Targeting a DNA binding motif of the EVI1 protein by a pyrrole-imidazole polyamide

Biochemistry

Volumn 50, Issue 48, 2011, Pages 10431-10441

  Zhang, Yi ^a   Sicot, Géraldine ^a   Cui, Xiaohui ^a   Vogel, Marion ^a   Wuertzer, Charles A ^a   Lezon Geyda, Kimberly ^b   Wheeler, John ^b   Harki, Daniel A ^c,d   Muzikar, Katy A ^c   Stolper, Daniel A ^e   Dervan, Peter B ^c   Perkins, Archibald S ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c California Institute of Technology   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

^e NONE

Author keywords

[No Author keywords available]

Indexed keywords

CELL LINES; CELL-PERMEABLE; COLONY FORMATION; CONTROL-CELL; CRITICAL FUNCTIONS; DNA BINDING; EFFECTIVE THERAPY; ELECTROMOBILITY; FOOTPRINTING; HIGH AFFINITY; IN-VIVO; LEUKEMIC CELLS; LEUKEMOGENESIS; PYRROLE-IMIDAZOLE POLYAMIDES; REPORTER ASSAY; SMALL MOLECULES; STRUCTURE-FUNCTION STUDIES; TRANSFORMING ACTIVITY; ZINC FINGER DOMAINS; ZINC FINGER PROTEIN;

ASSAYS; CELL CULTURE; CELLS; NITROGEN COMPOUNDS; TRANSCRIPTION FACTORS; ZINC;

DNA;

ANTILEUKEMIC AGENT; DEOXYRIBONUCLEASE I; EVI1 PROTEIN; POLYAMIDE; POLYAMIDE 1; POLYAMIDE 2; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ARTICLE; CANCER GROWTH; CONTROLLED STUDY; DNA BINDING MOTIF; DRUG PROTEIN BINDING; IN VIVO STUDY; LEUKEMIA; LEUKEMOGENESIS; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; DNA-BINDING PROTEINS; DRUG DELIVERY SYSTEMS; GROWTH INHIBITORS; HUMANS; IMIDAZOLES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MYELOID CELLS; NYLONS; PROTEIN BINDING; PROTO-ONCOGENES; PYRROLES; RATS; RETROVIRIDAE; TRANSCRIPTION FACTORS;

EID: 82455175405     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200962u     Document Type: Article

References (53)

