Direct inhibition of the DNA-binding activity of POU transcription factors Pit-1 and Brn-3 by selective binding of a phenyl-furan-benzimidazole dication

Nucleic Acids Research

Volumn 36, Issue 10, 2008, Pages 3341-3353

  Peixoto, Paul ^a,b   Liu, Yang ^c   Depauw, Sabine ^a,b   Hildebrand, Marie Paule ^a,b   Boykin, David W ^c   Bailly, Christian ^a,b,d   Wilson, W David ^c   David Cordonnier, Marie Hélène ^a,b  

^a Institut de Recherche sur le Cancer de Lille   (France)

^b IMPRT   (France)

^c GEORGIA STATE UNIVERSITY   (United States)

^d INSTITUT DE RECHERCHE PIERRE FABRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BENZIMIDAZOLE DERIVATIVE; DB 293; DEOXYRIBONUCLEASE I; DIAMIDINE DERIVATIVE; INTERFERON REGULATORY FACTOR 1; TRANSCRIPTION FACTOR PIT 1; TRANSCRIPTION FACTOR POU; TRANSCRIPTION FACTOR POU4; DB293; DNA; FURAN DERIVATIVE;

ARTICLE; AT RICH SEQUENCE; BINDING AFFINITY; BINDING SITE; CONSENSUS SEQUENCE; CONTROLLED STUDY; DNA BINDING; DNA FOOTPRINTING; DRUG STRUCTURE; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; INHIBITION KINETICS; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN MICROARRAY; STOICHIOMETRY; SURFACE PLASMON RESONANCE; BINDING COMPETITION; CHEMISTRY; DNA MICROARRAY; DRUG ANTAGONISM; METABOLISM; METHODOLOGY; NUCLEOTIDE SEQUENCE;

CHLOROCRAMBE HASTATA;

AT RICH SEQUENCE; BASE SEQUENCE; BENZIMIDAZOLES; BINDING SITES; BINDING, COMPETITIVE; CONSENSUS SEQUENCE; DNA; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FURANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SURFACE PLASMON RESONANCE; TRANSCRIPTION FACTOR BRN-3; TRANSCRIPTION FACTOR PIT-1;

EID: 45549100438     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn208     Document Type: Article

References (56)

