Sequence determinants of nuclear localization in the α and β isoforms of human topoisomerase II

Experimental Cell Research

Volumn 251, Issue 2, 1999, Pages 329-339

  Mirski, Shelagh E L ^a   Gerlach, James H ^a   Cole, Susan P C ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

Drug resistance; Nuclear localization signal; Topoisomerase II

Indexed keywords

ANTINEOPLASTIC AGENT; BETA GALACTOSIDASE; DNA TOPOISOMERASE (ATP HYDROLYSING); GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; ISOENZYME;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CANCER CHEMOTHERAPY; CELL STRAIN COS1; COMPUTER PROGRAM; CONTROLLED STUDY; DRUG RESISTANCE; ENZYME LOCALIZATION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; REPORTER GENE; SEQUENCE HOMOLOGY;

ANIMALIA;

EID: 0033568621     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.1999.4587     Document Type: Article

References (49)

1. Mirski S. E. L., Cole S. P. C. Multidrug resistance in small cell lung cancer. Bernal S. D. Drug Resistance in Oncology. 1997;Dekker, New York.
2. Austin C. A., Marsh K. L. Eukaryotic DNA topoisomerase IIβ BioEssays. 20:1998;215-226.
3. Osheroff N., Corbett A. H., Robinson M. J. Mechanism of action of topoisomerase II-targeted antineoplastic drugs. Liu L. F. DNA Topoisomerases: Topoisomerase-Targeting Drugs. 1994;Academic Press, San Diego.
4. Chen A. Y., Liu L. F. DNA topoisomerases: Essential enzymes and lethal targets. Annu. Rev. Pharmacol. Toxicol. 34:1994;191-218.
5. Jenkins J. R., Ayton P., Jones T., Davies S. L., Simmons D. L., Harris A. L., Sheer D., Hickson I. D. Isolation of cDNA clones encoding the β isozyme of human DNA topoisomerase II and localisation of the gene to chromosome 3p24. Nucleic Acids Res. 20:1992;5587-5592.
6. Drake F. H., Hofmann G. A., Bartus H. F., Mattern M. R., Crooke S. T., Mirabelli C. K. Biochemical and pharmacological properties of p170 and p180 forms of topoisomerase II. Biochemistry. 28:1989;8154-8160.
7. Brown G. A., McPherson J. P., Gu L., Hedley D. W., Toso R., Deuchars K. L., Freedman M. H., Goldenberg G. J. Relationship of DNA topoisomerase IIα and β expression to cytotoxicity of antineoplastic agents in human acute lymphoblastic leukemia cell lines. Cancer Res. 55:1995;78-82.
8. Perrin D., van Hille B., Hill B. T. Differential sensitivities of recombinant human topoisomerase IIα and β to various classes of topoisomerase II-interacting agents. Biochem. Pharmacol. 56:1998;503-507.
9. Cornarotti M., Tinelli S., Willmore E., Zunino F., Fisher L. M., Austin C. A., Capranico G. Drug sensitivity and sequence specificity of human recombinant DNA topoisomerase IIα (p170) and IIβ (p180). Mol. Pharmacol. 50:1996;1463-1471.
10. Lang A. J., Mirski S. E. L., Cummings H. J., Yu Q., Gerlach J. H., Cole S. P. C. Structural organization of the human TOP2A and TOP2B genes. Gene. 221:1998;255-266.
11. 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. 88:1991;7654-7658.
12. r 170,000 isozyme of DNA topoisomerase II in human tumor cells. Cancer Res. 53:1993;1373-1379.
13. 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. 51:1991;4729-4731.
14. Lee M.-S., 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 topoisomerase II. J. Mol. Biol. 223:1992;837-843.
15. Kohno K., Danks M. K., Matsuda T., Nitiss J. L., Kuwano M., Beck W. T. A novel mutation of DNA topoisomerase IIα gene in an etoposide-resistant human cancer cell line. Cell. Pharmacol. 2:1995;87-90.
