Abstract
The three-dimensional structure of the 67K amino-terminal fragment of Escherichia coli DNA topoisomerase I has been determined to 2.2 Å resolution. The polypeptide folds in an unusual way to give four distinct domains enclosing a hole large enough to accommodate a double-stranded DNA. The active-site tyrosyl residue, which is involved in the transient breakage of a DNA strand and the formation of a covalent enzyme–DNA intermediate, is present at the interface of two domains. The structure suggests a plausible mechanism by which E. coli DNA topoisomerase I and other members of the same DNA topoisomerase subfamily could catalyse the passage of one DNA strand through a transient break in another strand.
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 Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Gellert, M. A. Rev. Biochem. 50, 879–910 (1981).
Wang, J. C. A. Rev. Biochem. 54, 665–697 (1985).
Wang, J. C. J. biol. Chem. 266, 6659–6662 (1991).
Proc. Int. Symp. on DNA Topoisomerases in ChemotherapyNagoya Japan (eds Anhoh, T., Ikeda, H. & Oguro, M.) (CRC, Florida, 1993).
Liu, L. F. A. Rev. Biochem 58, 351–375 (1989).
Drlica, K. & Franco, R. J. Biochemistry 27, 2253–2259 (1988).
Wang, J. C. J. molec. Biol. 55, 523–533 (1971).
Dean, F. et al. Cold Spring Harbor Symp. quant. Biol. 47, 769–777 (1982).
DiGate, R. J. & Marians, K. J. J. biol. Chem. 264, 17924–17930 (1989).
Wallis, J. W., Chrebet, G., Brodsky, G., Rolfe, M. & Rothstein, R. Cell 58, 409–419 (1989).
Kim, R. A. & Wang, J. C. J. biol. Chem. 267, 17178–17185 (1992).
Kikuchi, A. & Asai, K. Nature 309, 677–681 (1984).
Confalonieri, F. et al. Proc. natn. Acad. Sci. U.S.A. 90, 4753–4757 (1993).
Wang, J. C. in Nucleases (eds Roberts, R. & Linn, S.) 41–57 (Cold Spring Harbor Laboratory, New York, 1982).
Kornberg, A. & Baker, T. DNA Replication (Freeman, New York, 1992).
Tse-Dinh, Y.-C. & Beran-Steed, R. K. J. biol. Chem. 263, 15857–15859 (1988).
Lynn, R. & Wang, J. C. Prot. Struct. Func. Genet. 6, 231–239 (1989).
Tse-Dinh, Y.-C. J. biol. Chem. 266, 14217–14320 (1991).
Lima, C. D., Wang, J. C. & Mondragón, A. J. molec. Biol. 232, 1213–1216 (1993).
Jones, T. A., Zou, J. Y., Cowan, S. W. & Kjeldgaard, M. Acta. crystallogr. A47, 110–119 (1991).
Hendrickson, W. A. & Konnert, J. H. in Biomolecular Structural, Function, Conformation and Evolution Vol. I (ed. Srinivisan, R.) 43–57 (Pergamon, Oxford, 1980).
Brunger, A. T., Kuriyan, J. & Karplus, M. Science 235, 458–460 (1987).
Brunger, A. T. Nature 355, 472–474 (1992).
Hodel, A., Kim, S.-H. & Brunger, A. T. Acta crystallogr. A48, 851–858 (1992).
Bränden, C.-I. Quart. Rev. Biophys. 13, 317–338 (1980).
Beese, L. S. & Steitz, T. A. EMBO J. 10, 25–33 (1991).
Domanico, P. L. & Tse-Dinh, Y.-C. J. inorg. Biochem. 42, 87–96 (1991).
Zumstein, L. & Wang, J. C. J. molec. Biol. 191, 333–340 (1986).
Lindsay, J. & Wang, J. C. Proc. natn. Acad. Sci. U.S.A. 88, 10485–10489 (1991).
Roca, J. & Wang, J. C. Cell 71, 833–840 (1992).
Grau, U. M., Tromer, W. E. & Rossmann, M. G. J. molec. Biol. 151, 289–307 (1981).
Eklund, H. Samana, J.-P. & Jones, T. A. Biochemistry 23, 5982–5996 (1984).
