Conversion of topoisomerase I cleavage complexes on the leading strand of ribosomal DNA into 5'-phosphorylated DNA double-strand breaks by replication runoff

Molecular and Cellular Biology

Volumn 20, Issue 11, 2000, Pages 3977-3987

  Strumberg, Dirk ^a,c   Pilon, André A ^a   Smith, Melanie ^b   Hickey, Robert ^b   Malkas, Linda ^b   Pommier, Yves ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CAMPTOTHECIN; DNA TOPOISOMERASE; DOUBLE STRANDED DNA; RIBOSOME DNA;

ARTICLE; CARCINOMA CELL; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA SEQUENCE; DNA STRAND BREAKAGE; ENZYME ACTIVITY; GENE CLUSTER; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; TRANSCRIPTION TERMINATION;

CAMPTOTHECIN; DNA; DNA DAMAGE; DNA REPLICATION; DNA TOPOISOMERASES, TYPE I; DNA, RIBOSOMAL; DNA, SINGLE-STRANDED; ENZYME INHIBITORS; HT29 CELLS; HUMANS; KINETICS; MULTIGENE FAMILY; PHOSPHORYLATION;

EID: 0034124053     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.11.3977-3987.2000     Document Type: Article

References (75)

1. Andersen, R. D., and N. A. Berger. 1994. Mutagenicity and cardnogenicity of topoisomerase-interactive drugs. Mutat. Res. 309:109-142.
2. Avemann, K., R. Knippers, T. Koller, and J. M. Sogo. 1988. Camptothecin, a specific inhibitor of type I DNA topoisomerase. induces DNA breakage at replication forks. Mol. Cell. Biol. 8:3026-3034.
3. Baker, S. D., R. M. Wadkins, C. F. Stewart, W. T. Beck, and M. K. Danks. 1995. Cell cycle analysis of amount and distribution of nuclear DNA topoisomerase I as determined by fluorescence digital imaging microscopy. Cytometry 19:134-145.
4. Bendixen, C., B. Thomsen, J. Alsner, and O. Westergaard. 1990. Camptothecin-stabilized topoisomerase I-DNA adducts cause premature termination of transcription. Biochemistry 29:5613-5619.
5. Bennett, C. B., T. J. Westmorland, J. R. Snipe, and M. A. Kesnick. 1996. A double-strand break within a yeast artificial chromosome (YAC) containing human DNA can result in YAC loss, deletion, or cell lethality. Mol. Cell. Biol. 16:4414-4425.
6. Brush, G. S., and T. J. Kelly. 1996. Mechanisms for replicating DNA. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
7. Buckwalter, C. A., A. H. Lin, A. Tanizawa, Y. G. Pommier, Y. C. Cheng, and S. H. Kaufmann. 1996. RNA synthesis inhibitors alter the subnuclear distribution of DNA topoisomerase I. Cancer Res. 56:1674-1681.
8. Bullock, P., J. J. Champoux, and M. Botchan. 1985. Association of crossover points with topoisomerase I cleavage sites: a model for nonhomologous recombination. Science 230:954-958.
9. Champoux, J. J., W. K. McCoubrey, Jr., and M. D. Been. 1984. DNA structural features that lead to strand breakage by eukaryotic type-I topoisomerase. Cold Spring Harbor Symp. Quant. Biol. 49:435-442.
10. Chen, C. L., J. C. Fuscoe, Q. Liu, C. H. Pui, H. H. Mahmoud, and M. V. Relling. 1996. Relationship between cytotoxicity and site-specific DNA recombination after in vitro exposure of leukemia cells to etoposide. J. Natl. Cancer Inst. 88:1840-1847.
11. Christiansen, K., A. B. Svejstrup, A. H. Andersen, and O. Westergaard. 1993. Eukaryotic topoisomerase I-mediated cleavage requires bipartite DNA interaction. Cleavage of DNA substrates containing strand interruptions implicates a role for topoisomerase I in illegitimate recombination. J. Biol. Chem. 268:9690-9701.
12. Cimmino, C., F. Santori, and P. Donini. 1995. Ligation of nonmatching DNA molecule ends. Plasmid 34:1-10.
13. Covey, J. M., C. Jaxel, K. W. Kohn, and Y. Pommier. 1989. Protein-linked DNA strand breaks induced in mammalian cells by camptothecin, an inhibitor of topoisomerase I. Cancer Res. 49:5016-5022.
14. Culotta, V., and B. Sollner-Wenb. 1988. Sites of topoisomerase I action on X. laevis ribosomal chromatin: transcriptionally active rDNA has an approximately 200 bp repeating structure. Cell 52:585-597.
