Runx1 regulation of Pu.1 corepressor/coactivator exchange identifies specific molecular targets for leukemia differentiation therapy

Journal of Biological Chemistry

Volumn 289, Issue 21, 2014, Pages 14881-14895

  Gu, Xiaorong ^a   Hu, Zhenbo ^a,d   Ebrahem, Quteba ^a   Crabb, John S ^b   Mahfouz, Reda Z ^a   Radivoyevitch, Tomas ^c   Crabb, John W ^b   Saunthararajah, Yogen ^a  

^a TAUSSIG CANCER INSTITUTE   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d WEIFANG MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; CYTOLOGY; GENES; MACROPHAGES; TRANSCRIPTION FACTORS;

CHROMATIN IMMUNOPRECIPITATION ANALYSIS; CO-OPERATIVE ASSEMBLY; HEMATOPOIETIC CELL; IMMUNOPRECIPITATIONS; MACROPHAGE DIFFERENTIATIONS; TANDEM MASS SPECTROMETRY; TERMINAL DIFFERENTIATION; TUMOR SUPPRESSOR GENES;

DISEASES;

ANTILEUKEMIC AGENT; BARRIER TO AUTOINTEGRATION FACTOR; BINDING PROTEIN; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 1 INHIBITOR; DNA METHYLTRANSFERASE INHIBITOR; POLYCOMB GROUP PROTEIN; POLYCOMB INHIBITOR; PROTEIN B WICH; PROTEIN COREST; PROTEIN NURD; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NUAT; TRANSCRIPTION FACTOR PU 1; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR SIN3A; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CANCER THERAPY; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG TARGETING; EPIGENETIC REPRESSION; GENE ACTIVATION; GENE DELETION; GENE LOCUS; GENE MUTATION; GENE REPRESSION; HEMATOPOIETIC CELL; HISTONE MODIFICATION; LEUKEMIA CELL; LEUKEMIA DIFFERENTIATION THERAPY; MACROPHAGE; MOUSE; MYELOID LEUKEMIA; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; WILD TYPE;

CHROMATIN MODIFYING ENZYMES; ENHANCEOSOME; ENZYME INHIBITORS; EPIGENETICS; LEUKEMOGENESIS; PROTEIN COMPLEXES; PROTEIN INTERACTOME; TRANSCRIPTION COACTIVATORS; TRANSCRIPTION REGULATION; TRANSCRIPTION REPRESSOR;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; CO-REPRESSOR PROTEINS; CORE BINDING FACTOR ALPHA 2 SUBUNIT; GENE EXPRESSION PROFILING; HEK293 CELLS; HUMANS; LEUKEMIA; MACROPHAGES; MICE; MICE, KNOCKOUT; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; TANDEM MASS SPECTROMETRY; TRANS-ACTIVATORS; TUMOR CELLS, CULTURED;

EID: 84901471487     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.562447     Document Type: Article

References (47)

