Polychlorinated biphenyl quinone metabolites poison human topoisomerase IIα: Altering enzyme function by blocking the N-terminal protein gate

Biochemistry

Volumn 45, Issue 33, 2006, Pages 10140-10152

  Bender, Ryan P ^a   Lehmler, Hans J ^b   Robertson, Larry W ^b   Ludewig, Gabriele ^b   Osheroff, Neu ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CHLORINATION; CHROMOSOMES; METABOLITES; PHENOLS; TUMORS;

HUMAN TOPOISOMERASE; N-TERMINAL GATES; POLYCHLORINATED BIPHENYLS (PCB); QUINONES;

PROTEINS;

1,4 BENZOQUINONE DERIVATIVE; 2 (2 CHLOROPHENYL) 1,4 BENZOQUINONE; 2 (3 CHLOROPHENYL) 1,4 BENZOQUINONE; 2 (3,5 DICHLOROPHENYL) 1,4 BENZOQUINONE; 2 (4 CHLOROPHENYL) 1,4 BENZOQUINONE; 3 (4 CHLOROPHENYL) 1,2 BENZOQUINONE; 4 (4 CHLOROPHENYL) 1,2 BENZOQUINONE; 4' CHLOROBIPHENYL 2,5 DIOL; CHLORPHENOTANE; DNA; DNA TOPOISOMERASE (ATP HYDROLYSING); MONOMER; PHENOL DERIVATIVE; POISON; POLYCHLORINATED BIPHENYL DERIVATIVE; QUINONE DERIVATIVE; TOPOISOMERASE IIALPHA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CHROMOSOME ABERRATION; CHROMOSOME DAMAGE; COMPLEX FORMATION; CONTROLLED STUDY; CROSS LINKING; DNA CLEAVAGE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; METABOLITE; MOLECULAR STABILITY; MOLECULAR WEIGHT; PLASMID; PRIORITY JOURNAL;

ANTIGENS, NEOPLASM; CELLS, CULTURED; CHROMOSOME ABERRATIONS; DNA DAMAGE; DNA TOPOISOMERASES, TYPE II, EUKARYOTIC; DNA-BINDING PROTEINS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HUMANS; POLYCHLORINATED BIPHENYLS; QUINONES;

RODENTIA;

EID: 33747466075     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0524666     Document Type: Article

References (93)

