Camptothecin resistance involving steps subsequent to the formation of protein-linked DNA breaks in human camptothecin-resistant KB cell lines

Cancer Research

Volumn 56, Issue 2, 1996, Pages 345-353

  Beidler, David R ^a,b   Chang, Jang Yang ^a,c   Zhou, Bing Sen ^a,d   Cheng, Yung Chi ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^d CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAMPTOTHECIN; DOUBLE STRANDED DNA;

ARTICLE; CELL STRAIN KB; CYTOSTASIS; DNA DAMAGE; DNA STRAND BREAKAGE; DRUG RESISTANCE; ENZYME ACTIVITY; ENZYME INHIBITION; GENETIC LINKAGE; GROWTH INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; REVERTANT; RNA SYNTHESIS;

BENZAMIDES; CAMPTOTHECIN; CELL CYCLE; CELL DIVISION; DNA DAMAGE; DNA TOPOISOMERASES, TYPE I; DNA, NEOPLASM; DNA-BINDING PROTEINS; DRUG RESISTANCE, NEOPLASM; ELECTROPHORESIS; ENZYME INHIBITORS; HUMANS; IMMUNOBLOTTING; KB CELLS; POLY(ADP-RIBOSE) POLYMERASES; RNA, NEOPLASM;

EID: 0030057744     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (69)

