Probing conformational changes in human DNA topoisomerase IIα by pulsed alkylation mass spectrometry

Journal of Biological Chemistry

Volumn 287, Issue 30, 2012, Pages 25660-25668

  Chen, Yu Tsung ^a   Collins, Tammy R L ^a,c   Guan, Ziqiang ^a   Chen, Vincent B ^a   Hsieh, Tao Shih ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTICANCER DRUG; ATP HYDROLYSIS; COFACTORS; CONFORMATIONAL CHANGE; DNA CLEAVAGE; DNA DUPLEXES; DNA TOPOISOMERASE; DOUBLE-STRAND BREAKS; ENZYME CONFORMATIONS; HUMAN TOPOISOMERASE; POTENTIAL DIFFERENCE; REACTIVITY CHANGES; SOLVENT ACCESSIBILITY; STRUCTURAL MODELS; THIOL REACTIVITY; TOPOISOMERASE II; TOPOISOMERASES; TYPE II;

ALKYLATION; AMINO ACIDS; ENZYMES; MASS SPECTROMETRY; MODEL STRUCTURES;

DNA;

ADENOSINE TRIPHOSPHATE; BROMOBIMANE; CYSTEINE; DNA; GYRASE INHIBITOR; MAGNESIUM ION;

ALKYLATION; AMINO ACID SEQUENCE; ARTICLE; CALIBRATION; CATALYSIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTROSPRAY MASS SPECTROMETRY; ENZYME MECHANISM; ENZYME STRUCTURE; HUMAN; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN HYDROLYSIS; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; ALKYLATION; ANTIGENS, NEOPLASM; BICYCLO COMPOUNDS; DNA BREAKS, DOUBLE-STRANDED; DNA TOPOISOMERASES, TYPE II; DNA-BINDING PROTEINS; HOLOENZYMES; HUMANS; HYDROLYSIS; MASS SPECTROMETRY; MODELS, MOLECULAR; PIPERAZINES; PROTEIN STRUCTURE, TERTIARY;

EID: 84864110457     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.377606     Document Type: Article

References (42)

