HDAC8 Inhibition Specifically Targets Inv(16) Acute Myeloid Leukemic Stem Cells by Restoring p53 Acetylation

Cell Stem Cell

Volumn 17, Issue 5, 2015, Pages 597-610

  Qi, Jing ^a   Singh, Sandeep ^a   Hua, Wei Kai ^a   Cai, Qi ^a   Chao, Shi Wei ^c   Li, Ling ^a   Liu, Hongjun ^a   Ho, Yinwei ^a   McDonald, Tinisha ^a   Lin, Allen ^a   Marcucci, Guido ^a   Bhatia, Ravi ^a   Huang, Wei Jan ^c   Chang, Chung I ^b   Kuo, Ya Huei ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; ENTINOSTAT; HISTONE DEACETYLASE 8; HISTONE DEACETYLASE 8 INHIBITOR; HISTONE DEACETYLASE INHIBITOR; HYBRID PROTEIN; NUTLIN 3; PROTEIN P53; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; HDAC8 PROTEIN, HUMAN; HISTONE DEACETYLASE; REPRESSOR PROTEIN;

ACUTE MYELOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER STEM CELL; CELL SURVIVAL; CONTROLLED STUDY; DEACETYLATION; DRUG EFFICACY; ENZYME INHIBITION; GENE MUTATION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IC50; INV(16) ACUTE MYELOBLASTIC LEUKEMIA STEM CELL; K562 CELL LINE; LEUKEMIA CELL; LOXP SITE; MOUSE; NONHUMAN; PERIPHERAL BLOOD STEM CELL; PRIORITY JOURNAL; PROTEIN ACETYLATION; T CELL DEPLETION; TARGET CELL; ACETYLATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; CHROMOSOME 16; DRUG EFFECTS; GENETICS; INBRED MOUSE STRAIN; K-562 CELL LINE; LEUKEMIA, MYELOID, ACUTE; METABOLISM; PATHOLOGY;

ACETYLATION; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CHROMOSOMES, HUMAN, PAIR 16; HEMATOPOIETIC STEM CELLS; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; K562 CELLS; LEUKEMIA, MYELOID, ACUTE; MICE; MICE, INBRED STRAINS; NEOPLASTIC STEM CELLS; REPRESSOR PROTEINS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84947865743     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2015.08.004     Document Type: Article

References (46)

