Prevention of cisplatin-DNA adduct repair and potentiation of cisplatin- induced apoptosis in ovarian carcinoma cells by proteasome inhibitors

Biochemical Pharmacology

Volumn 60, Issue 9, 2000, Pages 1343-1354

  Mimnaugh, Edward G ^a   Yunmbam, Manasses K ^b   Li, Qingdi ^b   Bonvini, Paolo ^a   Hwang, Sang Gu ^c   Trepel, Jane ^c   Reed, Eddie ^b   Neckers, Len ^a  

^a Arthr Rheumatism Br Natl I   (United States)

^b Devmtl Therapeut Dept Med B   (United States)

^c Molecular Recognition Section   (United States)

Author keywords

Cisplatin; DNA repair; ERCC 1; Nucleosomal histones; Proteasome; Ubiquitin

Indexed keywords

CISPLATIN; DNA; HISTONE H2A; LACTACYSTIN; MESSENGER RNA; N ACETYLLEUCYLLEUCYLNORLEUCINAL; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEASOME INHIBITOR; PROTEIN P53; UBIQUITIN;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA ADDUCT; DNA REPAIR; DRUG SENSITIZATION; EXCISION REPAIR; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEINASE INHIBITION;

ACETYLCYSTEINE; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELLS, CULTURED; CHROMATIN; CISPLATIN; CYSTEINE ENDOPEPTIDASES; CYTOSOL; DNA; DNA ADDUCTS; DNA REPAIR; DRUG INTERACTIONS; ENZYME INHIBITORS; FEMALE; HISTONES; HUMAN; LEUCINE; MULTIENZYME COMPLEXES; OVARIAN NEOPLASMS; PROTEINS; RNA, MESSENGER; UBIQUITINS;

EID: 0034333366     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(00)00455-X     Document Type: Article

References (73)

