Ubiquitin-mediated proteolysis: Biological regulation via destruction

BioEssays

Volumn 22, Issue 5, 2000, Pages 442-451

  Ciechanover, Aaron ^b   Orian, Amir ^c   Schwartz, Alan L ^a  

^a ST LOUIS CHILDREN S HOSPITAL   (United States)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

LIGASE; UBIQUITIN;

ANIMAL; FORECASTING; HUMAN; INTRACELLULAR FLUID; METABOLISM; REVIEW;

ANIMALS; FORECASTING; HUMANS; INTRACELLULAR FLUID; LIGASES; UBIQUITINS;

EID: 0034065822     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1521-1878(200005)22:5<442::AID-BIES6>3.0.CO;2-Q     Document Type: Review

References (90)

1. Hershko A, Ciechanover A. Mechanisms of intracellular protein breakdown Annu Rev Biochem 1982; 51:335-364.
2. Kornitzer D, Ciechanover, A. Modes of regulation of ubiquitin-mediated protein degradation. J Cell Physiol 2000; 182:1-11.
3. Laney JD, Hochstrasser M. Substrate targeting in the ubiquitin system Cell 1999;97427-430.
4. Koepp DM, Harper JW, Elledge SJ. How the cyclin became a cyclin: Regulated proteolysis in the cell cycle. Cell 1999;97:431-434.
5. Voges D, Zwickl P, Baumeister W. The 26S proteasome: A molecular machine designed for controlled proteolysis. Annu Rev Biochem 1999; 68:1015-1068.
6. DeMartino GN, Slaughter CA. The proteasome, a novel protease regulated by multiple mechanisms. J Biol Chem 1999;274:22123-22126.
7. Rock KL, Goldberg AL. Degradation of cell proteins and the generation of MHC class I-presented peptides. Annu Rev Immunol 1999;17: 739-779.
8. Page AW, Hieter P. The anaphase-promoting complex: New subunits and regulators. Annu Rev Biochem 1999;68:583-609.
9. Deshaies RJ. SCF and Cullin/Ring H2-based ubiquitin ligases. Annu Rev Cell Dev Biol 1999;15:435-467.
10. Peters J-M. Harris JR. Finley D, eds. Ubiquitin and the biology of the cell New York and London: Plenum Press; 1998. pp. 1-472.
11. Breitschopf K, Bengal E, Ziv T, Admon A, Ciechanover A. A novel site for ubiquitination: The N-termmal residue and not internal lysines of MyoD is essential for conjugation and degradation of the protein. EMBO J 1998;17:5964-5973.
12. Hofmann, RM, Pickart CM. Norcanonical MMS2-encoded ubiquitin-conjugating enzyme functions of assembly of novel polyubiquitin chains for DNA repair. Cell 1999;96645-653.
13. Mastrandrea LD, You J, Niles EG, Pickart CM. E2/E3-mediated assembly of lysine 29-linked polyubiquitin chains. J Biol Chem 1999;274: 27299-27306.
14. Koeg M, Hoppe T, Schlenker S. Ulrich HD, Mayer TU, Jentsch S. A novel ubiquit nation factor, E4, is involved in multiubiquitin chain assembly. Cell 1999;96:635-644.
15. Plemper RK, Wolf, DH. Retrograde protein translocation: ERADication of secretory proteins in health and disease. Trends Biochem Sci 1999;24: 266-270.
16. Bonifacino JS, Weissman AM. Ubiquitin and the control of protein fate in the secretory and endocytic pathways. Annu Rev Cell Dev Biol 1998;14: 19-57.
17. Varshavsky A. The N-end rule: functions, mysteries, uses. Proc Natl Acad Sci USA 1996; 93:12142-12149.
18. Heller H, Hershko A. A ubiquitin-protein ligase specific for type III protein substrates. J Biol Chem 1990;265:6532-6535.
19. Huibregtse JM, Scheffner M, Beaudenon S, Howley PM. A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc Natl Acad Sci USA 1995;92:2563-2567.
