Ubiquitin-dependent protein degradation

Annual Review of Genetics

Volumn 30, Issue , 1996, Pages 405-439

  Hochstrasser, Mark ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

26S protease; cell cycle; deubiquitinating enzyme; proteasome; yeast

Indexed keywords

PROTEASOME; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN PROTEIN LIGASE;

ANTIGEN PRESENTATION; CELL CYCLE; ENDOCYTOSIS; ENZYME SPECIFICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN MODIFICATION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; CYSTEINE ENDOPEPTIDASES; HYDROLYSIS; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; UBIQUITINS;

EID: 0030457014     PISSN: 00664197     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.genet.30.1.405     Document Type: Review

References (117)

1. Alagramam K, Naider F, Becker JM. 1995. A recognition component of the ubiquitin system is required for peptide transport in Saccharomyces cerevisiae. Mol. Microbiol. 15:225-34
2. Alkalay I, Yaron A, Hatzubai A, Orian A, Ciechanover A, Ben-Neriah Y. 1995. Stimulation-dependent IκBα phosphorylation marks the NFκB inhibitor for degradation via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA 92:10599-603
3. Amon A, Irniger S, Nasmyth K. 1994. Closing the cell cycle circle in yeast: G2 cyclin proteolysis initiated at mitosis persists until the activation of G1 cyclins in the next cycle. Cell 77:1037-50
4. Aristarkhov A, Eytan E, Moghe A, Admon A, Hershko A, Ruderman JV. 1996. E2-C, a cyclin-selective ubiquitin carrier protein required for the destruction of mitotic cyclins. Proc. Natl. Acad. Sci. USA 93:4294-99
5. Arnason T, Ellison MJ. 1994. Stress resistance in Saccharomyces cerevisiae is strongly correlated with assembly of a novel type of multiubiquitin chain. Mol. Cell Biol. 14:7876-83
6. Baboshina OV, Haas AL. 1996. Novel multiubiquitin chain linkages catalyzed by the conjugating enzymes E2EPF and RAD6 are recognized by 26S proteasome subunit 5. J. Biol. Chem. 271:2823-31
7. Bachmair A, Varshavsky A. 1989. The degradation signal in a short-lived protein. Cell 56:1019-32
8. Bailly V, Lamb J, Sung P, Prakash S, Prakash L. 1994. Specific complex formation between yeast RAD6 and RAD18 proteins: a potential mechanism for targeting RAD6 ubiquitin-conjugating activity to DNA damage sites. Genes Dev. 8:811-20
9. Baker RT, Tobias JW, Varshavsky A. 1992. Ubiquitin-specific proteases of Saccharomyces cerevisiae. Cloning of UBP2 and UBP3, and functional analysis of the UBP gene family. J. Biol. Chem. 267:23364-75
10. Bartel B, Wünning I, Varshavsky A. 1990. The recognition component of the N-end rule pathway. EMBO J. 9:3179-89
11. Berleth ES, Pickart CM. 1996. Mechanism of ubiquitin conjugating enzyme E2-230K: catalysis involving a thiol relay? Biochemistry. In press
12. Burch TJ, Haas AL. 1994. Site-directed mutagenesis of ubiquitin. Differential roles for arginine in the interaction with ubiquitin-activating enzyme. Biochemistry 33:7300-7
13. Chau V, Tobias JW, Bachmair A, Marriott D, Ecker DJ, et al. 1989. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243:1576-83
