The DNA binding and 3′-end preferential activity of human tyrosyl-DNA phosphodiesterase

Nucleic Acids Research

Volumn 38, Issue 7, 2010, Pages 2444-2452

  Dexheimer, Thomas S ^a   Stephen, Andrew G ^b   Fivash, Matthew J ^c   Fisher, Robert J ^b   Pommier, Yves ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; PHOSPHODIESTERASE; TYROSYL DNA PHOSPHODIESTERASE; UNCLASSIFIED DRUG; FLUORESCEIN; FLUORESCENT DYE; OLIGONUCLEOTIDE; OLIGONUCLEOTIDE PHOSPHOROTHIOATE; TDP1 PROTEIN, HUMAN;

ANISOTROPY; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DNA ADDUCT; DNA CLEAVAGE; DNA STRAND BREAKAGE; DNA STRUCTURE; ESCHERICHIA COLI; GENE ACTIVITY; GENE FUNCTION; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; SURFACE PLASMON RESONANCE; CHEMISTRY; FLUORESCENCE POLARIZATION; HUMAN; METABOLISM;

DNA; DNA CLEAVAGE; FLUORESCEIN; FLUORESCENCE POLARIZATION; FLUORESCENT DYES; HUMANS; OLIGONUCLEOTIDES; PHOSPHORIC DIESTER HYDROLASES; PHOSPHOROTHIOATE OLIGONUCLEOTIDES; SURFACE PLASMON RESONANCE;

EID: 77952300162     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp1206     Document Type: Article

References (35)

