Development of an oligonucleotide-based fluorescence assay for the identification of tyrosyl-DNA phosphodiesterase 1 (TDP1) inhibitors

Analytical Biochemistry

Volumn 454, Issue 1, 2014, Pages 17-22

  Walker, Sarah ^a   Meisenberg, Cornelia ^b   Bibby, Rachel A ^b   Askwith, Trevor ^a   Williams, Gareth ^a   Rininsland, Frauke H ^c   Pearl, Laurence H ^b   Oliver, Antony W ^b   El Khamisy, Sherif ^b,d   Ward, Simon ^a   Atack, John R ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

^c Gyrasol Technologies   (United States)

^d UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Assay; Fragment; High throughput screen; Inhibitor; TDP1; Topoisomerase

Indexed keywords

AMINO ACIDS; ASSAYS; CELL DEATH; CHEMOTHERAPY; DIAGNOSIS; ESTERS; FLUORESCENCE; MACHINERY; OLIGONUCLEOTIDES;

FRAGMENT; HIGH-THROUGHPUT SCREENS; INHIBITOR; TDP1; TOPOISOMERASES;

DNA;

CAMPTOTHECIN; CELL EXTRACT; DNA TOPOISOMERASE; OLIGONUCLEOTIDE; PHOSPHODIESTERASE I; PHOSPHODIESTERASE INHIBITOR; PHOSPHOTYROSINE; TYROSYL DNA PHOSPHODIESTERASE 1; TYROSYL DNA PHOSPHODIESTERASE 1 INHIBITOR; UNCLASSIFIED DRUG; ENZYME INHIBITOR; PHOSPHODIESTERASE; TDP1 PROTEIN, HUMAN;

ARTICLE; CANCER CELL; CANCER CHEMOTHERAPY; CELL STRAIN HEK293; CONTROLLED STUDY; COVALENT BOND; DNA STRAND BREAKAGE; DRUG IDENTIFICATION; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; FLUORESCENCE ANALYSIS; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; HYDROLYSIS; MOLECULAR LIBRARY; PRIORITY JOURNAL; WHOLE CELL; WHOLE CELL EXTRACT; COST BENEFIT ANALYSIS; DRUG SCREENING; ECONOMICS; GENETICS; HEK293 CELL LINE; KINETICS; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; PROCEDURES; SPECTROFLUOROMETRY;

BASE SEQUENCE; COST-BENEFIT ANALYSIS; DRUG EVALUATION, PRECLINICAL; ENZYME INHIBITORS; HEK293 CELLS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; KINETICS; MUTATION; OLIGONUCLEOTIDES; PHOSPHORIC DIESTER HYDROLASES; SPECTROMETRY, FLUORESCENCE;

EID: 84906858920     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2014.03.004     Document Type: Article

References (32)