14. Chen P, Johnson P, Sommer T, Jentsch S, Hochstrasser M. 1993. Multiple ubiquitin-conjugating enzymes participate in the in vivo degradation of the yeast MATα2 repressor. Cell 74:357-69
15. Chen ZJ, Hagler J, Palombella VJ, Melandri F, Scherer D, et al. 1995. Signal-induced site-specific phosphorylation targets IκBα to the ubiquitin-proteasome pathway. Genes Dev. 9:1586-97
16. Chen ZJ, Parent L, Maniatis T. 1996. Site-specific phosphorylation of IκBα by a novel ubiquitination-dependent protein kinase activity. Cell 84:853-62
17. Chen ZJ, Pickart CM. 1990. A 25-kilodalton ubiquitin carrier protein (E2) catalyzes multiubiquitin chain synthesis via lysine 48 of ubiquitin. J. Biol. Chem. 265:21835-42
18. Chiang H-L, Dice J. 1988. Peptide sequences that target proteins to lysosomes for enhanced degradation during serum withdrawal. J. Biol. Chem. 263:6797-805
19. Ciechanover A. 1994. The ubiquitin-proteasome proteolytic pathway. Cell 79:13-21
20. Cox JH, Galardy P, Bennink JR, Yewdell JW. 1995. Presentation of endogenous and exogenous antigens is not affected by inactivation of E1 ubiquitin-activating enzyme in temperature-sensitive cell lines. J. Immunol. 154:511-19
21. DeMarini DJ, Papa FR, Swaminathan S, Ursic D, Rasmussen TP, et al. 1995. The yeast SEN3 gene encodes a regulatory subunit of the 26S proteasome complex required for ubiquitin-dependent protein degradation in vivo. Mol. Cell. Biol. 15:6311-21
22. DeMartino GN, Proske RJ, Moomaw CR, Strong AA, Song X, et al. 1996. Identification, purification, and characterization of a PA700-dependent activator of the proteasome. J. Biol. Chem. 271:3112-18
23. Deshaies RJ. 1995. The self-destructive personality of a cell cycle in transition. Curr. Opin. Cell Biol. 7:781-89
24. Deveraux Q, Ustrell V, Pickart C, Rechsteiner M. 1994. A 26 S protease subunit that binds ubiquitin conjugates. J. Biol. Chem. 269:7059-61
25. Dick LR, Aldrich C, Jameson SC, Moomaw CR, Pramanik BC, et al. 1994. Proteolytic processing of ovalbumin and β-galactosidase by the proteasome to yield antigenic peptides. J. Immunol. 152:3884-94
26. Dohmen RJ, Madura K, Bartel B, Varshavsky A. 1991. The N-end rule is mediated by the UBC2(RAD6) ubiquitin-conjugating enzyme. Proc. Natl. Acad. Sci. USA 88:7351-55
27. Dohmen RJ, Stappen R, McGrath JP, Forrova H, Kolarov J, et al. 1995. An essential yeast gene encoding a homolog of ubiquitin-activating enzyme. J. Biol. Chem. 270:18099-109
28. Egner R, Kuchler K. 1996. The yeast multidrug transporter Pdr5 of the plasma membrane is ubiquitinated prior to endocytosis and degradation in the vacuole. FEBS Lett. 378:177-81
29. Falquet L, Paquet N, Frutiger S, Hughes GJ, Hoang-Van K, Jaton JC. 1995. A human de-ubiquitinating enzyme with both isopeptidase and peptidase activities in vitro. FEBS Lett. 359:73-77
30. Fehling HJ, Swat W, Laplace C, Kühn R, Rajewsky K, Müller U, von Boehmer H. 1994. MHC class I expression in mice lacking the proteasome subunit LMP-7. Science 265:1234-37
31. Fenteany G, Standaert RF, Lane WS, Choi S, Corey EJ, Schreiber SL. 1995. Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 268:726-31
32. Finley D, Chau V. 1991. Ubiquitination. Annu. Rev. Cell Biol. 7:25-69
