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PMID: 12711735 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

DNA relaxation by human topoisomerase I occurs in the closed clamp conformation of the protein.

Carey JF, Schultz SJ, Sisson L, Fazzio TG, Champoux JJ

Abstract

In cocrystal structures of human topoisomerase I and DNA, the enzyme is tightly clamped around the DNA helix. After cleavage and covalent attachment of the enzyme to the 3' end at the nick, DNA relaxation requires rotation of the DNA helix downstream of the cleavage site. Models based on the cocrystal structure reveal that there is insufficient space in the protein for such DNA rotation without some deformation of the cap and linker regions of the enzyme. Alternatively, it is conceivable that the protein clamp opens to facilitate the rotation process. To distinguish between these two possibilities, we engineered two cysteines into the opposing loops of the "lips" region of the enzyme, which allowed us to lock the protein via a disulfide crosslink in the closed conformation around the DNA. Importantly, the rate of DNA relaxation when the enzyme was locked on the DNA was comparable to that observed in the absence of the disulfide crosslink. These results indicate that DNA relaxation likely proceeds without extensive opening of the enzyme clamp.

MeSH Terms
Amino Acid Substitution Centrifugation, Density Gradient DNA/chemistry,metabolism DNA Topoisomerases, Type I/chemistry,genetics,isolation & purification,metabolism Humans Kinetics Models, Molecular Mutagenesis, Site-Directed Nucleic Acid Conformation Plasmids Protein Conformation Recombinant Proteins/chemistry,isolation & purification,metabolism
Chemicals
Recombinant Proteins DNA DNA Topoisomerases, Type I
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Carey James F
Department of Microbiology, School of Medicine, University of Washington, Seattle, WA 98195, USA.
Schultz Sharon J
Sisson Lisa
Fazzio Thomas G
Champoux James J
References (19)
19 references, click to expand
  1. DNA topoisomerase I-mediated nicking of circular duplex DNA.
    Methods Mol Biol. 2001;95:81-7 PMID: 11089222
  2. Probing the two-gate mechanism of DNA gyrase using cysteine cross-linking.
    Biochemistry. 1999 Oct 12;38(41):13502-11 PMID: 10521257
  3. DNA topoisomerases: structure, function, and mechanism.
    Annu Rev Biochem. 2001;70:369-413 PMID: 11395412
  4. Cellular roles of DNA topoisomerases: a molecular perspective.
    Nat Rev Mol Cell Biol. 2002 Jun;3(6):430-40 PMID: 12042765
  5. Conformational fluctuations of DNA helix.
    Proc Natl Acad Sci U S A. 1975 Nov;72(11):4275-9 PMID: 172901
  6. Action of nicking-closing enzyme on supercoiled and nonsupercoiled closed circular DNA: formation of a Boltzmann distribution of topological isomers.
    Proc Natl Acad Sci U S A. 1975 Nov;72(11):4280-4 PMID: 1060106
  7. Strand breakage by the DNA untwisting enzyme results in covalent attachment of the enzyme to DNA.
    Proc Natl Acad Sci U S A. 1977 Sep;74(9):3800-4 PMID: 198805
  8. The anatomy and taxonomy of protein structure.
    Adv Protein Chem. 1981;34:167-339 PMID: 7020376
  9. Disulphide bridges in globular proteins.
    J Mol Biol. 1981 Sep 15;151(2):261-87 PMID: 7338898
  10. Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I.
    J Biol Chem. 1985 Nov 25;260(27):14873-8 PMID: 2997227
  11. The basis for camptothecin enhancement of DNA breakage by eukaryotic topoisomerase I.
    Nucleic Acids Res. 1989 Nov 11;17(21):8521-32 PMID: 2555774
  12. The domain organization of human topoisomerase I.
    J Biol Chem. 1996 Mar 29;271(13):7602-8 PMID: 8631794
  13. DNA transport by a type II topoisomerase: direct evidence for a two-gate mechanism.
    Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):4057-62 PMID: 8633016
  14. DNA topoisomerases.
    Annu Rev Biochem. 1996;65:635-92 PMID: 8811192
  15. Reconstitution of human topoisomerase I by fragment complementation.
    J Mol Biol. 1997 Jun 13;269(3):355-72 PMID: 9199405
  16. Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA.
    Science. 1998 Mar 6;279(5356):1504-13 PMID: 9488644
  17. A model for the mechanism of human topoisomerase I.
    Science. 1998 Mar 6;279(5356):1534-41 PMID: 9488652
  18. Structural insights into the function of type IB topoisomerases.
    Curr Opin Struct Biol. 1999 Feb;9(1):29-36 PMID: 10047584
  19. The mechanism of type IA topoisomerase-mediated DNA topological transformations.
    Mol Cell. 2001 Feb;7(2):301-7 PMID: 11239459
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2003-05-13
Epub
2003-00-23
Pages
5640-5
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC156254
Subset
IM
Grants
NIGMS NIH HHS · R01 GM060330 · United States
NIGMS NIH HHS · GM60330 · United States
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