Eukaryotic Topoisomerase I-DNA Interaction is Stabilized by Helix Curvature

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 1991 Mar 25

PMID 1851553

Citations 14

Authors

S Krogh

U H Mortensen

O Westergaard

B J Bonven

Affiliations

Soon will be listed here.

Abstract

The influence of DNA structure on topoisomerase I-DNA interaction has been investigated using a high affinity binding site and mutant derivatives thereof. Parallel determinations of complex formation and helix structure in the absence of superhelical stress suggest that the interaction is intensified by stable helix curvature. Previous work showed that a topoisomerase I binding site consists of two functionally distinct subdomains. A region located 5' to the topoisomerase I cleavage site is essential for binding. The region 3' to the cleavage site is covered by the enzyme, but not essential. We report here that the helix conformation of the latter region is an important modulator of complex formation. Thus, complex formation is markedly stimulated, when an intrinsically bent DNA segment is installed in this region. A unique pattern of phosphate ethylation interferences in the 3'-part of the binding site indicates that sensing of curvature involves backbone contacts. Since dynamic curvature in supercoiled DNA may substitute for stable curvature, our findings suggest that topoisomerase I is able to probe DNA topology by assessment of writhe, rather than twist.

Citing Articles

Tricking enzymes in living cells: a mechanism-based strategy for design of DNA topoisomerase biosensors.

Ba S, Gao G, Li T, Zhang H J Nanobiotechnology. 2021; 19(1):407.

PMID: 34876137 PMC: 8650243. DOI: 10.1186/s12951-021-01155-1.

Mapping topoisomerase sites in mitochondrial DNA with a poisonous mitochondrial topoisomerase I (Top1mt).

Dalla Rosa I, Huang S, Agama K, Khiati S, Zhang H, Pommier Y J Biol Chem. 2014; 289(26):18595-602.

PMID: 24798329 PMC: 4140277. DOI: 10.1074/jbc.M114.555367.

The stability of a model substrate for topoisomerase 1-mediated DNA religation depends on the presence of mismatched base pairs.

Gmeiner W, Salsbury Jr F, Olsen C, Marky L J Nucleic Acids. 2011; 2011:631372.

PMID: 21904666 PMC: 3166759. DOI: 10.4061/2011/631372.

A functional type I topoisomerase from Pseudomonas aeruginosa.

Jain T, Roper B, Grove A BMC Mol Biol. 2009; 10:23.

PMID: 19317906 PMC: 2666729. DOI: 10.1186/1471-2199-10-23.

Topoisomerase I-mediated DNA cleavage induced by the minor groove-directed binding of bibenzimidazoles to a distal site.

Khan Q, Pilch D J Mol Biol. 2006; 365(3):561-9.

PMID: 17095016 PMC: 1849979. DOI: 10.1016/j.jmb.2006.10.032.

References

Jordan S, Pabo C . Structure of the lambda complex at 2.5 A resolution: details of the repressor-operator interactions. Science. 1988; 242(4880):893-9. DOI: 10.1126/science.3187530. View

Bresloff J, Crothers D . Equilibrium studies of ethidium--polynucleotide interactions. Biochemistry. 1981; 20(12):3547-53. DOI: 10.1021/bi00515a038. View

Liu L, Wang J . Supercoiling of the DNA template during transcription. Proc Natl Acad Sci U S A. 1987; 84(20):7024-7. PMC: 299221. DOI: 10.1073/pnas.84.20.7024. View

Goodman S, NASH H . Functional replacement of a protein-induced bend in a DNA recombination site. Nature. 1989; 341(6239):251-4. DOI: 10.1038/341251a0. View

Rose K, Szopa J, Han F, Cheng Y, Richter A, Scheer U . Association of DNA topoisomerase I and RNA polymerase I: a possible role for topoisomerase I in ribosomal gene transcription. Chromosoma. 1988; 96(6):411-6. DOI: 10.1007/BF00303034. View

