains to NEMO in NF-kappaB activation. Adv Exp Med Biol 2011;691:107-114.
62. Zhu G, Wu CJ, Zhao Y, Ashwell JD. Optineurin negatively regulates TNFalpha- induced NF-kappaB activation by competing with NEMO for ubiquitinated RIP. Curr Biol 2007;17:1438-1443.
63. Wild P, et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 2011;333:228-233.
64. Boyle KB, Randow F. The role of 'eat-me' signals and autophagy cargo receptors in innate immunity. Curr Opin Microbiol 2013;16:339-348.
65. Kensche T, Tokunaga F, Ikeda F, Goto E, Iwai K, Dikic I. Analysis of nuclear factor-kappaB (NF-kappaB) essential modulator (NEMO) binding to linear and lysine-linked ubiquitin chains and its role in the activation of NF-kappaB. J Biol Chem 2012;287:23626-23634.
66. Emmerich CH, et al. Activation of the canonical IKK complex by K63/M1-linked hybrid ubiquitin chains. Proc Natl Acad Sci USA 2013;110:15247-15252.
67. Tarantino N, et al. TNF and IL-1 exhibit distinct ubiquitin requirements for inducing NEMO-IKK supramolecular structures. J Cell Biol 2014;204:231-245.
68. Yoshikawa A, Sato Y, Yamashita M, Mimura H, Yamagata A, Fukai S. Crystal structure of the NEMO ubiquitin-binding domain in complex with Lys 63-linked di-ubiquitin. FEBS Lett 2009;583:3317-3322.
69. Filipe-Santos O, et al. X-linked susceptibility to mycobacteria is caused by mutations in NEMO impairing CD40-dependent IL-12 production. J Exp Med 2006;203:1745-1759.
70. Doffinger R, et al. X-linked anhidrotic ectodermal dysplasia with immunodeficiency is caused by impaired NF-kappaB signaling. Nat Genet 2001;27:277-285.
71. Hubeau M, et al. New mechanism of X-linked anhidrotic ectodermal dysplasia with immunodeficiency: impairment of ubiquitin binding despite normal folding of NEMO protein. Blood 2011;118:926-935.
72. Mattiroli F, Sixma TK. Lysine-targeting specificity in ubiquitin and ubiquitin-like modification pathways. Nat Struct Mol Biol 2014;21:308-316.
73. Boisson B, et al. Immunodeficiency, autoinflammation and amylopectinosis in humans with inherited HOIL-1 and LUBAC deficiency. Nat Immunol 2012;13:1178-1186.
74. Peltzer N, et al. HOIP deficiency causes embryonic lethality by aberrant TNFR1-mediated endothelial cell death. Cell Rep 2014;9:153-165.
75. Stieglitz B, Morris-Davies AC, Koliopoulos MG, Christodoulou E, Rittinger K. LUBAC synthesizes linear ubiquitin chains via a thioester intermediate. EMBO Rep 2012;13:840-846.
76. Smit JJ, Monteferrario D, Noordermeer SM, van Dijk WJ, van der Reijden BA, Sixma TK. The E3 ligase HOIP specifies linear ubiquitin chain assembly through its RING-IBR-RING domain and the unique LDD extension. EMBO J 2012;31:3833-3844.
77. Stieglitz B, et al. Structural basis for ligase-specific conjugation of linear ubiquitin chains by HOIP. Nature 2013;503:422-426.
78. Stieglitz B, Haire LF, Dikic I, Rittinger K. Structural analysis of SHARPIN, a subunit of a large multi-protein E3 ubiquitin ligase, reveals a novel dimerization function for the pleckstrin homology superfold. J Biol Chem 2012;287:20823-20829.
79. Sato Y, et al. Specific recognition of linear ubiquitin chains by the Npl4 zinc finger (NZF) domain of the HOIL-1L subunit of the linear ubiquitin chain assembly complex. Proc Natl Acad Sci USA 2011;108:20520-20525.
80. Damgaard RB. The ubiquitin ligase XIAP recruits LUBAC for NOD2 signaling in inflammation and innate immunity. Mol Cell 2012;46:746-758.
81. HogenEsch H, Gijbels MJ, Offerman E, van Hooft J, van Bekkum DW, Zurcher C. A spontaneous mutation characterized by chronic proliferative dermatitis in C57BL mice. Am J Pathol 1993;143:972-982.
82. Seymour RE, et al. Spontaneous mutations in the mouse Sharpin gene result in multiorgan inflammation, immune system dysregulation and dermatitis. Genes Immun 2007;8:416-421.
83. Kumari S, et al. Sharpin prevents skin inflammation by inhibiting TNFR1-induced keratinocyte apoptosis. Elife 2014;3:e03422.