1. Rosenfeld, M. G., Lunyak, V. V., and Glass, C. K. (2006) Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signaldependent programs of transcriptional response. Genes Dev. 20, 1405-1428 (Pubitemid 43830648)
2. Perissi, V., Jepsen, K., Glass, C. K., and Rosenfeld, M. G. (2010) Deconstructing repression: evolving models of co-repressor action. Nat. Rev. Genet. 11, 109-123
3. Wang, Z., Zang, C., Cui, K., Schones, D. E., Barski, A., Peng, W., and Zhao, K. (2009) Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138, 1019-1031
4. Ram, O., Goren, A., Amit, I., Shoresh, N., Yosef, N., Ernst, J., Kellis, M., Gymrek, M., Issner, R., Coyne, M., Durham, T., Zhang, X., Donaghey, J., Epstein, C. B., Regev, A., and Bernstein, B. E. (2011) Combinatorial patterning of chromatin regulators uncovered by genome-wide location analysis in human cells. Cell 147, 1628-1639
5. Niimi, H., Harada, H., Harada, Y., Ding, Y., Imagawa, J., Inaba, T., Kyo, T., and Kimura, A. (2006) Hyperactivation of the RAS signaling pathway in myelodysplastic syndrome with AML1/RUNX1 point mutations. Leukemia 20, 635-644
6. Miyoshi, H., Shimizu, K., Kozu, T., Maseki, N., Kaneko, Y., and Ohki, M. (1991) t(8;21) breakpoints on chromosome 21 in acute myeloid leukemia are clustered within a limited region of a single gene, AML1. Proc. Natl. Acad. Sci. U.S.A. 88, 10431-10434 (Pubitemid 21915849)
7. Yergeau, D. A., Hetherington, C. J., Wang, Q., Zhang, P., Sharpe, A. H., Binder, M., Marín-Padilla, M., Tenen, D. G., Speck, N. A., and Zhang, D. E. (1997) Embryonic lethality and impairment of haematopoiesis in mice heterozygous for an AML1-ETO fusion gene. Nat. Genet. 15, 303-306 (Pubitemid 27098728)
8. Puig-Kröger, A., Sanchez-Elsner, T., Ruiz, N., Andreu, E. J., Prosper, F., Jensen, U. B., Gil, J., Erickson, P., Drabkin, H., Groner, Y., and Corbi, A. L. (2003) RUNX/AML and C/EBP factors regulate CD11a integrin expression in myeloid cells through overlapping regulatory elements. Blood 102, 3252-3261 (Pubitemid 37314764)
9. Zhang, D. E., Hetherington, C. J., Meyers, S., Rhoades, K. L., Larson, C. J., Chen, H. M., Hiebert, S. W., and Tenen, D. G. (1996) CCAAT enhancerbinding protein (C/EBP) and AML1 (CBFα2) synergistically activate the macrophage colony-stimulating factor receptor promoter. Mol. Cell. Biol. 16, 1231-1240 (Pubitemid 26061693)
10. Petrovick, M. S., Hiebert, S. W., Friedman, A. D., Hetherington, C. J., Tenen, D. G., and Zhang, D. E. (1998) Multiple functional domains of AML1: PU.1 and C/EBPα synergize with different regions of AML1. Mol. Cell. Biol. 18, 3915-3925 (Pubitemid 28287915)
11. Elagib, K. E., Racke, F. K., Mogass, M., Khetawat, R., Delehanty, L. L., and Goldfarb, A. N. (2003) RUNX1 and GATA-1 coexpression and cooperation in megakaryocytic differentiation. Blood 101, 4333-4341 (Pubitemid 36857797)
12. Waltzer, L., Ferjoux, G., Bataillé, L., and Haenlin, M. (2003) Cooperation between the GATA and RUNX factors Serpent and Lozenge during Drosophila hematopoiesis. EMBO J. 22, 6516-6525 (Pubitemid 38009599)
13. Tagoh, H., Ingram, R., Wilson, N., Salvagiotto, G., Warren, A. J., Clarke, D., Busslinger, M., and Bonifer, C. (2006) The mechanism of repression of the myeloid-specific c-fms gene by Pax5 during B lineage restriction. EMBO J. 25, 1070-1080 (Pubitemid 43372120)
14. Huang, H., Yu, M., Akie, T. E., Moran, T. B., Woo, A. J., Tu, N., Waldon, Z., Lin, Y. Y., Steen, H., and Cantor, A. B. (2009) Differentiation-dependent interactions between RUNX-1 and FLI-1 during megakaryocyte development. Mol. Cell. Biol. 29, 4103-4115
15. Kim, W. Y., Sieweke, M., Ogawa, E., Wee, H. J., Englmeier, U., Graf, T., and Ito, Y. (1999) Mutual activation of Ets-1 andAML1DNAbinding by direct interaction of their autoinhibitory domains. EMBO J. 18, 1609-1620 (Pubitemid 29127073)
16. Goetz, T. L., Gu, T. L., Speck, N. A., and Graves, B. J. (2000) Auto-inhibition of Ets-1 is counteracted by DNA binding cooperativity with corebinding factorα2. Mol. Cell Biol. 20, 81-90 (Pubitemid 30002550)