33. Finley D, Sadis S, Monia BP, Boucher P, Ecker DJ, et al. 1994. Inhibition of proteolysis and cell cycle progression in a multiubiquitination-deficient yeast mutant. Mol. Cell Biol. 14:5501-9
34. Finley D, Varshavsky A. 1985. The ubiquitin system: functions and mechanisms. Trends Biochem. Sci. 10:343-46
35. Galan JM, Moreau V, Andre B, Volland C, Haguenauer-Tsapis R. 1996. Ubiquitination mediated by the Npi1p/Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J. Biol. Chem. 271:10946-52
36. Ghislain M, Udvardy A, Mann C. 1993. S. cerevisiae 26S protease mutants arrest cell division in G2/metaphase. Nature 366:358-62
37. Gottesman S, Maurizi M. 1992. Regulation by proteolysis: energy-dependent proteases and their targets. Microbiol. Rev. 56:592-621
38. Gray CW, Slaughter CA, DeMartino GN. 1994. PA28 activator protein forms regulatory caps on proteasome stacked rings. J. Mol. Biol. 236:7-15
39. Groettrup M, Ruppert T, Kuehn L, Seeger M, Standera S, et al. 1995. The interferon-γ-inducible 11S regulator (PA28) and the LMP2/LMP7 subunits govern the peptide production by the 20S proteasome in vitro. J. Biol. Chem. 270:23808-15
40. Groettrup M, Soza A, Eggers M, Kuehn L, Dick TP, et al. 1996. A role for the proteasome regulator PA28a in antigen presentation. Nature 381:166-68
41. Hadari T, Warms JVB, Rose IA, Hershko A. 1992. A ubiquitin C-terminal isopeptidase that acts on polyubiquitin chains - role in protein degradation. J. Biol. Chem. 267:719-27
42. Haracska L, Udvardy A. 1995. Cloning and sequencing a nonATPase subunit of the regulatory complex of the Drosophila 26S protease. Eur. J. Biochem. 231:720-25
43. Hein C, Springael J-Y, Volland C, Haguenauer-Tsapis R, Andre B. 1995. NPII, an essential yeast gene involved in induced degradation of Gap1 and Fur1 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol. Microbiol. 18:77-87
44. Hershko A, Ciechanover A. 1992. The ubiquitin system for protein degradation. Annu. Rev. Biochem. 61:761-807
45. Hershko A, Heller H, Elias S, Ciechanover A. 1983. Components of ubiquitin-protein ligase system: resolution, affinity purification, and role in protein breakdown. J. Biol. Chem. 258:8206-14
46. Hicke L, Riezman H. 1996. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84:277-87
47. Hilt W, Enenkel C, Gruhler A, Singer T, Wolf DH. 1993. The PRE4 gene codes for a subunit of the yeast proteasome necessary for peptidylglutamyl-peptide-hydrolyzing activity: Mutations link the proteasome to stress- and ubiquitin-dependent proteolysis. J. Biol. Chem. 268:3479-86
48. Hochstrasser M. 1995. Ubiquitin, proteasomes, and the regulation of intracellular protein degradation. Curr. Opin. Cell Biol. 7:215-23
49. Hochstrasser M. 1991. Functions of intracellular protein degradation in yeast. In Genetic Engineering, ed. JK Setlow, 13:307-29. New York: Plenum
50. Hochstrasser M, Varshavsky A. 1990. In vivo degradation of a transcriptional regulator: the yeast α2 repressor. Cell 61:697-708
51. Hogness DS, Cohn M, Monod J. 1955. Studies of the induced synthesis of β-galactosidase in Escherichia coli: the kinetics and mechanism of sulfur incorporation. Biochim. Biophys. Acta 16:99-116
52. Hou D, Cenciarelli C, Jensen JP, Nguygen HB, Weissman AM. 1994. Activation-dependent ubiquitination of a T cell antigen receptor subunit on multiple intracellular lysines. J. Biol. Chem. 269:14244-47