16. Patel S., Fisher L. M. Novel selection and genetic characterisation of an etoposide-resistant human leukaemic CCRF-CEM cell line. Br. J. Cancer. 67:1993;456-463.
17. Kubo A., Yoshikawa A., Hirashima T., Masuda N., Takada M., Takahara J., Fukuoka M., Nakagawa K. Point mutations of the topoisomerase IIα gene in patients with small cell lung cancer treated with etoposide. Cancer Res. 56:1996;1232-1236.
18. 1492 in the COOH-terminal region of topoisomerase IIα in human small cell lung cancer cells selected for resistance to etoposide results in an extranuclear enzyme localization. Cancer Res. 57:1997;4451-4454.
19. Yu Q., Mirski S. E. L., Sparks K. E., Cole S. P. C. Two COOH-terminal truncated cytoplasmic mutant forms of topoisomerase IIα in a VP-16-selected lung cancer cell line result from partial gene deletion and alternative splicing. Biochemistry. 36:1997;5868-5877.
20. r 160,000 topoisomerase IIα is associated with the loss of putative bipartite nuclear localization signals in a drug resistant human lung cancer cell line. Cancer Res. 55:1995;2129-2134.
21. Harker W. G., Slade D. L., Parr R. L., Holguin M. H. Selective use of an alternative stop codon and polyadenylation signal within intron sequences leads to a truncated topoisomerase IIα messenger RNA and protein in human HL-60 leukemia cells selected for resistance to mitoxantrone. Cancer Res. 55:1995;4962-4971.
22. Harker W. G., Slade D. L., Parr R. L., Feldhoff P. W., Sullivan D. M., Holguin M. H. 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 Res. 55:1995;1707-1716.
23. Dingwall C., Laskey R. A. Nuclear targeting sequences - A consensus. Trends Biochem. Sci. 16:1991;478-481.
24. Mirski S. E. L., Gerlach J. H., Cummings H. J., Zirngibl R., Greer P. A., Cole S. P. C. Bipartite nuclear localization signals in the C-terminus of human topoisomerase IIα Exp. Cell Res. 237:1997;452-455.
25. Zhu X., Chang K.-H., He D., Mancini M. A., Brinkley W. R., Lee W.-H. The C terminus of mitosin is essential for its nuclear localization, centromere/kinetochore targeting, and dimerization. J. Biol. Chem. 270:1995;19545-19550.
26. Romanelli M. G., Wighardt F., Biamonti G., Riva S., Morandi C. Sequence determinants for hnRNP I protein nuclear localization. Exp. Cell Res. 235:1997;300-304.
27. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:1994;4673-4680.
28. Tsai-Pflugfelder M., Liu L. F., Liu A. A., Tewey K. M., Whang-Peng J., Knutsen T., Huebner K., Croce C. M., Wang J. C. Cloning and sequencing of cDNA encoding human DNA topoisomerase II and localization of the gene to chromosome region 17q21-22. Proc. Natl. Acad. Sci. USA. 85:1988;7177-7181.
29. Davies S. L., Jenkins J. R., Hickson I. D. Human cells express two differentially spliced forms of topoisomerase IIβ mRNA. Nucleic Acids Res. 21:1993;3719-3723.
30. Crenshaw D. G., Hsieh T.-s. Function of the hydrophilic carboxyl terminus of type II DNA topoisomerase from Drosophila melanogaster. II. In vivo studies. J. Biol. Chem. 268:1993;21335-21343.
31. Jensen S., Andersen A. H., Kjeldsen E., Biersack H., Olsen E. H. N., Andersen T. B., Westergaard O., Jakobsen B. K. Analysis of functional domain organization in DNA topoisomerase II from humans and Saccharomyces cerevisiae. Mol. Cell. Biol. 16:1996;3866-3877.
32. Shiozaki K., Yanagida M. Functional dissection of the phosphorylated termini of fission yeast DNA topoisomerase II. J. Cell Biol. 119:1992;1023-1036.