15. Danks, M. K., K. E. Garrett, R. C. Marion, and D. O. Whipple. 1996. Subcellular redistribution of DNA topoisomerase I in anaplaslic astrocytoma cells treated with topotecan. Cancer Res. 56:1664-1673.
16. D'Arpa, P., C. Beardmore, and L. F. Liu. 1990. Involvement of nucleic acid synthesis in cell killing mechanisms of topoisomerase poisons. Cancer Res. 50:6919-6924.
17. Eng, W. K., L. Faucette, R. K. Johnson, and R. Sternglanz. 1988. Evidence that DNA topoisomerase I is necessary for the cytotoxic effects of camptothecin. Mol. Pharmacol. 34:755-760.
18. Gencheva, M., B. Anachkova, and G. Russev. 1996. Mapping the sites of initiation of DNA replication in rat and human rRNA genes. J. Biol. Chem. 271:2608-2614.
19. Gerber, J. K., E. Gogel, C. Berger, M. Wallisch, F. Muller, I. Grummt, and F. Grummt. 1997. Termination of mammalian rDNA replication: polar arrest of replication fork movement by transcription termination factor TTF-I. Cell 90:559-567.
20. Gilmour, D. S., G. Pflugfelder, J. C. Wang, and J. T. Lis. 1986. Topoisomerase I interacts with transcribed regions in Drosophila cells. Cell 44:401-407.
21. Gonzalez, I. L., and J. E. Sylvester. 1995. Complete sequence of the 43-kb human ribosomal DNA repeat: analysis of the intergenic spacer. Genomics 27:320-328.
22. Gupta, M., A. Fujimori, and Y. Pommier. 1995. Eukaryotic DNA topoisomerases I. Biochim. Biophys. Acta 1262:1-14.
23. Hernandez, P., L. Martin-Parras, M. L. Martinez-Robles, and J. B. Schvartzman. 1993. Conserved features in the mode of replication of eukaryotic ribosomal RNA genes. EMBO J. 12:1475-1485.
24. Holm, C., J. M. Covey, D. Kerrigan, and Y. Pommier. 1989. Differential requirement of DNA replication for the cytotoxicity of DNA topoisomerase I and II inhibitors in Chinese hamster DC3F cells. Cancer Res. 49:6365-6368.
25. Hsiang, Y. H., R. Hertzberg, S. Hecht, and L. F. Liu. 1985. Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I. J. Biol. Chem. 260:14873-14878.
26. Hsiang, Y. H., M. G. Lihou, and L. F. Liu. 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.
27. Lanza, A., S. Tornaletti, C. Rodolfo, M. C. Scanavini, and A. M. Pedrini. 1996. Human DNA topoisomerase I-mediated cleavages stimulated by ultraviolet light-induced DNA damage. J. Biol. Chem. 271:6978-6986.
28. Little, R. D., T. H. Platt, and C. L. Schildkraut. 1993. Initiation and termination of DNA replication in human rRNA genes. Mol. Cell. Biol. 13:6600-6613.
29. Liu, L. F., P. Duann, C. T. Lin, P. D'Arpa, and J. Wu. 1996. Mechanism of action of camptothecin. Ann. N.Y. Acad. Sci. 803:44-49.
30. Maxam, A. M., and W. Gilbert. 1980. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 65:499-560.
31. Meyer, K. N, E. Kjeldsen. T. Straub, B. K. Knudsen, I. D. Hickson, A. Kikuchi, H. Kreipe, and F. Boege. 1997. Cell cycle-coupled relocation of type I and II topoisomerases and modulation of catalytic enzyme activities. J. Cell Biol. 136:775-788.
32. Mueller, P. R., P. A. Garrity, and B. Wold. 1992. Ligation-mediated PCR, p. 15.5.1-15.5.26. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seideman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology. John Wiley & Sons, Inc., New York, N.Y.
33. Muller, M. T., W. P. Ptund, V. B. Mehta, and D. K. Trask. 1985 Eukaryotic type I topoisomerase is enriched in the nucleolus and catalytically active on ribosomal DNA. EMBO J. 4:1237-1243.
34. Nitiss, J. L. 1998. Investigating the biological functions of DNA topoisomerases in eukaiyotic cells. Biochim. Biophys. Acta 1400:63-81.
35. Osman, F., E. A. Fortunate, and S. Subramani. 1996. Double-strand breakinduced mitotic intrachromosomal recombination in the fission yeast Schizosaccharomyces pombe. Genetics 142:341-357.
