Effect of spermine conjugation on the cytotoxicity and cellular transport of acridine

Journal of Medicinal Chemistry

Volumn 45, Issue 23, 2002, Pages 5098-5111

  Delcros, Jean Guy ^a   Tomasi, Sophie ^a   Carrington, Simon ^b   Martin, Bénédicte ^a   Renault, Jacques ^a   Blagbrough, Ian S ^b   Uriac, Philippe ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

^b University of Bath   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOACRIDINE DERIVATIVE; EFLORNITHINE; N 1 (ACRIDIN 9 YL) 1,5,9,14,18 PENTAAZAOCTADECANE; N 1 (ACRIDIN 9 YL) 1,6,10,15,19 PENTAAZANONADECANE; N 1 (ACRIDIN 9 YL) 1,7,11,16,20 PENTAAZAEICOSANE; N 1 (ACRIDIN 9 YLCARBONYL) 1,5,9,14,18 PENTAAZAOCTADECANE; N 1 (ACRIDIN 9 YLCARBONYL) 1,6,10,15,19 PENTAAZANONADECANE; N 1 (ACRIDIN 9 YLCARBONYL) 1,7,11,16,20 PENTAAZAEICOSANE; ORNITHINE DECARBOXYLASE INHIBITOR; POLYAMINE; SPERMINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CANCER CELL; CELL GROWTH; CELL TRANSPORT; CHO CELL; CONJUGATE; CONJUGATION; CONTROLLED STUDY; CYTOTOXICITY; DERIVATIZATION; DNA SEQUENCE; DRUG EFFECT; DRUG POTENCY; DRUG POTENTIATION; DRUG SYNTHESIS; IC 50; NONHUMAN; PROTEIN TRANSPORT; UPREGULATION;

ACRIDINES; ANIMALS; BINDING, COMPETITIVE; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CELL DIVISION; CELL LINE; CRICETINAE; DNA; EFLORNITHINE; MUTATION; ORNITHINE DECARBOXYLASE; SPECTROMETRY, FLUORESCENCE; SPERMIDINE; SPERMINE;

EID: 0037038323     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm020843w     Document Type: Article

References (77)

1. Cohen, S. S. A Guide to the Polyamines; Oxford University Press: New York, 1998.
2. Pegg, A. E. Polyamine metabolism and its importance in neoplastic growth and as a target for chemotherapy. Cancer Res. 1988, 48, 759-774.
3. Seiler, N.; Dezeure, F. Polyamines transport in mammalian cells. Int. J. Biochem. 1990, 22, 211-218.
4. Seiler, N.; Delcros, J. G.; Moulinoux, J. P. Polyamine transport in mammalian cells. An update. Int. J. Biochem. Cell Biol. 1996, 28, 843-861.
5. Bachrach, U.; Seiler, N. Formation of acetylpolyamines and putrescine from spermidine by normal and transformed chick embryo fibroblasts. Cancer Res. 1981, 41, 1205-1208.
6. Chen, K. Y.; Rinehart, C. A., Jr. Difference in putrescine transport in undifferentiated versus differentiated mouse NB-15 neuroblastoma cells. Biochem. Biophys. Res. Commun. 1981, 101, 243-249.
7. Alhonen-Hongisto, L.; Seppanen, P.; Janne, J. Intracellular putrescine and spermidine deprivation induces increased uptake of the natural polyamines and methylglyoxal bis(guanylhydrazone). Biochem. J. 1980, 192, 941-945.
8. Minchin, R. F.; Raso, A.; Martin, R. L.; Ilett, K. F. Evidence for the existence of distinct transporters for the polyamines putrescine and spermidine in B16 melanoma cells. Eur. J. Biochem. 1991, 200, 457-462.
9. Rinehart, C. A. J.; Chen, K. Y. Characterization of the polyamine transport system in mouse neuroblastoma cells. Effects of sodium and system A amino acids. J. Biol. Chem. 1984, 259, 4750-4756.
10. Volkow, N.; Goldman, S. S.; Flamm, E. S.; Cravioto, H.; Wolf, A. P.; Brodie, J. D. Labeled putrescine as a probe in brain tumors. Science 1983, 221, 673-675.
11. 14C-labeled polyamines and methylglyoxal bis-(guanylhydrazone) by a rat prostate-derived tumor. Cancer Res. 1984, 44, 1034-1040.
