The role of polyamine architecture on the pharmacological activity of open lactone camptothecin-polyamine conjugates

Bioconjugate Chemistry

Volumn 19, Issue 11, 2008, Pages 2270-2279

  Samor, Cristian ^a   Guerrini, Andrea ^a   Varchi, Greta ^a   Beretta, Giovanni Luca ^b   Fontana, Gabriele ^c   Bombardelli, Ezio ^c   Carenini, Nives ^b   Zunino, Franco ^b   Bertucci, Carlo ^d   Fiori, Jessica ^d   Battaglia, Arturo ^a  

^a CNR   (Italy)

^b NATIONAL CANCER INSTITUTE   (Italy)

^c INDENA S P A   (Italy)

^d UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHITECTURE; BODY FLUIDS; CELL CULTURE; DNA;

AMMONIUM CATIONS; CAMPTOTHECINS; GROWTH INHIBITION; PHARMACOLOGICAL ACTIVITY; POLYAMINE CONJUGATES; POLYAMINES; POSITIVELY CHARGED; SIDE-CHAINS; SPERMIDINE; SYNTHESISED;

ESTERS;

17 ACETYLCAMPTOTHECIN 21 BENZYLAMIDE; 17 ACETYLCAMPTOTHECIN 21 BENZYLESTER; 17 ACETYLCAMPTOTHECINIC ACID; 4,8,13,17 TETRAZAICOSANE 1,20 DIAMINE; 7 ETHYL 10 HYDROXYCAMPTOTHECIN; AMIDE; AMINE; AMMONIA; CAMPTOTHECIN; CAMPTOTHECIN DERIVATIVE; CARBOXYLIC ACID DERIVATIVE; CATION; DNA TOPOISOMERASE; ETHANE 1,2 DIAMINE; HOMOSPERMIDINE; LACTONE; POLYAMINE; SPERMIDINE; TOPOTECAN; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; CANCER CELL CULTURE; CANCER INHIBITION; CELL PROLIFERATION; CHEMICAL BOND; CORRELATION ANALYSIS; DNA CLEAVAGE; DNA DAMAGE; DRUG ACETYLATION; DRUG CONJUGATION; DRUG EFFECT; DRUG INTERACTION; DRUG POTENCY; DRUG STRUCTURE; DRUG SYNTHESIS; HUMAN; HUMAN CELL; HYDROPHILICITY; IN VITRO STUDY; LIPOPHILICITY; LONG TERM EXPOSURE; LUNG NON SMALL CELL CANCER;

EID: 56749151286     PISSN: 10431802     EISSN: None     Source Type: Journal    
DOI: 10.1021/bc800033r     Document Type: Article

References (74)