20. Scheffner M, Nuber U, Huibregtse JM. Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thioester cascade. Nature 1995;373:81-83.
21. Scheffner M, Huibregtse JM, Vierstra RD, Howley PM. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 1993;75:495-505.
22. Oda H, Kumar S, Howley PM. Regulation of the Src family tyrosine kinase Blk through E6 AP-mediated ubiquitination. Proc Natl Acad Sci USA 1999;96:9557-9562.
23. Abriel H, Loffing J, Rebhun JF, Pratt JH, Schild L, Horisberger JD, Rotin D. Staub O Defective regulation of the epithelial Na+ channel by Nedd4 in Liddle's syndrome. J Clin Invest 1999;103:667-673.
24. Galan JM, Moreau V, André B. Volland C, Haguenauer-Tsapis R. Ubiquitination mediated by the Npi1p/Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J Biol Chem 1996;271:10946-10952.
25. Zhu H, KavsakP, Abdollah S. Wrana JL, Thomsen GH. A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 1999;400:687-693.
26. King RW, Peters JM, Tugendreich S Rolfe M, Hieter P, Kirschner MW. A 20S complex containing Cdc27 and Cdc16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell 1995;81:279-288.
27. Sudakin V, Ganoth D, Dahan A, Heller H, Hershko J, Luca FC, Ruderman JV, Hershko A. The cyclosome, a large complex containing cyclin-selective ubiquitin ligase activity, targets cyclins for destruction at the end of mitosis. Mol Biol Cell 1995;6:185-198.
28. Zachariae W, Shevchenko A, Andrews PD, Ciosk R, Galova M, Stark MJ, Mann M, Nasmyth K. Mass spectrometric analysis of the anaphase-promoting complex from yeast: identification of a subunit related to cullins. Science 1998;279:1216-1219.
29. Visintin R, Prinz S, Amon A. Cdc20 and Cdh1: a family of substrate-specific activators of APC-dependent proteolysis. Science 1997;278: 460-463
30. Kramer ER, Gieffers C, Holzl G, Hengstschlager M, Peters J-M. Activation of the human anaphase promoting complex by proteins of the Cdc20/Fizzy family. Curr Biol 1998;8:1207-1210.
31. Fang G, Yu H, Kirschner MW. The checkpoint protein MAD2 and the mitotic regulator Cdc20 form a ternary complex wth the anaphase-promoting complex to control anaphase initiation. Genes Dev 1998;12: 1871-1883.
32. Jasoersen SL, Charles JF, Morgan DO. Inhibitory phosphorylation of the APC regulator Hct1 is controlled by the kinase Cdc28 and the phosphatase Cdc14. Curr Biol 1999;9:227-236.
33. Shteinberg M, Protopopov Y, Listovsky T, Brandeis M, Hershko, A. Phosphorylation of the cyclosome is required for its stimulation by Fizzy/ cdc20. Biochem Biophys Res Commun 1999;260:193-198.
34. Gonen H, Bercovich B. Orian A, Carrano A, Takizawa C, Yamanaka K, Pagano M, Iwai K, Ciechanover A. Identification of the ubiquitin carrier proteins, E2s, involved in signal-induced conjugation and subsequent degradation of lκBα. J Biol Chem 1999;274:14823-14830.
35. Kamura T, Koepp DM, Conrad MN, Skowyra D, Moreland RJ, Ilipoulos O, Lane WS, Kaelin Jr. WG, Elledge SJ, Conaway RC Harper JW, Conaway JW, Rbx1, a component of the VHL tumor suppressor complex and SCF ubiquitin ligase. Science 1999;284:657-661.
36. Tan P, Fuchs SY, Chen A, Wu K, Gomez C Rona Z, Pan Z-Q. Recruitment of a Roc1-Cul1 ubiquitin ligase by Skp1 and HOS to catalyze the ubiquitination of lκBα. Mol Cell 1999;3:527-533.