1. Perkins, A. S., Fishel, R., Jenkins, N. A., and Copeland, N. G. (1991) Evi -1, a murine zinc finger proto-oncogene, encodes a sequence-specific DNA-binding protein Mol. Cell. Biol. 11, 2665-2674 (Pubitemid 21895646)
2. Delwel, R., Funabiki, T., Kreider, B., Morishita, K., and Ihle, J. (1993) Four of the seven zinc fingers of the Evi-1 myeloid transforming gene are required for sequence-specific binding to GA(C/T)AAGA(T/C)AAGATAA Mol. Cell. Biol. 13, 4291-4300 (Pubitemid 23187658)
3. Funabiki, T., Kreider, B. L., and Ihle, J. N. (1994) The carboxyl domain of zinc fingers of the Evi-1 myeloid transforming gene binds a consensus sequence GAAGATGAG Oncogene 9, 1575-1581 (Pubitemid 24163382)
4. Kilbey, A. and Bartholomew, C. (1998) Evi-1 ZF1 DNA binding activity and a second distinct transcriptional repressor region are both required for optimal transformation of Rat1 fibroblasts Oncogene 16, 2287-2291 (Pubitemid 28220659)
5. Perkins, A. and Kim, J. (1996) Zinc fingers 1-7 of EVI1 fail to bind to the GATA motif by itself but require the core site GACAAGATA for binding J. Biol. Chem. 271, 1104-1110 (Pubitemid 26034972)
6. Kreider, B., Orkin, S., and Ihle, J. (1993) Loss of erythropoietin responsiveness in erythroid progenitors due to expression of the Evi-1 myeloid transforming gene Proc. Natl. Acad. Sci. U. S. A. 90, 6454-6458 (Pubitemid 23207231)
7. Bartholomew, C., Kilbey, A., Clark, A., and Walker, M. (1997) The Evi-1 proto-oncogene encodes a transcriptional repressor activity associated with transformation Oncogene 14, 569-577 (Pubitemid 27090959)
8. Yuasa, H., Oike, Y., Iwama, A., Nishikata, I., Sugiyama, D., Perkins, A., Mucenski, M., Suda, T., and Morishita, K. (2005) Oncogenic transcription factor Evi1 regulates hematopoietic stem cell proliferation through GATA-2 expression EMBO J. 24, 1976-1987 (Pubitemid 40896169)
9. Morishita, K., Suzukawa, K., Taki, T., Ihle, J. N., and Yokota, J. (1995) EVI-1 zinc finger protein works as a transcriptional activator via binding to a consensus sequence of GACAAGATAAGATAAN1-28CTCATCTTC Oncogene 10, 1961-1967
10. Tanaka, T., Nishida, J., Mitani, K., Ogawa, S., Yazaki, Y., and Hirai, H. (1994) Evi-1 raises AP-1 activity and stimulates c- fos promoter transactivation with dependence on the second zinc finger domain J. Biol. Chem. 269, 24020-24026 (Pubitemid 24300933)
11. Izutsu, K., Kurokawa, M., Imai, Y., Maki, K., Mitani, K., and Hirai, H. (2001) The corepressor CtBP interacts with Evi-1 to repress transforming growth factor beta signaling Blood 97, 2815-2822
12. Palmer, S., Brouillet, J., Kilbey, A., Fulton, R., Walker, M., Crossley, M., and Bartholomew, C. (2001) Evi-1 transforming and repressor activities are mediated by CtBP co-repressor proteins J. Biol. Chem. 276, 25834-25840
13. Yatsula, B., Lin, S., Read, A., Poholek, A., Yates, K., Yue, D., Hui, P., and Perkins, A. (2005) Identification of binding sites of EVI1 in mammalian cells J. Biol. Chem. 280, 30712-30722 (Pubitemid 41291800)
14. Dervan, P. (2001) Molecular recognition of DNA by small molecules Bioorg. Med. Chem. 9, 2215-2235 (Pubitemid 32834613)
15. Dervan, P. and Edelson, B. (2003) Recognition of the DNA minor groove by pyrrole-imidazole polyamides Curr. Opin. Struct. Biol. 13, 284-299 (Pubitemid 36782454)
16. Kielkopf, C., Bermer, R., White, S., Szewczyk, J., Turner, J., Baird, E., Dervan, P., and Rees, D. (2000) Structural effects of DNA sequence on T · A recognition by hydroxypyrrole/pyrrole pairs in the minor groove J. Mol. Biol. 295, 557-567
17. Kielkopf, C. L., Baird, E. E., Dervan, P. B., and Rees, D. C. (1998) Nat. Struct. Biol. 5, 104-109