53. Hough R, Pratt G, Rechsteiner M. 1987. Purification of two high molecular weight proteases in rabbit reticulocyte lysate. J. Biol. Chem. 262:8303-13
54. Huang Y, Baker RT, Fischer-Vize JA. 1995. Control of cell fate by a deubiquitinating enzyme encoded by the fat facets gene. Science 270:1828-31
55. Huibregtse JM, Scheffher M, Beaudenon S, Howley PM. 1995. A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc. Natl. Acad. Sci. USA 92:2563-67
56. Huibregtse JM, Scheffner M, Howley PM. 1991. A cellular protein mediates association of p53 with the E6 oncoprotein of human papillomavirus Type-16 or Type-18. EMBO J. 10:4129-35
57. Jentsch S. 1992. The ubiquitin conjugation system. Annu. Rev. Genet. 26:177-205
58. Johnson ES, Gonda DK, Varshavsky A. 1990. cis-trans recognition and subunit-specific degradation of short-lived proteins. Nature 346:287-91
59. King RW, Peters J-M, Tugendreich S, Rolfe M, Hieter P, Kirschner MW. 1995. A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell 81:279-88
60. Knop M, Schiffer HH, Rupp S, Wolf DH. 1993. Vacuolar/lysosomal proteolysis: proteases, substrates, mechanisms. Curr. Opin. Cell Biol. 5:990-96
61. Kolling R, Hollenberg CP. 1994. The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J. 13:3261-71
62. 61a. Kornitzer D, Raboy B, Kulka RG, Fink GR. 1994. Regulated degradation of the transcription factor Gcn4. EMBO J. 13:6021-30
63. Kumar S. 1995. ICE-like proteases in apoptosis. Trends Biochem. Sci. 20:198-202
64. Lahav-Baratz S, Sudakin V, Ruderman JV, Hershko A. 1995. Reversible phosphorylation controls the activity of cyclosome-associated cyclin-ubiquitin ligase. Proc. Natl. Acad. Sci. USA 92:9303-7
65. Levchenko I, Luo L, Baker TA. 1995. Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes Dev. 9:2399-408
66. Loeb KR, Haas AL. 1992. The interferon-inducible 15-kDa ubiquitin homolog conjugates to intracellular proteins. J. Biol. Chem. 267:7806-13
67. Löwe J, Stock D, Jap B, Zwickl P, Baumeister W, Huber R. 1995. Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 Å resolution. Science 268:533-39
68. Ma CP, Slaughter CA, DeMartino GN. 1992. Identification, purification, and characterization of a protein activator (PA28) of the 20-S proteasome (Macropain). J. Biol. Chem. 267:10515-23
69. Ma CP, Vu JH, Proske RJ, Slaughter CA, DeMartino GN. 1994. Identification, purification, and characterization of a high molecular weight, ATP-dependent activator (PA700) of the 20 S proteasome. J. Biol. Chem. 269:3539-47
70. Maupin-Furlow JA, Ferry JG. 1995. A proteasome from the methanogenic archaeon Methanosarcina thermophila. J. Biol. Chem. 270:28617-22
71. 69a. McCracken AA, Brodsky JL. 1996. Assembly of ER-associated protein degradation in vitro: dependence on cytosol, calnexin, and ATP. J. Cell Biol. 132:291-98
72. Melloni E, Salamino F, Sparatore B. 1992. The calpain-calpastatin system in mammalian cells: properties and possible functions. Biochimie 74:217-23
73. Michalek M, Grant E, Gramm C, Goldberg AL, Rock K. 1993. A role for the ubiquitin-dependent proteolytic pathway in MHC class I-restricted antigen presentation. Nature 363:552-54