1. Horwitz, S. B., Chang, C-K., and Grollman, A. P. Studies on camptothecin. 1. Effects on nucleic acid and protein synthesis. Mol. Pharmacol., 7: 632-644, 1971.
2. Horwitz, S B., and Horwitz, M. S. Effects of camptothecin on the breakage and repair of DNA during the cell cycle. Cancer Res., 33: 2834-2836, 1973.
3. Kessel, D Effects of camptothecin on RNA synthesis in leukemia L1210 cells Biochim. Biophys. Acta, 240: 225-232, 1971.
4. Kessel, D., Bosmann, H. B., and Lohr, K. Camptothecin effects on DNA: synthesis in murine leukemia cells. Biochim. Biophys. Acta, 269: 210-216, 1972.
5. Hsiang, Y-H., Hertzberg, R., Hecht, S., and Liu, L. F. Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I. J. Biol. Chem., 260: 14873-14878, 1985.
6. Wang, J. C. Recent studies of DNA topoisomerases. Biochim. Biophys. Acta, 909: 1-9, 1987.
7. Wang, J. C. DNA topoisomerases. Annu. Rev. Biochem., 54: 665-697, 1985.
8. Liu, L F HeLa topoisomerase I. Methods Enzymol., 100: 133-180, 1983.
9. Champoux, J. Evidence for an Intermediate with a single-strand break in the reaction catalyzed by the DNA untwisting enzyme. Proc. Natl. Acad. Sci. USA, 73: 3488-3491, 1976
10. Champoux, J. Mechanism of the reaction catalyzed by the DNA untwisting enzyme: attachment of the enzyme to the 3′-terminus of the nicked DNA. J. Mol Biol., 118: 441-446, 1978.
11. Champoux, J. J. DNA is linked to the rat liver DNA nick-closing enzyme by a phosphodiester bond to tyrosine. J Biol. Chem., 256. 4805-4809, 1981.
12. Eng, W-k , Pandit, S. D., and Sternglanz, R. Mapping of the active site tyrosine of eukaryotic DNA topoisomerase I. J. Biol. Chem., 264: 13373-13376, 1989.
13. Lynn, R. M., Bjornsti, M-A., Caron, P R , and Wang, J C Peptide sequencing and site-directed mutagenesis identify tyrosine-727 as the active site tyrosine of Saccharomyces cerevisiae DNA topoisomerase I. Proc. Natl. Acad. Sci. USA, 86: 3559-3563, 1989.
14. Hsiang, Y-H., and Liu, L. F. Identification of mammalian DNA topoisomerase I as an intracellular target of the anticancer drug camptothecin Cancer Res., 48: 1722-1726, 1988.
15. Hsiang, Y-H., Lihou, M. G., and Liu, L. F. Arrest of replication forks by drug-stabilized topoisomerase I-DNA cleavable complexes as a mechanism of cell killing by camptothecin. Cancer Res , 49: 5077-5082, 1989
16. Li, L H., Fraser, T. J., Olin, E. J., and Bhuyan, B. K. Action of camptothecin on mammalian cells in culture Cancer Res., 32: 2643-2650, 1972.
17. Holm, C., Covey, J. M , Kerrigan, D , and Pommier, Y. Differential requirement of DNA. replication for the cytotoxicity of DNA topoisomerase I and II inhibitors in Chinese hamster DC3F Cells. Cancer Res., 49: 6365-6368, 1989
18. Nitiss, J., and Wang, J C. DNA topoisomerase-targeting antitumor drugs can be studied in yeast Proc. Natl. Acad. Sci USA, 85: 7501-7505, 1988.
19. Eng, W-K , Faucette, L , Johnson, R. K., and Sternglanz, R. Evidence that DNA topoisomerase I is necessary for the cytotoxic effects of camptothecin. Mol Pharmacol., 34: 755-760, 1988.
20. Smith, P J , Makinson, T A , and Watson, J. V. Enhanced sensitivity to camptothecin ataxia-telangiectasia and its relationship with the expression of DNA topoisomerase I Int. J. Radiat. Biol., 55: 217-231, 1989.
21. Squires, S., Oates, D J., Bouffler, S. D , and Johnson, R. T. Cockayne's syndrome fibroblasts are characterized by hypersensitivity to deoxyguanosine and abnormal DNA precursor pool metabolism in response to deoxyguanosine or ultraviolet light. Somatic Cell Mol. Genet., 18: 387-401, 1992
22. Andoh, T., Ishii, K., Suzuki, Y , Ikegami, Y., Kusunoki, Y., Takemoto, Y , and Okada, K. Characterization of a mammalian mutant with a camptothecin-resistant DNA topoisomerase I. Proc. Natl. Acad. Sci. USA, 84: 5565-5569, 1987.
23. Chang, J-Y., Dethleften, L. A., Barley, L. R., Zhou, B-s., and Cheng, Y-c. Characterization of camptothecin-resistant Chinese hamster lung cells. Biochem. Pharm., 43 2443-2452, 1992
24. Eng, W-K., McCabe, F L., Tan, K. B., Mattern, M. R., Hofmann, G. A., Woessner, R. D., Hertzberg, R. P., and Johnson, R. K. Development of a stable camptothecin-resistant subline of P388 leukemia with reduced topoisomerase I content. Mol. Pharmacol , 38: 471-480, 1990
25. Gupta, R. S., Gupta, R , Eng, B., Lock, R. B., Ross, W. E., Hertzberg, R. P., Caranfa, M. J., and Johnson, R K. Camptothecin-resistant mutants of Chinese hamster ovary cells contamine a resistant form of topoisomerase I. Cancer Res., 48: 6404-6410, 1988.
