Cell density-dependent VP-16 sensitivity of leukaemic cells is accompanied by the translocation of topoisomerase IIα from the nucleus to the cytoplasm

British Journal of Haematology

Volumn 108, Issue 2, 2000, Pages 331-345

  Valkov, N I ^a   Gump, J L ^a   Engel, R ^a   Sullivan, D M ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

Drug resistance; Leukaemia; Multiple myeloma; Topoisomerase II ; VP 16

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING); ETOPOSIDE;

ANIMAL CELL; ARTICLE; CELL DENSITY; CONTROLLED STUDY; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; INTRACELLULAR TRANSPORT; LEUKEMIA; LEUKEMIA CELL; MULTIPLE MYELOMA; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; QUANTITATIVE ASSAY;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; BLOTTING, WESTERN; CELL NUCLEUS; CYTOPLASM; DNA TOPOISOMERASES, TYPE I; DRUG RESISTANCE, NEOPLASM; ETOPOSIDE; FLOW CYTOMETRY; HUMANS; LEUKEMIA; MULTIPLE MYELOMA; PHENOTYPE; TRANSLOCATION, GENETIC; TUMOR CELLS, CULTURED;

EID: 0034053994     PISSN: 00071048     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2141.2000.01832.x     Document Type: Article

References (51)

