Dissecting Hierarchies of Epigenetic Control in Gene Silencing
The hormone-related estrogen receptor (ER)-alpha signaling has been intensively studied in breast cancer cells. Our
recent
study has implicated,
for
the
first time, the epigenetic influence (i.e., chromatin remodeling and DNA methylation) on the transcription of ER-alpha downstream target genes and
provides a new direction of research in this classical signaling pathway. We hypothesize that disruption of normal ER-alpha signaling in cancer
cells may
lead to long-term silencing of some downstream targets that are governed by epigenetic mechanisms. In this project, we will use computational and
microarray-based approaches to define the molecular sequences leading to this epigenetic establishment. A positional weight matrix approach will be
used to align and identify ~350 novel and known ER-alpha targets, the 5’-end sequences of which will be arrayed for triple microarray analysis. In
this
microarray study, the exon-containing portions (exon 1) of these loci will be used for measuring expression levels of transcripts, their promoter
sequences will be used for screening altered states of chromatin structure, and the GC-rich regions will be used for detecting changes of DNA
methylation in the target sequences. Triple microarray will be used to simultaneously analyze these ER targets in cultured breast cancer cells
in
which estrogen signaling is disrupted by small interference RNA. An empirical Bayesian approach will be used to model the sequences of epigenetic
alterations after the RNA interference. Additional microarray experiments will also be conducted to reverse this epigenetic event by treating breast
cancer cells with DNA demethylating agents and/or histone deacetylase inhibitors. The results may establish a model that upon ER-alpha signal
disruption,
polycomb repressors and histone deacetylases are recruited to initiate transcriptional silencing in the interrogating ER-alpha targets. This
event is
later accompanied by progressive accumulation of DNA methylation in the promoter regions of these targets, which leave a heritable mark that stably
passes down to cells’ progeny. Additional computation simulations will be used to explore other sequences of epigenetic events. The in vitro finding
will be confirmed by conducting methylation microarray analysis in primary breast tumors. This proposed study is expected to give new information that
hormonal insensitivity in breast cancer is, in part, attributed to epigenetically mediated silencing of multiple ER-alpha and hope to provide a
rationale for epigenetic therapies in breast cancer.
The Ohio State University:
Tim Huang, Principle Investigator
Ramana Davuluri, Co-Investigator
Dustin Potter, Postdoctoral Fellow
Hao Sun, Research Scientist
Joseph Liu, Research Specialist
Indiana University:
Lang Li, Co-Investigator
Relevant Publications:
- Li L, Shi H, Yiannoutsos C, Huang TH, Nephew KP.
Epigenetic hypothesis tests for methylation and acetylation in a triple microarray system.
J Comput Biol. 2005 April, 12(3):370-90.
- Alfred S.L. Cheng, Victor X. Jin, Meiyun Fan, Laura T. Smith, Sandya Liyanarachchi, Pearlly S. Yan, Yu-Wei Leu, Michael W.Y. Chan, Christoph Plass, Kenneth P. Nephew, Ramana V. Davuluri, and Tim H.-M. Huang
Combinatorial Analysis of Transcription Factor Partners Reveals Recruitment of c-MYC to Estrogen Receptor-a Responsive Promoters.
Molecular Cell. 2006 February 3, 21:393-404
- Yu-Wei Leu, Pearlly S. Yan, Meiyun Fan, Victor X. Jin, Joseph C. Liu, Edward M. Curran, Wade V. Welshons, Susan H. Wei, Ramana V. Davuluri, Christoph Plass, Kenneth P. Nephew, and Tim H-M. Huang
Loss of Estrogen Receptor Signaling Triggers Epigenetic Silencing of Downstream Targets in Breast Cancer
Cancer Research. 2004 November 15, 64:8184-8192
- Lang Li1, Alfred S.L. Cheng, Victor X. Jin, Henry H. Paik, Meiyun Fan, Xiaoman Li, Wei Zhang, Jason Robarge, Cur-tis Balch, Ramana V. Davuluri, Sun Kim, Tim H.-M. Huang, Kenneth P. Nephew
A Mixture Model Based Discriminate Analysis for Identifying Ordered Transcription Factor Binding Site Pairs in Gene Promoters Directly Regulated by Estrogen Receptor-a
Bioinformatics. 2006 June 29, Advance Access
- Alfred S.L. Cheng, Victor X. Jin, Meiyun Fan, Laura T. Smith, Sandya Liyanarachchi, Pearlly S. Yan, Yu-Wei Leu, Michael W.Y. Chan, Christoph Plass, Kenneth P. Nephew, Ramana V. Davuluri, and Tim H.-M. Huang
Combinatorial Analysis of Transcription Factor Partners Reveals Recruitment of c-MYC to Estrogen Receptor-a Responsive Promoters.
Molecular Cell. 2006 February 3, 21:393-404
- Lang Li, Huidong Shi, Constantin Yiannoutsos, Tim Hui-Ming Huang, and Kenneth P. Nephew
Epigenetic Hypothesis Tests for Methylation and Acetylation in a Triple Microarray System
Journal of Computational Biology. 2005 April, 12(3):370-390
- Victor X. Jin, Yu-Wei Leu, Sandya Liyanarachchi, Hao Sun, Meiyun Fan, Kenneth P. Nephew, Tim H.-M. Huang and Ramana V. Davuluri
Identifying estrogen receptor a target genes using integrated computational genomics and chromatin immunoprecipitation microarray
Nucleic Acid Research. 2004 December 17, 32(22):6627-6635
- Yu-Wei Leu, Pearlly S. Yan, Meiyun Fan, Victor X. Jin, Joseph C. Liu, Edward M. Curran, Wade V. Welshons, Susan H. Wei, Ramana V. Davuluri, Christoph Plass, Kenneth P. Nephew, and Tim H-M. Huang
Loss of Estrogen Receptor Signaling Triggers Epigenetic Silencing of Downstream Targets in Breast Cancer
Cancer Research. 2004 November 15, 64:8184-8192
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