1. Silberhorn, E. M., Glauert, H. P., and Robertson, L. W. (1990) Carcinogenicity of polyhalogenated biphenyls: PCBs and PBBs, Crit. Rev. Toxicol. 20, 440-496.
2. Erickson, M. D. (2001) Introduction: PCB properties, uses, occurrence, and regulatory history, in PCBs, Recent Advances in Environmental Toxicology and Health Effects (Robertson, L. W., and Hansen, L. G., Eds.) pp xi-xxx, University Press of Kentucky, Lexington, KY.
3. Kimbrough, R. D. (1987) Human health effects of polychlorinated biphenyls (PCBs) and polybrominated biphenyls (PBBs), Annu. Rev. Pharmacol. Toxicol. 27, 87-111.
4. Fiedler, H. (2001) Global and local disposition of PCBs, in PCBs, Recent Advances in Environmental Toxicology and Health Effects (Robertson, L. W., and Hansen, L. G., Eds.) pp 11-15, University Press of Kentucky, Lexington, KY.
5. Holoubek, I. (2001) Polychlorinated biphenyl (PCB) contaminated sites worldwide, in PCBs, Recent Advances in Environmental Toxicology and Health Effects (Robertson, L. W., and Hansen, L. G., Eds.) pp 17-26, University Press of Kentucky, Lexington, KY.
6. Safe, S. (1984) Polychlorinated biphenyls (PCBs) and polybrominated biphenyls (PBBs): biochemistry, toxicology, and mechanism of action, Crit. Rev. Toxicol. 13, 319-395.
7. Kimbrough, R. D. (1985) Laboratory and human studies on polychlorinated biphenyls (PCBs) and related compounds, Environ. Health. Perspect. 59, 99-106.
8. Robertson, L. W., Hansen, L. G. (2001) PCBs, Recent Advances in Environmental Toxicology and Health Effects, University Press of Kentucky, Lexington, KY.
9. Ludewig, G. (2001) Cancer Initiation by PCBs, in PCBs, Recent Advances in Environmental Toxicology and Health Effects (Robertson, L. W., and Hansen, L. G., Eds.) pp 337-354, University Press of Kentucky, Lexington, KY.
10. Sargent, L. (2001) Role of polychlorinated biphenyl exposure in the progression of neoplasia, in PCBs, Recent Advances in Environmental Toxicology and Health Effects (Robertson, L. W., and Hansen, L. G., Eds.) pp 373-379, University Press of Kentucky, Lexington, KY.
11. Sargent, L., Roloff, B., and Meisner, L. (1989) In vitro chromosome damage due to PCB interactions, Mutat. Res. 224, 79-88.
12. Kalina, I., Sram, R. J., Konecna, H., and Ondrussekova, A. (1991) Cytogenetic analysis of peripheral blood lymphocytes in workers occupationally exposed to polychlorinated biphenyls, Teratog., Carcinog., Mutagen. 11, 77-82.
13. Joksic, G., and Markovic, B. (1992) Cytogenetic changes in persons exposed to polychlorinated biphenyls, Arh. Hig. Rada. Toksikol. 43, 29-35.
14. Mayes, B. A., McConnell, E. E., Neal, B. H., Brunner, M. J., Hamilton, S. B., Sullivan, T. M., Peters, A. C., Ryan, M. J., Toft, J. D., Singer, A. W., Brown, J. F., Jr., Menton, R. G., and Moore, J. A. (1998) Comparative carcinogenicity in Sprague-Dawley rats of the polychlorinated biphenyl mixtures Aroclors 1016, 1242, 1254, and 1260, Toxicol. Sci. 41, 62-76.
15. Oakley, G. G., Robertson, L. W., and Gupta, R. C. (1996) Analysis of polychlorinated biphenyl-DNA adducts by 32P-postlabeling, Carcinogenesis 17, 109-114.
16. Oakley, G. G., Devanaboyina, U., Robertson, L. W., and Gupta, R. C. (1996) Oxidative DNA damage induced by activation of polychlorinated biphenyls (PCBs): implications for PCB-induced oxidative stress in breast cancer, Chem. Res. Toxicol. 9, 1285-1292.
17. Amaro, A. R., Oakley, G. G., Bauer, U., Spielmann, H. P., and Robertson, L. W. (1996) Metabolic activation of PCBs to quinones: reactivity toward nitrogen and sulfur nucleophiles and influence of superoxide dismutase, Chem. Res. Toxicol. 9, 623-629.
