BET and HDAC inhibitors induce similar genes and biological effects and synergize to kill in Myc-induced murine lymphoma

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 26, 2014, Pages

  Bhadury, Joydeep ^a   Nilsson, Lisa M ^a   Muralidharan, Somsundar Veppil ^a   Green, Lydia C ^a   Li, Zhoulei ^b   Gesner, Emily M ^c   Hansen, Henrik C ^c   Keller, Ulrich B ^b   McLure, Kevin G ^c   Nilsson, Jonas A ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c Zenith Epigenetics Corp   (Canada)

Author keywords

Brd2; Brd4; JQ1; Mouse models; Vorinostat

Indexed keywords

ANTINEOPLASTIC AGENT; HISTONE DEACETYLASE INHIBITOR; MYC PROTEIN; RVX 2135; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; B CELL LYMPHOMA; CANCER INHIBITION; CANCER SURVIVAL; CELL CYCLE ARREST; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; GENE REPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOMA CELL; MOUSE; NONHUMAN; OVERALL SURVIVAL; PHENOTYPE; PRIORITY JOURNAL; TRANSGENIC MOUSE;

BRD2; BRD4; JQ1; MOUSE MODELS; VORINOSTAT;

ANIMALS; APOPTOSIS; DRUG SYNERGISM; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONE DEACETYLASE INHIBITORS; LYMPHOMA; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; QUINAZOLINONES; RECEPTORS, CELL SURFACE; TRANSCRIPTION FACTORS;

EID: 84903712622     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1406722111     Document Type: Article

References (52)