1. Rosenberg B. Anticancer activity of cis-dichlorodiammineplatinum(II) and some relevant chemistry. Cancer Treat Rep. 63:1979;1433-1438.
2. Reed E., Parker R.J., Gill I., Bicher A., Dabholkar M., Vionnet J.A., Bostick-Bruton F., Tarone R., Muggia F.M. Platinum-DNA adduct in leukocyte DNA of a cohort of 49 patients with 24 different types of malignancies. Cancer Res. 53:1993;3694-3699.
3. Dabholkar M., Reed E. Cisplatin. Pinedo H.M., Longo D.L., Chabner B.A. Cancer Chemotherapy and Biological Response Modifiers Annual 16. Vol. 16:1996;88-110 Elsevier Science B. V. New York.
4. Sancar A. Mechanisms of DNA excision repair. Science. 266:1994;1954-1956.
5. Van Duin M., Koken M.H.M., van den Tol J., ten Dijke P., Odijk H., Westerveld A., Bootsma D., Hoeijmakers J.H.J. Genomic characterization of the human DNA excision repair gene ERCC-1. Nucleic Acids Res. 15:1987;9195-9213.
6. Lee K.B., Parker R.J., Bohr V., Cornelison T., Reed E. Cisplatin sensitivity/resistance in UV repair-deficient Chinese hamster ovary cells of complementation groups 1 and 3. Carcinogenesis. 14:1993;2177-2180.
7. Sancar A. DNA excision repair. Annu Rev Biochem. 65:1996;43-81.
8. Weeda G., Donker I., de Wit J., Morreau H., Janssens R., Vissers C.J., Nigg A., van Steeg H., Bootsma D., Hoeijmakers J.H.J. Disruption of mouse ERCC1 results in a novel repair syndrome with growth failure, nuclear abnormalities and senescence. Curr Biol. 7:1997;427-439.
9. Parker R.J., Eastman A., Bostick-Bruton F., Reed E. Acquired cisplatin resistance in human ovarian cancer cells is associated with enhanced repair of cisplatin-DNA lesions and reduced drug accumulation. J Clin Invest. 87:1991;772-777.
10. Choa C.C.-K. Cross-resistance to cis-diamminedichloroplatinum(II) of a multidrug-resistant lymphoma cell line associated with decreased drug accumulation and enhanced DNA repair. Eur J Pharmacol. 305:1996;213-222.
11. Aboussekhra A., Biggerstaff M., Shivji M.K.K., Vilpo J.A., Moncollin V., Podust V.N., Protic M., Hubscher U., Egly J.-M., Wood R.D. Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell. 80:1995;859-868.
12. Wood R.D. DNA damage recognition during nucleotide excision repair in mammalian cells. Biochimie. 81:1999;39-44.
13. van der Spek P.J., Visser C.E., Hanaoka F., Smit B., Hagemeijer A., Bootsma D., Hoeijmakers J.H.J. Cloning, comparative mapping, and RNA expression of the mouse homologues of the Saccharomyces cerevisiae nucleotide excision repair gene RAD23. Genomics. 31:1996;20-27.
14. Masutani C., Araki M., Sugasawa K., van der Spek P.J., Yamada A., Uchida A., Maekawa T., Bootsma D., Hoeijmakers J.H.J., Hanaoka F. Identification and characterization of XPA-binding domain of hHR23B. Mol Cell Biol. 17:1997;6915-6923.
15. Sugasawa K., Ng J.M.Y., Masutani C., Maekawa T., Uchida A., van der Spek P.J., Eker A.P., Rademakers S., Visser C., Aboussekhra A., Wood R.D., Hanaoka F., Bootsma D., Hoeijmakers J.H.J. Two human homologs of Rad23 are functionally interchangeable in complex formation and stimulation of XPC repair activity. Mol Cell Biol. 17:1997;6924-6931.
16. Shen Z., Pardington-Purtymun P.E., Comeaux J.C., Moyzis R.K., Chen D.J. Associations of UBE2I with RAD52, UBL1, p53 and RAD51 proteins in a yeast two-hybrid system. Genomics. 37:1996;183-186.
17. Jentsch S., McGrath J.P., Varshavsky A. The yeast DNA repair gene RAD6 encodes a ubiquitin-conjugating enzyme. Nature. 329:1987;131-134.
18. Bailly V., Lauders S., Prakash S., Prakash L. Yeast DNA repair proteins Rad6 and Rad18 form a heterodimer that has ubiquitin conjugating, DNA binding, and ATP hydrolytic activities. J Biol Chem. 272:1997;23360-23365.
19. Dor Y., Raboy B., Kulka R.G. Role of the conserved carboxy-terminal α-helix of Rad6p in ubiquitination and DNA repair. Mol Microbiol. 21:1996;1197-1206.
20. Koken M.H., Reynolds P., Jaspers-Dekker I., Prakash L., Prakash S., Bootsma D., Hoeijmakers J.H.J. Structural and functional conservation of two human homologs of the yeast DNA repair gene RAD6. Proc Natl Acad Sci USA. 88:1991;8865-8869.
21. Koken M.H.M., Hoogerbrugge J.W., Jaspers-Dekker I., de Wit J., Willemsen R., Roest H.P., Grootegoed J.A., Hoeijmakers J.H.J. Expression of the ubiquitin-conjugating DNA repair enzymes HHR6A and B suggests a role in spermatogenesis and chromatin modification. Dev Biol. 173:1996;119-132.
22. Nickel B.E., Allis C.D., Davie J.R. Ubiquitinated histone H2B is preferentially located in transcriptionally active chromatin. Biochemistry. 28:1989;958-963.
