Mass spectrometry reveals that the antibiotic simocyclinone D8 binds to DNA gyrase in a "bent-over" conformation: Evidence of positive cooperativity in binding

Biochemistry

Volumn 50, Issue 17, 2011, Pages 3432-3440

  Edwards, Marcus J ^a,d   Williams, Mark A ^b   Maxwell, Anthony ^a   McKay, Adam R ^c  

^a JOHN INNES CENTRE   (United Kingdom)

^b UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTICANCER DRUG; BIFUNCTIONAL INHIBITORS; BIFUNCTIONAL LIGAND; BINDING POCKETS; BIOMOLECULAR INTERACTIONS; BOUND STATE; COOPERATIVE BINDING; COOPERATIVITY; DISSOCIATION CONSTANT; DNA GYRASES; DNA TOPOLOGY; GENERAL APPROACH; GENERAL MODEL; MASS SPECTROMETRY DATA; MULTIPLE BINDING SITES; SIMOCYCLINONE; TIGHT BINDING; TOPOISOMERASES;

ANTIBIOTICS; BIOCHEMISTRY; COMPLEXATION; DISSOCIATION; DNA; MASS SPECTROMETRY; NUCLEIC ACIDS; X RAY CRYSTALLOGRAPHY;

BINDING SITES;

ANTIBIOTIC AGENT; DIMER; DNA TOPOISOMERASE (ATP HYDROLYSING); SIMOCYCLINONE D8; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; COMPLEX FORMATION; DRUG CONFORMATION; DRUG MECHANISM; DRUG PROTEIN BINDING; ENZYME SUBUNIT; MASS SPECTROMETRY; MOLECULAR MODEL; PRIORITY JOURNAL; STOICHIOMETRY; X RAY CRYSTALLOGRAPHY;

ALLOSTERIC REGULATION; ANTI-BACTERIAL AGENTS; COUMARINS; DNA GYRASE; GLYCOSIDES; MASS SPECTROMETRY; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS;

STREPTOMYCES;

EID: 79955415835     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101691k     Document Type: Article

References (40)

