DNA binding and antigene activity of a daunomycin-conjugated triplex-forming oligonucleotide targeting the P2 promoter of the human c-myc gene

Nucleic Acids Research

Volumn 32, Issue 8, 2004, Pages 2396-2410

  Carbone, Giuseppina M ^c   McGuffie, Eileen ^a   Napoli, Sara ^c   Flanagan, Courtney E ^a   Dembech, Chiara ^b   Negri, Umberto ^b   Arcamone, Federico ^b   Capobianco, Massimo L ^b   Catapano, Carlo V ^c  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b CNR   (Italy)

^c ONCOLOGY INSTITUTE OF SOUTHERN SWITZERLAND   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DAUNORUBICIN MONOCLONAL ANTIBODY CONJUGATE; MYC PROTEIN; OLIGONUCLEOTIDE; 11MER DAUNOMYCIN CONJUGATED GT; 11MER DAUNOMYCIN-CONJUGATED GT; ANTINEOPLASTIC ANTIBIOTIC; DAUNORUBICIN; DNA; TRIPLEX DNA;

ARTICLE; BINDING AFFINITY; BREAST CANCER; CANCER CELL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; COVALENT BOND; DNA BINDING; DNA FOOTPRINTING; DRUG MECHANISM; DRUG STRUCTURE; DRUG TARGETING; GEL MOBILITY SHIFT ASSAY; GENE CONSTRUCT; GENE SEQUENCE; GENE TARGETING; GENETIC TRANSCRIPTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VITRO STUDY; ONCOGENE C MYC; PRIORITY JOURNAL; PROSTATE CANCER; TRANSCRIPTION INITIATION; BINDING SITE; CHEMISTRY; DRUG DESIGN; DRUG EFFECT; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; ONCOGENE MYC; PROMOTER REGION; TUMOR CELL LINE;

ANTIBIOTICS, ANTINEOPLASTIC; BASE SEQUENCE; BINDING SITES; CELL LINE, TUMOR; DAUNORUBICIN; DNA; DRUG DESIGN; GENE TARGETING; GENES, MYC; HUMANS; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDES; PROMOTER REGIONS (GENETICS); TRANSCRIPTION, GENETIC;

EID: 2342461708     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkh527     Document Type: Article

References (77)

