Distribution of furamidine analogues in tumor cells: Targeting of the nucleus or mitochondria depending on the amidine substitution

Cancer Research

Volumn 62, Issue 24, 2002, Pages 7219-7229

  Lansiaux, Amélie ^a   Tanious, Farial ^b   Mishal, Zohar ^c   Dassonneville, Laurent ^a   Kumar, Arvind ^c   Stephens, Chad E ^c   Hu, Qiyue ^c   Wilson, W David ^c   Boykin, David W ^c   Bailly, Christian ^a,d  

^a CENTRE OSCAR LAMBRET   (France)

^b CNRS   (France)

^c GEORGIA STATE UNIVERSITY   (United States)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

2,5 BIS(4 AMIDINOPHENYL)FURAN; AMIDINE; DAUNORUBICIN; DEOXYRIBONUCLEASE I; DIPHENYLFURAN DERIVATIVE; DIPHENYLFURAN DIAMIDINE; FURAMIDINE ANALOGUES; FURAN DERIVATIVE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; APOPTOSIS; ARTICLE; BINDING SITE; BREAST ADENOCARCINOMA; CELL GRANULE; CELL NUCLEUS; CELL SURVIVAL; CELLULAR DISTRIBUTION; CHEMICAL STRUCTURE; COLON CARCINOMA; COMPARTMENT MODEL; CONTROLLED STUDY; CYTOTOXICITY; DNA BINDING; DNA FOOTPRINTING; DNA SEQUENCE; DRUG DISTRIBUTION; DRUG DNA INTERACTION; HUMAN; HUMAN CELL; LUNG CARCINOMA; MELANOMA; MITOCHONDRION; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROSTATE CARCINOMA; TUMOR CELL CULTURE;

ADENOCARCINOMA; ANIMALS; ANTINEOPLASTIC AGENTS; BASE SEQUENCE; BENZAMIDINES; CELL DIVISION; CELL NUCLEUS; DNA, NEOPLASM; HT29 CELLS; HUMANS; MALE; MELANOMA, EXPERIMENTAL; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; NEOPLASMS; PROSTATIC NEOPLASMS; STRUCTURE-ACTIVITY RELATIONSHIP; TUMOR CELLS, CULTURED;

EID: 0037115627     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (53)

