Linear polyubiquitin chains: A new modifier involved in NFκB activation and chronic inflammation including dermatitis

Cell Cycle

Volumn 10, Issue 18, 2011, Pages 3095-3104

  Iwai, Kazuhiro ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Chronic dermatitis; cpdm; Linear ubiquitination; LUBAC; NF B; SHARPIN; TNF ; Ubiquitin

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; POLYUBIQUITIN; SHARPIN; TUMOR NECROSIS FACTOR ALPHA; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

CELL NUCLEUS; CHRONIC INFLAMMATION; CONJUGATION; CYTOKINE PRODUCTION; DERMATITIS; ENZYME MECHANISM; GENE DELETION; GENE TARGETING; GENETIC TRANSCRIPTION; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PROTEIN PHOSPHORYLATION; REVIEW; UBIQUITINATION;

MAMMALIA; MUS;

EID: 80052906832     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.18.17437     Document Type: Review

References (73)

1. Hayden MS, Ghosh S. Shared principles in NFκB signaling. Cell 2008; 132:344-62; PMID:18267068; DOI:10.1016/j.cell.2008.01.020.
2. Staudt LM. Oncogenic activation of NFκB. Cold Spring Harb Perspect Biol 2010; 2:109; PMID:20516126; DOI:10.1101/cshperspect.a000109.
3. Kato M, Sanada M, Kato I, Sato Y, Takita J, Takeuchi K, et al. Frequent inactivation of A20 in B-cell lymphomas. Nature 2009; 459:712-6; PMID:19412163; DOI:10.1038/nature07969.
4. Paradisi A, Mehlen P. Netrin-1, a missing link between chronic inflammation and tumor progression. Cell Cycle 2010; 9:1253-62; PMID:20305387; DOI:10.4161/cc.9.7.11072.
5. Demchenko YN, Kuehl WM. A critical role for the NFκB pathway in multiple myeloma. Oncotarget 2010; 1:59-68; PMID:20890394.
6. Bonizzi G, Karin M. The two NFκB activation pathways and their role in innate and adaptive immunity. Trends Immunol 2004; 25:280-8; PMID:15145317; DOI:10.1016/j.it.2004.03.008.
7. Iwai K, Tokunaga F. Linear polyubiquitination: a new regulator of N NFκB activation. EMBO Rep 2009; 10:706-13; PMID:19543231; DOI:10.1038/embor.2009.144.
8. Skaug B, Jiang X, Chen ZJ. The role of ubiquitin in NFκB regulatory pathways. Annu Rev Biochem 2009; 78:769-96; PMID:19489733; DOI:10.1146/annurev. biochem.78.070907.102750.
9. Ciehanover A, Hod Y, Hershko A. A heat-stable polypeptide component of an ATP-dependent proteolytic system from reticulocytes. Biochem Biophys Res Commun 1978; 81:1100-5; PMID:666810; DOI:10.1016/0006-291X(78)91249-4.
10. Glickman MH, Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 2002; 82:373-428; PMID:11917093.
11. Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem 1998; 67:425-79; PMID:9759494; DOI:10.1146/annurev.biochem.67.1.425.
12. Ye Y, Rape M. Building ubiquitin chains: E2 enzymes at work. Nat Rev Mol Cell Biol 2009; 10:755-64; PMID:19851334; DOI:10.1038/nrm2780.
13. Yaron A, Hatzubai A, Davis M, Lavon I, Amit S, Manning AM, et al. Identification of the receptor component of the IκBα-ubiquitin ligase. Nature 1998; 396:590-4; PMID:9859996; DOI:10.1038/25159.
14. Winston JT, Strack P, Beer-Romero P, Chu CY, Elledge SJ, Harper JW. The SCFβTRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IκBα and β-catenin and stimulates IκBα ubiquitination in vitro. Genes Dev 1999; 13:270-83; PMID:9990852; DOI:10.1101/gad.13.3.270.