Zhang H, Wang J, Liu L . Involvement of DNA topoisomerase I in transcription of human ribosomal RNA genes. Proc Natl Acad Sci U S A. 1988; 85(4):1060-4. PMC: 279701. DOI: 10.1073/pnas.85.4.1060. View

Wu H, Shyy S, Wang J, Liu L . Transcription generates positively and negatively supercoiled domains in the template. Cell. 1988; 53(3):433-40. DOI: 10.1016/0092-8674(88)90163-8. View

Ness P, Koller T, Thoma F . Topoisomerase I cleavage sites identified and mapped in the chromatin of Dictyostelium ribosomal RNA genes. J Mol Biol. 1988; 200(1):127-39. DOI: 10.1016/0022-2836(88)90338-5. View

Camilloni G, Di Martino E, Caserta M, Di Mauro E . Eukaryotic DNA topoisomerase I reaction is topology dependent. Nucleic Acids Res. 1988; 16(14B):7071-85. PMC: 338352. DOI: 10.1093/nar/16.14.7071. View

10.

Linial M, Shlomai J . Sequence-directed bent DNA helix is the specific binding site for Crithidia fasciculata nicking enzyme. Proc Natl Acad Sci U S A. 1987; 84(23):8205-9. PMC: 299510. DOI: 10.1073/pnas.84.23.8205. View

11.

Maxwell A, Gellert M . Mechanistic aspects of DNA topoisomerases. Adv Protein Chem. 1986; 38:69-107. DOI: 10.1016/s0065-3233(08)60526-4. View

12.

Ryder K, Silver S, DeLucia A, Fanning E, Tegtmeyer P . An altered DNA conformation in origin region I is a determinant for the binding of SV40 large T antigen. Cell. 1986; 44(5):719-25. DOI: 10.1016/0092-8674(86)90838-x. View

13.

Gilmour D, PFLUGFELDER G, Wang J, Lis J . Topoisomerase I interacts with transcribed regions in Drosophila cells. Cell. 1986; 44(3):401-7. DOI: 10.1016/0092-8674(86)90461-7. View

14.

Burkhoff A, Tullius T . The unusual conformation adopted by the adenine tracts in kinetoplast DNA. Cell. 1987; 48(6):935-43. DOI: 10.1016/0092-8674(87)90702-1. View

15.

Busk H, Thomsen B, Bonven B, Kjeldsen E, Nielsen O, Westergaard O . Preferential relaxation of supercoiled DNA containing a hexadecameric recognition sequence for topoisomerase I. Nature. 1987; 327(6123):638-40. DOI: 10.1038/327638a0. View

16.

Thomsen B, Mollerup S, Bonven B, Frank R, Blocker H, Nielsen O . Sequence specificity of DNA topoisomerase I in the presence and absence of camptothecin. EMBO J. 1987; 6(6):1817-23. PMC: 553560. DOI: 10.1002/j.1460-2075.1987.tb02436.x. View

17.

Gilmour D, Elgin S . Localization of specific topoisomerase I interactions within the transcribed region of active heat shock genes by using the inhibitor camptothecin. Mol Cell Biol. 1987; 7(1):141-8. PMC: 365050. DOI: 10.1128/mcb.7.1.141-148.1987. View

18.

Muller M . Quantitation of eukaryotic topoisomerase I reactivity with DNA. Preferential cleavage of supercoiled DNA. Biochim Biophys Acta. 1985; 824(3):263-7. DOI: 10.1016/0167-4781(85)90057-0. View

19.

Bonven B, Gocke E, Westergaard O . A high affinity topoisomerase I binding sequence is clustered at DNAase I hypersensitive sites in Tetrahymena R-chromatin. Cell. 1985; 41(2):541-51. DOI: 10.1016/s0092-8674(85)80027-1. View

20.

Vosberg H . DNA topoisomerases: enzymes that control DNA conformation. Curr Top Microbiol Immunol. 1985; 114:19-102. DOI: 10.1007/978-3-642-70227-3_2. View