1. Trent, J. O., Clark, G. R., Kumar, A., Wilson, W. D., Boykin, D. W., Hall, J. E., Tidwell, R. R. Blagburn, B. L., and Neidle, S. Targeting the minor groove of DNA: Crystal structures of two complexes between furan derivatives of berenil and the DNA dodecamer d(CGCGAATTCGCG)2. J. Med. Chem., 39: 4554-4562, 1996.
2. Wilson, W. D., Tanious, F. A., Ding, D., Kumar, A., Boykin, D. W., Colson, P., Houssier, C., and Bailly, C. Nucleic acid interactions of unfused aromatic cations: Evaluation of proposed minor-groove, major-groove and intercalation binding modes. J. Am. Chem. Soc., 120: 10310-10321, 1998.
3. Mazur, S., Tanious. F. A., Ding, D., Kumar, A., Boykin, D. W., Simpson, I. J., Neidle, S., and Wilson, W. D. A thermodynamic and structural analysis of DNA minor groove complex formation. J. Mol. Biol. 300: 321-337, 2000.
4. Blagburn, B. L., Drain, K. L., Land, T. M., Moore, P. H., Lindsay, D. S., Kumar, A. J., Shi, J., Boykin, D. W., and Tidwell, R. R. Dicationic furans inhibit development of Cryptosporidium Parvum in HSD/ICR suckling mice. J. Parasitol., 84: 851-856, 1998.
5. Boykin, D. W., Kumar, A., Spychala, J., Zhou, M., Lombardi, R. L., Wilson, W. D., Dykstra, C. C., Jones, S. K., Hall, J. E., Tidwell, R. R., Laughton, C., Nunn, C. M., and Neidle, S. Dicationic diarylfurans as anti-Pneumocystis carinii agents. J. Med. Chem., 38: 912-916, 1995.
6. Das, B. P., and Boykin, D. W. Synthesis and antiprotozoal activity of 2, 5-bis(4-guanylphenyl)furans. J. Med. Chem., 20: 531-536, 1977.
7. Steck, E. A., Kinnamon, K. E., Rane, D. S., and Hanson, W. L. Leishmania donovani. Plasmodium berghi, Trypanosoma rhodesiense: Antiprotozoan effects of some amidine types. Exp. Parasitol., 52: 404-413, 1981.
8. Boykin, D. W., Kumar, A., Bender, B. K., Hall, J. E., and Tidwell, R. R. AntiPneumocystis activity of bis-amidoximes and bis-O-alkylamidoximes prodrugs. Bioorg. Med. Chem. Lett., 6: 3017-3020, 1996.
9. De Koning, H. P. Uptake of pentamidine in Trypanosoma brucei brucei is mediated by three distinct transporters: Implications for cross-resistance with arsenicals. Mol. Pharmacol., 59: 586-592, 2001.
10. Neidle, S., Kelland, L. R., Trent, J. O., Simpson, I. J., Boykin, D. W., Kumar, A., and Wilson, W. D. Cytotoxicity of bis(phenylamidinium)furan alkyl derivatives in human tumour cell lines: Relation to DNA minor groove binding. Bioorg. Med. Chem., 7: 1403-1408, 1997.
11. Lansiaux, A., Dassonneville, L., Facompré, M., Kumar, A., Stephens, C. E., Bajic, M., Tanious, F., Wilson, W. D., Boykin, D. W., and Bailly, C. Distribution of furamidine analogues in tumor cells: Influence of the number of positive charges. J. Med. Chem., 45: 1994-2002, 2002.
12. Ekelund, S., Nygren, P., and Larsson, R. Guanidino-containing drugs in cancer chemotherapy: Biochemical and clinical pharmacology. Biochem. Pharmacol., 61: 1183-1193, 2001.
13. Boykin, D. W., Kumar, A., Xiao, G., Wilson, W. D., Bender, B. C., McCurdy, D. R., Hall, J. E., and Tidwell, R. R. 2, 5-Bis[4-N-alkylamidino)phenyl]furans as anti-Pneumocystis carinii agents. J. Med. Chem., 41: 124-129, 1998.
14. Stephens, C. E., Tanious, F., Kim, S., Wilson, W. D., Schell, W. A., Perfect, J. R., Franzblau, S. G., and Boykin, D. W. Diguanidino and "reversed" diamidino 2, 5-diarylfurans as antimicrobial agents. J. Med. Chem., 44: 1741-1748, 2001.
15. Cory, A. H., Owen, T. C., Barltrop, J. A., and Cory, J. G. Use of an aqueous soluble tetrazolium/formazan assay for cell growth assays. Cancer Commun., 3: 207-212, 1991.
16. Wilson, W. D., Tanious, F. A., Fernandez-Saiz, M., and Rigl, C. T. Evaluation of drug-nucleic acid interactions by thermal melting curves. Methods Mol. Biol., 90: 219-240, 1997.
17. Bailly, C., and Waring, M. J. Comparison of different footprinting methodologies for detecting binding sites for a small ligand on DNA. J. Biomol. Struct. Dyn., 12: 869-898, 1995.