1. Wang, J. C. (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell Biol. 3, 430-440
2. Champoux, J. J. (2001) DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70, 369-413
3. 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 (Pubitemid 38829953)
4. Sundin, O., and Varshavsky, A. (1981) Arrest of segregation leads to accumulation of highly intertwined catenated dimers: dissection of the final stages of SV40 DNA replication. Cell 25, 659-669 (Pubitemid 11022967)
5. Morrison, A., and Cozzarelli, N. R. (1979) Site-specific cleavage ofDNAby E. coli DNA gyrase. Cell 17, 175-184 (Pubitemid 9188221)
6. Liu, L. F., Rowe, T. C., Yang, L., Tewey, K. M., and Chen, G. L. (1983) Cleavage of DNA by mammalian DNA topoisomerase II. J. Biol. Chem. 258, 15365-15370
7. Sander, M., and Hsieh, T. (1983) Double-strand DNA cleavage by type II DNA topoisomerase from Drosophila melanogaster. J. Biol. Chem. 258, 8421-8428
8. Schoeffler, A. J., and Berger, J. M. (2008)DNAtopoisomerases: harnessing and constraining energy to govern chromosome topology. Q. Rev. Biophys. 41, 41-101
9. Schmidt, B. H., Burgin, A. B., Deweese, J. E., Osheroff, N., and Berger, J. M. (2010) A novel and unified two-metal mechanism for DNA cleavage by type II and IA topoisomerases. Nature 465, 641-644
10. Lee, M. P., and Hsieh, T. S. (1994) Linker insertion mutagenesis of Drosophila topoisomerase II. Probing the structure of eukaryotic topoisomerase II. J. Mol. Biol. 235, 436-447
11. Austin, C. A., Marsh, K. L., Wasserman, R. A., Willmore, E., Sayer, P. J., Wang, J. C., and Fisher, L. M. (1995) Expression, domain structure, and enzymatic properties of an active recombinant human DNA topoisomerase IIβ. J. Biol. Chem. 270, 15739-15746
12. Li, W., and Wang, J. C. (1997) Footprinting of yeastDNAtopoisomerase II lysyl side chains involved in substrate binding and interdomain interactions. J. Biol. Chem. 272, 31190-31195 (Pubitemid 27527570)
13. Hanai, R., and Wang, J. C. (1994) Protein footprinting by the combined use of reversible and irreversible lysine modifications. Proc. Natl. Acad. Sci. U.S.A. 91, 11904-11908 (Pubitemid 24368572)
14. Atassi, M. Z., Suliman, A. M., and Habeeb, A. F. (1972) Enzymic and immunochemical properties of lysozyme. VI. Conformation, enzymic activity, and immunochemistry of derivatives modified at arginine residues. Immunochemistry 9, 907-920
15. Wood, T. D., Guan, Z., Borders, C. L., Jr., Chen, L. H., Kenyon, G. L., and McLafferty, F. W. (1998) Creatine kinase: essential arginine residues at the nucleotide-binding site identified by chemical modification and high-resolution tandem mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 95, 3362-3365 (Pubitemid 28173132)
16. Habeeb, A. F., Schrohenloher, R. E., and Bennett, J. C. (1972) Studies of the component chains of human IgM by citraconylation. Biochim. Biophys. Acta 263, 339-350
17. Tu, B. P., and Wang, J. C. (1999) Protein footprinting at cysteines: probing ATP-modulated contacts in cysteine substitution mutants of yeast DNA topoisomerase II. Proc. Natl. Acad. Sci. U.S.A. 96, 4862-4867 (Pubitemid 29214502)
18. Apuy, J. L., Park, Z. Y., Swartz, P. D., Dangott, L. J., Russell, D. H., and Baldwin, T. O. (2001) Pulsed alkylation mass spectrometry for the study of protein folding and dynamics: development and application to the study of a folding/unfolding intermediate of bacterial luciferase. Biochemistry 40, 15153-15163 (Pubitemid 33151930)
19. Kim, Y. J., Pannell, L. K., and Sackett, D. L. (2004) Mass spectrometric measurement of differential reactivity of cysteine to localize protein-ligand binding sites. Application to tubulin-binding drugs. Anal. Biochem. 332, 376-383 (Pubitemid 39485747)
20. Carven, G. J., and Stern, L. J. (2005) Probing the ligand-induced conformational change in HLA-DR1 by selective chemical modification and mass spectrometric mapping. Biochemistry 44, 13625-13637 (Pubitemid 41507444)
21. Wasserman, R. A., Austin, C. A., Fisher, L. M., and Wang, J. C. (1993) Use of yeast in the study of anticancer drugs targeting DNA topoisomerases: expression of a functional recombinant humanDNAtopoisomerase IIα in yeast. Cancer Res. 53, 3591-3596 (Pubitemid 23229642)