1. Belkina AC, Denis GV (2012) BET domain co-regulators in obesity, inflammation and cancer. Nat Rev Cancer 12(7):465-477.
2. Delmore JE, et al. (2011) BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell 146(6):904-917.
3. Filippakopoulos P, et al. (2010) Selective inhibition of BET bromodomains. Nature 468(7327):1067-1073.
4. Herrmann H, et al. (2012) Small-molecule inhibition of BRD4 as a new potent approach to eliminate leukemic stem-and progenitor cells in acute myeloid leukemia AML. Oncotarget 3(12):1588-1599.
5. Zuber J, et al. (2011) RNAi screen identifies Brd4 as a therapeutic target in acute myeloid leukaemia. Nature 478(7370):524-528.
6. Zhao X, et al. (2013) Disruption of the MYC-miRNA-EZH2 loop to suppress aggressive B-cell lymphoma survival and clonogenicity. Leukemia 27(12):2341-2350.
7. Tolani B, Gopalakrishnan R, Punj V, Matta H, Chaudhary PM (June 24, 2013) Targeting Myc in KSHV-associated primary effusion lymphoma with BET bromodomain inhibitors. Oncogene, 10.1038/onc.2013.242.
8. Gao L, et al. (2013) Androgen receptor promotes ligand-independent prostate cancer progression through c-Myc upregulation. PLoS ONE 8(5):e63563.
9. Cheng Z, et al. (2013) Inhibition of BET bromodomain targets genetically diverse glioblastoma. Clin Cancer Res 19(7):1748-1759.
10. Ott CJ, et al. (2012) BET bromodomain inhibition targets both c-Myc and IL7R in highrisk acute lymphoblastic leukemia. Blood 120(14):2843-2852.
11. Lockwood WW, Zejnullahu K, Bradner JE, Varmus H (2012) Sensitivity of human lung adenocarcinoma cell lines to targeted inhibition of BET epigenetic signaling proteins. Proc Natl Acad Sci USA 109(47):19408-19413.
12. Basu A, et al. (2013) An interactive resource to identify cancer genetic and lineage dependencies targeted by small molecules. Cell 154(5):1151-1161.
13. McLure KG, et al. (2013) RVX-208, an inducer of ApoA-I in humans, is a BET bromodomain antagonist. PLoS ONE 8(12):e83190.
14. Nicholls SJ, et al. (2011) Efficacy and safety of a novel oral inducer of apolipoprotein A-I synthesis in statin-treated patients with stable coronary artery disease: A randomized controlled trial. J Am Coll Cardiol 57(9):1111-1119.
15. Picaud S, et al. (2013) RVX-208, an inhibitor of BET transcriptional regulators with selectivity for the second bromodomain. Proc Natl Acad Sci USA 110(49):19754-19759.
16. Adams JM, et al. (1985) The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318(6046):533-538.
17. Kovalchuk AL, et al. (2000) Burkitt lymphoma in the mouse. J Exp Med 192(8): 1183-1190.
18. Segura MF, et al. (2013) BRD4 sustains proliferation and represents a new target for epigenetic therapy in melanoma. Cancer Res 73(20):6264-6276.
19. Da Costa D, et al. (2013) BET inhibition as a single or combined therapeutic approach in primary paediatric B-precursor acute lymphoblastic leukaemia. Blood Cancer J 3:e126.
20. Mertz JA, et al. (2011) Targeting MYC dependence in cancer by inhibiting BET bromodomains. Proc Natl Acad Sci USA 108(40):16669-16674.
21. Sears R, et al. (2000) Multiple Ras-dependent phosphorylation pathways regulate Myc protein stability. Genes Dev 14(19):2501-2514.
22. Krones-Herzig A, et al. (2005) Early growth response 1 acts as a tumor suppressor in vivo and in vitro via regulation of p53. Cancer Res 65(12):5133-5143.
23. Zhan Q, Chen IT, Antinore MJ, Fornace AJ, Jr. (1998) Tumor suppressor p53 can participate in transcriptional induction of the GADD45 promoter in the absence of direct DNA binding. Mol Cell Biol 18(5):2768-2778.
24. Zhang Q, et al. (2013) Domain-specific c-Myc ubiquitylation controls c-Myc transcriptional and apoptotic activity. Proc Natl Acad Sci USA 110(3):978-983.
25. Boone DN, Qi Y, Li Z, Hann SR (2011) Egr1 mediates p53-independent c-Myc-induced apoptosis via a noncanonical ARF-dependent transcriptional mechanism. Proc Natl Acad Sci USA 108(2):632-637.
26. Heller G, et al. (2008) Genome-wide transcriptional response to 5-aza-2'-deoxycytidine and trichostatin A in multiple myeloma cells. Cancer Res 68(1):44-54.
27. Bhaskara S, et al. (2008) Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control. Mol Cell 30(1):61-72.
28. Floyd SR, et al. (2013) The bromodomain protein Brd4 insulates chromatin from DNA damage signalling. Nature 498(7453):246-250.
29. Banerjee C, et al. (2012) BET bromodomain inhibition as a novel strategy for reactivation of HIV-1. J Leukoc Biol 92(6):1147-1154.
30. Bartholomeeusen K, Xiang Y, Fujinaga K, Peterlin BM (2012) Bromodomain and extraterminal (BET) bromodomain inhibition activate transcription via transient release of positive transcription elongation factor b (P-TEFb) from 7SK small nuclear ribonucleoprotein. J Biol Chem 287(43):36609-36616.
31. Boehm D, et al. (2013) BET bromodomain-targeting compounds reactivate HIV from latency via a Tat-independent mechanism. Cell Cycle 12(3):452-462.
32. Li Z, Guo J, Wu Y, Zhou Q (2013) The BET bromodomain inhibitor JQ1 activates HIV latency through antagonizing Brd4 inhibition of Tat-transactivation. Nucleic Acids Res 41(1):277-287.
33. Zhu J, et al. (2012) Reactivation of latent HIV-1 by inhibition of BRD4. Cell Reports 2(4):807-816.
34. Marshall NF, Peng J, Xie Z, Price DH (1996) Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase. J Biol Chem271(43):27176-27183.
35. Jang MK, et al. (2005) The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase II-dependent transcription. Mol Cell 19(4):523-534.
36. Yang Z, et al. (2005) Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Mol Cell 19(4):535-545.
37. Lovén J, et al. (2013) Selective inhibition of tumor oncogenes by disruption of superenhancers. Cell 153(2):320-334.
38. Ellis L, et al. (2009) The histone deacetylase inhibitors LAQ824 and LBH589 do not require death receptor signaling or a functional apoptosome to mediate tumor cell death or therapeutic efficacy. Blood 114(2):380-393.
39. Lindemann RK, et al. (2007) Analysis of the apoptotic and therapeutic activities of histone deacetylase inhibitors by using a mouse model of B cell lymphoma. Proc Natl Acad Sci USA 104(19):8071-8076.
40. Hargreaves DC, Horng T, Medzhitov R (2009) Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 138(1):129-145.
41. Zippo A, et al. (2009) Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138(6):1122-1136.
42. Rice AP (2013) P-TEFb as a target to reactivate latent HIV: Two Brds are now in hand. Cell Cycle 12(3):392-393.
43. Donner AJ, Ebmeier CC, Taatjes DJ, Espinosa JM (2010) CDK8 is a positive regulator of transcriptional elongation within the serum response network. Nat Struct Mol Biol 17(2):194-201.
44. Picaud S, et al. (2013) PFI-1, a highly selective protein interaction inhibitor, targeting BET bromodomains. Cancer Res 73(11):3336-3346.
45. Dawson MA, et al. (2011) Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia. Nature 478(7370):529-533.
46. Belkina AC, Nikolajczyk BS, Denis GV (2013) BET protein function is required for inflammation: Brd2 genetic disruption and BET inhibitor JQ1 impair mouse macrophage inflammatory responses. J Immunol 190(7):3670-3678.
47. Proserpio V, Fittipaldi R, Ryall JG, Sartorelli V, Caretti G (2013) The methyltransferase SMYD3 mediates the recruitment of transcriptional cofactors at the myostatin and c-Met genes and regulates skeletal muscle atrophy. Genes Dev 27(11):1299-1312.
48. Bhadury J, López MD, Muralidharan SV, Nilsson LM, Nilsson JA (2013) Identification of tumorigenic and therapeutically actionable mutations in transplantable mouse tumor cells by exome sequencing. Oncogenesis 2:e44.
49. Höglund A, Nilsson LM, Forshell LP, Maclean KH, Nilsson JA (2009) Myc sensitizes p53-deficient cancer cells to the DNA-damaging effects of the DNA methyltransferase inhibitor decitabine. Blood 113(18):4281-4288.
50. Schmitt CA, McCurrach ME, de Stanchina E, Wallace-Brodeur RR, Lowe SW (1999) INK4a/ARF mutations accelerate lymphomagenesis and promote chemoresistance by disabling p53. Genes Dev 13(20):2670-2677.
51. Nilsson LM, et al. (2012) Mouse genetics suggests cell-context dependency for Mycregulated metabolic enzymes during tumorigenesis. PLoS Genet 8(3):e1002573.
52. Eischen CM, Weber JD, Roussel MF, Sherr CJ, Cleveland JL (1999) Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis. Genes Dev 13(20):2658-2669.