36. Pommier, Y., J. Jenkim, G. Kohlhagen, and F. Leteurtre. 1995. DNA recombinase activity of eukaryotic DNA topoisomerase I: effects of camptothecin and other inhibitors. Mutat. Res. 337:135-145.
37. Pommier, Y., G. Kohlhagen, P. Pourquier, J. M. Sayer, H. Kroth, and D. M. Jerina. 2000. Benzo[a]pyrene epoxide adducts in DNA are potent inhibitors of a normal topoisomerase I cleavage site and powerful inducers of other topoisomerase I cleavages. Proc. Natl. Acad. Sci. USA 10:2040-2045.
38. Pommier, Y., G. Kohlhagen, C. Wu, and D. T. Simmons. 1998. Mammalian DNA topoisomerase I activity and poisoning by camptothecin are inhibited by simian virus 40 large T antigen. Biochemistry 37:3818-3823.
39. Pommier, Y., P. Pourquier, Y. Fan, and D. Strumberg. 1998. Mechanism of action of eukaryotic DMA topoisomerase I and drugs targeted to the enzyme. Biochim. Biophys. Acta 1400:83-105.
40. Pommier, Y., P. Pourquier, Y. Urasaki, J. Wu, and G. Laco. 1999. Topoisomerase I inhibitors: selectivity and cellular resistance. Drug Resistance Update 2:307-318.
41. Pondarré, C., D. Strumberg, A. Fujimori, R. Torres-Leon, and Y. Pommier. 1997. In vivo sequencing of camptothecin-induced topoisomerase I cleavage sites in human colon carcinoma cells. Nucleic Acids Res. 25:4111-4116.
42. Porter, S. E., and J. J. Champoux. 1989. The basis for camptothecin enhancement of DNA breakage by eukaryotic topoisomerase I. Nucleic Acids Res. 17:8521-8532.
43. Pouliot, J. J., K. C. Yao, C. A. Robertson, and H. A. Nash. 1999. Yeasl gene for a Tyr-DNA phosphodiesterase that repairs topo I covalent complexes. Science 286:552-555.
44. Pourquier, P., M. A. Bjomsli, and Y. Pommier. 1998. Induction of topoisomerase I cleavage complexes by the vinyl chloride adduct 1 ,N6-ethenoadenine. J. Biol. Chem. 273:27245-27249.
45. Pourquier, P., A. A. Pilon, G. Kohlhagen, A. Mazumder, A. Sharma, and Y. Pommier. 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.
46. Pourquier, P., Y. Takebayashi, Y. Urasaki, C. Gioffre, G. Kohlhagen, and Y. Pommier. 2000. Induction of topoisomerase I cleavage complexes by 1-β-D-arabinofuranosylcytosine (Ara-C) in vitro and in ara-C-treated cells. Proc. Natl. Acad. Sci. USA 97:1885-1890.
47. Pourquier, P., L. M. Ueng, J. Fertala, D. Wang, H. J. Park, J. M. Essigmann, M. A. Bjornsti, and Y. Pommier. 1999. Induction of reversible complexes between eukaryotic DNA topoisomerase I and DNA-containing oxidative base damages: 7,8-dihydro-8-oxoguanine and 5-hydroxycytosine. J. Biol. Chem. 274:8516-8523.
48. Pourquier, P., L. M. Ueng, G. Kohlhagen, A. Mazumder, M. Gupta, K. W. Kohn, and Y. Pommier. 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.
49. Redinbo, M. R-, L. Stewart, P. Kuhn, J. J. Champoux, and W. G. Hol. 1998. Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279:1504-1513.
50. Rosenstein, B. S., D. Subramanian, and M. T. Muller. 1997. The involvement of topoisomerase I in the induction of DNA-protein crosslinks and DNA single-strand breaks in cells of ultraviolet-irradiated human and frog cell lines. Radiat. Res. 148:575-579.
51. Ryan, A. J., S. Squires, H. L. Strutt, and R. T. Johnson. 1991. Camptothecin cytotoxicity in mammalian cells is associated with the induction of persistent double strand breaks in replicating DNA. Nucleic Acids Res. 19:3295-3300.
52. Sargent, R. G., M. A. Brenneman, and J. H. Wilson. 1997. Repair of site-specific double-strand breaks in a mammalian chromosome by homologous and illegitimate recombination. Mol. Cell. Biol. 17:267-277.
53. Sastry, S., and B. M. Ross. 1998. Mechanisms for the processing of a frozen topoisomerase-DNA conjugate by human cell-free extracts. J. Biol. Chem. 273:9942-9950.
54. Shan, Q., and M. M. Cox. 1998. On the mechanism of RecA-mediated repair of double-strand breaks: no role for four-strand DNA pairing intermediates. Mol. Cell 1:309-317.
