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PMID: 16751265 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Tyrosyl-DNA phosphodiesterase (Tdp1) participates in the repair of Top2-mediated DNA damage.

Nitiss KC, Malik M, He X, White SW, Nitiss JL

Abstract

Agents targeting topoisomerases are active against a wide range of human tumors. Stabilization of covalent complexes, converting topoisomerases into DNA-damaging agents, is an essential aspect of cell killing by these drugs. A unique aspect of the repair of topoisomerase-mediated DNA damage is the requirement for pathways that can remove protein covalently bound to DNA. Tyrosyl-DNA phosphodiesterase (Tdp1) is an enzyme that removes phosphotyrosyl moieties bound to the 3' end of DNA. Cells lacking Tdp1 are hypersensitive to camptothecin, consistent with a role for Tdp1 in processing 3' phosphotyrosyl protein-DNA covalent complexes. Because Top2p forms a 5' phosphotyrosyl linkage with DNA, previous work predicted that Tdp1p would not be active against lesions involving Top2p. We found that deletion of the TDP1 gene in yeast confers hypersensitivity to Top2 targeting agents. Combining tdp1 mutations with deletions of genes involved in nonhomologous end joining, excision repair, or postreplication repair enhanced sensitivity to Top2 targeting drugs over the level seen with single mutants, suggesting that Tdp1 may function in collaboration with multiple pathways involved in strand break repair. tdp1 mutations can sensitize yeast cells to drugs targeting Top2 even when TOP1 is deleted. Finally, bacterially expressed yeast Tdp1p is able to remove a peptide derived from yTop2 that is covalently bound to DNA by a 5' phosphotyrosyl linkage. Our results show that Tdp1 plays more general roles in DNA repair than repair of Top1 mediated DNA damage, and may participate in repairing many types of base damage to DNA.

MeSH Terms
Antigens, Neoplasm/genetics,metabolism DNA Damage DNA Repair DNA Repair Enzymes DNA Topoisomerases, Type I/genetics,metabolism DNA Topoisomerases, Type II/genetics,metabolism DNA, Fungal/metabolism DNA-Binding Proteins/genetics,metabolism Endodeoxyribonucleases/genetics,metabolism Endonucleases/genetics,metabolism Etoposide/metabolism Humans Mutation Nucleic Acid Synthesis Inhibitors/metabolism Phosphoric Diester Hydrolases/genetics,metabolism Poly-ADP-Ribose Binding Proteins Saccharomyces cerevisiae/genetics,metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism
Chemicals
Antigens, Neoplasm DNA, Fungal DNA-Binding Proteins Nucleic Acid Synthesis Inhibitors Poly-ADP-Ribose Binding Proteins Saccharomyces cerevisiae Proteins RAD2 protein, S cerevisiae Etoposide Endodeoxyribonucleases Endonucleases RAD1 protein, S cerevisiae Phosphoric Diester Hydrolases Tdp1 protein, S cerevisiae DNA Topoisomerases, Type I DNA Topoisomerases, Type II TOP2A protein, human DNA Repair Enzymes
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Nitiss Karin C
Department of Molecular Pharmacology, St. Jude Children's Research Hospital, Memphis, TN 38105, USA.
Malik Mobeen
He Xiaoping
White Stephen W
Nitiss John L
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Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2006-06-13
Epub
2006-00-02
Pages
8953-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1482547
Subset
IM
Grants
NCI NIH HHS · R01 CA082313 · United States
NCI NIH HHS · CA21765 · United States
NCI NIH HHS · CA52814 · United States
NCI NIH HHS · P30 CA021765 · United States
NCI NIH HHS · CA82313 · United States
NCI NIH HHS · R01 CA052814 · United States
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