Proteasomal recognition of ubiquitylated substrates

Trends in Plant Science

Volumn 15, Issue 7, 2010, Pages 375-386

  Fu, Hongyong ^a,b   Lin, Ya Ling ^a,b   Fatimababy, A S ^a  

^a INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

^b NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEASOME;

ANIMAL; ENZYME SPECIFICITY; HUMAN; METABOLISM; PROTEIN BINDING; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION;

ANIMALS; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; UBIQUITINATION;

EID: 77955276666     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2010.03.004     Document Type: Review

References (102)

1. Hershko A., Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 1998, 67:425-479.
2. Seet B.T., et al. Reading protein modifications with interaction domains. Nat. Rev. Mol. Cell Biol. 2006, 7:473-483.
3. Vierstra R.D. The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 2009, 10:385-397.
4. Hurley J., et al. Ubiquitin-binding domains. Biochem. J. 2006, 399:361-372.
5. Ikeda F., Dikic I. Atypical ubiquitin chains: new molecular signals. EMBO Rep. 2008, 9:536-542.
6. Pickart C.M., Fushman D. Polyubiquitin chains: polymeric protein signals. Curr. Opin. Chem. Biol. 2004, 8:610-616.
7. Thrower J., et al. Recognition of the polyubiquitin proteolytic signal. EMBO J. 2000, 19:94-102.
8. Haririnia A., et al. Mapping the interactions between Lys48 and Lys63-linked di-ubiquitins and a ubiquitin-interacting motif of S5a. J. Mol. Biol. 2007, 368:753-766.
9. Varadan R., et al. Solution conformation of Lys63-linked di-ubiquitin chain provides clues to functional diversity of polyubiquitin signaling. J. Biol. Chem. 2004, 279:7055-7063.
10. Beal R., et al. Surface hydrophobic residues of multiubiquitin chains essential for proteolytic targeting. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:861-866.
11. Raasi S., et al. Binding of polyubiquitin chains to ubiquitin-associated (UBA) domains of hHR23A. J. Mol. Biol. 2004, 341:1367-1379.
12. Varadan R., et al. Structural determinants for selective recognition of a Lys48-linked polyubiquitin chain by a UBA domain. Mol. Cell 2005, 18:687-698.
13. Trempe J., et al. Mechanism of Lys48-linked polyubiquitin chain recognition by the Mud1 UBA domain. EMBO J. 2005, 24:3178-3189.
14. Wang Q., et al. Ubiquitin recognition by the DNA repair protein hHR23a. Biochemistry 2003, 42:13529-13535.
15. Ryu K.-S., et al. Binding surface mapping of intra- and interdomain interactions among hHR23B, ubiquitin, and polyubiquitin binding site 2 of S5a. J. Biol. Chem. 2003, 278:36621-36627.
16. Jin L., et al. Mechanism of ubiquitin-chain formation by the human anaphase-promoting complex. Cell 2008, 133:653-665.
17. Johnson E.S., et al. A proteolytic pathway that recognizes ubiquitin as a degradation signal. J. Biol. Chem. 1995, 270:17442-17456.
18. van Nocker S., et al. 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. 1996, 16:6020-6028.
19. Husnjak K., et al. Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 2008, 453:481-488.
20. Schreiner P., et al. Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interaction. Nature 2008, 453:548-552.
21. Saeki Y., et al. Identification of ubiquitin-like protein-binding subunits of the 26S proteasome. Biochem. Bioph. Res. Co. 2002, 296:813-819.
22. Verma R., et al. Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitin-proteasome system. Cell 2004, 118:99-110.
23. Funakoshi M., et al. Budding yeast Dsk2p is a polyubiquitin-binding protein that can interact with the proteasome. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:745-750.
24. Kaplun L., et al. The DNA damage-inducible UbL-UbA protein Ddi1 participates in Mec1-mediated degradation of Ho endonuclease. Mol. Cell Biol. 2005, 25:5355-5362.
25. Elsasser S., Finley D. Delivery of ubiquitinated substrates to protein-unfolding machines. Nat. Cell Biol. 2005, 7:742-749.
