Investigation of the lactam side chain length necessary for optimal indenoisoquinoline topoisomerase I inhibition and cytotoxicity in human cancer cell cultures

Journal of Medicinal Chemistry

Volumn 50, Issue 9, 2007, Pages 2040-2048

  Morrell, Andrew ^a   Placzek, Michael S ^a   Steffen, Jamin D ^a   Antony, Smitha ^b   Agama, Keli ^b   Pommier, Yves ^b   Cushman, Mark ^a  

^a PURDUE UNIVERSITY   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINE; CARBON; DNA TOPOISOMERASE INHIBITOR; INDENOISOQUINOLINE DERIVATIVE; ISOQUINOLINE DERIVATIVE; LACTAM DERIVATIVE; NITROGEN; TOPOTECAN; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; CULTURE MEDIUM; DRUG CYTOTOXICITY; DRUG POTENCY; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME INHIBITION; HUMAN; HUMAN CELL; INFRARED SPECTROMETRY; REACTION ANALYSIS; STRUCTURE ANALYSIS;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; DNA TOPOISOMERASES, TYPE I; DRUG SCREENING ASSAYS, ANTITUMOR; HUMANS; INDENES; ISOQUINOLINES; LACTAMS; MODELS, MOLECULAR; PYRIDINES;

EID: 34247613433     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm0613119     Document Type: Article

References (41)