22. Kennelly, P. J., and Krebs, E. G. (1991) Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases. J. Biol. Chem. 266, 15555-15558 (Pubitemid 21907685)
23. Crenshaw, D. G., and Hsieh, T. (1993) Function of the hydrophilic carboxyl terminus of type II DNA topoisomerase from Drosophila melanogaster. II. In vivo studies. J. Biol. Chem. 268, 21335-21343 (Pubitemid 23292325)
24. Meczes, E. L., Gilroy, K. L., West, K. L., and Austin, C. A. (2008) The impact of the human DNA topoisomerase II C-terminal domain on activity. PLoS ONE 3, e1754
25. Dickey, J. S., and Osheroff, N. (2005) Impact of the C-terminal domain of topoisomerase IIα on the DNA cleavage activity of the human enzyme. Biochemistry 44, 11546-11554 (Pubitemid 41209090)
26. Hu, T., Sage, H., and Hsieh, T. S. (2002) ATPase domain of eukaryotic DNA topoisomerase II. Inhibition of ATPase activity by the anticancer drug bisdioxopiperazine and ATP/ADP-induced dimerization. J. Biol. Chem. 277, 5944-5951 (Pubitemid 34968375)
27. Kosower, E. M., Pazhenchevsky, B. (1980) Bimanes. 5. Synthesis and properties of syn- and anti-1,5-diazabicyclo[3.3.0]octadienediones (9,10-dioxabimanes). J. Am. Chem. Soc. 102, 4983-4993
28. Roy, A., Kucukural, A., and Zhang, Y. (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5, 725-738
29. Zhang, Y. (2007) Template-based modeling and free modeling by I-TASSER in CASP7. Proteins 69, 108-117
30. Fass, D., Bogden, C. E., and Berger, J. M. (1999) Quaternary changes in topoisomerase II may direct orthogonal movement of two DNA strands. Nat. Struct. Biol. 6, 322-326
31. Wei, H., Ruthenburg, A. J., Bechis, S. K., and Verdine, G. L. (2005) Nucleotide- dependent domain movement in the ATPase domain of a human type IIA DNA topoisomerase. J. Biol. Chem. 280, 37041-37047 (Pubitemid 41587788)
32. Chen, V. B., Davis, I. W., and Richardson, D. C. (2009) KING (Kinemage, Next Generation): a versatile interactive molecular and scientific visualization program. Protein Sci. 18, 2403-2409
33. Word, J. M., Lovell, S. C., LaBean, T. H., Taylor, H. C., Zalis, M. E., Presley, B. K., Richardson, J. S., and Richardson, D. C. (1999) Visualizing and quantifying molecular goodness-of-fit: small-probe contact dots with explicit hydrogen atoms. J. Mol. Biol. 285, 1711-1733 (Pubitemid 29060466)
34. Hsieh, T. (1983) Purification and properties of type II DNA topoisomerase from embryos of Drosophila melanogaster. Methods Enzymol. 100, 161-170
35. 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
36. Roca, J., Ishida, R., Berger, J. M., Andoh, T., and Wang, J. C. (1994) Anti-tumor bisdioxopiperazines inhibit yeast DNA topoisomerase II by trapping the enzyme in the form of a closed protein clamp. Proc. Natl. Acad. Sci. U.S.A. 91, 1781-1785 (Pubitemid 24080289)
37. Classen, S., Olland, S., and Berger, J. M. (2003) Structure of the topoisomerase II ATPase region and its mechanism of inhibition by the chemotherapeutic agent ICRF-187. Proc. Natl. Acad. Sci. U.S.A. 100, 10629-10634 (Pubitemid 37140080)
38. Bender, R. P., Lehmler, H. J., Robertson, L. W., Ludewig, G., and Osheroff, N. (2006) Polychlorinated biphenyl quinone metabolites poison human topoisomerase IIα: altering enzyme function by blocking the N-terminal protein gate. Biochemistry 45, 10140-10152 (Pubitemid 44257408)
39. Wu, X., Liang, H., O'Hara, K. A., Yalowich, J. C., and Hasinoff, B. B. (2008) Thiol-modulated mechanisms of the cytotoxicity of thimerosal and inhibition of DNA topoisomerase IIα. Chem. Res. Toxicol. 21, 483-493
40. Jensen, L. H., Thougaard, A. V., Grauslund, M., Søkilde, B., Carstensen, E. V., Dvinge, H. K., Scudiero, D. A., Jensen, P. B., Shoemaker, R. H., and Sehested, M. (2005) Substituted purine analogues define a novel structural class of catalytic topoisomerase II inhibitors. Cancer Res. 65, 7470-7477 (Pubitemid 41161282)
41. Bender, R. P., Ham, A. J., and Osheroff, N. (2007) Quinone-induced enhancement of DNA cleavage by human topoisomerase IIα: adduction of cysteine residues 392 and 405. Biochemistry 46, 2856-2864 (Pubitemid 46420241)
42. Lin, R. K., Zhou, N., Lyu, Y. L., Tsai, Y. C., Lu, C. H., Kerrigan, J., Chen, Y. T., Guan, Z., Hsieh, T. S., and Liu, L. F. (2011) Dietary isothiocyanateinduced apoptosis via thiol modification of DNA topoisomerase IIα. J. Biol. Chem. 286, 33591-33600