12. Chaney, J. E.; Kobayashi, K.; Goto, R.; Digenis, G. A. Tumor selective enhancement of radioactivity uptake in mice treated with alpha-difluoromethylornithine prior to administration of 14C-putrescine. Life Sci. 1983, 32, 1237-1241.
13. Redgate, E. S.; Grudziak, A. G.; Deutsch, M.; Boggs, S. S. Difluoromethylornithine enhanced uptake of tritiated putrescine in 9L rat brain tumors. Int. J. Radiat. Oncol. Biol. Phys. 1997, 38, 169-174.
14. Holley, J. L.; Mather, A.; Wheelhouse, R. T.; Cullis, P. M.; Hartley, J. A.; Bingham, J. P.; Cohen, G. M. Targeting of tumor cells and DNA by a chlorambucil-spermidine conjugate. Cancer Res. 1992, 52, 4190-4195.
15. Cullis, P. M.; Merson-Davies, L.; Weaver, R. Mechanism and reactivity of chlorambucil and chlorambucil-spermidine conjugate. J. Am. Chem. Soc. 1995, 117, 8033-8034.
16. Stark, P. A.; Thrall, B. D.; Meadows, G. G.; Abdel-Monem, M. M. Synthesis and evaluation of novel spermidine derivatives as targeted cancer chemotherapeutic agents. J. Med. Chem. 1992, 35, 4264-4269.
17. Holley, J.; Mather, A.; Cullis, P.; Symons, M. R.; Wardman, P.; Watt, R. A.; Cohen, G. M. Uptake and cytotoxicity of novel nitroimidazole-polyamine conjugates in Ehrlich ascites tumour cells. Biochem. Pharmacol. 1992, 43, 763-769.
18. Heston, W. D.; Uy, L.; Fair, W. R.; Covey, D. F. Cytotoxic activity of aziridinyl putrescine enhanced by polyamine depletion with alpha-difluoromethylornithine. Biochem. Pharmacol. 1985, 34, 2409-2410.
19. Yuan, Z. M.; Egorin, M. J.; Rosen, D. M.; Simon, M. A.; Callery, P. S. Cellular pharmacology of N1- and N8-aziridinyl analogues of spermidine. Cancer Res. 1994, 54, 742-748.
20. Eiseman, J. L.; Rogers, F. A.; Guo, Y.; Kauffman, J.; Sentz, D. L.; Klinger, M. F.; Callery, P. S.; Kyprianou, N. Tumor-targeted apoptosis by a novel spermine analogue, 1,12-diaziridinyl-4,9- diazadodecane, results in therapeutic efficacy and enhanced radiosensitivity of human prostate cancer. Cancer Res. 1998, 58, 4864-4870.
21. Huber, M.; Pelletier, J. G.; Torossian, K.; Dionne, P.; Gamache, I.; Charestgandreault, R.; Audette, M.; Poulin, R. 2,2′-Dithiobis(N-ethyl-spermine-5-carboxamide) is a high affinity, membrane-impermeant antagonist of the mammalian polyamine transport system. J. Biol. Chem. 1996, 271, 27556-27563.
22. Byers, T. L.; Pegg, A. E. Regulation of polyamine transport in Chinese hamster ovary cells. J. Cell. Physiol. 1990, 143, 460- 467.
23. Muller, S.; Luchow, A.; McCann, P. P.; Walter, R. D. Effect of bis(benzyl)polyamine derivatives on polyamine transport and survival of Brugia pahangi. Parasitol. Res. 1991, 77, 612-615.
24. Marton, L. J.; Levin, V. A.; Hervatin, S. J.; Koch-Weser, J.; McCann, P. P.; Sjoerdsma, A. Potentiation of the antitumor therapeutic effects of 1,3-bis(2-chloroethyl)-1-nitrosourea by alpha-difluoromethylornithine, an ornithine decarboxylase inhibitor. Cancer Res. 1981, 41, 4426-4431.
25. Aziz, S. M.; Yatin, M.; Worthen, D. R.; Lipke, D. W.; Crooks, P. A. A novel technique for visualizing the intracellular localization and distribution of transported polyamines in cultured pulmonary artery smooth muscle cells. J. Pharm. Biomed. Anal. 1998, 17, 307-320.
26. Demeunynck, M.; Charmantray, F.; Martelli, A. Interest of acridine derivatives in the anticancer chemotherapy. Curr. Pharm. Des. 2001, 7, 1703-1724.