1. 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.
2. Wang, J. C. (1996) DNA topoisomerases. Annu. Rev. Biochem. 65, 635-692.
3. Champoux, J. J. (1998) Domains of human topoisomerase I and associated functions. Prog. Nucleic Acid Res. Mol. Biol. 60, 111-132.
4. Wu, J. X., and Liu, L. F. (1997) Processing of topoisomerase I cleavable complexes into DNA damage by transcription. Nucleic Acids Res. 25, 4181-4186.
5. Redinbo, M. R., Stewart, L., Kuhn, P., Champoux, J. J., and Hol, W. G. J. (1998) Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279, 1504-1513.
6. Staker, B. L., Feese, M. D., Cushman, M., Pommier, Y., Zembower, D., Stewart, L., and Burgin, A. B. (2005) Structures of three classes of anticancer agents bound to the human topoisomerase I-DNA covalent complex. J. Med. Chem. 48, 2336-2345.
7. Marchand, C., Antony, S., Kohn, K. W., Cushman, M., Ioanoviciu, A., Staker, B. L., Burgin, A. B., Lance Stewart, L., and Pommier, Y. (2006) A novel norindenoisoquinoline structure reveals a common interfacial inhibitor paradigm for ternary trapping of the topoisomerase I-DNA covalent complex. Mol. Cancer Ther. 5, 287-295.
8. Sanna, N., Chillemi, G., Grandi, A., Castelli, S., Desideri, A., and Barone, V. (2005) New hints on the pH-driven tautomeric equilibria of the topotecan anticancer drug in aqueous solutions from an integrated spectroscopic and quantum-mechanical approach. J. Am. Chem. Soc. 127, 15429-15436.
9. Bocian, W., Kawecki, R., Bednarek, E., Sitkowski, J., Pietrzyk, A., Williamson, M. P., Hansen, P. E., and Kozerski, L. (2004) Multiple binding modes of the camptothecin family to DNA oligomers. Chem. Eur. J. 10, 5776-5787.
10. Fan, Y., Weinstein, J. N., Kohn, K. W., Shi, L. M., and Pommier, Y. (1998) Molecular modeling studies of the DNA-topoisomerase I ternary cleavable complex with camptothecin. J. Med Chem. 41, 2216-2226.
11. Kerrigan, J. E., and Pilch, D. S. (2001) A structural model for the ternary cleavable complex formed between human topoisomerase I, DNA, and camptothecin. Biochemistry 40, 9792-9798.
12. Laco, G. S., Collins, J. R., Luke, B. T., Kroth, H., Sayer, J. M., Jerina, D. M., and Pommier, Y. (2002) Human topoisomerase I inhibition: Docking camptothecin and derivatives into a structure-based active site model. Biochemistry 41, 1428-1435.
13. Lauria, A., Ippolito, M., and Almerico, A. M. (2007) Molecular docking approach on the Topoisomerase I inhibitors series included in the NCI anti-cancer agents mechanism database. J. Mol. Modeling 13, 393-400.
14. Xiao, X., and Cushman, M. (2005) Effect of E-ring modifications in camptothecin on topoisomerase I inhibition: A quantum mechanics treatment. J. Org. Chem. 70, 9584-9587.
15. Gupta, M., Fujimori, A., and Pommier, Y. (1995) Eukariotic DNA topoisomerases-I. Biochim. Biophys. Acta 1262, 1-14.
16. Wall, M. E. (1969) Biochemie und Physiologie der Alkaloide (Mothes, K., and Schreiber, K., Eds.) pp 77-87, Akademie Verlag, Berlin.
17. Slichenmeyer, W. J., Rowinsky, E. K., Donehower, R. C., and Kaufman, S. H. (1993) The current status of camptothecin analogs as antitumour agents. J. Natl. Cancer Inst. 85, 271-291.
18. Wani, M. C., Nicholas, A. W., Manikumar, G., and Wall, M. E. (1987) Plant antitumor agents. Total synthesis oand antileukemic activity of ring A substituted camptothecin analogs. Structure activity correlations. J. Med. Chem. 30, 1774-1779.
19. Giovanella, B. C., Hinz, H. R., Kozielski, A. J., Stehlin, J. S., Silber, R., and Potmesil, M. (1991) Complete growth-inhibition of human cancer xenografts in nude-mice by treatment with 20-(S)-camptothecin. Cancer Res. 51, 3052-3055.
20. Fleury, F., Kudelina, I., and Nabiev, I. (1997) Interactions of lactone, carboxylate and self-aggregated forms of camptothecin with human and bovine serum albumins. FEBS Lett. 406, 151-156.