1. Dexheimer,T.S., Antony,S., Marchand,C. and Pommier,Y. (2008) Tyrosyl-DNA phosphodiesterase as a target for anticancer therapy. Anticancer Agents Med. Chem., 8, 381-389.
2. Yang,S.W., Burgin,A.B. Jr, Huizenga,B.N., Robertson,C.A., Yao,K.C. and Nash,H.A. (1996) A eukaryotic enzyme that can disjoin dead-end covalent complexes between DNA and type I topoisomerases. Proc. Natl Acad. Sci. USA, 93, 11534-11539.
3. Interthal,H., Pouliot,J.J. and Champoux,J.J. (2001) The tyrosyl-DNA phosphodiesterase Tdp1 is a member of the phospholipase D superfamily. Proc. Natl Acad. Sci. USA, 98, 12009-12014.
4. Debethune,L., Kohlhagen,G., Grandas,A. and Pommier,Y. (2002) Processing of nucleopeptides mimicking the topoisomerase I-DNA covalent complex by tyrosyl-DNA phosphodiesterase. Nucleic Acids Res., 30, 1198-1204.
5. Inamdar,K.V., Pouliot,J.J., Zhou,T., Lees-Miller,S.P., Rasouli-Nia,A. and Povirk,L.F. (2002) Conversion of phosphoglycolate to phosphate termini on 3′ overhangs of DNA double strand breaks by the human tyrosyl-DNA phosphodiesterase hTdp1. J. Biol. Chem., 277, 27162-27168.
6. Interthal,H., Chen,H.J. and Champoux,J.J. (2005) Human Tdp1 cleaves a broad spectrum of substrates, including phosphoamide linkages. J. Biol. Chem., 280, 36518-36528.
7. Karimi-Busheri,F., Daly,G., Robins,P., Canas,B., Pappin,D.J., Sgouros,J., Miller,G.G., Fakhrai,H., Davis,E.M., Le Beau,M.M. et al. (1999) Molecular characterization of a human DNA kinase. J. Biol. Chem., 274, 24187-24194.
8. Karimi-Busheri,F., Lee,J., Tomkinson,A.E. and Weinfeld,M. (1998) Repair of DNA strand gaps and nicks containing 3′-phosphate and 5′-hydroxyl termini by purified mammalian enzymes. Nucleic Acids Res., 26, 4395-4400.
9. Wilson,D.M. 3rd (2007) Processing of nonconventional DNA strand break ends. Environ. Mol. Mutagen., 48, 772-782.
10. Takashima,H., Boerkoel,C.F., John,J., Saifi,G.M., Salih,M.A., Armstrong,D., Mao,Y., Quiocho,F.A., Roa,B.B., Nakagawa,M. et al. (2002) Mutation of TDP1, encoding a topoisomerase I-dependent DNA damage repair enzyme, in spinocerebellar ataxia with axonal neuropathy. Nat. Genet., 32, 267-272.
11. El-Khamisy,S.F., Hartsuiker,E. and Caldecott,K.W. (2007) TDP1 facilitates repair of ionizing radiation-induced DNA single-strand breaks. DNA Repair, 6, 1485-1495.
12. El-Khamisy,S.F., Saifi,G.M., Weinfeld,M., Johansson,F., Helleday,T., Lupski,J.R. and Caldecott,K.W. (2005) Defective DNA single-strand break repair in spinocerebellar ataxia with axonal neuropathy-1. Nature, 434, 108-113.
13. Interthal,H., Chen,H.J., Kehl-Fie,T.E., Zotzmann,J., Leppard,J.B. and Champoux,J.J. (2005) SCAN1 mutant Tdp1 accumulates the enzyme-DNA intermediate and causes camptothecin hypersensitivity. EMBO J., 24, 2224-2233.
14. Miao,Z.H., Agama,K., Sordet,O., Povirk,L., Kohn,K.W. and Pommier,Y. (2006) Hereditary ataxia SCAN1 cells are defective for the repair of transcription-dependent topoisomerase I cleavage complexes. DNA Repair, 5, 1489-1494.
15. Hirano,R., Interthal,H., Huang,C., Nakamura,T., Deguchi,K., Choi,K., Bhattacharjee,M.B., Arimura,K., Umehara,F., Izumo,S. et al. (2007) Spinocerebellar ataxia with axonal neuropathy: consequence of a Tdp1 recessive neomorphic mutation? EMBO J., 26, 4732-4743.
16. Katyal,S., el-Khamisy,S.F., Russell,H.R., Li,Y., Ju,L., Caldecott,K.W. and McKinnon,P.J. (2007) TDP1 facilitates chromosomal single-strand break repair in neurons and is neuroprotective in vivo. EMBO J., 26, 4720-4731.
17. Rideout,M.C., Raymond,A.C. and Burgin,A.B. Jr (2004) Design and synthesis of fluorescent substrates for human tyrosyl-DNA phosphodiesterase I. Nucleic Acids Res., 32, 4657-4664.
18. Antony,S., Marchand,C., Stephen,A.G., Thibaut,L., Agama,K.K., Fisher,R.J. and Pommier,Y. (2007) Novel high-throughput electrochemiluminescent assay for identification of human tyrosyl-DNA phosphodiesterase (Tdp1) inhibitors and characterization of furamidine (NSC 305831) as an inhibitor of Tdp1. Nucleic Acids Res., 35, 4474-4484.
19. Marchand,C., Lea,W.A., Jadhav,A., Dexheimer,T.S., Austin,C.P., Inglese,J., Pommier,Y. and Simeonov,A. (2009) Identification of phosphotyrosine mimetic inhibitors of human tyrosyl-DNA phosphodiesterase I by a novel AlphaScreen high-throughput assay. Mol. Cancer Ther., 8, 240-248.
20. Nitiss,K.C., Malik,M., He,X., White,S.W. and Nitiss,J.L. (2006) Tyrosyl-DNA phosphodiesterase (Tdp1) participates in the repair of Top2-mediated DNA damage. Proc. Natl Acad Sci. USA, 103, 8953-8958.
21. Barthelmes,H.U., Habermeyer,M., Christensen,M.O., Mielke,C., Interthal,H., Pouliot,J.J., Boege,F. and Marko,D. (2004)TDP1 overexpression in human cells counteracts DNA damage mediated by topoisomerases I and II J. Biol. Chem., 279, 55618-55625.
22. He,X., van Waardenburg,R.C., Babaoglu,K., Price,A.C., Nitiss,K.C., Nitiss,J.L., Bjornsti,M.A. and White,S.W. (2007) Mutation of a conserved active site residue converts tyrosyl-DNA phosphodiesterase I into a DNA topoisomerase I-dependent poison. J. Mol. Biol., 372, 1070-1081.
23. Davies,D.R., Interthal,H., Champoux,J.J. and Hol,W.G. (2002) The crystal structure of human tyrosyl-DNA phosphodiesterase, Tdp1. Structure, 10, 237-248.
24. Fisher,R.J., Fivash,M.J., Stephen,A.G., Hagan,N.A., Shenoy,S.R., Medaglia,M.V., Smith,L.R., Worthy,K.M., Simpson,J.T., Shoemaker,R. et al. (2006) Complex interactions of HIV-1 nucleocapsid protein with oligonucleotides. Nucleic Acids Res., 34, 472-484.
25. Lakowicz,J.R. (1999) Principles of Fluorescence Spectroscopy, 2nd edn. Springer-Verlag, New York.
26. Crockett,A.O. and Wittwer,C.T. (2001) Fluorescein-labeled oligonucleotides for real-time pcr: using the inherent quenching of deoxyguanosine nucleotides. Anal. Biochem., 290, 89-97.
27. Nazarenko,I., Pires,R., Lowe,B., Obaidy,M. and Rashtchian,A. (2002) Effect of primary and secondary structure of oligodeoxyribonucleotides on the fluorescent properties of conjugated dyes. Nucleic Acids Res., 30, 2089-2195.
28. Hergenrother,P.J., Haas,M.K. and Martin,S.F. (1997) Chromogenic assay for phospholipase D from Streptomyces chromofuscus: application to the evaluation of substrate analogs. Lipids, 32, 783-788.
29. Sasnauskas,G., Connolly,B.A., Halford,S.E. and Siksnys,V. (2007) Site-specific DNA transesterification catalyzed by a restriction enzyme. Proc. Natl Acad. Sci. USA, 104, 2115-2120.
30. Pouliot,J.J., Yao,K.C., Robertson,C.A. and Nash,H.A. (1999) Yeast gene for a Tyr-DNA phosphodiesterase that repairs topoisomerase I complexes. Science, 286, 552-555.
31. Davies,D.R., Interthal,H., Champoux,J.J. and Hol,W.G. (2003) Crystal structure of a transition state mimic for Tdp1 assembled from vanadate, DNA, and a topoisomerase I-derived peptide. Chem. Biol., 10, 139-147.
32. Redinbo,M.R., Stewart,L., Kuhn,P., Champoux,J.J. and Hol,W.G. (1998) Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science, 279, 1504-1513.
33. Pommier,Y., Barcelo,J., Rao,V.A., Sordet,O., Jobson,A.G., Thibaut,L., Miao,Z., Seiler,J., Zhang,H., Marchand,C. et al. (2006) Repair of topoisomerase I-mediated DNA damage. Prog. Nucleic Acid Res. Mol. Biol., 81, 179-229.
34. Nitiss,J.L. (2009) Targeting DNA topoisomerase II in cancer chemotherapy. Nat. Rev. Cancer, 9, 338-350.
35. Cortes Ledesma,F., El Khamisy,S.F., Zuma,M.C., Osborn,K. and Caldecott,K.W. (2009) A human 5′-tyrosyl DNA phosphodiesterase that repairs topoisomerase-mediated DNA damage. Nature, 461, 674-678.