Biochemical and proteomics approaches to characterize topoisomerase IIα cysteines and DNA as targets responsible for cisplatin-induced inhibition of topoisomerase IIα

Molecular Pharmacology

Volumn 67, Issue 3, 2005, Pages 937-947

  Hasinoff, Brian B ^a   Wu, Xing ^a   Krokhin, Oleg V ^a   Ens, Werner ^a   Standing, Kenneth G ^a   Nitiss, John L ^b   Sivaram, Tejomoortula ^c   Giorgianni, Angela ^c   Yang, Shaohua ^c   Jiang, Yu ^c   Yalowich, Jack C ^c  

^a UNIVERSITY OF MANITOBA   (Canada)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

10 (2,5 DIHYDRO 2,5 DIOXO 1H PYRROL 1 YL) 9 METHOXY 3 OXO 3H NAPHTHO[2,1B]PYRAN 2 CARBOXYLIC ACID METHYL ESTER; CISPLATIN; CYSTEINE DERIVATIVE; DITHIOTHREITOL; DNA TOPOISOMERASE (ATP HYDROLYSING); DNA TOPOISOMERASE ALPHA (ATP HYDROLYSING); ETOPOSIDE; KINETOPLAST DNA; MALEIMIDE DERIVATIVE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CATALYSIS; CONTROLLED STUDY; DISULFIDE BOND; DNA ADDUCT; DRUG ANTAGONISM; DRUG EFFECT; DRUG TARGETING; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME MECHANISM; ENZYME STABILITY; GROWTH INHIBITION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEOMICS; SPECTROPHOTOMETRY;

ANTIGENS, NEOPLASM; CELL DIVISION; CISPLATIN; CYSTEINE; DISULFIDES; DITHIOTHREITOL; DNA TOPOISOMERASES, TYPE II, EUKARYOTIC; DNA-BINDING PROTEINS; HUMANS; K562 CELLS; KINETICS; PLASMIDS; PROTEOME;

EID: 20144362708     PISSN: 0026895X     EISSN: None     Source Type: Journal    
DOI: 10.1124/mol.104.004416     Document Type: Article

References (39)