21. Mi, Z., and Burke, T. G. (1994) Marked interspecies variations concerning the interactions of camptothecin with serum albumins - a frequency-domain fluorescence spectroscopic study. Biochemistry 33, 12540-12545.
22. Kingsbury, W. D., Bohem, J C., Jakas, D. R., Holden, K. G., Hecht, S. M., Gallagher, G., Carafa, M. J., McCabe, F. L., Faucette, L. F., Johnson, R. K., and Hertzberg, R. P. (1991) Synthesis of water-soluble (aminoalkyl)camptothecin analogs - inhibition of topoisomerase-i and antitumor-activity. J. Med. Chem. 34, 98-107.
23. Masuda, N., Fukuoka, Y., Kusunoki, K., Matsui, N., Takifuji, S., Kudoly, S., Negoro, M., Nishioka, K., Nakagawa, H., and Takada, J. (1992) A new derivative of camptothecin for the treatment of refractory or relapsed small-cell lung-cancer. J. Clin. Oncol. 10, 1225-1229.
24. Macdonald, J. S., Benedetti, J. K., Modiano, M., and Alberts, D. S. (1997) Phase II evaluation of topotecan in patients with advanced colorectal cancer - A Southwest Oncology Group Trial (SWOG 9241). Invest. New Drugs 15, 357-359.
25. Saltz, L. B., Schwartz, G. K., Ilson, D. H., Quan, V., and Kelsen, D. P. (1997) A phase II study of topotecan administered five times daily in patients with advanced gastric cancer. Am. J. Clin. Oncol. 20, 621-625.
26. http://www.pharmcast.com/WarningLetters/Yr2003/Nov2003/Pfizer1103.htm.
27. Dubowchik, G. M., and Walker, M. A. (1999) Receptor-mediated and enzyme-dependent targeting of cytotoxic anticancer drugs. Pharmacol. Ther. 83, 67-123.
28. Huang, P. S., and Oliff, A. (2001) Drug-targeting strategies in cancer therapy. Curr. Opin. Gen. Dev. 11, 104-110.
29. De Groot, F. M. H., Damen, E. W. P., and Scheeren, H. W. (2001) Anticancer prodrugs for application in monotherapy: Targeting hypoxia, tumor-associated enzymes, and receptors. Curr. Med. Chem. 8, 1093-1122.
30. Fassberg, J., and Stella, V. J. (1992) A kinetic and mechanistic study of the hydrolysis of camptothecin and some analogs. J. Pharm. Sci. 81, 676-684.
31. Zhao, H., Lee, C., Sai, P., Choe, Y. H., Boro, M., Pendri, A., Guan, S., and Greenwald, R. B. (2000) 20-O-acylcamptothecin derivatives: Evidence for lactone stabilization. J. Org. Chem. 65, 4601-4606.
32. Yang, L.-X., Pan, X., and Wang, H.-J. (2002) Novel camptothecin derivatives. Part 1: Oxyalkanoic acid esters of camptothecin and their in vitro and in vivo antitumor activity. Bioorg. Med. Chem. Lett. 12, 1241-1244.
33. Cao, Z., Harris, N., Kozielski, A., Vardeman, D., Stehlin, J. S., and Giovanella, B. (1998) Alkyl esters of camptothecin and 9-nitrocamptothecin: Synthesis, in vitro pharmacokinetics, toxicity, and antitumor activity. J. Med. Chem. 41, 31-37.
34. De Groot, F. M. H., Busscher, G. F., Aben, R. W. M., and Scheeren, H. W. (2002) Novel 20-carbonate linked prodrugs of camptothecin and 9-aminocamptothecin designed for activation by tumour-associated plasmin. Bioorg. Med. Chem. Lett. 12, 2371-2376.
35. Lerchen, H.-G., and Von dem Bruch, K. (2000) Synthesis of 20-O-linked 20(S)-camptothecin glycoconjugates: Impact of the side chain of the ester-linked amino acid on epimerization during the acylation reaction and on hydrolytic stability of the final glycoconjugates. J. Prakt. Chem. 342, 753-760.
36. Prijovicha, Z. M., Leub, Y.-L., and Roffler, S. R. (2003) Stability of the new prodrug 9-aminocamptothecin glucuronide (9ACG) in the presence of human serum albumin. Biochem. Pharmacol. 66, 1181-1187.
37. Matteucci, M., Lin, K.-Y., Huang, T., Wagner, R., Sternbach, D. D., Mehrotra, M., and Besterman, J. M. (1997) Sequence-specific targeting of duplex DNA using a camptothecin triple helix forming oligonucleotide conjugate and topoisomerase I. J. Am. Chem. Soc. 119, 6939-6940.
