A Ubiquitin Replacement Strategy in Human Cells Reveals Distinct Mechanisms of IKK Activation by TNFα and IL-1β

Molecular Cell

Volumn 36, Issue 2, 2009, Pages 302-314

  Xu, Ming ^a   Skaug, Brian ^a   Zeng, Wenwen ^a   Chen, Zhijian J ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

MOLIMMUNO; PROTEINS; SIGNALING

Indexed keywords

I KAPPA B KINASE; INTERLEUKIN 1BETA; LYSINE DERIVATIVE; POLYUBIQUITIN; TUMOR NECROSIS FACTOR ALPHA; UBIQUITIN;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME REGULATION; ENZYME REPLACEMENT; HUMAN; HUMAN CELL; PROTEIN INDUCTION; UBIQUITINATION;

BIOCATALYSIS; ENZYME ACTIVATION; GENE KNOCK-IN TECHNIQUES; GENETIC TECHNIQUES; HUMANS; I-KAPPA B KINASE; INHIBITOR OF APOPTOSIS PROTEINS; INTERLEUKIN-1BETA; LYSINE; NUCLEAR PORE COMPLEX PROTEINS; POLYUBIQUITIN; RNA-BINDING PROTEINS; TETRACYCLINE; TUMOR NECROSIS FACTOR-ALPHA; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATION;

EID: 70350015537     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2009.10.002     Document Type: Article

References (46)