1. Austin, C.A., Marsh, K.L., Wasserman, R.A., Willmore, E., Sayer, P.J., Wang, J.C. & Fisher, L.M. (1995) Expression, domain structure, and enzymatic properties of an active recombinant human DNA topoisomerase IIβ. Journal of Biological Chemistry, 270, 15739-15746.
2. Beidler, D.R. & Cheng, Y.-C. (1995) Camptothecin induction of a time-and concentration-dependent decrease of topoisomerase I and its implication in camptothecin activity. Molecular Pharmacology, 47, 907-914.
3. Boege, F.A., Andersen, A.H., Jensen, S., Zeidler, R. & Kreipe, H. (1995) Proliferation-associated nuclear antigen Ki-S1 is identical with topoisomerase II alpha. American Journal of Pathology, 146, 1302-1308.
4. Burden, D.A., Goldsmith, L.J. & Sullivan, D.M. (1993) Cell-cycle-dependent phosphorylation and activity of Chinese hamster ovary topoisomerase II. Biochemical Journal, 293, 297-304.
5. Burden, D.A., Kingma, P.S., Froelich-Ammon, S.J., Bjornsti, M.-A., Patchan, M.W., Thompson, R.B. & Osheroff, N. (1996) Topoisomerase II * etoposide interactions direct the formation of drug-induced enzyme-DNA cleavage complexes. Journal of Biological Chemistry, 271, 29238-29244.
6. Burden, D.A. & Sullivan, D.M. (1994) Phosphorylation of the α-and β-isoforms of DNA topoisomerase II is qualitatively different in interphase and mitosis in Chinese hamster ovary cells. Biochemistry, 33, 14651-14655.
7. Chapuis, J.-C., Keng, P.C. & Siemann, D.W. (1992) Activity of etoposide (VP-16) and teniposide (VM-26) in exponential and plateau phase human tumor cell cultures. Anti-Cancer Drugs, 3, 245-252.
8. Chow, K.-C. & Ross, W.E. (1987) Topoisomerase-specific drug sensitivity in relation to cell cycle progression. Molecular and Cellular Biology, 7, 3119-3123.
9. Croix, B.S. & Kerbel, R.S. (1997) Cell adhesion and drug resistance in cancer. Current Opinions in Oncology, 9, 549-556.
10. Dang, Q., Alghisi, G.C. & Gasser, S.M. (1994) Phosphorylation of the C-terminal domain of yeast topoisomerase II by casein kinase II affects DNA-protein interaction. Journal of Molecular Biology, 243, 10-24.
11. 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. (1987) Purification of topoisomerase II from amsacrine-resistant P388 leukemia cells. Evidence for two forms of the enzyme. Journal of Biological Chemistry, 262, 16739-16747.
12. Estey, E., Adlakha, R.C., Hittelman, W.N. & Zwelling, L.A. (1987) Cell cycle stage dependent variations in drug-induced topoisomerase II mediated DNA cleavage and cytotoxicity. Biochemistry, 26, 4338-4344.
13. Fairman, R. & Brutlag, D.L. (1988) Expression of the Drosophila type II topoisomerase is developmentally regulated. Biochemistry, 27, 560-565.
14. Furukawa, M., Uchiumi, T., Nomoto, M., Takano, H., Morimoto, R.I., Naito, S., Kuwano, M. & Kohno, K. (1998) The role of an inverted CCAAT element in transcriptional activation of the human DNA topoisomerase IIα gene by heat shock. Journal of Biological Chemistry, 273, 10550-10555.
15. Gudkov, A.V., Zelnick, C.R., Kazarov, A.R., Thimmapaya, R., Suttle, D.P., Beck, W.T. & Roninson, I.B. (1993) Isolation of genetic suppressor elements, inducing resistance to topoisomerase II-interactive cytotoxic drugs, from human topoisomerase II cDNA. Proceedings of the National Academy of Sciences of the United States of America, 90, 3231-3235.
16. Harker, W.G., Slade, D.L., Parr, R.L., Feldhoff, P.W., Sullivan, D.M. & Holguin, M.H. (1995) Alterations in the topoisomerase IIα gene, messenger RNA, and subcellular protein distribution as well as reduced expression of the DNA topoisomerase IIβ enzyme in a mitoxantrone-resistant HL-60 human leukemia cell line. Cancer Research, 55, 1707-1716.
17. Heck, M.M.S. & Earnshaw, W.C. (1986) Topoisomerase II: a specific marker for cell proliferation. Journal of Cell Biology, 103, 2569-2581.
18. Heck, M.M.S., Hittelman, W.N. & Earnshaw, W.C. (1988) Differential expression of DNA topoisomerases I and II during the eukaryotic cell cycle. Proceedings of the National Academy of Sciences of the United States of America, 85, 1086-1090.
19. Hirano, T. & Mitchison, T.J. (1993) Topoisomerase II does not play a scaffolding role in the organization of mitotic chromosomes assembled in Xenopus eggs extracts. Journal of Cell Biology, 120, 601-612.
20. Hochhauser, D., Valkov, N.I., Gump, J.L., Wei, I., O'Hare, C., Hartley, J., Fan, J., Bertino, J.R., Banerjee, D. & Sullivan, D.M. (1999) Effects of wild-type p53 expression on the quantity and activity of topoisomerase IIα and β in various human cancer cell lines. Journal of Cellular Biochemistry, 75, 245-257.
21. Holden, J.A., Rolfson, D.H. & Wittwer, C.T. (1990) Human DNA topoisomerase II: evaluation of enzyme activity in normal and neoplastic tissues. Biochemistry, 29, 2127-2134.
22. Hsiang, Y.-H., Wu, H.-Y. & Liu, L.F. (1988) Proliferation-dependent regulation of DNA topoisomerase II in cultured human cells. Cancer Research, 48, 3230-3235.
23. Isaacs, R.J., Harris, A.L. & Hickson, I.D. (1996) Regulation of the human topoisomerase IIα gene promoter in confluence-arrested cells. Journal of Biological Chemistry, 271, 16741-16747.
24. Kaufmann, S.H., McLaughlin, S.J., Kastan, M.B., Liu, L.F., Karp, J.E. & Burke, P.J. (1991) Topoisomerase II levels during granulocytic maturation in vitro and in vivo. Cancer Research, 51, 3534-3543.
25. Liu, L.F. (1989) DNA topoisomerase poisons as antitumor drugs. Annual Review of Biochemistry, 58, 351-375.
