lncRNA-dependent mechanisms of androgen-receptor-regulated gene activation programs
A study of prostate cancer cells reveals a transcriptional activation role for long non-coding RNAs (PRNCR1 and PCGEM1) that bind to the androgen receptor, and is also observed for the truncated androgen receptor characteristic of many aggressive prostate cancers. Cancer growth influenced by long no...
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| Published in | Nature (London) Vol. 500; no. 7464; pp. 598 - 602 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
29.08.2013
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | A study of prostate cancer cells reveals a transcriptional activation role for long non-coding RNAs (PRNCR1 and PCGEM1) that bind to the androgen receptor, and is also observed for the truncated androgen receptor characteristic of many aggressive prostate cancers.
Cancer growth influenced by long non-coding RNAs
Several long non-coding RNAs (lncRNAs) are known to be overexpressed in prostate cancer. Michael Rosenfeld and colleagues have investigated the mechanistic and biological roles of two of these, known as PRNCR1 and PCGEM1. Both are found to interact with the androgen receptor (AR) dependent on specific post-translational modifications, and to enhance the looping of AR-bound enhancers to target gene promoters, leading to enhanced gene expression. They also enhance AR-mediated proliferation in prostate cancer cells and are required for tumour growth in a prostate cancer xenograft mouse model. PRNCR1 and PCGEM1 are upregulated in castration-resistant prostate cancer cell lines. The regulatory roles of lncRNAs in prostate cancer uncovered in this manuscript may open the way to new therapeutic approaches.
Although recent studies have indicated roles of long non-coding RNAs (lncRNAs) in physiological aspects of cell-type determination and tissue homeostasis
1
, their potential involvement in regulated gene transcription programs remains rather poorly understood. The androgen receptor regulates a large repertoire of genes central to the identity and behaviour of prostate cancer cells
2
, and functions in a ligand-independent fashion in many prostate cancers when they become hormone refractory after initial androgen deprivation therapy
3
. Here we report that two lncRNAs highly overexpressed in aggressive prostate cancer, PRNCR1 (also known as PCAT8) and PCGEM1, bind successively to the androgen receptor and strongly enhance both ligand-dependent and ligand-independent androgen-receptor-mediated gene activation programs and proliferation in prostate cancer cells. Binding of PRNCR1 to the carboxy-terminally acetylated androgen receptor on enhancers and its association with DOT1L appear to be required for recruitment of the second lncRNA, PCGEM1, to the androgen receptor amino terminus that is methylated by DOT1L. Unexpectedly, recognition of specific protein marks by PCGEM1-recruited pygopus 2 PHD domain enhances selective looping of androgen-receptor-bound enhancers to target gene promoters in these cells. In ‘resistant’ prostate cancer cells, these overexpressed lncRNAs can interact with, and are required for, the robust activation of both truncated and full-length androgen receptor, causing ligand-independent activation of the androgen receptor transcriptional program and cell proliferation. Conditionally expressed short hairpin RNA targeting these lncRNAs in castration-resistant prostate cancer cell lines strongly suppressed tumour xenograft growth
in vivo
. Together, these results indicate that these overexpressed lncRNAs can potentially serve as a required component of castration-resistance in prostatic tumours. |
|---|---|
| AbstractList | While recent studies indicated roles of long non-coding RNAs (lncRNAs) in physiologic aspects of cell-type determination and tissue homeostasis
1
yet their potential involvement in regulated gene transcription programs remain rather poorly understood. Androgen receptor (AR) regulates a large repertoire of genes central to the identity and behavior of prostate cancer cells
2
, and functions in a ligand-independent fashion in many prostate cancers when they become hormone refractory after initial androgen deprivation therapy
3
. Here, we report that two lncRNAs highly overexpressed in aggressive prostate cancer,
PRNCR1
and
PCGEM1
, bind successively to the AR and strongly enhance both ligand-dependent and ligand-independent AR-mediated gene activation programs and proliferation in prostate cancer cells. Binding of
PRNCR1
to the C-terminally acetylated AR on enhancers and its association with DOT1L appear to be required for recruitment of the second lncRNA,
PCGEM1
, to the DOT1L-mediated methylated AR N-terminus. Unexpectedly, recognition of specific protein marks by
PCGEM1
-recruited Pygopus2 PHD domain proves to enhance selective looping of AR-bound enhancers to target gene promoters in these cells. In “resistant” prostate cancer cells, these overexpressed lncRNAs can interact with, and are required for, the robust activation of both truncated and full length AR, causing ligand-independent activation of the AR transcriptional program and cell proliferation. Conditionally-expressed short hairpin RNA (shRNA) targeting of these lncRNAs in castration-resistant prostate cancer (CRPC) cell lines strongly suppressed tumor xenograft growth
in vivo