1. N. Adya, T. Stacy, N.A. Speck, and P.P. Liu The leukemic protein core binding factor beta (CBFbeta)-smooth-muscle myosin heavy chain sequesters CBFalpha2 into cytoskeletal filaments and aggregates Mol. Cell. Biol. 18 1998 7432 7443
2. J.M. Amann, J. Nip, D.K. Strom, B. Lutterbach, H. Harada, N. Lenny, J.R. Downing, S. Meyers, and S.W. Hiebert ETO, a target of t(8;21) in acute leukemia, makes distinct contacts with multiple histone deacetylases and binds mSin3A through its oligomerization domain Mol. Cell. Biol. 21 2001 6470 6483
3. S. Balasubramanian, J. Ramos, W. Luo, M. Sirisawad, E. Verner, and J.J. Buggy A novel histone deacetylase 8 (HDAC8)-specific inhibitor PCI-34051 induces apoptosis in T-cell lymphomas Leukemia 22 2008 1026 1034
4. O. Ben-Ami, D. Friedman, D. Leshkowitz, D. Goldenberg, K. Orlovsky, N. Pencovich, J. Lotem, A. Tanay, and Y. Groner Addiction of t(8;21) and inv(16) acute myeloid leukemia to native RUNX1 Cell Rep. 4 2013 1131 1143
5. M. Bots, I. Verbrugge, B.P. Martin, J.M. Salmon, M. Ghisi, A. Baker, K. Stanley, J. Shortt, G.J. Ossenkoppele, J. Zuber, and et al. Differentiation therapy for the treatment of t(8;21) acute myeloid leukemia using histone deacetylase inhibitors Blood 123 2014 1341 1352
6. L.H. Castilla, C. Wijmenga, Q. Wang, T. Stacy, N.A. Speck, M. Eckhaus, M. Marín-Padilla, F.S. Collins, A. Wynshaw-Boris, and P.P. Liu Failure of embryonic hematopoiesis and lethal hemorrhages in mouse embryos heterozygous for a knocked-in leukemia gene CBFB-MYH11 Cell 87 1996 687 696
7. M.A. Christophorou, D. Martin-Zanca, L. Soucek, E.R. Lawlor, L. Brown-Swigart, E.W. Verschuren, and G.I. Evan Temporal dissection of p53 function in vitro and in vivo Nat. Genet. 37 2005 718 726
8. C. Dai, and W. Gu p53 post-translational modification: deregulated in tumorigenesis Trends Mol. Med. 16 2010 528 536
9. M.-S. Dai, S.X. Zeng, Y. Jin, X.-X. Sun, L. David, and H. Lu Ribosomal protein L23 activates p53 by inhibiting MDM2 function in response to ribosomal perturbation but not to translation inhibition Mol. Cell. Biol. 24 2004 7654 7668
10. M.A. Deardorff, M. Bando, R. Nakato, E. Watrin, T. Itoh, M. Minamino, K. Saitoh, M. Komata, Y. Katou, D. Clark, and et al. HDAC8 mutations in Cornelia de Lange syndrome affect the cohesin acetylation cycle Nature 489 2012 313 317
11. K.L. Durst, B. Lutterbach, T. Kummalue, A.D. Friedman, and S.W. Hiebert The inv(16) fusion protein associates with corepressors via a smooth muscle myosin heavy-chain domain Mol. Cell. Biol. 23 2003 607 619
12. Y. Fu, P. Zhang, J. Ge, J. Cheng, W. Dong, H. Yuan, Y. Du, M. Yang, R. Sun, and H. Jiang Histone deacetylase 8 suppresses osteogenic differentiation of bone marrow stromal cells by inhibiting histone H3K9 acetylation and RUNX2 activity Int. J. Biochem. Cell Biol. 54 2014 68 77
13. S. Goyama, J. Schibler, L. Cunningham, Y. Zhang, Y. Rao, N. Nishimoto, M. Nakagawa, A. Olsson, M. Wunderlich, K.A. Link, and et al. Transcription factor RUNX1 promotes survival of acute myeloid leukemia cells J. Clin. Invest. 123 2013 3876 3888
14. C. Haferlach, F. Dicker, H. Herholz, S. Schnittger, W. Kern, and T. Haferlach Mutations of the TP53 gene in acute myeloid leukemia are strongly associated with a complex aberrant karyotype Leukemia 22 2008 1539 1541
15. W.-J. Huang, Y.-C. Wang, S.-W. Chao, C.-Y. Yang, L.-C. Chen, M.-H. Lin, W.-C. Hou, M.-Y. Chen, T.-L. Lee, P. Yang, and C.I. Chang Synthesis and biological evaluation of ortho-aryl N-hydroxycinnamides as potent histone deacetylase (HDAC) 8 isoform-selective inhibitors ChemMedChem 7 2012 1815 1824