27. Edwards, M. L.; Snyder, R. D.; Stemerick, D. M. Synthesis and DNA-binding properties of polyamine analogues. J. Med. Chem. 1991, 34, 2414-2420.
28. Feuerstein, B. G.; Williams, L. D.; Basu, H. S.; Marton, L. J. Implications and concepts of polyamine-nucleic acid interactions. J. Cell. Biochem. 1991, 46, 37-47.
29. Cohen, G. N.; Cullis, P. M.; Hartley, J. A.; Mather, A.; Symons, M. C. R.; Wheelhouse, R. T. Targeting of cytotoxic agents by polyamines-synthesis of a chlorambucil spermidine conjugate. J. Chem. Soc. Chem. Commun. 1992, 298-300.
30. Rodger, A.; Blagbrough, I. S.; Adlam, G.; Carpenter, M. L. DNA binding of a spermine derivative: Spectroscopic study of anthracene-9-carbonyl-N-1-spermine with poly[d(G-C).(d(G-C)] and poly [d(A-T).d(A-T)]. Biopolymers 1994, 34, 1583-1593.
31. Rodger, A.; Taylor, S.; Adlam, G.; Blagbrough, I. S.; Haworth, I. S. Multiple DNA binding modes of anthracene-9-carbonyl-N1-spermine. Bioorg. Med. Chem. 1995, 3, 861-872.
32. 1-(acridin-9-ylcarbonyl)spermine at homopurine sites of duplex DNA. Chem. Commun. 1998, 929-930.
33. Phanstiel, O. I.; Price, H. L.; Wang, L.; Juusola, J.; Kline, M.; Shah, S. M. The effect of polyamine homologation on the transport and cytotoxicity properties of polyamine-(DNA-intercalator) conjugates. J. Org. Chem. 2000, 65, 5590-5599.
34. Wang, L.; Price, H. L.; Juusola, J.; Kline, M.; Phanstiel, O. I. Influence of polyamine architecture on the transport and topoisomerase II inhibitory properties of polyamine DNA-intercalator conjugates. J. Med. Chem. 2001, 44, 3682-3691.
35. Bergeron, R. J.; Feng, Y.; Weimar, W. R.; McManis, J. S.; Dimova, H.; Porter, C.; Raisler, B.; Phanstiel, O. A comparison of structure-activity relationships between spermidine and spermine analogue antineoplastics. J. Med. Chem. 1997, 40, 1475-1494.
36. Siddiqui, A. Q.; Merson-Davies, L.; Cullis, P. M. 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. Trans. 1999, 1, 3243-3252.
37. Cullis, P. M.; Green, R. E.; Merson-Davies, L.; Travis, N. Probing the mechanism of transport and compartmentalisation of polyamines in mammalian cells. Chem. Biol. 1999, 6, 717-729.
38. Martin, B.; Possémé, F.; Le Barbier, C.; Carreaux, F.; Carboni, B.; Seiler, N.; Moulinoux, J. P.; Delcros, J. G. N-benzylpolyamines as vectors of boron and fluorine for cancer therapy and imaging: Synthesis and biological evaluation. J. Med. Chem. 2001, 44, 3653-3664.
39. Porter, C. W.; Miller, J.; Bergeron, R. J. Aliphatic chain length specificity of the polyamine transport system in ascites L1210 leukemia cells. Cancer Res. 1984, 44, 126-128.
40. Bergeron, R. J.; McManis, J. S.; Weimar, W. R.; Schreier, K. M.; Gao, F.; Wu, Q.; Ortiz-Ocasio, J.; Luchetta, G. R.; Porter, C.; Vinson, J. R. The role of charge in polyamine analogue recognition. J. Med. Chem. 1995, 38, 2278-2285.
41. Mancuso, A. J.; Huang, S. L.; Swern, D. Oxidation of long-chain and related alcohols to carbonyl by dimethyl sulfoxide "activated" by oxalyl chloride. J. Org. Chem. 1978, 43, 2480-2482.
42. Moya, E.; Blagbrough, I. S. Total syntheses of polyamine amides PhTX-4.3.3 and PhTX-3.4.3: Reductive alkylation is a rapid, practical route to philanthotoxins. Tetrahedron Lett. 1995, 36, 9401-9404.
