The ubiquitin-proteasome pathway in cancer

British Journal of Cancer

Volumn 77, Issue 3, 1998, Pages 448-455

  Spataro, V ^a,b   Norbury, C ^a   Harris, A L ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Ospedale Civico Lugano   (Switzerland)

Author keywords

Drug resistance; Immune escape; Oncogenesis; Proteasome; Ubiquitin

Indexed keywords

7 HYDROXYSTAUROSPORINE; ACLARUBICIN; ANTIGEN; CAFFEINE; DOXORUBICIN; LACTACYSTIN; LEPTOMYCIN B; MULTIDRUG RESISTANCE PROTEIN; PACLITAXEL; PROTEASOME; PROTEIN; PROTEIN P27; PROTEIN P53; PROTEINASE INHIBITOR; STAUROSPORINE; TRANSCRIPTION FACTOR; UBIQUITIN; UNCLASSIFIED DRUG;

ANTIGEN PRESENTATION; CANCER; CARCINOGENESIS; CELL CYCLE; GENE EXPRESSION REGULATION; HUMAN; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; VIRUS CARCINOGENESIS; WART VIRUS;

EID: 0031973765     PISSN: 00070920     EISSN: None     Source Type: Journal    
DOI: 10.1038/bjc.1998.71     Document Type: Review

References (101)