18. Srinivasan, A., Lehmler, H. J., Robertson, L. W., and Ludewig, G. (2001) Production of DNA strand breaks in vitro and reactive oxygen species in vitro and in HL-60 cells by PCB metabolites, Toxicol. Sci. 60, 92-102.
19. Srinivasan, A., Robertson, L. W., and Ludewig, G. (2002) Sulfhydryl binding and topoisomerase inhibition by PCB metabolites, Chem. Res. Toxicol. 15, 497-505.
20. Wang, J. C. (1996) DNA topoisomerases, Annu. Rev. Biochem. 65, 635-692.
21. Burden, D. A., and Osheroff, N. (1998) Mechanism of action of eukaryotic topoisomerase II and drugs targeted to the enzyme, Biochim. Biophys. Acta 1400, 139-154.
22. Nitiss, J. L. (1998) Investigating the biological functions of DNA topoisomerases in eukaryotic cells, Biochim. Biophys. Acta 1400, 63-81.
23. Wang, J. C. (1998) Moving one DNA double helix through another by a type II DNA topoismerase: the story of a simple molecular machine, Q. Rev. Biophys. 31, 107-144.
24. Fortune, J. M., 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.
25. Champoux, J. J. (2001) DNA topoisomerases: structure, function, and mechanism, Annu. Rev. Biochem. 70, 369-413.
26. Wang, J. C. (2002) Cellular roles of DNA topoisomerases: a molecular perspective, Nat. Rev. Mol. Cell. Biol. 3, 430-440.
27. Wilstermann, A. M., and Osheroff, N. (2003) Stabilization of eukaryotic topoisomerase II-DNA cleavage complexes, Curr. Top. Med. Chem. 3, 321-338.
28. Sander, M., and Hsieh, T. (1983) Double strand DNA cleavage by type II DNA topoisomerase from Drosophila melanogaster, J. Biol. Chem. 258, 8421-8428.
29. Liu, L. F., Rowe, T. C., Yang, L., Tewey, K. M., and Chen, G. L. (1983) Cleavage of DNA by mammalian DNA topoisomerase II, J. Biol. Chem. 258, 15365-15370.
30. Zechiedrich, E. L., Christiansen, K., Andersen, A. H., Westergaard, O., and Osheroff, N. (1989) Double-stranded DNA cleavage/religation reaction of eukaryotic topoisomerase II: evidence for a nicked DNA intermediate, Biochemistry 28, 6229-6236.
31. Kaufmann, S. H. (1998) Cell death induced by topoisomerase-targeted drugs: more questions than answers, Biochim. Biophys. Acta 1400, 195-211.
32. Kaufmann, S. H., Gore, S. D., Miller, C. B., Jones, R. J., Zwelling, L. A., Schneider, E., Burke, P. J., and Karp, J. E. (1998) Topoisomerase II and the response to antileukemic therapy, Leuk. Lymphoma 29, 217-237.
33. Rowley, J. D. (1998) The critical role of chromosome translocations in human leukemias, Annu. Rev. Genet. 32, 495-519.
34. Felix, C. A. (1998) Secondary leukemias induced by topoisomerase-targeted drugs, Biochim. Biophys. Acta 1400, 233-255.
35. Sordet, O., Khan, Q. A., Kohn, K. W., and Pommier, Y. (2003) Apoptosis induced by topoisomerase inhibitors, Curr. Med. Chem.: Anti-Cancer Agents 3, 271-290.
36. Hande, K. R. (1998) Clinical applications of anticancer drugs targeted to topoisomerase II. Biochim. Biophys. Acta 1400, 173-184.
37. Li, T. K., and Liu, L. F. (2001) Tumor cell death induced by topoisomerase-targeting drugs, Annu. Rev. Pharmacol. Toxicol. 41, 53-77.
38. Toonen, T. R., and Hande, K. R. (2001) Topoisomerase II inhibitors, Cancer Chemother. Biol. Response Modif. 19, 129-147.
39. Walker, J. V., and Nitiss, J. L. (2002) DNA topoisomerase II as a target for cancer chemotherapy, Cancer Invest. 20, 570-589.
40. Baldwin, E. L., and Osheroff, N. (2005) Etoposide, topoisomerase II and cancer, Curr. Med. Chem.: Anti-Cancer Agents 5, 363-372.
41. Pommier, Y., and Marchand, C. (2005) Interfacial inhibitors of protein-nucleic acid interactions, Curr. Med. Chem.: Anti-Cancer Agents 5, 421-429.
