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Chromatin, Epigenetics, and RNA Regulation

Integrative Analysis Reveals the Transcriptional Collaboration between EZH2 and E2F1 in the Regulation of Cancer-Related Gene Expression

Han Xu, Kexin Xu, Housheng H. He, Chongzhi Zang, Chen-Hao Chen, Yiwen Chen, Qian Qin, Su Wang, Chenfei Wang, Shengen Hu, Fugen Li, Henry Long, Myles Brown and X. Shirley Liu
Han Xu
1Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute and Harvard School of Public Health, Boston, Massachusetts.
2Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Kexin Xu
1Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute and Harvard School of Public Health, Boston, Massachusetts.
2Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, Massachusetts.
3Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
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Housheng H. He
1Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute and Harvard School of Public Health, Boston, Massachusetts.
2Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, Massachusetts.
3Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
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Chongzhi Zang
1Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute and Harvard School of Public Health, Boston, Massachusetts.
2Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Chen-Hao Chen
1Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute and Harvard School of Public Health, Boston, Massachusetts.
2Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Yiwen Chen
1Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute and Harvard School of Public Health, Boston, Massachusetts.
2Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Qian Qin
2Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Su Wang
2Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Chenfei Wang
2Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Shengen Hu
2Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Fugen Li
2Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Henry Long
2Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Myles Brown
2Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, Massachusetts.
3Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
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  • For correspondence: xsliu@jimmy.harvard.edu myles_brown@dfci.harvard.edu
X. Shirley Liu
1Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute and Harvard School of Public Health, Boston, Massachusetts.
2Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, Massachusetts.
4School of Life Science and Technology, Tongji University, Shanghai, China.
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  • For correspondence: xsliu@jimmy.harvard.edu myles_brown@dfci.harvard.edu
DOI: 10.1158/1541-7786.MCR-15-0313 Published February 2016
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Abstract

Overexpression of EZH2 is frequently linked to the advanced and metastatic stage of cancers. The mechanisms of its oncogenic function can be context specific, and may vary depending on the protein complexes that EZH2 interacts with. To identify novel transcriptional collaborators of EZH2 in cancers, a computational approach was developed that integrates protein–DNA binding data, cell perturbation gene expression data, and compendiums of tumor expression profiles. This holistic approach identified E2F1, a known mediator of the Rb tumor suppressor, as a transcriptional collaborator of EZH2 in castration-resistant prostate cancer. Subsequent analysis and experimental validation found EZH2 and E2F1 cobind to a subset of chromatin sites lacking H3K27 trimethylation, and activate genes that are critical for prostate cancer progression. The collaboration of EZH2 and E2F1 in transcriptional regulation is also observed in diffuse large B-cell lymphoma cell lines, where activation of the transcriptional network is concordant with the cellular response to the EZH2 inhibitor.

Implications: The direct collaboration between EZH2 and Rb/E2F1 pathway provides an innovative mechanism underlying the cascade of tumor progression, and lays the foundation for the development of new anticancer targets/strategies. Mol Cancer Res; 14(2); 163–72. ©2015 AACR.

This article is featured in Highlights of This Issue, p. 125

Footnotes

  • Note: Supplementary data for this article are available at Molecular Cancer Research Online (http://mcr.aacrjournals.org/).

  • Received July 16, 2015.
  • Revision received November 16, 2015.
  • Accepted November 21, 2015.
  • ©2015 American Association for Cancer Research.
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Molecular Cancer Research: 14 (2)
February 2016
Volume 14, Issue 2
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Integrative Analysis Reveals the Transcriptional Collaboration between EZH2 and E2F1 in the Regulation of Cancer-Related Gene Expression
Han Xu, Kexin Xu, Housheng H. He, Chongzhi Zang, Chen-Hao Chen, Yiwen Chen, Qian Qin, Su Wang, Chenfei Wang, Shengen Hu, Fugen Li, Henry Long, Myles Brown and X. Shirley Liu
Mol Cancer Res February 1 2016 (14) (2) 163-172; DOI: 10.1158/1541-7786.MCR-15-0313

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Integrative Analysis Reveals the Transcriptional Collaboration between EZH2 and E2F1 in the Regulation of Cancer-Related Gene Expression
Han Xu, Kexin Xu, Housheng H. He, Chongzhi Zang, Chen-Hao Chen, Yiwen Chen, Qian Qin, Su Wang, Chenfei Wang, Shengen Hu, Fugen Li, Henry Long, Myles Brown and X. Shirley Liu
Mol Cancer Res February 1 2016 (14) (2) 163-172; DOI: 10.1158/1541-7786.MCR-15-0313
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