26. Raasi S., Wolf D.H. Ubiquitin receptors and ERAD: A network of pathways to the proteasome. Semin. Cell Dev. Biol. 2007, 18:780-791.
27. Alexandru G., et al. UBXD7 binds multiple ubiquitin ligases and implicates p97 in HIF1α turnover. Cell 2008, 134:804-816.
28. Ravid T., Hochstrasser M. Diversity of degradation signals in the ubiquitin-proteasome system. Nat. Rev. Mol. Cell Bio. 2008, 9:679-690.
29. Ufo1 complexes. Mol. Cell Biol. 2006, 26:1579-1588.
30. Fu H., et al. Subunit interaction maps for the regulatory particle of the 26S proteasome and the COP9 signalosome. EMBO J. 2001, 20:7096-7107.
31. Dantuma N.P., et al. The ubiquitin receptor Rad23: At the crossroads of nucleotide excision repair and proteasomal degradation. DNA Repair 2009, 8:449-460.
32. Gabriely G., et al. Different domains of the UBL-UBA ubiquitin receptor, Ddi1/Vsm1, are involved in its multiple cellular roles. Mol. Biol. Cell 2008, 19:3625-3637.
33. Hicke L., et al. Ubiquitin-binding domains. Nat. Rev. Mol. Cell Bio. 2005, 6:610-621.
34. Wang B., et al. Structure and ubiquitin interactions of the conserved zinc finger domain of Npl4. J. Biol. Chem. 2003, 278:20225-20234.
35. Yuan X., et al. Structure, dynamics and interactions of p47, a major adaptor of the AAA ATPase, p97. EMBO J. 2004, 23:1463-1473.
36. Park S., et al. Ufd1 exhibits the AAA-ATPase fold with two distinct ubiquitin interaction sites. Structure 2005, 13:995-1005.
37. Fatimababy A.S., et al. Cross-species divergence of the major recognition pathways of ubiquitylated substrates for ubiquitin/26S proteasome-mediated proteolysis. FEBS J. 2010, 277:796-816.
38. Raasi S., et al. Diverse polyubiquitin interaction properties of ubiquitin-associated domains. Nat. Struct. Mol. Biol. 2005, 12:708-714.
39. Fu H., et al. Multiubiquitin chain binding and protein degradation are mediated by distinct domains within the 26 S proteasome subunit Mcb1. J. Biol. Chem. 1998, 273:1970-1981.
40. Wang Q., et al. Structure of S5a bound to monoubiquitin provides a model for polyubiquitin recognition. J. Mol. Biol. 2005, 348:727-739.
41. Young P., et al. Characterization of two polyubiquitin binding sites in the 26 S protease subunit 5a. J. Biol. Chem. 1998, 273:5461-5467.
42. Zhang D., et al. Affinity makes the difference: nonselective interaction of the UBA domain of ubiquilin-1 with monomeric ubiquitin and polyubiquitin chains. J. Mol. Biol. 2008, 377:162-180.
43. Ohno A., et al. Structure of the UBA domain of Dsk2p in complex with ubiquitin: molecular determinants for ubiquitin recognition. Structure 2005, 13:521-532.
44. Lowe E., et al. Structures of the Dsk2 UBL and UBA domains and their complex. Acta Crystallogr. D Biol. Crystallogr. 2006, 62:177-188.
45. Elsasser S., et al. Proteasome subunit Rpn1 binds ubiquitin-like protein domains. Nat. Cell Biol. 2002, 4:725-730.
46. Elsasser S., et al. Rad23 and Rpn10 serve as alternative ubiquitin receptors for the proteasome. J. Biol. Chem. 2004, 279:26817-26822.
47. Ishii T., et al. Yeast Pth2 is a UBL domain-binding protein that participates in the ubiquitin-proteasome pathway. EMBO J. 2006, 25:5492-5503.
48. Seeger M., et al. Interaction of the anaphase-promoting complex/cyclosome and proteasome protein complexes with multiubiquitin chain-binding proteins. J. Biol. Chem. 2003, 278:16791-16796.
49. Matiuhin Y., et al. Extraproteasomal Rpn10 restricts access of the polyubiquitin-binding protein Dsk2 to proteasome. Mol. Cell 2008, 32:415-425.
50. Hiyama H., et al. Interaction of hHR23 with S5a. The ubiquitin-like domain of hHR23 mediates interaction with S5a subunit of 26 S proteasome. J. Biol. Chem. 1999, 274:28019-28025.
51. Kang Y., et al. Defining how ubiquitin receptors hHR23a and S5a bind polyubiquitin. J. Mol. Biol. 2007, 369:168-176.