37. Kitagawa K, Skowyra D, Elledge SJ, Harper JW, Hieter P. SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a novel subunit of the SCF ubiquitin ligase complex. Mol Cell 1999;4: 21-33.
38. Yaron A, Hatzubai A, Davis M, Lavon I, Amit S, Manning AM, Andersen JS, Mann M, Mercuno F, Ben-Neriah Y. Identification of the receptor component of the lκ-Bα-ubiquitin ligase. Nature 1998;396: 590-594.
39. Kitagawa M, Hatakeyama S, Shirane M, Matsumoto M, Ishida N, Hattori K, Nakamichi I, Kikuchi A, Nakayama K, Nakayama K. An F-box protein, FWD1, mediates ubiquitin-dependent proteolysis of β-catenin. EMBO J 1999;18:2401-2410.
40. Margottin F, Bour SP, Durand H, Selig L, Benichou S, Richard V, Thomas D, Strebel K, Benarous R. A novel human WD protein, h-β-TrCp, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif. Mol Cell 1998;1:565-574.
41. Skp2 and E2F-1 underlies regulation of E2F-1 degradation. Nature Cell Biol 1999;1:14-19.
42. Carrano AC, Eytan E, Hershko A, Pagano M. Skp2 is required for ubiquitin-mediated degradation of the Cdk inhibitor p27. Nature Cell Biol 1999;1:193-199.
43. Lorick KL, Jensen JP, Fang S, Ong AM, Hatakeyama S, Weissman AM. RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc Natl Acad Sci USA 1999;96: 11364-11369.
44. Lee PSW, Wang Y, Dominguez MG, Yeung YG, Murphy MA, Bowtell DDL, Stanley ER. The cbl protooncoprotein stimulates CSF-1 receptor multiubiquitination and endocytosis, and attenuates macrophage proliferation. EMBO J 1999;18:3616-3628.
45. Levkowitz G, Waterman H, Ettenberg SA, Katz M, Tsygankov AY, Alroy I, Lavi S, Iwai K, Reiss Y, Ciechanover A, Lipkowitz S, Yarden Y. Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol Cell 1999;4:1029-1040
46. Miyake S, Mullane-Robinson KP, Lill NL, Douillard P, Band H. Cbl-mediated negative regulation of platelet-derived growth factor receptor-dependent cell proliferation. A critical role for Cbl tyrosine kinase-binding domain. J Biol Chem 1999;274:16619-16628.
47. Xie Y, Varshavsky A. The E2-E3 interaction in the N-end rule pathway: the RING-H2 finger of E3 is required for the synthesis of multiubiquitin chain. EMBO J 1999;18:6832-6844.
48. Lisztwan J, Imbert G, Wirbelauer C, Gstaiger M, Krek W. The von Hippel-Lindau tumor suppressor protein is a component of an E3 ubiquitin-protein ligase activity. Genes Dev 1999;13:1822-1833.
49. Iwai K, Yamanaka K, Kamura T, Minato N, Conaway RC, Conaway JW, Klausner RD, Pause A. Identification of the von Hippel-Lindau tumor suppressor protein as part of an active E3 ubiquitin ligase complex. Proc Natl Acad Sci USA 1999;96:12436-12441.
50. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999;399:271-275.
51. Glickman MH, Rubin DM, Coux O, Wefes I, Pfeifer G, Cjeka Z, Baumeister W, Fried VA, Finley D. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and elF3. Cell 1998;94:615-623.
52. van Nocker S, Sadis S, Rubin DM, Glickman M, Fu H, Coux O, Wefes I, Finley D, Vierstra RD 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 lurnover. Mol Cell Biol 1996;16:6020-6028.
53. Gröll M, Ditzel L, Lowe J, Stock D, Bochtler M, Bartunik HD, Huber, R. Structure of 20S proteasome from yeast at 2.4 Å resolution. Nature 1997;386:463-471.
54. Braun BC, Glickman M, Kraft R, Dahlmann B, Kloetzel P-M, Finley D, Schmidt M. The base of the proteasome regulatory particle exhibits chaperone-like activity. Nature Cell Biol 1999;1:221-226.
