Epigenetic and genetic inactivation of tyrosyl-DNA-phosphodiesterase 1 (TDP1) in human lung cancer cells from the NCI-60 panel

DNA Repair

Volumn 13, Issue 1, 2014, Pages 1-9

  Gao, Rui ^a   Das, Benu Brata ^a,b   Chatterjee, Raghunath ^a,c   Abaan, Ogan D ^a   Agama, Keli ^a   Matuo, Renata ^a   Vinson, Charles ^a   Meltzer, Paul S ^a   Pommier, Yves ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b DEPARTMENT OF MATERIALS SCIENCE   (India)

^c INDIAN STATISTICAL INSTITUTE   (India)

Author keywords

CellMiner; Promoter hypermethylation; TDP1; Topoisomerases; Topotecan

Indexed keywords

AMINO ACID; GENOMIC DNA; MESSENGER RNA; MITOCHONDRIAL ENZYME; PHOSPHODIESTERASE I; TOPOTECAN; TYROSYL DNA PHOSPHODIESTERASE 1; UNCLASSIFIED DRUG;

ARTICLE; BIOINFORMATICS; CANCER CELL CULTURE; CANCER INHIBITION; CELL LYSATE; CELL SURVIVAL; CLONOGENIC ASSAY; CPG ISLAND; DNA DAMAGE; DNA METHYLATION; ENZYME ACTIVITY; ENZYME INACTIVATION; EPIGENETIC REPRESSION; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSFECTION; GENOMIC INSTABILITY; HIGH THROUGHPUT SEQUENCING; HOMOZYGOTE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LUNG CANCER; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN STRUCTURE; WESTERN BLOTTING;

CELLMINER; PROMOTER HYPERMETHYLATION; TDP1; TOPOISOMERASES; TOPOTECAN;

AMINO ACID SEQUENCE; CELL LINE, TUMOR; CONSERVED SEQUENCE; DNA METHYLATION; DNA TOPOISOMERASES, TYPE I; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC VARIATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; LUNG NEOPLASMS; MUTATION; NATIONAL CANCER INSTITUTE (U.S.); PHOSPHORIC DIESTER HYDROLASES; PROMOTER REGIONS, GENETIC; UNITED STATES;

EID: 84891166157     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2013.09.001     Document Type: Article

References (45)

