Human topoisomerase IIα nuclear export is mediated by two CRM-1-dependent nuclear export signals

Journal of Cell Science

Volumn 117, Issue 14, 2004, Pages 3061-3071

  Turner, Joel G ^a   Engel, Roxanne ^a   Derderian, Jennifer A ^a   Jove, Richard ^a   Sullivan, Daniel M ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

CRM 1; Microinjection; Nuclear export signal (NES); Site directed mutagenesis; Topoisomerase II alpha (topo II )

Indexed keywords

AMINO ACID DERIVATIVE; DNA TOPOISOMERASE (ATP HYDROLYSING); EXPORTIN 1; FLUORESCEIN ISOTHIOCYANATE; LEPTOMYCIN B; PLASMID DNA; SIGNAL PEPTIDE; CELL RECEPTOR; DNA BINDING PROTEIN; DNA TOPOISOMERASE II ALPHA; EXPORTIN 1 PROTEIN; KARYOPHERIN; TUMOR ANTIGEN;

ARTICLE; CONJUGATE; CONTROLLED STUDY; CYTOPLASM; DIMERIZATION; ENZYME SUBUNIT; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HYDROPHOBICITY; MICROINJECTION; MYELOMA CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; ACTIVE TRANSPORT; AMINO ACID SEQUENCE; CELL NUCLEUS; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEAR LOCALIZATION SIGNAL; PHYSIOLOGY; TUMOR CELL LINE;

NES;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; ANTIGENS, NEOPLASM; CELL LINE, TUMOR; CELL NUCLEUS; CYTOPLASM; DNA TOPOISOMERASES, TYPE II, EUKARYOTIC; DNA-BINDING PROTEINS; HUMANS; KARYOPHERINS; MICROINJECTIONS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEAR LOCALIZATION SIGNALS; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 4344627104     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01147     Document Type: Article

References (63)