1. Wang, J. C. DNA Topoisomerases. Annu. Rev. Biochem. 1996, 65, 635-692.
2. Nitiss, J. L. Investigating the Biological Functions of DNA Topoisomerases in Eukaryotic Cells. Biochim. Biophys. Acta 1998, 1400, 63-81.
3. Champoux, J. J. DNA Topoisomerases: Structure, Function, and Mechanism. Annu. Rev. Biochem. 2001, 70, 369-413.
4. Wang, J. C. Cellular Roles of DNA Topoisomerases: A Molecular Perspective. Nat. Rev. Mol. Cell Biol. 2002, 3, 430-440.
5. Hsiang, Y. H.; Hertzberg, R.; Hecht, S.; Liu, L. F. Camptothecin Induces Protein-Linked DNA Breaks via Mammalian DNA Topoisomerase I. J. Biol. Chem. 1985, 260, 14873-14878.
6. Pommier, Y.; Pourquier, P.; Fan, Y.; Strumberg, D. Mechanism of Action of Eukaryotic DNA Topoisomerase I and Drugs Targeted to the Enzyme. Biochim. Biophys. Acta 1998, 1400, 83-106.
7. Takimoto, C. H.; Wright, J.; Arbuck, S. G. Clinical Applications of the Camptothecins. Biochim. Biophys. Acta 1998, 1400, 107-119.
8. Pommier, Y. Topoisomerase I Inhibitors: Camptothecins and Beyond. Nat. Rev. Cancer 2006, 6, 789-802.
9. Jaxel, C.; Kohn, K. W.; Wani, M. C.; Wall, M. E.; Pommier, Y. Structure-Activity Study of the Actions of Camptothecin Derivatives on Mammalian Topoisomerase I: Evidence for a Specific Receptor Site and a Relation to Antitumor Activity. Cancer Res. 1989, 49, 1465-1469.
10. Minami, H.; Beijnen, J. H.; Verweij, J.; Ratain, M. J. Limited Sampling Model for Area Under the Concentration Time Curve of Total Topotecan. Clin. Cancer Res. 1996, 2 (1), 43-46.
11. Danks, M. K.; Pawlik, C. A.; Whipple, D. O.; Wolverton, J. S. Intermittent Exposure of Medulloblastoma Cells to Topotecan Produces Growth Inhibition Equivalent to Continuous Exposure. Curr. Top. Med. Chem. 1997, 3 (10), 1731-1738.
12. Haas, N. B.; LaCreta, F. P.; Walczak, J.; Hudes, G. R.; Brennan, J. M.; Ozols, R. F.; O'Dwyer, P. J. Phase-I Pharmacokinetic Study of Topotecan by 24-Hour Continuous-Infusion Weekly. Cancer Res. 1994, 54 (5), 1220-1226.
13. Kohlhagen, G.; Paull, K. D.; Cushman, M.; Nagafuji, P.; Pommier, Y. Protein-Linked DNA Strand Breaks Induced by NSC 314622, a Novel Noncamptothecin Topoisomerase I Poison. Mol. Pharmacol. 1998, 54, 50-58.
14. Staker, B. L.; Hjerrild, K.; Feese, M. D.; Behnke, C. A.; Burgin, Jr., A. B.; Stewart, L. The Mechanism of Topoisomerase I Poisoning by a Camptothecin Analog. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 15387-15392.
15. Staker, B. L.; Feese, M. D.; Cushman, M.; Pommier, Y.; Zembower, D. L. S.; Burgin, A. B. Structures of Three Classes of Anticancer Agents Bound to the Human Topoisomerase I-DNA Covalent Complex. J. Med. Chem. 2005, 48, 2336-2345.
16. Ioanoviciu, A.; Antony, S.; Pommier, Y.; Staker, B. L.; Stewart, L.; Cushman, M. Synthesis and Mechanism of Action Studies of a Series of Norindenoisoquinoline Topoisomerase I Poisons Reveal an Inhibitor with a Flipped Orientation in the Ternary DNA-Enzyme-Inhibitor Complex As Determined by X-ray Crystallographic Analysis. J. Med. Chem. 2005, 48, 4803-4814.
17. Marchand, C.; Antony, S.; Kohn, K. W.; Cushman, M.; Ioanoviciu, A.; Staker, B. L.; Burgin, A. B.; Stewart, L.; Pommier, Y. A Novel Norindenoisoquinoline Structure Reveals a Common Interfacial Inhibitor Paradigm for Ternary Trapping of the Topoisomerase I-DNA Covalent Complex. Mol. Cancer Ther. 2006, 5, 287-295.
18. Xiao, X.; Cushman, M. An Ab Initio Quantum Mechanics Calculation that Correlates with Ligand Orientation and DNA Cleavage Site Selectivity in Camptothecin-DNA-Topoisomerase I Ternary Cleavage Complexes. J. Am. Chem. Soc. 2005, 127, 9960-9961.
19. Nagarajan, M.; Morrell, A.; Fort, B. C.; Meckley, M. R.; Antony, S.; Kohlhagen, G.; Pommier, Y.; Cushman, M. Synthesis and Anticancer Activity of Simplified Indenoisoquinoline Topoisomerase I Inhibitors Lacking Substituents on the Aromatic Rings. J. Med. Chem. 2004, 47, 5651-5661.
20. Strumberg, D.; Pommier, Y.; Paull, K.; Jayaraman, M.; Nagafuji, P.; Cushman, M. Synthesis of Cytotoxic Indenoisoquinoline Topoisomerase I Poisons. J. Med. Chem. 1999, 42, 446-457.
21. Cushman, M.; Jayaraman, M.; Vroman, J. A.; Fukunaga, A. K.; Fox, B. M.; Kohlhagen, G.; Strumberg, D.; Pommier, Y. Synthesis of New Indeno[1,2-c] isoquinolines: Cytotoxic Non-Camptothecin Topoisomerase I Inhibitors. J. Med. Chem. 2000, 43, 3688-3698.
22. Jayaraman, M.; Fox, B. M.; Hollingshead, M.; Kohlhagen, G.; Pommier, Y.; Cushman, M. Synthesis of New Dihydroindeno[1,2-c]isoquinoline and Indenoisoquinolinium Chloride Topoisomerase I Inhibitors Having High In Vivo Anticancer Acitivity in the Hollow Fiber Animal Model. J. Med. Chem. 2002, 45, 242-249.