33. Adachi N., Miyaike M., Kato S., Kanamaru R., Koyama H., Kikuchi A. Cellular distribution of mammalian DNA topoisomerase II is determined by its catalytically dispensable C-terminal domain. Nucleic Acids Res. 25:1997;3135-3142.
34. Petrov P., Drake F. H., Loranger A., Huang W., Hancock R. Localization of DNA topoisomerase II in Chinese hamster fibroblasts by confocal and electron microscopy. Exp. Cell Res. 204:1993;73-81.
35. Negri C., Scovassi A. I., Braghetti A., Guano F., Ricotti G. B. C. A. DNA topoisomerase II β: Stability and distribution in different animal cells in comparison to DNA topoisomerase I and II α Exp. Cell Res. 206:1993;128-133.
36. Meyer K. N., Kjeldsen E., Straub T., Knudsen B. R., Hickson I. D., Kikuchi A., Kreipe H., Boege F. Cell cycle-coupled relocation of types I and II topoisomerases and modulation of catalytic enzyme activities. J. Cell Biol. 136:1997;775-788.
37. Earnshaw W. C., Halligan B., Cooke C. A., Heck M. M. S., Liu L. F. Topoisomerase II is a structural component of mitotic chromosome scaffolds. J. Cell Biol. 100:1985;1706-1715.
38. Boege F., Kjeldsen E., Gieseler F., Alsner J., Biersack H. A drug-resistant variant of topoisomerase IIα in human HL-60 cells exhibits alterations in catalytic pH optimum, DNA binding and sub-nuclear distribution. Eur. J. Biochem. 218:1993;575-584.
39. Turley H., Comley M., Houlbrook S., Nozaki N., Kikuchi A., Hickson I. D., Gatter K., Harris A. L. The distribution and expression of the two isoforms of DNA topoisomerase II in normal and neoplastic human tissues. Br. J. Cancer. 75:1997;1340-1346.
40. Cowell I. G., Willmore E., Chalton D., Marsh K. L., Jazrawi E., Fisher L. M., Austin C. A. Nuclear distribution of human DNA topoisomerase beta: A nuclear targeting signal resides in the 116-residue C-terminal tail. Exp. Cell Res. 243:1998;232-240.
41. Danks M. K., Qiu J., Catapano C. V., Schmidt C. A., Beck W. T., Fernandes D. J. Subcellular distribution of the α and β topoisomerase II-DNA complexes stabilized by VM-26. Biochem. Pharmacol. 48:1994;1785-1795.
42. Feldhoff P. W., Mirski S. E. L., Cole S. P. C., Sullivan D. M. M. Altered subcellular distribution of topoisomerase IIα in a drug resistant human small cell lung cancer cell line. Cancer Res. 54:1994;756-762.
43. Harker W. G., Slade D. L., Drake F. H., Parr R. L. Mitoxantrone resistance in HL-60 leukemia cells: Reduced nuclear topoisomerase II catalytic activity and drug-induced DNA cleavage in association with reduced expression of the topoisomerase II β isoform. Biochemistry. 30:1991;9953-9961.
44. Jans D. A. The regulation of protein transport to the nucleus by phosphorylation. Biochem. J. 311:1995;705-716.
45. Ohta Y., Nishida E., Sakai H., Miyamoto E. Dephosphorylation of cofilin accompanies heat shock-induced nuclear accumulation of cofilin. J. Biol. Chem. 264:1989;16143-16148.
46. c-rel. Mol. Cell. Biol. 11:1991;5867-5877.
47. Norris J. L., Manley J. L. Selective nuclear transport of the Drosophila morphogen dorsal can be established by a signaling pathway involving the transmembrane protein Toll and protein kinase A. Genes Dev. 6:1992;1654-1667.
48. Hickson I. D., Davies S. L., Isaacs R. J., Redwood C., Sandri M. I., Wells N. J. Cell cycle phase-specific regulation of topoisomerase II in mammalian cells. Anti-Cancer Drugs. 7:1996;19-25.
49. Kimura K., Nozaki N., Enomoto T., Tanaka M., Kikuchi A. Analysis of M phase-specific phosphorylation of DNA topoisomerase II. J. Biol. Chem. 271:1996;21439-21445.