42. Wang, H., Mao, Y., Chen, A. Y., Zhou, N., LaVoie, E. J., and Liu, L. F. (2001) Stimulation of topoisomerase II-mediated DNA damage via a mechanism involving protein thiolation, Biochemistry 40, 3316-3323.
43. Lindsey, R. H., Jr., Bromberg, K. D., Felix, C. A., and Osheroff, N. (2004) 1,4-Benzoquinone is a topoisomerase II poison, Biochemistry 43, 7563-7574.
44. Bender, R. P., Lindsey, R. H., Jr., Burden, D. A., and Osheroff, N. (2004) N-acetyl-p-benzoquinone imine, the toxic metabolite of acetaminophen, is a topoisomerase II poison, Biochemistry 43, 3731-3739.
45. Drake, F. H., Zimmerman, J. P., McCabe, F. L., Bartus, H. F., Per, S. R., Sullivan, D. M., Ross, W. E., Mattern, M. R., Johnson, R. K., Crooke, S. T., and Mirabelli, C. K. (1987) Purification of topoisomerase II from amsacrine-resistant P388 leukemia cells. Evidence for two forms of the enzyme, J. Biol. Chem. 262, 16739-16747.
46. Jenkins, J. R., Ayton, P., Jones, T., Davies, S. L., Simmons, D. L., Harris, A. L., Sheer, D., and Hickson, I. D. (1992) Isolation of cDNA clones encoding the beta isozyme of human DNA topoisomerase II and localisation of the gene to chromosome 3p24, Nucleic Acids Res. 20, 5587-5592.
47. Tan, K. B., Dorman, T. E., Falls, K. M., Chung, T. D., Mirabelli, C. K., Crooke, S. T., and Mao, J. (1992) Topoisomerase II alpha and topoisomerase II beta genes: characterization and mapping to human chromosomes 17 and 3, respectively, Cancer Res. 52, 231-234.
48. Austin, C. A., and Marsh, K. L. (1998) Eukaryotic DNA topoisomerase II beta, BioEssays 20, 215-226.
49. Heck, M. M., and Earnshaw, W. C. (1986) Topoisomerase II: A specific marker for cell proliferation, J. Cell Biol. 103, 2569-2581.
50. Isaacs, R. J., Davies, S. L., Sandri, M. I., Redwood, C., Wells, N. J., and Hickson, I. D. (1998) Physiological regulation of eukaryotic topoisomerase II, Biochim. Biophys. Acta 1400, 121-137.
51. Grue, P., Grasser, A., Sehested, M., Jensen, P. B., Uhse, A., Straub, T., Ness, W., and Boege, F. (1998) Essential mitotic functions of DNA topoisomerase IIα are not adopted by topoisomerase IIβ in human H69 cells, J. Biol. Chem. 273, 33660-33666.
52. Worland, S. T., and Wang, J. C. (1989) Inducible overexpression, purification, and active site mapping of DNA topoisomerase II from the yeast Saccharomyces cerevisiae, J. Biol. Chem. 264, 4412-4416.
53. Elsea, S. H., Hsiung, Y., Nitiss, J. L., and Osheroff, N. (1995) A yeast type II topoisomerase selected for resistance to quinolones. Mutation of histidine 1012 to tyrosine confers resistance to nonintercalative drugs but hypersensitivity to ellipticine, J. Biol. Chem. 270, 1913-1920.
54. Kingma, P. S., Greider, C. A., and Osheroff, N. (1997) Spontaneous DNA lesions poison human topoisomerase IIα and stimulate cleavage proximal to leukemic 11q23 chromosomal breakpoints, Biochemistry 36, 5934-5939.
55. McLean, M. R., Bauer, U., Amaro, A. R., and Robertson, L. W. (1996) Identification of catechol and hydroquinone metabolites of 4-monochlorobiphenyl, Chem. Res. Toxicol. 9, 158-164.
56. Espandiari, P., Glauert, H. P., Lehmler, H. J., Lee, E. Y., Srinivasan, C., and Robertson, L. W. (2004) Initiating activity of 4-chlorobiphenyl metabolites in the resistant hepatocyte model, Toxicol. Sci. 79, 41-46.
57. Fortune, J. M., and Osheroff, N. (1998) Merbarone inhibits the catalytic activity of human topoisomerase IIα by blocking DNA cleavage, J. Biol. Chem. 273, 17643-17650.