16. R.K. Hyde, L. Zhao, L. Alemu, and P.P. Liu Runx1 is required for hematopoietic defects and leukemogenesis in Cbfb-MYH11 knock-in mice Leukemia 29 2015 1771 1778
17. A. Ito, Y. Kawaguchi, C.-H. Lai, J.J. Kovacs, Y. Higashimoto, E. Appella, and T.-P. Yao MDM2-HDAC1-mediated deacetylation of p53 is required for its degradation EMBO J. 21 2002 6236 6245
18. L.J. Juan, W.J. Shia, M.H. Chen, W.M. Yang, E. Seto, Y.S. Lin, and C.W. Wu Histone deacetylases specifically down-regulate p53-dependent gene activation J. Biol. Chem. 275 2000 20436 20443
19. Y. Kamikubo, L. Zhao, M. Wunderlich, T. Corpora, R.K. Hyde, T.A. Paul, M. Kundu, L. Garrett, S. Compton, G. Huang, and et al. Accelerated leukemogenesis by truncated CBF β-SMMHC defective in high-affinity binding with RUNX1 Cancer Cell 17 2010 455 468
20. Y. Kamikubo, R.K. Hyde, L. Zhao, L. Alemu, C. Rivas, L.J. Garrett, and P.P. Liu The C-terminus of CBFβ-SMMHC is required to induce embryonic hematopoietic defects and leukemogenesis Blood 121 2012 638 642
21. Y. Kanno, T. Kanno, C. Sakakura, S.C. Bae, and Y. Ito Cytoplasmic sequestration of the polyomavirus enhancer binding protein 2 (PEBP2)/core binding factor alpha (CBFalpha) subunit by the leukemia-related PEBP2/CBFbeta-SMMHC fusion protein inhibits PEBP2/CBF-mediated transactivation Mol. Cell. Biol. 18 1998 4252 4261
22. N. Khan, M. Jeffers, S. Kumar, C. Hackett, F. Boldog, N. Khramtsov, X. Qian, E. Mills, S.C. Berghs, N. Carey, and et al. Determination of the class and isoform selectivity of small-molecule histone deacetylase inhibitors Biochem. J. 409 2008 581 589
23. K. Kojima, M. Konopleva, I.J. Samudio, M. Shikami, M. Cabreira-Hansen, T. McQueen, V. Ruvolo, T. Tsao, Z. Zeng, L.T. Vassilev, and M. Andreeff MDM2 antagonists induce p53-dependent apoptosis in AML: implications for leukemia therapy Blood 106 2005 3150 3159
24. R. Kühn, F. Schwenk, M. Aguet, and K. Rajewsky Inducible gene targeting in mice Science 269 1995 1427 1429
25. Y.-H. Kuo, S.F. Landrette, S.A. Heilman, P.N. Perrat, L. Garrett, P.P. Liu, M.M. Le Beau, S.C. Kogan, and L.H. Castilla Cbf beta-SMMHC induces distinct abnormal myeloid progenitors able to develop acute myeloid leukemia Cancer Cell 9 2006 57 68
26. Y.-H. Kuo, R.M. Gerstein, and L.H. Castilla Cbfbeta-SMMHC impairs differentiation of common lymphoid progenitors and reveals an essential role for RUNX in early B-cell development Blood 111 2008 1543 1551
27. Y.-H. Kuo, S.K. Zaidi, S. Gornostaeva, T. Komori, G.S. Stein, and L.H. Castilla Runx2 induces acute myeloid leukemia in cooperation with Cbfbeta-SMMHC in mice Blood 113 2009 3323 3332
28. P. Liu, S.A. Tarlé, A. Hajra, D.F. Claxton, P. Marlton, M. Freedman, M.J. Siciliano, and F.S. Collins Fusion between transcription factor CBF β/PEBP2 β and a myosin heavy chain in acute myeloid leukemia Science 261 1993 1041 1044
29. P.P. Liu, C. Wijmenga, A. Hajra, T.B. Blake, C.A. Kelley, R.S. Adelstein, A. Bagg, J. Rector, J. Cotelingam, C.L. Willman, and F.S. Collins Identification of the chimeric protein product of the CBFB-MYH11 fusion gene in inv(16) leukemia cells Genes Chromosomes Cancer 16 1996 77 87
30. J. Long, B. Parkin, P. Ouillette, D. Bixby, K. Shedden, H. Erba, S. Wang, and S.N. Malek Multiple distinct molecular mechanisms influence sensitivity and resistance to MDM2 inhibitors in adult acute myelogenous leukemia Blood 116 2010 71 80
31. A.T. Look Oncogenic transcription factors in the human acute leukemias Science 278 1997 1059 1064