18. Bailly, C. Tardy, C., Wang, L., Armitage, B., Hopkins, K., Kumar, A., Schuster, G. B., Boykin, D. W., and Wilson, W. D. Recognition of ATGA sequences by the unfused aromatic dication DB293 forming stacked dimers in the DNA minor groove. Biochemistry, 40: 9770-9779, 2001.
19. Wang, L., Bailly, C., Kumar, A., Ding, D., Bajic, M., Boykin, D. W., and Wilson, W. D. Specific molecular recognition of mixed nucleic acid sequences: An aromatic dication that binds in the DNA minor groove as a dimer. Proc. Natl. Acad. Sci. USA, 97: 12-16, 2000.
20. E20. Wang, L., Carrasco, C., Kumar, A., Stephens, C. E., Bailly, C., Boykin, D. W., and Wilson, W. D. Evaluation of the influence of compound structure on stacked-dimer formation in the DNA minor groove. Biochemistry, 40: 2511-2521, 2001.
21. Lacy, E. R., Le, N. M., Price, C. A., Lee, M., and Wilson, W. D. Influence of a terminal formamido group on the sequence recognition of DNA by polyamides. J. Am. Chem. Soc., 124: 2153-2163, 2002.
22. Davis, T. M., and Wilson, W. D. Determination of the refractive index increments of small molecules for correction of surface plasmon resonance data. Anal. Biochem., 284: 348-353, 2000.
23. Davis, T. M., and Wilson, W. D. Surface plasmon resonance biosensor analysis of RNA-small molecule interactions. Methods Enzymol., 340: 22-51, 2001.
24. Suzuki, T., Fujikura, K., Higashiyama, T., and Takata, K. DNA staining for fluorescence and laser confocal microscopy. J. Histochem. Cytochem., 45: 49-53, 1997.
25. Salvioli, S., Ardizzoni, A., Franceschi, C., and Cossarizza, A. JC-1, but not DiOC6(3) or rhodamine 123, is a reliable fluorescent probe to assess ΔΨ changes in intact cells: Implications for studies on mitochondrial functionality during apoptosis. FEBS Lett., 411: 77-82, 1997.
26. Kluza, J., Lansiaux, A., Wattez, N., Mahieu, C., Osheroff, N., and Bailly, C. Apoptotic response of HL-60 human leukemia cells to the antitumor drug TAS-103. Cancer Res., 60: 4077-4084, 2000.
27. Smiley, S. T., Reers, M., Mottolahartshom, C., Lin, M., Chen, A., Smith, T. W., Steele, G. D., and Chen, L. B. Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate forming lipophilic cation. Proc. Natl. Acad. Sci. USA, 88: 3671-3675, 1991.
28. Bulychev, A., Trouet, A., and Tulkens, P. Uptake and intracellular distribution of neutral red in cultured fibroblasts. Exp. Cell Res., 115: 343-355, 1978.
29. Sousa, C., Sa e Melo, T., Geze, M., Gaullier, J. M., Maziere, J. C., and Santus, R. Solvent polarity and pH effects on the spectroscopic properties of neutral red: Application to lysosomal microenvironment probing in living cells. Photochem. Photobiol., 63: 601-607, 1996.
30. Egorin, M. J., Hildebrand, R. C., Cimino, E. F., and Bachur, N. R. Cytofluorescence localization of adriamycin and daunomycin. Cancer Res., 34: 2243-2245, 1974.
31. Gervasoni, J. E., Jr., Fields, S. Z., Krishna, S., Baker, M. A., Rosado, M., Thuraisamy, K., Hindenburg, A. A., and Taub, R. N. Subcellular distribution of daunorubicin in P-glycoprotein-positive and -negative drug-resistant cell lines using laser-assisted confocal microscopy. Cancer Res., 51: 4955-4963, 1991.
32. Marquardt, D., and Center, M. S. Drug transport mechanism in HL60 cells isolated for resistance to adriamycin: Evidence for nuclear drug accumulation and redistribution in resistant cells. Cancer Res., 52: 3157-3163, 1992.
33. Johnson, L. V., Walsh, M. L., and Chen, L. B. Localization of mitochondria in living cells with rhodamine 123. Proc. Natl. Acad. Sci. USA, 77: 990-994, 1980.
34. Costantini, P., Jacotot, E., Decaudin, D., Kroemer, G. Mitochondrion as a novel target of anticancer chemotherapy. J. Natl. Cancer Inst., 92: 1042-1053, 2000.