23. Davie J.R. Histone modifications, chromatin structure, and the nuclear matrix. J Cell Biochem. 62:1996;149-157.
24. Robzyk K., Recht J., Osley M.A. Rad6-dependent ubiquitination of histone H2B in yeast. Science. 287:2000;501-504.
25. van Holde K.E., Lohr D.E., Robert C. What happens to nucleosomes during transcription? J Biol Chem. 267:1992;2837-2840.
26. Wolffe A.P., Hayes J.J. Chromatin disruption and modification. Nucleic Acids Res. 27:1999;711-720.
27. Baxter B.K., Smerdon M.J. Nucleosome unfolding during DNA repair in normal and xeroderma pigmentosum (group C) human cells. J Biol Chem. 273:1998;17517-17524.
28. Cai S.-Y., Babbitt R.W., Marchesi V.T. A mutant deubiquitinating enzyme (Ubp-M) associates with mitotic chromosomes and blocks cell division. Proc Natl Acad Sci USA. 96:1999;2828-2833.
29. Mimnaugh E.G., Chen H.Y., Davie J.R., Celis J.E., Neckers L. Rapid deubiquitination of nucleosomal histones in human tumor cells caused by proteasome inhibitors and stress response inducers Effects on replication, transcription, translation, and the cellular stress response . Biochemistry. 36:1997;14418-14429.
30. Johnson S.W., Swiggard P.A., Handel L.M., Brennan J.M., Godwin A.K., Ozols R.F., Hamilton T.C. Relationship between platinum-DNA adduct formation and removal and cisplatin cytotoxicity in cisplatin-sensitive and -resistant human ovarian cancer cells. Cancer Res. 54:1994;5911-5916.
31. LeRoy A.F. Some quantitative data on cis-dichlorodiammineplatinum(II) species in solution. Cancer Treat Rep. 63:1979;231-233.
32. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., Fujimoto E.K., Goeke N.M., Olson B.J., Klenk D.C. BCA protein assay. Anal Biochem. 150:1985;76-85.
33. Swerdlow P.S., Finley D., Varshavsky A. Enhancement of immunoblot sensitivity by heating of hydrated filters. Anal Biochem. 156:1986;147-153.
34. Bobrow M.N., Harris T.D., Shaughnessy K.J., Litt G.J. Catalyzed reporter disposition, a novel method of signal amplification. J Immunol Methods. 125:1989;279-285.
35. Delcuve G.P., Davie J.R. Western blotting and immunochemical detection of histones electrophoretically resolved on acid-urea-Triton- and sodium dodecyl sulfate-polyacrylamide gels. Anal Biochem. 200:1992;339-341.
36. Flamm W.G., Birnstiel M.L., Walker P.M.B. Preparation and fractionation, and isolation of single strands, of DNA by isopycnic ultra-centrifugation in fixed-angle rotors. Birnie G., Fox S.M. Subcellular Components, Preparation and Fractionation. 1969;125-155 Butterworth, London.
37. Parker R.J., Gill I., Tarone R., Vionnet J.A., Grunberg S., Muggia F.M., Reed E. Platinum-DNA damage in leukocyte DNA of patients receiving carboplatin and cisplatin chemotherapy, measured by atomic absorption spectrometry. Carcinogenesis. 12:1991;1253-1258.
38. Li Q., Gardner K., Zhang L., Tsang B., Bostick-Bruton F., Reed E. Cisplatin induction of ERCC-1 mRNA expression in A2780/CP70 human ovarian cancer cells. J Biol Chem. 273:1998;23419-23425.
39. Snedecor GW, Statistical Methods. Iowa State University Press, Ames, IA, 1956.
40. Hochstrasser M. Ubiquitin and intracellular protein degradation. Curr Opin Cell Biol. 4:1992;1024-1031.
41. Hershko A., Ciechanover A. The ubiquitin system for protein degradation. Annu Rev Biochem. 61:1992;761-807.
42. Deshaies R.J. Make it or break it The role of ubiquitin-dependent proteolysis in cellular regulation . Trends Cell Biol. 5:1995;428-434.
43. Matsui S., Seon B.K., Sandberg A.A. Disappearance of a structural chromatin protein A24 in mitosis Implications for molecular basis of chromatin condensation . Proc Natl Acad Sci USA. 76:1979;6386-6390.
44. Cowden R.R., Curtis S.K. Microfluorometric investigations of chromatin structure. I. Evaluation of nine DNA-specific fluorochromes as probes of chromatin organization. Histochemistry. 72:1981;11-23.
45. Li Q., Bostick-Bruton F., Reed E. Effect of interleukin-1 and tumour necrosis factor-α on cisplatin-induced ERCC-1 mRNA expression in a human ovarian carcinoma cell line. Anticancer Res. 18:1998;2283-2287.
46. Li Q., Tsang B., Bostick-Bruton F., Reed E. Modulation of excision repair cross complementation group 1 (ERCC-1) mRNA expression by pharmacological agents in human ovarian carcinoma cells. Biochem Pharmacol. 57:1999;347-353.
47. Henkels K.M., Turchi J.J. Induction of apoptosis in cisplatin-sensitive and -resistant human ovarian cancer cell lines. Cancer Res. 57:1997;4488-4492.
48. Imajoh-Ohmi S.I., Kawaguchi T., Sugiyama S., Tanaka K., Omura S., Kikuchi H. Lactacystin, a specific inhibitor of the proteasome, induces apoptosis in human monoblast U937 cells. Biochem Biophys Res Commun. 217:1995;1070-1077.