17. Wilson, N. K., Foster, S. D., Wang, X., Knezevic, K., Schütte, J., Kaimakis, P., Chilarska, P. M., Kinston, S., Ouwehand, W. H., Dzierzak, E., Pimanda, J. E., de Bruijn, M. F., and Göttgens, B. (2010) Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell 7, 532-544
18. Zhang, D. E., Hohaus, S., Voso, M. T., Chen, H. M., Smith, L. T., Hetherington, C. J., and Tenen, D. G. (1996) Function of PU.1 (Spi-1), C/EBP, and AML1 in early myelopoiesis: regulation of multiple myeloid CSF receptor promoters. Curr. Top. Microbiol. Immunol. 211, 137-147 (Pubitemid 26024018)
19. Xu, G., Kanezaki, R., Toki, T., Watanabe, S., Takahashi, Y., Terui, K., Kitabayashi, I., and Ito, E. (2006) Physical association of the patient-specific GATA1 mutants with RUNX1 in acute megakaryoblastic leukemia accompanying Down syndrome. Leukemia 20, 1002-1008 (Pubitemid 43797291)
20. Hu, Z., Gu, X., Baraoidan, K., Ibanez, V., Sharma, A., Kadkol, S., Munker, R., Ackerman, S., Nucifora, G., and Saunthararajah, Y. (2011) RUNX1 regulates corepressor interactions of PU.1. Blood 117, 6498-6508
21. Saunthararajah, Y., Triozzi, P., Rini, B., Singh, A., Radivoyevitch, T., Sekeres, M., Advani, A., Tiu, R., Reu, F., Kalaycio, M., Copelan, E., Hsi, E., Lichtin, A., and Bolwell, B. (2012) p53-independent, normal stem cell sparing epigenetic differentiation therapy for myeloid and other malignancies. Semin. Oncol. 39, 97-108
22. Sun, W., and Downing, J. R. (2004) Haploinsufficiency of AML1 results in a decrease in the number of LTR-HSCs while simultaneously inducing an increase in more mature progenitors. Blood 104, 3565-3572 (Pubitemid 39564428)
23. Walsh, J. C., DeKoter, R. P., Lee, H. J., Smith, E. D., Lancki, D. W., Gurish, M. F., Friend, D. S., Stevens, R. L., Anastasi, J., and Singh, H. (2002) Cooperative and antagonistic interplay between PU.1 and GATA-2 in the specification of myeloid cell fates. Immunity 17, 665-676 (Pubitemid 35351511)
24. Gentles, A. J., Plevritis, S. K., Majeti, R., and Alizadeh, A. A. (2010) Association of a leukemic stem cell gene expression signature with clinical outcomes in acute myeloid leukemia. JAMA 304, 2706-2715
25. Weigelt, K., Lichtinger, M., Rehli, M., and Langmann, T. (2009) Transcriptomic profiling identifies a PU.1 regulatory network in macrophages. Biochem. Biophys. Res. Commun. 380, 308-312
26. Huang da, W., Sherman, B. T., and Lempicki, R. A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57
27. Agrawal, S., Hofmann, W. K., Tidow, N., Ehrich, M., van den Boom, D., Koschmieder, S., Berdel, W. E., Serve, H., and Müller-Tidow, C. (2007) The C/EBPδ tumor suppressor is silenced by hypermethylation in acute myeloid leukemia. Blood 109, 3895-3905 (Pubitemid 46641742)
28. Negrotto, S., Ng, K. P., Jankowska, A. M., Bodo, J., Gopalan, B., Guinta, K., Mulloy, J. C., Hsi, E., Maciejewski, J., and Saunthararajah, Y. (2012) CpG methylation patterns and decitabine treatment response in acute myeloid leukemia cells and normal hematopoietic precursors. Leukemia 26, 244-254
29. Ng, K. P., Ebrahem, Q., Negrotto, S., Mahfouz, R. Z., Link, K. A., Hu, Z., Gu, X., Advani, A., Kalaycio, M., Sobecks, R., Sekeres, M., Copelan, E., Radivoyevitch, T., Maciejewski, J., Mulloy, J. C., and Saunthararajah, Y. (2011) p53 independent epigenetic-differentiation treatment in xenotransplant models of acute myeloid leukemia. Leukemia 25, 1739-1750
30. Hu, Z., Negrotto, S., Gu, X., Mahfouz, R., Ng, K. P., Ebrahem, Q., Copelan, E., Singh, H., Maciejewski, J. P., and Saunthararajah, Y. (2010) Decitabine maintains hematopoietic precursor self-renewal by preventing repression of stem cell genes by a differentiation-inducing stimulus. Mol. Cancer Ther. 9, 1536-1543
31. Rush, M., Appanah, R., Lee, S., Lam, L. L., Goyal, P., and Lorincz, M. C. (2009) Targeting of EZH2 to a defined genomic site is sufficient for recruitment of Dnmt3a but not de novo DNA methylation. Epigenetics 4, 404-414
32. Viré, E., Brenner, C., Deplus, R., Blanchon, L., Fraga, M., Didelot, C., Morey, L., Van Eynde, A., Bernard, D., Vanderwinden, J. M., Bollen, M., Esteller, M., Di Croce, L., de Launoit, Y., and Fuks, F. (2006) The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439, 871-874 (Pubitemid 43255707)