1. Uil,T,G., Haisma,H.J. and Rots,M.G. (2003) Therapeutie modulation of endogenous gene function by gents with designed DNA-sequence specificities. Nucleic Acids Res., 31, 6064-6078.
2. Gniazdowski,M., Denny,W.A., Nelson,S.M. and Czyz,M. (2003) Transcription factors as targets for DNA-interacting drugs. Curr. Med. Chem., 10, 909-924.
3. Gniazdowski,M., Denny,W.A., Nelson,S.M. and Czyz,M. (2005) Effects of anticancer drugs on transcription factor-DNA interactions. Expert Opin. Ther. Targets, 9, 471-489.
4. D'Incalci,M., Brunelli,D., Marangon,E., Simone,M., Tavecchio,M., Gescher,A. and Mantovani,R. (2007) Modulation of gene transcription by natural products - a viable anticancer strategy. Curr. Pharm. Des. 13, 2744-2750.
5. Wemmer,D.E. and Dervan,P.B. (1997) Targeting the minor groove of DNA. Curr. Opin. Struct. Biol., 7, 355-361.
6. Dervan,P.B. and Edelson,B.S. (2003) Recognition of the DNA minor groove by pyrrole-imidazole polyamides. Curr. Opin. Struct. Biol., 13 284-299.
7. Melander,C., Burnett,R. and Gottesfeld,J.M. (2004) Regulation of gene expression with pyrrole-imidazole polyamides. J. Biotechnol., 112, 195-220.
8. Dickinson,L.A., Burnett,R., Melander,C., Edelson,B.S., Arora,P.S., Dervan,P.B. and Gottesfeld,J.M. (2004) Arresting cancer proliferation by small-molecule gene regulation. Chem. Biol., 11, 1583-1594.
9. Arndt,H.D. and Schoof,S. (2007) Polyamide- and RNA-based activators in living cells: A major step towards controlling gene expression. Chembiochem., 8, 1095-1098.
10. Nickols,N.G. and Dervan,P.B. (2007) Suppression of androgen receptor-mediated gene-expression by a sequence-specific DNA-binding polyamide. Proc. Natl Acad. Sci. USA, 104, 10418-10423.
11. Le,N.M., Sielaff,A.M., Cooper,A.J., Mackay,H, Brown,T., Kotecha,M., O'Hare,C., Hochhauser,D., Lee,M. and Hartley,J.A. (2006) Binding of f-PIP, a pyrrole- and imidazole-containing triamide, to the inverted CCAAT box-2 of the topoisomerase IIalpha promoter and modulation of gene expression in cells. Bioorg. Med. Chem. Lett., 16, 6161-6164.
12. Matsuda,H., Fukuda,N., Ueno,T., Tahira,Y., Ayame,H., Zhang,W., Bando,T., Sugiyama,H., Saito,S., Matsumoto,K. et al. (2006) Development of gene silencing pyrrole-imidazole polyamide targeting the TGF-beta1 promoter for treatment of progressive renal diseases. J. Am. Soc. Nephrol., 17, 422-432.
13. Olenyuk,B.Z., Zhang,G.J., Klco,J.M., Nickols,N.G., Kaelin,W.G. Jr. and Dervan,P.B. (2004) Inhibition of vascular endothelial growth factor with a sequence-specific hypoxia response element antagonist. Proc. Natl Acad. Sci. USA, 101, 16768-16773.
14. Nickols,N.G., Jacobs,C.S., Farkas,M.E. and Dervan,P.B. (2007) Improved nuclear localization of DNA-binding polyamides. Nucleic Acids Res. 35, 363-370.
15. Blume,S.W., Snyder,R.C., Ray,R., Thomas,S., Koller,C.A. and Miller,D.M. (1991) Mithramycin inhibits SP1 binding and selectively inhibits transcriptional activity of the dihydrofolate reductase gene in vitro and in vivo. J. Clin. Invest., 88, 1613-1621.
16. Lee,T.J., Jung,E.M., Lee,J.T., Kim,S., Park,J.W., Choi,K.S. and Kwon,T.K. (2006) Mithramycin A sensitizes cancer cells to TRAIL-mediated apoptosis by down-regulation of XIAP gene promoter through Sp1 sites. Mol. Cancer Ther., 5, 2737-2746.
17. Olajide,O.A., Heiss,E.H., Schachner,D., Wright,C.W., Vollmar,A.M. and Dirsch,V.M. (2007) Synthetic cryptolepine inhibits DNA binding of NF-kappaB. Bioorg. Med. Chem., 15, 43-49.
18. Kong,D., Park,E.J., Stephen,A.G., Calvani,M., Cardellina,J.H., Monks,A., Fisher,R.J., Shoemaker,R.H. and Melillo,G. (2005) Echinomycin, a small-molecule inhibitor of hypoxia-inducible factor-1 DNA-binding activity. Cancer Res., 65, 9047-9055.
19. Nickols,N.G., Jacobs,C.S., Farkas,M.E. and Dervan,P.B. (2007) Modulating hypoxia-inducible transcription by disrupting the HIF-1-DXA interface. ACS Chem. Biol., 2, 561-571.
20. Blagburn,B.L., Drain,K.L, Land,T.M., Moore,P.H., Kinard,R.G., Lindsay,D.S., Kumar,A., Shi,J., Boykin,D.W. and Tidwell,R.R. (1998) Dicationic furans inhibit development of Cryptosporidium parvum in HSD/ ICR suckling Swiss mice. J. Parasitol., 84, 851-856.