1. Chan,P.P. and Glazer,P.M. (1997) Triplex DNA: fundamentals, advances and potential applications for gene therapy. Mol. Med., 75, 267-282.
2. Praseuth,D., Guieysse,A.L. and Helene,C. (1999) Triple helix formation and the antigene strategy for sequence-specific control of gene expression. Biochim. Biophys. Acta, 1489, 181-206.
3. Casey,B.P. and Glazer,P.M. (2001) Gene targeting via triple-helix formation. Prog. Nucleic Acid Res. Mol. Biol., 67, 163-192.
4. Winters,T.A. (2000) Gene targeted agents: new opportunities for rational drug development. Curr. Opin. Mol. Ther., 2, 670-681.
5. Moser,H.E. and Dervan,P.B. (1987) Sequence-specific cleavage of double helical DNA by triple helix formation. Science, 238, 645-650.
6. Beal,P.A. and Dervan,P.B. (1991) Second structural motif for recognition of DNA by oligonucleotide-directed triple-helix formation. Science, 251, 1360-1363.
7. Singleton,S.F. and Dervan,P.B. (1992) Influence of pH on the equilibrium association constants for oligodeoxyribonucleotide-directed triple helix formation at single DNA sites. Biochemistry, 31, 10995-11003.
8. Durland,R.H., Kessler,D.J., Gunnell,S., Duvic,M., Pettitt,B.M. and Hogan,M.E. (1991) Binding of triple helix forming oligonucleotides to sites in gene promoters. Biochemistry, 30, 9246-9255.
9. Maher,L.J.,III (1996) Prospects for the therapeutic use of antigene oligonucleotides. Cancer Invest., 14, 66-82.
10. Maher,L.J.,III, Dervan,P.B. and Wold,B.J. (1990) Kinetic analysis of oligodeoxyribonucleotide-directed triple-helix formation on DNA. Biochemistry, 29, 8820-8826.
11. Svinarchuk,F., Bertrand,J.R. and Malvy,C. (1994) A short purine oligonucleotide forms a highly stable triple helix with the promoter of the murine c-pim-1 proto-oncogene. Nucleic Acids Res., 22, 3742-3747.
12. Svinarchuk,F., Paoletti,J. and Malvy,C. (1995) An unusually stable purine(purine-pyrimidine) short triplex. The third strand stabilizes double-stranded DNA. J. Biol. Chem., 270, 14068-14071.
13. Alunni-Fabbroni,M., Pirulli,D., Manzini,G. and Xodo,L.E. (1996) (A,G)-oligonucleotides form extraordinary stable triple helices with a critical R.Y sequence of the murine c-Ki-ras promoter and inhibit transcription in transfected NIH 3T3 cells. Biochemistry, 35, 16361-16369.
14. Maher,L.J., Wold,B. and Dervan,P.B. (1989) Inhibition of DNA binding proteins by oligonucleotide-directed triple helix formation. Science, 245, 725-730.
15. Maher,L.J.D., Dervan,P.B. and Wold,B. (1992) Analysis of promoter-specific repression by triple-helical DNA complexes in a eukaryotic cell-free transcription system. Biochemistry, 31, 70-81.
16. Guieysse,A.L., Praseuth,D., Grigoriev,M., Harel-Bellan,A. and Helene,C. (1996) Detection of covalent triplex within human cells. Nucleic Acids Res., 24, 4210-4216.
17. Giovannangeli,C., Diviacco,S., Labrousse,V., Gryaznov,S., Charneau,P. and Helene,C. (1997) Accessibility of nuclear DNA to triplex-forming oligonucleotides: the integrated HIV-1 provirus as a target. Proc. Natl Acad. Sci. USA, 94, 79-84.
18. Lin,F.L., Majumdar,A., Klotz,L.C., Reszka,A.P., Neidle,S. and Seidman,M.M. (2000) Stability of DNA triplexes on shuttle vector plasmids in the replication pool in mammalian cells. J. Biol. Chem., 275, 39117-39124.
19. Maine,J.P. and Kodadek,T. (1994) Efficient unwinding of triplex DNA by a DNA helicase. Biochem. Biophys. Res. Commun., 204, 1119-1124.
20. Kopel,V., Pozner,A., Baran,N. and Manor,H. (1996) Unwinding of the third strand of a DNA triple helix, a novel activity of the SV40 large T-antigen helicase. Nucleic Acids Res., 24, 330-335.
21. Sandor,Z. and Bredberg,A. (1994) Repair of triple helix directed psoralen adducts in human cells. Nucleic Acids Res., 22, 2051-2056.
22. Degols,G., Clarenc,J.P., Lebleu,B. and Leonetti,J.P. (1994) Reversible inhibition of gene expression by a psoralen functionalized triple helix forming oligonucleotide in intact cells. J. Biol. Chem., 269, 16933-16937.
