Target specificity of the E3 ligase LUBAC for ubiquitin and NEMO relies on different minimal requirements

Journal of Biological Chemistry

Volumn 288, Issue 44, 2013, Pages 31728-31737

  Smit, Judith J ^a   Van Dijk, Willem J ^a   El Atmioui, Dris ^a   Merkx, Remco ^a   Ovaa, Huib ^a   Sixma, Titia K ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHAIN ELONGATION; LINEAR CHAIN; LYSINE MODIFICATION; N TERMINUS; N-TERMINALS; NEGATIVELY CHARGED; PRECISE POSITIONING; UBIQUITINATION;

AMINO ACIDS; MACHINERY;

CHAINS;

HOIL 1L PROTEIN; HOIP PROTEIN; I KAPPA B KINASE GAMMA; LINEAR UBIQUITIN CHAIN ASSEMBLY COMPLEX; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONTROLLED STUDY; PRIORITY JOURNAL; PROTEIN DOMAIN; UBIQUITINATION;

E3 UBIQUITIN LIGASE; ENZYME MECHANISMS; LINEAR UBIQUITIN CHAIN; LUBAC; MOLECULAR BIOLOGY; NF-ΚB (NF-KB); RNF31; UBIQUITINATION;

CATALYSIS; HUMANS; I-KAPPA B KINASE; MULTIENZYME COMPLEXES; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84887121929     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.495846     Document Type: Article

References (40)

