Molecular cloning and characterization of the human topoisomerase IIα and IIβ genes: Evidence for isoform evolution through gene duplication

Biochimica et Biophysica Acta - Gene Structure and Expression

Volumn 1444, Issue 3, 1999, Pages 395-406

  Sng, Jen Hwei ^a   Heaton, Victoria J ^a   Bell, Margaret ^b   Maini, Pankaj ^a   Austin, Caroline A ^b   Fisher, L Mark ^c  

^a ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c NONE

Author keywords

Enzyme isoform; Evolution; Exon intron structure; Genomic DNA; Human topoisomerase II

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING);

ARTICLE; DNA SEQUENCE; EXON; GENE DUPLICATION; GENE REARRANGEMENT; GENE STRUCTURE; HUMAN; INTRON; MOLECULAR CLONING; MOLECULAR EVOLUTION; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ANTIGENS, NEOPLASM; CHROMOSOME MAPPING; CLONING, MOLECULAR; CONSERVED SEQUENCE; COSMIDS; DNA TOPOISOMERASES, TYPE II; DNA TOPOISOMERASES, TYPE II, EUKARYOTIC; DNA-BINDING PROTEINS; EVOLUTION, MOLECULAR; EXONS; GENE DUPLICATION; HUMANS; INTRONS; ISOENZYMES; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT;

EID: 0033583094     PISSN: 01674781     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0167-4781(99)00020-2     Document Type: Article

References (60)