18. Kielkopf, C. L., White, S., Szewczyk, J. W., Turner, J. M., Baird, E. E., Dervan, P. B., and Rees, D. C. (1998) Science 282, 111-115
19. Trauger, J. W., Baird, E. E., and Dervan, P. B. (1996) Nature 382, 559-561
20. Hsu, C. F., Phillips, J. W., Trauger, J. W., Farkas, M. E., Belitsky, J. M., Heckel, A., Olenyuk, B. Z., Puckett, J. W., Wang, C. C., and Dervan, P. B. (2007) Tetrahedron 63, 6146-6151
21. Dudouet, B., Burnett, R., Dickinson, L. A., Wood, M. R., Melander, C., Belitsky, J. M., Edelson, B., Wurtz, N., Briehn, C., Dervan, P. B., and Gottesfeld, J. M. (2003) Chem. Biol. 10, 859-867
22. Best, T., Edelson, B., Nickols, N., and Dervan, P. (2003) Nuclear localization of pyrrole-imidazole polyamide-fluorescein conjugates in cell culture Proc. Natl. Acad. Sci. U. S. A. 100, 12063
23. Edelson, B., Best, T., Olenyuk, B., Nickols, N., Doss, R., Foister, S., Heckel, A., and Dervan, P. (2004) Influence of structural variation on nuclear localization of DNA-binding polyamide-fluorophore conjugates Nucleic Acids Res. 32, 2802
24. Olenyuk, B., Zhang, G., Klco, J., Nikols, N., Kaelin, W., and Dervan, P. (2004) Inhibition of vascular endothelial growth factor with a sequence-specific hypoxia response element antagonist Proc. Natl. Acad. Sci. U. S. A. 101, 16768-16773 (Pubitemid 39601313)
25. Nickols, N., Jacobs, C., Farkas, M., and Dervan, P. (2007) Modulating Hypoxia-Inducible Transcription by Disrupting the HIF-1-DNA Interface ACS Chem. Biol. 2, 561
26. Nickols, N., Jacobs, C., Farkas, M., and Dervan, P. (2007) Improved nuclear localization of DNA-binding polyamides Nucleic Acids Res. 35, 363-370 (Pubitemid 46237387)
27. Muzikar, K. A., Nickols, N. G., and Dervan, P. B. (2009) Proc. Natl. Acad. Sci. U. S. A. 106, 16598-16603
28. Belitsky, J., Nguyen, D., Wurtz, N., and Dervan, P. (2002) Solid-phase synthesis of DNA binding polyamides on oxim resin Bioorg. Med. Chem. 10, 2767-2774 (Pubitemid 34626240)
29. Dose, C., Farkas, M. E., Chenoweth, D. M., and Dervan, P. B. (2008) Next generation hairpin polyamides with (R)-3,4-diaminobutyric acid turn unit J. Am. Chem. Soc. 130, 6859-6866 (Pubitemid 351748424)
30. Chenoweth, D., Harki, D., Phillips, J., Dose, C., and Dervan, P. (2009) Cyclic pyrrole-imidazole polyamides targeted to the androgen response element J. Am. Chem. Soc. 131, 7182-7188
31. Trauger, J. and Dervan, P. (2001) Footprinting methods for analysis of pyrrole-imidazole polyamide/DNA complexes Methods Enzymol. 340, 450-466 (Pubitemid 32751714)
32. Iverson, B. and Dervan, P. (1987) Adenine specific DNA chemical sequencing reaction Nucleic Acids Res. 15, 7823-7830
33. Maxam, A. and Gilbert, W. (1980) Sequencing end-labeled DNA with base-specific chemical cleavages Methods Enzymol. 65, 499-560
34. Kunkel, T. (1993) Oligonucleotide-directed mutagenesis without phenotypic selection, in Current Protocols in Molecular Biology (Ausubel, F., Brent, R., Kingston, R., Moore, D., Seidman, J., Smith, J., and Struhl, K., Eds.) pp 8.1.1-8.1.6, John Wiley and Sons, New York.
35. Morgenstern, J. and Land, H. (1990) Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line Nucleic Acids Res. 18, 3587-3596
36. Lavau, C., Szilvassy, S., Slany, R., and Cleary, M. (1997) Immortalization and leukemic transformation of a myelomonocytic precursor by retrovirally transduced HRX-ENL EMBO J. 16, 4226-4237 (Pubitemid 27298175)
37. Ausubel, F., Brent, R., Kingston, R., Moore, D., Seidman, J., Smith, J., and Struhl, K. (1997) (Chanda, V., Ed.) John Wiley & Sons, Inc., Hoboken, NJ.