38. Arimondo, P. B., Boutorine, A., Baldeyrou, B., Bailly, C., Kuwahara, M., Hecht, S. M., Sun, J.-S., Garestier, T., and Hél̀ene, C. (2002) Design and optimization of camptothecin conjugates of triple helix-forming oligonucleotides for sequence-specific DNA cleavage by topoisomerase. J. Biol. Chem. 277, 3132-3140.
39. Arimondo, P. B., Angenault, S., Halby, L., Boutorine, A., Schmidt, F., Monneret, C., Garestier, T., Sun, J.-S., Bailly, C., and Hélène, C. (2003) Spatial organization of topoisomerase I-mediated DNA cleavage induced by camptothecin-oligonucleotide conjugates. Nucleic Acids Res. 31, 4031-4040.
40. Arimondo, P. B., Bailly, C., Boutorine, A., Ryabinin, V., Syniakov, A., Sun, J.-S., Garestier, T., and Hélène, C. (2001) Directing topoisomerase I mediated DNA cleavage to specific sites by camptothecin tethered to minor- and major-groove ligands. Angew. Chem., Int. Ed. 40, 3045-3048.
41. Wang, C. C., and Dervan, P. B. (2001) Sequence-specific trapping of Topoisomerase I by DNA binding polyamide-camptothecin conjugates. J. Am. Chem. Soc. 123, 8657-8661.
42. Adamovics, J. A., and Hutchinson, C. R. (1979) Prodrug analogs of the anti-tumor alkaloid camptothecin. J. Med. Chem. 3, 310-314.
43. Sawada, S., Yaegashi, T., Furuta, T., Yokokura, T., and Miyasaka, T. (1993) Chemical modification of an antitumor alkaloid, 20(S)-camptothecin: E-lactone ring-modified water-soluble derivatives of 7ethylcamptothecin. Chem. Pharm. Bull. 41, 310-313.
44. Ogawa, T., Yaegashi,T., Sawada, S., Furuta, T. (2001) U.S. Patent 6,310,210 B1.
45. Greenwald, R. B., Zhao, H., and Xia, J. (2003) Tripartate poly(ethylene glycol) prodrugs of the open lactone form of camptothecin. Bioorg. Med. Chem. 11, 2635-2639.
46. 1-dimediylaminoetiiyl amide dipartates are not stable enough to survive cell tissue culture experiments, undergoing rapid cyclization to the lactone form at physiological pH. Hence, compound 4 should be in vitro active.
47. Beretta, G. L., Petrangolini, G., De.Cesare, M., Pratesi, G., Perego, P., Tinelli, S., Tortoreto, M., Zucchetti, M., Frapolli, R., Bello, E., Manzotti, C., Fontana, G., Bombardelli, E., Battaglia, A., Samorì, C., and Zunino, F. (2006) Biological properties of IDN5174, a new synthetic camptothecin with the open lactone ring. Cancer Res. 66, 10976-10982.
48. Cohen, S. S. (1998) A Guide to the Polyamines, Oxford University Press, Oxford.
49. Igarashi, K., and Kashiwagi, K. (2000) Polyamines: Mysterious modulators of cellular functions. Biochem. Biophys. Res. 271, 559-564.
50. Yoshida, M., Kashiwagi, K., Shigemasa, A., Taniguchi, S., Yamamoto, K., Makinoshima, H., Ishihama, A., and Igarashi, K. (2004) A unifying model for the role of polyamines in bacterial cell growth, the polyamine modulon. J. Biol. Chem. 279, 46008-46013.
51. Cullis, P. M., Green, R. E., Merson.Davies, L., and Travis, N. (1999) Probing the mechanism of transport and compartmentalisation of polyamines in mammalian cells. Chem. Biol. 6, 717-729, and references therein.
52. Bloomfield, V. A. (1997) DNA condensation by multivalent cations. Biopolymers 44, 269-282.
53. Feuerstein, B. G., Williams, L. D., Basu, H. S., and Marton, L. J. (1991) Implications and concepts of polyamine-nucleic acid interactions. J. Cell Biochem. 46, 37-47.
54. Kashiwagi, K., Yamaguchi, Y., Sakai, Y., Kobayashi, H., and Igarashi, K. (1990) Identification of the polyamine-induced protein as a periplasmic oligopeptide binding-protein. J. Biol. Chem. 265, 8387-8391.
55. Fukuchi, J., Hiipakka, R. A., Kokontis, J. M., Nishimura, K., Igarashi, K., and Liao, S. (2004) TATA-binding protein-associated factor 7 regulates polyamine transport activity and polyamine analog-induced apoptosis. J. Biol. Chem. 279, 29921-29929.
56. Uemura, T., Tachihara, K., Tomitori, H., Kashiwagi, K., and Igarashi, K. (2005) Characteristics of the polyamine transporter TPO1 and regulation of its activity and cellular localization by phosphorylation. J. Biol. Chem. 280, 9646-9652.
