Home LiteratureArticle Details
PMID: 23129625 Published · ppublish English Journal Article Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't

Sensitivity of human lung adenocarcinoma cell lines to targeted inhibition of BET epigenetic signaling proteins.

Lockwood WW, Zejnullahu K, Bradner JE, Varmus H

Abstract

Bromodomain and extra terminal domain (BET) proteins function as epigenetic signaling factors that associate with acetylated histones and facilitate transcription of target genes. Inhibitors targeting the activity of BET proteins have shown potent antiproliferative effects in hematological cancers through the suppression of c-MYC and downstream target genes. However, as the epigenetic landscape of a cell varies drastically depending on lineage, transcriptional coactivators such as BETs would be expected to have different targets in cancers derived from different cells of origin, and this may influence the activity and mechanism of action of BET inhibitors. To test this hypothesis, we treated a panel of lung adenocarcinoma (LAC) cell lines with the BET inhibitor JQ1 and found that a subset is acutely susceptible to BET inhibition. In contrast to blood tumors, we show that LAC cells are inhibited by JQ1 through a mechanism independent of c-MYC down-regulation. Through gene expression profiling, we discovered that the oncogenic transcription factor FOSL1 and its targets are suppressed by JQ1 in a dose-dependant manner. Knockdown of BRD4 also decreased FOSL1 levels, and inhibition of FOSL1 phenocopied the effects of JQ1 treatment, suggesting that loss of this transcription factor may be partly responsible for the cytotoxic effects of BET inhibition in LAC cells, although ectopic expression of FOSL1 alone did not rescue the phenotype. Together, these findings suggest that BET inhibitors may be useful in solid tumors and that cell-lineage-specific differences in transcriptional targets of BETs may influence the activity of inhibitors of these proteins in different cancer types.

MeSH Terms
Adenocarcinoma/drug therapy,genetics,pathology Adenocarcinoma of Lung Azepines/pharmacology,therapeutic use Cell Cycle Proteins Cell Line, Tumor Cell Proliferation/drug effects Down-Regulation/drug effects,genetics Drug Screening Assays, Antitumor Epigenesis, Genetic/drug effects Gene Expression Regulation, Neoplastic/drug effects Gene Knockdown Techniques Humans Lung Neoplasms/drug therapy,genetics,pathology Molecular Targeted Therapy Nuclear Proteins/antagonists & inhibitors,metabolism Proto-Oncogene Proteins c-fos/genetics,metabolism Proto-Oncogene Proteins c-myc/genetics,metabolism Signal Transduction/drug effects,genetics Transcription Factors/metabolism Triazoles/pharmacology,therapeutic use
Chemicals
(+)-JQ1 compound Azepines BRD4 protein, human Cell Cycle Proteins Nuclear Proteins Proto-Oncogene Proteins c-fos Proto-Oncogene Proteins c-myc Transcription Factors Triazoles fos-related antigen 1
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Lockwood William W
Cancer Biology and Genetics Section, Cancer Genetics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD 20892, USA. william.lockwood@nih.gov
Zejnullahu Kreshnik
Bradner James E
Varmus Harold
References (24)
24 references, click to expand
  1. BET bromodomain inhibition as a therapeutic strategy to target c-Myc.
    Cell. 2011 Sep 16;146(6):904-17 PMID: 21889194
  2. Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia.
    Nature. 2011 Oct 02;478(7370):529-33 PMID: 21964340
  3. Increased bone formation and osteosclerosis in mice overexpressing the transcription factor Fra-1.
    Nat Med. 2000 Sep;6(9):980-4 PMID: 10973316
  4. Targeting MYC dependence in cancer by inhibiting BET bromodomains.
    Proc Natl Acad Sci U S A. 2011 Oct 4;108(40):16669-74 PMID: 21949397
  5. Suppression of inflammation by a synthetic histone mimic.
    Nature. 2010 Dec 23;468(7327):1119-23 PMID: 21068722
  6. Brd4 marks select genes on mitotic chromatin and directs postmitotic transcription.
    Mol Biol Cell. 2009 Dec;20(23):4899-909 PMID: 19812244
  7. The double bromodomain-containing chromatin adaptor Brd4 and transcriptional regulation.
    J Biol Chem. 2007 May 4;282(18):13141-5 PMID: 17329240
  8. Gene bookmarking accelerates the kinetics of post-mitotic transcriptional re-activation.
    Nat Cell Biol. 2011 Oct 09;13(11):1295-304 PMID: 21983563
  9. Histone recognition and large-scale structural analysis of the human bromodomain family.
    Cell. 2012 Mar 30;149(1):214-31 PMID: 22464331
  10. FRA-1 proto-oncogene induces lung epithelial cell invasion and anchorage-independent growth in vitro, but is insufficient to promote tumor growth in vivo.
    Cancer Res. 2007 Jul 1;67(13):6204-11 PMID: 17616677
  11. Brd4 recruits P-TEFb to chromosomes at late mitosis to promote G1 gene expression and cell cycle progression.
    Mol Cell Biol. 2008 Feb;28(3):967-76 PMID: 18039861
  12. Epigenetic protein families: a new frontier for drug discovery.
    Nat Rev Drug Discov. 2012 Apr 13;11(5):384-400 PMID: 22498752
  13. Chromatin modifications and their function.
    Cell. 2007 Feb 23;128(4):693-705 PMID: 17320507
  14. The Fos family of transcription factors and their role in tumourigenesis.
    Eur J Cancer. 2005 Nov;41(16):2449-61 PMID: 16199154
  15. RNAi screen identifies Brd4 as a therapeutic target in acute myeloid leukaemia.
    Nature. 2011 Aug 03;478(7370):524-8 PMID: 21814200
  16. PIM1-dependent phosphorylation of histone H3 at serine 10 is required for MYC-dependent transcriptional activation and oncogenic transformation.
    Nat Cell Biol. 2007 Aug;9(8):932-44 PMID: 17643117
  17. Deciphering AP-1 function in tumorigenesis: fra-ternizing on target promoters.
    Cell Cycle. 2007 Nov 1;6(21):2633-9 PMID: 17957143
  18. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles.
    Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15545-50 PMID: 16199517
  19. Selective inhibition of BET bromodomains.
    Nature. 2010 Dec 23;468(7327):1067-73 PMID: 20871596
  20. AP-1: a double-edged sword in tumorigenesis.
    Nat Rev Cancer. 2003 Nov;3(11):859-68 PMID: 14668816
  21. The double bromodomain proteins Brd2 and Brd3 couple histone acetylation to transcription.
    Mol Cell. 2008 Apr 11;30(1):51-60 PMID: 18406326
  22. Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation.
    Cell. 2009 Sep 18;138(6):1122-36 PMID: 19766566
  23. Role and regulation of activator protein-1 in toxicant-induced responses of the lung.
    Am J Physiol Lung Cell Mol Physiol. 2002 Dec;283(6):L1161-78 PMID: 12424143
  24. BET bromodomain inhibition targets both c-Myc and IL7R in high-risk acute lymphoblastic leukemia.
    Blood. 2012 Oct 4;120(14):2843-52 PMID: 22904298
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2012-11-20
Epub
2012-00-05
Pages
19408-13
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3511085
Subset
IM
Grants
Canadian Institutes of Health Research · Canada
Intramural NIH HHS · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com