15. Spencer E, Jiang J, Chen ZJ. Signal-induced ubiquitination of IκBα by the F-box protein Slimb/β-TrCP. Genes Dev 1999; 13:284-94; PMID:9990853; DOI:10.1101/gad.13.3.284.
16. Deng L, Wang C, Spencer E, Yang L, Braun A, You J, et al. Activation of the IκB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 2000; 103:351-61; PMID:11057907; DOI:10.1016/S0092-8674(00)00126-4.
17. Spence J, Sadis S, Haas AL, Finley D. A ubiquitin mutant with specific defects in DNA repair and multiubiquitination. Mol Cell Biol 1995; 15:1265-73; PMID:7862120.
18. Reyes-Turcu FE, Ventii KH, Wilkinson KD. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 2009; 78:363-97; PMID:19489724; DOI:10.1146/annurev.biochem.78.082307.091526.
19. Peng J, Schwartz D, Elias JE, Thoreen CC, Cheng D, Marsischky G, et al. A proteomics approach to understanding protein ubiquitination. Nat Biotechnol 2003; 21:921-6; PMID:12872131; DOI:10.1038/nbt849.
20. Kirisako T, Kamei K, Murata S, Kato M, Fukumoto H, Kanie M, et al. A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J 2006; 25:4877-87; PMID:17006537; DOI:10.1038/sj.emboj.7601360.
21. Tokunaga F, Sakata S, Saeki Y, Satomi Y, Kirisako T, Kamei K, et al. Involvement of linear polyubiquitylation of NEMO in NFκB activation. Nat Cell Biol 2009; 11:123-32; PMID:19136968; DOI:10.1038/ncb1821.
22. Hofmann RM, Pickart CM. Noncanonical MMS2- encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 1999; 96:645-53; PMID:10089880; DOI:10.1016/S0092-8674(00)80575-9.
23. Wickliffe KE, Lorenz S, Wemmer DE, Kuriyan J, Rape M. The mechanism of linkage-specific ubiquitin chain elongation by a single-subunit E2. Cell 2011; 144:769-81; PMID:21376237; DOI:10.1016/j.cell.2011.01.035.
24. Pierce NW, Kleiger G, Shan SO, Deshaies RJ. Detection of sequential polyubiquitylation on a millisecond timescale. Nature 2009; 462:615-9; PMID:19956254; DOI:10.1038/nature08595.
25. Haldeman MT, Xia G, Kasperek EM, Pickart CM. Structure and function of ubiquitin conjugating enzyme E2-25K: the tail is a core-dependent activity element. Biochemistry 1997; 36:10526-37; PMID:9265633; DOI:10.1021/bi970750u.
26. Deshaies RJ, Joazeiro CA. RING domain E3 ubiquitin ligases. Annu Rev Biochem 2009; 78:399- 434; PMID:19489725; DOI:10.1146/annurev.biochem.78.101807. 093809.
27. Kim HT, Kim KP, Lledias F, Kisselev AF, Scaglione KM, Skowyra D, et al. Certain pairs of ubiquitinconjugating enzymes (E2s) and ubiquitin-protein ligases (E3s) synthesize nondegradable forked ubiquitin chains containing all possible isopeptide linkages. J Biol Chem 2007; 282:17375-86; PMID:17426036; DOI:10.1074/jbc.M609659200.
28. Yamamoto M, Okamoto T, Takeda K, Sato S, Sanjo H, Uematsu S, et al. Key function for the Ubc13 E2 ubiquitin-conjugating enzyme in immune receptor signaling. Nat Immunol 2006; 7:962-70; PMID:16862162; DOI:10.1038/ni1367.
29. Tokunaga F, Nakagawa T, Nakahara M, Saeki Y, Taniguchi M, Sakata S, et al. SHARPIN is a component of the NFκB-activating linear ubiquitin chain assembly complex. Nature 2011; 471:633-6; PMID:21455180; DOI:10.1038/ nature09815.
