Position- and orientation-specific enhancement of topoisomerase I cleavage complexes by triplex DNA structures

Nucleic Acids Research

Volumn 32, Issue 17, 2004, Pages 5163-5173

  Antony, Smitha ^b   Arimondo, Paola B ^a   Sun, Jian Sheng ^a   Pommier, Yves ^b  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAMPTOTHECIN; DNA TOPOISOMERASE; OLIGONUCLEOTIDE; DNA; TRIPLEX DNA;

3' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; DNA BINDING; DNA CLEAVAGE; DNA SEQUENCE; DNA STRUCTURE; ENZYME ACTIVITY; HUMAN; MOLECULAR MODEL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; ENZYME ACTIVATION; METABOLISM;

BASE SEQUENCE; DNA; DNA TOPOISOMERASES, TYPE I, EUKARYOTIC; ENZYME ACTIVATION; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION;

EID: 4944266359     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkh847     Document Type: Article

References (53)

1. Wang,J.C. (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nature Rev. Mol. Cell. Biol., 3, 430-440.
2. Champoux,J.J. (2001) DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem., 70, 369-413.
3. Pommier,Y., Pourquier,P., Fan,Y. and Strumberg,D. (1998) Mechanism of action of eukaryotic DNA topoisomerase I and drugs targeted to the enzyme. Biochim. Biophys. Acta, 1400, 83-105.
4. Osheroff,N. (ed.) (1998) DNA Topoisomerases. Elsevier, Amsterdam.
5. Tian,L., Claeboe,C.D., Hecht,S.M. and Shuman,S. (2003) Guarding the genome: electrostatic repulsion of water by DNA suppresses a potent nuclease activity of topoisomerase IB. Mol. Cell, 12, 199-208.
6. Pommier,Y. (1996) Eukaryotic DNA topoisomerase I: genome gatekeeper and its intruders, camptothecins. Semin. Oncol., 23 1-10.
7. Chen,A.Y. and Liu,L.F. (1994) DNA topoisomerases: essential enzymes and lethal targets. Annu. Rev. Pharmacol. Toxicol., 94 194-218.
8. Nitiss,J.L. and Wang,J.C. (1996) Mechanisms of cell killing by drugs that trap covalent complexes between DNA topoisomerases and DNA. Mol. Pharmacol., 50, 1095-1102.
9. Pommier,Y., Redon,C., Rao,A., Seiler,J.A., Sordet,O., Takemura,H., Antony,S., Meng,L.-H., Liao, Z.Y., Kehlhagen, G. et al. (2003) Repair of and checkpoint response to Topoisomerase I-modified DNA damage. Mutat Res., 532, 173-203.
10. Rich,A. (1993) DNA comes in many forms. Gene, 135 99-109.
11. Mills,M., Lacroix,L., Arimondo,P.B., Leroy,J.L., Francois,J.C., Klump,H. and Mergny,J.L. (2002) Unusual DNA conformations: implications for telomeres. Curr. Med. Chem. Anti-Canc. Agents, 2, 627-644.
12. Hélène,C., Thuong,N.T. and Harel-Bellan,A. (1992) Control of gene expression by triple helix-forming oligonucleotides. The antigene strategy. Ann. NY Acad. Sci., 660, 27-36.
13. Hoyne,P.R., Gacy,A.M., McMurray,C.T. and Maher,L.J.,III (2000) Stabilities of intrastrand pyrimidine motif DNA and RNA triple helices. Nucleic Acids Res., 28, 770-775.
14. Goni,J.R., de la Cruz,X. and Orozco,M. (2004) Triplex-forming oligonucleotide target sequences in the human genome. Nucleic Acids Res., 32, 354-360.
15. Giovannangeli,C. and Hélène,C. (2000) Triplex-forming molecules for modulation of DNA information processing. Curr. Opin. Mol. Ther., 2, 288-296.
16. Arimondo,P.B., Boutorine,A., Baldeyrou,B., Bailly,C., Kuwahara,M., Hecht,S.M., Sun,J.-S., Garestier,T. and Hélè ne,C. (2002) Design and optimization of camptothecin conjugates of triple helix-forming oligonucleotides for sequence-specific DNA cleavage by topoisomerase I. J. Biol. Chem., 277, 3132-3140.
17. Arimondo,P.B., Angenault,S., Halby,L., Boutorine,A., Schmidt,F., Monneret,C., Garestier,T., Sun,J.S., Bailly,C. and Hélène,C. (2003) Spatial organization of topoisomerase I-mediated DNA cleavage induced by camptothecin-oligonucleotide conjugates. Nucleic Acids Res., 31, 4031-4040.