23. Sandor,Z. and Bredberg,A. (1995) Deficient DNA repair of triple helix-directed double psoralen damage in human cells. FEBS Lett., 374, 287-291.
24. Wang,G. and Glazer,P.M. (1995) Altered repair of targeted psoralen photoadducts in the context of an oligonucleotide-mediated triple helix. J. Biol. Chem., 270, 22595-22601.
25. Raha,M., Wang,G., Seidman,M.M. and Glazer,P.M. (1996) Mutagenesis by third-strand-directed psoralen adducts in repair-deficient human cells: high frequency and altered spectrum in a xeroderma pigmentosum variant. Proc. Natl Acad. Sci. USA, 93, 2941-2946.
26. Wang,G., Seidman,M.M. and Glazer,P.M. (1996) Mutagenesis in mammalian cells induced by triple helix formation and transcription-coupled repair. Science, 271, 802-805.
27. Musso,M., Wang,J.C. and Van Dyke,M.W. (1996) In vivo persistence of DNA triple helices containing psoralen-conjugated oligodeoxyribonucleotides. Nucleic Acids Res., 24, 4924-4932.
28. Barre,F.X., Asseline,U. and Harel-Bellan,A. (1999) Asymmetric recognition of psoralen interstrand crosslinks by the nucleotide excision repair and the error-prone repair pathways. J. Mol. Biol., 286, 1379-1387.
29. Barre,F.X., Giovannangeli,C., Helene,C. and Harel-Bellan,A. (1999) Covalent crosslinks introduced via a triple helix-forming oligonucleotide coupled to psoralen are inefficiently repaired. Nucleic Acids Res., 27, 743-749.
30. Asseline,U., Delarue,M., Lancelot,G., Toulme,F., Thuong,N.T., Montenay-Garestier,T. and Helene,C. (1984) Nucleic acid-binding molecules with high affinity and base sequence specificity: intercalating agents covalently linked to oligodeoxynucleotides. Proc. Natl Acad. Sci. USA, 81, 3297-3301.
31. Asseline,U., Toulme,F., Thuong,N.T., Delarue,M., Montenay-Garestier,T. and Helene,C. (1984) Oligodeoxynucleotides covalently linked to intercalating dyes as base sequence-specific ligands. Influence of dye attachment site. EMBO J., 3, 795-800.
32. Sun,J.S., Francois,J.C., Montenay-Garestier,T., Saison-Behmoaras,T., Roig,V., Thuong,N.T. and Helene,C. (1989) Sequence-specific intercalating agents: intercalation at specific sequences on duplex DNA via major groove recognition by oligonucleotide-intercalator conjugates. Proc. Natl Acad. Sci. USA, 86, 9198-9202.
33. Takasugi,M., Guendouz,A., Chassignol,M., Decout,J.L., Lhomme,J., Thuong,N.T. and Helene,C. (1991) Sequence-specific photo-induced cross-linking of the two strands of double-helical DNA by a psoralen covalently linked to a triple helix-forming oligonucleotide. Proc. Natl Acad. Sci. USA, 88, 5602-5606.
34. Orson,F.M., Kinsey,B.M. and McShan,W.M. (1994) Linkage structures strongly influence the binding cooperativity of DNA intercalators conjugated to triplex forming oligonucleotides. Nucleic Acids Res., 22, 479-484.
35. Gasparro,F.P., Havre,P.A., Olack,G.A., Gunther,E.J. and Glazer,P.M. (1994) Site-specific targeting of psoralen photoadducts with a triple helix-forming oligonucleotide: characterization of psoralen monoadduct and crosslink formation. Nucleic Acids Res., 22, 2845-2852.
36. Lacoste,J., Francois,J.C. and Helene,C. (1997) Triple helix formation with purine-rich phosphorothioate-containing oligonucleotides covalently linked to an acridine derivative. Nucleic Acids Res., 25, 1991-1998.
37. Grigoriev,M., Praseuth,D., Robin,P., Hemar,A., Saison-Behmoaras,T., Dautry-Varsat,A., Thuong,N.T., Helene,C. and Harel-Bellan,A. (1992) A triple helix-forming oligonucleotide-intercalator conjugate acts as a transcriptional repressor via inhibition of NF kappa B binding to interleukin-2 receptor alpha-regulatory sequence. J. Biol. Chem., 267, 3389-3395.
38. Duval-Valentin,G., Thuong,N.T. and Helene,C. (1992) Specific inhibition of transcription by triple helix-forming oligonucleotides. Proc. Natl Acad. Sci. USA, 89, 504-508.
39. Grigoriev,M., Praseuth,D., Guieysse,A.L., Robin,P., Thuong,N.T., Helene,C. and Harel-Bellan,A. (1993) Inhibition of gene expression by triple helix-directed DNA cross-linking at specific sites. Proc. Natl Acad. Sci. USA, 90, 3501-3505.