1. C.A. Austin, L.M. Fisher, DNA topoisomerases: enzymes that change the shape of DNA, Sci. Prog. 74 (1990) 147-161.
2. P.M. Watt, I.D. Hickson, Structure and function of type II DNA topoisomerases, Biochem. J. 303 (1994) 681-685.
3. J.C. Wang, DNA topoisomerases, Annu. Rev. Biochem. 65 (1996) 635-692.
4. J.M. Berger, S.J. Gamblin, S.C. Harrison, J.C. Wang, Structure and mechanism of DNA topoisomerase II, Nature 379 (1996) 225-232.
5. K.G. Miller, L.F. Liu, P.T. Englund, A homogeneous type II DNA topoisomerase from HeLa cell nuclei, J. Biol. Chem. 256 (1981) 9334-9339.
6. F.H. Drake, J.P. Zimmerman, F.L. McCabe, H.F. Bartus, S.R. Per, D.M. Sullivan, W.E. Ross, M.R. Mattern, R.K. Johnson, S.T. Crooke, C.K. Mirabelli, Purification of topoisomerase II from amsacrine-resistant P388 leukemia cells: Evidence for two forms of the enzyme, J. Biol. Chem. 262 (1997) 16739-16747.
7. F.H. Drake, G.A. Hofman, H.F. Bartus, M.R. Mattern, S.T. Crooke, C.K. Mirabelli, Biochemical and pharmacological properties of p170 and p180 forms of topoisomerase II, Biochemistry 28 (1989) 154-160.
8. T.D.Y. Chung, F.H. Drake, K.B. Tan, S.R. Per, S.T. Crooke, C.K. Mirabelli, Characterisation and immunological identification of cDNA clones encoding two human DNA topoisomerase II isozymes, Proc. Natl. Acad. Sci. USA 86 (1989) 9431-9435.
9. C.A. Austin, L.M. Fisher, Isolation and characterisation of a human cDNA clone encoding a novel DNA topoisomerase II homologue from HeLa cells, FEBS Lett. 266 (1990) 115-117.
10. C.A. Austin, J.-H. Sng, S. Patel, L.M. Fisher, Novel HeLa topoisomerase II is the IIβ isoform: complete coding sequence and homology with other type II topoisomerases, Biochim. Biophys. Acta 1172 (1993) 283-291.
11. J.R. Jenkins, P. Ayton, T. Jones, S.L. Davies, D.L. Simmons, A.L. Harris, D. Sheer, I.D. Hickson, Isolation of cDNA clones encoding the β isozyme of human DNA topoisomerase II and localization of the gene to chromosome 3p24, Nucleic Acids Res. 20 (1992) 5587-5592.
12. C.A. Austin, K.L. Marsh, Eukaryotic DNA topoisomerase IIβ, BioEssays 20 (1998) 215-226.
13. M. Tsai-Pflugfelder, L.F. Liu, A.A. Liu, K.M. Tewey, J. Whang-Peng, T. Knutsen, K. Huebner, C.M. Croce, J.C. Wang, 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.
14. K.B. Tan, T.E. Dorman, K.M. Falls, T.D. Chung, C.K. Mirabelli, S.T. Crooke, J. Mao, Topoisomerase IIα and topoisomerase IIβ genes: characterization and mapping to human chromosomes 17 and 3, respectively, Cancer Res. 52 (1992) 231-234.
15. S.L. Davies, J.R. Jenkins, I.D. Hickson, Human cells express two differentially spliced forms of topoisomerase IIβ RNA, Nucleic Acids Res. 21 (1993) 3719-3723.
16. J. Coutts, J.A. Plumb, R. Brown, W.N. Keith, Expression of topoisomerase II alpha and beta in an adenocarcinoma cell line carrying amplified topoisomerase II alpha and retinoic acid receptor alpha genes, Br. J. Cancer 68 (1993) 793-800.
17. W.N. Keith, F. Douglas, G.C Wishart, H.M. McCallum, W.D. George, S.B. Kaye, R. Brown, Co-amplification or erbB2, topoisomerase IIα and the retinoic acid receptor α genes in breast cancer and allelic loss at topoisomerase I on chromosome 20, Eur. J. Cancer 29A (1993) 1469-1473.
18. R.A. Wasserman, C.A. Austin, L.M. Fisher, J.C. Wang, Use of yeast in the study of anticancer drugs targeting DNA topoisomerases: expression of a functional recombinant human DNA topoisomerase IIα in yeast, Cancer Res. 53 (1993) 3591-3596.
19. S. Jensen, C.S. Redwood, J.R. Jenkins, A.H. Andersen, I.D. Hickson, Human DNA topoisomerase IIα and IIβ can functionally substitute for yeast TOP2 in chromosome segregation and recombination, Mol. Gen. Genet. 252 (1996) 79-86.
20. E.L. Meczes, K.L. Marsh, L.M. Fisher, M.P. Rogers, C.A. Austin, Complementation of temperature-sensitive topoisomerase II mutations in S. cerevisiae by a human TOP2β construct allows the study of topoisomerase IIβ inhibitors in yeast, Cancer Chemother. Pharmacol. 39 (1997) 367-375.
