Tryptophane-205 of human topoisomerase I is essential for camptothecin inhibition of negative but not positive supercoil removal

Nucleic Acids Research

Volumn 35, Issue 18, 2007, Pages 6170-6180

  Frøhlich, Rikke From ^a   Veigaard, Christopher ^a,c   Andersen, Félicie Faucon ^a   Mcclendon, A Kathleen ^b   Gentry, Amanda C ^b   Andersen, Anni Hangaard ^a   Osheroff, Neil ^b   Stevnsner, Tinna ^a   Knudsen, Birgitta Ruth ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CAMPTOTHECIN; DNA TOPOISOMERASE; TRYPTOPHAN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; DNA STRAND; DNA SUPERCOILING; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME STRUCTURE; HUMAN; MUTANT; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; SIMULATION; WILD TYPE;

CAMPTOTHECIN; DNA TOPOISOMERASES, TYPE I, EUKARYOTIC; DNA, SUPERHELICAL; ENZYME INHIBITORS; HUMANS; KINETICS; MUTATION; PLASMIDS; TRYPTOPHAN;

EID: 35548983057     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm669     Document Type: Article

References (36)

1. Brill,S.J., DiNardo,S., Voelkel-Meiman,K. and Sternglanz,R. (1987) Need for DNA topoisomerase activity as a swivel for DNA replication for transcription of ribosomal RNA. Nature, 326, 414-416.
2. Brill,S.J. and Sternglanz,R. (1988) Transcription-dependent DNA supercoiling in yeast DNA topoisomerase mutants. Cell, 54, 403-411.
3. Liu,L.F. and Wang,J.C. (1987) Supercoiling of the DNA template during transcription. Proc. Natl Acad. Sci. USA, 84, 7024-7027.
4. Wang,J.C. (2002) Cellular roles of DNA topoisomerases: A molecular perspective. Nat. Rev. Mol. Cell. Biol., 3, 430-440.
5. Shuman,S. (1998) Vaccinia virus DNA topoisomerase: A model eukaryotic type IB enzyme. Biochim. Biophys. Acta, 1400, 321-337.
6. Champoux,J.J. and Dulbecco,R. (1972) An activity from mammalian cells that untwists superhelical DNA - a possible swivel for DNA replication (polyoma-ethidium bromide-mouse-embryo cells-dye binding assay). Proc. Natl Acad. Sci. USA, 69, 143-146.
7. Camilloni,G., Di Martino,E., Caserta,M. and di Mauro,E. (1988) Eukaryotic DNA topoisomerase I reaction is topology dependent. Nucleic Acids Res., 16, 7071-7085.
8. Camilloni,G., Di Martino,E., Di Mauro,E. and Caserta,M. (1989) Regulation of the function of eukaryotic DNA topoisomerase I: topological conditions for inactivity. Proc. Natl Acad. Sci. USA, 86, 3080-3084.
9. Leppard,J.B. and Champoux,J.J. (2005) Human DNA topoisomerase I: relaxation, roles, and damage control. Chromosoma, 114, 75-85.
10. Champoux,J.J. (2001) DNA topoisomerases: Structure, function, and mechanism. Annu. Rev. Biochem., 70, 369-413.
11. Kaster,D.A., Palle,K., Bot,E.S., Bjornsti,M.A. and Dekker,N.H. (2007) Antitumour drugs impede DNA uncoiling by topoisomerase I. Nature, 448, 213-217.
12. Koster,D.A., Croquette,V., Dekker,C., Shuman,S. and Dekker,N.H. (2005) Friction and torque govern the relaxation of DNA supercoils by eukaryotic topoisomerase IB. Nature, 434, 671-674.
13. 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.
14. Redinbo,M.R., Champoux,J.J. and Hol,W.G. (1999) Structural insights into the function of type IB topoisomerases. Curr. Opin. Struct. Biol., 9, 29-36.
15. Redinbo,M.R., Stewart,L., Kuhn,P., Champoux,J.J. and Hol,W.G. (1998) Crystal structures of human topoisomerase I in covalent and poncovalent complexes with DNA. Science, 279, 1504-1513.
16. Stewart,L., Ireton,G.C. and Champoux,J.J. (1999) A functional linker in human topoisomerase I is required for maximum sensitivity to camptothecin in a DNA relaxation assay. J. Biol. Chem., 274, 32950-32960.