40. Havre,P.A. and Glazer,P.M. (1993) Targeted mutagenesis of simian virus 40 DNA mediated by a triple helix-forming oligonucleotide. J. Virol., 67, 7324-7231.
41. Havre,P.A., Gunther,E.J., Gasparro,F.P. and Glazer,P.M. (1993) Targeted mutagenesis of DNA using triple helix-forming oligonucleotides linked to psoralen. Proc. Natl Acad. Sci. USA, 90, 7879-7883.
42. Wang,G., Levy,D.D., Seidman,M.M. and Glazer,P.M. (1995) Targeted mutagenesis in mammalian cells mediated by intracellular triple helix formation. Mol. Cell. Biol., 15, 1759-1768.
43. Frederick,C.A., Williams,L.D., Ughetto,G., van der Marel,G.A., van Boom,J.H., Rich,A. and Wang,A.H. (1990) Structural comparison of anticancer drug-DNA complexes: adriamycin and daunomycin. Biochemistry, 29, 2538-2549.
44. Chaires,J.B., Satyanarayana,S., Suh,D., Fokt,I., Przewloka,T. and Priebe,W. (1996) Parsing the free energy of anthracycline antibiotic binding to DNA. Biochemistry, 35, 2047-2053.
45. Garbesi,A., Bonazzi,S., Zanella,S., Capobianco,M.L., Giannini,G. and Arcamone,F. (1997) Synthesis and binding properties of conjugates between oligodeoxynucleotides and daunorubicin derivatives. Nucleic Acids Res., 25, 2121-2128.
46. Dang,C.V. (1999) c-Myc target genes involved in cell growth, apoptosis and metabolism. Mol. Cell. Biol., 19, 1-11.
47. Coller,H.A., Grandori,C., Tamayo,P., Colbert,T., Lander,E.S., Eisenman,R.N. and Golub,T.R. (2000) Expression analysis with oligonucleotide microarrays reveals that MYC regulates genes involved in growth, cell cycle, signaling and adhesion. Proc. Natl Acad. Sci. USA, 97, 3260-3265.
48. Spencer,C.A. and Groudine,M. (1991) Control of c-myc regulation in normal and neoplastic cells. Adv. Cancer Res., 56, 1-48.
49. Grandori,C., Cowley,S.M., James,L.P. and Eisenman,R.N. (2000) The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu. Rev. Cell. Dev. Biol., 16, 653-699.
50. Skorski,T., Nieborowska-Skorska,M., Campbell,K., Iozzo,R.V., Zon,G., Darzynkiewicz,Z. and Calabretta,B. (1995) Leukemia treatment in severe combined immunodeficiency mice by antisense oligodeoxynucleotides targeting cooperating oncogenes. J. Exp. Med., 182, 1645-1653.
51. Leonetti,C., D'Agnano,I., Lozupone,F., Valentini,A., Geiser,T., Zon,G., Calabretta,B., Citro,G.C. and Zupi,G. (1996) Antitumor effect of c-myc antisense phosphorothioate oligodeoxynucleotides on human melanoma cells in vitro and and in mice (see comments). J. Natl Cancer Inst., 88, 419-429.
52. Skorski,T., Perrotti,D., Nieborowska-Skorska,M., Gryaznov,S. and Calabretta,B. (1997) Antileukemia effect of c-myc N3′→ P5′ phosphoramidate antisense oligonucleotides in vivo. Proc. Natl Acad. Sci. USA, 94, 3966-3971.
53. Felsher,D.W. and Bishop,J.M. (1999) Reversible tumorigenesis by MYC in hematopoietic lineages. Mol. Cell, 4, 199-207.
54. Cooney,M., Czernuszewicz,G., Postel,E.H., Flint,S.J. and Hogan,M.E. (1988) Site-specific oligonucleotide binding represses transcription of the human c-myc gene in vitro. Science, 241, 456-459.
55. Postel,E.H., Flint,S.J., Kessler,D.J., Hogan,M.E. (1991) Evidence that a triplex-forming oligodeoxyribonucleotide binds to the c-myc promoter in HeLa cells, thereby reducing c-myc mRNA levels. Proc. Natl Acad. Sci. USA, 88, 8227-8231.
56. Thomas,T.J., Faaland,C.A., Gallo,M.A. and Thomas,T. (1995) Suppression of c-myc oncogene expression by a polyamine-complexed triplex forming oligonucleotide in MCF-7 breast cancer cells. Nucleic Acids Res., 23, 3594-3599.
57. Kim,H.G. and Miller,D.M. (1995) Inhibition of in vitro transcription by a triplex-forming oligonucleotide targeted to human c-myc P2 promoter. Biochemistry, 34, 8165-8171.
58. Kim,H.G., Reddoch,J.F., Mayfield,C., Ebbinghaus,S., Vigneswaran,N., Thomas,S., Jones,D.E.,Jr and Miller,D.M. (1998) Inhibition of transcription of the human c-myc protooncogene by intermolecular triplex. Biochemistry, 37, 2299-2304.