35. Koya, K., Li, Y., Wang, H., Ukai, T., Tatsuta, N., Kawakami, M., Shishido, T., and Chen, L. B. MKT-077, a novel rhodacyanine dye in clinical trials, exhibits anticarcinoma activity in preclinical studies based on selective mitochondrial accumulation. Cancer Res., 56: 538-543, 1996.
36. Weisberg, E. L., Koya, K., Modica-Napolitano, J., Li, Y., and Chen, L. B. In vivo administration of MKT-077 causes partial yet reversible impairment of mitochondrial function. Cancer Res., 56: 551-555, 1996.
37. Modica-Napolitano, J. S., Koya, K., Weisberg, E., Brunelli, B. T., Li, Y., and Chen, L. B. Selective damage to carcinoma mitochondria by the rhodacyanine MKT-077. Cancer Res., 56: 544-550, 1996.
38. Modica-Napolitano, J. S., Brunelli, B. T., Koya, K., and Chen, L. B. Photoactivation enhances the mitochondrial toxicity of the cationic rhodacyanine MKT-077. Cancer Res., 58: 71-75, 1998.
39. Fellous, R., Coulaud, D., El Abed, I., Roques, B. P., Le Pecq, J. B., Delain, E., and Gouyette, A. Cytoplasmic accumulation of ditercalinium in rat hepatocytes and induction of mitochondrial damages. Cancer Res., 48: 6542-6549, 1988.
40. Soslau, G., and Nass, M. M. Effects of ethidium bromide on the cytochrome content and ultrastructure of L1210 cell mitochondria. J. Cell Biol., 51: 514-524, 1971.
41. Nass, M. M. Analysis of methylglyoxal bis(guanylhydrazone)-induced alterations of hamster tumor mitochondria by correlated studies of selective rhodamine binding, ultrastructural damage. DNA replication, and reversibility. Cancer Res., 44: 2677-2688, 1984.
42. Downes, C. S., Ord, M. J., Mullinger, A. M., Collins, A. R., and Johnson, R. T. Novobiocin inhibition of DNA excision repair may occur through effects on mitochondrial structure and ATP metabolism, not on repair topoisomerases. Carcinogenesis (Lond.), 6: 1343-1352, 1985.
43. Ueda, T., Hirai, K., and Ogawa, K. Effects of paraquat on the mitochondrial structure and Ca-ATPase activity in rat hepatocytes. J. Electron Microsc. (Tokyo), 34: 85-91, 1985.
44. Wessendorf, M. W. Fluoro-Gold: Composition, and mechanism of uptake. Brain Res., 553: 135-148, 1991.
45. Snapper, I., Schneid, G., Greenspan, E., and Lieben, F. On the deposition of stilbamidine and 2-hydroxystilbamidine in cytoplasm and nuclei of different organs and tumors. Bull. N. Y. Acad. Med., 26: 269-270, 1950.
46. Snapper, I., Schneid, G., and Kurnik, N. The presence of diamidines in myeloma cells after treatment with stilbamidine and 2-hydroxystilbamidine. Acta Haematol., 3: 129-134, 1950.
47. Snapper, I., Schneid, G., Lieben, F., Gerber, I., and Greenspan, E. Influence of nucleic acid upon the fluorescence of nuclei and cytoplasm after injection of aromatic diamidines. J. Lab. Clin. Med., 37: 562-574, 1951.
48. Festy, B., and Daune, M. Hydroxystilbamidine. A nonintercalating drug as a probe of nucleic acid conformation. Biochemistry, 12, 4827-4834, 1973.
49. Festy, B., Sturm, J., and Daune, M. Interaction between hydroxystilbamidine and DNA. I. Binding isotherms and thermodynamics of the association. Biochim. Biophys. Acta, 407, 24-42, 1975.
50. Gresh, N., and Pullman, B. A theoretical study of the nonintercalative binding of berenil and stilbamidine to double-stranded (dA-dT)n oligomers. Mol. Pharmacol., 25: 452-458, 1984.
51. de Duve, C., de Barsy, T., Poole, B., Trouyet, A., Tulkens, P., and Van Hoof, F. Lysosomotropic agents. Biochem. Pharmacol., 23: 2495-2531, 1974.
52. Ohkuma, S., and Poole, B. (1981) Cytoplasmic vacuolation of mouse peritoneal macrophages and the uptake into lysosomes of weakly basic substances. J. Cell. Biol., 90: 656-664, 1981.
53. Marchetti, P., Susin, S. A., Decaudin, D., Gamen, S., Castedo, M., Hirsch, T., Zamzami, N., Naval, J., Senik, A., and Kroemer, G. Apoptosis-associated derangement of mitochondrial function in cells lacking mitochondrial DNA. Cancer Res., 56: 2033-2038, 1996.