Molecular determinants of topoisomerase I poisoning by lamellarins: Comparison with camptothecin and structure-activity relationships

Journal of Medicinal Chemistry

Volumn 48, Issue 11, 2005, Pages 3796-3807

  Marco, Esther ^a   Laine, William ^b   Tardy, Christelle ^b   Lansiaux, Amélie ^b   Iwao, Masatomo ^c   Ishibashi, Fumito ^c   Bailly, Christian ^b   Gago, Federico ^a  

^a UNIVERSITY OF ALCALÁ   (Spain)

^b CENTRE OSCAR LAMBRET   (France)

^c NAGASAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; CAMPTOTHECIN; CAMPTOTHECIN DERIVATIVE; DNA; DNA TOPOISOMERASE; DNA TOPOISOMERASE INHIBITOR; DOUBLE STRANDED DNA; GLUTAMIC ACID; HOMOCAMPTOTHECIN; HYDROGEN; HYDROXYL GROUP; LAMELLARIN D; LAMELLARIN DERIVATIVE; TOPOTECAN; UNCLASSIFIED DRUG;

AQUEOUS SOLUTION; ARTICLE; CELL LINE; CELL STRAIN CEM C2; CONTROLLED STUDY; DNA CLEAVAGE; DNA PROTEIN COMPLEX; DRUG SENSITIVITY; ENERGY; ENZYME INHIBITION; GC RICH SEQUENCE; HUMAN; HUMAN CELL; HYDROGEN BOND; INTERCALATION COMPLEX; MOLECULAR DYNAMICS; MOLECULAR MODEL; STRUCTURE ACTIVITY RELATION; THERMODYNAMICS;

ANTINEOPLASTIC AGENTS; CAMPTOTHECIN; CELL LINE, TUMOR; COMPUTER SIMULATION; COUMARINS; DNA TOPOISOMERASES, TYPE I; DRUG RESISTANCE, NEOPLASM; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HUMANS; INTERCALATING AGENTS; ISOQUINOLINES; MODELS, MOLECULAR; PROTEIN BINDING; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS;

EID: 20144369676     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm049060w     Document Type: Article

References (50)