1. Ali-Osman F, Berger MS, Rajagopal S, Spence A, and Livingston RB (1993) Topoisomerase II inhibition and altered kinetics of formation and repair of nitrosourea and cisplatin-induced DNA interstrand cross-links and cytotoxicity in human glioblastoma cells. Cancer Res 53:5663-5668.
2. Barnabé N and Hasinoff BB (2001) High-throughput fluorescence flow injection topoisomerase II inhibition assay. J Chromatogr B Biomed Sci Appl 760:263-269.
3. Barret JM, Calsou P, Larsen AK, and Salles B (1994) A cisplatin-resistant murine leukemia cell line exhibits increased topoisomerase II activity. Mol Pharmacol 46:431-436.
4. Burden DA, Froelich-Ammon SJ, and Osheroff N (2001) Topisomerase II-mediated cleavage of plasmid DNA. Methods Mol Biol 95:283-289.
5. Crul M, van Waardenburg RC, Beijnen JH, and Schellens JH (2002) DNA-based drug interactions of cisplatin. Cancer Treat Rev 28:291-303.
6. Dabrowiak JC, Goodisman J, and Souid AK (2002) Kinetic study of the reaction of cisplatin with thiols. Drug Metab Dispos 30:1378-1384.
7. Davies MS, Berners-Price SJ, and Hambley TW (2000) Slowing of cisplatin aquation in the presence of DNA but not in the presence of phosphate: improved understanding of sequence selectivity and the roles of monoaquated and diaquated species in the binding of cisplatin to DNA. Inorg Chem 39:5603-5613.
8. Eder JP Jr, Chan VT, Ng SW, Rizvi NA, Zacharoulis S, Teicher BA, and Schnipper LE (1995) DNA topoisomerase IIα expression is associated with alkylating agent resistance. Cancer Res 55:6109-6116.
9. Einhorn LH (2002) Curing metastatic testicular cancer. Proc Natl Acad Sci USA 99:4592-4595.
10. Fabisiak JP, Sedlov A, and Kagan VE (2002) Quantification of oxidative/nitrosative modification of CYS(34) in human serum albumin using a fluorescence-based SDS-PAGE assay. Antioxid Redox Signal 4:855-865.
11. Fattman C, Allan WP, Hasinoff BB, and Yalowich JC (1996) Collateral sensitivity to the bisdioxopiperazine dexrazoxane (ICRF-187) in etoposide (VP-16) resistant human leukemia K562 cells. Biochem Pharmacol 52:635-642.
12. Fortune JM and Osheroff N (2000) Topoisomerase II as a target for anticancer drugs: when enzymes stop being nice. Prog Nucleic Acid Res Mol Biol 64:221-253.
13. Gantchev TG and Hunting DJ (1998) The ortho-quinone metabolite of the anticancer drug etoposide (VP-16) is a potent inhibitor of the topoisomerase II/DNA cleavable complex. Mol Pharmacol 53:422-428.
14. Gorman JJ, Wallis TP, and Pitt JJ (2002) Protein disulfide bond determination by mass spectrometry. Mass Spectrom Rev 21:183-216.
15. Hagrman D, Goodisman J, Dabrowiak JC, and Souid AK (2003) Kinetic study on the reaction of cisplatin with metallothionein. Drug Metab Dispos 31:916-923.
16. Hasinoff BB, Kozlowska H, Creighton AM, Allan WP, Thampatty P, and Yalowich JC (1997) Mitindomide is a catalytic inhibitor of DNA topoisomerase II that acts at the bisdioxopiperazine binding site. Mol Pharmacol 52:839-845.
17. 2(levrazoxane), of the topoisomerase II inhibitors dexrazoxane (ICRF-187) and levrazoxane (ICRF-186). J Inorg Biochem 98:616-624.
18. Ishikawa T and Ali-Osman F (1993) Glutathione-associated cis-diamminedichloro-platinum(II) metabolism and ATP-dependent efflux from leukemia cells. Molecular characterization of glutathione-platinum complex and its biological significance. J Biol Chem 268:20116-20125.
19. Ivanov AI, Christodoulou J, Parkinson JA, Barnham KJ, Tucker A, Woodrow J, and Sadler PJ (1998) Cisplatin binding sites on human albumin. J Biol Chem 273:14721-14730.
20. Jensen LH, Renodon-Corniere A, Wessel I, Langer SW, Sokilde B, Carstensen EV, Sehested M, and Jensen PB (2002) Maleimide is a potent inhibitor of topoisomerase II in vitro and in vivo: a new mode of catalytic inhibition. Mol Pharmacol 61:1235-1243.
21. Kagan VE, Kuzmenko AI, Tyurina YY, Shvedova AA, Matsura T, and Yalowich JC (2001) Pro-oxidant and antioxidant mechanisms of etoposide in HL-60 cells: role of myeloperoxidase. Cancer Res 61:7777-7784.
22. Krokhin OV, Cheng K, Sousa SL, Ens W, Standing KG, and Wilkins JA (2003) Mass spectrometric based mapping of the disulfide bonding patterns of integrin alpha chains. Biochemistry 42:12950-12959.
23. Krokhin O, Qian Y, McNabb JR, Spicer V, Ens W, and Standing KG (2002) An off-line interface for HPLC and orthogonal MALDITOF, in 50th ASMS Conference on Mass Spectrometry and Allied Topics; 2002 Jun 2-6; Orlando, Florida. American Society for Mass Spectrometry, Santa Fe, NM.
24. Li TK and Liu LF (2001) Tumor cell death induced by topoisomerase- targeting drugs. Annu Rev Pharmacol Toxicol 41:53-77.
25. Lindsey RH, Felix CA, and Osheroff N (2004) p-Benzoquinone is a human topoisomerase IIα poison. Am Assoc Cancer Res 45:711.
26. Loboda AV, Krutchinsky AN, Bromirski M, Ens W, and Standing KG (2000) A tandem quadrupole/time-of-flight mass spectrometer with a matrix-assisted laser desorption/ionization source: design and performance. Rapid Commun Mass Spectrom 14:1047-1057.
27. Neumann S, Simon H, Zimmer C, and Quinones A (1996) The antitumor agent cisplatin inhibits DNA gyrase and preferentially induces gyrB gene expression in Escherichia coli. Biol Chem 377:731-739.
28. Reedijk J (1996) Improved understanding in platinum antitumor chemistry. Chem Commun (7):801-806.
29. Ritke MK, Allan WP, Fattman C, Gunduz NN, and Yalowich JC (1994a) Reduced phosphorylation of topoisomerase II in etoposide-resistant human leukemia K562 cells. Mol Pharmacol 46:58-66.
30. Ritke MK, Roberts D, Allan WP, Raymond J, Bergoltz W, and Yalowich JC (1994b) Altered stability of etoposide-induced topoisomerase II-DNA complexes in resistant human leukemia K562 cells. Br J Cancer 69:687-697.
31. Ritke MK and Yalowich JC (1993) Altered gene expression in human leukemia K562 cells selected for resistance to etoposide. Biochem Pharmacol 46:2007-2020.
32. Sadowitz PD, Hubbard BA, Dabrowiak JC, Goodisman J, Tacka KA, Aktas MK, Cunningham MJ, Dubowy RL, and Souid AK (2002) Kinetics of cisplatin binding to cellular DNA and modulations by thiol-blocking agents and thiol drugs. Drug Metab Dispos 30:183-190.
33. Sehested M, Wessel I, Jensen LH, Holm B, Oliveri RS, Kenwrick S, Creighton AM, Nitiss JL, and Jensen PB (1998) Chinese hamster ovary cells resistant to the topoisomerase II catalytic inhibitor ICRF-159: a Tyr49Phe mutation confers high-level resistance to bisdioxopiperazines. Cancer Res 58:1460-1468.
34. van Waardenburg RC, de Jong LA, van Eijndhoven MA, Verseyden C, Pluim D, Jansen LE, Bjornsti MA, and Schellens JH (2004) Platinated DNA adducts enhance poisoning of DNA topoisomerase I by camptothecin. J Biol Chem 279:54502-54509.
35. Wang H, Mao Y, Chen AY, Zhou N, LaVoie EJ, and Liu LF (2001) Stimulation of topoisomerase II-mediated DNA damage via a mechanism involving protein thiolation. Biochemistry 40:3316-3323.
36. Wasserman RA, Austin CA, Fisher LM, and Wang JC (1993) Use of yeast in the study of anticancer drugs targeting DNA topoisomerases: expression of a functional recombinant human DNA topoisomerase II alpha in yeast. Cancer Res 53:3591-3596.
37. Waud WR (1995) Platinum complexes, in Cancer Chemotherapeutic Agents (Foye WO ed) pp 121-133, American Chemical Society, Washington, DC.
38. Yalowich JC, Kagan VE, Do D, Yang S, Giorgianni A, McDonald P, Fan Y, Day BW, Riviere J, and Wagner JR (2004) Myeloperoxidase-dependent pro-oxidant effects of etoposide: implications for etoposide-induced leukemogenesis. Proc Am Assoc Cancer Res 45:3084.
39. Zhou N, Xiao H, Li TK, Nur EKA, and Liu LF (2003) DNA damage-mediated apoptosis induced by selenium compounds. J Biol Chem 278:29532-29537.