. Together, these results suggest that these overexpressed lncRNAs can potentially serve as a required component of castration-resistance in prostatic tumors. A study of prostate cancer cells reveals a transcriptional activation role for long non-coding RNAs (PRNCR1 and PCGEM1) that bind to the androgen receptor, and is also observed for the truncated androgen receptor characteristic of many aggressive prostate cancers. A study of prostate cancer cells reveals a transcriptional activation role for long non-coding RNAs (PRNCR1 and PCGEM1) that bind to the androgen receptor, and is also observed for the truncated androgen receptor characteristic of many aggressive prostate cancers. Cancer growth influenced by long non-coding RNAs Several long non-coding RNAs (lncRNAs) are known to be overexpressed in prostate cancer. Michael Rosenfeld and colleagues have investigated the mechanistic and biological roles of two of these, known as PRNCR1 and PCGEM1. Both are found to interact with the androgen receptor (AR) dependent on specific post-translational modifications, and to enhance the looping of AR-bound enhancers to target gene promoters, leading to enhanced gene expression. They also enhance AR-mediated proliferation in prostate cancer cells and are required for tumour growth in a prostate cancer xenograft mouse model. PRNCR1 and PCGEM1 are upregulated in castration-resistant prostate cancer cell lines. The regulatory roles of lncRNAs in prostate cancer uncovered in this manuscript may open the way to new therapeutic approaches. Although recent studies have indicated roles of long non-coding RNAs (lncRNAs) in physiological aspects of cell-type determination and tissue homeostasis.sup.1, their potential involvement in regulated gene transcription programs remains rather poorly understood. The androgen receptor regulates a large repertoire of genes central to the identity and behaviour of prostate cancer cells.sup.2, and functions in a ligand-independent fashion in many prostate cancers when they become hormone refractory after initial androgen deprivation therapy.sup.3. Here we report that two lncRNAs highly overexpressed in aggressive prostate cancer, PRNCR1 (also known as PCAT8) and PCGEM1, bind successively to the androgen receptor and strongly enhance both ligand-dependent and ligand-independent androgen-receptor-mediated gene activation programs and proliferation in prostate cancer cells. Binding of PRNCR1 to the carboxy-terminally acetylated androgen receptor on enhancers and its association with DOT1L appear to be required for recruitment of the second lncRNA, PCGEM1, to the androgen receptor amino terminus that is methylated by DOT1L. Unexpectedly, recognition of specific protein marks by PCGEM1-recruited pygopus 2 PHD domain enhances selective looping of androgen-receptor-bound enhancers to target gene promoters in these cells. In 'resistant' prostate cancer cells, these overexpressed lncRNAs can interact with, and are required for, the robust activation of both truncated and full-length androgen receptor, causing ligand-independent activation of the androgen receptor transcriptional program and cell proliferation. Conditionally expressed short hairpin RNA targeting these lncRNAs in castration-resistant prostate cancer cell lines strongly suppressed tumour xenograft growth in vivo. Together, these results indicate that these overexpressed lncRNAs can potentially serve as a required component of castration-resistance in prostatic tumours. Although recent studies have indicated roles of long non-coding RNAs (lncRNAs) in physiological aspects of cell-type determination and tissue homeostasis, their potential involvement in regulated gene transcription programs remains rather poorly understood. The androgen receptor regulates a large repertoire of genes central to the identity and behaviour of prostate cancer cells, and functions in a ligand-independent fashion in many prostate cancers when they become hormone refractory after initial androgen deprivation therapy. Here we report that two lncRNAs highly overexpressed in aggressive prostate cancer, PRNCR1 (also known as PCAT8) and PCGEM1, bind successively to the androgen receptor and strongly enhance both ligand-dependent and ligand-independent androgen-receptor-mediated gene activation programs and proliferation in prostate cancer cells. Binding of PRNCR1 to the carboxy-terminally acetylated androgen receptor on enhancers and its association with DOT1L appear to be required for recruitment of the second lncRNA, PCGEM1, to the androgen receptor amino terminus that is methylated by DOT1L. Unexpectedly, recognition of specific protein marks by PCGEM1-recruited pygopus 2 PHD domain enhances selective looping of androgen-receptor-bound enhancers to target gene promoters in these cells. In 'resistant' prostate cancer cells, these overexpressed lncRNAs can interact with, and are required for, the robust activation of both truncated and full-length androgen receptor, causing ligand-independent activation of the androgen receptor transcriptional program and cell proliferation. Conditionally expressed short hairpin RNA targeting these lncRNAs in castration-resistant prostate cancer cell lines strongly suppressed tumour xenograft growth in vivo. Together, these results indicate that these overexpressed lncRNAs can potentially serve as a required component