38. Morishita, K., Parker, D. S., Mucenski, M. L., Jenkins, N. A., Copeland, N. G., and Ihle, J. N. (1988) Retroviral activation of a novel gene encoding a zinc finger protein in IL3-dependent myeloid leukemia cell lines Cell 54, 831-840
39. Smith, D. (1993) Purification of glutathione-S-transferase fusion proteins Methods Mol. Cell. Biol. 4, 220-229
40. Chodosh, L. A., Carthew, R. W., and Sharp, P. A. (1986) A single polypeptide possesses the binding and transcription activities of the adenovirus major late transcription factor Mol. Cell. Biol. 6, 4723-4733
41. Pavletich, N. and Pabo, C. (1991) Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A Science 252, 809-817 (Pubitemid 121000517)
42. Blumberg, H., Eisen, A., Sledziewski, A., Bader, D., and Young, E. (1987) Two zinc fingers of a yeast regulatory protein shown by genetic evidence to be essential for function Nature 328, 443-445 (Pubitemid 17097779)
43. Wilson, T., Day, M., Pexton, T., Padgett, K., Johnston, M., and Milbrandt, J. (1992) In vivo mutational analysis of the NGFI-A zinc fingers J. Biol. Chem. 267, 3718-3724
44. Luo, R., Lavau, C., Du, C., Simone, F., Polak, P., Kawamata, S., and Thirman, M. (2001) The elongation domain of ELL is dispensible but its ELL-associated factor 1 interaction domain is essential for MLL-ELL-induced leukemogenesis Mol. Cell. Biol. 21, 5678-5687 (Pubitemid 32702470)
45. White, S., Szewczyk, J., Turner, J., Baird, E., and Dervan, P. (1998) Recognition of the four Watson-Crick base pairs in the DNA minor groove by synthetic ligands Nature 391, 468-471 (Pubitemid 28086542)
46. Shockett, P., Difilippantonio, M., Hellman, N., and Schatz, D. (1995) A modified tetracycline-regulated system provides autoregulatory, inducible gene expression in cultured cells and transgenic mice Proc. Natl. Acad. Sci. U. S. A. 92, 6522-6
47. del Campo, J., Wuertzer, C., Xiao, Y.-Y., Zhang, Y., Lin, S., Dudley, J., Tuck, D., Yatsula, B., and Perkins, A. EVI1 blocks apoptosis in myeloid leukemia cells via enhanced transcription of the prosurvival gene Bcl2a1 (A1). Blood, in revision.
48. Lai, Y., Fukuda, N., Ueno, T., Matsuda, H., Saito, S., Matsumoto, K., Ayame, H., Bando, T., Sugiyama, H., Mugishima, H., and Serie, K. (2005) Synthetic pyrrole-imidazole polyamide inhibits expression of the human transforming growth factor-β1 gene J. Pharm. Exp. Ther. 315, 571-575 (Pubitemid 41500721)
49. Yao, E., Fukuda, N., Ueno, T., Matsuda, H., Matsumoto, K., Nagase, H., Matsumoto, Y., Takasaka, A., Serie, K., Sugiyama, H., and Sawamura, T. (2008) Novel Gene Silencer Pyrrole-Imidazole Polyamide Targeting Lectin-Like Oxidized Low-Density Lipoprotein Receptor-1 Attenuates Restenosis of the Artery After Injury Hypertension 52, 86-92
50. Campos, L., Guyotat, D., Archimbaud, E., Calmard-Oriol, P., Tsuruo, T., Troncy, J., D, T., and Fiere, D. (1992) Clinical significance of multidrug resistance P-glycoprotein expression on acute nonlymphoblastic leukemia cells at diagnosis Blood 79, 473-476
51. Kurokawa, M., Mitani, K., Irie, K., Matsuyama, T., Takahashi, T., Chiba, S., Yazaki, Y., Matsumoto, K., and Hirai, H. (1998) The oncoprotein Evi-1 represses TGF-beta signalling by inhibiting Smad3 Nature 394, 92-96 (Pubitemid 28321809)
52. Alliston, T., Ko, T., Cao, Y., Liang, Y.-Y., Feng, X.-H., Chang, C., and Derynck, R. (2005) Repression of bone morphogenetic protein and activin-inducible transcription by Evi-1 J. Biol. Chem. 280, 24227-24237 (Pubitemid 40894644)
53. Kim, J., Hui, P., Yue, D., Aycock, J., Leclerc, C., Bjoring, A., and Perkins, A. (1998) Identification of candidate target genes for EVI1, a zinc finger oncoprotein, using a novel selection strategy Oncogene 17, 1527-1538 (Pubitemid 28472757)