An insight into the mechanism of inhibition of unusual bi-subunit topoisomerase I from Leishmania donovani by 3,3′-di-indolylmethane, a novel DNA topoisomerase I poison with a strong binding affinity to the enzyme

Biochemical Journal

Volumn 409, Issue 2, 2008, Pages 611-622

  Roy, Amit ^a   Das, Benu Brata ^b   Ganguly, Agneyo ^a   Bose Dasgupta, Somdeb ^a   Khalkho, Neeta V M ^a   Pal, Churala ^a   Dey, Sumit ^a   Giri, Venkatachalam Sesha ^a   Jaisankar, Parasuraman ^a   Dey, Sanjit ^c   Majumder, Hemanta K ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF CALCUTTA   (India)

Author keywords

3,3 di indolylmethane (DIM); Cleavable complex; Leishmania donovani; Reconstitution; Topoisomerase I; Topoisomerase poison

Indexed keywords

CRUCIFEROUS VEGETABLES; LEISHMANIA DONOVANI; TOPOISOMERASE I; TOPOISOMERASE POISON;

DIALYSIS; DNA; ENZYME ACTIVITY; ENZYME INHIBITION; SUBSTRATES;

PROTOZOA;

3,3' DIINDOLYLMETHANE; AMINO ACID; CAMPTOTHECIN; DNA TOPOISOMERASE; DNA TOPOISOMERASE INHIBITOR; POISON; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; COMPARATIVE STUDY; COMPLEX FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA CLEAVAGE; DRUG DESIGN; DRUG MECHANISM; ENZYME ASSAY; ENZYME BINDING; ENZYME INHIBITION; ENZYME SUBSTRATE; IN VITRO STUDY; IN VIVO STUDY; LEISHMANIA DONOVANI; LEISHMANIASIS; NONHUMAN; PRIORITY JOURNAL; WILD TYPE;

ANIMALS; BINDING SITES; CAMPTOTHECIN; CATALYSIS; DNA; DNA TOPOISOMERASES, TYPE I, EUKARYOTIC; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; HUMANS; INDOLES; LEISHMANIA DONOVANI; PROTEIN SUBUNITS; PROTOZOAN PROTEINS;

LEISHMANIA DONOVANI;

EID: 38749133374     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20071286     Document Type: Article

References (35)