21. M.M.S. Heck, W.N. Hittleman, W.C. Earnshaw, Differential expression of DNA topoisomerase I and II during the eukaryotic cell cycle, Proc. Natl. Acad. Sci. USA 85 (1988) 1086-1090.
22. R.D. Woessner, M.R. Mattern, C.K. Mirabelli, R.K. Johnson, F.H. Drake, 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 Differ. 2 (1991) 209-214.
23. G. Capranico, S. Tinelli, C.A. Austin, L.M. Fisher, F. Zunino, Different patterns of gene expression of topoisomerase II isoforms in differentiated tissues during murine development, Biochim. Biophys. Acta 1132 (1992) 43-48.
24. N. Zini, A.M. Martelli, P. Sabatelli, S. Santi, C. Negri, G.C.B.A. Ricotti, N.M. Maraldi, The 180-kDa isoform of topoisomerase II is localized in the nucleolus and belongs to the structural elements of the nucleolar remnant, Exp. Cell Res. 200 (1992) 460-466.
25. N. Chaly, D.L. Brown, Is DNA topoisomerase IIβ a nucleolar protein?, J. Cell. Biochem. 63 (1996) 162-173.
26. I.G. Cowell, E. Willmore, D. Chalton, K.L. Marsh, E. Jazrawi, L.M. Fisher, C.A. Austin, Nuclear distribution of human DNA topoisomerase IIβ: a nuclear targeting signal resides in the 116-residue C-terminal tail, Exp. Cell Res. 243 (1998) 232-240.
27. J. Qui, C. Catapano, D.J. Fernandes, Formation of topoisomerase IIα complexes with nascent DNA is related to VM-26-induced cytotoxicity, Biochemistry 35 (1996) 16354-16360.
28. L.F. Liu, DNA topoisomerase poisons as antitumor drugs, Annu. Rev. Biochem. 58 (1989) 351-375.
29. K.L. Marsh, E. Willmore, S. Tinelli, M. Cornarotti, E.L. Meczes, G. Capranico, L.M. Fisher, C.A. Austin, Amsacrine-promoted DNA cleavage site determinants for the two human DNA topoisomerase II isoforms, α and β, Biochem. Pharmacol. 52 (1996) 1675-1685.
30. M. Cornarotti, S. Tinelli, E. Willmore, F. Zunino, L.M. Fisher, C.A. Austin, G. Capranico, Drug sensitivity and sequence specificity of human recombinant DNA topoisomerase IIα (p170) and IIβ (p180), Mol. Pharmacol. 50 (1996) 1463-1471.
31. S. Dereuddre, S. Frey, C. Delaporte, A. Jacquemin-Sablon, Cloning and characterisation of full length cDNAs coding for the topoisomerase IIβ from Chinese hamster lung cells sensitive and resistant to 9-OH-ellipticine, Biochim. Biophys. Acta 1264 (1995) 178-182.
32. S. Dereuddre, C. Delaporte, A. Jacquemin-Sablon, Role of topoisomerase IIβ in the resistance of 9-OH-ellipticine-resistant Chinese hamster fibroblasts to topoisomerase II inhibitors, Cancer Res. 57 (1997) 4301-4308.
33. W.G. Harker, D.L. Slade, R.L. Parr, P.W. Feldhoff, D.M. Sullivan, M.H. Holguin, Alterations in the DNA topoisomerase IIα gene, messenger RNA, and subcellular protein distribution as well as reduced expression of DNA topoisomerase IIβ enzyme in a mitoxantrone-resistant HL-60 human leukemia cell line, Cancer Res. 55 (1995) 1707-1716.
34. S. Withof, W.N. Keith, A.J. Knol, J.C. Coutts, S.F. Hoare, N.H. Mulder, E.B. de Vries, Selection of a subpopulation with fewer DNA topoisomerase II alpha gene copies in a doxorubicin-resistant cell line panel, Br. J. Cancer 74 (1996) 502-507.
35. J.P. McPherson, G.A. Brown, G.J. Goldenberg, Characterization of a DNA topoisomerase IIα gene rearrangement in adriamycin-resistant P388 leukaemia: expression of a fusion messenger RNA transcript encoding topoisomerase IIα and the retinoic acid receptor α locus, Cancer Res. 53 (1993) 5885-5889.
36. P.W. Feldhof, S.E.L. Mirski, S.P.C. Cole, D.M. Sullivan, Altered subcellular distribution of topoisomerase IIα in a drug-resistant human small cell lung cancer cell line, Cancer Res. 54 (1994) 756-762.
37. r 160,000 topoisomerase IIα is associated with loss of putative bipartite nuclear localization signals in a drug-resistant human lung cancer cell line, Cancer Res. 55 (1995) 2129-2134.