18. Redinbo,M.R., Stewart,L., Kuhn,P., Champoux,J.J. and Hol,W.G.J. (1998) Crystal structure of human topoisomerase I in covalent and noncovalent complexes with DNA. Science, 279, 1504-1513.
19. Pourquier,P., Ueng,L.-M., Kohlhagen,G., Mazumder,A., Gupta,M., Kohn,K.W. and Pommier,Y. (1997) Effects of uracil incorporation, DNA mismatches, and abasic sites on cleavage and religation activities of mammalian topoisomerase I. J. Biol. Chem., 272, 7792-7796.
20. Pourquier,P., Ueng,L.-M., Fertala,J., Wang,D., Park,H.-J., Essigman,J.M., Bjornsti,M.-A. and Pommier,Y. (1999) Induction of reversible complexes between eukaryotic DNA topoisomerase I and DNA-containing oxidative base damages. J. Biol. Chem., 274, 8516-8523.
21. Pommier,Y., Laco,G.S., Kohlhagen,G., Sayer,J.M., Kroth,H. and Jerina,D.M. (2000) 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. USA, 97 10739-10744.
22. Lesher,D.T., Pommier,Y., Stewart,L. and Redinbo,M.R. (2002) 8-Oxoguanine rearranges the active site of human topoisomerase I. Proc. Natl Acad. Sci. USA, 99, 12102-12107.
23. Andersen,A.H., Gocke,E., Bonven,B.J., Nielsen,O.F. and Westergaard,O. (1985) Topoisomerase I has a strong binding preference for a conserved hexadecameric sequence in the promoter region of the rRNA gene from Tetrahymena pyriformis. Nucleic Acids Res., 13, 1543-1557.
24. Cantor,C.R., Warshaw,M.M. and Shapiro,H. (1970) Oligonucleotide interactions. 3. Circular dichroism studies of the conformation of deoxyoligonucleotides. Biopolymers, 9, 1059-1077.
25. Antony,S., Jayaraman,M., Laco,G., Kohlhagen,G., Kohn,K.W., Cushman,M. and Pommier,Y. (2003) Differential induction of topoisomerase I-DNA cleavage complexes by the indenoisoquinoline MJ-III-65 (NSC 706744) and camptothecin: base sequence analysis and activity against camptothecin-resistant topoisomerases I. Cancer Res., 63, 7428-7435.
26. Lavery,R. and Sklenar,H. (1988) The definition of generalized helicoidal parameters and of axis curvature for irregular nucleic acids. J. Biomol. Struct. Dyn., 6, 63-91.
27. Lavery,R., Sklenar,H., Zakrzewska,K. and Pullman,B. (1986) The flexibility of the nucleic acids: (II). the calculation of internal energy and applications to mononucleotide repeat DNA. J. Biomol. Struct. Dyn., 3, 989-1014.
28. Chomilier,J., Sun,J.S., Collier,D.A., Garestier,T., Hélène,C. and Lavery,R. (1992) A computational and experimental study of the bending induced at a double-triple helix junction. Biophys. Chem., 45, 143-152.
29. Ouali,M., Letellier,R., Adnet,F., Liquier,J., Sun,J.S., Lavery,R. and Taillandier,E. (1993) A possible family of B-like triple helix structures: comparison with the Arnott A-like triple helix. Biochemistry, 32, 2098-2103.
30. Hsiang,Y.H., Hertzberg,R., Hecht,S. and Liu,L.F. (1985) Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I. J. Biol. Chem., 260, 14873-14878.
31. Tanizawa,A., Kohn,K.W., Kohlhagen,G., Leteurtre,F. and Pommier,Y. (1995) Differential stabilization of eukaryotic DNA topoisomerase I cleavable complexes by camptothecin derivatives. Biochemistry, 34, 7200-7206.
32. Pourquier,P. and Pommier,Y. (2001) Topoisomerase I-mediated DNA damage. Adv. Cancer Res., 80, 189-216.
33. Wang,X., Henningfeld,K.A. and Hecht,S.M. (1998) DNA topoisomerase I-mediated formation of structurally modified DNA duplexes. Effects of metal ions and topoisomerase I inhibitors. Biochemistry, 37, 2691-2700.
34. Cheng,C. and Shuman,S. (2000) Recombinogenic flap ligation pathway for intrinsic repair of topoisomerase IB-induced double-strand breaks. Mol. Cell. Biol., 20, 8059-8068.
35. Sekiguchi,J., Cheng,C. and Shuman,S. (1997) Kinetic analysis of DNA and RNA strand transfer reactions catalyzed by vaccinia topoisomerase. J. Biol. Chem., 272, 15721-15728.