1. Pouliot J.J., Yao K.C., Robertson C.A., Nash H.A. Yeast gene for a Tyr-DNA phosphodiesterase that repairs topo I covalent complexes. Science 1999, 286:552-555.
2. Interthal H., Pouliot J.J., Champoux J.J. The tyrosyl-DNA phosphodiesterase Tdp1 is a member of the phospholipase D superfamily. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:12009-12014.
3. Das B.B., Dexheimer T.S., Maddali K., Pommier Y. Role of tyrosyl-DNA phosphodiesterase (TDP1) in mitochondria. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:19790-19795.
4. Yang S.W., Burgin A.B., Huizenga B.N., Robertson C.A., Yao K.C., Nash H.A. A eukaryotic enzyme that can disjoin dead-end covalent complexes between DNA and type I topoisomerases. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:11534-11539.
5. Debethune L., Kohlhagen G., Grandas A., Pommier Y. Processing of nucleopeptides mimicking the topoisomerase I-DNA covalent complex by tyrosyl-DNA phosphodiesterase. Nucleic Acids Research 2002, 30:1198-1204.
6. Interthal H., Chen H.J., Champoux J.J. Human Tdp1 cleaves a broad spectrum of substrates, including phosphoamide linkages. Journal of Biological Chemistry 2005, 280:36518-36528.
7. Zhou T., Akopiants K., Mohapatra S., Lin P.S., Valerie K., Ramsden D.A., Lees-Miller S.P., Povirk L.F. Tyrosyl-DNA phosphodiesterase and the repair of 3'-phosphoglycolate-terminated DNA double-strand breaks. DNA Repair 2009, 8:901-911.
8. Murai J., Huang S.Y., Das B.B., Dexheimer T.S., Takeda S., Pommier Y. Tyrosyl-DNA phosphodiesterase 1 (TDP1) repairs DNA damage induced by topoisomerases I and II and base alkylation in vertebrate cells. Journal of Biological Chemistry 2012, 287:12848-12857.
9. Huang S.Y., Murai J., Dalla Rosa I., Dexheimer T.S., Naumova A., Gmeiner W.H., Pommier Y. TDP1 repairs nuclear and mitochondrial DNA damage induced by chain-terminating anticancer and antiviral nucleoside analogs. Nucleic Acids Research 2013, 41:7793-7803.
10. Nitiss K.C., Malik M., He X., White S.W., Nitiss J.L. Tyrosyl-DNA phosphodiesterase (Tdp1) participates in the repair of Top2-mediated DNA damage. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:8953-8958.
11. Bahmed K., Nitiss K.C., Nitiss J.L. Yeast Tdp1 regulates the fidelity of nonhomologous end joining. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:4057-4062.
12. 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., Stockton D.W., Lupski J.R. Mutation of TDP1, encoding a topoisomerase I-dependent DNA damage repair enzyme, in spinocerebellar ataxia with axonal neuropathy. Nature Genetics 2002, 32:267-272.
13. Wang J.C. A journey in the world of DNA rings and beyond. Annual Review of Biochemistry 2009, 78:31-54.
14. Pommier Y., Leo E., Zhang H., Marchand C. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chemistry and Biology 2010, 17:421-433.
15. Pommier Y. DNA topoisomerase I inhibitors: chemistry, biology, and interfacial inhibition. Chemical Reviews 2009, 109:2894-2902.
16. Pommier Y., Barcelo J.M., Rao V.A., Sordet O., Jobson A.G., Thibaut L., Miao Z.H., Seiler J.A., Zhang H., Marchand C., Agama K., Nitiss J.L., Redon C. Repair of topoisomerase I-mediated DNA damage. Progress in Nucleic Acid Research and Molecular Biology 2006, 81:179-229.
17. Liu C., Zhou S., Begum S., Sidransky D., Westra W.H., Brock M., Califano J.A. Increased expression and activity of repair genes TDP1 and XPF in non-small cell lung cancer. Lung Cancer 2007, 55:303-311.
18. Huang S.Y., Pommier Y., Marchand C. Tyrosyl-DNA phosphodiesterase 1 (Tdp1) inhibitors. Expert Opinion on Therapeutic Patents 2011, 21:1285-1292.
19. Scherf U., Ross D.T., Waltham M., Smith L.H., Lee J.K., Tanabe L., Kohn K.W., Reinhold W.C., Myers T.G., Andrews D.T., Scudiero D.A., Eisen M.B., Sausville E.A., Pommier Y., Botstein D., Brown P.O., Weinstein J.N. A gene expression database for the molecular pharmacology of cancer. Nature Genetics 2000, 24:236-244.
20. Liu H., D'Andrade P., Fulmer-Smentek S., Lorenzi P., Kohn K.W., Weinstein J.N., Pommier Y., Reinhold W.C. mRNA and microRNA expression profiles of the NCI-60 integrated with drug activities. Molecular Cancer Therapeutics 2010, 9:1080-1091.
21. Reinhold W.C., Sunshine M., Liu H., Varma S., Kohn K.W., Morris J., Doroshow J., Pommier Y. CellMiner: a web-based suite of genomic and pharmacologic tools to explore transcript and drug patterns in the NCI-60 cell line set. Cancer Research 2012, 72:3499-3511.
22. Abaan O.D., Polley E.C., Davis S.R., Zhu Y.J., Bilke S., Walker R.L., Pineda M., Gindin Y., Jiang Y., Reinhold W.C., Holbeck S.L., Simon R.M., Doroshow J.H., Pommier Y., Meltzer P.S. The exomes of the NCI-60 panel: a genomic resource for cancer biology and systems pharmacology. Cancer Research 2013, 73:4372-4382.