49. Shinohara K., Tomioka M., Nakano H., Tone S., Ito H., Kawashima S. Apoptosis induction resulting from proteasome inhibition. Biochem J. 317:1996;385-388.
50. Tanimoto Y., Onishi Y., Hashimoto S., Kizaki H. Peptidyl aldehyde inhibitors of proteasome induce apoptosis rapidly in mouse lymphoma RVC cells. J Biochem (Tokyo). 121:1997;542-549.
51. Tewari M., Quan L.T., O'Rourke K., Desnoyers S., Zeng Z., Beidler D.R., Poirier G.G., Salvesen G.S., Dixit V.M. Yama/CPP32β, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell. 81:1995;801-809.
52. Mueller R.D., Yasuda H., Hatch C.L., Bonner W.M., Bradbury E.M. Identification of ubiquitinated histones 2A and 2B in Physarum polycephalum. Disappearance of these proteins at metaphase and reappearance at anaphase. J Biol Chem. 260:1985;5147-5153.
53. Haas A.L., Bright P.M. The immunochemical detection and quantitation of intracellular ubiquitin-protein conjugates. J Biol Chem. 260:1985;12464-12473.
54. Andersen M.W., Ballal N.R., Goldknopf I.L., Busch H. Protein A24 lyase activity in nucleoli of thioacetamide-treated rat liver releases histone 2A and ubiquitin from conjugated protein A24. Biochemistry. 20:1981;1100-1104.
55. Li W., Nagaraja S., Delcuve G.P., Hendzel M.J., Davie J.R. Effects of histone acetylation, ubiquitination and variants on nucleosome stability. Biochem J. 296:1993;737-744.
56. Prakash L. Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations. Mol Gen Genet. 184:1981;471-478.
57. Bailly V., Lamb J., Sung P., Prakash S., Prakash L. Specific complex formation between yeast RAD4 and RAD18 proteins A potential mechanism for targeting RAD6 ubiquitin-conjugating activity to DNA damage sites . Genes Dev. 8:1994;811-820.
58. Sung P., Prakash S., Prakash L. The RAD6 protein of Saccharomyces cerevisiae polyubiquitinates histones, and its acidic domain mediates this activity. Genes Dev. 2:1988;1476-1485.
59. Wu R.S., Kohn K.W., Bonner W.M. Metabolism of ubiquitinated histones. J Biol Chem. 256:1981;5916-5920.
60. Ullrich O., Reinheckel T., Sitte N., Hass R., Grune T., Davies K.J.A. Poly-ADP ribose polymerase activates nuclear proteasome to degrade oxidatively damaged histones. Proc Natl Acad Sci USA. 96:1999;6223-6228.
61. Wood R.D. DNA repair in eukaryotes. Annu Rev Biochem. 65:1996;135-167.
62. Schauber C., Chen L., Tongaokkar P., Vega I., Lambertson D., Potts W., Madura K. RAD23 links DNA repair to the ubiquitin/proteasome pathway. Nature. 391:1998;715-718.
63. Bush K.T., Goldberg A.L., Nigam S.K. Proteasome inhibition leads to a heat-shock response, induction of endoplasmic reticulum chaperones and thermotolerance. J Biol Chem. 272:1997;9086-9092.
64. Mathew A., Mathur S.K., Morimoto R.I. Heat shock response and protein degradation Regulation of HSF2 by the ubiquitin-proteasome pathway . Mol Cell Biol. 18:1998;5091-5098.
65. Li Q., Ding L., Yu J.J., Mu C., Tsang B., Bostick-Bruton F., Reed E. Cisplatin and phorbol ester independently induce ERCC1 protein in human ovarian tumor cells. Int J Oncol. 13:1998;987-992.
66. Wetzel C.C., Berberich S.J. DNA binding activities of p53 protein following cisplatin damage of ovarian cells. Oncol Res. 10:1998;151-161.
67. Eastman A. Activation of programmed cell death by anticancer agents Cisplatin as a model system . Cancer Cells. 2:1990;275-280.
68. Fritsche M., Haessler C., Brandner G. Induction of nuclear accumulation of the tumor-suppressor protein p53 by DNA-damaging agents. Oncogene. 8:1993;307-318.
69. Maki C.G., JM H., Howley P.M. In vivo ubiquitination and proteasome-mediated degradation of p53. Cancer Res. 56:1997;2649-2654.
70. Sherwood S.W., Kung A.L., Roitelman J., Simoni R.D., Schimke R.T. In vivo inhibition of cyclin B degradation and induction of cell-cycle arrest in mammalian cells by the neutral cysteine protease inhibitor N-acetylleucylleucylnorleucinal. Proc Natl Acad Sci USA. 90:1993;3353-3357.
71. Lopes U.G., Erhardt P., Yao R., Cooper G.M. p53-dependent induction of apoptosis by proteasome inhibitors. J Biol Chem. 272:1997;12893-12896.
72. Delmastro D.A., Li J., Vaisman A., Solle M., Chaney S.G. DNA damage inducible-gene expression following platinum treatment in human ovarian carcinoma cell lines. Cancer Chemother Pharmacol. 39:1997;245-253.
73. Adams J, Palombella VJ, Sausville EA, Johnson J, Destree A, Lazarus DD, Maas J, Pien CS, Prakash S and Elliott PJ, Proteasome inhibitors: A novel class of potent and effective antitumor agents. Cancer Res 59: 2615-2622, 1999.