A kinetic proofreading mechanism for disentanglement of DNA by topoisomerases (original) (raw)
- Letter
- Published: 28 October 1999
Nature volume 401, pages 932–935 (1999)Cite this article
- 983 Accesses
- 101 Citations
- Metrics details
Abstract
Cells must remove all entanglements between their replicated chromosomal DNAs to segregate them during cell division. Entanglement removal is done by ATP-driven enzymes that pass DNA strands through one another, called type II topoisomerases. In vitro, some type II topoisomerases can reduce entanglements much more than expected, given the assumption that they pass DNA segments through one another in a random way1. These type II topoisomerases (of less than 10 nm in diameter) thus use ATP hydrolysis to sense and remove entanglements spread along flexible DNA strands of up to 3,000 nm long. Here we propose a mechanism for this, based on the higher rate of collisions along entangled DNA strands, relative to collision rates on disentangled DNA strands. We show theoretically that if a type II topoisomerase requires an initial ‘activating’ collision before a second strand-passing collision, the probability of entanglement may be reduced to experimentally observed levels. This proposed two-collision reaction is similar to ‘kinetic proofreading’ models of molecular recognition2,3.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Additional access options:
Similar content being viewed by others
References
- Rybenkov,V. V., Ullsperger,C., Vologodskii,A. V. & Cozzarelli,N. R. Simplification of DNA topology below equilibrium values by type II topoisomerases. Science 277, 690–693 (1997).
Article CAS PubMed Google Scholar - Hopfield,J. J. Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proc. Natl Acad. Sci. USA 71, 4135–4139 (1974).
Article ADS CAS PubMed PubMed Central Google Scholar - Ninio,J. Kinetic amplification of enzyme discrimination. Biochimie 57, 587–595 (1975).
Article CAS PubMed Google Scholar - Frank-Kamenetskii,M. D., Lukashin,A. V. & Vologodskii,A. V. Statistical mechanics and topology of polymer chains. Nature 258, 398–402 (1975).
Article ADS CAS PubMed Google Scholar - Klenin,K. V., Vologodskii,A. V., Anshelevich,V. V., Dykhne,A. M. & Frank-Kamenetskii,M. D. Effect of excluded volume on topological properties of circular DNA. J. Biomol. Struct. Dyn. 5, 1173–1185 (1988).
Article CAS PubMed Google Scholar - Shaw,S. Y. & Wang,J. C. Knotting of a DNA chain during ring closure. Science 260, 533–536 (1993).
Article ADS CAS PubMed Google Scholar - Rybenkov,A. V., Cozzarelli,N. R. & Vologodskii,A. V. Probability of DNA knotting and the effective diameter of the DNA double helix. Proc. Natl Acad. Sci. USA 90, 5307–5311 (1993).
Article ADS CAS PubMed PubMed Central Google Scholar - Vologodskii,A. V. in RECOMB 98: Proceedings of the second annual international conference on computational molecular biology 266–269 (Association for Computing Machinery, New York, 1998).
Book Google Scholar - Deguchi,T. & Tsurusaki,K. A statistical study of random knotting using the Vassiliev invariants. J. Knot Theory Ramific. 3, 321–353 (1994).
Article MathSciNet MATH Google Scholar - Roca,J. & Wang,J. C. DNA transport by a type II DNA topoisomerase: evidence in favor of a two-gate mechanism. Cell 77, 609–616 (1994).
Article CAS PubMed Google Scholar - Roca,J. & Wang,J. C. The capture of a DNA double helix by an ATP-dependent protein clamp: a key step in DNA transport by type II DNA topoisomerases. Cell 71, 833–840 (1992).
Article CAS PubMed Google Scholar - Roca,J., Berger,J. M. & Wang,J. C. On the simultaneous binding of eukaryotic DNA topoisomerase II to a pair of double-stranded DNA helices. J. Biol. Chem. 268, 14250–14255 (1993).
Article CAS PubMed Google Scholar - Harkins,T. T. & Lindsley,J. E. Pre-steady-state analysis of ATP hydrolysis by Saccaromyces cerevisiae DNA topoisomerase II. 1. A DNA-dependent burst in ATP hydrolysis. Biochemistry 37, 7292–7299 (1998).
Article CAS PubMed Google Scholar - Harkins,T. T. & Lindsley,J. E. Pre-steady-state analysis of ATP hydrolysis by Saccaromyces cerevisiae DNA topoisomerase II. 2. Kinetic mechanism for the sequential hydrolysis of two ATP. Biochemistry 37, 7299–7312 (1998).
Article CAS PubMed Google Scholar - Worcel,A. & Burgi,E. On the structure of the folded chromosome of Escherichia coli. J. Mol. Biol. 71, 127–147 (1972).
Article CAS PubMed Google Scholar - Sinden,R. R. & Pettijohn,D. E. Chromosomes in living Escherichia coli cells are segregated into domains of supercoiling. Proc. Natl Acad. Sci. USA 78, 224–228 (1981).
Article ADS CAS PubMed PubMed Central Google Scholar
Acknowledgements
We thank D. Chatenay, N. R. Cozzarelli, G. B. Mindlin, V. Rybenkov, E. D. Siggia, A. V. Vologodskii and E. L. Zechiedrich for discussions. J.F.M. and J.Y. acknowledge the support of the NSF, the Research Corporation, the Petroleum Research Fund, and the Whitaker Foundation. M.O.M. acknowledges support of the Sloan Foundation and the Mathers Foundation.
Author information
Authors and Affiliations
- Department of Physics, The University of Illinois at Chicago, 845 West Taylor Street, Chicago, 60607, Illinois, USA
Jie Yan & John F. Marko - Center for Studies in Physics and Biology, The Rockefeller University, 1230 York Avenue, New York, 10021, New York, USA
Marcelo O. Magnasco
Authors
- Jie Yan
You can also search for this author inPubMed Google Scholar - Marcelo O. Magnasco
You can also search for this author inPubMed Google Scholar - John F. Marko
You can also search for this author inPubMed Google Scholar
Corresponding author
Correspondence toJohn F. Marko.
Rights and permissions
About this article
Cite this article
Yan, J., Magnasco, M. & Marko, J. A kinetic proofreading mechanism for disentanglement of DNA by topoisomerases.Nature 401, 932–935 (1999). https://doi.org/10.1038/44872
- Received: 22 December 1998
- Accepted: 18 August 1999
- Issue Date: 28 October 1999
- DOI: https://doi.org/10.1038/44872
This article is cited by
Ratcheting synthesis
- Stefan Borsley
- James M. Gallagher
- Benjamin M. W. Roberts
Nature Reviews Chemistry (2023)
Biological Implications of Dynamical Phases in Non-equilibrium Networks
- Arvind Murugan
- Suriyanarayanan Vaikuntanathan
Journal of Statistical Physics (2016)
Controlling gene expression by DNA mechanics: emerging insights and challenges
- David Levens
- Laura Baranello
- Fedor Kouzine
Biophysical Reviews (2016)
The dynamic interplay between DNA topoisomerases and DNA topology
- Yeonee Seol
- Keir C. Neuman
Biophysical Reviews (2016)
Controlling gene expression by DNA mechanics: emerging insights and challenges
- David Levens
- Laura Baranello
- Fedor Kouzine
Biophysical Reviews (2016)