30. Ikeda F, Deribe YL, Skanland SS, Stieglitz B, Grabbe C, Franz-Wachtel M, et al. SHARPIN forms a linear ubiquitin ligase complex regulating NFκB activity and apoptosis. Nature 2011; 471:637-41; PMID:21455181; DOI:10.1038/nature09814.
31. Gerlach B, Cordier SM, Schmukle AC, Emmerich CH, Rieser E, Haas TL, et al. Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 2011; 471:591-6; PMID:21455173; DOI:10.1038/nature09816.
32. Schmidt-Supprian M, Bloch W, Courtois G, Addicks K, Israel A, Rajewsky K, et al. NEMO/ IKK γ-deficient mice model incontinentia pigmenti. Mol Cell 2000; 5:981-92; PMID:10911992; DOI:10.1016/S1097-2765(00)80263-4.
33. Rudolph D, Yeh WC, Wakeham A, Rudolph B, Nallainathan D, Potter J, et al. Severe liver degeneration and lack of N NFκB activation in NEMO/ IKKγ-deficient mice. Genes Dev 2000; 14:854-62; PMID:10766741.
34. Li ZW, Chu W, Hu Y, Delhase M, Deerinck T, Ellisman M, et al. The IKKbeta subunit of IκB kinase (IKK) is essential for nuclear factor κB activation and prevention of apoptosis. J Exp Med 1999; 189:1839-45; PMID:10359587; DOI:10.1084/ jem.189.11.1839.
35. Lim S, Sala C, Yoon J, Park S, Kuroda S, Sheng M, et al. Sharpin, a novel postsynaptic density protein that directly interacts with the shank family of proteins. Mol Cell Neurosci 2001; 17:385-97; PMID:11178875; DOI:10.1006/mcne. 2000.0940.
36. Seymour RE, Hasham MG, Cox GA, Shultz LD, Hogenesch H, Roopenian DC, et al. Spontaneous mutations in the mouse Sharpin gene result in multiorgan inflammation, immune system dysregulation and dermatitis. Genes Immun 2007; 8:416-21; PMID:17538631; DOI:10.1038/sj.gene.6364403.
37. 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; 143:972-82; PMID:8362989.
38. Lo YC, Lin SC, Rospigliosi CC, Conze DB, Wu CJ, Ashwell JD, et al. Structural basis for recognition of diubiquitins by NEMO. Mol Cell 2009; 33:602-15; PMID:19185524; DOI:10.1016/j.molcel.2009.01.012.
39. Rahighi S, Ikeda F, Kawasaki M, Akutsu M, Suzuki N, Kato R, et al. Specific recognition of linear ubiquitin chains by NEMO is important for NFκB activation. Cell 2009; 136:1098-109; PMID:19303852; DOI:10.1016/j.cell.2009.03.007.
40. Chiu YH, Zhao M, Chen ZJ. Ubiquitin in NFκB signaling. Chem Rev 2009; 109:1549-60; PMID:19281271; DOI:10.1021/cr800554j.
41. Laplantine E, Fontan E, Chiaravalli J, Lopez T, Lakisic G, Veron M, et al. NEMO specifically recognizes K63-linked poly-ubiquitin chains through a new bipartite ubiquitin-binding domain. EMBO J 2009; 28:2885-95; PMID:19763089; DOI:10.1038/emboj.2009.241.
42. Kanayama A, Seth RB, Sun L, Ea CK, Hong M, Shaito A, et al. TAB2 and TAB3 activate the NFκB pathway through binding to polyubiquitin chains. Mol Cell 2004; 15:535-48; PMID:15327770; DOI:10.1016/j.molcel.2004.08.008.
43. Chen F, Bhatia D, Chang Q, Castranova V. Finding NEMO by K63-linked polyubiquitin chain. Cell Death Differ 2006; 13:1835-8; PMID:16858426; DOI:10.1038/sj.cdd.4402014.
44. Wang C, Deng L, Hong M, Akkaraju GR, Inoue J, Chen ZJ. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 2001; 412:346-51; PMID:11460167; DOI:10.1038/35085597.