1. Hayden, M. S., and Ghosh, S. (2012) NF-κB, the first quarter-century. Remarkable progress and outstanding questions. Genes Dev. 26, 203-234
2. Vallabhapurapu, S., and Karin, M. (2009) Regulation and function of NF-κB transcription factors in the immune system. Annu. Rev. Immunol. 27, 693-733
3. Niu, J., Shi, Y., Iwai, K., and Wu, Z. H. (2011) LUBAC regulates NF-κB activation upon genotoxic stress by promoting linear ubiquitination of NEMO. EMBOJ. 30, 3741-3753
4. Tokunaga, F., and Iwai, K. (2009) Involvement of LUBAC-mediated linear polyubiquitination of NEMO in NF-κB activation. Tanpakushitsu KakusanKoso 54, 635-642
5. Tokunaga, F., and Iwai, K. (2012) Linear ubiquitination. A novel NF-κB regulatory mechanism for inflammatory and immune responses by the LUBAC ubiquitin ligase complex. Endocr. J. 59, 641-652
6. Blackwell, K., Zhang, L., Workman, L. M., and Ting., A. T., Iwai, K., and Habelhah, H. (2013) Two coordinated mechanisms underlie tumor necrosis factor α-induced immediate and delayed IKB kinase activation. Mol. Cell Biol. 33, 1901-1915
7. Chen, Z. J. (2012) Ubiquitination in signaling to and activation of IKK. Immunol. Rev. 246, 95-106
8. Haas, T. L., and Emmerich., C. H., Gerlach, B., Schmukle, A. C, Cordier, S. M., Rieser, E., Feltham, R., Vince, J., Warnken, U, Wenger, T., Koschny, R., Komander, D., Silke, J., and Walczak, H. (2009) Recruitment of the linear ubiquitin chain assembly complex stabilizes the TNF-R1 signaling complex and is required for TNF-mediated gene induction. Mol. Cell 36, 831-844
9. Gerlach, B., and Cordier., S. M., Schmukle, A. C, Emmerich, C. H., Rieser, E., and Haas., T. L., Webb, A. I., Rickard, J. A., Anderton, H., and Wong., W. W., Nachbur, U, Gangoda, L., Warnken, U, and Purcell., A. W., Silke, J., and Walczak, H. (2011) Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 471, 591-596
10. Iwai, K., and Tokunaga, F. (2009) Linear polyubiquitination. A new regulator of NF-κB activation. EMBO Rep. 10, 706-713
11. Kirisako, T., Kamei, K., Murata, S., Kato, M., Fukumoto, H, Kanie, M., Sano, S., Tokunaga, F., Tanaka, K., and Iwai, K. (2006) A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBOJ. 25, 4877-4887 (Pubitemid 44607032)
12. Komander, D., and Rape, M. (2012) The ubiquitin code. Annu. Rev. Biochem. 81, 203-229
13. Lo, Y. C, Lin, S. C, Rospigliosi, C. C, Conze, D. B., and Wu., C. J., Ashwell, J. D., Eliezer, D., and Wu, H. (2009) Structural basis for recognition of diubiquitins by NEMO. Mol. Cell 33, 602-615
14. Rahighi, S., Ikeda, F., Kawasaki, M., Akutsu, M., Suzuki, N., Kato, R., Kensche, T., Uejima, T., Bloor, S., Komander, D., Randow, F., Wakatsuki, S., and Dikic, I. (2009) Specific recognition of linear ubiquitin chains by NEMO is important for NF-κB activation. Cell 136, 1098-1109
15. Sato, Y., Fujita, H., Yoshikawa, A., Yamashita, M., Yamagata, A., Kaiser, S. E., Iwai, K., and Fukai, S. (2011) 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. U.S.A. 108, 20520-20525
16. Verhelst, K., Carpentier, I., Kreike, M., Meloni, L., Verstrepen, L., Kensche, T., Dikic, I., and Beyaert, R. (2012) A20 inhibits LUBAC-mediated NF-κB activation by binding linear polyubiquitin chains via its zinc finger 7. EMBOJ. 31, 3845-3855
17. Tokunaga, F., Nishimasu, H, Ishitani, R., Goto, E., Noguchi, T., Mio, K., Kamei, K., Ma, A., Iwai, K., and Nureki, O. (2012) Specific recognition of linear polyubiquitin by A20 zinc finger 7 is involved in NF-κB regulation. EMBOJ. 31, 3856-3870
18. Pickart, C. M. (2001) Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70, 503-533 (Pubitemid 32663902)
19. Schulman, B. A., and Harper, J. W. (2009) Ubiquitin-like protein activation by E1 enzymes. The apex for downstream signalling pathways. Nat. Rev. Mol. Cell Biol. 10, 319-331
20. Ye, Y., and Rape, M. (2009) Building ubiquitin chains. E2 enzymes at work. Nat. Rev. Mol. Cell Biol. 10, 755-764
21. Morett, E., and Bork, P. (1999) A novel transactivation domain in parkin. Trends Biochem. Sci. 24, 229-231 (Pubitemid 29317288)
22. van der Reijden, B. A., Erpelinck-Verschueren, C A., Löwenberg, B., and Jansen, J.H. (1999) TRIADs. A new class of proteins with a novel cysteinerich signature. Protein Sci. 8, 1557-1561 (Pubitemid 29328239)
23. Trempe, J. F., Sauvé, V., Grenier, K., Seirafi, M., Tang, M. Y., Ménade, M., Al-Abdul-Wahid, S., Krett, J., Wong, K., Kozlov, G., Nagar, B., Fon, E. A., and Gehring, K. (2013) Structure of Parkin reveals mechanisms for ubiquitin ligase activation. Science 340, 1451-1455