26. Kanzawa, F., Sugimoto, Y , Minato, K., Kasahara, K., Bungo, M., Nakagawa, K , Fujiwara, Y , Liu, L. F., and Saijo, N. Establishment of a camptothecin analogue (CPT-11)-resistant cell line of human non-small cell lung cancer: characterization and mechanism of resistance. Cancer Res., 50: 5919-5924, 1990.
27. Madelaine, I., Prost, S., Naudin, A , Riou, G , Lavelle, F., and Riou, J-F. Sequential modifications of topoisomerase I: activity in a camptothecin-resistant cell line established by progressive adaptation. Biochem Pharm., 45: 339-348, 1993
28. Matsumoto, Y , Fujiwara, T., Honjo, Y., Sasaoka, N., Tsuchida, T., and Nagao, S Quantitative analysis of DNA topoisomerase I. Activity in human and rat glioma: characterization and mechanism of resistance to antitopoisomerase chemical, camptothecin-11. J Surg. Oncol., 53. 97-103, 1993.
29. Oguro, M , Seki, Y., Okada, K., and Andoh, T. Collateral drug sensitivity in CPT-11 (a novel derivative of camptothecin)-resistant cell lines. Biomediques Pharmacotherapeutics, 44 209-216, 1990.
30. Sugimoto, Y , Tsukahara, S , Oh-hara, T., Liu, L. F., and Tsuruo, T. Elevated expression of topoisomerase II in camptothecin-resistant human tumor cell lines. Cancer Res., 50: 7962-7965, 1990.
31. Sugimoto, Y., Tsukahara, S., Oh-hara, T., Isoe, T , and Tsuruo, T Decreased expression of DNA topoisomerase I in camptothecin-resistant tumor cell lines as determined by a monoclonal antibody Cancer Res., 50: 6925-6930, 1990.
32. Tan, K. B., Mattern, M. R , Eng, W-K., McCabe, F. L , and Johnson, R. K. Nonproductive rearrangement of DNA topoisomerase I and II genes, correlation with resistance to topoisomerase inhibitors. J. Natl Cancer Inst., 81: 1732-1735, 1989.
33. Tanizawa, A., and Pommier, Y Topoisomerase I: alteration in a camptothecin-resistant cell line derived from Chinese hamster DC3F cells in culture. Cancer Res., 52: 1848-1854, 1992
34. Woessner, R. D., Eng, W-K , Hofmann, G A., Rieman, D. J., McCabe, F. L., Hertzberg, R. P., Mattern, M. R , Tan, K B , and Johnson, R. K. Camptothecin hyper-resistant P388 cells: drug-dependent reduction in topoisomerase I content. Oncol Res., 4: 481-488, 1992.
35. Jett, J H. Mathematical analysis of DNA. histograms from asynchronous and synchronous cell populations. In: D. Lutz (ed.), Pulse Cytophotometry, pp 93-102. Brussels, Belgium: European Press, 1978.
36. Liu, L. F., and Miller, K. G. Eukaryotic DNA topoisomerases: two forms of type I DNA topoisomerases from HeLa cell nuclei Proc. Natl. Acad Sci USA, 78: 3487-3491, 1981.
37. Beidler, D R., and Cheng, Y-C. Camptothecin induction of a time- and concentration-dependent decrease of topoisomerase I and its implication in camptothecin activity. Mol Pharmacol., 47: 907-914, 1995
38. Zhou, B-s , Beidler, D. R., and Cheng, Y-c. Identification of antisense RNA transcripts from a human DNA topoisomerase I pseudogene. Cancer Res., 52: 4280-4285, 1992.
39. Denko, N., Giaccia, A , Peters, B., and Stamato, T D. An asymmetric field inversion gel electrophoresis method for the separation of large DNA molecules. Anal Biochem., 178: 172-176, 1989.
40. Stamato, T. D., and Denko, N. Asymmetric field inversion gel electrophoresis: a new method for detecting DNA double-strand breaks in mammalian cells. Radiat Res., 121: 196-205, 1990.
41. Ryan, A. J., Squires, S., Strutt, H. L , and Johnson, R T Camptothecin cytotoxicity in mammalian cells is associated with the induction of persistent double strand breaks in replicating DNA. Nucleic Acids Res., 19: 3295-3300, 1991.
42. Iliakis, G. E., Metzger, L , Denko, N., and Stamato, T D. Detection of DNA Double-strand breaks in synchronous cultures of CHO cells by means of asymmetric field inversion gel electrophoresis. Int. J. Radiat. Biol., 59: 321-341, 1991
43. Ormerod, M. G., Collins, M K. L., Rodriguez-Tarduchy, G., and Robertson, D. Apoptosis in interleukin-3-dependent haemopoietic cells. J. Immunol. Methods, 153: 57-65, 1992.
44. Hsiang, Y-H , Liu, L. F , Wall, M E., Wani, M. C , Nicholas, A. W., Manikumar, G , Kirschenbaum, S., Silber, R., and Potmesil, M DNA topoisomerase I-mediated DNA: cleavage and cytotoxicity of camptothecin analogues. Cancer Res., 49: 4385-4389, 1989.
45. Covey, J M., Jaxel, C., Kohn, K W., and Pommier, Y Protein-linked DNA strand breaks induced in mammalian cells by camptothecin, an inhibitor of topoisomerase I. Cancer Res., 49: 5016-5022, 1989.
