Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitin-proteasome system

Cell

Volumn 118, Issue 1, 2004, Pages 99-110

  Verma, Rati ^a   Oania, Robert ^a   Graumann, Johannes ^a   Deshaies, Raymond J ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BINDING PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR; PROTEASOME; UBIQUITIN;

ARTICLE; BINDING AFFINITY; GENETIC ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN;

EID: 3142566639     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2004.06.014     Document Type: Article

References (55)

1. Amerik A., Swaminathan S., Krantz B.A., Wilkinson K.D., Hochstrasser M. In vivo disassembly of free polyubiquitin chains by yeast Ubp14 modulates rates of protein degradation by the proteasome. EMBO J. 16:1997;4826-4838
2. Cao K., Nakajima R., Meyer H.H., Zheng Y. The AAA-ATPase Cdc48/p97 regulates spindle disassembly at the end of mitosis. Cell. 115:2003;355-367
3. Chau V., Tobias J.W., Bachmair A., Marriott D., Ecker D.J., Gonda D.K., Varshavsky A. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science. 243:1989;1576-1583
4. Chen L., Madura K. Rad23 promotes the targeting of proteolytic substrates to the proteasome. Mol. Cell. Biol. 22:2002;4902-4913
5. Dai R.M., Li C.C. Valosin-containing protein is a multi-ubiquitin chain-targeting factor required in ubiquitin-proteasome degradation. Nat. Cell Biol. 3:2001;740-744
6. Demand J., Alberti S., Patterson C., Hohfeld J. Cooperation of a ubiquitin domain protein and an E3 ubiquitin ligase during chaperone/proteasome coupling. Curr. Biol. 11:2001;1569-1577
7. Deshaies R.J., Chau V., Kirschner M. Ubiquitination of the G1 cyclin Cln2p by a Cdc34p-dependent pathway. EMBO J. 14:1995;303-312
8. Deveraux Q., Ustrell V., Pickart C., Rechsteiner M. A 26S protease subunit that binds ubiquitin conjugates. J. Biol. Chem. 269:1994;7059-7061
9. Deveraux Q., van Nocker S., Mahaffey D., Vierstra R., Rechsteiner M. Inhibition of ubiquitin-mediated proteolysis by the Arabidopsis 26 S protease subunit S5a. J. Biol. Chem. 270:1995;29660-29663
10. Elsasser S., Gali R.R., Schwickart M., Larsen C.N., Leggett D.S., Muller B., Feng M.T., Tubing F., Dittmar G.A., Finley D. Proteasome subunit Rpn1 binds ubiquitin-like protein domains. Nat. Cell Biol. 4:2002;725-730
11. Flierman D., Ye Y., Dai M., Chau V., Rapoport T.A. Polyubiquitin serves as a recognition signal, rather than a ratcheting molecule, during retrotranslocation of proteins across the endoplasmic reticulum membrane. J. Biol. Chem. 278:2003;34774-34782
12. Flynn J.M., Neher S.B., Kim Y.I., Sauer R.T., Baker T.A. Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol. Cell. 11:2003;671-683
13. Fu H., Sadis S., Rubin D.M., Glickman M., van Nocker S., Finley D., 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
14. Fu X., Ng C., Feng D., Liang C. Cdc48p is required for the cell cycle commitment point at Start via degradation of the G1-CDK inhibitor Far1p. J. Cell Biol. 163:2003;21-26
15. Funakoshi M., Sasaki T., Nishimoto T., Kobayashi H. Budding yeast Dsk2p is a polyubiquitin-binding protein that can interact with the proteasome. Proc. Natl. Acad. Sci. USA. 99:2002;745-750
16. Glickman M.H., Rubin D.M., Fried V.A., Finley D. The regulatory particle of the Saccharomyces cerevisiae proteasome. Mol. Cell. Biol. 18:1998;3149-3162
17. Harper J.W., Burton J.L., Solomon M.J. The anaphase-promoting complex. it's not just for mitosis any more Genes Dev. 16:2002;2179-2206