24. Duda, D. M., and Olszewski., J. L., Schuermann, J. P., Kurinov, I., Miller, D. J., Nourse, A., and Alpi., A. F., and Schulman, B. A. (2013) Structure of HHARI, a RING-IBR-RING ubiquitin ligase. Autoinhibition of an ariadne-family E3 and insights into ligation mechanism. Structure 21, 1030-1041
25. Wauer, T., and Komander, D. (2013) Structure of the human Parkin ligase domain in an autoinhibited state. EMBOJ. 32, 2099-2112
26. Riley, B. E., Lougheed, J. C, Callaway, K., Velasquez, M., Brecht, E., Nguyen, L., Shaler, T., Walker, D., Yang, Y., Regnstrom, K., Diep, L., Zhang, Z., Chiou, S., Bova, M., Artis, D. R., Yao, N, Baker, J., Yednock, T., and Johnston, J. A. (2013) Structure and function of Parkin E3 ubiquitin ligase reveals aspects of RING and HECT ligases. Nat. Commun. 4, 1982
27. Wenzel, D. M., Lissounov, A., Brzovic, P. S., and Klevit, R. E. (2011) UBCH7 reactivity profile reveals parkin and HHARI to be RING/HECT hybrids. Nature 474, 105-108
28. Smit, J. J., Monteferrario, D., Noordermeer, S. M., van Dijk, W. J., van der Reijden, B. A., and Sixma, T. K. (2012) The E3 ligase HOIP specifies linear ubiquitin chain assembly through its RING-IBR-RING domain and the unique LDD extension. EMBOJ. 31, 3833-3844
29. Stieglitz, B., Morris-Davies, A. C., Koliopoulos, M. G., Christodoulou, E., and Rittinger, K. (2012) LUBAC synthesizes linear ubiquitin chains via a thioester intermediate. EMBO Rep. 13, 840-846
30. Ikeda, F., and Deribe., Y. L., Skånland, S. S., Stieglitz, B., Grabbe, C., Franz-Wachtel, M., van Wijk, S. J., Goswami, P., Nagy, V., Terzic, J., Tokunaga, F., Androulidaki, A., Nakagawa, T., Pasparakis, M., Iwai, K., Sundberg, J. P., Schaefer, L., Rittinger, K., Macek, B., and Dikic, I. (2011) SHARPIN forms a linear ubiquitin ligase complex regulating NF-κB activity and apoptosis. Nature 471, 637-641
31. Tokunaga, F., Nakagawa, T., Nakahara, M., Saeki, Y., Taniguchi, M., Sakata, S., Tanaka, K., Nakano, H., and Iwai, K. (2011) SHARPIN is a component of the NF-κB-activating linear ubiquitin chain assembly complex. Nature 471, 633-636
32. Yagi, H., Ishimoto, K., Hiromoto, T., Fujita, H., Mizushima, T., Uekusa, Y., Yagi-Utsumi, M., Kurimoto, E., Noda, M., Uchiyama, S., Tokunaga, F., Iwai, K., and Kato, K. (2012) A non-canonical UBA-UBL interaction forms the linear-ubiquitin-chain assembly complex. EMBO Rep 13, 462-468
33. Hadian, K., and Griesbach., R. A., Dornauer, S., Wanger, T. M., Nagel, D., Metlitzky, M., Beisker, W., Schmidt-Supprian, M., and Krappmann, D. (2011) NF-κB essential modulator (NEMO) interaction with linear and Lys-63 ubiquitin chains contributes to NF-κB activation. J. Biol. Chem. 286, 26107-26117
34. Tokunaga, F., Sakata, S., Saeki, Y., Satomi, Y., Kirisako, T., Kamei, K., Nakagawa, T., Kato, M., Murata, S., Yamaoka, S., Yamamoto, M., Akira, S., Takao, T., Tanaka, K., and Iwai, K. (2009) Involvement of linear polyubiquitylation of NEMO in NF-κB activation. Nat Cell Biol. 11, 123-132
35. Buchwald, G., van der Stoop, P., Weichenrieder, O., Perrakis, A., van Lohuizen, M., and Sixma, T. K. (2006) Structure and E3-ligase activity of the Ring-Ring complex of polycomb proteins Bmi1 and Ring1b. EMBOJ. 25, 2465-2474 (Pubitemid 44012229)
36. El Oualid, F., Merkx, R., Ekkebus, R., Hameed, D. S., and Smit., J. J., de Jong, A., Hilkmann, H, and Sixma., T. K., and Ovaa, H. (2010) Chemical synthesis of ubiquitin, ubiquitin-based probes, and diubiquitin. Angew. Chem. Int. Ed. Engl.49, 10149-10153
37. Marteijn, J. A., van der Meer, L. T., Smit, J. J., Noordermeer, S. M., Wissink, W., Jansen, P., Swarts, H. G., Hibbert, R. G., de Witte, T., Sixma, T. K., Jansen, J. H., and van der Reijden, B. A. (2009) The ubiquitin ligase Triad1 inhibits myelopoiesis through UbcH7 and Ubc13 interacting domains. Leukemia 23, 1480-1489
38. Pickart, C. M., and Raasi, S. (2005) Controlled synthesis of polyubiquitin chains. Methods Enzymol. 399, 21-36 (Pubitemid 41772719)
39. Keusekotten, K., and Elliott., P. R., Glockner, L., Fiil, B. K., and Damgaard., R. B., Kulathu, Y., Wauer, T., Hospenthal, M. K., Gyrd-Hansen, M., Krappmann, D., Hofmann, K., and Komander, D. (2013) OTULIN antagonizes LUBAC signaling by specifically hydrolyzing Met1-linked polyubiquitin. Cell 153, 1312-1326
40. Rivkin, E., and Almeida., S. M., Ceccarelli, D. F., Juang, Y. C, MacLean, T. A., Srikumar, T., Huang, H., Dunham, W. H., Fukumura, R., Xie, G., Gondo, Y., Raught, B., Gingras, A. C, Sicheri, F., and Cordes, S. P. (2013) The linear ubiquitin-specific deubiquitinase gumby regulates angiogenesis. Nature 498, 318-324