84. Micheau O, Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 2003;114:181-190.
85. Rickard JA, et al. TNFR1-dependent cell death drives inflammation in Sharpin-deficient mice. Elife 2014;3:e03464.
86. Berger SB, et al. Cutting edge: RIP1 kinase activity is dispensable for normal development but is a key regulator of inflammation in SHARPIN-deficient mice. J Immunol 2014;192:5476-5480.
87. Sasaki Y, et al. Defective immune responses in mice lacking LUBAC-mediated linear ubiquitination in B cells. EMBO J 2013;32:2463-2476.
88. Oshima S, et al. ABIN-1 is a ubiquitin sensor that restricts cell death and sustains embryonic development. Nature 2009;457:906-909.
89. Lavrik IN, Krammer PH. Regulation of CD95/Fas signaling at the DISC. Cell Death Differ 2012;19:36-41.
90. Shirley S, Morizot A, Micheau O. Regulating TRAIL receptor-induced cell death at the membrane: a deadly discussion. Recent Pat Anticancer Drug Discov 2011;6:311-323.
91. Falschlehner C, Emmerich CH, Gerlach B, Walczak H. TRAIL signalling: decisions between life and death. Int J Biochem Cell Biol 2007;39:1462-1475.
92. Fiil BK, et al. OTULIN restricts Met1-linked ubiquitination to control innate immune signaling. Mol Cell 2013;50:818-830.
93. Donley C, et al. Identification of RBCK1 as a novel regulator of FKBPL: implications for tumor growth and response to tamoxifen. Oncogene 2014;33:3441-3450.
94. Dubois SM, et al. A catalytic-independent role for the LUBAC in NF-kappaB activation upon antigen receptor engagement and in lymphoma cells. Blood 2014;123:2199-2203.
95. Ehrlund A, Jonsson P, Vedin LL, Williams C, Gustafsson JA, Treuter E. Knockdown of SF-1 and RNF31 affects components of steroidogenesis, TGFbeta, and Wnt/beta-catenin signaling in adrenocortical carcinoma cells. PLoS ONE 2012;7:e32080.
96. Gustafsson N, Zhao C, Gustafsson JA, Dahlman-Wright K. RBCK1 drives breast cancer cell proliferation by promoting transcription of estrogen receptor alpha and cyclin B1. Cancer Res 2010;70:1265-1274.
97. Gustafsson Sheppard N, Heldring N, Dahlman-Wright K. Estrogen receptor-alpha, RBCK1, and protein kinase C beta 1 cooperate to regulate estrogen receptor-alpha gene expression. J Mol Endocrinol 2012;49:277-287.
98. He L, Ingram A, Rybak AP, Tang D. Shank-interacting protein-like 1 promotes tumorigenesis via PTEN inhibition in human tumor cells. J Clin Invest 2010;120:2094-2108.
99. Li J, et al. SHARPIN overexpression induces tumorigenesis in human prostate cancer LNCaP, DU145 and PC-3 cells via NF-kappaB/ERK/Akt signaling pathway. Med Oncol 2015;32:444.
100. Pouwels J, et al. SHARPIN regulates uropod detachment in migrating lymphocytes. Cell Rep 2013;5:619-628.
101. Queisser MA, et al. HOIL-1L functions as the PKCzeta ubiquitin ligase to promote lung tumor growth. Am J Respir Crit Care Med 2014;190:688-698.
102. Thompson HG, Harris JW, Lin L, Brody JP. Identification of the protein Zibra, its genomic organization, regulation, and expression in breast cancer cells. Exp Cell Res 2004;295:448-459.
103. Tomonaga M, et al. Activation of nuclear factor-kappa B by linear ubiquitin chain assembly complex contributes to lung metastasis of osteosarcoma cells. Int J Oncol 2012;40:409-417.
104. Yang Y, et al. Essential role of the linear ubiquitin chain assembly complex in lymphoma revealed by rare germline polymorphisms. Cancer Discov 2014;4:480-493.
105. Zhang Y, et al. Activation of nuclear factor kappaB pathway and downstream targets survivin and livin by SHARPIN contributes to the progression and metastasis of prostate cancer. Cancer 2014;120:3208-3218.
106. Zhu J, et al. The atypical ubiquitin ligase RNF31 stabilizes estrogen receptor alpha and modulates estrogen-stimulated breast cancer cell proliferation. Oncogene 2014;33:4340-4351.
107. Elliott PR, et al. Molecular basis and regulation of OTULIN-LUBAC interaction. Mol Cell 2014;54:335-348.
108. Schaeffer V, Akutsu M, Olma MH, Gomes LC, Kawasaki M, Dikic I. Binding of OTULIN to the PUB domain of HOIP controls NF-kappaB signaling. Mol Cell 2014;54:349-361.
109. Sun SC. CYLD: a tumor suppressor deubiquitinase regulating NF-[kappa]B activation and diverse biological processes. Cell Death Differ 2010;17:25-34.