Mechanisms for defining supercoiling set point of DNA gyrase orthologs: I. A nonconserved acidic C-terminal tail modulates escherichia coli gyrase activity

Journal of Biological Chemistry

Volumn 287, Issue 22, 2012, Pages 18636-18644

  Tretter, Elsa M ^a   Berger, James M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C TERMINUS; C-TERMINAL DOMAINS; C-TERMINAL TAIL; CATALYTIC DOMAINS; COUPLING EFFICIENCY; DNA BINDING; DNA GYRASES; DNA SUPERCOILING; E. COLI; GYRA-CTD; ORTHOLOGS; SETPOINTS; SUPERCOILING; TOPOISOMERASES; TYPE IIA; WILD TYPES;

ESCHERICHIA COLI; FIBER OPTIC SENSORS;

DNA;

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; DNA TOPOISOMERASE (ATP HYDROLYSING);

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CROSS COUPLING REACTION; DNA SUPERCOILING; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME SPECIFICITY; ESCHERICHIA COLI; GENETIC CONSERVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; WILD TYPE;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; BASE SEQUENCE; CATALYTIC DOMAIN; DNA GYRASE; DNA PRIMERS; ESCHERICHIA COLI; HYDROLYSIS; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID;

ESCHERICHIA COLI; PROKARYOTA;

EID: 84861534674     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.345678     Document Type: Article

References (46)

