Reduced expression of DNA topoisomerase II confers resistance to etoposide (VP-16) in small cell lung cancer cell lines established from a refractory tumor of a patient and by in vitro selection

Oncology Research

Volumn 8, Issue 6, 1996, Pages 229-238

  Andoh, Toshiwo ^a,b   Nishizawa, Miwako ^a   Hida, Toyoaki ^a   Ariyoshi, Yutaka ^a   Takahashi, Takashi ^a   Ueda, Ryuzo ^a  

^a AICHI CANCER CENTER HOSPITAL   (Japan)

^b SOKA UNIVERSITY   (Japan)

Author keywords

atypical MDR; DNA topoisomerase II; resistance; SCLC; VP 16

Indexed keywords

ANTINEOPLASTIC AGENT; DNA TOPOISOMERASE; DNA TOPOISOMERASE (ATP HYDROLYSING); DOXORUBICIN; ETOPOSIDE; IRINOTECAN; SOBUZOXANE; VINCRISTINE;

ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; DRUG RESISTANCE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LUNG SMALL CELL CANCER; PRIORITY JOURNAL;

EID: 0029964884     PISSN: 09650407     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. 1. Wang, J. C. DNA topoisomerases. Annu. Rev. Biochem. 54:665-697; 1985.
2. 2. Osheroff, N. Biochemical basis for the interactions of type I and type II topoisomerases with DNA. Pharmacol. Ther. 41:223-241; 1989.
3. 3. Watt, P. M.; Hickson, I. D. Structure and function of type II DNA topoisomerases. Biochem. J. 303:681-695; 1994.
4. 4. DiNardo, S.; Voelkel, K.; Sternglanz, R. DNA topoisomerase II mutant of Saccharomyces cerevisiae: topoisomerase II is required for segregation of daughter molecules at the termination of DNA replication. Proc. Natl. Acad. Sci. USA 81:2616-2620; 1984.
5. 5. Uemura, T.; Yanagida, M. Isolation of type I and II DNA topoisomerase mutants from fission yeast: single and double mutants show different phenotypes in cell growth and chromatin organization. EMBO J. 3:1737-1744; 1984.
6. 6. Uemura, T.; Yanagida, M. Mitotic spindle pulls but fails to separate chromosomes in type II DNA topoisomerase mutants: uncoordinated mitosis. EMBO J. 5:1003-1010; 1986.
7. 7. Uemura, T.; Ohkura, H.; Adachi, Y.; Morino, K.; Shiozaki, K.; Yanagida, M. DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50:917-925; 1987.
8. 8. Holm, C.; Goto, T.; Wang, J. C.; Botstein, D. DNA topoisomerase II is required at the time of mitosis in yeast. Cell 41:553-563; 1985.
9. 9. Newport, J.; Spann, T. Disassembly of the nucleus in mitotic extracts: membrane vesicularization, lamin disassembly, and chromosome condensation are independent processes. Cell 48:219-230; 1987.
10. 10. Wood, E. R.; Earnshaw, W. C. Mitotic chromatin condensation in vitro using somatic cell extracts and nuclei with variable levels of endogenous topoisomerase II. J. Cell Biol. 111:2839-2850; 1990.
11. 11. Adachi, Y.; Luke, M.; Laemmli, UK Chromosome assembly in vitro: topoisomerase II is required for condensation. Cell 64:137-148; 1991.
12. 12. Downes, C. S.; Mullinger, A. M.; Johnson, R. T. Inhibitors of DNA topoisomerase II prevent chromatid separation in mammalian cells but do not prevent exit from mitosis. Proc. Natl. Acad. Sci. USA 88:8895-8899; 1991.
13. 13. Shamu, C. E.; Murray, A. W. Sister chromatid separation in frog egg extracts requires DNA topoisomerase II activity during anaphase. J. Cell Biol. 117:921-934; 1992.
14. 14. Hirano, T.; Mitchison, T. J. Cell cycle control of higher-order chromatin assembly around naked DNA in vitro. J. Cell Biol. 115:1479-1489; 1991.
15. 15. Drake, F. H.; Hoffmann, G. A.; Mong, S.-M.; Bartus, H. F.; Hertzberg, R. P.; Johnson, R. K.; Mattern, M. R.; Mirabelli, C. K. In vitro and intracellular inhibition of topoisomerase II by the antitumor agent merbarone. Cancer Res. 49:2578-2583; 1989.
