Investigations into the auto-FAT10ylation of the bispecific E2 conjugating enzyme UBA6-specific E2 enzyme 1

FEBS Journal

Volumn 281, Issue 7, 2014, Pages 1848-1859

  Aichem, Annette ^a   Catone, Nicola ^a   Groettrup, Marcus ^a,b  

^a UNIVERSITY OF KONSTANZ   (Switzerland)

^b UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

FAT10; proteasome; UBA6 specific E2 enzyme 1 (USE1)

Indexed keywords

HLA F ADJACENT TRANSCRIPT 10; MEMBRANE PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UBA6 SPECIFIC E2 ENZYME 1; UBIQUITIN; UNCLASSIFIED DRUG;

ANTIBODY SPECIFICITY; ARTICLE; CELL CYCLE REGULATION; CHROMOSOME SEGREGATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME MODIFICATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NEGATIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; UBIQUITINATION;

FAT10; PROTEASOME; UBA6-SPECIFIC E2 ENZYME 1 (USE1);

FEEDBACK, PHYSIOLOGICAL; HEK293 CELLS; HUMANS; MUTATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEOLYSIS; UBIQUITINATION; UBIQUITINS;

EID: 84897533879     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12745     Document Type: Article

References (37)

1. Finley D, (2009) Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem 78, 477-513.
2. van der Veen AG, &, Ploegh HL, (2012) Ubiquitin-like proteins. Annu Rev Biochem 81, 323-357.
3. Hipp MS, Kalveram B, Raasi S, Groettrup M, &, Schmidtke G, (2005) FAT10, a ubiquitin-independent signal for proteasomal degradation. Mol Cell Biol 25, 3483-3491. (Pubitemid 40559557)
4. Schmidtke G, Kalveram B, &, Groettrup M, (2009) Degradation of FAT10 by the 26S proteasome is independent of ubiquitylation but relies on NUB1L. FEBS Lett 583, 591-594.
5. Schmidtke G, Aichem A, &, Groettrup M, (2013) FAT10ylation as a signal for proteasomal degradation. Biochim Biophys Acta 1843, 97-102.
6. Fan W, Cai W, Parimoo S, Lennon GG, &, Weissman SM, (1996) Identification of seven new human MHC class I region genes around the HLA-F locus. Immunogenetics 44, 97-103. (Pubitemid 26164207)
7. Raasi S, Schmidtke G, Giuli RD, &, Groettrup M, (1999) A ubiquitin-like protein which is synergistically inducible by interferon-g and tumor necrosis factor-a. Eur J Immunol 29, 4030-4036.
8. Canaan A, Yu XF, Booth CJ, Lian J, Lazar I, Gamfi SL, Castille K, Kohya N, Nakayama Y, Liu YC, et al,. (2006) FAT10/diubiquitin-like protein-deficient mice exhibit minimal phenotypic differences. Mol Cell Biol 26, 5180-5189. (Pubitemid 43955829)
9. Lee CG, Ren J, Cheong IS, Ban KH, Ooi LL, Yong Tan S, Kan A, Nuchprayoon I, Jin R, Lee KH, et al,. (2003) Expression of the FAT10 gene is highly upregulated in hepatocellular carcinoma and other gastrointestinal and gynecological cancers. Oncogene 22, 2592-2603. (Pubitemid 36605607)
10. Lukasiak S, Schiller C, Oehlschlaeger P, Schmidtke G, Krause P, Legler DF, Autschbach F, Schirmacher P, Breuhahn K, &, Groettrup M, (2008) Proinflammatory cytokines cause FAT10 upregulation in cancers of liver and colon. Oncogene 27, 6068-6074.
11. Schliehe C, Bitzer A, van den Broek M, &, Groettrup M, (2012) Stable antigen is most effective for eliciting CD8+ T-cell responses after DNA vaccination and infection with recombinant vaccinia virus in vivo. J Virol 86, 9782-9793.
12. Ebstein F, Lehmann A, &, Kloetzel PM, (2012) The FAT10- and ubiquitin-dependent degradation machineries exhibit common and distinct requirements for MHC class I antigen presentation. Cell Mol Life Sci 69, 2443-2454.
13. Buchsbaum S, Bercovich B, Ziv T, &, Ciechanover A, (2012) Modification of the inflammatory mediator LRRFIP2 by the ubiquitin-like protein FAT10 inhibits its activity during cellular response to LPS. Biochem Biophys Res Commun 428, 11-16.
14. Ren JW, Wang Y, Gao Y, Mehta SBK, &, Lee CGL, (2011) FAT10 mediates the effect of TNF-alpha in inducing chromosomal instability. J Cell Sci 124, 3665-3675.
15. Aichem A, Kalveram B, Spinnenhirn V, Kluge K, Catone N, Johansen T, &, Groettrup M, (2012) The proteomic analysis of endogenous FAT10 substrates identifies p62/SQSTM1 as a substrate of FAT10ylation. J Cell Sci 125, 4576-4585.
16. Kerscher O, Felberbaum R, &, Hochstrasser M, (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22, 159-180.
17. Groettrup M, Pelzer C, Schmidtke G, &, Hofmann K, (2008) Activating the ubiquitin family: UBA6 challenges the field. Trends Biochem Sci 33, 230-237.