45. Hubeau M, Ngadjeua F, Puel A, Israel L, Feinberg J, Chrabieh M, et al. A new mechanism of X-linked anhidrotic ectodermal dysplasia with immunodeficiency: impairment of ubiquitin binding despite normal folding of NEMO protein. Blood 2011.
46. 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; 583:3317-22; PMID:19766637; DOI:10.1016/j.febslet. 2009.09.028.
47. Vince JE, Wong WW, Khan N, Feltham R, Chau D, Ahmed AU, et al. IAP antagonists target cIAP1 to induce TNFα-dependent apoptosis. Cell 2007; 131:682-93; PMID:18022363; DOI:10.1016/j. cell.2007.10.037.
48. Varfolomeev E, Blankenship JW, Wayson SM, Fedorova AV, Kayagaki N, Garg P, et al. IAP antagonists induce autoubiquitination of c-IAPs, NFκB activation and TNFalpha-dependent apoptosis. Cell 2007; 131:669-81; PMID:18022362; DOI:10.1016/j.cell.2007.10.030.
49. Dynek JN, Goncharov T, Dueber EC, Fedorova AV, Izrael-Tomasevic A, Phu L, et al. c-IAP1 and UbcH5 promote K11-linked polyubiquitination of RIP1 in TNF signalling. EMBO J 2010; 29:4198-209; PMID:21113135; DOI:10.1038/emboj.2010.300.
50. Xu M, Skaug B, Zeng W, Chen ZJ. A Ubiquitin replacement strategy in human cells reveals distinct mechanisms of IKK activation by TNFα and IL-1β. Mol Cell 2009; 36:302-14; PMID:19854138; DOI:10.1016/j.molcel.2009. 10.002.
51. Wagner S, Carpentier I, Rogov V, Kreike M, Ikeda F, Lohr F, et al. Ubiquitin binding mediates the N NFκB inhibitory potential of ABIN proteins. Oncogene 2008; 27:3739-45; PMID:18212736; DOI:10.1038/sj.onc.1211042.
52. Papoutsopoulou S, Symons A, Tharmalingham T, Belich MP, Kaiser F, Kioussis D, et al. ABIN-2 is required for optimal activation of Erk MAP kinase in innate immune responses. Nat Immunol 2006; 7:606-15; PMID:16633345; DOI:10.1038/ni1334.
53. Gijbels MJ, Zurcher C, Kraal G, Elliott GR, HogenEsch H, Schijff G, et al. Pathogenesis of skin lesions in mice with chronic proliferative dermatitis (cpdm/cpdm). Am J Pathol 1996; 148:941-50; PMID:8774148.
54. Pasparakis M, Courtois G, Hafner M, Schmidt- Supprian M, Nenci A, Toksoy A, et al. TNF-mediated inflammatory skin disease in mice with epidermis-specific deletion of IKK2. Nature 2002; 417:861-6; PMID:12075355; DOI:10.1038/ nature00820.
55. Nenci A, Huth M, Funteh A, Schmidt-Supprian M, Bloch W, Metzger D, et al. Skin lesion development in a mouse model of incontinentia pigmenti is triggered by NEMO deficiency in epidermal keratinocytes and requires TNF signaling. Hum Mol Genet 2006; 15:531-42; PMID:16399796; DOI:10.1093/hmg/ddi470.
56. Rushworth SA, Zaitseva L, Langa S, Bowles KM, MacEwan DJ. FLIP regulation of HO-1 and TNF signalling in human acute myeloid leukemia provides a unique secondary anti-apoptotic mechanism. Oncotarget 2010; 1:359-66; PMID:21307400.
57. Stratis A, Pasparakis M, Rupec RA, Markur D, Hartmann K, Scharffetter-Kochanek K, et al. Pathogenic role for skin macrophages in a mouse model of keratinocyte-induced psoriasis-like skin inflammation. J Clin Invest 2006; 116:2094-104; PMID:16886058; DOI:10.1172/JCI27179.