1. Amon A, Irniger S and 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: 1037-1050
2. Beck S, Kelly A, Radley E, Khurshid F, Alderton RP and Trowsdale J (1992) DNA sequence analysis of 66 kb of the human MHC class II region encoding a cluster of genes for antigen processing. J Mol Biol 228: 433-441
3. Beg AA and Baltimore D (1996) An essential role for NF-κB in preventing TNF-alfa-induced cell death. Science 274: 782-784
4. Belich MP, Glynne RJ, Senger G, Sheer D and Trowsdale J (1994) Proteasome components with reciprocal expression to that of the MHC-encoded LMP proteins. Curr Biol 4: 769-776
5. Betticher DC (1996). Cyclin D1, another molecule of the year? Ann Oncol 7: 223-225
6. Brandeis M (1996) The proteolysis of mitotic cyclins in mammalian cells persists from the end of mitosis until the onset of S phase. Embo J 15: 5280-5289
7. Catzavelos C, Bhattacharya N, Ung YC, Wilson JA, Roncari L, Sandhu C, Shaw P, Yeger H, Morava-Protzner I, Kapusta L, Franssen E, Pritchard KI and Slingerland JM (1997) Decreased levels of the cell-cycle inhibitor p27/Kip 1 protein: prognostic implications in primary breast cancer. Nature Med 3: 227-230
8. Cerundolo V, Benham A, Braud V, Mukherjee S, Gould K, Macino B, Neefjes J and Townsend A (1997) The proteasome-specific inhibitor lactacystin blocks presentation of cytotoxic T lymphocyte epitopes in human and murine cells. Eur J Immunol 27: 336-341
9. Chowdary DR, Dermody JJ, Jha KK and Ozer HL (1994) Accumulation of p53 in a mutant cell line defective in the ubiquitin pathway. Mol Cell Biol 14: 1997-2003
10. Ciechanover A (1994) The ubiquitin-proteasome proteolytic pathway. Cell 79: 13-21
11. Ciechanover A, Shkedy D, Oren M and Bercovich B (1994) Degradation of the tumor suppressor protein p53 by the ubiquitin-mediated proteolytic system requires a novel species of ubiquitin-carrier protein. E2. J Biol Chem 269: 9582-9589
12. Ciocca DR, Fuqua SA, Lock Lim S, Toft DO, Welch WJ and McGuire WL (1992) Response of human breast cancer cells to heat shock and chemotherapeutic drugs. Cancer Res 52: 3648-3654
13. Claret FX, Hibi M, Dhut S, Toda T and Karin M (1996) A new group of conserved coactivators that increase the specificity of AP-1 transcription factors. Nature 383: 453-157
14. Clurman B, Sheaff R, Thress K, Groudine M and Roberts J (1996) Turnover of cyclin E by the ubiquitin-proteasome pathway is regulated by CDK2 binding and cyclin phosphorylation. Genes Dev 10: 1979-1990
15. Cox LS and Lane DP (1995) Tumour suppressors, kinases and clamps: how p53 regulates the cell cycle in response to DNA damage. Bioessays 17: 501-508
16. Diehl JA, Zindy F and Sherr CJ (1997) Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev. 11: 957-972
17. Dubiel W, Ferrell K and Rechsteiner M (1995a) Subunits of the regulatory complex of the 26S protease. Mol Biol Rep 21: 27-34
18. Dubiel W, Ferrell K, Dumdey R, Standera S, Prehn S and Rechsteiner M (1995b) Molecular cloning and expression of subunit 12: a non-MCP and non-ATPase subunit of the 26S protease. FEBS Lett 363: 97-100
19. Fehling HJ, Swat W, Laplace C, Kühn R, Rajewsky K, Müller U and von Boehmer H (1994) MHC class 1 expression in mice lacking the proteasome subunit LMP-7. Science 265: 1234-1237
20. Fenteany G (1995) Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 268: 726-731
21. Fenteany G, Standaert RF, Reichard GA, Corey EJ and Schreiber SL (1994) A beta-lactone related to lactacystin induces neurite outgrowth in a neuroblastoma cell line and inhibits cell cycle progression in an osteosarcoma cell line. Proc Natl Acad Sci USA 91: 3358-3362
22. Ferrando A (1996) Mutational analysis of the human cyclin dependent kinase inhibitor p27/kip1 in primary breast carcinomas. Hum Genet 97: 91-94
