Abstract
Tyrosyl-DNA phosphodiesterase-1 (Tdp1) is the only known enzyme to remove tyrosine from complexes in which the amino acid is linked to the 3'-end of DNA fragments. Such complexes can be produced following DNA processing by topoisomerase I, and recent studies in yeast have demonstrated the importance of TDP1 for cell survival following topoisomerase I-mediated DNA damage. In the present study, we used synthetic oligodeoxynucleotide-peptide conjugates (nucleopeptides) and recombinant yeast Tdp1 to investigate the molecular determinants for Tdp1 activity. We find that Tdp1 can process nucleopeptides with up to 13 amino acid residues but is poorly active with a 70 kDa fragment of topoisomerase I covalently linked to a suicide DNA substrate. Furthermore, Tdp1 was more effective with nucleopeptides with one to four amino acids than 15 amino acids. Tdp1 was also more effective with nucleopeptides containing 15 nt than with homolog nucleopeptides containing 4 nt. These results suggest that DNA binding contributes to the activity of Tdp1 and that Tdp1 would be most effective after topoisomerase I has been proteolyzed in vivo.
MeSH Terms
Amino Acid Sequence
Base Sequence
DNA/chemistry,metabolism
DNA Topoisomerases, Type I/metabolism
Kinetics
Macromolecular Substances
Models, Chemical
Nucleoproteins/chemistry,metabolism
Oligodeoxyribonucleotides/chemistry,metabolism
Peptides/chemistry,metabolism
Phosphoric Diester Hydrolases/metabolism
Saccharomyces cerevisiae/enzymology
Substrate Specificity
Chemicals
Macromolecular Substances
Nucleoproteins
Oligodeoxyribonucleotides
Peptides
DNA
Phosphoric Diester Hydrolases
tyrosyl-DNA phosphodiesterase
DNA Topoisomerases, Type I
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Debéthune Laurent
Department of Organic Chemistry, Faculty of Chemistry, University of Barcelona, Martí i Franquès 1-11, E-08028 Barcelona, Spain.
Kohlhagen Glenda
Grandas Anna
Pommier Yves
References (23)
23 references, click to expand
-
Benzo[a]pyrene diol epoxide adducts in DNA are potent suppressors of a normal topoisomerase I cleavage site and powerful inducers of other topoisomerase I cleavages.
Proc Natl Acad Sci U S A. 2000 Feb 29;97(5):2040-5
PMID: 10688881
-
A eukaryotic enzyme that can disjoin dead-end covalent complexes between DNA and type I topoisomerases.
Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11534-9
PMID: 8876170
-
DNA topoisomerases: structure, function, and mechanism.
Annu Rev Biochem. 2001;70:369-413
PMID: 11395412
-
Topoisomerase I inhibitors: selectivity and cellular resistance.
Drug Resist Updat. 1999 Oct;2(5):307-318
PMID: 11504505
-
The tyrosyl-DNA phosphodiesterase Tdp1 is a member of the phospholipase D superfamily.
Proc Natl Acad Sci U S A. 2001 Oct 9;98(21):12009-14
PMID: 11572945
-
Effects of uracil incorporation, DNA mismatches, and abasic sites on cleavage and religation activities of mammalian topoisomerase I.
J Biol Chem. 1997 Mar 21;272(12):7792-6
PMID: 9065442
-
Conservation of structure and mechanism between eukaryotic topoisomerase I and site-specific recombinases.
Cell. 1998 Mar 20;92(6):841-50
PMID: 9529259
-
Trapping of mammalian topoisomerase I and recombinations induced by damaged DNA containing nicks or gaps. Importance of DNA end phosphorylation and camptothecin effects.
J Biol Chem. 1997 Oct 17;272(42):26441-7
PMID: 9334220
-
New technique for uncoupling the cleavage and religation reactions of eukaryotic topoisomerase I. The mode of action of camptothecin at a specific recognition site.
J Mol Biol. 1991 Dec 5;222(3):669-78
PMID: 1660929
-
Position-specific trapping of topoisomerase I-DNA cleavage complexes by intercalated benzo[a]- pyrene diol epoxide adducts at the 6-amino group of adenine.
Proc Natl Acad Sci U S A. 2000 Sep 26;97(20):10739-44
PMID: 10995470
-
Teaching a new dog old tricks?
Structure. 1998 May 15;6(5):543-8
PMID: 9634692
-
Ubiquitin/26S proteasome-mediated degradation of topoisomerase I as a resistance mechanism to camptothecin in tumor cells.
Cancer Res. 2001 Aug 1;61(15):5926-32
PMID: 11479235
-
Induction of topoisomerase I cleavage complexes by 1-beta -D-arabinofuranosylcytosine (ara-C) in vitro and in ara-C-treated cells.
Proc Natl Acad Sci U S A. 2000 Feb 15;97(4):1885-90
PMID: 10677551
-
Pathways for repair of topoisomerase I covalent complexes in Saccharomyces cerevisiae.
Genes Cells. 2001 Aug;6(8):677-87
PMID: 11532027
-
DNA topoisomerases.
Annu Rev Biochem. 1996;65:635-92
PMID: 8811192
-
DNA topoisomerases: essential enzymes and lethal targets.
Annu Rev Pharmacol Toxicol. 1994;34:191-218
PMID: 8042851
-
Conversion of topoisomerase I cleavage complexes on the leading strand of ribosomal DNA into 5'-phosphorylated DNA double-strand breaks by replication runoff.
Mol Cell Biol. 2000 Jun;20(11):3977-87
PMID: 10805740
-
Camptothecin induction of a time- and concentration-dependent decrease of topoisomerase I and its implication in camptothecin activity.
Mol Pharmacol. 1995 May;47(5):907-14
PMID: 7538195
-
Topoisomerase I-mediated DNA damage.
Adv Cancer Res. 2001;80:189-216
PMID: 11034544
-
Eukaryotic DNA topoisomerases I.
Biochim Biophys Acta. 1995 May 17;1262(1):1-14
PMID: 7772596
-
DNA recombinase activity of eukaryotic DNA topoisomerase I; effects of camptothecin and other inhibitors.
Mutat Res. 1995 Sep;337(2):135-45
PMID: 7565862
-
Two classes of DNA end-joining reactions catalyzed by vaccinia topoisomerase I.
J Biol Chem. 1992 Aug 25;267(24):16755-8
PMID: 1324909
-
Yeast gene for a Tyr-DNA phosphodiesterase that repairs topoisomerase I complexes.
Science. 1999 Oct 15;286(5439):552-5
PMID: 10521354