55. Wilkinson KD. Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. FASEB J 1997;11:1245-1256.
56. Moazed D, Johnson D. A deubiquitinating enzyme interacts with SIR4 and regulates silencing in S. cerevisiae. Cell 1996;86:667-877.
57. Huang Y, Baker RT, Fischer-Vize JA. Control of cell fate by a deubiquitinating enzyme encoded by the fat facets gene. Science 1995;270:1828-1831.
58. Zhu Y, Carroll M, Papa FR, Hochstrasser M, D'Andrea AD. DUB-1, a deubiquitinating enzyme with growth-suppressing activity. Proc Natl Acad Sci USA 1996;93:3275-3279.
59. Saigon K, Wang YL, Suh JG, Yamanishi T, Sakai Y, Kiyosawa H, Harada T, Ichihara N, Wakana S, Kikuchi T, Wada K. Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice. Nat Genet 1999;23:47-51.
60. Freedman DA, Levine AJ. Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol Cell Biol 1998;18:7288-7293.
61. Kip1 is instigated by Jab1. Nature 1999;398:160-165.
62. Hayashi S, Murakami Y, Matsufuji S. Ornithine decarboxylase antizyme: a novel type of regulatory protein. Trends Biochem Sci 1996;21: 27-30.
63. Hicke L. Gettin' down with ubiquitin: turning off cell-surface receptors, transporters and channels. Trends Cell Biol 1999;9:107-112.
64. Lin L, Ghosh S. A glycine-rich region in NF-κB p105 functions as a processing signal for generation of the p50 subunit. Mol Cell Biol 1996;16:2248-2254.
65. Orian A, Schwartz AL, Israël A, Whiteside S, Kahana C, Ciechanover A. Structural motifs involved in ubiquitin-mediated processing of the NF-κB precursor p105: roles of the glycine-rich region and a downstream ubiquitination domain. Mol Cell Biol 1999;19:3664-3673.
66. Heissmeyer V, Krappmann D, Wulczyn FG, Scheidereit C. NFκB p105 is a target of lκB kinases and controls signal induction of Bcl-3-p50 complexes. EMBO J 1999;18:4766-4778.
67. Lecker SH, Solomon V, Mitch WE, Goldberg AL. Muscle protein breakdown and the critical role of ubiquitin-proteasome pathway in normal and disease states. J Nutr 1999;129:227S-237S.
68. Haas AL, Baboshina O, Williams B, Schwartz LM. Coordinated induction of the ubiquitin conjugation pathway accompanies the developmentally programmed death of insect skeletal muscle. J Biol Chem 1995; 270:9407-9412.
69. Skp2 are essential elements of the cyclin A-CDK2 S phase kinase. Cell 1995; 82:915-925.
70. Nishizawa M, Okazaki K, Furuno N, Watanabe N, Sagata N. The 'second-codon rule' and autophosphorylation govern the stability and activity of Mos during the meiotic cell cycle in Xenopus oocytes. EMBO J 1992;11: 2433-2446.
71. Okazak K, Sagata N. The Mos/MAP kinase pathway stabilizes c-Fos by phosphorylation and augments its transforming activity in NIH 3T3 cells. EMBO J. 1995;14:5048-5059.
72. Dimmeler S. Breitschopf K, Haendeler J, Zeiher AM. Dephosphorylation targets Bcl-2 for ubiquitin-dependent degradation: a link between the apoptosome and the proteasome pathway. J Exp Med 1999;189: 1815-1822.
73. Lee DH, Sherman MY, Goldberg AL. Involvement of the molecular chaperone YdJ1 in the ubiquitin-dependent degradation of short-lived and abnormal proteins in Saccharomyces cerevisiae. Mol Cell Biol 1996;16:4773-4781.
74. Bercovich B, Stancovski I, Mayer A, Blumenfeld N, Laszlo A, Scnwartz AL, Ciechanover A. Ubiquitin-dependent degradation of certain protein substrates in vitro requires the molecular chaperone Hsc70. J Biol Chem 1997;272:9002-9010.