1. Ruotolo, B. T., Giles, K., Campuzano, I., Sandercock, A. M., Bateman, R. H., and Robinson, C. V. (2005) Evidence for macromolecular protein rings in the absence of bulk water Science 310, 1658-1661 (Pubitemid 41780783)
2. Leary, J. A., Schenauer, M. R., Stefanescu, R., Andaya, A., Ruotolo, B. T., Robinson, C. V., Thalassinos, K., Scrivens, J. H., Sokabe, M., and Hershey, J. W. (2009) Methodology for measuring conformation of solvent-disrupted protein subunits using T-WAVE ion mobility MS: An investigation into eukaryotic initiation factors J. Am. Soc. Mass Spectrom. 20, 1699-1706
3. Scarff, C. A., Patel, V. J., Thalassinos, K., and Scrivens, J. H. (2009) Probing hemoglobin structure by means of traveling-wave ion mobility mass spectrometry J. Am. Soc. Mass Spectrom. 20, 625-631
4. Scarff, C. A., Thalassinos, K., Hilton, G. R., and Scrivens, J. H. (2008) Travelling wave ion mobility mass spectrometry studies of protein structure: Biological significance and comparison with X-ray crystallography and nuclear magnetic resonance spectroscopy measurements Rapid Commun. Mass Spectrom. 22, 3297-3304
5. Smith, D. P., Knapman, T. W., Campuzano, I., Malham, R. W., Berryman, J. T., Radford, S. E., and Ashcroft, A. E. (2009) Deciphering drift time measurements from travelling wave ion mobility spectrometry-mass spectrometry studies Eur. J. Mass Spectrom. 15, 113-130
6. Ruotolo, B. T. and Robinson, C. V. (2006) Aspects of native proteins are retained in vacuum Curr. Opin. Chem. Biol. 10, 402-408 (Pubitemid 44375072)
7. Heck, A. J. (2008) Native mass spectrometry: A bridge between interactomics and structural biology Nat. Methods 5, 927-933
8. Heck, A. J. and Van Den Heuvel, R. H. (2004) Investigation of intact protein complexes by mass spectrometry Mass Spectrom. Rev. 23, 368-389
9. Hernandez, H. and Robinson, C. V. (2007) Determining the stoichiometry and interactions of macromolecular assemblies from mass spectrometry Nat. Protoc. 2, 715-726 (Pubitemid 47040033)
10. Loo, J. A. (1997) Studying noncovalent protein complexes by electrospray ionization mass spectrometry Mass Spectrom. Rev. 16, 1-23 (Pubitemid 127583217)
11. Sharon, M. and Robinson, C. V. (2007) The role of mass spectrometry in structure elucidation of dynamic protein complexes Annu. Rev. Biochem. 76, 167-193
12. McCammon, M. G. and Robinson, C. V. (2004) Structural change in response to ligand binding Curr. Opin. Chem. Biol. 8, 60-65 (Pubitemid 38201479)
13. Bligh, S. W., Haley, T., and Lowe, P. N. (2003) Measurement of dissociation constants of inhibitors binding to Src SH2 domain protein by non-covalent electrospray ionization mass spectrometry J. Mol. Recognit. 16, 139-148
14. Tjernberg, A., Carno, S., Oliv, F., Benkestock, K., Edlund, P. O., Griffiths, W. J., and Hallen, D. (2004) Determination of dissociation constants for protein-ligand complexes by electrospray ionization mass spectrometry Anal. Chem. 76, 4325-4331 (Pubitemid 39014001)
15. Daniel, J. M., Friess, S. D., Rajagopalan, S., Wendt, S., and Zenobi, R. (2002) Quantitative determination of noncolvant binding interactions using soft ionisation mass spectrometry Int. J. Mass Spectrom. 216, 1-27
16. Bates, A. and Maxwell, A. (2005) DNA Topology, 2nd ed., Oxford University Press, New York.
17. Schoeffler, A. J. and Berger, J. M. (2008) DNA topoisomerases: Harnessing and constraining energy to govern chromosome topology Q. Rev. Biophys. 41, 41-101
18. 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 (Pubitemid 46634704)
19. Pommier, Y. (2009) DNA topoisomerase I inhibitors: Chemistry, biology, and interfacial inhibition Chem. Rev. 109, 2894-2902
20. Gatto, B., Capranico, G., and Palumbo, M. (1999) Drugs acting on DNA topoisomerases: Recent advances and future perspectives Curr. Pharm. Des. 5, 195-215 (Pubitemid 29159611)
21. Maxwell, A. (1999) DNA gyrase as a drug target Biochem. Soc. Trans. 27, 48-53 (Pubitemid 29086006)
22. Flatman, R. H., Howells, A. J., Heide, L., Fiedler, H. P., and Maxwell, A. (2005) Simocyclinone D8, an inhibitor of DNA gyrase with a novel mode of action Antimicrob. Agents Chemother. 49, 1093-1100 (Pubitemid 40327729)
23. Holzenkampfer, M., Walker, M., Zeeck, A., Schimana, J., and Fiedler, H. P. (2002) Simocyclinones, novel cytostatic angucyclinone antibiotics produced by Streptomyces antibioticus Tu 6040 II. Structure elucidation and biosynthesis J. Antibiot. 55, 301-307 (Pubitemid 34296242)
24. Schimana, J., Fiedler, H. P., Groth, I., Sussmuth, R., Beil, W., Walker, M., and Zeeck, A. (2000) Simocyclinones, novel cytostatic angucyclinone antibiotics produced by Streptomyces antibioticus Tu 6040. I. Taxonomy, fermentation, isolation and biological activities J. Antibiot. 53, 779-787
25. Theobald, U., Schimana, J., and Fiedler, H. P. (2000) Microbial growth and production kinetics of Streptomyces antibioticus Tu 6040 Antonie van Leeuwenhoek 78, 307-313 (Pubitemid 32401252)
26. Edwards, M. J., Flatman, R. H., Mitchenall, L. A., Stevenson, C. E., Le, T. B., Clarke, T. A., McKay, A. R., Fiedler, H. P., Buttner, M. J., Lawson, D. M., and Maxwell, A. (2009) A crystal structure of the bifunctional antibiotic simocyclinone D8, bound to DNA gyrase Science 326, 1415-1418
27. Hunter, C. A. and Anderson, H. L. (2009) What is cooperativity? Angew. Chem., Int. Ed. 48, 7488-7499
28. Whitty, A. (2008) Cooperativity and biological complexity Nat. Chem. Biol. 4, 435-439 (Pubitemid 352019765)
29. Potier, N., Rogniaux, H., Chevreux, G., and Van Dorsselaer, A. (2005) Ligand-metal ion binding to proteins: Investigation by ESI mass spectrometry Methods Enzymol. 402, 361-389 (Pubitemid 43053132)
30. McCammon, M. G., Scott, D. J., Keetch, C. A., Greene, L. H., Purkey, H. E., Petrassi, H. M., Kelly, J., and Robinson, C. V. (2002) Screening transthyretin amyloid fibril inhibitiors: Characterization of novel multiprotein multiligand complexes by mass spectrometry Structure 10, 851-863 (Pubitemid 34628713)
31. Rogniaux, H., Sanglier, S., Strupat, K., Azza, S., Roitel, O., Ball, V., Tritsch, D., Branlant, G., and Van Dorsselaer, A. (2001) Mass spectrometry as a novel approach to probe cooperativity in multimeric enzymatic systems Anal. Biochem. 291, 48-61 (Pubitemid 32324523)
32. Maxwell, A. and Howells, A. J. (1999) Overexpression and purification of bacterial DNA gyrase Methods Mol. Biol. 94, 135-144
33. Reece, R. J. and Maxwell, A. (1991) Probing the limits of the DNA breakage-reunion domain of the Escherichia coli DNA gyrase A protein J. Biol. Chem. 266, 3540-3546 (Pubitemid 21909247)
34. Edwards, M. J., Flatman, R. H., Mitchenall, L. A., Stevenson, C. E., Maxwell, A., and Lawson, D. M. (2009) Crystallization and preliminary X-ray analysis of a complex formed between the antibiotic simocyclinone D8 and the DNA breakage-reunion domain of Escherichia coli DNA gyrase Acta Crystallogr. F65, 846-848
35. Williams, J. W. and Morrison, J. F. (1979) The kinetics of reversible tight-binding inhibition Methods Enzymol. 63, 437-467
36. Copeland, R. A. (2005) Tight binding inhibition. In Evaluation of enzyme inhibitors in drug discovery, pp 178 - 213, John Wiley and Sons Inc., New York.
37. Swillens, S. (1995) Interpretation of binding curves obtained with high receptor concentrations: Practical aid for computer analysis Mol. Pharmacol. 47, 1197-1203
38. Press, W. H., Teukolsky, S. A., Vetterling, W. T., and Flannery, B. P. (2007) Numerical Recipies: The Art of Scientific Computing, 3rd ed., Cambridge University Press, Cambridge, U.K.
39. Monod, J., Wyman, J., and Changeux, J. P. (1965) On the Nature of Allosteric Transitions: A Plausible Model J. Mol. Biol. 12, 88-118
40. Koshland, D. E., Jr., Nemethy, G., and Filmer, D. (1966) Biochemistry 5, 365-85