23. Figueiredo Pereira ME, Chen WE, Li J and Johdo O (1996) The antitumor drug aclacinomycin A, which inhibits the degradation of ubiquitinated proteins, shows selectivity for the chymotrypsin-like activity of the bovine pituitary 20S proteasome. J Biol Chem 271: 16455-16459
24. Fornerod M, Van Deursen J, Van Baal S, Reynolds A, Davis D, Murti KG, Fransen J and Grosveld G (1997) The human homologue of yeast CRMI is in a dynamic subcomplex with CAN/Nup214 and a novel nuclear pore component Nup88. Embo J 16: 807-816
25. Fruh K, Gossen M, Wang K, Bujard H, Peterson PA and Yang Y (1994) Displacement of housekeeping proteasome subunits by MHC-encoded LMPs: a newly discovered mechanism for modulating the multicatalylic proteinase complex. Embo J 13: 3236-3244
26. Fujita H, Mukasa T, Tsukahara T, Arahata K, Omura S and Momoi T (1996) Enhancement of CPP32-like activity in the TNF-treated U937 cells by the proteasome inhibitors. Biochem Biophys Res Commun 224: 74-79
27. Gaczynska M, Goldberg AL, Tanaka K, Hendil KB and Rock KL (1996) Proteasome subunits X and Y alter peptidase activities in opposite ways to the interferon-gamma-induced subunits LMP2 and LMP7. J Biol Chem 271: 17275-17280
28. Glotzer M, Murray AW and Kirschner MW (1991) Cyclin is degraded by the ubiquitin pathway. Nature 349: 132-138
29. Gordon C, McGurk G, Dillon P, Rosen C and Hastie ND (1993) Defective mitosis due to a mutation in the gene for a fission yeast 26S protease subunit. Nature 366: 355-357
30. Gordon C, McGurk G, Wallace M and Hastie ND (1996) A conditional lethal mutant in the fission yeast 26S protease subunit mts3+ is defective in metaphase to anaphase transition. J Biol Chem 271: 5704-5711
31. Gray DA, Inazawa J, Gupta K, Wong A, Ueda R and Takahashi T (1995) Elevated expression of Unph, a proto-oncogene at 3p21.3, in human lung tumors. Oncogene 10: 2179-2183
32. Groettrup M, Ruppert T, Kuehn L, Seeger M, Standera S, Koszinowski U and Kloetzel PM (1995) The interferon-gamma-inducible 11S regulator (PA28) and the LMP2/LMP7 subunits govern the peptide production by the 20S proteasome in vitro. J Biol Chem 270: 23808-23815
33. Groettrup M, Kraft R, Kostka S, Standera S, Stohwasser R and Kloetzel PM (1996) A third interferon-gamma-induced subunit exchange in the 20S proteasome. Eur J Immunol 26: 863-869
34. Groll M, Ditzel L, Löwe J, Stock D, Bochtler M, Bartunik HD and Huber R (1997) Structure of the 20S proteasome from yeast at 2.4 Å resolution. Nature 386: 463-471
35. Harris CC (1996) Structure and function of the p53 tumor suppressor gene: clues for rational cancer therapeutic strategies. J Natl Cancer Inst 88: 1442-1455
36. Hauft Y, Maya R, Kazaz A and Oren M (1997) Mdm2 promotes the rapid degradation of p53. Nature 387: 296-303
37. Hengst L and Reed SI (1996) Translational control of p27Kipl accumulation during the cell cycle. Science 271: 1861-1864
38. Hermida Matsumoto ML, Chock PB, Curran T and Yang DC (1996) Ubiquitinylation of transcription factors c-Jun and c-Fos using reconstituted ubiquitinylating enzymes. J Biol Chem 271: 4930-4936
39. Hisamatsu H, Shimbara N, Saito Y, Kristensen P, Hendil KB, Fujiwara T, Takahashi E, Tanahashi N, Tamura T, Ichihara A and Tanaka K (1996) Newly identified pair of proteasomal subunits regulated reciprocally by interferon gamma. J Exp Med 183: 1807-1816
40. Hochstrasser M (1995) Ubiquitin, proteasomes, and the regulation of intracellular protein degradation. Curr Opin Cell Biol 7: 215-223
41. Hou D, Cenciarelli C, Jensen JP, Nguygen HB and Weissman AM (1994) Activation-dependent ubiquitination of a T cell antigen receptor subunit on multiple intracellular lysines. J Biol Chem 269: 14244-14247
42. Hunter T and Pines J (1994) Cyclins and cancer. II. Cyclin D and CDK inhibitors come of age (see comments). Cell 79: 573-582