57. Mani, K., Sandgren, S., Lilja, J., Cheng, F., Svensson, K., Persson, L., and Belting, M. (2007) HIV-Tat protein transduction domain specifically attenuates growth of polyamine deprived tumor cells. Mol. Cancer Ther. 6, 782-788.
58. Vassylyev, D. G., Tomitori, H., Kashiwagi, K., Morikawa, K, and Igarashi, K. (1998) Crystal structure and mutational analysis of the Escherichia coli putrescine receptor. J. Biol. Chem. 273, 17604-17609.
59. Phanstiel, O., IV, Price, H. L., Wang, L., Juusola, J., Kline, M., and Shah, S. M. (2000) The effect of polyamine homologation on the transport and cytotoxicity properties of polyamine-(DNA-intercalator) conjugates. J. Org. Chem. 65, 5590-5599.
60. Wang, C., Delcros, J.-G., Cannon, L., Konate, F., Carias, H., Biggerstaff, J., Gardner, R. A., and Phanstiel, O. V. (2003) Defining the molecular requirements for the selective delivery of polyamine conjugates into cells containing active polyamine transporters. J. Med. Chem. 46, 5129-5138.
61. Gardner, R. A., Delcros, J.-G., Konate, F., Breitbeil, I. I. I., Martin, B., Sigman, M., Huang, M., and Phanstiel, O. (2004) N-1-substituent effects in the selective delivery of polyamine conjugates into cells containing active polyamine transporters. J. Med. Chem. 47, 6055-6069.
62. Phanstiel, O., IV, Kauri, N., and Delcros, J.-G. (2007) Structure-activity investigations of polyamine-anthracene conjugates and their uptake via the polyamine transporter. Amino Acids 33, 305-313.
63. Burns, M. R., Carlson, C. L., Vanderwerf, S. M., Ziemer, J. R., Weeks, R. S., Cai, F., Webb, H. K., and Graminski, G. F. (2001) Amino acid/spermine conjugates: Polyamine amides as potent spermidine uptake inhibitors. J. Med Chem. 44, 3632-3644.
64. Holley, J., Mather, A., Cullis, P., Symons, M. R., Wardman, P., Watt, R. A., and Cohen, G. M. (1992) Uptake and cytotoxicity of novel nitroimidazole-polyamine conjugates in ehrlich ascites tumor-cells. Biochem. Pharmacol. 43, 763-769.
65. Siddiqui, A. Q., Merson-Davies, L., and Cullis, P. M. (1999) The synthesis of novel polyamine-nitroimidazole conjugates designed to probe the structural specificities of the polyamine uptake system in A549 lung carcinoma cells. J. Chem. Soc., Perkin Trans. 1, 3243-3252.
66. Jakobs, A., Bernadou, J., and Meunier, B. (1997) Preparation of tetracationic metalloporphyrin - Spermine conjugates. J. Org. Chem. 62, 3505-3510.
67. Rauter, H., Di.Domenico, R., Menta, E., Oliva, O., Qu, Y., and Farrell, N. (1997) Selective platination of biologically relevant polyamines. Linear coordinating spermidine and spermine as amplifying linkers in dinuclear platinum complexes. Inorg. Chem. 36, 3919-3927.
68. Popaj, K., Guggisberg, A., and Hesse, M. (2000) Synthetic analogues to the spermidine-spermine alkaloid tenuilobine. Helv. Chim. Acta 83, 3021-3034.
69. Dallavalle, S., Giannini, G, Alloatti, D., Casati, A., Marastoni, E., Musso, L., Merlini, L., Morini, G., Penco, S., Pisano, C., Tinelli, S., De.Cesare, M., Beretta, G. L., and Zunino, F. (2006) Synthesis and cytotoxic activity of polyamine analogues of camptotiiecin. J. Med. Chem 49, 5177-5186.
70. Hu, V. W., and Hesse, M. (1996) The synthesis of p-Cumaroylspermidines. Helv. Chim. Acta 79, 548-559.
71. Blagbrough, I. S., and Geall, A. J. (1998) Practical synthesis of unsymmetrical polyamine amides. Tetrahedron Lett. 39, 439-442.
72. Bombardelli, E., and Verotta, L. (2000) U.S. Patent 6,121,277.
73. Miller, K. A., Kumar, E. V. K. S., Wood, S. J., Cromer, J. R., Datta, A., and David, S. A. (2005) Lipopolysaccharide sequestrants: Structural correlates of activity and toxicity in novel acylhomospermines. J. Med. Chem. 48, 2589-2599.
74. Marchesini, R., Colombo, A., and Caserini, C. (1996) Interaction of ionizing radiation with topotecan in two human tumor cell lines. Int. J. Cancer 66, 342-346.