23. Dexheimer T.S., Stephen A.G., Fivash M.J., Fisher R.J., Pommier Y. The DNA binding and 3'-end preferential activity of human tyrosyl-DNA phosphodiesterase. Nucleic Acids Research 2010, 38:2444-2452.
24. Gao R., Huang S.Y., Marchand C., Pommier Y. Biochemical characterization of human tyrosyl-DNA phosphodiesterase 2 (TDP2/TTRAP): a Mg2+/Mn2+-dependent phosphodiesterase specific for the repair of topoisomerase cleavage complexes. Journal of Biological Chemistry 2012, 287:30842-30852.
25. Nakken S., Alseth I., Rognes T. Computational prediction of the effects of non-synonymous single nucleotide polymorphisms in human DNA repair genes. Neuroscience 2007, 145:1273-1279.
26. Shankavaram U.T., Varma S., Kane D., Sunshine M., Chary K.K., Reinhold W.C., Pommier Y., Weinstein J.N. CellMiner: a relational database and query tool for the NCI-60 cancer cell lines. BMC Genomics 2009, 10:277.
27. Gardiner-Garden M., Frommer M. CpG islands in vertebrate genomes. Journal of Molecular Biology 1987, 196:261-282.
28. El-Khamisy S.F., Saifi G.M., Weinfeld M., Johansson F., Helleday T., Lupski J.R., Caldecott K.W. Defective DNA single-strand break repair in spinocerebellar ataxia with axonal neuropathy-1. Nature 2005, 434:108-113.
29. Miao Z.H., Agama K., Sordet O., Povirk L., Kohn K.W., Pommier Y. Hereditary ataxia SCAN1 cells are defective for the repair of transcription-dependent topoisomerase I cleavage complexes. DNA Repair 2006, 5:1489-1494.
30. Das B.B., Antony S., Gupta S., Dexheimer T.S., Redon C.E., Garfield S., Shiloh Y., Pommier Y. Optimal function of the DNA repair enzyme TDP1 requires its phosphorylation by ATM and/or DNA-PK. EMBO Journal 2009, 28:3667-3680.
31. Liu C., Pouliot J.J., Nash H.A. Repair of topoisomerase I covalent complexes in the absence of the tyrosyl-DNA phosphodiesterase Tdp1. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:14970-14975.
32. Katyal S., el-Khamisy S.F., Russell H.R., Li Y., Ju L., Caldecott K.W., McKinnon P.J. TDP1 facilitates chromosomal single-strand break repair in neurons and is neuroprotective in vivo. EMBO Journal 2007, 26:4720-4731.
33. Hirano R., Interthal H., Huang C., Nakamura T., Deguchi K., Choi K., Bhattacharjee M.B., Arimura K., Umehara F., Izumo S., Northrop J.L., Salih M.A., Inoue K., Armstrong D.L., Champoux J.J., Takashima H., Boerkoel C.F. Spinocerebellar ataxia with axonal neuropathy: consequence of a Tdp1 recessive neomorphic mutation?. EMBO Journal 2007, 26:4732-4743.
34. Yang M.Q., Koehly L.M., Elnitski L.L. Comprehensive annotation of bidirectional promoters identifies co-regulation among breast and ovarian cancer genes. PLoS Computational Biology 2007, 3:e72.
35. Shu J., Jelinek J., Chang H., Shen L., Qin T., Chung W., Oki Y., Issa J.P. Silencing of bidirectional promoters by DNA methylation in tumorigenesis. Cancer Research 2006, 66:5077-5084.
36. Anfinsen C.B. The formation and stabilization of protein structure. Biochemical Journal 1972, 128:737-749.
37. Fersht A.R. Transition-state structure as a unifying basis in protein-folding mechanisms: contact order, chain topology, stability, and the extended nucleus mechanism. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:1525-1529.
38. Makarov D.E., Plaxco K.W. The topomer search model: a simple, quantitative theory of two-state protein folding kinetics. Protein Science: A Publication of the Protein Society 2003, 12:17-26.
39. Dobson C.M. Getting out of shape. Nature 2002, 418:729-730.
40. El-Khamisy S.F. To live or to die: a matter of processing damaged DNA termini in neurons. EMBO Molecular Medicine 2011, 3:78-88.
41. Pommier Y. Drugging topoisomerases: lessons and challenges. ACS Chemical Biology 2013, 8:82-95.
42. Zhang Y.W., Regairaz M., Seiler J.A., Agama K.K., Doroshow J.H., Pommier Y. Poly(ADP-ribose) polymerase and XPF-ERCC1 participate in distinct pathways for the repair of topoisomerase I-induced DNA damage in mammalian cells. Nucleic Acids Research 2011, 39:3607-3620.
43. Regairaz M., Zhang Y.W., Fu H., Agama K.K., Tata N., Agrawal S., Aladjem M.I., Pommier Y. Mus81-mediated DNA cleavage resolves replication forks stalled by topoisomerase I-DNA complexes. Journal of Cell Biology 2011, 195:739-749.
44. Kim Y., Spitz G.S., Veturi U., Lach F.P., Auerbach A.D., Smogorzewska A. Regulation of multiple DNA repair pathways by the Fanconi anemia protein SLX4. Blood 2012, 121:54-63.
45. Zeng Z., Sharma A., Ju L., Murai J., Umans L., Vermeire L., Pommier Y., Takeda S., Huylebroeck D., Caldecott K.W., El-Khamisy S.F. TDP2 promotes repair of topoisomerase I-mediated DNA damage in the absence of TDP1. Nucleic Acids Research 2012, 40:8371-8380.