55. Shao, R-G., C.-X. Cao, H. Zhang, K. W. Kohn, M. S. Wold, and Y. Pommier. 1999. Replication-mediated DNA damage by camptothecin induces phosphorylation of RPA by DNA-dependent protein kinase and dissociates RPA: DNA-PK complexes. EMBO J. 18:1397-1406.
56. Shin, C. G., and R. M. Snapka. 1990. Exposure to camptothecin breaks leading and lagging strand simian virus 40 DNA replication forks. Biochem. Biophys. Res. Commun. 168:135-140.
57. Shuman, S. 1992. DNA strand transfer reactions catalyzed by vaccinia topoisomerase I. J. Biol. Chem. 267:8620-8627.
58. Shuman, S. 1992. Two classes of DNA end-joining reactions catalyzed by vaccinia topoisomerase I. J. Biol. Chem. 267:16755-16758.
59. Snapka, R. M., and P. A. Permana. 1993. SV40 DNA replication intermediates: analysis of drugs which target mammalian DNA replication. Bioessays 15:121-127.
60. Squires, S., A. J. Ryan, H. L. Strutt, and R. T. Johnson. 1993. Hypersensitivity of Cockayne's syndrome cells to camptothecin is associated with the generation of abnormally high levels of double strand breaks in nascent DNA. Cancer Res. 53:2012-2019.
61. Stewart, L., M. R. Redinbo, X. Qiu, W. G. Hol, and J. J. Champoux. 1998. A model for the mechanism of human topoisomerase I. Science 279:1534-1541.
62. Subramanian, D., B. S. Rosenstein, and M. T. Muller. 1998. Ultraviolet-induced DNA damage stimulates topoisomerase I-DNA complex formation in vivo: possible relationship with DNA repair. Cancer Res. 58:976-984.
63. Svejstrup, J. Q., K. Christiansen, A. H. Andersen, K. Lund, and O. Westergaard. 1990. Minimal DNA duplex requirements for topoisomerase I-mediated cleavage in vitro. J. Biol. Chem. 265:12529-12535.
64. Svoboda, D. L., and J. M. Vos. 1995. Differential replication of a single, UV-induced lesion in the leading or lagging strand by a human cell extract: fork uncoupling or gap formation. Proc. Natl. Acad. Sci. USA 92:11975-11979.
65. Sylvester, J. E., R. Petersen, and R. D. Schmickel. 1989. Human ribosomal DNA: novel sequence organization in a 4.5-kb region upstream from the promoter. Gene 84:193-196.
66. Takebayashi, Y., P. Pourquier, A. Yoshida, G. Kohlhagen, and Y. Pommier. 1999. Poisoning of human DNA topoisomerase I by ecteinascidin 743, an anticancer drug that selectively alkylates DNA in the minor groove. Proc. Natl. Acad. Sci. USA 96:7196-7201.
67. Tanizawa, A., K. W. Kohn, G. Kohlhagen, F. Leteurtre, and Y. Pommier. 1995. Differential stabilization of eukaiyotic DNA topoisomerase I cleavable complexes by camptothecin derivatives. Biochemistry 34:7200-7206.
68. Tsao, Y. P., A. Russo, G. Nyamuswa, R. Silber, and L. F. Liu. 1993. Interaction between replication forks and topoisomerase I-DNA cleavable complexes: studies in a cell-free SV40 DNA replication system. Cancer Res. 53:5908-5914.
69. Tsukamoto, Y., and H. Ikeda. 1998. Double-strand break repair mediated by DNA end-joining. Genes Cells 3:135-144.
70. Veaute, X., and A. Sarasin. 1997. Differential replication of a single N-2-acetylaminofluorene lesion in the leading or lagging strand DNA in a human cell extract. J. Biol. Chem. 272:15351-15357.
71. Wang, J. C. 1996. DNA topoisomerases. Annu. Rev. Biochem. 65:635-692.
72. Wu, J., and L. F. Liu. 1997. Processing of topoisomerase I cleavable complexes into DNA damage by transcription. Nucleic Acids Res. 25:4181-4186.
73. Yeh, Y. C., H. F. Liu, C. A. Ellis, and A. L. Lu. 1994. Mammalian topoisomerase I has base mismatch nicking activity. J. Biol. Chem. 269:15498-15504.
74. Yoon, Y., J. A. Sanchez, C. Brun, and J. A. Huberman. 1995. Mapping of replication initiation sites in human ribosomal DNA by nascent-strand abundance analysis. Mol. Cell. Biol. 15:2482-2489.
75. Zhang, H., J. C. Wang, and L. F. Liu. 1988. Involvement of DNA topoisomerase I in transcription of human ribosomal RNA genes. Proc. Natl. Acad. Sci. USA 85:1060-1064.