1. Ackerman, P., Glover, C. V. and Osheroff, N. (1985). Phosphorylation of DNA topoisomerase II by casein kinase II: modulation of eukaryotic topoisomerase II activity in vitro. Proc. Natl. Acad. Sci. USA 82, 3164-3168.
2. Arlucea, J., Andrade, R., Alonso, R. and Aréhaga, J. (1998). The nuclear basket of the nuclear pore complex is part of a higher-order filamentous network that is related to chromatin. J. Struct. Biol. 124, 51-58.
3. Bairoch, A. and Apweiler, R. (2000). The SWISS-PROT protein sequence database and its supplement TREMBL in 2000. Nucleic Acids Res. 28, 45-48.
4. Bjergbeck, L., Jensen, S., Westergaard, O. and Andersen, A. (1999). Using a biochemical approach to identify the primary dimerization regions in human DNA topoisomerase Hoc. J. Biol. Chem. 274, 26529-26536.
5. Buckwalter, C. A., Lin, A. H., Tanizawa, A., Pommier, Y. G., Cheng, Y. and Kaufmann, S. H. (1996). RNA synthesis inhibitors alter the subnuclear distribution of DNA topoisomerase I. Cancer Res. 56, 1674-168 1.
6. Burden, D. A., Kingma, P. S., Froelich-Ammon, S. J., Bjornsti, M. A., Patchan, M. W., Thompson, R. B. and Osheroff, N. (1996). Topoisomerase II: etoposide interactions direct the formation of drug-induced enzyme-DNA cleavage complexes. J. Biol. Chem. 271, 29238-29244.
7. Cokol, M., Nair, R. and Rost, B. (2000). Finding nuclear localization signals. EMBO Rep. 1, 411-415.
8. Cronshaw, J. M., Krutchinsky, A. N., Zhang, W., Chait, B. T. and Matunis, M. J. (2002). Proteomic analysis of the mammalian nuclear pore complex. J. Cell Biol. 5, 915-927.
9. Cowell, I. G., Willmore, E., Chalton, D., Marsh, K. L., Jazrawi, E., Fisher, L. M. and Austin, C. A. (1998). Nuclear distribution of human DNA topoisomerase IIβ: a nuclear targeting signal resides in the II 6-residue C-terminal tail. Exp. Cell Res. 243, 232-240.
10. Damelin, M., Silver, P. A. and Corbett, A. H. (2002). Nuclear protein transport. Methods Enzymol. 351, 587-607.
11. Danks, M. K., Garrett, K. E., Marion, R. C. and Whipple, D. O. (1996). Subcellular redistribution of DNA topoisomerase I in anaplastic astrocytoma cells treated with topotecan. Cancer Res. 56, 1664-1673.
12. Dreger, M. (2003). Subcellular proteomics. Mass Spectrom. 22, 27-56.
13. Engel, R., Valkov, N. I. and Sullivan, D. M. (2003). In vitro and in vivo drug resistance to DNA topoisomerase I and II inhibitors. Recent Research Developments in Cellular Biochemistry 1, 207-232.
14. Engel, R., Valkov, N. L, Gump, J. L., Hazlehurst, L., Dalton, W. S. and Sullivan, D. M. (2004). The cytoplasmic trafficking of DNA topoisomerase IIα correlates with etoposide resistance in human myeloma cells. Exp. Cell Res. 295, 421-431.
15. Ernst, A. L, Soltermann, A., Sigrist, J. A., Widmer, L., Gasser, S. M. and Stahel, R. A. (2000). Ectopic expression of human topoisomerase IIα fragments and etoposide resistance in mammalian cells. Int. J. Cancer 88, 99-107.
16. Fass, D., Bogden, C. E. and Berger, J. M. (1999). Quaternary changes in topoisomerase II may direct orthogonal movements of two DNA strand. Nat. Struct. Biol. 6, 322-326.
17. Fischer, U., Huber, J., Boelens, W. C., Mattaj, I. W. and Luhrmann, R. (1995). The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell 82, 463-473.
18. Fornerod, M., Ohno, M., Yoshida, M. and Mattaj, I. W. (1997). CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90, 1051-1060.
19. Frere, V., Sourgen, F., Monnot, M., Troalen, F. and Fermandjian, S. (1995). A peptide fragment of human DNA topoisomerase II alpha forms a stable coiled-coil structure in solution. J. Biol. Chem. 270, 17502-17507.
20. Frere-Gallois, V., Krebs, D., Scala, D., Troalen, F. and Fermandjian, S. (1997). Peptide fragments of DNA topoisomerase II with helix-forming and coiled-coil-forming properties act as inhibitors of the enzyme forms a stable coiled-coil structure in solution. Eur J. Biochem. 249, 142-148.
21. Fridell, R. A., Fisher, U., Luhrmann, R., Meyer, B. E., Meinkoth, J. L., Malim, M. H. and Cullen, B. R. (1996). Amphibian transcription factor IIIA proteins contain a sequence element functionally equivalent to the nuclear export signal of human immunodeficiency virus type 1 rev. Proc. Mal. Acad. Sci. USA 93, 2936-2940.