17. Lisby,M., Olesen,J.R., Skouboe,C., Krogh,B.O., Straub,T., Boege,V., Velmurugan,S., Martensen,P.M., Andersen,A.H. et al. (2001) Residues within the N-terminal domain of human topoisomerase I play a direct role in relaxation. J. Biol. Chem., 276, 20220-20227.
18. McClendon,A.K. and Osheroff,N. (2006) The geometry of DNA supercoils modulates topoisomerase-mediated DNA cleavage and enzyme response to anticancer drugs. Biochemistry, 45, 3040-3050.
19. McClendon,A.K., Rodriguez,A.C. and Osheroff,N. (2005) Human topoisomerase IIalpha rapidly relaxes positively supercoiled DNA: implications for enzyme action ahead of replication forks. J. Biol. Chem., 280, 39337-39345.
20. Sari,L. and Andricioaei,I. (2005) Rotation of DNA around intact strand in human topoisomerase I implies distinct mechanisms for positive and negative supercoil relaxation. Nucleic Acids Res., 33, 6621-6634.
21. Stewart,L., Ireton,G.C. and Champoux,J.J. (1996) The domain organization of human topoisomerase I. J. Biol. Chem., 271, 7602-76081.
22. Stewart,L., Ireton,G.C., Parker,L.H., Madden,K.R. and Champoux,J.J. (1996) Biochemical and biophysical analyses of recombinant forms of human topoisomerase I. J. Biol. Chem., 271, 7593-7601.
23. 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.
24. 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 stryctures. J. Mol. Biol., 292, 685-696.
25. Staker,B.L., Hjerrild,K., Feese,M.D., Behnke,C.A., Burgin,A.B.Jr and Stewart,L. (2002) The mechanism of topoisomerase I poisoning by a camptothecin analog. Proc. Natl Acad. Sci. USA., 99, 15387-15392.
26. Frohlich,R.F., Andersen,F.F., Westergaard,O., Andersen,A.H. and Knudsen,B.R. (2004) Regions within the N-terminal domain of human topoisomerase I exert important functiong during strand rotation and DNA binding. J. Mol. Biol., 336, 93-103.
27. Carey,J.F., Schultz,S.J., Sisson,L., Fazzio,T.G. and Champoux,J.J. (2003) DNA relaxation by human topoisomerase I occurs in the closed clamp conformation of the protein. Proc. Natl Acad. Sci. USA, 100, 5640-5645.
28. Woo,M.H., Losasso,C., Guo,H., Pattarello,L., Benedetti,P. and Bjornsti,M.A. (2003) Locking the DNA topoisomerase I protein clamp inhibits DNA rotation and induces cell lethality. Proc. Natl Acad. Sci. USA, 100 13767-13772.
29. McConaughy,B.L., Young,L.S. and Champoux,J.J. (1981) The effect of salt on the binding of the eucaryotic DNA nicking-closing enzyme to DNA and chromatin. Biochim. Biophys. Acta, 655, 1-8.
30. Postow,L., Crisona,N.J., Peter,B.J., Hardy,C.D. and Cozzarelli,N.R. (2001) Topological challenges to DNA replication: Conformations at the fork. Proc. Natl Acad. Sci. USA, 98, 8219-822.
31. Mondal,N., Zhang,Y., Jonsson,Z., Dhar,S.K., Kannapiran,M. and Parvin,J.D. (2003) Elongation by RNA polymerase II on chromatin templates requires topoisomerase activity. Nucleic Acids Res., 31, 5016-5024.
32. Salceda,J., Fernandez,X. and Roca,J. (2006) Topoisomerase II, not topoisomerase I, is the proficient relaxase of nucleosomal DNA. EMBO J., 25, 2575-2583.
33. Hsiang,Y.H., Lihou,M.G. and Liu,L.F. (1989) Arrest of replication forks by drug-stabilized topoisomerase I-DNA cleavable complexes as a mechanism of cell killing by camptothecin. Cancer Res., 49, 5077-5082.
34. Pommier,Y., Redon,C., Rao,V.A., Seiler,J.A., Sordet,O., Takemura,H., Antony,S., Meng,L., Liao,Z. et al. (2003) Repair of and checkpoint response to topoisomerase I-mediated DNA damage. Mutat. Res., 532, 173-203.
35. Strumberg,D., Pilon,A.A., Smith,M., Hickey,R., Malkas,L. and Pommier,Y. (2000) 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., 20, 3977-3987.
36. Staker,B.L., Feese,M.D., Cushman,M., Pommier,Y., Zembower,D., Stewart,L. and Burgin,A.B. (2005) Structures of three classes of anticancer agents bound to the human topoisomerase I-DNA covalent complex. J. Med. Chem., 48, 2336-2345.