1. J.C. Wang Cellular roles of DNA topoisomerases: a molecular perspective Nat. Rev. Mol. Cell Biol. 3 2002 430 440
2. M. Alagoz, D.C. Gilbert, S. El-Khamisy, and A.J. Chalmers DNA repair and resistance to topoisomerase I inhibitors: mechanisms, biomarkers and therapeutic targets Curr. Med. Chem. 19 2012 3874 3885
3. K.W. Caldecott Single-strand break repair and genetic disease Nat. Rev. Genet. 9 2008 619 631
4. C.P. Lin, Y. Ban, Y.L. Lyu, S.D. Desai, and L.F. Liu A ubiquitin-proteasome pathway for the repair of topoisomerase I-DNA covalent complexes J. Biol. Chem. 283 2008 21074 21083
5. M. Alagoz, S.C. Chiang, A. Sharma, and S.F. El-Khamisy ATM deficiency results in accumulation of DNA-topoisomerase I covalent intermediates in neural cells PLoS One 8 2013 e58239
6. H. Interthal, J.J. Pouliot, and J.J. Champoux The tyrosyl-DNA phosphodiesterase Tdp1 is a member of the phospholipase D superfamily Proc. Natl. Acad. Sci. U.S.A. 98 2001 12009 12014
7. K.V. Inamdar, J.J. Pouliot, T. Zhou, S.P. Lees-Miller, A. Rasouli-Nia, and L.F. Povirk 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 2002 27162 27168
8. N.A. Lebedeva, N.I. Rechkunova, and O.I. Lavrik AP-site cleavage activity of tyrosyl-DNA phosphodiesterase 1 FEBS Lett. 585 2011 683 686
9. M. Alagoz, O.S. Wells, and S.F. El-Khamisy TDP1 deficiency sensitizes human cells to base damage via distinct topoisomerase I and PARP mechanisms with potential applications for cancer therapy Nucleic Acids Res. 42 2014 3089 3103
10. H. Takashima, C.F. Boerkoel, J. John, G.M. Saifi, M.A. Salih, D. Armstrong, Y. Mao, F.A. Quiocho, B.B. Roa, M. Nakagawa, D.W. Stockton, and J.R. Lupski Mutation of TDP1, encoding a topoisomerase I-dependent DNA damage repair enzyme, in spinocerebellar ataxia with axonal neuropathy Nat. Genet. 32 2002 267 272
11. H. Interthal, H.J. Chen, T.E. Kehl-Fie, J. Zotzmann, J.B. Leppard, and J.J. Champoux SCAN1 mutant Tdp1 accumulates the enzyme - DNA intermediate and causes camptothecin hypersensitivity EMBO J. 24 2005 2224 2233
12. Z.H. Miao, K. Agama, O. Sordet, L. Povirk, K.W. Kohn, and Y. Pommier Hereditary ataxia SCAN1 cells are defective for the repair of transcription-dependent topoisomerase I cleavage complexes DNA Repair (Amst.) 5 2006 1489 1494
13. B.B. Das, S. Antony, S. Gupta, T.S. Dexheimer, C.E. Redon, S. Garfield, Y. Shiloh, and Y. Pommier Optimal function of the DNA repair enzyme TDP1 requires its phosphorylation by ATM and/or DNA-PK EMBO J. 28 2009 3667 3680
14. S.C. Chiang, J. Carroll, and S.F. El-Khamisy TDP1 serine 81 promotes interaction with DNA ligase IIIalpha and facilitates cell survival following DNA damage Cell Cycle 9 2010 588 595
15. J.J. Hudson, S.C. Chiang, O.S. Wells, C. Rookyard, and S.F. El-Khamisy SUMO modification of the neuroprotective protein TDP1 facilitates chromosomal single-strand break repair Nat. Commun. 3 2012 733
16. M.C. Nivens, T. Felder, A.H. Galloway, M.M. Pena, J.J. Pouliot, and H.T. Spencer Engineered resistance to camptothecin and antifolates by retroviral coexpression of tyrosyl DNA phosphodiesterase-I and thymidylate synthase Cancer Chemother. Pharmacol. 53 2004 107 115
17. H.U. Barthelmes, M. Habermeyer, M.O. Christensen, C. Mielke, H. Interthal, J.J. Pouliot, F. Boege, and D. Marko TDP1 overexpression in human cells counteracts DNA damage mediated by topoisomerases I and II.J. Biol. Chem. 279 2004 55618 55625
18. C. Liu, S. Zhou, S. Begum, D. Sidransky, W.H. Westra, M. Brock, and J.A. Califano Increased expression and activity of repair genes TDP1 and XPF in non-small cell lung cancer Lung Cancer 55 2007 303 311
19. T.J. Cheng, P.G. Rey, T. Poon, and C.C. Kan Kinetic studies of human tyrosyl-DNA phosphodiesterase, an enzyme in the topoisomerase I DNA repair pathway Eur. J. Biochem. 269 2002 3697 3704
20. S. Antony, C. Marchand, A.G. Stephen, L. Thibaut, K.K. Agama, R.J. Fisher, and Y. Pommier 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 2007 4474 4484
21. C. Marchand, W.A. Lea, A. Jadhav, T.S. Dexheimer, C.P. Austin, J. Inglese, Y. Pommier, and A. Simeonov Identification of phosphotyrosine mimetic inhibitors of human tyrosyl-DNA phosphodiesterase I by a novel AlphaScreen high-throughput assay Mol. Cancer Ther. 8 2009 240 248
22. G.J. Thomson, N.S. Hamilton, G.V. Hopkins, I.D. Waddell, A.J. Watson, and D.J. Ogilvie A fluorescence-based assay for the apurinic/apyrimidinic-site cleavage activity of human tyrosyl-DNA phosphodiesterase 1 Anal. Biochem. 440 2013 1 5
23. P.W. Jensen, M. Falconi, E.L. Kristoffersen, A.T. Simonsen, J.B. Cifuentes, L.B. Marcussen, R. Frøhlich, J. Vagner, C. Harmsen, S. Juul, Y.P. Ho, M.A. Withers, J.R. Lupski, J. Koch, A. Desideri, B.R. Knudsen, and M. Stougaard Real-time detection of TDP1 activity using a fluorophore-quencher coupled DNA-biosensor Biosens. Bioelectron. 48 2013 230 237
24. J.H. Zhang, T.D. Chung, and K.R. Oldenburg A simple statistical parameter for use in evaluation and validation of high throughput screening assays J. Biomol. Screen. 4 1999 67 73
25. F. Cortes Ledesma, S.F. El Khamisy, M.C. Zuma, K. Osborn, and K.W. Caldecott A human 5′-tyrosyl DNA phosphodiesterase that repairs topoisomerase-mediated DNA damage Nature 461 2009 674 678
26. S. Katyal, S.F. el-Khamisy, H.R. Russell, Y. Li, L. Ju, K.W. Caldecott, and P.J. McKinnon TDP1 facilitates chromosomal single-strand break repair in neurons and is neuroprotective in vivo EMBO J. 26 2007 4720 4731
27. Z. Zeng, F. Cortes-Ledesma, S.F. El Khamisy, and K.W. Caldecott TDP2/TTRAP is the major 5′-tyrosyl DNA phosphodiesterase activity in vertebrate cells and is critical for cellular resistance to topoisomerase II-induced DNA damage J. Biol. Chem. 286 2011 403 409
28. Z. Zeng, A. Sharma, L. Ju, J. Murai, L. Umans, L. Vermeire, Y. Pommier, S. Takeda, D. Huylebroeck, K.W. Caldecott, and S.F. El-Khamisy TDP2 promotes repair of topoisomerase I-mediated DNA damage in the absence of TDP1 Nucleic Acids Res. 40 2012 8371 8380
29. A.C. Raymond, B.L. Staker, and A.B. Burgin Substrate specificity of tyrosyl-DNA phosphodiesterase I (Tdp1) J. Biol. Chem. 280 2005 22029 22035
30. H. Interthal, H.J. Chen, and J.J. Champoux Human Tdp1 cleaves a broad spectrum of substrates, including phosphoamide linkages J. Biol. Chem. 280 2005 36518 36528
31. J. Barker, S. Courtney, T. Hesterkamp, D. Ullmann, and M. Whittaker Fragment screening by biochemical assay Expert Opin. Drug Discov. 1 2006 225 236
32. A. Boettcher, S. Ruedisser, P. Erbel, D. Vinzenz, N. Schiering, U. Hassiepen, P. Rigollier, L.M. Mayr, and J. Woelcke Fragment-based screening by biochemical assays: systematic feasibility studies with trypsin and MMP12 J. Biomol. Screen. 15 2010 1029 1041