59. Catapano,C.V., McGuffie,E.M., Pacheco,D. and Carbone,G.M. (2000) Inhibition of gene expression and cell proliferation by triple helix-forming oligonucleotides directed to the c-myc gene. Biochemistry, 39, 5126-5138.
60. McGuffie,E.M., Pacheco,D., Carbone,G.M. and Catapano,C.V. (2000) Antigene and antiproliferative effects of a c-myc-targeting phosphorothioate triple helix-forming oligonucleotide in human leukemia cells. Cancer Res., 60, 3790-3799.
61. Pandolfi,D., Rauzi,F. and Capobianco,M.L. (1999) Evaluation of different types of end-capping modifications on the stability of oligonucleotides toward 3′- and 5′-exonucleases. Nucl. Nucl., 18, 2051-2069.
62. McGuffie,E.M. and Catapano,C.V. (2002) Design of a novel triple helix-forming oligonucleotide directed to the major promoter of the c-myc gene. Nucleic Acids Res., 30, 2701-2709.
63. Rutherford,A.V. and Willingham,M.C. (1993) Ultrastructural localization of daunomycin in multidrug-resistant cultured cells with modulation of the multidrug transporter. J. Histochem. Cytochem., 41, 1573-1577.
64. Carbone,G.M., McGuffie,E.M., Collier,A. and Catapano,C.V. (2003) Selective inhibition of transcription of the Ets2 gene in prostate cancer cells by a triplex-forming oligonucleotide. Nucleic Acids Res., 31, 833-843.
65. Majello,B., De Luca,P., Suske,G. and Lania,L. (1995) Differential transcriptional regulation of c-myc promoter through the same DNA binding sites targeted by Sp1-like proteins. Oncogene, 10, 1841-1848.
66. Bossone,S.A., Asselin,C., Patel,A.J. and Marcu,K.B. (1992) MAZ, a zinc finger protein, binds to c-MYC and C2 gene sequences regulating transcriptional initiation and termination. Proc. Natl Acad. Sci. USA, 89, 7452-7456.
67. Roussel,M.F., Davis,J.N., Cleveland,J.L., Ghysdael,J. and Hiebert,S.W. (1994) Dual control of myc expression through a single DNA binding site targeted by ets family proteins and E2F-1. Oncogene, 9, 405-415.
68. Hiebert,S.W., Lipp,M. and Nevins,J.R. (1989) E1A-dependent transactivation of the human MYC promoter is mediated by the E2F factor. Proc. Natl Acad. Sci. USA, 86, 3594-3598.
69. Thalmeier,K., Synovzik,H., Mertz,R., Winnacker,E.L. and Lipp,M. (1989) Nuclear factor E2F mediates basic transcription and transactivation by E1a of the human MYC promoter. Genes Dev., 3, 527-536.
70. Kiuchi,N., Nakajima,K., Ichiba,M., Fukada,T., Narimatsu,M., Mizuno,K., Hibi,M. and Hirano,T. (1999) STAT3 is required for the gp130-mediated full activation of the c-myc gene. J. Exp. Med., 189, 63-73.
71. Asselin,C., Nepveu,A. and Marcu,K.B. (1989) Molecular requirements for transcriptional initiation of the murine c-myc gene. Oncogene, 4, 549-558.
72. Albert,T., Wells,J., Funk,J.O., Pullner,A., Raschke,E.E., Stelzer,G., Meisterernst,M., Farnham,P.J. and Eick,D. (2001) The chromatin structure of the dual c-myc promoter P1/P2 is regulated by separate elements. J. Biol. Chem, 276, 20482-20490.
73. Gewirtz,A.M., Sokol,D.L. and Ratajczak,M.Z. (1998) Nucleic acid therapeutics: state of the art and future prospects. Blood, 92, 712-736.
74. Jorcyk,C.L., Watson,D.K., Mavrothalassitis,G.J. and Papas,T.S. (1991) The human ETS1 gene: genomic structure; promoter characterization and alternative splicing. Oncogene, 6, 523-532.
75. Vasquez,K.M., Dagle,J.M., Weeks,D.L. and Glazer,P.M. (2001) Chromosome targeting at short polypurine sites by cationic triplex-forming oligonucleotides. J. Biol. Chem, 276, 38536-38541.
76. Arimondo,P., Bailly,C., Boutorine,A., Asseline,U., Sun,J.S., Garestier,T. and Helene,C. (2000) Linkage of a triple helix-forming oligonucleotide to amsacrine-4-carboxamide derivatives modulates the sequence-selectivity of topoisomerase II-mediated DNA cleavage. Nucl. Nucl. Nucleic Acids, 19, 1205-1218.
77. Arimondo,P.B., Boutorine,A., Baldeyrou,B., Bailly,C., Kuwahara,M., Hecht,S.M., Sun,J.S., Garestier,T. and Helene,C. (2002) Design and optimization of camptothecin conjugates of triple helix-forming oligonucleotides for sequence-specific DNA cleavage by topoisomerase I. J. Biol. Chem., 277, 3132-3140.