23. Fox, B. M.; Xiao, X.; Antony, S.; Kohlhagen, G.; Pommier, Y.; Staker, B. L.; Stewart, L.; Cushman, M. Design, Synthesis, and Biological Evaluation of Cytotoxic 11-Alkenylindenoisoquinoline Topoisomerase I Inhibitors and Indenoisoquinoline-Camptothecin Hybrids. J. Med. Chem. 2003, 46, 3275-3282.
24. Nagarajan, M.; Xiao, X.; Antony, S.; Kohlhagen, G.; Pommier, Y.; Cushman, M. Design, Synthesis, and Biological Evaluation of Indenoisoquinoline Topoisomerase I Inhibitors Featuring Polyamine Side Chains on the Lactam Nitrogen. J. Med. Chem. 2003, 46, 5712-5724.
25. Antony, S.; Jayaraman, M.; Laco, G.; Kohlhagen, G.; Kohn, K. W.; Cushman, M.; Pommier, Y. Differential Induction of Topoisomerase I-DNA Cleavage Complexes by the Indenoisoquinoline MJ-III-65 (NSC 706744) and Camptothecin: Base Sequence Analysis and Activity against Camptothecin-Resistant Topoisomerase I. Cancer Res. 2003, 63, 7428-7435.
26. Morrell, A.; Antony, S.; Kohlhagen, G.; Pommier, Y.; Cushman, M. Synthesis of Nitrated Indenoisoquinolines as Topoisomerase I Inhibitors. Bioorg. Med. Chem. Lett. 2004, 14, 3659-3663.
27. Xiao, X.; Antony, S.; Kohlhagen, G.; Pommier, Y.; Cushman, M. Design, Synthesis, and Biological Evaluation of Cytotoxic 11- Aminoalkenylindenoisoquinoline and 11-Diaminoalkenylindenoisoquinoline Topoisomerase I Inhibitors. Bioorg. Med. Chem. 2004, 12, 5147-5160.
28. Antony, S.; Kohlhagen, G.; Agama, K.; Jayaraman, M.; Cao, S.; Durrani, F. A.; Rustum, Y. M.; Cushman, M.; Pommier, Y. Cellular Topoisomerase I Inhibition and Antiproliferative Activity by MJ-III-65 (NSC 706744), an Indenoisoquinoline Topoisomerase I Poison. Mol. Pharmacol. 2005, 67, 523-530.
29. Morrell, A.; Antony, S.; Kohlhagen, G.; Pommier, Y.; Cushman, M. Synthesis of Benz[d]indeno[1,2-b]pyran-5,11-diones: Versatile Intermediates for the Design and Synthesis of Topoisomerase I Inhibitors. Bioorg. Med. Chem. Lett. 2006, 16, 1846-1849.
30. Morrell, A.; Jayaraman, M.; Nagarajan, M.; Fox, B. M.; Meckley, M. R.; Ioanoviciu, A.; Pommier, Y.; Antony, S.; Hollingshead, M.; Cushman, M. Evaluation of Indenoisoquinoline Topoisomerase I Inhibitors Using a Hollow Fiber Assay. Bioorg. Med. Chem. Lett. 2006, 16, 4395-4399.
31. Skehan, P.; Storeng, R.; Scudiero, D.; Monks, A.; McMahon, J. New Colorimetric Cytotoxicity Assay for Anticancer-Drug Screening. J. Natl. Cancer Inst. 1990, 82 (13), 1107-1112.
32. Boyd, M. R.; Paull, K. D. Some Practical Considerations and Applications of the National Cancer Institute In-Vitro Anticancer Drug Discovery Screen. Drug Dev. Res. 1995, 34, 91-109.
33. Nagarajan, M.; Morrell, A.; Antony, S.; Kohlhagen, G.; Agama, K.; Hollingshead, M.; Pommier, Y.; Cushman, M. Synthesis and Biological Evaluation of Bisindenoisoquinolines as Topoisomerase I Inhibitors. J. Med. Chem. 2006, 49, 5129-5140.
34. Nagarajan, M.; Morrell, A.; Ioanoviciu, A.; Antony, S.; Kohlhagen, G.; Hollingshead, M.; Pommier, Y.; Cushman, M. Synthesis and Evaluation of Indenoisoquinoline Topoisomerase I Inhibitors Substituted with Nitrogen Heterocycles. J. Med. Chem. 2006, 49, 6283-6289.
35. Demant, E. J. F.; Friche, E. Equilibrium Binding of Anthracycline Cytostatics to Serum Albumin and Small Unilamellar Phospholipid Vesicles as Measured by Gel Filtration. Biochem. Pharmacol. 1998, 55, 27-32.
36. Demant, E. J. F.; Friche, E. Kinetics of Anthracycline Accumulation in Multidrug-resistant Tumor Cells: Relationship to Drug Lipophilicity and Serum Albumin Binding. Biochem. Pharmacol. 1998, 56, 1209-1217.
37. Stermitz, F. R.; Gillespie, J. P.; Amoros, L. G.; Romero, R.; Stermitz, T. A. Synthesis and Biological Activity of Some Antitumor Benzophenanthridinium Salts. J. Med. Chem. 1975, 18, 708-713.
38. Cushman, M.; Mohan, P.; Smith, E. C. R. Synthesis and Biological Activity of Structural Analogues of the Anticancer Benzophenanthridine Alkaloid Nitidine Chloride. J. Med. Chem. 1984, 27, 544-547.
39. Fang, S.-D.; Wang, L.-K.; Hecht, S. M. Inhibitors of DNA Topoisomerase I Isolated from the Roots of Zanthoxylum nitidum. J. Org. Chem. 1993, 58, 5025-5027.
40. Sethi, M. L. Inhibition of Reverse Transcriptase Activity by Benzophenanthridine Alkaloids. J. Nat. Prod. 1979, 42, 187-196.
41. Pourquier, P.; Ueng, L.-M.; Fertala, J.; Wang, D.; Park, H.-K.; Essigmann, J. M.; Bjornsti, M.-A.; Pommier, Y. Induction of Reversible Complexes Between Eukaryotic DNA Topoisomerase I and DNA-containing Oxidative Base Damages. 7,8-Dihydro-8-Oxoguanine and 5-Hydroxycytosine. J. Biol. Chem. 1999, 274, 8516-8523.