38. L. Wessel, P.B. Jensen, J. Falck, S.E.L. Mirski, S.P.C. Cole, M. Sehested, Loss of amino acids (1490)Lys-Ser-Lys(1492) in the COOH-terminal region of topoisomerase II alpha in human small cell lung cancer cell lines selected for resistance to etoposide results in an extranuclear localization, Cancer Res. 57 (1997) 4451-4454.
39. Q. Yu, S.E.L. Mirski, K.E. Sparks, S.P.C. Cole, Two COOH-terminal truncated cytoplasmic 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.
40. E. Willmore, A.J. Frank, K. Padget, M.J. Tilby, C.A. Austin, Etoposide targets topoisomerase IIα and IIβ in leukaemic cells: isoform-specific cleavable complexes visualised and quantified by a novel immunofluorescence technique, Mol. Pharmacol. 53 (1998) 78-85.
41. D. Hochhauser, C.A. Stanway, A.L. Harris, I.D. Hickson, Cloning and characterisation of the 5′-flanking region of the human topoisomerase IIα gene, J. Biol. Chem. 267 (1992) 18961-18965.
42. S.H. Ng, Y. Liu, L. Schnipper, Cloning and characterization of the 5′-flanking region for the human DNA topoisomerase II beta gene, Gene 203 (1997) 113-119.
43. H. Lehrach, in: K.E. Davies, S.M. Tilghman (Eds.), Genome Analysis vol. 1: Genetic and Physical Mapping, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1990, pp 39-81.
44. D. Hanahan, M. Meselson, Plasmid screening at high colony density, Gene 10 (1980) 63.
45. D. Hanahan, M. Meselson, Plasmid screening at high colony density, Methods Enzymol. 100 (1983) 333.
46. J. Sambrook, T. Maniatis, E.F. Fritsch, Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1989.
47. D. Kioussis, F. Wilson, C. Daniels, C. Leveton, J. Taverne, J.H. Playfair, Expression and rescuing of a cloned human tumour necrosis factor gene using an EBV-based shuffle cosmid vector, EMBO J. 6 (1987) 355-361.
48. T.P. Whitehead, G.H.G. Thorpe, T.J.N. Carter, C. Groucutt, C.L.J. Kricka, Enhanced luminescence procedure for sensitive determination of peroxidase-labeled conjugates in immunoassay, Nature 305 (1983) 158-159.
49. H.R. Rackwitz, G. Zehetner, A.M. Frischauf, H. Lehrach, Rapid restriction mapping of DNA cloned in lambda phage vectors, Gene 30 (1984) 95-200.
50. H.R. Rackwitz, G. Zehetner, H. Murialdo, H. Delius, J.H. Chai, A. Poustka, A.M. Frischauf, H. Lehrach, Analysis of cosmids using linearization by phage lambda terminase, Gene 40 (1985) 259-266.
51. F. Sanger, S. Nicklen, A.R. Coulson, DNA sequencing with chain-terminating inhibitors, Proc. Natl. Acad. Sci. USA 74 (1977) 5463-5467.
52. S. Henikoff, Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing, Gene 28 (1984) 357-359.
53. J.-H. Sng, Cloning and Characterisation of the Human Topoisomerase IIα Gene, Ph.D Thesis, University of London, 1995.
54. R.A. Padgett, P.J. Grabowski, M.M. Konarska, S. Seiler, P.A. Sharp, Splicing of messenger RNA precursors, Annu. Rev. Biochem. 55 (1986) 1119-1150.
55. R.J. Britten, W.F. Baron, D.B. Stout, E.H. Davidson, Sources and evolution of human Alu repeated sequences, Proc. Natl. Acad. Sci. USA 85 (1988) 4770-4774.
56. P.L. Deininger, V.K. Slagel, Recently amplified Alu family members share a common parental Alu sequence, Mol. Cell. Biol. 8 (1988) 4566-4569.
57. J.D. Hawkins, A survey on intron and exon lengths, Nucleic Acids Res. 21 (1988) 9893-9905.
58. Y.S. Vassetzky, G.-C. Alghisi, S.M. Gasser, DNA topoisomerase II mutations and resistance to anti-tumor drugs, BioEssays 17 (1995) 767-774.
59. C.A. Austin, K.L. Marsh, R.A. Wasserman, E. Willmore, P.J. Sayer, J.C. Wang, L.M. Fisher, Expression, domain structure and enzymatic properties of an active recombinant human DNA topoisomerase IIβ, J. Biol. Chem. 270 (1995) 15739-15746.
60. A new map of the human genome: GeneMap '98. Accessed at http://www.ncbi.nlm.nih.gov/genemap98.