43. Ikehata H, Kaneda S, Yamao F, Seno T, Ono T and Hanaoka H (1997) Incubation at the nonpermissive temperature induces deficiencies in UV resistance and mutagenesis in mouse mutant cells expressing a temperature-sensitive ubiquitin-activating enzyme (E1). Mol Cell Biol 17: 1484-1489
44. Imajoh Ohmi S, Kawaguchi T, Sugiyama S, Tanaka K, Omura S and Kikuchi H (1995) Lactacystin, a specific inhibitor of the proteasome, induces apoptosis in human monoblast U937 cells. Biochem Biophys Res Commun 217: 1070-1077
45. Jariel Encontre I, Pariat M, Martin F, Carillo S, Salvat C and Piechaczyk M (1995) Ubiquitinylation is not an absolute requirement for degradation of c-Jun protein by the 26S proteasome. J Biol Chem 270: 11623-11627
46. Keyomarsi K and Pardee AB (1993) Redundant cyclin overexpression and gene amplification in breast cancer cells. Proc Natl Acad Sci USA 90: 1112-1116
47. Keyomarsi K, O'Leary N, Molnar G, Lees E, Fingert HJ and Pardee AB (1994) Cyclin E, a potential prognostic marker for breast cancer. Cancer Res 54: 380-385
48. Keyomarsi K, Conte D, Jr, Toyofuku W and Fox MP (1995) Deregulation of cyclin E in breast cancer. Oncogene 11: 941-950
49. King RW (1996) How proteolysis drives the cell cycle. Science 274: 1652-1659
50. Kuckelkorn U, Frentzel S, Kraft R, Kostka S, Groettrup M and Klbetzel PM (1995) Incorporation of major histocompatibility complex-encoded subunits LMP2 and LMP7 changes the quality of the 20S proteasome polypeptide processing products independent of interferon-gamma. Eur J Immunol 25: 2605-2611
51. Kumada K, Yanagida M and Toda T (1996) Caffeine-resistance in fission yeast is caused by mutations in a single essential gene, crm1+. Mol Gen Genet. 250: 59-68
52. Lam YA, Xu W, DeMartino GN and Cohen RE (1997) Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome. Nature 385: 737-740
53. Lee HW, Smith L, Pettit GR, Vinitsky A and Smith JB (1996) Ubiquitination of protein kinase C-alpha and degradation by the proteasome. J Biol Chem 271: 20973-20976
54. Lillington DM, MacCallum PK, Lister TA and Gibbons B (1993) Translocation t(6;9)(p23;q34) in acute myeloid leukemia without myelodysplasia or basophilia: two cases and a review of the literature. Leukemia 7: 527-531
55. Loda M, Cukor B, Tam SW, Luvin P, Fiorentino M, Draetta GF, Jessup JM and Pagano M (1997) Increased proteasome-dependent degradation of the cyclin-dependent kinase inhibitor p27 in aggressive colorectal carcinomas. Nature Med 3: 231-234
56. Löwe J, Stock D, Jap B, Zwickl P, Baumeister W and Huber R (1995) Crystal structure of the 20S proteasome from the Archaeon T. acidophilum at 3.4 Å resolution. Science 268: 533-539
57. Maki CG, Huibregtse JM and Howley PM (1996) In vivo ubiquitination and proteasome-mediated degradation of p53. Cancer Res 56: 2649-2654
58. Masutani C, Sugasawa K, Yanagisawa J, Sonoyama T, Ui M, Enomoto T, Takio K, Tanaka K, Van der Spek PJ, Bootsma D, Hoeijmakers JHJ and Hanaoka F (1994) Purification and cloning of a nucleotide excision repair complex involving the xeroderma pigmentosum group C protein and a human homologue ot yeast RAD23. Embo J 13: 1831-1843
59. Michalek MT, Grant EP, Gramm C, Goldberg AL and Rock KL (1993) A role for the ubiquitin-dependent proteolytic pathway in MHC class I-restricted antigen presentation. Nature 363: 552-554
60. Moffat GJ, McLaren AW and Wolf CR (1994) Involvement of Jun and Fos proteins in regulating transcriptional activation of the human pi class glutathione S-transferase gene in multidrug-resistant MCF7 breast cancer cells. J Biol Chem 269: 16397-16402
61. Mori S, Kanaki H, Tanaka K, Morisaki N and Saito Y (1995) Ligand-activated platelet-derived growth factor beta-receptor is degraded through proteasome-dependent proteolytic pathway. Biochem Biophys Commun 217: 224-229