58. O'Reilly, E. K., and Kreuzer, K. N. (2002) A unique type II topoisomerase mutant that is hypersensitive to a broad range of cleavage-inducing antitumor agents, Biochemistry 41, 7989-7997.
59. Byl, J. A., Fortune, J. M., Burden, D. A., Nitiss, J. L., Utsugi, T., Yamada, Y., and Osheroff, N. (1999) DNA topoisomerases as targets for the anticancer drug TAS-103: primary cellular target and DNA cleavage enhancement, Biochemistry 38, 15573-15579.
60. Fortune, J. M., Dickey, J. S., Lavrukhin, O. V., Van Etten, J. L., Lloyd, R. S., and Osheroff, N. (2002) Site-specific DNA cleavage by Chlorella virus topoisomerase II, Biochemistry 41, 11761-11769.
61. Fortune, J. M., Lavrukhin, O. V., Gurnon, J. R., Van Etten, J. L., Lloyd, R. S., and Osheroff, N. (2001) Topoisomerase II from Chlorella virus PBCV-1 has an exceptionally high DNA cleavage activity, J. Biol. Chem. 276, 24401-24408.
62. Vaughn, J., Huang, S., Wessel, I., Sorensen, T. K., Hsieh, T., Jensen, L. H., Jensen, P. B., Sehested, M., and Nitiss, J. L. (2005) Stability of the topoisomerase II closed clamp conformation may influence DNA-stimulated ATP hydrolysis, J. Biol. Chem. 280, 11920-11929.
63. Subramanian, D., Kraut, E., Staubus, A., Young, D. C., and Muller, M. T. (1995) Analysis of topoisomerase I/DNA complexes in patients administered topotecan, Cancer Res. 55, 2097-2103.
64. Byl, J. A., Cline, S. D., Utsugi, T., Kobunai, T., Yamada, Y., and Osheroff, N. (2001) DNA topoisomerase II as the target for the anticancer drug TOP-53: mechanistic basis for drug action, Biochemistry 40, 712-718.
65. Lindsey, R. H., Jr., Bender, R. P., and Osheroff, N. (2005) Effects of benzene metabolites on DNA cleavage mediated by human topoisomerase II alpha: 1,4-hydroquinone is a topoisomerase II poison, Chem. Res. Toxicol. 18, 761-770.
66. Shen, Y., Shen, H. M., Shi, C. Y., and Ong, C. N. (1996) Benzene metabolites enhance reactive oxygen species generation in HL60 human leukemia cells, Hum. Exp. Toxicol. 15, 422-427.
67. Cavalieri, E. L., Stack, D. E., Devanesan, P. D., Todorovic, R., Dwivedy, I., Higginbotham, S., Johansson, S. L., Patil, K. D., Gross, M. L., Gooden, J. K., Ramanathan, R., Cerny, R. L., and Rogan, E. G. (1997) Molecular origin of cancer: catechol estrogen-3,4-quinones as endogenous tumor initiators, Proc. Natl. Acad. Sci. U.S.A. 94, 10937-10942.
68. Snyder, R. (2000) Overview of the toxicology of benzene, J. Toxicol. Environ. Health, Part A 61, 339-346.
69. Kingma, P. S., and Osheroff, N. (1998) Topoisomerase II-mediated DNA cleavage and religation in the absence of base pairing: abasic lesions as a tool to dissect enzyme mechanism, J. Biol. Chem. 273, 17999-18002.
70. Cline, S. D., Jones, W. R., Stone, M. P., and Osheroff, N. (1999) DNA abasic lesions in a different light: solution structure of an endogenous topoisomerase II poison, Biochemistry 38, 15500-15507.
71. Cline, S. D., and Osheroff, N. (1999) Cytosine arabinoside (araC) lesions are position-specific topoisomerase II poisons and stimulate DNA cleavage mediated by the human type II enzymes, J. Biol. Chem. 274, 29740-29743.
72. Sabourin, M., and Osheroff, N. (2000) Sensitivity of human type II topoisomerases to DNA damage: stimulation of enzyme-mediated DNA cleavage by abasic, oxidized and alkylated lesions, Nucleic Acids Res. 28, 1947-1954.
73. Velez-Cruz, R., Riggins, J. N., Daniels, J. S., Cai, H., Guengerich, F. P., Marnett, L. J., and Osheroff, N. (2005) Exocyclic DNA lesions stimulate DNA cleavage mediated by human topoisomerase II alpha in vitro and in cultured cells, Biochemistry 44, 3972-3981.