74. Murakami Y, Matsufuji S, Kameji T, Hayashi S, Igarashi K, et al. 1992. Ornithine decarboxylase is degraded by the 26S proteasome without ubiquitination. Nature 360:597-99
75. Narasimhan J, Rasmussen JL, Haas AL. 1996. Conjugation of the 15-kDa interferon-induced ubiquitin homolog is distinct from that of ubiquitin. J. Biol. Chem. 27:324-30
76. Nishizawa M, Furuno N, Okazaki K, Tanaka H, Ogawa Y, Sagata N. 1993. Degradation of Mos by the N-terminal proline (Pro2)-dependent ubiquitin pathway on fertilization of Xenopus eggs: possible significance of natural selection for Pro2 in Mos. EMBO J. 12:4021-27
77. Nuber U, Schwarz S, Kaiser P, Schneider R, Scheffner M. 1996. Cloning of human ubiquitin-conjugating enzymes UbcH6 and UbcH7 (E2-F1) and characterization of their interaction with E6-AP and RSP5. J. Biol. Chem. 271:2795-800
78. Orlowski M. 1990. The multicatalytic proteinase complex, a major extralysomal proteolytic system. Biochemistry 29:10289-97
79. Palombella VJ, Rando OJ, Goldberg AL, Maniatis T. 1994. The ubiquitin-proteasome pathway is required for processing the NF-κ-B1 precursor protein and the activation of NF-κB. Cell 78:773-85
80. Papa F, Hochstrasser M. 1993. The yeast DOA4 gene encodes a deubiquitinating enzyme related to a product of the human tre-2 oncogene. Nature 366:313-19
81. Parsell DA, Lindquist S. 1993. The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu. Rev. Genet. 27:437-96
82. Peters J-M, Cejka Z, Harris JR, Kleinschmidt JA, Baumeister W. 1993. Structural features of the 26 S proteasome complex. J. Mol. Biol. 234:932-37
83. Peters J-M, Franke WW, Kleinschmidt JA. 1994. Distinct 19S and 20S subcomplexes of the 26S proteasome and their distribution in the nucleus and the cytoplasm. J. Biol. Chem. 269:7709-18
84. Pickart CM. 1988. Ubiquitin activation and ligation. In Ubiquitin, ed. M Rechsteiner, pp. 77-100. New York: Plenum
85. Pickart CM, Rose IA. 1985. Ubiquitin carboxyl-terminal hydrolase acts on ubiquitin carboxyl-terminal amides. J. Biol. Chem. 260:7903-10
86. Pühler G, Weinkauf S, Bachmann L, Muller S, Engel A, et al. 1992. Subunit stoichiometry and three-dimensional arrangement in proteasomes from Thermoplasma acidophilum. EMBO J. 11:1607-16
87. Rechsteiner M. 1988. Regulation of enzyme levels by proteolysis: the role of PEST regions. Adv. Enzyme Regul. 27:135-51
88. Reiss Y, Kaim D, Hershko A. 1988. Specificity of binding of NH2-terminal residue of proteins to ubiquitin-protein ligase. Use of amino acid derivatives to characterize specific binding sites. J. Biol. Chem. 263:2693-98
89. Robinson MS, Watts C, Zerial M. 1996. Membrane dynamics in endocytosis. Cell 84:13-21
90. Rubin DM, Finley D. 1995. The proteasome: a protein-degrading organelle? Curr. Biol. 5:854-58
91. Sadis S, Atienza C, Finley D. 1995. Synthetic signals for ubiquitin-dependent proteolysis. Mol. Cell. Biol. 15:1265-73
92. Scheffner M, Nuber U, Huibregtse JM. 1995. Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thioester cascade. Nature 373:81-83
93. Scherer DC, Brockman JA, Chen Z, Maniatis T, Ballard DW. 1995. Signal-induced degradation of IκBα requires site-specific ubiquitination. Proc. Natl. Acad. Sci. USA 92:11259-63