1. Bertrand M.J., Milutinovic S., Dickson K.M., Ho W.C., Boudreault A., Durkin J., Gillard J.W., Jaquith J.B., Morris S.J., and Barker P.A. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol. Cell 30 (2008) 689-700
2. Boone D.L., Turer E.E., Lee E.G., Ahmad R.C., Wheeler M.T., Tsui C., Hurley P., Chien M., Chai S., Hitotsumatsu O., et al. The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat. Immunol. 5 (2004) 1052-1060
3. Brummelkamp T.R., Nijman S.M., Dirac A.M., and Bernards R. Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-kappaB. Nature 424 (2003) 797-801
4. Chau V., Tobias J.W., Bachmair A., Marriott D., Ecker D.J., Gonda D.K., and Varshavsky A. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243 (1989) 1576-1583
5. Chen Z.J. Ubiquitin signalling in the NF-kappaB pathway. Nat. Cell Biol. 7 (2005) 758-765
6. Chen Z.J., Parent L., and Maniatis T. Site-specific phosphorylation of IkappaBalpha by a novel ubiquitination-dependent protein kinase activity. Cell 84 (1996) 853-862
7. Chen Z.J., and Sun L.J. Nonproteolytic functions of ubiquitin in cell signaling. Mol. Cell 33 (2009) 275-286
8. Deng L., Wang C., Spencer E., Yang L., Braun A., You J., Slaughter C., Pickart C., and Chen Z.J. Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103 (2000) 351-361
9. Ea C.K., Deng L., Xia Z.P., Pineda G., and Chen Z.J. Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol. Cell 22 (2006) 245-257
10. Finley D., Ozkaynak E., and Varshavsky A. The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses. Cell 48 (1987) 1035-1046
11. Fukushima T., Matsuzawa S., Kress C.L., Bruey J.M., Krajewska M., Lefebvre S., Zapata J.M., Ronai Z., and Reed J.C. Ubiquitin-conjugating enzyme Ubc13 is a critical component of TNF receptor-associated factor (TRAF)-mediated inflammatory responses. Proc. Natl. Acad. Sci. USA 104 (2007) 6371-6376
12. Gesellchen V., Kuttenkeuler D., Steckel M., Pelte N., and Boutros M. An RNA interference screen identifies Inhibitor of Apoptosis Protein 2 as a regulator of innate immune signalling in Drosophila. EMBO Rep. 6 (2005) 979-984
13. Hershko A. Ubiquitin: roles in protein modification and breakdown. Cell 34 (1983) 11-12
14. Hofmann R.M., and Pickart C.M. Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 96 (1999) 645-653
15. Holler N., Zaru R., Micheau O., Thome M., Attinger A., Valitutti S., Bodmer J.L., Schneider P., Seed B., and Tschopp J. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol. 1 (2000) 489-495
16. Israel A. NF-kappaB activation: Nondegradative ubiquitination implicates NEMO. Trends Immunol. 27 (2006) 395-397
17. Kanayama A., Seth R.B., Sun L., Ea C.K., Hong M., Shaito A., Chiu Y.H., Deng L., and Chen Z.J. TAB2 and TAB3 activate the NF-kappaB pathway through binding to polyubiquitin chains. Mol. Cell 15 (2004) 535-548
18. Kleino A., Valanne S., Ulvila J., Kallio J., Myllymaki H., Enwald H., Stoven S., Poidevin M., Ueda R., Hultmark D., et al. Inhibitor of apoptosis 2 and TAK1-binding protein are components of the Drosophila Imd pathway. EMBO J. 24 (2005) 3423-3434
19. Kovalenko A., Chable-Bessia C., Cantarella G., Israel A., Wallach D., and Courtois G. The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature 424 (2003) 801-805
20. Krappmann D., and Scheidereit C. A pervasive role of ubiquitin conjugation in activation and termination of IkappaB kinase pathways. EMBO Rep. 6 (2005) 321-326
21. Laplantine E., Fontan E., Chiaravalli J., Lopez T., Lakisic G., Veron M., Agou F., and Israel A. NEMO specifically recognizes K63-linked poly-ubiquitin chains through a new bipartite ubiquitin-binding domain. EMBO J. 28 (2009) 2885-2895
22. Li H., Kobayashi M., Blonska M., You Y., and Lin X. Ubiquitination of RIP is required for tumor necrosis factor alpha-induced NF-kappaB activation. J. Biol. Chem. 281 (2006) 13636-13643
23. Lo Y.C., Lin S.C., Rospigliosi C.C., Conze D.B., Wu C.J., Ashwell J.D., Eliezer D., and Wu H. Structural Basis for Recognition of Diubiquitins by NEMO. Mol. Cell 33 (2009) 602-615
24. Mahoney D.J., Cheung H.H., Mrad R.L., Plenchette S., Simard C., Enwere E., Arora V., Mak T.W., Lacasse E.C., Waring J., and Korneluk R.G. Both cIAP1 and cIAP2 regulate TNFalpha-mediated NF-kappaB activation. Proc. Natl. Acad. Sci. USA 105 (2008) 11778-11783
25. Newton K., Matsumoto M.L., Wertz I.E., Kirkpatrick D.S., Lill J.R., Tan J., Dugger D., Gordon N., Sidhu S.S., Fellouse F.A., et al. Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies. Cell 134 (2008) 668-678
26. Ninomiya-Tsuji J., Kishimoto K., Hiyama A., Inoue J., Cao Z., and Matsumoto K. The kinase TAK1 can activate the NIK-I kappaB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 398 (1999) 252-256
27. Pickart C.M. Back to the future with ubiquitin. Cell 116 (2004) 181-190
28. 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 136 (2009) 1098-1109
29. Sun L., Deng L., Ea C.K., Xia Z.P., and Chen Z.J. The TRAF6 ubiquitin ligase and TAK1 kinase mediate IKK activation by BCL10 and MALT1 in T lymphocytes. Mol. Cell 14 (2004) 289-301
30. Ting A.T., Pimentel-Muinos F.X., and Seed B. RIP mediates tumor necrosis factor receptor 1 activation of NF-kappaB but not Fas/APO-1-initiated apoptosis. EMBO J. 15 (1996) 6189-6196
31. 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
32. Trompouki E., Hatzivassiliou E., Tsichritzis T., Farmer H., Ashworth A., and Mosialos G. CYLD is a deubiquitinating enzyme that negatively regulates NF-kappaB activation by TNFR family members. Nature 424 (2003) 793-796
33. Vallabhapurapu S., Matsuzawa A., Zhang W., Tseng P.H., Keats J.J., Wang H., Vignali D.A., Bergsagel P.L., and Karin M. Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-kappaB signaling. Nat. Immunol. 9 (2008) 1364-1370
34. VanDemark A.P., Hofmann R.M., Tsui C., Pickart C.M., and Wolberger C. Molecular insights into polyubiquitin chain assembly: crystal structure of the Mms2/Ubc13 heterodimer. Cell 105 (2001) 711-720
35. Varfolomeev E., Goncharov T., Fedorova A.V., Dynek J.N., Zobel K., Deshayes K., Fairbrother W.J., and Vucic D. c-IAP1 and c-IAP2 are critical mediators of tumor necrosis factor alpha (TNFalpha)-induced NF-kappaB activation. J. Biol. Chem. 283 (2008) 24295-24299
36. Vince J.E., Wong W.W., Khan N., Feltham R., Chau D., Ahmed A.U., Benetatos C.A., Chunduru S.K., Condon S.M., McKinlay M., et al. IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis. Cell 131 (2007) 682-693
37. Wang C., Deng L., Hong M., Akkaraju G.R., Inoue J., and Chen Z.J. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412 (2001) 346-351
38. Wang L., Du F., and Wang X. TNF-alpha induces two distinct caspase-8 activation pathways. Cell 133 (2008) 693-703
39. 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 430 (2004) 694-699
40. Wu C.J., Conze D.B., Li T., Srinivasula S.M., and Ashwell J.D. Sensing of Lys 63-linked polyubiquitination by NEMO is a key event in NF-kappaB activation. Nat. Cell Biol. 8 (2006) 398-406
41. Xia Z.P., Sun L., Chen X., Pineda G., Jiang X., Adhikari A., Zeng W., and Chen Z.J. Direct activation of protein kinases by unanchored polyubiquitin chains. Nature 461 (2009) 114-119
42. Yamamoto M., Okamoto T., Takeda K., Sato S., Sanjo H., Uematsu S., Saitoh T., Yamamoto N., Sakurai H., Ishii K.J., et al. Key function for the Ubc13 E2 ubiquitin-conjugating enzyme in immune receptor signaling. Nat. Immunol. 7 (2006) 962-970
43. Yamamoto M., Sato S., Saitoh T., Sakurai H., Uematsu S., Kawai T., Ishii K.J., Takeuchi O., and Akira S. Cutting Edge: Pivotal Function of Ubc13 in Thymocyte TCR Signaling. J. Immunol. 177 (2006) 7520-7524
44. Zarnegar B.J., Wang Y., Mahoney D.J., Dempsey P.W., Cheung H.H., He J., Shiba T., Yang X., Yeh W.C., Mak T.W., et al. Noncanonical NF-kappaB activation requires coordinated assembly of a regulatory complex of the adaptors cIAP1, cIAP2, TRAF2 and TRAF3 and the kinase NIK. Nat. Immunol. 9 (2008) 1371-1378
45. Zhong Q., Gao W., Du F., and Wang X. Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 121 (2005) 1085-1095
46. Zhou R., Silverman N., Hong M., Liao D.S., Chung Y., Chen Z.J., and Maniatis T. The role of ubiquitination in Drosophila innate immunity. J. Biol. Chem. 280 (2005) 34048-34055