1. Schoeffler, A. J., and Berger, J. M. (2008)DNAtopoisomerases: harnessing and constraining energy to govern chromosome topology. Q. Rev. Biophys. 41, 41-101
2. Gellert, M., Mizuuchi, K., O'Dea, M. H., and Nash, H. A. (1976) DNA gyrase: an enzyme that introduces superhelical turns into DNA. Proc. Natl. Acad. Sci. U.S.A. 73, 3872-3876
3. Forterre, P., Gribaldo, S., Gadelle, D., and Serre, M. C. (2007) Origin and evolution of DNA topoisomerases. Biochimie 89, 427-446 (Pubitemid 46656307)
4. Kampranis, S. C., and Maxwell, A. (1996) Conversion of DNA gyrase into a conventional type II topoisomerase. Proc. Natl. Acad. Sci. U.S.A. 93, 14416-14421 (Pubitemid 26418981)
5. Reece, R. J., and Maxwell, A. (1991) The C-terminal domain of the Escherichia coli DNA gyrase A subunit is a DNA-binding protein. Nucleic Acids Res. 19, 1399-1405 (Pubitemid 21913228)
6. Ruthenburg, A. J., Graybosch, D. M., Huetsch, J. C., and Verdine, G. L. (2005) A superhelical spiral in the Escherichia coli DNA gyrase A C-terminal domain imparts unidirectional supercoiling bias. J. Biol. Chem. 280, 26177-26184 (Pubitemid 41022213)
7. Corbett, K. D., Shultzaberger, R. K., and Berger, J. M. (2004) The C-terminal domain of DNA gyrase A adopts a DNA-bending β-pinwheel fold. Proc. Natl. Acad. Sci. U.S.A. 101, 7293-7298 (Pubitemid 38638026)
8. Brown, P. O., and Cozzarelli, N. R. (1979) A sign inversion mechanism for enzymatic supercoiling of DNA. Science 206, 1081-1083 (Pubitemid 10208881)
9. Liu, L. F., and Wang, J. C. (1978)DNA-DNAgyrase complex: the wrapping of the DNA duplex outside the enzyme. Cell 15, 979-984
10. Ward, D., and Newton, A. (1997) Requirement of topoisomerase IV parC and parE genes for cell cycle progression and developmental regulation in Caulobacter crescentus. Mol. Microbiol. 26, 897-910 (Pubitemid 27507875)
11. Tretter, E. M., Lerman, J. C., and Berger, J. M. (2010) A naturally chimeric type IIA topoisomerase in Aquifex aeolicus highlights an evolutionary path for the emergence of functional paralogs. Proc. Natl. Acad. Sci. U.S.A. 107, 22055-22059
12. Corbett, K. D., Schoeffler, A. J., Thomsen, N. D., and Berger, J. M. (2005) The structural basis for substrate specificity in DNA topoisomerase IV. J. Mol. Biol. 351, 545-561
13. Hsieh, T. J., Farh, L., Huang, W. M., and Chan, N. L. (2004) Structure of the topoisomerase IV C-terminal domain: a broken β-propeller implies a role as geometry facilitator in catalysis. J. Biol. Chem. 279, 55587-55593 (Pubitemid 40066562)
14. Crisona, N. J., Strick, T. R., Bensimon, D., Croquette, V., and Cozzarelli, N. R. (2000) Preferential relaxation of positively supercoiled DNA by E. coli topoisomerase IV in single-molecule and ensemble measurements. Genes Dev. 14, 2881-2892
15. Peng, H., and Marians, K. J. (1993) Decatenation activity of topoisomerase IV during oriC and pBR322 DNA replication in vitro. Proc. Natl. Acad. Sci. U.S.A. 90, 8571-8575 (Pubitemid 23277711)
16. Roca, J., Berger, J. M., Harrison, S. C., and Wang, J. C. (1996) DNA transport by a type II topoisomerase: direct evidence for a two-gate mechanism. Proc. Natl. Acad. Sci. U.S.A. 93, 4057-4062 (Pubitemid 26144245)
17. Charvin, G., Bensimon, D., and Croquette, V. (2003) Single-molecule study of DNA unlinking by eukaryotic and prokaryotic type-II topoisomerases. Proc. Natl. Acad. Sci. U.S.A. 100, 9820-9825 (Pubitemid 37087025)
18. McClendon, A. K., Gentry, A. C., Dickey, J. S., Brinch, M., Bendsen, S., Andersen, A. H., and Osheroff, N. (2008) Bimodal recognition of DNA geometry by human topoisomerase II α: preferential relaxation of positively supercoiled DNA requires elements in the C-terminal domain. Biochemistry 47, 13169-13178
19. Zechiedrich, E. L., Khodursky, A. B., Bachellier, S., Schneider, R., Chen, D., Lilley, D. M., and Cozzarelli, N. R. (2000) Roles of topoisomerases in maintaining steady-state DNA supercoiling in Escherichia coli. J. Biol. Chem. 275, 8103-8113 (Pubitemid 30159724)
20. Drlica, K. (1992) Control of bacterial DNA supercoiling. Mol. Microbiol. 6, 425-433
21. Kapust, R. B., Tözsér, J., Fox, J. D., Anderson, D. E., Cherry, S., Copeland, T. D., and Waugh, D. (2001) Tobacco etch virus protease: mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency. Protein Eng. 14, 993-1000 (Pubitemid 34137240)
22. Shuman, S. (1998) Vaccinia virus DNA topoisomerase: a model eukaryotic type IB enzyme. Biochim. Biophys. Acta 1400, 321-337
23. Champoux, J. J., and Dulbecco, R. (1972) An activity from mammalian cells that untwists superhelical DNA: a possible swivel for DNA replication (polyoma-ethidium bromide-mouse-embryo cells-dye binding assay). Proc. Natl. Acad. Sci. U.S.A. 69, 143-146