52. Jentsch S., Rumpf S. Cdc48 (p97): a 'molecular gearbox' in the ubiquitin pathway?. Trends Biochem. Sci. 2007, 32:6-11.
53. Wang Q., et al. Molecular perspectives on p97-VCP: progress in understanding its structure and diverse biological functions. J. Struct. Biol. 2004, 146:44-57.
54. Ye Y. Diverse functions with a common regulator: Ubiquitin takes command of an AAA ATPase. J. Struct. Biol. 2006, 156:29-40.
55. Bays N.W., et al. HRD4/NPL4 is required for the proteasomal processing of ubiquitinated ER proteins. Mol. Biol. Cell 2001, 12:4114-4128.
56. Meyer H., et al. Direct binding of ubiquitin conjugates by the mammalian p97 adaptor complexes, p47 and Ufd1-Npl4. EMBO J. 2002, 21:5645-5652.
57. Neuber O., et al. Ubx2 links the Cdc48 complex to ER-associated protein degradation. Nat. Cell Biol. 2005, 7:993-998.
58. Schuberth C., et al. Shp1 and Ubx2 are adaptors of Cdc48 involved in ubiquitin-dependent protein degradation. EMBO Rep. 2004, 5:818-824.
59. Ballar P., et al. The role of a novel p97/Valosin-containing protein-interacting motif of gp78 in endoplasmic reticulum-associated degradation. J. Biol. Chem. 2006, 281:35359-35368.
60. Richly H., et al. A series of ubiquitin binding factors connects CDC48/p97 to substrate multiubiquitylation and proteasomal targeting. Cell 2005, 120:73-84.
61. Kim I., et al. Multiple interactions of Rad23 suggest a mechanism for ubiquitylated substrate delivery important in proteolysis. Mol. Biol. Cell 2004, 15:3357-3365.
62. Rumpf S., Jentsch S. Functional division of substrate processing cofactors of the ubiquitin-selective Cdc48 chaperone. Mol. Cell 2006, 21:261-269.
63. Ye Y., et al. 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. 2003, 162:71-84.
64. Davies J.M., et al. Conformational changes of p97 during nucleotide hydrolysis determined by small-angle X-Ray scattering. Structure 2005, 13:183-195.
65. Schuberth C., Buchberger A. Membrane-bound Ubx2 recruits Cdc48 to ubiquitin ligases and their substrates to ensure efficient ER-associated protein degradation. Nat. Cell Biol. 2005, 7:999-1006.
66. Wilson J.D., et al. Sel1p/Ubx2p participates in a distinct Cdc48p-dependent endoplasmic reticulum-associated degradation pathway. Traffic 2006, 7:1213-1223.
67. Shiozawa K., et al. The common phospholipid-binding activity of the N-terminal domains of PEX1 and VCP/p97. FEBS J. 2006, 273:4959-4971.
68. Hochstrasser M. Lingering mysteries of ubiquitin-chain assembly. Cell 2006, 124:27-34.
69. Eddins M.J., et al. Mms2-Ubc13 covalently bound to ubiquitin reveals the structural basis of linkage-specific polyubiquitin chain formation. Nat. Struct. Mol. Biol. 2006, 13:915-920.
70. Petroski M.D., Deshaies R.J. Mechanism of lysine 48-linked ubiquitin-chain synthesis by the Cullin-RING ubiquitin-ligase complex SCF-Cdc34. Cell 2005, 123:1107-1120.
71. Peschard P., et al. Structural basis for ubiquitin-mediated dimerization and activation of the ubiquitin protein ligase Cbl-b. Mol. Cell 2007, 27:475-485.
72. Newton K., et al. Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies. Cell 2008, 134:668-678.
73. Hoeller D., et al. Regulation of ubiquitin-binding proteins by monoubiquitination. Nat. Cell Biol. 2006, 8:163-169.
74. Miller S.L.H., et al. Analysis of the role of ubiquitin-interacting motifs in ubiquitin binding and ubiquitylation. J. Biol. Chem. 2004, 279:33528-33537.
75. Goh A., et al. Components of the ubiquitin-proteasome pathway compete for surfaces on Rad23 family proteins. BMC Biochem. 2008, 9:4.
76. Walters K.J., et al. DNA-repair protein hHR23a alters its protein structure upon binding proteasomal subunit S5a. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:12694-12699.
77. Sasaki T., et al. Budding yeast Dsk2 protein forms a homodimer via its C-terminal UBA domain. Biochem. Bioph. Res. Co. 2005, 336:530-535.