1. 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.
2. Kim, D. K.; Lee, N. Recent advances in topoisomerase I-targeting agents, camptothecin analogues. Mini-Rev. Med. Chem. 2002, 2, 611-619.
3. Oberlies, N. H.; Kroll, D. J. Camptothecin and taxol: historic achievements in natural products research. J. Nat. Prod. 2004, 67, 129-135.
4. Thomas, C. J.; Rahier, N. J.; Hecht, S. M. Camptothecin: current perspectives. Bioorg. Med. Chem. 2004, 12, 1585-1604.
5. Mi, Z.; Burke, T. G. Differential interactions of camptothecin lactone and carboxylate forms with human blood components. Biochemistry 1994, 33, 10325-10336.
6. Fassberg, J.; Stella, V. J. A kinetic and mechanistic study of the hydrolysis of camptothecin and some analogues. J. Pharm. Sci. 1992, 81, 676-684.
7. Burke, T. G.; Mi, Z. Preferential binding of the carboxylate form of camptothecin by human serum albumin. Anal. Biochem. 1993, 212, 285-287.
8. Pourquier, P.; Pommier, Y. Topoisomerase I-mediated DNA damage. Adv. Cancer Res. 2001, 80, 189-216.
9. Lavergne, O.; Lesueur-Ginot, L.; Plá-Rodas, F.; Bigg, D. C. H. BN 80245: An E-ring modified camptothecin with potent anti-proliferative and topoisomerase I inhibitory activities. Bioorg. Med. Chem. Lett. 1997, 7, 2235-2238.
10. Bailly C. Homocamptothecins: potent topoisomerase I inhibitors and promising anticancer drugs. Crit. Rev. Oncol. Hematol. 2003, 45, 91-108.
11. Laco, G. S.; Du, W.; Kohlhagen, G.; Sayer, J. M.; Jerina, D. M.; Burke, T. G.; Curran, D. P.; Pommier, Y. Analysis of human topoisomerase I inhibition and interaction with the cleavage site +1 deoxyguanosine, via in vitro experiments and molecular modeling studies. Bioorg. Med. Chem. 2004, 12, 5225-5235.
12. Bailly, C.; Lansiaux, A.; Dassonneville, L.; Demarquay, D.; Coulomb, H.; Huchet, M.; Lavergne, O.; Bigg, D. C. H. Homocamptothecin, an E-ring modified camptothecin analog, generates new topoisomerase I-mediated DNA breaks. Biochemistry 1999, 38, 15556-15563.
13. Meng, L. H.; Liao, Z. Y.; Pommier, Y. Non-camptothecin DNA topoisomerase I inhibitors in cancer therapy. Curr. Top. Med. Chem. 2003, 3, 305-320.
14. Bailly, C. Lamellarins, from A to Z: a family of anticancer marine pyrrole alkaloids. Curr. Med Chem.: Anti-Cancer Agents 2004, 4, 363-378.
15. Andersen, R. J.; Faulkner, D. J.; Cun-heng, H.; Van Duyne, G. D.; Clardy, J. Metabolites of the marine prosobranch mollusc Lamellaria sp. J. Am. Chem. Soc. 1985, 107, 5492-5495.
16. Vanhuyse, M.; Kluza, J.; Tardy, C.; Otero, G.; Cuevas, C.; Bailly, C.; Lansiaux, A. Lamellarin D: A novel pro-apoptotic agent from marine origin insensitive to P-glycoprotein-mediated drug efflux. Cancer Lett. 2005, 221, 165-175.
17. Facompré, M.; Tardy, C.; Bal-Mayeu, C.; Colson, P.; Pérez, C.; Manzanares, I.; Cuevas, C.; Bailly, C. Lamellarin D: a novel potent inhibitor of topoisomerase I. Cancer Res. 2003, 63, 7392-7399.
18. Valler, M. J.; Green, D. Diversity screening versus focussed screening in drug discovery. Drug Discovery Today. 2000, 5, 286-293.
19. Tardy, C.; Facompré, M.; Laine M.; Baldeyrou, B.; García-Grávalos, D.; Francesch, A.; Mateo, C.; Pastor, A.; Jiménez, J. A.; Manzanares, I.; Cuevas, C.; Bailly, C. Topoisomerase I-mediated DNA cleavage as a guide to the development of antitumor agents derived from the marine alkaloid lamellarin D: Triester derivatives incorporating amino acid residues. Bioorg. Med. Chem. 2004, 12, 1697-1712.
20. Ishibashi, F.; Tanabe, S.; Oda, T.; Iwao, M. Synthesis and structure-activity relationship study of lamellarin derivatives. J. Nat. Prod. 2002, 65, 500-504.
21. Staker, B. L.; Hjerrild, K.; Feese, M. D.; Behnke, C. A.; Burgin, A. B., Jr.; Stewart, L. The mechanism of topoisomerase I poisoning by a camptothecin analog. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 15387-15392.
22. Been, M. D.; Burgess, R. R.; Champoux, J. J. Nucleotide sequence preference at rat liver and wheat germ type 1 DNA topoisomerase breakage sites in duplex SV40 DNA. Nucleic Acids Res. 1984, 12, 3097-3114.
23. Jaxel, C.; Capranico, G.; Kerrigan, D.; Kohn, K. W.; Pommier, Y. Effect of local DNA sequence on topoisomerase I cleavage in the presence or absence of camptothecin. J. Biol. Chem. 1991, 266, 20418-20423.
24. Fujimori, A.; Harker, W. G.; Kohlhagen, G.; Hoki, Y.; Pommier, Y. Mutation at the catalytic site of topoisomerase I in CEM/C2, a human leukemia cell line resistant to camptothecin. Cancer Res. 1995, 55, 1339-1346.