36. Yakovleva,L., Tian,L., Sayer,J.M., Kalena,G.P., Kroth,H., Jerina,D.M. and Shuman,S. (2003) Site-specific DNA transesterification by vaccinia topoisomerase: effects of benzo[alpha]pyrene-dA, 8-oxoguanine, 8-oxoadenine and 2-aminopurine modifications. J. Biol. Chem., 278, 42170-42177.
37. Redinbo,M.R., Champoux,J.J. and Hol,W.G. (2000) Novel insights into catalytic mechanism from a crystal structure of human topoisomerase I in complex with DNA. Biochemistry, 39, 6832-6840.
38. Stewart,L., Redinbo,M.R., Qiu,X., Hol,W.G. and Champoux,J.J. (1998) A model for the mechanism of human topoisomerase I. Science, 279, 1534-1541.
39. Redinbo,M.R., Stewart,L., Champoux,J.J. and Hol,W.G. (1999) Structural flexibility in human topoisomerase I revealed in multiple non-isomorphous crystal structures. J. Mol. Biol., 292, 685-696.
40. Liao,S., Mao,C., Birktoft,J.J., Shuman,S. and Seeman,N.C. (2004) Resolution of undistorted symmetric immobile DNA junctions by vaccinia topoisomerase I. Biochemistry, 43, 1520-1531.
41. Arimondo,P.B., Riou,J.F., Mergny,J.L., Tazi,J., Sun,J.S., Garestier,T. and Hélène,C. (2000) Interaction of human DNA topoisomerase I with G-quartet structures. Nucleic Acids Res., 28, 4832-4838.
42. Marchand,C., Pourquier,P., Laco,G.S., Jing,N. and Pommier,Y. (2002) Interaction of human nuclear topoisomerase I with guanosine quartet-forming and guanosine-rich single-stranded DNA and RNA oligonucleotides. J. Biol. Chem., 277, 8906-8911.
43. Bonven,B.J., Gocke,E. and Westergaard,O. (1985) A high affinity topoisomerase I binding sequence is clustered at DNAase I hypersensitive sites in Tetrahymena R-chromatin. Cell, 41, 541-551.
44. Pourquier,P., Pilon,A.A., Kohlhagen,G., Mazumder,A., Sharma,A. and Pommier,Y. (1997) 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., 272, 26441-26447.
45. Arimondo,P.B., Bailly,C., Boutorine,A.S., Moreau,P., Prudhomme,M., Sun,J.S., Garestier,T. and Hélène,C. (2001) Triple helix-forming oligonucleotides conjugated to indolocarbazole poisons direct topoisomerase I-mediated DNA cleavage to a specific site. Bioconjug. Chem., 12, 501-509.
46. Laco,G.S., Collins,JR., Luke,B.T., Kroth,H., Sayer,J.M., Jerina,D.M. and Pommier,Y. (2002) Human topoisomerase I inhibition: docking camptothecin and derivatives into a structure-based active site model. Biochemistry, 41, 1428-1435.
47. Plum,G.E. and Breslauer,K.J. (1995) Thermodynamics of an intramolecular DNA triple helix: a calorimetric and spectroscopic study of the pH and salt dependence of thermally induced structural transitions. J. Mol. Biol., 248, 679-695.
48. Kjeldsen,E., Svejstrup,J.Q., Gromova,I.I., Alsner,J. and Westergaard,O. (1992) Camptothecin inhibits both the cleavage and religation reactions of eukaryotic DNA topoisomerase I. J. Mol. Biol. 228, 1025-1030.
49. Jaxel,C., Kohn,K.W. and Pommier,Y. (1988) Topoisomerase I interaction with SV40 DNA in the presence and absence of camptothecin. Nucleic Acids Res., 16, 11157-11170.
50. Pommier,Y., Kohlhagen,G., Pourquier,P., Sayer,J.M., Kroth,H. and Jerina,D.M. (2000) 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. USA 97, 2040-2045.
51. Cassidy,S.A., Strekowski,L., Wilson,W.D. and Fox,K.R. (1994) Effect of a triplex-binding ligand on parallel and antiparallel DNA triple helices using short unmodified and acridine-linked oligonucleotides. Biochemistry, 33, 15338-15347.
52. Krogh,S., Mortensen,U.H., Westergaard,O. and Bonven,B.J. (1991) Eukaryotic topoisomerase I-DNA interaction is stabilized by helix curvature. Nucleic Acids Res., 19, 1235-1241.
53. Htun,H. and Dahlberg,J.E. (1989) Topology and formation of triple-stranded H-DNA. Science, 243, 1571-1576.