of castration-resistance in prostatic tumours. Although recent studies have indicated roles of long non-coding RNAs (lncRNAs) in physiological aspects of cell-type determination and tissue homeostasis, their potential involvement in regulated gene transcription programs remains rather poorly understood. The androgen receptor regulates a large repertoire of genes central to the identity and behaviour of prostate cancer cells, and functions in a ligand-independent fashion in many prostate cancers when they become hormone refractory after initial androgen deprivation therapy. Here we report that two lncRNAs highly overexpressed in aggressive prostate cancer, PRNCR1 (also known as PCAT8) and PCGEM1, bind successively to the androgen receptor and strongly enhance both ligand-dependent and ligand-independent androgen-receptor-mediated gene activation programs and proliferation in prostate cancer cells. Binding of PRNCR1 to the carboxy-terminally acetylated androgen receptor on enhancers and its association with DOT1L appear to be required for recruitment of the second lncRNA, PCGEM1, to the androgen receptor amino terminus that is methylated by DOT1L. Unexpectedly, recognition of specific protein marks by PCGEM1- recruited pygopus 2 PHD domain enhances selective looping of androgen-receptor-bound enhancers to target gene promoters in these cells. In 'resistant' prostate cancer cells, these overexpressed lncRNAs can interact with, and are required for, the robust activation of both truncated and full-length androgen receptor, causing ligand-independent activation of the androgen receptor transcriptional programand cell proliferation.Conditionally expressed short hairpin RNA targeting these lncRNAs in castration-resistant prostate cancer cell lines strongly suppressed tumour xenograftgrowth in vivo. Together, these results indicate that these overexpressed lncRNAs can potentially serve as a required component of castration-resistance in prostatic tumours. [PUBLICATION ABSTRACT] A study of prostate cancer cells reveals a transcriptional activation role for long non-coding RNAs (PRNCR1 and PCGEM1) that bind to the androgen receptor, and is also observed for the truncated androgen receptor characteristic of many aggressive prostate cancers. Cancer growth influenced by long non-coding RNAs Several long non-coding RNAs (lncRNAs) are known to be overexpressed in prostate cancer. Michael Rosenfeld and colleagues have investigated the mechanistic and biological roles of two of these, known as PRNCR1 and PCGEM1. Both are found to interact with the androgen receptor (AR) dependent on specific post-translational modifications, and to enhance the looping of AR-bound enhancers to target gene promoters, leading to enhanced gene expression. They also enhance AR-mediated proliferation in prostate cancer cells and are required for tumour growth in a prostate cancer xenograft mouse model. PRNCR1 and PCGEM1 are upregulated in castration-resistant prostate cancer cell lines. The regulatory roles of lncRNAs in prostate cancer uncovered in this manuscript may open the way to new therapeutic approaches. Although recent studies have indicated roles of long non-coding RNAs (lncRNAs) in physiological aspects of cell-type determination and tissue homeostasis 1 , their potential involvement in regulated gene transcription programs remains rather poorly understood. The androgen receptor regulates a large repertoire of genes central to the identity and behaviour of prostate cancer cells 2 , and functions in a ligand-independent fashion in many prostate cancers when they become hormone refractory after initial androgen deprivation therapy 3 . Here we report that two lncRNAs highly overexpressed in aggressive prostate cancer, PRNCR1 (also known as PCAT8) and PCGEM1, bind successively to the androgen receptor and strongly enhance both ligand-dependent and ligand-independent androgen-receptor-mediated gene activation programs and proliferation in prostate cancer cells. Binding of PRNCR1 to the carboxy-terminally acetylated androgen receptor on enhancers and its association with DOT1L appear to be required for recruitment of the second lncRNA, PCGEM1, to the androgen receptor amino terminus that is methylated by DOT1L. Unexpectedly, recognition of specific protein marks by PCGEM1-recruited pygopus 2 PHD domain enhances selective looping of androgen-receptor-bound enhancers to target gene promoters in these cells. In ‘resistant’ prostate cancer cells, these overexpressed lncRNAs can interact with, and are required for, the robust activation of both truncated and full-length androgen receptor, causing ligand-independent activation of the androgen receptor transcriptional program and cell proliferation. Conditionally expressed short hairpin RNA targeting these lncRNAs in castration-resistant prostate cancer cell lines strongly suppressed tumour xenograft growth in vivo . Together, these results indicate that these overexpressed lncRNAs can potentially serve as a required component of castration-resistance in prostatic tumours. |
| Audience | Academic |
| Author | Merkurjev, Daria Ohgi, Kenneth A. Tanasa, Bogdan Rosenfeld, Michael G. Meng, Da Evans, Christopher P. Yang, Liuqing Lin, Chunru Yang, Joy C. Zhang, Jie Jin, Chunyu Li, Wenbo |