78. Kang Y., et al. UBL/UBA ubiquitin receptor proteins bind a common tetraubiquitin chain. J. Mol. Biol. 2006, 356:1027-1035.
79. Bertolaet B.L., et al. UBA domains mediate protein-protein interactions between two DNA damage-inducible proteins. J. Mol. Biol. 2001, 313:955-963.
80. Kang Y., et al. Ubiquitin receptor proteins hHR23a and hPLIC2 interact. J. Mol. Biol. 2007, 365:1093-1101.
81. Ghaboosi N., Deshaies R.J. A conditional yeast E1 mutant blocks the ubiquitin-proteasome pathway and reveals a role for ubiquitin conjugates in targeting Rad23 to the proteasome. Mol. Biol. Cell 2007, 18:1953-1963.
82. Kim I., et al. The Png1-Rad23 complex regulates glycoprotein turnover. J. Cell Biol. 2006, 172:211-219.
83. Wagner S., et al. Ubiquitin binding mediates the NF-[kappa]B inhibitory potential of ABIN proteins. Oncogene 2008, 27:3739-3745.
84. Parker J.L., et al. Contributions of ubiquitin- and PCNA-binding domains to the activity of polymerase η in Saccharomyces cerevisiae. Nucl. Acids Res. 2007, 35:881-889.
85. Hobeika M., et al. Coordination of Hpr1 and ubiquitin binding by the UBA domain of the mRNA export factor Mex67. Mol. Biol. Cell 2007, 18:2561-2568.
86. Hoyt M., Coffino P. Ubiquitin-free routes into the proteasome. Cell Mol. Life Sci. 2004, 61:1596-1600.
87. Corn P.G., et al. Tat-binding protein-1, a component of the 26S proteasome, contributes to the E3 ubiquitin ligase function of the von Hippel-Lindau protein. Nat. Genet. 2003, 35:229-237.
88. Xie Y., Varshavsky A. Physical association of ubiquitin ligases and the 26S proteasome. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:2497-2502.
89. Jager S., et al. Cic1, an adaptor protein specifically linking the 26S proteasome to its substrate, the SCF component Cdc4. EMBO J. 2001, 20:4423-4431.
90. Coleman M., et al. Ras promotes p21(Waf1/Cip1) protein stability via a cyclin D1-imposed block in proteasome-mediated degradation. EMBO J. 2003, 22:2036-2046.
91. Nakamura Y., et al. Structure of the oncoprotein gankyrin in complex with S6 ATPase of the 26S proteasome. Structure 2007, 15:179-189.
92. Alberti S., et al. Ubiquitylation of BAG-1 suggests a novel regulatory mechanism during the sorting of chaperone substrates to the proteasome. J. Biol. Chem. 2002, 277:45920-45927.
93. Saeki Y., et al. Ubiquitin-like proteins and Rpn10 play cooperative roles in ubiquitin-dependent proteolysis. Biochem. Biophy. Res. Comm. 2002, 293:986-992.
94. Farmer L.M., et al. The RAD23 family provides an essential connection between the 26S proteasome and ubiquitylated proteins in Arabidopsis. Plant Cell 2010, 22:124-142.
95. Smalle J., et al. The pleiotropic role of the 26S proteasome subunit RPN10 in Arabidopsis growth and development supports a substrate-specific function in abscisic acid signaling. Plant Cell 2003, 15:965-980.
96. Girod P., et al. Multiubiquitin chain binding subunit MCB1 (RPN10) of the 26S proteasome is essential for developmental progression in Physcomitrella patens. Plant Cell 1999, 11:1457-1472.
97. Shimada M., et al. Proteasomal ubiquitin receptor RPN-10 controls sex determination in Caenorhabditis elegans. Mol. Biol. Cell 2006, 17:5356-5371.
98. Gallois J.-L., et al. The Arabidopsis proteasome RPT5 subunits are essential for gametophyte development and show accession-dependent redundancy. Plant Cell 2009, 21:442-459.
99. Lam Y.A., et al. A proteasomal ATPase subunit recognizes the polyubiquitin degradation signal. Nature 2002, 416:763-767.
100. 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. 2002, 277:11691-11695.
101. Hamazaki J., et al. Rpn10-mediated degradation of ubiquitinated proteins is essential for mouse development. Mol. Cell Biol. 2007, 27:6629-6638.
102. Szlanka T., et al. Deletion of proteasomal subunit S5a/Rpn10/p54 causes lethality, multiple mitotic defects and overexpression of proteasomal genes in Drosophila melanogaster. J. Cell Sci. 2003, 116:1023-1033.