75. Johnson PR, Swanson R, Rakhilina L, Hochstrasser M. Degradation signal masking by heterodimerization of MATα2 and MATa1 blocks their mutual destruction by the ubiquitin-proteasome pathway. Cell 1998;94: 217-227.
76. Abu-Shaar M, Mann RS. Generation of multiple antagonistic domains along the proximodistal axis during Drosophila leg development. Development 1998;125:3821-3830.
77. Abu Hatoum O, Gross-Mesilaty S, Breitschopf K, Hoffman A, Gonen H, Ciechanover A, Bengal E. Degradation of myogenic transcription factor MyoD by the ubiquitin pathway in vivo and in vitro: regulation by specific DNA binding. Mol Cell Biol 1998;18:5670-5677.
78. Fang P, Lev-Lehman E, Tsai TF, Matsuura T. Benton CS. Sutcliffe JS. Christian SL, Kubota T, Halley DJ, Meijers-Heijboer H, Langlois S, Graham JM Jr, Beuten J, Willems PJ, Ledbetter DH, Beaudet AL. The spectrum of mutations in UBE3A causing Angelman syndrome. Hum Mol Genet 1999;8:129-135.
79. Iwasaha T, Oh-uchida M, Matsuo N, Yokoyama M, Fukuda K, Hara K, Fukuyama K, Hori K, Sugimori H. Correlation between HPV positivity and state of the p53 gene in cervical carcinoma cell lines. Gynecol Oncol 1993;48:104-109.
80. Tsihlias J, Kapusta L, Slingerland J. The prognostic significance of altered cyclin-dependent kinase inhibitors in human cancer. Annu Rev Med 1999;50:401-423.
81. van Leeuwen FW, de Kleijn DP, van den Hurk HH, Neubauer A, Sonnemans MA, Sluijs JA, Koycu S, Ramdjielal RDJ, Salehi A, Martens GJM, Grosveld FG, Peter J, Burbach H, Hol EM. Frameshift mutants of β amyloid precursor protein and ubiquitin-B in Alzheimer's and Down patients. Science 1998;279:242-247.
82. Leroy E, Boyer R, Auburger G, Leube B, Ulm G, Mezey E, Harta G, Brownstein MJ, Jonnalagada S, Chernova T, Dehejia A, Lavedan C, Gasser T, Steinbach PJ, Wilkinson KD, Polymeropoulos MH. The ubiquitin pathway in Parkinson's disease. Nature 1998;395:451-452.
83. Pallares-Trujillo J, Lopez-Soriano FJ, Argiles JM. The involvement of the ubiquitin system in Alzheimer's disease. Int J Mol Med 1998;2:3-15.
84. Sieradzan KA, Mechan AO Jones L, Wanker EE, Nukina N, Mann DM. Huntington's disease intranuclear inclusions contain truncated, ubiquitinated huntingtin protein. Exp Neurol 1999;156:92-99.
85. Cummings CJ, Mancini MA, Antalffy B, DeFranco DB, Orr HT, Zoghbi HY. Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1. Nature Genet 1998;19:148-154.
86. Yamagishi H, Garg V, Matsuoka R, Thomas T, Srivastava D. A molecular pathway revealing a genetic basis for human cardiac and craniofacial defects. Science 1999;283:1158-1160.
87. Johnson ES, Ma PC, Ota IM, Varshavsky A. A proteolytic pathway that recognizes ubiquitin as a degradation signal. J Biol Chem 1995;270:17442-17456.
88. Ward CL, Omura S, Kopito RR. Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 1995;83:121-127.
89. Levitskaya J, Sharipo A, Leonchiks A, Ciechanover A, Masucci MG. Inhibition of ubiquitin/proteasome-dependent protein degradation by the Gly-Ala repeat domain of the Epstein-Barr virus nuclear antigen 1. Proc Natl Acad Sci USA 1997;94:12616-12621.
90. Shamu CE, Story CM, Rapoport TA, Ploegh HL. The pathway of US11-dependent degradation of MHC class I heavy chains involves a ubiquitin-conjugated intermediate. J Cell Biol 1999;147:45-58.