DNA chirality-dependent stimulation of topoisomerase IV activity by the C-terminal AAA+ domain of FtsK

Nucleic Acids Research

Volumn 38, Issue 9, 2010, Pages 3031-3040

  Bigot, Sarah ^a   Marians, Kenneth J ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DNA; DNA TOPOISOMERASE IV; FTSK PROTEIN; UNCLASSIFIED DRUG; CATENATED DNA; ESCHERICHIA COLI PROTEIN; FTSK PROTEIN, E COLI; MEMBRANE PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHIRALITY; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA SUPERCOILING; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME STABILITY; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; CHEMISTRY; METABOLISM; PROTEIN TERTIARY STRUCTURE;

DNA TOPOISOMERASE IV; DNA, CATENATED; DNA, SUPERHELICAL; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; PROTEIN STRUCTURE, TERTIARY;

EID: 77953236795     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp1243     Document Type: Article

References (37)

1. Espeli, O. and Marians, K.J. (2004) Untangling intracellular DNA topology. Mol. Microbiol., 52, 925-931.
2. Wang, J.C. (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell Biol., 3, 430-440.
3. Nollmann, M., Crisona, N.J. and Arimondo, P.B. (2007) Thirty years of Escherichia coli DNA gyrase: from in vivo function to single-molecule mechanism. Biochimie, 89, 490-499.
4. Hiasa, H. and Marians, K.J. (1994) Topoisomerase IV can support oriC DNA replication in vitro. J. Biol. Chem., 269, 16371-16375.
5. Hiasa, H. and Marians, K.J. (1996) Two distinct modes of strand unlinking during theta-type DNA replication. J. Biol. Chem., 271, 21529-21535.
6. Khodursky, A.B., Peter, B.J., Schmid, M.B., DeRisi, J., Botstein, D., Brown, P.O. and Cozzarelli, N.R. (2000) Analysis of topoisomerase function in bacterial replication fork movement: use of DNA microarrays. Proc. Natl Acad. Sci. USA, 97, 9419-9424.
7. Champoux, J.J. (2001) DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem., 70, 369-413.
8. 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.
9. Peng, H. and Marians, K.J. (1993) Escherichia coli topoisomerase IV. Purification, characterization, subunit structure, and subunit interactions. J. Biol. Chem., 268, 24481-24490.
10. Corbett, K.D. and Berger, J.M. (2004) Structure, molecular mechanisms, and evolutionary relationships in DNA topoisomerases. Annu. Rev. Biophys. Biomol. Struct., 33, 95-118.
11. 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.
12. Kang, S., Han, J.S., Park, J.H., Skarstad, K. and Hwang, D.S. (2003) SeqA protein stimulates the relaxing and decatenating activities of topoisomerase IV. J. Biol. Chem., 278, 48779-48785.
13. Madabhushi, R. and Marians, K.J. (2009) Actin homolog MreB affects chromosome segregation by regulating topoisomerase IV in Escherichia coli. Mol. Cell, 33, 171-180.
14. Espeli, O., Lee, C. and Marians, K.J. (2003b) A physical and functional interaction between Escherichia coli FtsK and topoisomerase IV. J. Biol. Chem., 278, 44639-44644.
15. Bigot, S., Sivanathan, V., Possoz, C., Barre, F.X. and Cornet, F. (2007) FtsK, a literate chromosome segregation machine. Mol. Microbiol., 64, 1434-1441.
16. Lesterlin, C., Barre, F.X. and Cornet, F. (2004) Genetic recombination and the cell cycle: what we have learned from chromosome dimers. Mol. Microbiol., 54, 1151-1160.
17. Grainge, I., Bregu, M., Vazquez, M., Sivanathan, V., Ip, S.C. and Sherratt, D.J. (2007) Unlinking chromosome catenanes in vivo by site-specific recombination. EMBO J., 26, 4228-4238.
18. Aussel, L., Barre, F.X., Aroyo, M., Stasiak, A., Stasiak, A.Z. and Sherratt, D. (2002) FtsK is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell, 108, 195-205.
19. Marians, K.J. (1987) DNA gyrase-catalyzed decatenation of multiply linked DNA dimers. J. Biol. Chem., 262, 10362-10368.
20. McClendon, A.K., Rodriguez, A.C. and Osheroff, N. (2005) Human topoisomerase II alpha rapidly relaxes positively supercoiled DNA: implications for enzyme action ahead of replication forks. J. Biol. Chem., 280, 39337-39345.
21. Peng, H. and Marians, K.J. (1993) Decatenation activity of topoisomerase IV during oriC and pBR322 DNA replication in vitro. Proc. Natl Acad. Sci. USA, 90, 8571-8575.
22. 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.
23. Forterre, P., Bergerat, A. and Lopez-Garcia, P. (1996) The unique DNA topology and DNA topoisomerases of hyperthermophilic archaea. FEMS Microbiol. Rev., 18, 237-248.
24. Pease, P.J., Levy, O., Cost, G.J., Gore, J., Ptacin, J.L., Sherratt, D., Bustamante, C. and Cozzarelli, N.R. (2005) Sequence-directed DNA translocation by purified FtsK. Science, 307, 586-590.
25. Saleh, O.A., Perals, C., Barre, F.X. and Allemand, J.F. (2004) Fast, DNA-sequence independent translocation by FtsK in a single-molecule experiment. EMBO J., 23, 2430-2439.
26. 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. USA, 96, 8414-8419.
27. Schoeffler, A.J. and Berger, J.M. (2005) Recent advances in understanding structure-function relationships in the type II topoisomerase mechanism. Biochem. Soc. Trans., 33, 1465-1470.
28. Lindsley, J.E. and Wang, J.C. (1993) On the coupling between ATP usage and DNA transport by yeast DNA topoisomerase II. J. Biol. Chem., 268, 8096-8104.
29. Mueller-Planitz, F. and Herschlag, D. (2008) Coupling between ATP binding and DNA cleavage by DNA topoisomerase II: a unifying kinetic and structural mechanism. J. Biol. Chem., 283, 17463-17476.
30. Osheroff, N. (1986) Eukaryotic topoisomerase II. Characterization of enzyme turnover. J. Biol. Chem., 261, 9944-9950.
31. Nurse, P., Bahng, S., Mossessova, E. and Marians, K.J. (2000) Mutational analysis of Escherichia coli topoisomerase IV. II. ATPase negative mutants of parE induce hyper-DNA cleavage. J. Biol. Chem., 275, 4104-4111.
32. 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. USA, 100, 9820-9825.
33. Neuman, K.C., Charvin, G., Bensimon, D. and Croquette, V. (2009) Mechanisms of chiral discrimination by topoisomerase IV. Proc. Natl Acad. Sci. USA, 106, 6986-6991.
34. 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. USA, 93, 4057-4062.
35. Roca, J. and Wang, J.C. (1994) DNA transport by a type II DNA topoisomerase: evidence in favor of a two-gate mechanism. Cell, 77, 609-616.
36. Stone, M.D., Bryant, Z., Crisona, N.J., Smith, S.B., Vologodskii, A., Bustamante, C. and Cozzarelli, N.R. (2003) Chirality sensing by Escherichia coli topoisomerase IV and the mechanism of type II topoisomerases. Proc. Natl Acad. Sci. USA, 100, 8654-8659.
37. Lowe, J., Ellonen, A., Allen, M.D., Atkinson, C., Sherratt, D.J. and Grainge, I. (2008) Molecular mechanism of sequence-directed DNA loading and translocation by FtsK. Mol. Cell, 31, 498-509.