46. Samuels, S. D , and Shimizu, N. The predominant form of mammalian DNA topoisomerase I in vivo has a molecular mass of 100 kDa Mol. Biol. Rep , 19: 99-103, 1994.
47. Alsner, J , Svejstrup, J. Q., Kjeldsen, E., Sorensen, B. S , and Westergaard, O. Identification of an N-terminal domain of eukaryotic DNA topoisomerase I dispensable for catalytic activity but essential for in vivo function. J. Biol. Chem., 267: 12408-12411, 1992.
48. Gallo, R. C., Whang-Peng, J , and Adamson, R. H. Studies on the antitumor activity, mechanism of action, and cell cycle effects of camptothecin. J. Natl Cancer Inst., 46: 789-795, 1971.
49. Tobey, R. A. Effects of cytosine arabinoside, daunomycin, mithramycin, azacytidine, Adriamycin, and camptothecin on mammalian cell cycle traverse Cancer Res., 32: 2720-2725, 1972.
50. 2 arrest: altered regulation of P34cdc2/cyclin B. Cancer Res., 52. 1823-1829, 1992.
51. Bertrand, R., Sarang, M., Jenkin, J., Kerrigan, D., and Pommier, Y. Differential induction of secondary DNA: fragmentation by topoisomerase II inhibitors in human tumor cell lines with amplified c-myc expression. Cancer Res , 51. 6280-6285, 1991.
52. Kaufmann, S. H. Induction of endonucleolytic DNA cleavage in human acute myelogenous leukemia cells by etoposide, camptothecin, and other cytotoxic anticancer drugs: a cautionary note. Cancer Res., 49: 5870-5878, 1989.
53. Boulikas, T. Relation between carcinogenesis, chromatin structure, and Poly(ADP-ribosylation)(Review). Anticancer Res., 11: 489-528, 1991.
54. Satoh, M S., and Lindahl, T. Role of Poly(ADP-ribose) formation in DNA repair Nature (Lond.), 356: 356-358, 1992.
55. Banasik, M., Komura, H , Shimoyama, M., and Ueda, K. Specific inhibitors of poly(ADP-ribose) synthetase and mono(ADP-ribosyl)transferase. J. Biol. Chem., 267: 1569-1575, 1992.
56. Rankin, P. W , Jacobson, E. L., Benjamin, R. C., Moss, J., and Jacobson, M. K. Quantitative studies of inhibitors of ADP-ribosylation in vitro and in vivo. J. Biol. Chem., 264: 4312-4317, 1989.
57. Durkacz, B W., Omidiji, O , Gray, D. A , and Shall, S. (ADP-ribose) participants in DNA excision repair. Nature (Lond.), 283: 593-596, 1980.
58. Ben-hur, E., Utsumi, H., and Blkind, M. M. Inhibitors of poly(ADP-ribose) synthesis enhance X-ray killing of log-phase Chinese hamster cells. Radiat. Res., 97: 546-555, 1984
59. Huet, J., and Laval, F. Potentiation of cell killing by inhibitors of poly(adenosine diphosphate ribose) synthesis in bleomycin-treated Chinese hamster ovary cells. Cancer Res., 45. 987-991, 1985.
60. Chen, G , and Zeller, W. J. Reversal of acquired cisplatin resistance by nicotinamide in vitro and in vivo. Cancer Chemother. Pharmacol., 33: 157-162, 1993.
61. Ferro, A. M., Higgins, N. P., and Olivera, B. M. Poly(ADP-ribosylation) of a DNA topoisomerase. J. Biol. Chem., 258: 6000-6003, 1983.
62. Ferro, A. M., and Olivera, B. M. Poly(ADP-Ribosylation) of DNA topoisomerase I from calf thymus. J. Biol. Chem., 259: 547-554, 1984.
63. Jongstra-Bilen, J., Ittel, M-E., Niedergang, C., Vosberg, H-P., and Mandel, P. DNA topoisomerase from calf thymus is inhibited in vitro by poly(ADP-ribosylation). Eur. J. Biochem., 136: 391-396, 1983.
64. Kasid, U. N., Halligan, B , Liu, L. F., Dritschilo, A., and Smulson, M. Poly(ADP-ribose)-mediated post-translational modification of chromatin-associated human topoisomerase I. J. Biol Chem., 264: 18687-18692, 1989.
65. Krupitza, G., and Cerutti, P. ADP-ribosylation of ADPR-transferase and topoisomerase I in intact mouse epidermal cells JB6. Biochemistry, 28: 2034-2040, 1989.
66. Mattern, M. R., Mong, S-M , Bartus, H. F., Mirabelli, C. K , Crooke, S. T., and Johnson, R. K. Relationship between the intracellular effects of camptothecin and the inhibition of DNA topoisomerase I in cultured L1210 cells. Cancer Res , 47: 1793-1798, 1987.
67. Chatterjee, S., Cheng, M. F , and Berger, N. A. Hypersensitivity to clinically useful alkylating agents and radiation in poly(ADP-ribose) polymerase-deficient cell lines. Cancer Commun., 2: 401-407, 1990.
68. Chatterjee, S., Cheng, M-F., Trivedi, D., Petzold, S. J., and Berger, N. A. Camptothecin hypersensitivity in poly(adenosine diphosphate-ribose) polymerase-deficient cell lines. Cancer Commun., 1. 389-394, 1990.
69. Rosemann, M , Kanon, B., Konings, A. W. T , and Kampinga, H. H. An image analysis technique for detection of radiation-induced DNA fragmentation after CHEF electrophoresis. Int. J. Radiat. Biol., 64: 245-249, 1993.