25. Chrencik, J. E.; Staker, B. L.; Burgin, A. B.; Pourquier, P.; Pommier, Y.; Lance, S.; Redinbo, M. R. Mechanisms of camptothecin resistance by human topoisomerase I mutations. J. Mol. Biol. 2004, 339, 773-784.
26. PDB entries 1k4t, 1rr8, and 1rrj, respectively.
27. Redinbo, M. R.; Stewart, L.; Kuhn, P.; Champoux, J. J.; Hol, W. G. J. Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 1998, 279, 1504-1513.
28. Redinbo, M. R.; Stewart, L.; Champoux, J. J.; Hol, W. G. Structural flexibility in human topoisomerase I revealed in multiple non-isomorphous crystal structures. J. Mol. Biol. 1999, 292, 685-696.
29. García-Nieto, R.; Manzanares, I.; Cuevas, C.; Gago, F. Bending of DNA upon binding of ecteinascidin 743 and phthalascidin 650 studied by unrestrained molecular dynamics simulations. J. Am. Chem. Soc. 2000, 122, 7172-7182.
30. Marco, E.; García-Nieto, R.; Gago, F. Assessment by molecular dynamics simulations of the structural determinants of DNA-binding specificity for transcription factor Sp1. J. Mol. Biol. 2003, 328, 9-32.
31. Marco, E.; García-Nieto, R.; Mendieta, J.; Manzanares, I.; Cuevas, C.; Gago, F. A 3·(ET743)-DNA complex that both resembles an RNA-DNA hybrid and mimics zinc finger-induced DNA structural distortions. J. Med. Chem. 2002, 45, 871-880.
32. Marco, E.; Martín-Santamaría, S.; Cuevas, C.; Gago, F. Structural basis for the binding of didemnins to human elongation factor eEF1A and rationale for the potent antitumor activity of these marine natural products. J. Med. Chem. 2004, 47, 4439-4452.
33. Fiorani, P.; Bruselles, A.; Falconi, M.; Chillemi, G.; Desideri, A.; Benedetti, P. Single mutation in the linker domain confers protein flexibility and camptothecin resistance to human topoisomerase I. J. Biol. Chem. 2003, 278, 43268-43275.
34. Pearlman, D. A.; Charifson, P. S. Are free energy calculations useful in practice? A comparison with rapid scoring functions for the p38 MAP kinase protein system. J. Med. Chem. 2001, 44, 3417-3423.
35. de la Fuente, J. A.; Manzanaro, S.; Martín, M. J.; de Quesada, T. G.; Reymundo, I., Luengo, S. M.; Gago, F. Synthesis, activity, and molecular modeling studies of novel human aldose reductase inhibitors based on a marine natural product. J. Med. Chem. 2003, 46, 5208-5221.
36. Laco, G. S.; Collins, J. R.; Luke, B. T.; Kroth, H.; Sayer, J. M.; Jerina, D. M.; Pommier, Y. Human topoisomerase I inhibition: docking camptothecin and derivatives into a structure-based active site model. Biochemistry 2002, 41, 1428-1435.
37. Rossi, F.; Labourier, E.; Forné, T.; Divita, G.; Derancourt, J.; Riou, J. F.; Antoine, E.; Cathala, G.; Brunel, C.; Tazi, J. Specific phosphorylation of SR proteins by mammalian DNA topoisomerase I. Nature 1996, 381, 80-82.
38. Bailly, C. DNA relaxation and cleavage assays to study topoisomerase I inhibitors. Methods Enzymol. 2001, 340, 610-623.
39. Cieplak, P.; Cornell, W. D.; Bayly, C. I.; Kollman, P. A. Application of the multimolecule and multiconformational RESP methodology to biopolymers: charge derivation for DNA, RNA and proteins. J. Comput. Chem. 1995, 16, 1357-1377.
40. Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. M.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 1995, 117, 5179-5197.
41. Åqvist, J. Ion-water interaction potentials derived from free energy perturbation simulations. J. Phys. Chem. 1990, 94, 8021-8024.
42. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 1983, 79, 926-935.
43. URL: http://amber.scripps.edu/doc8/.
44. Ryckaert, J. P.; Ciccoti, G.; Berendsen, H. J. C. Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 1977, 23, 327-341.
45. URL: http://amber.scripps.edu/doc6/.
46. Pearlmann, D. A. Determining the contributions of constraints in free energy calculations: development, characterization, and recommendations. J. Chem. Phys. 1993, 98, 8946-8957.
47. Insight II, version 98.0; Molecular Simulations Inc. (9685 Scranton Road, San Diego, CA 92121-2777), 1998.
48. Gallego, J.; Ortiz, A. R.; de Pascual-Teresa, B.; Gago, F. Structure-affinity relationships for the binding of actinomycin D to DNA. J. Comput.-Aided Mol. Des. 1997, 11, 114-128.
49. Pérez, C.; Ortiz, A. R.; Pastor, M.; Gago, F. Comparative binding energy analysis of HIV-1 protease inhibitors: incorporation of solvent effects and validation as a powerful tool in receptor-based drug design. J. Med. Chem. 1998, 41, 836-852.
50. Staker, B. L.; Feese, M. D.; Cushman, M.; Pommier, Y.; Zembower, D.; Stewart, L.; 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.