74. Capranico, G., and Binaschi, M. (1998) DNA sequence selectivity of topoisomerases and topoisomerase poisons, Biochim. Biophys. Acta 1400, 185-194.
75. Osheroff, N. (1989) Effect of antineoplastic agents on the DNA cleavage/religation reaction of eukaryotic topoisomerase II: inhibition of DNA religation by etoposide, Biochemistry 28, 6157-6160.
76. Bromberg, K. D., Burgin, A. B., and Osheroff, N. (2003) A two drug model for etoposide action against human topoisomerase IIα, J. Biol. Chem. 278, 7406-7412.
77. Robinson, M. J., Martin, B. A., Gootz, T. D., McGuirk, P. R., Moynihan, M., Sutcliffe, J. A., and Osheroff, N. (1991) Effects of quinolone derivatives on eukaryotic topoisomerase II. A novel mechanism for enhancement of enzyme-mediated DNA cleavage, J. Biol. Chem. 266, 14585-14592.
78. Bromberg, K. D., Burgin, A. B., and Osheroff, N. (2003) Quinolone action against human topoisomerase IIalpha: stimulation of enzyme-mediated double-stranded DNA cleavage, Biochemistry 42, 3393-3398.
79. Morris, S. K., Baird, C. L., and Lindsley, J. E. (2000) Steady-state and rapid kinetic analysis of topoisomerase II trapped as the closed-clamp intermediate by ICRF-193, J. Biol. Chem. 275, 2613-2618.
80. Berger, J. M., Gamblin, S. J., Harrison, S. C., and Wang, J. C. (1996) Structure and mechanism of DNA topoisomerase II, Nature 379, 225-232.
81. Osheroff, N. (1986) Eukaryotic topoisomerase II. Characterization of enzyme turnover, J. Biol. Chem. 261, 9944-9950.
82. Roca, J. (2004) The path of the DNA along the dimer interface of topoisomerase II, J. Biol. Chem. 279, 25783-25788.
83. Roca, J., and Wang, J. C. (1992) The capture of a DNA double helix by an ATP-dependent protein clamp: a key step in DNA transport by type II DNA topoisomerases, Cell 71, 833-840.
84. Roca, J., Ishida, R., Berger, J. M., Andoh, T., and Wang, J. C. (1994) Antitumor bisdioxopiperazines inhibit yeast DNA topoisomerase II by trapping the enzyme in the form of a closed protein clamp, Proc. Natl. Acad. Sci. U.S.A. 91, 1781-1785.
85. Waite, J. H. (1990) The phylogeny and chemical diversity of quinone-tanned glues and varnishes, Comp. Biochem. Physiol, B 97, 19-29.
86. Mason, D. E., and Liebler, D. C. (2003) Quantitative analysis of modified proteins by LC-MS/MS of peptides labeled with phenyl isocyanate, J. Proteome Res. 2, 265-272.
87. Weis, M., Morgenstern, R., Cotgreave, I. A., Nelson, S. D., and Moldeus, P. (1992) N-acetyl-p-benzoquinone imine-induced protein thiol modification in isolated rat hepatocytes, Biochem. Pharmacol. 43, 1493-1505.
88. Kim, K. S., and Kang, J. H. (2005) Aggregation of a-synuclein induced by oxidized catecholamines as a potential mechanism of Lewy body, Bull. Korean Chem. Soc. 26, 1255-1259.
89. Padget, K., Pearson, A. D., and Austin, C. A. (2000) Quantitation of DNA topoisomerase IIalpha and beta in human leukaemia cells by immunoblotting, Leukemia 14, 1997-2005.
90. Weiss, S. J., and Slivka, A. (1982) Monocyte and granulocyte-mediated tumor cell destruction. A role for the hydrogen peroxide-myeloperoxidase- chloride system, J. Clin. Invest. 69, 255-262.
91. Andoh, T., and Ishida, R. (1998) Catalytic inhibitors of DNA topoisomerase II, Biochim. Biophys. Acta 1400, 155-171.
92. Larsen, A. K., Escargueil, A. E., and Skladanowski, A. (2003) Catalytic topoisomerase II inhibitors in cancer therapy, Pharmacol. Ther. 99, 167-181.
93. Jensen, L. H., Nitiss, K. C., Rose, A., Dong, J., Zhou, J., Hu, T., Osheroff, N., Jensen, P. B., Sehested, M., and Nitiss, J. L. (2000) A novel mechanism of cell killing by anti-topoisomerase II bisdioxopiperazines, J. Biol. Chem. 275, 2137-2146.