The amino-terminal domain of the androgen receptor co-opts extracellular signal-regulated kinase (ERK) docking sites in ELK1 protein to induce sustained gene activation that supports prostate cancer cell growth

The ETS domain transcription factor ELK1 is in a repressive association with growth genes and is transiently activated through phosphorylation by ERK1/2. In prostate cancer (PCa) cells the androgen receptor (AR) is recruited by ELK1, via its amino-terminal domain (A/B), as a transcriptional co-activ...

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Main Authors: Rosati, Rayna, Patki, Mugdha, Chari, Venkatesh, Dakshnamurthy, Selvakumar, McFall, Thomas, Saxton, Janice, Kidder, Benjamin L., Shaw, Peter E., Ratnam, Manohar
Format: Article
Published: American Society for Biochemistry and Molecular Biology 2016
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Online Access:https://eprints.nottingham.ac.uk/41159/
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author Rosati, Rayna
Patki, Mugdha
Chari, Venkatesh
Dakshnamurthy, Selvakumar
McFall, Thomas
Saxton, Janice
Kidder, Benjamin L.
Shaw, Peter E.
Ratnam, Manohar
author_facet Rosati, Rayna
Patki, