The ubiquitin-proteasome system in cancer, a major player in DNA repair. Part 1: Post-translational regulation

Journal of Cellular and Molecular Medicine

Volumn 13, Issue 9 B, 2009, Pages 3006-3018

  Vlachostergios, Panagiotis J ^a   Patrikidou, Anna ^a   Daliani, Danai D ^a   Papandreou, Christos N ^a  

^a UNIVERSITY HOSPITAL OF LARISSA   (Greece)

Author keywords

Base excision repair; DNA repair; Double strand break repair; Fanconi anaemia pathway; MGMT; Mismatch repair; NEDD8; Nucleotide excision repair; Post replication repair; SUMO; Ubiquitin proteasome system

Indexed keywords

NUCLEOTIDE; PROTEASOME; TRANSCRIPTION FACTOR; UBIQUITIN;

ANIMAL; CHO CELL; CRICETULUS; DNA DAMAGE; DNA REPAIR; FANCONI ANEMIA; HAMSTER; HUMAN; METABOLISM; NEOPLASM; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; DNA DAMAGE; DNA REPAIR; FANCONI ANEMIA; HUMANS; NEOPLASMS; NUCLEOTIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UBIQUITIN;

EID: 74549153376     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2009.00824.x     Document Type: Review

References (98)

1. Hansen WK, Kelley MR. Review of mammalian DNA repair and translational implications. J Pharmacol Exp Ther. 2000, 295:1-9.
2. Christmann M, Tomicic MT, Roos WP. Mechanisms of human DNA repair: an update. Toxicology. 2003, 193:3-34.
3. Wood RD, Mitchell M, Lindahl T. Human DNA repair genes. Mutat Res. 2005, 577:275-83.
4. Pourquier P. La réparation de l' ADN, cible potentielle d'un développement thérapeutique en cancérologie. Bull Cancer. 2006, 124-44. hors série
5. Sánchez-Pérez I. DNA inhibitors in cancer treatment. Clin Transl Oncol. 2006, 8:642-6.
6. Damia G, D'Incalci M. Targetting DNA repair as a promising approach in cancer therapy. Eur J Cancer. 2007, 43:1791-801.
7. Barbour L, Xiao W. Regulation of alternative replication bypass pathways at stalled replication forks and its effects on genome stability: a yeast model. Mutat Res. 2003, 532:137-55.
8. Kennedy RD, D' Andrea AD. The Fanconi Anemia/BRCA pathway: new faces in the crowd. Genes Dev. 2005, 19:2925-40.
9. Tsantoulis PK, Kotsinas A, Sfikakis PP. Oncogene-induced replication stress preferentially targets common fragile sites in preneoplastic lesions. A genome-wide study. Oncogene. 2008, 27:3256-64.
10. Gorgoulis VG, Vassiliou LV, Karakaidos P. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature. 2005, 434:907-13.
11. Baumeister W, Walz J, Zuhl F. The proteasome: paradigm of a self-compartmentalizing protease. Cell. 1998, 92:367-80.
12. Ciechanover A, Orian A, Schwartz AL. The ubiquitin-mediated proteolytic pathway: mode of action and clinical implications. J Cell Biochem Suppl. 2000, 34:40-51.
13. Adams J. The proteasome: structure, function, and role in the cell. Cancer Treat Rev. 2003, 29(Suppl 1):S3-9.
14. Behuliak M, Celec P, Gardlik R. Ubiquitin - the kiss of death goes Nobel. Will you be quitting. Bratisl Lek Listy 2005, 106:93-100.
15. Hermann J, Lerman LO, Lerman A. Ubiquitin and ubiquitin-like proteins in protein regulation. Circ Res. 2007, 100:1276-91.
16. Ciechanover A. Intracellular protein degradation: from a vague idea through the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Cell Death Differ. 2005, 12:1178-90.
17. Reinstein E, Ciechanover A. Narrative review: protein degradation and human diseases: the ubiquitin connection. Ann Intern Med. 2006, 145:676-84.
18. Sun F, Anantharam V, Latchoumycandane C. Dieldrin induces ubiquitin-proteasome dysfunction in alpha-synuclein overexpressing dopaminergic neuronal cells and enhances susceptibility to apoptotic cell death. J Pharmacol Exp Ther. 2005, 315:69-79.
19. Sun F, Kanthasamy A, Anantharam V. Environmental neurotoxic chemicals-induced ubiquitin proteasome system dysfunction in the pathogenesis and progression of Parkinson's disease. Pharmacol Ther. 2007, 114:327-44.
20. Mani A, Gelmann EP. The ubiquitin-proteasome pathway and its role in cancer. J Clin Oncol. 2005, 23:4776-89.
21. Haglund K, Dikic I. Ubiquitylation and cell signalling. EMBO J. 2005, 24:3353-9.
22. Pegg AE, Wiest L, Mummert C. Use of antibodies to human O6-alkylguanine-DNA alkyltransferase to study the content of this protein in cells treated with O6-benzylguanine or N-methyl-N'-nitro-N-nitrosoguanidine. Carcinogenesis. 1991, 12:1679-83.
23. Srivenugopal KS, Yuan XH, Friedman HS. Ubiquitination-dependent proteolysis of O6-methylguanine-DNA methyltransferase in human and murine tumor cells following inactivation with O6-benzylguanine or 1,3-bis(2-chloroethyl)-1-nitrosourea. Biochemistry. 1996, 35:1328-34.
24. Xu-Welliver M, Pegg AE. Degradation of the alkylated form of the DNA repair protein, O6-alkylguanine-DNA alkyltransferase. Carcinogenesis. 2002, 23:823-30.
25. Hernandez-Pigeon H, Laurent G, Humbert O. Degradation of mismatch repair hMutSα heterodimer by the ubiquitin-proteasome pathway. FEBS Lett. 2004, 562:40-4.
26. El-Shemerly M, Janscak P, Hess D. Degradation of human exonuclease 1b upon DNA synthesis inhibition. Cancer Res. 2005, 65:3604-9.
27. Hardeland U, Kunz C, Focke F. Cell cycle regulation as a mechanism for functional separation of the apparently redundant uracil DNA glycosylases TDG and UNG2. Nucleic Acids Res. 2007, 35:3859-67.
28. Wang T, Simbulan-Rosenthal CM, Smulson ME. Polyubiquitylation of PARP-1 through ubiquitin K48 is modulated by activated DNA, NAD+, and dipeptides. J Cell Biochem. 2008, 104:318-28.
29. Lommel L, Chen L, Madura K. The 26S proteasome negatively regulates the level of overall genomic nucleotide excision repair. Nucleic Acids Res. 2000, 28:4839-45.
30. Lommel L, Ortolan T, Chen L. Proteolysis of a nucleotide excision repair protein by the 26S proteasome. Curr Genet. 2002, 42:9-20.
31. Sweder K, Madura K. Regulation of repair by the 26S proteasome. J Biomed Biotechnol. 2002, 2:94-105.
32. Ng JM, Vermeulen W, van der Horst GT. A novel regulation mechanism of DNA repair by damage-induced and RAD23-dependent stabilization of xeroderma pigmentosum group C protein. Genes Dev. 2003, 17:1630-45.
33. Madura K. The ubiquitin-associated (UBA) domain. Cell Cycle. 2002, 1:235-44.
34. Goh AM, Walters KJ, Elsasser S. Components of the ubiquitin-proteasome pathway compete for surfaces on Rad23 family proteins. BMC Biochem. 2008, 9:4-13.
35. Okuda Y, Nishi R, Ng JM. Relative levels of the two mammalian Rad23 homologs determine composition and stability of the xeroderma pigmentosum group C protein complex. DNA Repair. 2004, 3:1285-95.
36. Hiyama H, Yokoi M, Masutani C. Interaction of hHR23 with S5a. The ubiquitin-like domain of hHR23 mediates interaction with S5a subunit of 26S proteasome. J Biol Chem. 1999, 274:28019-25.
37. Chen L, Shinde U, Ortolan TG. Ubiquitin-associated (UBA) domains in Rad23 bind ubiquitin and promote inhibition if multi-ubiquitin chain assembly. EMBO Rep. 2001, 2:933-8.
38. Raasi S, Pickart CM. Rad23-ubiquitin associated domains (UBA) inhibit 26S proteasome-catalysed proteolysis by sequestering lysine 48-linked polyubiquitin chains. J Biol Chem. 2003, 278:8951-9.
39. Heessen S, Masucci MG, Dantuma NP. The UBA2 domain functions as an intrinsic stabilization signal that protects Rad23 from proteasomal degradation. Mol Cell. 2005, 18:225-35.
40. Lambertson D, Chen L, Madura K. Pleiotropic defects caused by loss of the proteasome-interacting factors Rad23 and Rpn10 of Saccharomyces cerevisiae. Genetics. 1999, 153:69-79.
41. Chen L, Madura K. Rad23 promotes the targeting of proteolytic substrates to the proteasome. Mol Cell Biol. 2002, 22:4902-13.
42. El-Mahdy LA, Zhu Q, Wang QE. Cullin 4A-mediated proteolysis of DDB2 protein at DNA damage sites regulates in vivo lesion recognition by XPC. J Biol Chem. 2006, 281:13404-11.
43. Huang TT, D' Andrea AD. Regulation of DNA repair by ubiquitylation. Nat Rev Mol Cell Biol. 2006, 7:323-34.
44. Bergink S, Jaspers NG, Vermeulen W. Regulation of UV-induced DNA damage response by ubiquitylation. DNA Repair. 2007, 6:1231-42.
45. Wakasugi M, Sancar A. Assembly, subunit composition, and footprint of human DNA repair excision nuclease. Proc Natl Acad Sci USA. 1998, 95:6669-74.
46. Wang QE, Praetorius-Ibba M, Zhu Q. Ubiquitylation-independent degradation of Xeroderma pigmentosum group C protein is required for efficient nucleotide excision repair. Nucleic Acids Res. 2007, 35:5338-50.
47. Wang QE, Wani MA, Chen J. Cellular ubiquitination and proteasomal functions positively modulate mammalian nucleotide excision repair. Mol Carcinog. 2005, 42:53-64.
48. Baker DJ, Wuenschell G, Xia L. Nucleotide excision repair eliminates unique DNA-protein cross-links from mammalian cells. J Biol Chem. 2007, 282:22592-604.
49. Krogan NJ, Lam MH, Fillingham J. Proteasome involvement in the repair of DNA double-strand breaks. Mol Cell. 2004, 16:1027-34.
50. Starita LM, Parvin JD. The multiple nuclear functions of BRCA1: transcription, ubiquitination and DNA repair. Curr Opin Cell Biol. 2003, 15:345-50.
51. Gudmundsdottir K, Lord CJ, Ashworth A. The proteasome is involved in determining differential utilization of double-strand break repair pathways. Oncogene. 2007, 26:7601-6.
52. Bennett BT, Knight KL. Cellular localization of human Rad51C and regulation of ubiquitin-mediated proteolysis of Rad51. J Cell Biochem. 2005, 96:1095-109.
53. Murakawa Y, Sonoda E, Barber LJ. Inhibitors of the proteasome suppress homologous DNA recombination in mammalian cells. Cancer Res. 2007, 67:8536-43.
54. Jacquemont C, Taniguchi T. Proteasome function is required for DNA damage response and fanconi anemia pathway activation. Cancer Res. 2007, 67:7395-405.
55. Robison JG, Dixon K, Bissler JJ. Cell cycle- and proteasome-dependent formation of etoposide-induced replication protein A (RPA) or Mre11/Rad50/Nbs1 (MRN) complex repair foci. Cell Cycle. 2007, 6:2399-407.
56. Gama V, Yoshida T, Gomez JA. Involvement of the ubiquitin in decreasing Ku70 levels in response to drug-induced apoptosis. Exp Cell Res. 2006, 312:488-99.
57. Postow L, Ghenoiu C, Woo EM. Ku80 removal from DNA through double strand break-induced ubiquitylation. J Cell Biol. 2008, 182:467-79.
58. Podlaska A, McIntyre J, Skoneczna A. The link between 20S proteasome activity and post-replication DNA repair in Saccharomyces cerevisiae. Mol Microbiol. 2003, 49:1321-32.
59. McIntyre J, Podlaska A, Sconeczna A. Analysis of the spontaneous mutator phenotype associated with 20S proteasome deficiency in S. cerevisiae. Mut Res. 2006, 593:153-63.
60. Sconeczna A, McIntyre J, Sconeczny M. Polymerase eta is a short-lived, proteasomally degraded protein that is temporarily stabilized following UV irradiation in Saccharomyces cerevisiae. J Mol Biol. 2007, 366:1074-86.
61. Miyase S, Tateishi S, Watanabe K. Differential regulation of Rad18 through Rad6-dependent mono- and poly-ubiquitination. J Biol Chem. 2005, 280:515-24.
62. Takezawa J, Ishimi Y, Yamada K. Proteasome inhibitors remarkably prevent translesion replication in cancer cells but not normal cells. Cancer Sci. 2008, 99:863-71.
63. Zhang S, Zhou Y, Trusa S. A novel DNA damage response: rapid degradation of the p12 subunit of DNA polymerase δ. J Biol Chem. 2007, 282:15330-40.
64. Heinrich MC, Silvey KV, Stone S. Posttranscriptional cell cycle-dependent regulation of human FANCC expression. Blood. 2000, 95:3970-7.
65. Nijman SM, Huang TT, Dirac AM. The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol Cell. 2005, 17:331-9.
66. Smogorzewska A, Matsuoka S, Vinciguerra P. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell. 2007, 129:289-301.
67. Grompe M, van de Vrugt H. The Fanconi family adds a fraternal twin. Dev Cell. 2007, 12:661-2.
68. Hardeland U, Steinacher R, Jiricny J. Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J. 2002, 21:1456-64.
69. Moschos SJ, Mo YY. Role of SUMO/Ubc9 in DNA damage repair and tumorigenesis. J Mol Hist. 2006, 37:309-19.
70. Masson M, de Murcia JM, Matei MG. Poly(ADP-ribose) polymerase interacts with a novel human ubiquitin conjugating enzyme: hUbc9. Gene. 1997, 190:287-96.
71. Gocke CB, Yu H, Kang J. Systematic identification and analysis of mammalian small ubiquitin-like modifier substrates. J Biol Chem. 2005, 280:5004-12.
72. Gudmundsdottir K, Lord CJ, Witt E. DSS1 is required for Rad51 focus formation and genomic stability in mammalian cells. EMBO Rep. 2004, 5:989-93.
73. Sone T, Saeki Y, Toh-e A. Sem1p is a novel subunit of the 26S proteasome from Saccharomyces cerevisiae. J Biol Chem. 2004, 279:28807-16.
74. Collavoli A, Comelli A, Rainaldi G. A yeast-based genetic screening to identify human proteins that increase homologous recombination. FEMS Yeast Res. 2008, 8:351-61.
75. Kovalenko OV, Plug AW, Haaf T. Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes. Proc Natl Acad Sci USA. 1996, 93:2958-63.
76. Shen Z, Pardington-Purtymun PE, Comeaux JC. Associations of UBE2I with RAD52, UBL1, p53, and RAD51 proteins in a yeast two-hybrid system. Genomics. 1996a, 37:183-6.