22. Fukuda, M., Gotoh, L, Gotoh, Y. and Nishida, E. (1996). Cytoplasmic localization of mitogen-activated protein kinase kinase directed by its NH2-terminal, leucine-rich short amino acid sequence, which acts as a nuclear export signal. J. Biol. Chem. 271, 20024-20028.
23. Fukuda, M., Asano S., Nakamura, T., Adachi, M., Yoshida, M., Yanagida, M. and Nisbida, E. (1997). CRMI is responsible for intracellular transport mediated by the nuclear export signal. Nature 390, 308-311.
24. Görlich, D. (1998). Transport into and out of the cell nucleus. EMBO J. 17, 2721-2727.
25. Gottardi, C. J., Arpin, M., Fanning, A. S. and Louvard, D. (1996). The junction-associated protein, zonula occludens-1, localizes to the nucleus before the maturation and during the remodeling of cell-cell contacts. Proc. Natl. Acad. Sci. USA 93, 10779-10784.
26. Hamamoto, T., Gunji, S., Tsuji, H. and Beppu, T. (1983a). Leptomycins A and B, new antifungal antibiotics. I. Taxonomy of the producing strain and their fermentation, purification and characterization. J. Antibiot. 36, 639-645.
27. Hamamoto, T., Seto, H. and Beppu, T. (1983b). Leptomycins A and B, new antifungal antibiotics. II. Structure elucidation. J Antibiot. 36, 646-650.
28. Hamamoto, T., Uozumi, T. and Beppu, T. (1985). Leptomycins A and B, new antifungal antibiotics. III. Mode of action of leptomycin B on Schizosaccharomyces pombe. J. Antibiot. 38, 1573-1580.
29. Harker, W. G., Slade, D. L., Parr, R. L. and Holguin, M. H. (1995). Selective use of an alternative stop codon and polyadenylation signal within intron sequences leads to a truncated topoisomerase II alpha messenger RNA and protein in human HL-60 leukemia cells selected for resistance to mitoxantrone. Cancer Res. 55, 4962-4971.
30. Hazelhurst, L. A., Valkov, N. I., Wisner, L., Storey, J. A., Boulware, D., Sullivan, D. M. and Dalton, W. S. (2001). Reduction in drug-induced DNA double-strand breaks associated with beta1 integrin-mediated adhesion correlates with drug resistance in U937 cells. Blood 98, 1897-1903.
31. Kalesse, M., Christmann, M., Bhatt, U., Quitschalle, M., Claus, E., Saeed, A., Burzlaff, A., Kasper, C., Haustedt, L. O., Hofer, E. et al. (2001). The chemistry and biology of ratjadone. Chembiochem. 9, 709-714.
32. Kang, M. R. and Chung, I. K. (2002). Down-regulation of DNA topoisomerase II alpha in human colorectal carcinoma cells resistant to a protoberberine alkaloid, berberrubine. Mol. Pharmacol. 4, 879-884.
33. Kau, T. R. and Silver, P. A. (2003). Nuclear transport as a target for cell growth. Drug Discov. Today 8, 78-85.
34. Koster, M., Lykke-Andersen, S., Elnakady, Y. A., Gerth, K., Washausen, P., Hoffe, G., Sasse, F., Kjems, J. and Hauser, H. (2003). Ratjadones inhibit nuclear export by blocking CRM1/exportin 1. Exp. Cell Res. 286, 321-331.
35. La Cour, T., Gupta, R., Ropacki, K., Skriver, K., Poulsen, F. M. and Burnak, S. (2003). NESbase version 1.0: a database of nuclear export signals. Nucleic Acids Res. 31, 393-396.
36. Low, R. L., Orton, S. and Friedman, D. B. (2003). A truncated form of DNA topoisomerase IIβ associates with the mtDNA genome in mammalian mitochondria. Ear J. Biochem. 270, 4173-4186.
37. Mirski, S. E., Gerlach, J. H. and Cole, S. P. (1999). Sequence determinants of nuclear localization in the alpha and beta isoforms of human topoisomerase II. Exp. Cell Res. 251, 329-339.
38. Mirski, S. E., Bielawski, J. C. and Cole, S. P. (2003). Identification of functional nuclear export sequences in human topoisomerase II alpha and beta. Biochem. Biophys. Res. Commun. 306, 905-911.
39. Mo, Y-Y., Wang, C. and Beek, W. T. (2000). A novel nuclear localization signal in human DNA topoisomerase I. J. Biol. Chem. 275, 41107-41113.
40. Nishi, K., Yoshida, M., Fujiwara, D., Nishikawa, M., Horinouchi, S. and Beppu, T. (1994). Leptomycin B targets a regulatory cascade of crm1, a fission yeast nuclear protein, involved in control of higher order chromosome structure and gene expression. J. Biol. Chem. 269, 6320-6324.
41. Nix, D. A. and Beckerle, M. C. (1997). Nuclear-cytoplasmic shuttling of the focal contact protein, zyxin: a potential mechanism for communication between sites of cell adhesion and the nucleus. J. Cell Biol. 138, 1139-1147.
42. Oloumi, A., MacPhail, S. H., Johnston, P. J., Banath, J. B. and Olive, P. L. (2000). Changes in subcellular distribution of topoisomerase II alpha correlate with etoposide resistance in multicell spheroids and xenograft tumors. Cancer Res. 60, 5747-5753.