33. Ptasinska, A., Assi, S. A., Mannari, D., James, S. R., Williamson, D., Dunne, J., Hoogenkamp, M., Wu, M., Care, M., McNeill, H., Cauchy, P., Cullen, M., Tooze, R. M., Tenen, D. G., Young, B. D., Cockerill, P. N., Westhead, D. R., Heidenreich, O., and Bonifer, C. (2012) Depletion of RUNX1/ETO in t(8;21)AMLcells leads to genome-wide changes in chromatin structure and transcription factor binding. Leukemia 26, 1829-1841
34. Bröske, A. M., Vockentanz, L., Kharazi, S., Huska, M. R., Mancini, E., Scheller, M., Kuhl, C., Enns, A., Prinz, M., Jaenisch, R., Nerlov, C., Leutz, A., Andrade-Navarro, M. A., Jacobsen, S. E., and Rosenbauer, F. (2009) DNA methylation protects hematopoietic stem cell multipotency from myeloerythroid restriction. Nat. Genet. 41, 1207-1215
35. Trowbridge, J. J., Sinha, A. U., Zhu, N., Li, M., Armstrong, S. A., and Orkin, S. H. (2012) Haploinsufficiency of Dnmt1 impairs leukemia stem cell function through derepression of bivalent chromatin domains. Genes Dev. 26, 344-349
36. Schenk, T., Chen, W. C., Göllner, S., Howell, L., Jin, L., Hebestreit, K., Klein, H. U., Popescu, A. C., Burnett, A., Mills, K., Casero, R. A., Jr., Marton, L., Woster, P., Minden, M. D., Dugas, M., Wang, J. C., Dick, J. E., Müller-Tidow, C., Petrie, K., and Zelent, A. (2012) Inhibition of the LSD1 (KDM1A) demethylase reactivates the all-trans-retinoic acid differentiation pathway in acute myeloid leukemia. Nat. Med. 18, 605-611
37. Harris, W. J., Huang, X., Lynch, J. T., Spencer, G. J., Hitchin, J. R., Li, Y., Ciceri, F., Blaser, J. G., Greystoke, B. F., Jordan, A. M., Miller, C. J., Ogilvie, D. J., and Somervaille, T. C. (2012) The histone demethylase KDM1A sustains the oncogenic potential of MLL-AF9 leukemia stem cells. Cancer Cell 21, 473-487
38. Warrell, R. P., Jr., He, L. Z., Richon, V., Calleja, E., and Pandolfi, P. P. (1998) Therapeutic targeting of transcription in acute promyelocytic leukemia by use of an inhibitor of histone deacetylase. J. Natl. Cancer Inst. 90, 1621-1625 (Pubitemid 28523436)
39. Kosugi, H., Towatari, M., Hatano, S., Kitamura, K., Kiyoi, H., Kinoshita, T., Tanimoto, M., Murate, T., Kawashima, K., Saito, H., and Naoe, T. (1999) Histone deacetylase inhibitors are the potent inducer/enhancer of differentiation in acute myeloid leukemia: a new approach to anti-leukemia therapy. Leukemia 13, 1316-1324 (Pubitemid 29429756)
40. Wang, J., Saunthararajah, Y., Redner, R. L., and Liu, J. M. (1999) Inhibitors of histone deacetylase relieve ETO-mediated repression and induce differentiation of AML1-ETO leukemia cells. Cancer Res. 59, 2766-2769 (Pubitemid 29283104)
41. Nowak, D., Stewart, D., and Koeffler, H. P. (2009) Differentiation therapy of leukemia: 3 decades of development. Blood 113, 3655-3665
42. Stopka, T., Zakova, D., Fuchs, O., Kubrova, O., Blafkova, J., Jelinek, J., Necas, E., and Zivny, J. (2000) Chromatin remodeling gene SMARCA5 is dysregulated in primitive hematopoietic cells of acute leukemia. Leukemia 14, 1247-1252 (Pubitemid 30445032)
43. Saunthararajah, Y. (2013) Key clinical observations after 5-azacytidine and decitabine treatment of myelodysplastic syndromes suggest practical solutions for better outcomes. Hematology Am. Soc. Hematol. Educ. Program 2013, 511-521
44. Grand, F., Kulkarni, S., Chase, A., Goldman, J. M., Gordon, M., and Cross, N. C. (1999) Frequent deletion of hSNF5/INI1, a component of the SWI/ SNF complex, in chronic myeloid leukemia. Cancer Res. 59, 3870-3874 (Pubitemid 29393542)
45. Saunthararajah, Y., and Maciejewski, J. (2012) Polycomb segment myeloid malignancies. Blood 119, 1097-1098
46. Goodliffe, J. M., Wieschaus, E., and Cole, M. D. (2005) Polycomb mediates Myc autorepression and its transcriptional control of many loci in Drosophila. Genes Dev. 19, 2941-2946 (Pubitemid 41798110)
47. R Core Team (2012) R: A language and environment for statistical computing. ISBN 3-900051-07-0, R Foundation for Statistical Computing, Vienna, Austria