16. 16. Bojanowski, K.; Lelievre, S.; Markovits, J.; Couprie, J.; Jacquemin-Sablon, A.; Larsen, A. K. Suramin is an inhibitor of DNA topoisomerase II in vitro and in Chinese hamster fibrosarcoma cells. Proc. Natl. Acad. Sci. USA 89:3025-3029; 1992.
17. 17. Tanabe, K.; Ikegami, Y.; Ishida, R.; Andoh, T. Inhibition of topoisomerase II by antitumor agents bis(2,6-dioxopiperazine) derivatives. Cancer Res. 51:4903-4908; 1991.
18. 18. Ishida, R.; Miki, T.; Narita, T.; Yui, R.; Sato, M.; Utsumi, K. R.; Tanabe, K.; Andoh.T. Inhibition of intracellular topoisomerase II by antitumor bis(2,6-dioxopiperazine) derivatives: mode of cell growth inhibition distinct from that of cleavable complex-forming type inhibitors. Cancer Res. 51:4909-4916; 1991.
19. 19. Ishida, R.; Sato, M.; Narita, T.; Utsumi, K. R.; Nishimoto, T.; Morita, T.; Nagata, H.; Andoh, T. Inhibition of DNA topoisomerase II by ICRF-193 induces polyploidization by uncoupling chromosome dynamics from other cell cycle events. J. Cell Biol. 126:1341-1351; 1994.
20. 20. Gorbsky, G. J. Cell cycle progression and chromosome segregation in mammalian cells cultured in the presence of the topoisomerase inhibitors ICRF-187 [(+)-1,2-bis(3,5-dioxopiperazinyl-1-yl)propane; ADR-529] and ICRF-159 (Razoxane). Cancer Res. 54:1042-1048; 1994.
21. 21. Liu, L. F. DNA topoisomerase poisons as antitumor drugs. Annu. Rev. Biochem. 58:351-375; 1989.
22. 22. Osheroff, N.; Corbett, A. H.; Robinson, M. J. Mechanism of action of topoisomerase II-targeted anti-neoplastic drugs. In Liu, L. F., ed., DNA topoisomerases: topoisomerase-targeting drugs. Adv. Pharmacol. 29B, New York: Academic Press; 1994: pp. 105-126.
23. 23. Gottesman, M. M.; Schoenlein, P. V.; Currier, S. J.; Bruggemann, E. P.; Pastan, I. Biochemical basis for multidrug resistance in cancer. In: Pretlow, T.; Pretlow, T., eds. Biochemical and molecular aspects of selected cancers, vol. 1. San Diego: Academic Press; 1991:pp. 339-371.
24. 24. Cole, S. P. C; Bhardwaj, G.; Gerlach, J. H.; MacKie, J. E.; Grant, C. E.; Almquist, K. C.; Stewart, A. J.; Kurz, E. U.; Duncan, A. M. V. ; Deeley, R. G. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258:1650-1654; 1992.
25. 25. Sullivan, D. M.; Ross, W. E. Resistance to inhibitors of DNA topoisomerases. In: Ozols, R. F., ed. Molecular and clinical advances in anticancer drug resistance. Boston: Kluwer Academic; 1991; pp. 57-99.
26. 26. Beck, W. T.; Danks, M. K.; Wolverton, J. S.; Kim, R.; Chen, M. Drug resistance associataed with altered DNA topoisomerase II. Adv. Enzyme Regul. 33:113-127; 1993.
27. 27. Beck, W. T.; Danks, M. K.; Wolverton, J. S.; Chen, M.; Granzen, B.; Kim, R.; Suttle, D. P. Resistance of mammalian tumor cells to inhibitors of DNA topoisomerase II. In: Liu, L. F. ed, DNA topoisomerases: topoisomerase-targeting drugs. New York: Academic Press; 1994:pp. 145-169.
28. 28. Glisson, B.; Gupta, R.; Smallwood-Kentro, S.; Ross, W. Characterization of acquired epipodophyllotoxin resistance in a Chinese hamster ovary cell line: loss of drug-stimulated DNA cleavage activity. Cancer Res. 46: 1934-1938; 1986.
29. 29. Danks, M. K.; Yalowich, J. Y; Beck, W. T. Atypical multiple drug resistance in a human leukemic cell line selected for resistance to teniposide (VM-26). Cancer Res. 47:1297-1301; 1987.
30. 30. Friche, E.; Danks, M. K.; Schmidt, C. A.; Beck, W. T. Decreased DNA topoisomerase II in daunorubicin-resistant Ehrlich ascites tumor cells. Cancer Res. 51: 4213-4218; 1991.
31. 31. Deffie, A. M.; Batra, J. K.; Goldenberg, G. J. Direct correlation between DNA topoisomerase II activity and cytotoxicity in adriamycin-sensitive and -resistant P388 leukemia cell lines. Cancer Res. 49:58-62; 1989.