18. Hartmann-Petersen R., Hendil K.B., Gordon C. Ubiquitin binding proteins protect ubiquitin conjugates from disassembly. FEBS Lett. 535:2003;77-81
19. Henchoz S., Chi Y., Catarin B., Herskowitz I., Deshaies R.J., Peter M. Phosphorylation- and ubiquitin-dependent degradation of the cyclin-dependent kinase inhibitor Far1p in budding yeast. Genes Dev. 11:1997;3046-3060
20. Hershko A., Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 67:1998;425-479
21. Hofmann K., Bucher P. The UBA domain. a sequence motif present in multiple enzyme classes of the ubiquitination pathway Trends Biochem. Sci. 21:1996;172-173
22. Jaquenoud M., Gulli M.P., Peter K., Peter M. The Cdc42p effector Gic2p is targeted for ubiquitin-dependent degradation by the SCFGrr1 complex. EMBO J. 17:1998;5360-5373
23. Jarosch E., Taxis C., Volkwein C., Bordallo J., Finley D., Wolf D.H., Sommer T. Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nat. Cell Biol. 4:2002;134-139
24. Johnson E.S., Ma P.C., Ota I.M., Varshavsky A. A proteolytic pathway that recognizes ubiquitin as a degradation signal. J. Biol. Chem. 270:1995;17442-17456
25. Kleijnen M.F., Shih A.H., Zhou P., Kumar S., Soccio R.E., Kedersha N.L., Gill G., Howley P.M. The hPLIC proteins may provide a link between the ubiquitination machinery and the proteasome. Mol. Cell. 6:2000;409-419
26. Lam Y.A., Lawson T.G., Velayutham M., Zweier J.L., Pickart C.M. A proteasomal ATPase subunit recognizes the polyubiquitin degradation signal. Nature. 416:2002;763-767
27. Lambertson D., Chen L., Madura K. Pleiotropic defects caused by loss of the proteasome-interacting factors Rad23 and Rpn10 of Saccharomyces cerevisiae. Genetics. 153:1999;69-79
28. Leggett D.S., Hanna J., Borodovsky A., Crosas B., Schmidt M., Baker R.T., Walz T., Ploegh H., Finley D. Multiple associated proteins regulate proteasome structure and function. Mol. Cell. 10:2002;495-507
29. Levchenko I., Seidel M., Sauer R.T., Baker T.A. A specificity-enhancing factor for the ClpXP degradation machine. Science. 289:2000;2354-2356
30. Li Z., Wang C.C. Functional characterization of the 11 non-ATPase subunit proteins in the trypanosome 19 S proteasomal regulatory complex. J. Biol. Chem. 277:2002;42686-42693
31. Link A.J., Eng J., Schieltz D.M., Carmack E., Mize G.J., Morris D.R., Garvik B.M., Yates J.R. III Direct analysis of protein complexes using mass spectrometry. Nat. Biotechnol. 17:1999;676-682
32. Ortolan T.G., Tongaonkar P., Lambertson D., Chen L., Schauber C., Madura K. The DNA repair protein rad23 is a negative regulator of multi-ubiquitin chain assembly. Nat. Cell Biol. 2:2000;601-608
33. Pickart C.M., Cohen R.E. Proteasomes and their kin. proteases in the machine age Nat. Rev. Mol. Cell Biol. 5:2004;177-187
34. Raasi S., 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
35. Rao H., Sastry A. Recognition of specific ubiquitin conjugates is important for the proteolytic functions of the ubiquitin-associated domain proteins Dsk2 and Rad23. J. Biol. Chem. 277:2002;11691-11695
36. Saeki Y., Saitoh A., Toh-e A., Yokosawa H. Ubiquitin-like proteins and Rpn10 play cooperative roles in ubiquitin-dependent proteolysis. Biochem. Biophys. Res. Commun. 293:2002;986-992. a
37. Saeki Y., Sone T., Toh-e A., Yokosawa H. Identification of ubiquitin-like protein-binding subunits of the 26S proteasome. Biochem. Biophys. Res. Commun. 296:2002;813-819. b