1. Champoux, J. J. (2001) DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70, 369-413
2. Liu, L. F. (1989) DNA topoisomerase poisons as antitumor drugs. Annu. Rev. Biochem. 58, 351-375
3. Wang, J. C. (1996) DNA topoisomerases. Annu. Rev. Biochem. 65, 635-692
4. Fortune, J. M. and Osheroff, N. (1998) Merbarone inhibits the catalytic activity of human topoisomerase II alpha by blocking DNA cleavage. J. Biol. Chem. 273, 17643-17650
5. Bridewell, D. J., Finlay, G. J. and Baguley, B. C. (1997) Differential actions of aclarubicin and doxorubicin: the role of topoisomerase I. Oncol. Res. 9, 535-542
6. Hsiang, Y. H., Hertzberg, R., Hecht, S. and Liu, L. F. (1985) Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I. J. Biol. Chem. 260, 14873-14878
7. Li, C. J., Averboukh, L. and Pardee, A. B. (1993) Beta-lapachone, a novel DNA topoisomerase I inhibitor with a mode of action different from camptothecin. J. Biol. Chem. 268, 22463-22468
8. Ray, S., Hazra, B., Mittra, B., Das, A. and Majumder, H. K. (1998) Diospyrin, an isnaphthoquinone: a novel inhibitor of type I DNA topoisomerase of Leishmania donovani. Mol. Pharmacol. 54, 994-999
9. Chowdhury, A. R., Mandal, S., Mittra, B., Sharma, S., Mukhopadhyay, S. and Majumder, H. K. (2002) Betulinic acid, a potent inhibitor of eukaryotic topoisomerase I: identification of the inhibitory step, the major functional group responsible and development of more potent derivatives. Med. Sci. Monit. 8, BR254-BR265
10. Chowdhury, A. R., Mandal, S., Goswami, A., Ghosh, M., Mandal, L., Chakraborty, D., Ganguly, A., Tripathi, G., Mukhopadhyay, S., Bandyopadhyay, S. and Majumder, H. K. (2003) Dihydrobetulinic acid induces apoptosis in Leishmania donovani by targeting DNA topoisomerase I and II: implications in antileishmanial therapy. Mol. Med. 9, 26-36
11. Chowdhury, A. R., Sharma, S., Mandal, S., Goswami, A., Mukhopadhyay, S. and Majumder, H. K. (2002) Luteolin, an emerging anti-cancer flavonoid, poisons eukaryotic DNA topoisomerase I. Biochem. J. 366, 653-661
12. Das, B. B., Sen, N., Ganguly, A. and Majumder, H. K. (2004) Reconstitution and functional characterization of the unusual bi-subunit type I DNA topoisomerase from Leishmania donovani. FEBS Lett. 565, 81-88
13. Das, B. B., Sen, N., Dasgupta, S. B., Ganguly, A. and Majumder, H. K. (2005) N-terminal region of the large subunit of Leishmania donovani bisubunit topoisomerase I is involved in DNA relaxation and interaction with the smaller subunit. J. Biol. Chem. 280, 16335-16344
14. Mittra, B., Saha, A., Chowdhury, A. R., Pal, C., Mandal, S., Mukhopadhyay, S., Bandyopadhyay, S. and Majumder, H. K. (2000) Luteolin, an abundant dietary component is a potent anti-leishmanial agent that acts by inducing topoisomerase II-mediated kinetoplast DNA cleavage leading to apoptosis. Mol. Med. 6, 527-541
15. Das, B. B., Sen, N., Roy, A., Dasgupta, S. B., Ganguly, A., Mohanta, B. C., Dinda, B. and Majumder, H. K. (2006) Differential induction of Leishmania donovani bi-subunit topoisomerase I-DNA cleavage complex by selected flavones and camptothecin: activity of flavones against camptothecin-resistant topoisomerase I. Nucleic Acids Res. 34, 1121-1132
16. Bodley, A. L. and Shapiro, T. A. (1995) Molecular and cytotoxic effects of camptothecin, a topoisomerase I inhibitor, on trypanosomes and Leishmania. Proc. Natl. Acad. Sci. U.S.A. 92, 3726-3730
17. Tiwari, R. K., Guo, L., Bradlow, H. L., Telang, N. T. and Osborne, M. P. (1994) Selective responsiveness of human breast cancer cells to indole-3-carbinol, a chemopreventive agent. J. Natl. Cancer Inst. 86, 126-131
18. Hong, C., Kim, H. A., Firestone, G. L. and Bjeldanes, L. F. (2002) 3,3′-Diindolylmethane (DIM) induces a G(1) cell cycle arrest in human breast cancer cells that is accompanied by Sp1-mediated activation of p21 (WAF1/CIP1) expression. Carcinogenesis 23, 1297-1305
19. Chen, I., McDougal, A., Wang, F. and Safe, S. (1998) Aryl hydrocarbon receptor-mediated antiestrogenic and antitumorigenic activity of diindolylmethane. Carcinogenesis 19, 1631-1639
20. Xue, L., Firestone, G. L. and Bjeldanes, L. F. (2005) DIM stimulates IFNgamma gene expression in human breast cancer cells via the specific activation of JNK and p38 pathways. Oncogene 24, 2343-2353
21. Hong, C., Firestone, G. L. and Bjeldanes, L. F. (2002) Bcl-2 family-mediated apoptotic effects of 3,3′-diindolylmethane (DIM) in human breast cancer cells. Biochem. Pharmacol. 63, 1085-1097
22. Rahman, K. W. and Sarkar, F. H. (2005) Inhibition of nuclear translocation of nuclear factor-κB contributes to 3,3′- diindolylmethane-induced apoptosis in breast cancer cells. Cancer Res. 65, 364-371
23. Riby, J. E., Xue, L., Chatterji, U., Bjeldanes, E. L., Firestone, G. L. and Bjeldanes, L. F. (2006) Activation and potentiation of interferon-gamma signaling by 3,3′-diindolylmethane in MCF-7 breast cancer cells. Mol. Pharmacol. 69, 430-439
24. Gong, Y., Firestone, G. L. and Bjeldanes, L. F. (2006) 3,3′-diindolylmethane is a novel topoisomerase II alpha catalytic inhibitor that induces S-phase retardation and mitotic delay in human hepatoma HepG2 cells. Mol. Pharmacol. 69, 1320-1327
25. Hertzberg, R. P., Caranfa, M. J. and Hecht, S. M. (1989) On the mechanism of topoisomerase I inhibition by camptothecin: evidence for binding to an enzyme-DNA complex. Biochemistry 28, 4629-4638
26. Sen, N., Das, B. B., Ganguly, A., Mukherjee, T., Tripathi, G., Bandyopadhyay, S., Rakshit, S., Sen, T. and Majumder, H. K. (2004) Camptothecin induced mitochondrial dysfunction leading to programmed cell death in unicellular hemoflagellate Leishmania donovani. Cell Death Differ. 11, 924-936
27. 3-HMTA as a methylene donor: one-pot synthesis of diindolylmethane (DIM) and its derivatives. Synthesis 11, 1779-1782
28. Osheroff, N., Shelton, E. R. and Brutlag, D. L. (1983) DNA topoisomerase II from Drosophila melanogaster. Relaxation of supercoiled DNA. J. Biol. Chem. 258, 9536-9543
29. Sen, N., Benerjee, B., Das, B. B., Ganguly, A., Sen, T., Paramanik, S., Mukhopadhyay, S. and Mahumder, H. K. (2006) Apoptosis is induced in leishmania cells by a novel protein kinase inhibitor withaferin A and is facilitated by apoptotic topoisomerase I-DNA complex. Cell Death Differ. 14, 358-367
30. Sengupta, T., Mukherjee, M., Das, A., Mandal, C., Das, R., Mukherjee, T. and Majumder, H. K. (2005) Characterization of the ATPase activity of topoisomerase II from Leishmania donovani and identification of residues conferring resistance to etoposide. Biochem. J. 390, 419-426
31. Isin, E. M. and Guengerich, F. P. (2006) Kinetics and thermodynamics of ligand binding by cytochrome P450 3A4. J. Biol. Chem. 281, 9127-9136
32. Guharay, J., Sengupta, B. and Sengupta, P. K. (2001) Protein-flavonol interaction: fluorescence spectroscopic study. Proteins 43, 75-81
33. Scatchard, G. (1949) The attraction of protein for small molecules and ions. Ann. N.Y. Acad. Sci. 51, 660-671
34. LePecq, J. B. and Paoletti, C. (1967) A fluorescent complex between ethidium bromide and nucleic acids. Physical-chemical characterization. J. Mol. Biol. 27, 87-106
35. Ganguly, A., Das, B. B., Sen, N., Roy, A., Dasgupta, S. B. and Majumder, H. K. (2006) 'LeishMan' topoisomerase I: an ideal chimera for unraveling the role of the small subunit of unusual bi-subunit topoisomerase I from Leishmania donovani. Nucleic Acids Res. 34, 6286-6297