32. 32. Ferguson, P. J.; Fisher, M. H.; Stephenson, J.; Li, D., Zhou, B.; Cheng. Y.-C. Combined modalities of resistance in etoposide-resistant human KB cell lines. Cancer Res. 48:5956-5964, 1988.
33. 33. Matsuo, K.; Kohno, K.; Takano, H.; Sato, S.; Kiue, A.; Kuwano, M. Reduction of drug accumulation and DNA topoisomerase II activity in acquired teniposide-resistant human cancer KB cell lines. Cancer Res. 50:5819-5824, 1990.
34. 34. Takano, H.; Kohno, K.; Ono, M.; Uchida, Y.; Kuwano, M. Increased phosphorylation of DNA topoisomerase II in etoposide-resistant mutants of human cancer KB cells. Cancer Res. 51:3951-3957; 1991.
35. 35. Campain, J. A.; Padmanabhan, R.; Hwang, J.; Gottesman, M. M.; Pastan, I. Characterization of an unusual mutant of human melanoma cells resistant to anticancer drugs that inhibit topoisomerase II. J. Cell. Physiol. 155:414-425; 1993.
36. 36. Vassetzky, Y. S.; Alghisi, G.-C.; Gasser, S. M. DNA topoisomerase II mutants and resistance to antitumor drugs. BioEssays 17:767-774; 1995.
37. 37. Danks, M. K.; Schmidt, C. A.; Cirtain, M. C.; Suttle, D. P.; Beck, W. T. Altered catalytic activity of and DNA cleavage by DNA topoisomerase II from human leukemic cells selected for resistance to VM-26. Biochemistry 27:8861-8869; 1988.
38. 38. Danks, M. K.; Schmidt, C. A.; Deneka, D. A.; Beck, W. T. Increased ATP requirement for activity of and complex formation by DNA topoisomerase II from human leukemic CCRF-CEM cells selected for resistance to teniposide. Cancer Commun. 1:101-109; 1989.
39. r 170,000 isozyme of DNA topoisomerase II in human tumor cells. Cancer Res. 53:1373-1379; 1993.
40. 40. Zwelling, L. A.; Hinds, M.; Chan, D.; Mayes, J.; Sie, K. L.; Parker, E.; Silberman, L.; Radcliff, A.; Beran, M.; Blick, M. Characterization of an amsacrine-resistant line of human leukemia cells. J. Biol. Chem. 264:16411-16420; 1989.
41. 41. Sullivan, D. M.; Latham, M. D.; Rowe, T. C.; Ross, W. E. Purification and characterization of an altered topoisomerase II from a drug-resistant chinese hamster ovary cell line. Biochemistry 28:5680-5687; 1989.
42. 42. Bugg, B. Y.; Danks, M. K.; Beck, W. T.; Suttle, D. P. Expression of a mutant DNA topoisomerase II in CCRF-CEM human leukemic cells selected for resistance to teniposide. Proc. Natl. Acad. Sci. USA 88:7654-7658, 1991.
43. 43. Hinds, M.; Deisseroth, K.; Mayes, J.; Altschuler, E.; Jansen, R.; Ledley, F. D.; Zwelling, L. A. Identification of a point mutation in the topoisomerase II gene from a human leukemia cell line containing an amsacrine-resistant form of topoisomerase II. Cancer Res. 51:4729-4731; 1991.
44. 44. Lee, M.-D.; Wang, J. C.; Beran, M. Two independent amsacrine-resistant human myeloid leukemia cell lines share an identical point mutation in the 170 kDa form of human topoisomerase II. J. Mol. Biol. 223:837-843; 1992.
45. 45. Chan, V. T.; Ng, S. W.; Eder, J. P.; Schnipper, L. E. Molecular cloning and identification of a point mutation in the topoisomerase II cDNA from an etoposide-resis-tant Chinese hamster ovary cell line. J. Biol. Chem. 268:2160-2165; 1993.
46. 46. Patel, S.; Fisher, L. M. Novel selection and genetic characterization of an etoposide-resistant human leukemic CCRF-CEM cell line. Br. J. Cancer 67:456-463; 1993.
47. 47. Harker, W. G.; Knight, C.; Slade, D. L.; Kapoor, R.; Parr, R. Reduced topoisomerase II activity in human CEM leukemia cells selected for resistance to mitoxantrone. Proc. Am. Assoc. Cancer Res. Annu. Meet. 33:452; 1992.
48. 48. Ritke, M. K.; Roberts, W. P.; Raymond, A. J.; Bergoltz, V. V.; Yalowich, J. C. Altered stability of etoposide-induced topoisomerase II-DNA complexes in resistant human leukaemia K562 cells. Br. J. Cancer 69:687-697; 1994.