21. Wilson,W.D., Nguyen,B., Tanious,F.A., Mathis,A., Hall,J.E., Stephens,C.E. and Boykin,D.W. (2005) Dications that target the DNA minor groove: Compound design and preparation, DNA interactions, cellular distribution and biological activity. Curr. Med. Chem. Anticancer Agents, 5, 389-408.
22. Bailly,C., Dassonneville,L., Carrasco,C., Lucas,D., Kumar,A., Boykin,D.W. and Wilson,W.D. (1999) Relationships between topoisomerase II inhibition, sequence-specificity and DNA binding mode of dicationic diphenylfuran derivatives. Anticancer Drug Des., 14, 47-60.
23. Wilson,W.D., Tanious,F., Ding,D., Kumar,A., Boykin,D.W., Colson,P., Houssier,C. and Bailly,C. (1998) 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.
24. Bailly,C., Tardy,C., Wang,L., Armitage,B., Hopkins,K., Kumar,A., Schuster,G.B., Boykin,D.W. and Wilson,W.D. (2001) Recognition of ATGA sequences by the unfused aromatic dication DB293 forming stacked dimers in the DNA minor groove. Biochemistry, 40, 9770-9779.
25. Wang,L., Bailly,C., Kumar,A., Ding,D., Bajic,M., Boykin,D.W. and Wilson,W. D. (2000) 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.
26. Tanious,F.A., Wilson,W.D., Wang,L., Kumar,A., Boykin,D.W., Marty,C., Baldeyrou,B. and Bailly,C. (2003) Cooperative dimerization of a heterocyclic diamidine determines sequence-specific DNA recognition. Biochemistry, 42, 13576-13586.
27. Coccia,E.M., Del Russo,N., Stellacci,E., Orsatti,R., Benedetti,E., Marziali,G., Hiscott,J. and Battistini,A. (1999) Activation and repression of the 2-5A synthetase and p21 gene promoters by IRF-1 and IRF-2. Oncogene, 18, 2129-2137.
28. Garcia,A., Alvarez,C.V., Smith,R. and Dieguez,C. (2001) Regulation of Pit-1 expression by ghrelin and GHRP-6 through the GH secretagogue receptor. Mol. Endocrinol., 15, 1484-1495.
29. Suaud,L., Formstecher,P. and Laine,B. (1999) The activity of the activation function 2 of the human hepatocyte nuclear factor 4 (HNF-4alpha) is differently modulated by F domains from various origins. Biochem. J., 340, 161-169.
30. Liu,W., Khare,S.L., Liang,X., Peters,M.A., Liu,X., Cepko,C.L. and Xiang,M. (2000) All Brn3 genes can promote retinal ganglion cell differentiation in the chick. Development, 127, 3237-3247.
31. Lam,R. and Li,X. (2002) An array-based method for specifically profiling multiple transcription factor activity. Am. Biotechnol. Lab., 8 22-26.
32. Xiang,M., Zhou,L., Macke,J.P., Yoshioka,T., Hendry,S.H., Eddy,R.L., Shows,T.B. and Nathans,J. (1995) The Brn-3 family of POU-domain factors: primary structure, binding specificity, and expression in subsets of retinal ganglion cells and somatosensory neurons. J. Neurosci., 15, 4762-4785.
33. Mangalam,H.J., Albert,V.R., Ingraham,H.A., Kapiloff,M., Wilson,L., Nelson,Ch., Elsholtz,H. and Rosenfeld,M.G. (1989) A pituitary POU domain protein, Pit-1, activates both growth hormone and prolactin promoters transcriptionally. Genes Dev., 3, 946-958.
34. Tanaka,N., Kawakami,T. and Taniguchi,T. (1993) Recognition DNA sequences of interferon regulatory factor 1 (IRF-1) and IRF-2, regulators of cell growth and the interferon system. Mol. Cell. Biol., 13, 4531-4538.
35. Fraser,J.D., Martinez,V., Straney,R. and Briggs,M.R. (1998) DNA binding and transcription activation specificity of hepatocyte nuclear factor 4. Nucleic Acids Res., 26, 2702-2707.
36. David-Cordonnier,M.H., Laine,W., Lansiaux,A., Rosu,F., Colson,P., de Pauw,E., Michel,S., Tillequin,F., Koch,M., Hickman,J.A. et al. (2005) Covalent binding of antitumor benzoacronycines to double-stranded DNA induces helix opening and the formation of single-stranded DNA: unique consequences of a novel DNA-bonding mechanism. Mol Cancer Ther., 4, 71-80.
37. David-Cordonnier,M.-H., Hamdane,M., Bailly,C. and D'Halluin,J.-C. (1998) The DNA binding domain of the human c-Abl tyrosine kinase preferentially binds to DNA sequences containing an AAC-motif and to distorted DNA structures. Biochemistry, 37, 6065-6016.