94. Schimke RT. 1973. Control of enzyme levels in mammalian tissues. Adv. Enzymol. 37:135-87
95. Schoenheimer R. 1942. The Dynamic State of Body Constituents. Cambridge: Harvard Univ. Press. 78 pp.
96. Seemüller E, Lupas A, Stock D, Löwe J, Huber R, Baumeister W. 1995. Proteasome from Thermoplasma acidophilum: a threonine protease. Science 268:579-82
97. Seufert W, Futcher B, Jentsch S. 1995. A ubiquitin-conjugating enzyme involved in the degradation of both S- and M-phase cyclins. Nature 373:78-81
98. Seufert W, Jentsch S. 1990. Ubiquitin-conjugating enzymes UBC4 and UBC5 mediate selective degradation of short-lived and abnormal proteins. EMBO J. 9:543-50
99. Shaeffer JR, Kania MA. 1995. Degradation of monoubiquitinated alpha-globin by 26S proteasomes. Biochemistry 34:4015-21
100. Spence J, Sadis S, Haas AL, Finley D. 1995. A ubiquitin mutant with specific defects in DNA repair and multiubiquitination. Mol. Cell Biol. 15:1265-73
101. Sudakin V, Ganoth D, Dahan A, Heller H, Hershko J, et al. 1995. The cyclosome, a large complex containing cyclin-selective ubiquitin ligase activity, targets cyclins for destruction at the end of mitosis. Mol. Biol. Cell. 6:185-97
102. Thanos D, Maniatis T. 1995. NF-κB: a lesson in family values. Cell 80:529-32
103. Todd MJ, Lorimer GH, Thirumalai D. 1996. Chaperonin-facilitated protein folding: optimization of rate and yield by an iterative annealing mechanism. Proc. Natl. Acad. Sci. USA 93:4030-35
104. Udvardy A. 1993. Purification and characterization of a multiprotein component of the Drosophila 26 S (1500 kDa) proteolytic complex. J. Biol. Chem. 268:9055-62
105. Van Kaer L, Ashton-Rickardt PG, Eichelberger M, Gaczynska M, Nagashima K, et al. 1994. Altered peptidase and viral-specific T cell response in LMP2 mutant mice. Immunity 1:533-41
106. van Nocker S, Deveraux Q, Rechsteiner M, Vierstra RD. 1996. Arabidopsis MBP1 gene encodes a conserved ubiquitin recognition component of the 26S proteasome. Proc. Natl. Acad. Sci. USA 93:856-60
107. van Nocker S, Vierstra RD. 1993. Multiubiquitin chains linked through lysine 48 are abundant in vivo and are competent intermediates in the ubiquitin proteolytic pathway. J. Biol. Chem. 268:24766-73
108. Varshavsky A. 1992. The N-end rule. Cell 69:725-35
109. Wickner S, Gottesman S, Skowyra D, Hoskins J, McKenney K, Maurizi MR. 1994. A molecular chaperone, ClpA, functions like DnaK and DnaJ. Proc. Natl. Acad. Sci. USA 91:12218-22
110. Wiertz EJHJ, Jones TR, Sun L, Bogyo M, Geuze HJ, Ploegh HL. 1996. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84:769-80
111. Wilkinson KD. 1995. Roles of ubiquitinylation in proteolysis and cellular regulation. Annu. Rev. Nutr. 15:161-89
112. Wilkinson KD, Tashayev VL, O'Connor LB, Larsen CN, Kasperek E, Pickart CM. 1995. Metabolism of the polyubiquitin degradation signal: structure, mechanism, and role of isopeptidase T. Biochemistry 34:14535-46
113. Yaglom J, Linskens HK, Sadis S, Rubin DM, Futcher B, Finley D. 1995. p34Cdc28-mediated control of Cln3 cyclin degradation. Mol. Cell Biol. 15:731-41
114. Yang Y, Früh K, Ahn K, Peterson PA. 1995. In vivo assembly of the proteasomal complexes, implications for antigen presentation. J. Biol. Chem. 270:27687-94
115. Yu H, King RW, Peters J-M, Kirschner MW. 1996. A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Curr. Biol. 6:455-66
116. Zeng H, Qian Z, Myers MP, Rosbash M. 1996. A light-entrainment mechanism for the Drosophila circadian clock. Nature 380:129-35
117. Zhu Y, Carroll M, Papa FR, Hochstrasser M, D'Andrea AD. 1996. DUB-1, a novel deubiquitinating enzyme with growth-suppressing activity. Proc. Natl. Acad. Sci. USA 93:3275-79