77. Shen Z, Pardington-Purtymun PE, Comeaux JC. UBL1, a human ubiquitin-like protein associating with human RAD51/RAD52 proteins. Genomics. 1996b, 36:271-9.
78. Sacher M, Pfander B, Hoege C. Control of Rad52 recombination activity by double-strand break-induced SUMO modification. Nat Cell Biol. 2006, 8:1284-90.
79. Ohuchi T, Seki M, Branzei D. Rad52 sumoylation and its involvement in the efficient induction of homologous recombination. DNA Repair. 2008, 7:879-89.
80. Foster RE, Nnakwe C, Woo L. Monoubiquitination of the nonhomologous end joining protein XRCC4. Biochem Biophys Res Commun. 2006, 341:175-83.
81. Yurchenko V, Xue Z, Sadofsky MJ. SUMO modification of human XRCC4 regulates its localization and function in DNA double-strand break repair. Mol Cell Biol. 2006, 26:1786-94.
82. Lee KY, Myung K. PCNA modifications for regulation of post-replication repair pathways. Mol Cells. 2008, 26:5-11.
83. Plosky BS, Vidal AE, Fernández de Henestrosa AR. Controlling the subcellular localization of DNA polymerases ι and η via interactions with ubiquitin. EMBO J. 2006, 25:2847-55.
84. Wang QE, Zhu Q, Wani G. DNA repair factor XPC is modified by SUMO-1 and ubiquitin following UV irradiation. Nucleic Acids Res. 2005, 33:4023-34.
85. Russell SJ, Reed SH, Huang W. The 19S regulatory complex of the proteasome functions independently of proteolysis in nucleotide excision repair. Mol Cell. 1999, 3:687-95.
86. Gillette TG, Huang W, Russell SJ. The 19S complex of the proteasome regulates nucleotide excision repair in yeast. Genes Dev. 2001, 15:1528-39.
87. Reed SH, Gillette TG. Nucleotide excision repair and the ubiquitin proteasome pathway-Do all roads lead to Rome. DNA Repair. 2007, 6:149-56.
88. Gillette TG, Yu S, Zhou Z. Distinct functions of the ubiquitin-proteasome pathway influence nucleotide excision repair. EMBO J. 2006, 25:2529-38.
89. Liu G, Warbrick E. The p66 and p12 subunits of DNA polymerase delta are modified by ubiquitin and ubiquitin-like proteins. Biochem Biophys Res Commun. 2006, 349:360-6.
90. Jones J, Wu K, Yang Y. A targeted proteomic analysis of the ubiquitin-like modifier Nedd8 and associated proteins. J Proteome Res. 2008, 7:1274-87.
91. Norman JA, Shiekhattar R. Analysis of Nedd8-associated polypeptides: a model for deciphering the pathway for ubiquitin-like modifications. Biochemistry. 2006, 45:3014-9.
92. Michael D, Oren M. The p53-Mdm2 module and the ubiquitin system. Semin Cancer Biol. 2003, 13:49-58.
93. Brooks CL, Gu W. Dynamics in the p53-Mdm2 ubiquitination pathway. Cell Cycle. 2004, 3:895-9.
94. Schoenfeld AR, Apgar S, Dolios G. BRCA2 is ubiquitinated in vivo and interacts with USP11, a deubiquitinating enzyme that exhibits prosurvival function in the cellular response to DNA damage. Mol Cell Biol. 24:7444-55.
95. Adimoolam S, Ford JM. p53 and regulation of DNA damage recognition during nucleotide excision repair. DNA Repair. 2003, 2:947-54.
96. Gatz SA, Wiesmüller L. p53 in recombination and repair. Cell Death Differ. 2006, 13:1003-16.
97. Hartman AR, Ford JM. BRCA1 and p53: compensatory roles in DNA repair. J Mol Med. 2003, 81:700-7.
98. Wang Y, Cortez D, Yazdi P. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev. 2000, 14:927-39.