38. Sakata E., Yamaguchi Y., Kurimoto E., Kikuchi J., Yokoyama S., Yamada S., Kawahara H., Yokosawa H., Hattori N., Mizuno Y., et al. Parkin binds the Rpn10 subunit of 26S proteasomes through its ubiquitin-like domain. EMBO Rep. 4:2003;301-306
39. Schauber C., Chen L., Tongaonkar P., Vega I., Lambertson D., Potts W., Madura K. Rad23 links DNA repair to the ubiquitin/proteasome pathway. Nature. 391:1998;715-718
40. Seol J., Feldman R., Zachariae W., Shevchenko A., Correll C., Lyapina S., Chi Y., Galova M., Claypool J., Sandmeyer S., et al. Cdc53/cullin and the essential Hrt1 RING-H2 subunit of SCF define a ubiquitin ligase module that activates the E2 enzyme Cdc34. Genes Dev. 13:1999;1614-1626
41. Skowyra D., Koepp D.M., Kamura T., Conrad M.N., Conaway R.C., Conaway J.W., Elledge S.J., Harper J.W. Reconstitution of G1 cyclin ubiquitination with complexes containing SCFGrr1 and rbx1. Science. 284:1999;662-665
42. Swanson R., Locher M., Hochstrasser M. A conserved ubiquitin ligase of the nuclear envelope/endoplasmic reticulum that functions in both ER-associated and Matalpha2 repressor degradation. Genes Dev. 15:2001;2660-2674
43. Szlanka T., Haracska L., Kiss I., Deak P., Kurucz E., Ando I., Viragh E., Udvardy A. Deletion of proteasomal subunit S5a/Rpn10/p54 causes lethality, multiple mitotic defects and overexpression of proteasomal genes in Drosophila melanogaster. J. Cell Sci. 116:2003;1023-1033
44. Thrower J., Hoffman L., Rechsteiner M., Pickart C. Recognition of the polyubiquitin proteolytic signal. EMBO J. 19:2000;94-102
45. Tsai B., Ye Y., Rapoport T.A. Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nat. Rev. Mol. Cell Biol. 3:2002;246-255
46. van Nocker S., Sadis S., Rubin D.M., Glickman M., Fu H., Coux O., Wefes I., Finley D., 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
47. Verma R., Annan R.S., Huddleston M.J., Carr S.A., Reynard G., Deshaies R.J. Phosphorylation of Sic1p by G1 Cdk required for its degradation and entry into S phase. Science. 278:1997;455-460
48. Verma R., Chen S., Feldman R., Schieltz D., Yates J., Dohmen R.J., Deshaies R.J. Proteasomal proteomics. identification of nucleotide-sensitive proteasome-interacting proteins by mass spectrometric analysis of affinity-purified proteins Mol. Biol. Cell. 11:2000;3425-3439
49. Verma R., McDonald H., Yates J.R. III, Deshaies R.J. Selective degradation of ubiquitinated Sic1 by purified 26S proteasome yields active S phase cyclin-Cdk. Mol. Cell. 8:2001;439-448
50. Verma R., Aravind L., Oania R., McDonald W.H., Yates J.R. III, Koonin E.V., Deshaies R.J. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science. 298:2002;611-615
51. Whittaker C.A., Hynes R.O. Distribution and evolution of von Willebrand/integrin A domains. widely dispersed domains with roles in cell adhesion and elsewhere Mol. Biol. Cell. 13:2002;3369-3387
52. Wilkinson C.R., Seeger M., Hartmann-Petersen R., Stone M., Wallace M., Semple C., Gordon C. Proteins containing the UBA domain are able to bind to multi-ubiquitin chains. Nat. Cell Biol. 3:2001;939-943
53. Xie Y., Varshavsky A. UFD4 lacking the proteasome-binding region catalyses ubiquitination but is impaired in proteolysis. Nat. Cell Biol. 4:2002;1003-1007
54. Yao T., Cohen R.E. A cryptic protease couples deubiquitination and degradation by the proteasome. Nature. 419:2002;403-407
55. Ye Y., Meyer H.H., Rapoport T.A. Function of the p97-Ufd1-Npl4 complex in retrotranslocation from the ER to the cytosol. dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains J. Cell Biol. 162:2003;71-84