62. Morosetti R, Kawamata N, Gombart AF, Miller CW, Hatta Y, Hirama T, Said JW, Tomonaga M and Koeffler HP (1995) Alterations of the p27KIP1 gene in non-Hodgkin's lymphomas and adult T-cell leukemia/lymphoma. Blood 86: 1924-1930
63. Musti AM, Treier M and Bohmann D (1997) Reduced ubiquitin-dependent degradation of c-Jun after phosphorylation by MAP kinases. Science 275: 400-402
64. Nandi D, Jiang H and Monaco JJ (1996) Identification of MECL-1 (LMP-10) as the third IFN-gamma-inducible proteasome subunit. J Immunol 156: 2361-2364
65. Pagano M, Tam SW, Theodoras AM, Beer Romero P, Del Sal G, Chau V, Yew PR, Draetta GF and Rolfe M (1995) Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science 269: 682-685
66. Pahl HL and Baeuerle PA (1996) Control of gene expression by proteolysis. Curr Opin Cell Biol 8: 340-347
67. Palombella VJ, Rando OJ, Goldberg AL and Maniatis T (1994) The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B. Cell 78: 773-785
68. Papa FR and Hochstrasser M (1993) The yeast DOA4 gene encodes a deubiquitinating enzyme related to a product of the human tre-2 oncogene. Nature 366: 313-319
69. Peters JM (1994) Proteasomes: protein degradation machines of the cell. Trends Biochem Sci 19: 377-382
70. Peters JM, Cejka Z, Harris JR, Kleinschmidt JA and Baumeister W (1993) Structural features of the 26 S proteasome complex. J Mol Biol 234: 932-937
71. Philip PA and Harris AL (1995) Potential for protein kinase C inhibitors in cancer therapy. Cancer Treat Res 78: 3-27
72. Pinkus R, Weiner LM and Daniel V (1996) Role of oxidants and antioxidants in the induction of AP-1, NF-kappaB, and glutathione S-transferase gene expression. J Biol Chem 271: 13422-13429
73. Polyak K (1994) p27/kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev 8: 9-22
74. Porter PL, Malone KE, Heagerty PJ, Alexander GM, Gatti LA, Firpo EJ, Daling JR and Roberts JM (1997) Expression of cell-cycle regulators p27/Kip1 and cyclin E, alone or in combination, correlate with survival in young breast cancer patients. Nature Med 3: 222-225
75. Restifo NP, Esquivel F, Kawakami Y, Yewdell JW, Mule JJ, Rosenberg SA and Bennink JR (1993) Identification of human cancers deficient in antigen processing. J Exp Med 177: 265-272
76. Ritke MK, Bergoltz VV, Allan WP and Yalowich JC (1994) Increased c-jun/AP-1 levels in etoposide-resistant human leukemia K562 cells. Biochem Pharmacol 48: 525-533
77. Rock KL, Gramm C, Rothstein L, Clark K, Stein R, Dick L, Hwang D and Goldberg AL (1994) Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class 1 molecules. Cell 78: 761-771
78. Rolfe M, Beer Romero P, Glass S, Eckstein J, Berdo I, Theodoras A, Pagano M and Draetta G (1995) Reconstitution of p53-ubiquitinylation reactions from purified components; the role of human ubiquitin-conjugating enzyme UBC4 and E6-associated protein (E6AP). Proc Natl Acad Sci USA 92: 3264-3268
79. Rotem Yehudar R, Groettrup M, Soza A, Kloetzel PM and Ehrlich R (1996) LMP-associated proteolytic activities and TAP-dependent peptide transport for class 1 MHC molecules are suppressed in cell lines transformed by the highly oncogenic adenovirus 12. J Exp Med 183: 499-514
80. Rubin D and Finley D (1995) The proteasome: a protein-degrading organelle. Curr Biol 5: 854-858
81. Sadoul R, Fernandez PA, Quiquerez, AL, Martinou I, Maki M, Schroter M, Becherer JD, Irmler M, Tschopp J and Martinou JC (1996) Involvement of the proteasome in the programmed cell death of NGF-deprived sympathetic neurons. Embo J 15: 3845-3852
82. Scheffner M, Werness BA, Huibregtse JM, Levine AJ and Howley PM (1990) The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63: 1129-1136