38. Munde,M., Ismail,M.A., Arafa,R., Peixoto,P., Collar,C.J., Liu,Y., Hu,L., David-Cordonnier,M.-H., Lansiaux,A., Bailly,C. et al. (2007) Design of DNA minor groove binding diamidines that recognize GC base pair sequences: A novel dimeric-hinge motif. JACS, 129, 13732-13743.
39. Tanious,F.A., Nguyen,B. and Wilson,W.D. (2008) Biosensor-surface plasmon resonance methods for quantitative analysis of biomolecular interactions. Methods Cell Biol., 84, 53-77.
40. Lillycrop,K.A., Budrahan,V.S., Lakin,N.D., Terrenghi,G., Wood,J.N., Polak,J.M. and Latchman,D.S. (1992) A novel POU family transcription factor is closely related to Brn-3 but has a distinct expression pattern in neuronal cells. Nucleic Acids Res., 20, 5093-5096.
41. Ninkina,N.N., Stevens,G.E., Wood,J.N. and Richardson,W.D. (1993) A novel Brn3-like POU transcription factor expressed in subsets of rat sensory and spinal cord neurons. Nucleic Acids Res., 21, 3175-3182.
42. Jacobson,E.M., Li,P., Leon-del-Rio,A., Rosenfeld,M.G. and Aggarwal,A.K. (1997) Structure of Pit-1 POU domain bound to DNA as a dimer: Unexpected arrangement and flexibility. Genes Dev., 11, 198-212.
43. Tanious,F.A., Hamelberg,D., Bailly,C., Czarny,A., Boykin,D.W. and Wilson,W.D. (2004) DNA sequence dependent monomer-dimer binding modulation of asymmetric benzimidazole derivatives. J. Am. Chem. Soc. 126, 143-153.
44. Escalante,C.R., Yie,J., Thanos,D. and Aggarwal,A.K. (1998) Structure of IRF-1 with bound DNA reveals determinants of interferon regulation. Nature, 391, 103-106.
45. Herr,W. and, Cleary,M.A. (1995) The POU domain: Versatility in transcriptional regulation by a flexible two-in-one DNA-binding domain. Genes Dev., 9, 1679-1693.
46. Klemm,J.D., Rould,M.A., Aurora,R., Herr,W. and Pabo,C.O. (1994) Crystal structure of the Oct-1 POU domain bound to an actamer site: DNA recognition with tethered DNA-binding modules. Cell, 77, 21-32.
47. Scully,K.M., Jacobson,E.M., Jepsen,K., Lunyak,V., Viadiu,H., Carrière,C., Rose,D.W., Hooshmand,F., Aggarwal,A.K. and Rosenfeld,M.G. (2000) Allosteric effects of Pit-1 DNA sites on long-term repression in cell type specification. Science, 290, 1127-1131.
48. Ndisdang,D., Morris,P.J., Chapman,C., Ho,L., Singer,A. and Latchman,D.S. (1998) The HPV-activating cellular transcription factor Brn-3a is overexpressed in CIN3 cervical lesions. J. Clin. Invest., 101 1687-1692.
49. Dennis,J.H., Budhram-Mahadeo,V. and Latchman,DS. (2001) The Brn-3b POU family transcription factor regulates the cellular growth, proliferation, and anchorage dependence of MCF7 human breast cancer cells. Oncogene, 20, 4961-4971.
50. Budhram-Mahadeo,V., Ndisang,D., Ward,T., Weber,B.L. and Latchman,D.S. (1999) The Brn-3b POU family transcription factor represses expression of the BRCA-1 anti-oncogene in breast cancer cells. Oncogene, 18, 6684-6691.
51. Samady,L., Dennis,J., Budhram-Mahadeo,V. and Latchman,D.S. (2004) Activation of CDK4 gene expression in human breast cancer cells by the Brn-3b POU family transcription factor. Cancer Biol. Ther., 3 317-323.
52. Li,S., Crenshaw,E.B. 3rd, Rawson,E.J., Simmons,D.M., Swanson,L.W. and Rosenfeld,M.G. (1990) Dwarf locus mutants lacking three pituitary cell types result from mutations in the POU-domain gene pit-1. Nature, 347, 528-533.
53. Castrillo,J.L., Theill,L.E. and Karin,M. (1991) Function of the homeodomain protein GHF1 in pituitary cell proliferation. Science, 253, 197-199.
54. Asa,S.L., Puy,L.A., Lew,A.M., Sundmark,V.C. and Elsholtz,H.P. (1993) Cell type-specific expression of the pituitary transcription activator pit-1 in the human pituitary and pituitary adenomas. J. Clin. Endocrinol. Metab., 77, 1275-1280.
55. Pellegrini,I., Barlier,A., Gunz,G., Figarella-Branger.D., Enjalbert,A., Grisoli,F. and Jaquet,P. Pit-1 gene expression in the human pituitary and pituitary adenomas. J. Clin. Endocrinol. Metab., 79, 189-196.
56. Gil-Puig,C., Seoane,S., Blanco,M., Macia,M., Garcia-Caballero,T., Segura,C. and Perez-Fernandez,R. (2005) Pit-1 is expressed in normal and tumorous human breast and regulates GH secretion and cell proliferation. Eur. J. Endocrinol., 153, 335-344.