Together, Rpn10 and Dsk2 Can Serve as a Polyubiquitin Chain-Length Sensor

Molecular Cell

Volumn 36, Issue 6, 2009, Pages 1018-1033

  Zhang, Daoning ^a   Chen, Tony ^a   Ziv, Inbal ^b   Rosenzweig, Rina ^b   Matiuhin, Yulia ^b   Bronner, Vered ^c   Glickman, Michael H ^b   Fushman, David ^a  

^a Bldg 142   (United States)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^c Bio Rad Haifa   (Israel)

Author keywords

PROTEINS; SIGNALING

Indexed keywords

BINDING PROTEIN; POLYUBIQUITIN; PROTEASOME; PROTEIN DSK2; PROTEIN RPN10; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SENSOR; SIGNAL TRANSDUCTION;

CELL CYCLE PROTEINS; MODELS, MOLECULAR; POLYUBIQUITIN; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; UBIQUITINS;

EID: 72149114101     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2009.11.012     Document Type: Article

References (40)

1. Beal R., Deveraux Q., Xia G., Rechsteiner M., and Pickart C. Surface hydrophobic residues of multiubiquitin chains essential for proteolytic targeting. Proc. Natl. Acad. Sci. USA 93 (1996) 861-866
2. Beal R.E., Toscano-Cantaffa D., Young P., Rechsteiner M., and Pickart C.M. The hydrophobic effect contributes to polyubiquitin chain recognition. Biochemistry 37 (1998) 2925-2934
3. Bech-Otschir D., Helfrich A., Enenkel C., Consiglieri G., Seeger M., Holzhutter H.G., Dahlmann B., and Kloetzel P.M. Polyubiquitin substrates allosterically activate their own degradation by the 26S proteasome. Nat. Struct. Mol. Biol. 16 (2009) 219-225
4. Chen L., and Madura K. Rad23 promotes the targeting of proteolytic substrates to the proteasome. Mol. Cell. Biol. 22 (2002) 4902-4913
5. Chen L., Shinde U., Ortolan T.G., and Madura K. Ubiquitin-associated (UBA) domains in Rad23 bind ubiquitin and promote inhibition of multi-ubiquitin chain assembly. EMBO Rep. 2 (2001) 933-938
6. Chen T., Zhang D., Matiuhin Y., Glickman M., and Fushman D. 1H, 13C, and 15N resonance assignment of the ubiquitin-like domain from Dsk2p. Biomol. NMR Assign. 2 (2008) 147-149
7. Deveraux Q., Ustrell V., Pickart C., and Rechsteiner M. A 26 S protease subunit that binds ubiquitin conjugates. J. Biol. Chem. 269 (1994) 7059-7061
8. Deveraux Q., van Nocker S., Mahaffey D., Vierstra R., and Rechsteiner M. Inhibition of ubiquitin-mediated proteolysis by the Arabidopsis 26 S protease subunit S5a. J. Biol. Chem. 270 (1995) 29660-29663
9. Elsasser S., and Finley D. Delivery of ubiquitinated substrates to protein-unfolding machines. Nat. Cell Biol. 7 (2005) 742-749
10. Fu H., Sadis S., Rubin D.M., Glickman M., van Nocker S., Finley D., and Vierstra R.D. Multiubiquitin chain binding and protein degradation are mediated by distinct domains within the 26 S proteasome subunit Mcb1. J. Biol. Chem. 273 (1998) 1970-1981
11. Glickman M.H., and Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82 (2002) 373-428
12. Glickman M.H., Rubin D.M., Coux O., Wefes I., Pfeifer G., Cjeka Z., Baumeister W., Fried V.A., and Finley D. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94 (1998) 615-623
13. Guterman A., and Glickman M.H. Complementary roles for Rpn11 and Ubp6 in deubiquitination and proteolysis by the proteasome. J. Biol. Chem. 279 (2004) 1729-1738
14. Haririnia A., D'Onofrio M., and Fushman D. Mapping the interactions between Lys48 and Lys63-linked di-ubiquitins and a ubiquitin-interacting motif of S5a. J. Mol. Biol. 368 (2007) 753-766
15. Haririnia A., Verma R., Purohit N., Twarog M.Z., Deshaies R.J., Bolon D., and Fushman D. Mutations in the hydrophobic core of ubiquitin differentially affect its recognition by receptor proteins. J. Mol. Biol. 375 (2008) 979-996
16. Hartmann-Petersen R., and Gordon C. Proteins interacting with the 26S proteasome. Cell. Mol. Life Sci. 61 (2004) 1589-1595
17. Hershko A., and Heller H. Occurrence of a polyubiquitin structure in ubiquitin-protein conjugates. Biochem. Biophys. Res. Commun. 128 (1985) 1079-1086
18. Hofmann K., and Falquet L. A ubiquitin-interacting motif conserved in components of the proteasomal and lysosomal protein degradation systems. Trends Biochem. Sci. 26 (2001) 347-350
19. Hurley J.H., Lee S., and Prag G. Ubiquitin-binding domains. Biochem. J. 399 (2006) 361-372