26. Liu, L.F., Rowe, T.C., Yang, L., Tewey, K.M. & Chen, G.L. (1983) Cleavage of DNA by mammalian DNA topoisomerase II. Journal of Biological Chemistry, 258, 15365-15370.
27. Markovits, J., Pommier, Y., Kerrigan, D., Covey, J.M., Tilchen, E.J. & Kohn, K.W. (1987) Topoisomerase II-mediated DNA breaks and cytotoxicity in relation to cell proliferation and the cell cycle in NIH 3T3 fibroblasts and L1210 leukemia cells. Cancer Research, 47, 2050-2055.
28. Meyer, K.N., Kjeldsen, E., Straub, T., Knudsen, B.R., Hickson, I.D., Kikuchi, A., Kreipe, H. & Boege, F. (1997) Cell cycle-coupled relocation of types I and II topoisomerases and modulation of catalytic enzyme activities. Journal of Cell Biology, 136, 775-788.
29. Nakajima, T., Morita, K., Ohi, N., Arai, T., Nozaki, N., Kikuchi, A., Osaka, F., Yamao, F. & Oda, K. (1996) Degradation of topoisomerase IIα during adenovirus E1A-induced apoptosis is mediated by the activation of the ubiquitin proteolysis system. Journal of Biological Chemistry, 271, 24842-24849.
30. Nelson, E.M., Tewey, K.M. & Liu, L.F. (1984) Mechanism of antitumor drug action: poisoning of mammalian DNA topoisomerase II on DNA by 4′-(9-acridinylamino)-methanesulfon-m-anisidide. Proceedings of the National Academy of Sciences of the United States of America, 81, 1361-1365.
31. Nigg, E.A. (1997) Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature, 386, 779-787.
32. Qiu, J., Catapano, C.V. & Fernandes, D.J. (1996) Formation of topoisomerase IIα complexes with nascent DNA is related to VM-26-induced cytotoxicity. Biochemistry, 35, 16354-16360.
33. II protein kinase C. Molecular Pharmacology, 48, 798-805.
34. Robbie, M.A., Baguley, B.C., Denny, W.A., Gavin, J.B. & Wilson, W.R. (1988) Mechanism of resistance of noncycling mammalian cells to 4′-(9-acridinylamino) methanesulfon-m-anisidide: comparison of uptake, metabolism, and DNA breakage in log-and plateau-phase Chinese hamster fibroblast cell cultures. Cancer Research, 48, 310-319.
35. Schneider, E., Darkin, S.J., Robbie, M.A., Wilson, W.R. & Ralph, R.K. (1988) Mechanism of resistance of non-cycling mammalian cells to 4′-(9-acridinylamino) methanesulfon-m-anisidide: role of DNA topoisomerase II in log-and plateau-phase CHO cells. Biochimica et Biophysica Acta, 949, 264-272.
36. Sechler, J.L. & Schwarzbauer, J.E. (1998) Control of cell cycle progression by fibronectin matrix architecture. Journal of Biological Chemistry, 273, 25533-25536.
37. Smalheiser, N.R. (1996) Proteins in unexpected locations. Molecular Biology of the Cell, 7, 1003-1014.
38. Sugimoto, K., Yamada, K., Egashira, M., Yazaki, Y., Hirai, H., Kikuchi, A. & Oshimi, K. (1998) Temporal and spatial distribution of DNA topoisomerase II alters during proliferation, differentiation, and apoptosis in HL-60 cells. Blood, 91, 1407-1417.
39. Sullivan, D.M., Glisson, B.S., Hodges, P.K., Smallwood-Kentro, S. & Ross, W.E. (1986) Proliferation dependence of topoisomerase II mediated drug action. Biochemistry, 25, 2248-2256.
40. Sullivan, D.M., Latham, M.D. & Ross, W.E. (1987) Proliferation-dependent topoisomerase II content as a determinant of anti-neoplastic drug action in human, mouse, and Chinese hamster ovary cells. Cancer Research, 47, 3973-3979.
41. Sullivan, D.M., Latham, M.D., Rowe, T.C. & Ross, W.E. (1989) Purification and characterization of an altered topoisomerase II from a drug-resistant Chinese hamster ovary cell line. Biochemistry, 28, 5680-5687.
42. Sumner, A.T. (1996) The distribution of topoisomerase II on mammalian chromosomes. Chromosome Research, 4, 5-14.
43. Swedlow, J.R., Sedat, J.W. & Agard, D.A. (1993) Multiple chromosomal populations of topoisomerase II detected in vivo by time-lapse, three-dimensional wide-field microscopy. Cell, 73, 97-108.
44. Taagepera, S., McDonald, D., Loeb, J.E., Whitaker, L.L., McElroy, A.K., Wang, J.Y.J. & Hope, T.J. (1998) Nuclear-cytoplasmic shuttling of C-ABL tyrosine kinase. Proceedings of the National Academy of Sciences of the United States of America, 95, 7457-7462.
45. Tricoli, J.V., Sahai, B.M., McCormick, P.J., Jarlinski, S.J., Bertram, J.S. & Kowalski, D. (1985) DNA topoisomerase I and II activities during cell proliferation and the cell cycle in cultured mouse embryo fibroblast (C3H 10T/2) cells. Experimental Cell Research, 158, 1-14.
46. Turley, H., Comley, M., Houlbrook, S., Nozaki, N., Kikuchi, A., Hickson, I.D., Gatter, K. & Harris, A.L. (1997) The distribution and expression of the two isoforms of DNA topoisomerase II in normal and neoplastic human tissues. British Journal of Cancer, 75, 1340-1346.
47. Valkov, N.I. & Sullivan, D.M. (1997) Drug resistance to DNA topoisomerase I and II inhibitors in human leukemia, lymphoma, and multiple myeloma. Seminars in Hematology, 34, 48-62.
48. Wang, J.C. (1996) DNA topoisomerases. Annual Review of Biochemistry, 65, 635-692.
49. 1492 in the COOH-terminal region of topoisomerase Ha in human small cell lung cancer cells selected for resistance to etoposide results in an extranuclear enzyme localization. Cancer Research, 57, 4451-4454.
50. Whalen, A.M., McConnell, M. & Fisher, P.A. (1991) Developmental regulation of Drosophila DNA topoisomerase II. Journal of Cell Biology, 112, 203-213.
51. Woessner, R.D., Mattern, M.R., Mirabelli, C.K., Johnson, R.K. & Drake, F.H. (1991) Proliferation-and cell cycle-dependent differences in expression of the 170 kilodalton and 180 kilodalton forms of topoisomerase II in NIH-3T3 cells. Cell Growth and Differentiation, 2, 209-214.