49. 49. Chen, M.; Wolverton, J. S.; Beck, W. T. Pleiotropic effects of altered DNA topoisomerase II in VM-26-resistant CEM cells. Proc. Am. Assoc. Cancer Res. Annu. Meet. 33:2707; 1992.
50. 50. Hida, T.; Ueda, R.; Takahashi, T.; Watanabe, H.; Kato, T.; Suyaraa, M.; Sugiura, T.; Ariyoshi, Y.; Takahashi, T. Chemosensitivity of small cell lung cancer cell lines studied by a newly developed 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) hybrid assay. Cancer Res. 49:4785-4790; 1989.
51. 51. Hida, T.; Ariyoshi, Y.; Kuwabara, M.; Sugiura, T.; Takahashi, T.; Takahashi, T.; Hosoda, K.; Niitsu, Y.; Ueda, R. Glutathione S-transferase π levels in a panel of lung cancer cell lines and its relation to chemo-radiosensitivity. Jpn. J. Clin. Oncol. 23:14-19; 1993.
52. 52. Mosmann, T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65:55-63; 1983.
53. 53. Hamburger, A.; Salmon, S. E. Primary bioassay of human myeloma stem cells. J. Clin. Invest. 60:846-854; 1977.
54. 54. Ishii, K.; Hasegawa, T.; Fujisawa, K.; Andoh, T. Rapid purification and characterization of DNA topoisomerase I from cultured mouse mammary carcinoma FM3A cells. J. Biol. Chem. 258:12728-12732; 1983.
55. 55. Liu, L. F.; Davis, J. L. Novel topologically knotted DNA from bacteriophage P4 capsids: studies with DNA topoisomerases. Nucl. Acids Res. 9:3979-3989; 1981.
56. 56. Laemmli, UK Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685; 1970.
57. 57. Chomczynski, P.; Sacchi, N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159; 1987.
58. 58. Sambrook, J.; Fritsch, E. F.; Maniatis, T. Analysis of RNA. In: Molecular cloning. A laboratory manual, 2nd ed. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 1989: pp. 7.37-7.52.
59. 59. Tsutsui, K.; Tsutsui, K.; Okada, S.; Watanabe, M.; Shohmori, T.; Seki, S.; Inoue, Y. Molecular cloning of partial cDNAs for rat DNA topoisomerase II isoforms and their differential expression in brain development. J. Biol. Chem. 268:19076-19083; 1993.
60. 60. Tamura, H.; Kohchi, C.; Yamada, R.; Ikeda, T.; Koiwai, O.; Patterson, E.; Keene, J.; Okada, K.; Kjeldsen, E.; Nishikawa, K.; Andoh, T. Molecular cloning of a cDNA of a camptothecin-resistant human DNA topoisomerase I and identification of mutation sites. Nucl. Acids Res. 19:69-75; 1991.
61. 61. Nakajima-Iijima, S.; Hamada, H.; Reddy, P.; Kakunaga, T. Molecular structure of the human cytoplasmic β-actin gene: interspecies homology of sequences in the introns. Proc. Natl. Acad. Sci. USA 82:6133-6137; 1985.
62. 62. Chung, T. D. Y.; Drake, F. H.; Tan, K. B.; Per, S. R.; Crooke, S. T.; Mirabelli, C. K. Characterization and immunological identification of cDNA clones encoding two human DNA topoisomerase II isozymes. Proc. Natl. Acad. Sci. USA 86:9431-9435; 1989.
63. 63. 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.; Mirabelli, C. K. Purification of topoisomerase II from amsacrine-resistant P388 leukemia cells: evidence for two forms of the enzyme. J. Biol. Chem. 262:16739-16747; 1987.
64. 64. Drake, F. H.; Hoffmann, G. A.; Bartus, H. F.; Mattern, M. R.; Crooke, S. T.; Mirabelli, C. K. Biochemical and pharmacological properties of p 170 and p 180 forms of topoisomerase II. Biochemistry 28:8154-160; 1989.
65. 65. deJong, S.; Kooistra, A. J.; deVries, E. G. E.; Mulder, N. H.; Zijlstra, J. G. Topoisomerase II as a target of VM-26 and 4′-(9-acridinylamino)-methanesulfon-m-aniside in atypical multidrug resistant human small cell lung carcinoma cells. Cancer Res. 53:1064-1071; 1993.
66. 66. Kubo, T.; Kohno, K.; Ohga, T.; Taniguchi, K.; Kawanami, K,; Wada, M.; Kuwano, M. DNA topoisomerase IIα gene expression under transcriptional control in etoposide/teniposide-resistant human cancer cells. Cancer Res. 55:3860-3964; 1995.