20. Husnjak K., Elsasser S., Zhang N., Chen X., Randles L., Shi Y., Hofmann K., Walters K.J., Finley D., and Dikic I. Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453 (2008) 481-488
21. Ikeda F., and Dikic I. Atypical ubiquitin chains: new molecular signals. 'Protein Modifications: Beyond the Usual Suspects' Review Series. EMBO Rep. 9 (2008) 536-542
22. Kang Y., Chen X., Lary J.W., Cole J.L., and Walters K.J. Defining how ubiquitin receptors hHR23a and S5a bind polyubiquitin. J. Mol. Biol. 369 (2007) 168-176
23. Kravtsova-Ivantsiv Y., Cohen S., and Ciechanover A. Modification by single ubiquitin moieties rather than polyubiquitination is sufficient for proteasomal processing of the p105 NF-κB precursor. Mol. Cell 33 (2009) 496-504
24. Matiuhin Y., Kirkpatrick D., Ziv I., Kim W., Dakshinamurthy A., Kleifeld O., Gygi S.P., Reis N., and Glickman M.H. Extraproteasomal Rpn10 restricts access of the polyubiquitin-binding protein Dsk2 to proteasome. Mol. Cell 32 (2008) 415-425
25. Mayor T., Graumann J., Bryan J., MacCoss M.J., and Deshaies R.J. Quantitative profiling of ubiquitylated proteins reveals proteasome substrates and the substrate repertoire influenced by the Rpn10 receptor pathway. Mol. Cell. Proteomics 6 (2007) 1885-1895
26. Ohno A., Jee J., Fujiwara K., Tenno T., Goda N., Tochio H., Kobayashi H., Hiroaki H., and Shirakawa M. Structure of the UBA domain of Dsk2p in complex with ubiquitin molecular determinants for ubiquitin recognition. Structure 13 (2005) 521-532
27. Ortolan T.G., Tongaonkar P., Lambertson D., Chen L., Schauber C., and Madura K. The DNA repair protein rad23 is a negative regulator of multi-ubiquitin chain assembly. Nat. Cell Biol. 2 (2000) 601-608
28. Raasi S., and Pickart C.M. Rad23 ubiquitin-associated domains (UBA) inhibit 26 S proteasome-catalyzed proteolysis by sequestering lysine 48-linked polyubiquitin chains. J. Biol. Chem. 278 (2003) 8951-8959
29. Raasi S., Varadan R., Fushman D., and Pickart C.M. Diverse polyubiquitin interaction properties of ubiquitin-associated domains. Nat. Struct. Mol. Biol. 12 (2005) 708-714
30. Seong K.M., Baek J.H., Ahn B.Y., Yu M.H., and Kim J. Rpn10p is a receptor for ubiquitinated Gcn4p in proteasomal proteolysis. Mol. Cells 24 (2007) 194-199
31. Seong K.M., Baek J.H., Yu M.H., and Kim J. Rpn13p and Rpn14p are involved in the recognition of ubiquitinated Gcn4p by the 26S proteasome. FEBS Lett. 581 (2007) 2567-2573
32. Thrower J.S., Hoffman L., Rechsteiner M., and Pickart C.M. Recognition of the polyubiquitin proteolytic signal. EMBO J. 19 (2000) 94-102
33. van Nocker S., Sadis S., Rubin D.M., Glickman M., Fu H., Coux O., Wefes I., Finley D., and Vierstra R.D. The multiubiquitin-chain-binding protein Mcb1 is a component of the 26S proteasome in Saccharomyces cerevisiae and plays a nonessential, substrate-specific role in protein turnover. Mol. Cell. Biol. 16 (1996) 6020-6028
34. Varadan R., Walker O., Pickart C., and Fushman D. Structural properties of polyubiquitin chains in solution. J. Mol. Biol. 324 (2002) 637-647
35. Verma R., Oania R., Graumann J., and Deshaies R.J. Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitin-proteasome system. Cell 118 (2004) 99-110
36. Verma R., Peters N.R., D'Onofrio M., Tochtrop G.P., Sakamoto K.M., Varadan R., Zhang M., Coffino P., Fushman D., Deshaies R.J., and King R.W. Ubistatins inhibit proteasome-dependent degradation by binding the ubiquitin chain. Science 306 (2004) 117-120
37. Wang Q., Young P., and Walters K.J. Structure of S5a bound to monoubiquitin provides a model for polyubiquitin recognition. J. Mol. Biol. 348 (2005) 727-739
38. Young P., Deveraux Q., Beal R.E., Pickart C.M., and Rechsteiner M. Characterization of two polyubiquitin binding sites in the 26 S protease subunit 5a. J. Biol. Chem. 273 (1998) 5461-5467
39. Zhang D., Raasi S., and Fushman D. Affinity makes the difference: nonselective interaction of the UBA domain of Ubiquilin-1 with monomeric ubiquitin and polyubiquitin chains. J. Mol. Biol. 377 (2008) 162-180
40. Zhang N., Wang Q., Ehlinger A., Randles L., Lary J.W., Kang Y., Haririnia A., Storaska A.J., Cole J.L., Fushman D., and Walters K.J. Structure of the s5a:k48-linked diubiquitin complex and its interactions with rpn13. Mol. Cell 35 (2009) 280-290