Van der Laan, J. M. et al. Biochemistry 28, 7199–7205 (1989).
Karplus, P. A. & Schulz, G. E. J. molec. Biol. 195, 701–729 (1987).
Kirkegaard, K., Pflugfelder, G. & Wang, J. C. Cold Spring Harbor Symp. quant. Biol. 49, 411–419 (1984).
Gilson, M. K., Sharp, K. A. & Honig, B. H. J. comp. Chem. 9, 327–335 (1987).
Nicholls, A., Sharp, K. A. & Honig, B. H. Prot. Struct. Fund. Genet. 11, 281–286 (1991).
Beran-Steed, R. K. & Tse-Dinh, Y.-C. Prot. Struct. Funct. Genet. 6, 249–258 (1989).
Kong, X.-P., Onrust, R., O'Donnell, M. & Kuriyan, J. Cell 69, 425–437 (1992).
Nikolov, D. B. et al. Nature 360, 40–46 (1992).
Kim, J. L., Nikolov, D. B. & Burley, S. K. Nature 356, 520–527 (1993).
Kim, Y., Geiger, J. H., Hahn, S. & Sigler, P. B. Nature 365, 512–520 (1993).
Brown, P. O. & Cozzarelli, N. R. Proc. natn. Acad. Sci. U.S.A. 78, 843–847 (1981).
Tse, Y.-C. & Wang, J. C. Cell 22, 269–277 (1980).
Kirkegaard, K. & Wang, J. C. J. molec. Biol. 185, 625–637 (1985).
Champoux, J. J. in DNA Topology and its Biological Effects (eds Cozzarelli, N. R. & Wang, J. C.) 217–242 (Cold Spring Harbor Laboratory Press, New York, 1990).
Durbin, R. M. et al. Science 232, 1127–1132 (1986).
Blum, M., Metcalf, P., Harrison, S. C. & Wiley, D. C. J. appl. Cryst. 20, 235–242 (1987).
Harrison, S. C. J. appl. Cryst. 1, 84–90 (1968).
Kabsch, W. J. appl. Cryst. 21, 67–71 (1988).
Kabsch, W. J. appl. Cryst. 21, 916–924 (1988).
Hope, H. Acta. crystallogr. B44, 22–26 (1988).
CCP4 SERC (UK) Collaborative Computing Project 4 (Daresbury Laboratory, Warrington WA44AD, 1979).
Teng, T.-Y. J. appl. Cryst. 23, 387–391 (1990).
Otwinowski, Z. in Isomorphous Replacement and Anomalous Scattering 80–86 (Daresbury Laboratory, UK (1991).
Wang, B. C. Meth. Enzym. 115, 90–112 (1985).
Leslie, A. G. W. Acta. crystallogr. A43, 134–135 (1987).
Sim, G. A. Acta. crystallogr. 13, 511–512 (1960).
Laskowski, R. A., MacArthur, M. W., Moss, D. S. & Thornton, J. M. J. appl. Cryst. 26, 283–291 (1993).
Kraulis, P. J. J. appl. Cryst. 24, 946–950 (1991).
Evans, S. V. J. molec. Graph. 11, 134–138 (1993).
Ivey, D. M., Cheng, J. & Krulwich, T. A. Nucleic Acids Res. 20, 4928 (1992).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lima, C., Wang, J. & Mondragón, A. Three-dimensional structure of the 67K N-terminal fragment of E. coli DNA topoisomerase I. Nature 367, 138–146 (1994). https://doi.org/10.1038/367138a0
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/367138a0
This article is cited by
-
Molecular Evolution of DNA Topoisomerase III Beta (TOP3B) in Metazoa
Journal of Molecular Evolution (2021)
-
Direct observation of topoisomerase IA gate dynamics
Nature Structural & Molecular Biology (2018)
-
An orthogonal single-molecule experiment reveals multiple-attempt dynamics of type IA topoisomerases
Nature Structural & Molecular Biology (2017)
-
Kinetic insights into the temperature dependence of DNA strand cleavage and religation by topoisomerase III from the hyperthermophile Sulfolobus solfataricus
Scientific Reports (2017)
-
The dynamic interplay between DNA topoisomerases and DNA topology
Biophysical Reviews (2016)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.