| AuthorAffiliation | 6 Neurosciences Graduate Program, Department of Biological Sciences, University of California San Diego, La Jolla 92093, USA 5 Bioinformatics and System Biology Program, Department of Bioengineering, University of California San Diego, La Jolla 92093, USA 4 Graduate Program, Kellogg School of Science and Technology, The Scripps Research Institute, La Jolla 92037, USA 2 Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA 1 Howard Hughes Medical Institute, Department of Medicine, University of California San Diego, La Jolla 92093, USA 3 Department of Urology, School of Medicine, University of California Davis, Sacramento 95817, USA |
| AuthorAffiliation_xml | – name: 5 Bioinformatics and System Biology Program, Department of Bioengineering, University of California San Diego, La Jolla 92093, USA – name: 2 Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – name: 1 Howard Hughes Medical Institute, Department of Medicine, University of California San Diego, La Jolla 92093, USA – name: 6 Neurosciences Graduate Program, Department of Biological Sciences, University of California San Diego, La Jolla 92093, USA – name: 3 Department of Urology, School of Medicine, University of California Davis, Sacramento 95817, USA – name: 4 Graduate Program, Kellogg School of Science and Technology, The Scripps Research Institute, La Jolla 92037, USA |
| Author_xml | – sequence: 1 givenname: Liuqing surname: Yang fullname: Yang, Liuqing email: lyang7@mdanderson.org organization: Department of Medicine, Howard Hughes Medical Institute, University of California San Diego, Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center – sequence: 2 givenname: Chunru surname: Lin fullname: Lin, Chunru email: clin2@mdanderson.org organization: Department of Medicine, Howard Hughes Medical Institute, University of California San Diego, Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center – sequence: 3 givenname: Chunyu surname: Jin fullname: Jin, Chunyu organization: Department of Medicine, Howard Hughes Medical Institute, University of California San Diego – sequence: 4 givenname: Joy C. surname: Yang fullname: Yang, Joy C. organization: Department of Urology, School of Medicine, University of California Davis – sequence: 5 givenname: Bogdan surname: Tanasa fullname: Tanasa, Bogdan organization: Department of Medicine, Howard Hughes Medical Institute, University of California San Diego, Graduate Program, Kellogg School of Science and Technology, The Scripps Research Institute – sequence: 6 givenname: Wenbo surname: Li fullname: Li, Wenbo organization: Department of Medicine, Howard Hughes Medical Institute, University of California San Diego – sequence: 7 givenname: Daria surname: Merkurjev fullname: Merkurjev, Daria organization: Department of Medicine, Howard Hughes Medical Institute, University of California San Diego, Department of Bioengineering, Bioinformatics and System Biology Program, University of California San Diego – sequence: 8 givenname: Kenneth A. surname: Ohgi fullname: Ohgi, Kenneth A. organization: Department of Medicine, Howard Hughes Medical Institute, University of California San Diego – sequence: 9 givenname: Da surname: Meng fullname: Meng, Da organization: Department of Biological Sciences, Neurosciences Graduate Program, University of California San Diego – sequence: 10 givenname: Jie surname: Zhang fullname: Zhang, Jie organization: Department of Medicine, Howard Hughes Medical Institute, University of California San Diego – sequence: 11 givenname: Christopher P. surname: Evans fullname: Evans, Christopher P. organization: Department of Urology, School of Medicine, University of California Davis – sequence: 12 givenname: Michael G. surname: Rosenfeld fullname: Rosenfeld, Michael G. email: mrosenfeld@ucsd.edu organization: Department of Medicine, Howard Hughes Medical Institute, University of California San Diego |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23945587$$D View this record in MEDLINE/PubMed |
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| Snippet | A study of prostate cancer cells reveals a transcriptional activation role for long non-coding RNAs (PRNCR1 and PCGEM1) that bind to the androgen receptor, and... Although recent studies have indicated roles of long non-coding RNAs (lncRNAs) in physiological aspects of cell-type determination and tissue homeostasis,... While recent studies indicated roles of long non-coding RNAs (lncRNAs) in physiologic aspects of cell-type determination and tissue homeostasis 1 yet their... |
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| SubjectTerms | 631/337/384/2568 631/337/572 631/67 Androgens Animals Binding sites Castration Cell Line, Tumor Cell Proliferation Development and progression Efficiency Enhancer Elements, Genetic - genetics Experiments Gene expression Genetic aspects Genetic regulation Humanities and Social Sciences Humans letter Male Mass spectrometry Mice Mice, Nude multidisciplinary Neoplasm Transplantation Physiological aspects Promoter Regions, Genetic - genetics Prostate cancer Prostatic Neoplasms - genetics Prostatic Neoplasms - pathology Proteins Receptors, Androgen - metabolism Recruitment RNA, Long Noncoding - genetics Science Transcription Factors - metabolism Transcriptional Activation - genetics Up-Regulation - genetics |
| Title | lncRNA-dependent mechanisms of androgen-receptor-regulated gene activation programs |
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