43. Ossareh-Nazari, B., Bachelerie, E. and Dargemont, C. (1997). Evidence for a role of CRM1 in signal-mediated nuclear protein export. Science 278, 141-144.
44. Ribbeck, K., Lipowsky, G., Kent, H. M., Stewart, M. and Görlich, D. (1998). NTF2 mediates nuclear import of Ran. EMBO J. 17, 6587-6598.
45. Roth, J., Dobbelstein, M., Freedman, D. A., Shenk, T. and Levine, A. J. (1998). Nucleo-cytoplasmic shuttling of the hdm2 oncoprotein regulates the levels of the p53 protein via a pathway used by the human immunodeficiency virus rev protein. EMBO J. 17, 554-564.
46. Rout, M. P., Aitchison, J. D., Suprapto, A., Hjertaas, K., Zhao, Y., Chait, B. T. (2000). The yeast nuclear pore complex: composition, architecture, and transport mechanism. J. Cell Biol. 4, 635-651.
47. Siomi, M. C., Eder, P. S., Kataoka, N., Wan, L., Liu, Q. and Dreyfuss, G. (1997). Transportin-mediated nuclear import of heterogeneous nuclear RNP proteins. J. Cell Biol. 138, 1181-1192.
48. Sodek, J., Hodges, R. S., Smillie, L. B. and Jurasek, L. (1972). Amino-acid sequence of rabbit skeletal tropomyosin and its coiled-coil structure. Proc. Natl. Acad. Sci. USA 69, 3800-3804.
49. Stommel, J. M., Marchenko, N. D., Jimenez, G. S., Moll, U. M., Hope, T. J. and Wahl, G. M. (1999). A leucine-rich nuclear export signal in the p53 tetramerization domain: regulation of subcellular localization and p53 activity by NES masking. EMBO J. 18, 1660-1672.
50. Sullivan, D. M., Latham, M. D. and Ross, W. E. (1987). Proliferation-dependent topoisomerase II content as a determinant of antineoplastic drug action in human, mouse, and Chinese hamster ovary cells. Cancer Res. 47, 3973-3979.
51. Taagepera, S., McDonald, D., Loeb, J. E., Whitaker, L. L., McElroy, A. M., Wang, J. Y. and Hope, T. J. (1998). Nuclear-cytoplasmic shuttling of C-ABL tyrosine kinase. Proc. Natl. Acad. Sci. USA 95, 7457-7462.
52. Valkov, N. I., Gump, J. L. and Sullivan, D. M. (1997). Quantitative immunofluorescence and immunoclectron microscopy of the topoisomerase II alpha associated with nuclear matrices from wild-type and drug-resistant Chinese hamster ovary cell lines. J. Cell Biochem. 67, 112-130.
53. Valkov, N. I., Gump, J. L., Engel, R. and Sullivan, D. M. (2000). Cell density-dependent VP-16 sensitivity of leukaemic cells is accompanied by the translocation of topoisomerase II alpha from the nucleus to the cytoplasm. Br. J. Haematol. 108, 331-345.
54. Van den Hoff, M. J., Moorman, A. E. and Lamers, W. H. (1992). Electroporation in 'intracellular' buffer increases cell survival. Nucleic Acids Res. 20, 2902.
55. Wada, A., Fukuda, M., Mishima, M. and Nishida, E. (1998). Nuclear export of actin: a novel mechanism regulating the subcellular localization of a major cytoskeletal protein. EMBO J. 17, 1635-1641.
56. Wang, J. C. (2002). Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell. Biol. 3, 430-440.
57. Watt, P. M. and Hickson, I. D. (1994). Structure and function of type II DNA topoisomerases. Biochem. J. 303, 681-695.
58. Weis, K. (2003). Regulating access to the genome: nucleocytoplasmic transport throughout the cell cycle. Cell 112, 441-451.
59. Wen, W., Meinkoth, J. L., Tsien, R. Y. and Taylor, S. S. (1995). Identification of a signal for rapid export of proteins from the nucleus. Cell 82, 463-473.
60. Wessel, I., Jensen, P. B., Falck, J., Mirski, S. E., Cole, S. P. and Sehested, M. (1997). Loss of amino acids 1490Lys-Ser-Lys1492 in the COOH-terminal region of topoisomerase II alpha in human small cell lung cancer cells selected for resistance to etoposide results in an extranuclear enzyme localization. Cancer Res. 57, 4451-4454.
61. Wu, C. H., Huang, H., Arminski, L., Castro-Alvear, J., Chen, Y., Hu, Z. Z., Ledley, R. S., Lewis, K. C., Mewes, H. W., Orcutt, B. C., et al. (2002). The Protein Information Resource: an integrated public resource of functional annotation of proteins. Nucleic Acids Res. 30, 35-37.
62. Yoneda, Y., Hieda, M., Nagoshi, E. and Miyamoto, Y. (1999). Nucleocytoplasmic protein transport and recycling of Ran. Cell Struct. Funct. 24, 425-433.
63. Zolotokhin, A. S. and Felber, B. K. (1997). Mutations in the nuclear export signal of human ran-binding protein RanBP1 block the Rev-mediated posttranscriptional regulation of human immunodeficiency virus type 1. J. Biol. Chem. 273, 11356-11360.