32. S.M. Lukasik, L. Zhang, T. Corpora, S. Tomanicek, Y. Li, M. Kundu, K. Hartman, P.P. Liu, T.M. Laue, R.L. Biltonen, and et al. Altered affinity of CBF β-SMMHC for Runx1 explains its role in leukemogenesis Nat. Struct. Biol. 9 2002 674 679
33. J. Luo, F. Su, D. Chen, A. Shiloh, and W. Gu Deacetylation of p53 modulates its effect on cell growth and apoptosis Nature 408 2000 377 381
34. B. Lutterbach, Y. Hou, K.L. Durst, and S.W. Hiebert The inv(16) encodes an acute myeloid leukemia 1 transcriptional corepressor Proc. Natl. Acad. Sci. USA 96 1999 12822 12827
35. D.A. Moreno, C.A. Scrideli, M.A.A. Cortez, R. de Paula Queiroz, E.T. Valera, V. da Silva Silveira, J.A. Yunes, S.R. Brandalise, and L.G. Tone Differential expression of HDAC3, HDAC7 and HDAC9 is associated with prognosis and survival in childhood acute lymphoblastic leukaemia Br. J. Haematol. 150 2010 665 673
36. O.M. Odenike, S. Alkan, D. Sher, J.E. Godwin, D. Huo, S.J. Brandt, M. Green, J. Xie, Y. Zhang, D.H. Vesole, and et al. Histone deacetylase inhibitor romidepsin has differential activity in core binding factor acute myeloid leukemia Clin. Cancer Res. 14 2008 7095 7101
37. I. Oehme, H.E. Deubzer, D. Wegener, D. Pickert, J.-P. Linke, B. Hero, A. Kopp-Schneider, F. Westermann, S.M. Ulrich, A. von Deimling, and et al. Histone deacetylase 8 in neuroblastoma tumorigenesis Clin. Cancer Res. 15 2009 91 99
38. T. Okuda, J. van Deursen, S.W. Hiebert, G. Grosveld, and J.R. Downing AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis Cell 84 1996 321 330
39. T. Prébet, N. Boissel, S. Reutenauer, X. Thomas, J. Delaunay, J.Y. Cahn, A. Pigneux, B. Quesnel, F. Witz, S. Thépot, et al. Acute Leukemia French Association Groupe Ouest-Est des leucémies et autres maladies du sang (GOELAMS) Core Binding Factor Acute Myeloid Leukemia (CBF AML) intergroup Acute myeloid leukemia with translocation (8;21) or inversion (16) in elderly patients treated with conventional chemotherapy: a collaborative study of the French CBF-AML intergroup J. Clin. Oncol. 27 2009 4747 4753
40. F.G. Rücker, R.F. Schlenk, L. Bullinger, S. Kayser, V. Teleanu, H. Kett, M. Habdank, C.-M. Kugler, K. Holzmann, V.I. Gaidzik, and et al. TP53 alterations in acute myeloid leukemia with complex karyotype correlate with specific copy number alterations, monosomal karyotype, and dismal outcome Blood 119 2012 2114 2121
41. N.A. Speck, and D.G. Gilliland Core-binding factors in haematopoiesis and leukaemia Nat. Rev. Cancer 2 2002 502 513
42. C. Ustun, and G. Marcucci Emerging diagnostic and therapeutic approaches in core binding factor acute myeloid leukaemia Curr. Opin. Hematol. 22 2015 85 91
43. Q. Wang, T. Stacy, J.D. Miller, A.F. Lewis, T.L. Gu, X. Huang, J.H. Bushweller, J.C. Bories, F.W. Alt, G. Ryan, and et al. The CBFbeta subunit is essential for CBFalpha2 (AML1) function in vivo Cell 87 1996 697 708
44. G. Yang, M.A. Thompson, S.J. Brandt, and S.W. Hiebert Histone deacetylase inhibitors induce the degradation of the t(8;21) fusion oncoprotein Oncogene 26 2007 91 101
45. L. Zhao, J.L. Cannons, S. Anderson, M. Kirby, L. Xu, L.H. Castilla, P.L. Schwartzberg, R. Bosselut, and P.P. Liu CBFB-MYH11 hinders early T-cell development and induces massive cell death in the thymus Blood 109 2007 3432 3440
46. Z. Zhao, J. Zuber, E. Diaz-Flores, L. Lintault, S.C. Kogan, K. Shannon, and S.W. Lowe p53 loss promotes acute myeloid leukemia by enabling aberrant self-renewal Genes Dev. 24 2010 1389 1402