43. Ashton, M. R.; Moya, E.; Blagbrough, I. S. Total synthesis of modified JSTX toxins: Reductive alkylation is a practical route to hexahydropyrimidine polyamine amides. Tetrahedron Lett. 1995, 36, 9397-9400.
44. Lucente, G.; Pinnen, F.; Zanotti, G. A new method for oxidative decarboxylation of N-acyl-α-amino acids and peptides. Tetrahedron Lett. 1978, 34, 3155-3158.
45. Shono, T.; Matsumura, Y.; Kanasawa, T.; Habuka, M.; Unchida, K.; Toyoda, K. Electro-organic chemistry. Part 80. α-hydroxylation of N-acylated cyclic amine and utilization of the products as amino-aldehyde equivalents. J. Chem. Res. 1984, S, 320-321.
46. 1-alkoxy-carbonylpyrrolidines. Heterocycles 1987, 26, 617-625.
47. Quibell, M.; Turnell, W. G.; Johnson, T. Synthesis of azapeptides by the Fmoc/tert-butyl/polyamide technique. J. Chem. Soc. Perkin Trans. 1 1993, 2843-2849.
48. Takeuchi, Y.; Tokuda, S. I.; Takagi, T.; Koike, M.; Abe, H.; Harayama, T.; Shibata, Y.; Kim, H. S.; Wataya, Y. Synthesis and antimalaral activity of DL-deoxyfebrifugine. Heterocycles 1999, 51, 1869-1875.
49. Blagbrough, I. S.; Geall, A. J. Practical synthesis of unsymmetrical polyamine amides. Tetrahedron Lett. 1998, 39, 439- 442.
50. Dupre, D. J.; Robinson, F. A. N-Substituted 5-aminoacridines. J. Chem. Soc. 1945, 549-551.
51. Ghaneolhosseini, H.; Tjarks, W.; Sjoberg, S. Synthesis of novel boronated acridines- and spermidines as possible agents for BNCT. Tetrahedron 1998, 54, 3877-3884.
52. Qarawi, M. A.; Carrington, S.; Blagbrough, I. S.; Moss, S. H.; Pouton, C. W. Optimization of the MTT assay for B16 murine melanoma cells and its application in assessing growth inhibition by polyamines and novel polyamine conjugates. Pharm. Sci. 1997, 3, 235-239.
53. Schreiber, J. P.; Daune, M. P. Fluorescence of complexes of acridine dye with synthetic polydeoxyribonucleotides: A physical model of frameshift mutation. J. Mol. Biol. 1974, 83, 487-501.
54. Hansen, J. B.; Koch, T.; Buchardt, O.; Nielsen, P. E.; Norden, B. M. W. Trisintercalation in DNA by N-[3-(9-acridinylamino)-propyl]-N,N-bis[6-(9-acridinylamino)hexyl]amine. J. Chem. Soc. Chem. Commun. 1984, 509-511.
55. Krey, A. K.; Hahn, F. E. Studies on the complex of distamycin a with calf thymus DNA. FEBS Lett. 1970, 10, 175-178.
56. Dougherty, G.; Pilbrow, J. R. Physicochemical probes of intercalation. Int. J. Biochem. 1984, 16, 1179-1192.
57. Morgan, A. R.; Lee, J. S.; Pulleyblank, D. E.; Murray, N. L.; Evans, D. H. Review: ethidium fluorescence assays. Part 1. Physicochemical studies. Nucleic Acids Res. 1979, 7, 547-569.
58. McConnaughie, A. W.; Jenkins, T. C. Novel acridine-triazenes as prototype combilexins: synthesis, DNA binding, and biological activity. J. Med. Chem. 1995, 38, 3488-3501.
59. Baguley, B. C. Nonintercalative DNA-binding antitumour compounds. Mol. Cell. Biochem. 1982, 43, 167-181.
60. Bailly, C.; Pommery, N.; Houssin, R.; Henichart, J. P. Design, synthesis, DNA binding, and biological activity of a series of DNA minor-groove-binding intercalating drugs. J. Pharm. Sci. 1989, 78, 910-917.
61. Antonini, I.; Polucci, P.; Jenkins, T. C.; Kelland, L. R.; Menta, E.; Pescalli, N.; Stefanska, B.; Mazerski, J.; Martelli, S. 1-[(ω-aminoalkyl)amino]-4-[N-(ω-aminoalkyl)carbamoyl]- 9-oxo-9,10-dihydroacridines as intercalating cytotoxic agents: synthesis, DNA binding, and biological evaluation. J. Med. Chem. 1997, 40, 3749-3755.