83. Scheffner M, Huibregtse JM, Vierstra RD and Howley PM (1993) The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75: 495-505
84. Schreiber M, Baumann B, Cotten M, Angel P and Wagner EF (1995) Fos is an essential component of the mammalian UV response. Embo 714: 5338-5349
85. Seliger B, Hohne A, Knuth A, Bernhard H, Meyer T, Tampe R, Momburg F and Huber C (1996) Analysis of the major histocompatibility complex class I antigen presentation machinery in normal and malignant renal cells: evidence for deficiencies associated with transformation and progression. Cancer Res 56: 1756-1760
86. Sepp Lorenzino L, Ma Z, Lebwohl DE, Vinitsky A and Rosen N (1995) Herbimycin A induces the 20 S proteasome- und ubiquitin-dependent degradation of receptor tyrosine kinases. J Biol Chem 270: 16580-16587
87. Shaeffer JR and Cohen RE (1996) Differential effects of ubiquitin aldehyde on ubiquitin and ATP-dependent protein degradation. Biochemistry 35: 10886-10893
88. Shimanuki M, Saka Y, Yanagida M and Toda T (1995) A novel essential fission yeast gene pad1+ positively regulates pap1(+)-dependent transcription and is implicated in the maintenance of chromosome structure. J Cell Sci 108: 569-579
89. Shinohara K, Tomioka M, Nakano H, Tone S, Ito H and Kawashima S (1996) Apoptosis induction resulting from proteasome inhibition. Biochem J 317: 385-388
90. Sibille C, Gould KG, Willard Gallo K, Thomson S, Rivett AJ, Powis S, Butcher GW and De Baetselier P (1995) LMP2+ proteasomes are required for the presentation of specific antigens to cytotoxic T lymphocytes. Curr Biol 5: 923-930
91. Slingerland JM (1994) A novel inhibitor of cyclin/Cdk activity detected in TGF-beta arrested epithelial cells. Mol Cell Biol 14: 3683-3694
92. Spataro V, Toda T, Craig R, Seeger M, Dubiel W, Harris AL and Norbury C (1997) Resistance to diverse drugs and to ultraviolet light conferred by overexpression of a novel human 265 proteasome subunit. J Biol Chem (in press)
93. Toda T, Shimanuki M, Saka Y, Yamano H, Adachi Y, Shirakawa M, Kyogoku Y and Yanagida M (1992) Fission yeast pap1-dependent transcription is negatively regulated by an essential nuclear protein, crm1. Mol Cell Biol 12: 5474-5484
94. Treier M, Staszewski LM and Bohmann D (1994) Ubiquitin-dependent c-Jun degradation in vivo is mediated by the delta domain. Cell 78: 787-798
95. Tsurumi C, Ishida N, Tamura T, Kakizuka, A, Nishida E, Okumura E, Kishimoto T, Inagaki M, Okazaki K, Sagata N, Ishihara A and Tanaka K (1995a) Degradation of c-Fos by the 26S proteasome is accelerated by c-Jun and multiple protein kinases. Mol Cell Biol 15: 5682-5687
96. Tsurumi C, DeMartino GN, Slaughter CA, Shimbara N and Tanaka K (1995b) cDNA cloning of p40, a regulatory subunit of the human 26S proteasome, and a homolog of the Mov-34 gene product. Biochem Biophys Res Commun 210: 600-608
97. Van Antwerp DJ, Martin SJ, Kafri T, Green D and Verma IM (1996) Suppression of TNF-alfa-induecd apoptosis by NF-κB. Science 274: 787-789
98. Wang CY, Mayo MW and Baldwin ASJ (1996) TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-κB. Science 274: 784-787
99. Watkins JF, Sung P, Prakash L and Prakash S (1993) The Saccharomyces cerevisiae DNA repair gene RAD23 encodes a nuclear protein containing a ubiquitin-like domain for biological function. Mol Cell Biol 13: 7757-7765
100. Yao KS, Godwin AK, Johnson SW, Ozols RF, O'Dwyer PJ and Hamilton TC (1995) Evidence for altered regulation of gamma-glutamylcysteine synthetase gene expression among cisplatin-sensitive and cisplatin-resistant human ovarian cancer cell lines. Cancer Res 55: 4367-1374
101. Zhou M, Wu X and Ginsberg HN (1996) Evidence that a rapidly turning over protein, normally degraded by proteasomes, regulates hsp72 gene transcription in HepG2 cells. J Biol Chem 271: 24769-24775