24. Dynan, W. S., Jendrisak, J. J., Hager, D. A., and Burgess, R. R. (1981) Purification and characterization of wheat germ DNA topoisomerase I (nicking- closing enzyme). J. Biol. Chem. 256, 5860-5865
25. Hsieh, T. J., Yen, T. J., Lin, T. S., Chang, H. T., Huang, S. Y., Hsu, C. H., Farh, L., and Chan, N. L. (2010) Twisting of the DNA-binding surface by a β-strand-bearing proline modulates DNA gyrase activity. Nucleic Acids Res. 38, 4173-4181
26. McGuffin, L. J., Bryson, K., and Jones, D. T. (2000) The PSIPRED protein structure prediction server. Bioinformatics 16, 404-405 (Pubitemid 30417087)
27. Lakowicz, J. R. (2006) Principles of Fluorescence Spectroscopy, Springer- Verlag New York Inc., New York
28. Rau, D. C., Gellert, M., Thoma, F., and Maxwell, A. (1987) Structure of the DNA gyrase-DNA complex as revealed by transient electric dichroism. J. Mol. Biol. 193, 555-569 (Pubitemid 17025289)
29. Heddle, J. G., Mitelheiser, S., Maxwell, A., and Thomson, N. H. (2004) Nucleotide binding to DNA gyrase causes loss of DNA wrap. J. Mol. Biol. 337, 597-610 (Pubitemid 38326880)
30. Kampranis, S. C., Bates, A. D., and Maxwell, A. (1999) A model for the mechanism of strand passage by DNA gyrase. Proc. Natl. Acad. Sci. U.S.A. 96, 8414-8419 (Pubitemid 29354805)
31. Wigley, D. B., Davies, G. J., Dodson, E. J., Maxwell, A., and Dodson, G. (1991) Crystal structure of an N-terminal fragment of the DNA gyrase B protein. Nature 351, 624-629 (Pubitemid 21896650)
32. Clark, D. J., and Leblanc, B. (2009) Analysis of DNA supercoiling induced by DNA-protein interactions. Methods Mol. Biol. 543, 523-535
33. Gellert, M., Mizuuchi, K., O'Dea, M. H., Itoh, T., and Tomizawa, J. I. (1977) Nalidixic acid resistance: a second genetic character involved in DNA gyrase activity. Proc. Natl. Acad. Sci. U.S.A. 74, 4772-4776 (Pubitemid 8227005)
34. Lanzetta, P. A., Alvarez, L. J., Reinach, P. S., and Candia, O. A. (1979) An improved assay for nanomole amounts of inorganic phosphate. Anal. Biochem. 100, 95-97 (Pubitemid 10157636)
35. Maxwell, A., and Gellert, M. (1984) The DNA dependence of the ATPase activity of DNA gyrase. J. Biol. Chem. 259, 14472-14480 (Pubitemid 15222266)
36. Costenaro, L., Grossmann, J. G., Ebel, C., and Maxwell, A. (2005) Smallangle X-ray scattering reveals the solution structure of the full-length DNA gyrase A subunit. Structure 13, 287-296 (Pubitemid 40247704)
37. Baker, N. M., Weigand, S., Maar-Mathias, S., and Mondragón, A. (2011) Solution structures of DNA-bound gyrase. Nucleic Acids Res. 39, 755-766
38. Sugino, A., and Cozzarelli, N. R. (1980) The intrinsic ATPase of DNA gyrase. J. Biol. Chem. 255, 6299-6306
39. Cullis, P. M., Maxwell, A., and Weiner, D. P. (1992) Energy coupling in DNA gyrase: a thermodynamic limit to the extent of DNA supercoiling. Biochemistry 31, 9642-9646
40. Roca, J., and Wang, J. C. (1992) 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
41. Blanche, F., Cameron, B., Bernard, F. X., Maton, L., Manse, B., Ferrero, L., Ratet, N., Lecoq, C., Goniot, A., Bisch, D., and Crouzet, J. (1996) Differential behaviors of Staphylococcus aureus and Escherichia coli type II DNA topoisomerases. Antimicrob. Agents Chemother. 40, 2714-2720 (Pubitemid 26404331)
42. Champion, K., and Higgins, N. P. (2007) Growth rate toxicity phenotypes and homeostatic supercoil control differentiate Escherichia coli from Salmonella enterica serovar Typhimurium. J. Bacteriol. 189, 5839-5849 (Pubitemid 47236136)
43. Aubry, A., Fisher, L. M., Jarlier, V., and Cambau, E. (2006) First functional characterization of a singly expressed bacterial type II topoisomerase: the enzyme from Mycobacterium tuberculosis. Biochem. Biophys. Res. Commun. 348, 158-165 (Pubitemid 44177674)
44. García-Estrada, C., Prada, C. F., Fernández-Rubio, C., Rojo-Vázquez, F., and Balaña-Fouce, R. (2010) DNA topoisomerases in apicomplexan parasites: promising targets for drug discovery. Proc. Biol. Sci. 277, 1777-1787
45. Bates, A. D., O'Dea, M. H., and Gellert, M. (1996) Energy coupling in Escherichia coli DNA gyrase: the relationship between nucleotide binding, strand passage, and DNA supercoiling. Biochemistry 35, 1408-1416 (Pubitemid 26055276)
46. Tretter, E. M., and Berger, J. M. (March 28, 2012) Mechanisms for defining supercoiling set point of DNA gyrase orthologs. II. The shape of the GyrA CTD is not a sole determinant for controlling supercoiling efficiency. J. Biol. Chem. 287, 18645-18654