62. Seiler, N.; Douaud, F.; Renault, J.; Delcros, J. G.; Havouis, R.; Uriac, P.; Moulinoux, J. P. Polyamine sulfonamides with NMDA antagonist properties are potent calmodulin antagonists and cytotoxic agents. Int. J. Biochem. Cell Biol. 1998, 30, 393-406.
63. Tomasi, S.; Le Roch, M.; Renault, J.; Corbel, J. C.; Uriac, P.; Carboni, B.; Moncoq, D.; Martin, B.; Delcros, J. G. Solid-phase organic synthesis of polyamine derivatives and initial biological evaluation of their antitumoral activity. Bioorg. Med. Chem. Lett. 1998, 8, 635-640.
64. Delcros, J. G.; Vaultier, M.; LeRoch, N.; Havouis, R.; Moulinoux, J. P.; Seiler, N. Bis(7-amino-4-azaheptyl)dimethylsilane: A new tetramine with polyamine-like features. Effects on cell growth. Anticancer Drug Des. 1997, 12, 35-48.
65. Porter, C. W.; Ganis, B.; Vinson, T.; Marton, L. J.; Kramer, D. L.; Bergeron, R. J. Comparison and characterization of growth inhibition in L1210 cells by alpha-difluoromethylornithine, an inhibitor of ornithine decarboxylase, and N1,N8-bis(ethyl)-spermidine, an apparent regulator of the enzyme. Cancer Res. 1986, 46, 6279-6285.
66. Byers, T. L.; Pegg, A. E. Properties and physiological function of the polyamine transport system. Am. J. Physiol. 1989, 257, C545-C553.
67. Mitchell, J. L.; Diveley, R. R., Jr.; Bareyal-Leyser, A. Feedback repression of polyamine uptake into mammalian cells requires active protein synthesis. Biochem. Biophys. Res. Commun. 1992, 186, 81-88.
68. Kramer, D. L.; Miller, J. T.; Bergeron, R. J.; Khomutov, R.; Khomutov, A.; Porter, C. W. Regulation of polyamine transport by polyamines and polyamine analogues. J. Cell. Physiol. 1993, 155, 399-407.
69. Mi, Z.; Kramer, D. L.; Miller, J. T.; Bergeron, R. J.; Bernacki, R.; Porter, C. W. Human prostatic carcinoma cell lines display altered regulation of polyamine transport in response to polyamine analogues and inhibitors. Prostate 1998, 34, 51-60.
70. Weeks, R. S.; Vanderwerf, S. M.; Carlson, C. L.; Burns, M. R.; O'Day, C. L.; Cai, F.; Devens, B. H.; Webb, H. K. Novel lysine-spermine conjugate inhibits polyamine transport and inhibits cell growth when given with DFMO. Exp. Cell Res. 2000, 261, 293-302.
71. Heston, W. D.; Charles, M. Calmodulin antagonist inhibition of polyamine transport in prostatic cancer cells in vitro. Biochem. Pharmacol. 1988, 37, 2511-2514.
72. Khan, N. A.; Sezan, A.; Quemener, V.; Moulinoux, J. P. Polyamine transport regulation by calcium and calmodulin: Role of Ca(2+)-ATPase. J. Cell. Physiol. 1993, 157, 493-501.
73. Scemama, J. L.; Grabie, V.; Seidel, E. R. Characterization of univectorial polyamine transport in duodenal crypt cell line. Am. J. Physiol. 1993, 265, G851-G856.
74. Louwrier, S.; Tuynman, A.; Hiemstra, H. Synthesis of bicyclic guanidines from pyrrolidin-2-one. Tetrahedron 1996, 52, 2629- 2646.
75. Delcros, J. G.; Sturkenboom, M. C.; Basu, H. S.; Shafer, R. H.; Szollosi, J.; Feuerstein, B. G.; Marton, L.J. Differential effects of spermine and its analogues on the structures of polynucleotides complexed with ethidium bromide. Biochem. J. 1993, 291, 269-274.
76. Mosmann, T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65, 55-63.
77. Lowry, O. H.; Rosenbrough, N. J.; Farr, A. L.; Randall, R. J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193, 265-275.