58. HogenEsch H, Torregrosa SE, Boggess D, Sundberg BA, Carroll J, Sundberg JP. Increased expression of type 2 cytokines in chronic proliferative dermatitis (cpdm) mutant mice and resolution of inflammation following treatment with IL-12. Eur J Immunol 2001; 31:734-42; PMID:11241277 DOI:10.1002/1521- 4141(200103)31:3<734::AIDIMMU734>3.0.CO;2-9.
59. Niu J, Shi Y, Iwai K, Wu ZH. LUBAC regulates NFκB activation upon genotoxic stress by promoting linear ubiquitination of NEMO. EMBO J, In press; PMID:21811235.
60. Wertz IE, O'Rourke KM, Zhou H, Eby M, Aravind L, Seshagiri S, et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NFκB signalling. Nature 2004; 430:694-9; PMID:15258597; DOI:10.1038/nature02794.
61. Brummelkamp TR, Nijman SM, Dirac AM, Bernards R. Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NFκB. Nature 2003; 424:797-801; PMID:12917690; DOI:10.1038/nature01811.
62. Kovalenko A, Chable-Bessia C, Cantarella G, Israel A, Wallach D, Courtois G. The tumour suppressor CYLD negatively regulates NFκB signalling by deubiquitination. Nature 2003; 424:801-5; PMID:12917691; DOI:10.1038/ nature01802.
63. Trompouki E, Hatzivassiliou E, Tsichritzis T, Farmer H, Ashworth A, Mosialos G. CYLD is a deubiquitinating enzyme that negatively regulates NFκB activation by TNFR family members. Nature 2003; 424:793-6; PMID:12917689; DOI:10.1038/nature01803.
64. 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; 10:466-73; PMID:19373254; DOI:10.1038/embor.2009.55.
65. Shembade N, Harhaj E. A20 inhibition of NFκB and inf lammation: targeting E2:E3 ubiquitin enzyme complexes. Cell Cycle 2010; 9:2481-2; PMID:20543575; DOI:10.4161/cc.9.13.12269.
66. Sun SC. CYLD: a tumor suppressor deubiquitinase regulating NFκB activation and diverse biological processes. Cell Death Differ 2010; 17:25-34; PMID:19373246; DOI:10.1038/cdd.2009.43.
67. Haas TL, Emmerich CH, Gerlach B, Schmukle AC, Cordier SM, Rieser E, 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; 36:831-44; PMID:20005846; DOI:10.1016/j.molcel.2009.10.013.
68. Kulathu Y, Akutsu M, Bremm A, Hofmann K, Komander D. Two-sided ubiquitin binding explains specificity of the TAB2 NZF domain. Nat Struct Mol Biol 2009; 16:1328-30; PMID:19935683; DOI:10.1038/nsmb.1731.
69. Sims JJ, Cohen RE. Linkage-specific avidity defines the lysine 63-linked polyubiquitinbinding preference of rap80. Mol Cell 2009; 33:775-83; PMID:19328070; DOI:10.1016/j.molcel.2009.02.011.
70. Sato Y, Yoshikawa A, Mimura H, Yamashita M, Yamagata A, Fukai S. Structural basis for specific recognition of Lys 63-linked polyubiquitin chains by tandem UIMs of RAP80. EMBO J 2009; 28:2461-8; PMID:19536136; DOI:10.1038/emboj.2009.160.
71. Wild P, Farhan H, McEwan DG, Wagner S, Rogov VV, Brady NR, et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 2011; 333:228-33; PMID:21617041; DOI:10.1126/science.1205405.
72. Zhu G, Wu CJ, Zhao Y, Ashwell JD. Optineurin negatively regulates TNFα-induced NFκB activation by competing with NEMO for ubiquitinated RIP. Curr Biol 2007; 17:1438-43; PMID:17702576; DOI:10.1016/j.cub.2007.07.041.
73. Maruyama H, Morino H, Ito H, Izumi Y, Kato H, Watanabe Y, et al. Mutations of optineurin in amyotrophic lateral sclerosis. Nature 2010; 465:223-6; PMID:20428114; DOI:10.1038/nature08971.