18. Pelzer C, Kassner I, Matentzoglu K, Singh RK, Wollscheid HP, Scheffner M, Schmidtke G, &, Groettrup M, (2007) UBE1L2, a novel E1 enzyme specific for ubiquitin. J Biol Chem 282, 23010-23014. (Pubitemid 47311897)
19. Jin JP, Li X, Gygi SP, &, Harper JW, (2007) Dual E1 activation systems for ubiquitin differentially regulate E2 enzyme charging. Nature 447, 1135-1137.
20. Chiu YH, Sun Q, &, Chen ZJ, (2007) E1-L2 activates both ubiquitin and FAT10. Mol Cell 27, 1014-1023. (Pubitemid 47488190)
21. Aichem A, Pelzer C, Lukasiak S, Kalveram B, Sheppard PW, Rani N, Schmidtke G, &, Groettrup M, (2010) USE1 is a bispecific conjugating enzyme for ubiquitin and FAT10, which FAT10ylates itself in cis. Nat Commun 1, 13, doi: 10.1038/ncomms1012.
22. Gavin JM, Chen JJ, Liao H, Rollins N, Yang XF, Xu Q, Ma JY, Loke HK, Lingaraj T, Brownell JE, et al,. (2012) Mechanistic studies on activation of ubiquitin and di-ubiquitin-like protein, FAT10, by ubiquitin-like modifier activating enzyme 6, Uba6. J Biol Chem 287, 15512-15522.
23. Gu X, Zhao F, Zheng M, Fei X, Chen X, Huang S, Xie Y, &, Mao Y, (2007) Cloning and characterization of a gene encoding the human putative ubiquitin conjugating enzyme E2Z (UBE2Z). Mol Biol Rep 34, 183-188. (Pubitemid 47124945)
24. Raasi S, Schmidtke G, &, Groettrup M, (2001) The ubiquitin-like protein FAT10 forms covalent conjugates and induces apoptosis. J Biol Chem 276, 35334-35343.
25. Buchsbaum S, Bercovich B, &, Ciechanover A, (2012) FAT10 is a proteasomal degradation signal that is itself regulated by ubiquitination. Mol Biol Cell 23, 225-232.
26. Hsiao HH, Meulmeester E, Frank BTC, Melchior F, &, Urlaub H, (2009) 'ChopNSpice', a mass spectrometric approach that allows identification of endogenous small ubiquitin-like modifier-conjugated peptides. Mol Cell Proteomics 8, 2664-2675.
27. Pichler A, Knipscheer P, Oberhofer E, vanDijk WJ, Korner R, Olsen JV, Jentsch S, Melchior F, &, Sixma TK, (2005) SUMO modification of the ubiquitin-conjugating enzyme E2-25K. Nat Struct Mol Biol 12, 264-269. (Pubitemid 43079369)
28. Rani N, Aichem A, Schmidtke G, Kreft SG, &, Groettrup M, (2012) FAT10 and NUB1L bind to the VWA domain of Rpn10 and Rpn1 to enable proteasome-mediated proteolysis. Nat Commun 3, 749.
29. Bencsath KP, Podgorski MS, Pagala VR, Slaughter CA, &, Schulman BA, (2002) Identification of a multifunctional binding site on Ubc9p required for Smt3p conjugation. J Biol Chem 277, 47938-47945. (Pubitemid 36159322)
30. Knipscheer P, Flotho A, Klug H, Olsen JV, van Dijk WJ, Fish A, Johnson ES, Mann M, Sixma TK, &, Pichler A, (2008) Ubc9 sumoylation regulates SUMO target discrimination. Mol Cell 31, 371-382.
31. Schmidtke G, Kalveram B, Weber E, Bochtler P, Lukasiak S, Hipp MS, &, Groettrup M, (2006) The UBA domains of NUB1L are required for binding but not for accelerated degradation of the ubiquitin-like modifier FAT10. J Biol Chem 281, 20045-20054. (Pubitemid 44065779)
32. Kalveram B, Schmidtke G, &, Groettrup M, (2008) The ubiquitin-like modifier FAT10 interacts with HDAC6 and localizes to aggresomes under proteasome inhibition. J Cell Sci 121, 4079-4088.
33. Liu Y, Pan J, Zhang C, Fan W, Collinge M, Bender JR, &, Weissman SM, (1999) A MHC-encoded ubiquitin-like protein (FAT10) binds noncovalently to the spindle assembly checkpoint protein MAD2. Proc Natl Acad Sci USA 96, 4313-4318. (Pubitemid 29190333)
34. Ross MJ, Wosnitzer MS, Ross MD, Granelli B, Gusella GL, Husain M, Kaufman L, Vasievich M, D'Agati VD, Wilson PD, et al,. (2006) Role of ubiquitin-like protein FAT10 in epithelial apoptosis in renal disease. J Am Soc Nephrol 17, 996-1004.
35. Ren JW, Kan A, Leong SH, Ooi LLPJ, Jeang KT, Chong SS, Kon OL, &, Lee CGL, (2006) FAT10 plays a role in the regulation of chromosomal stability. J Biol Chem 281, 11413-11421. (Pubitemid 43855566)
36. Lee PC, Sowa ME, Gygi SP, &, Harper JW, (2011) Alternative ubiquitin activation/conjugation cascades interact with N-end rule ubiquitin ligases to control degradation of RGS proteins. Mol Cell 43, 392-405.
37. Hipp MS, Raasi S, Groettrup M, &, Schmidtke G, (2004) NEDD8 ultimate buster-1L interacts with the ubiquitin-like protein FAT10 and accelerates its degradation. J Biol Chem 279, 16503-16510. (Pubitemid 38509349)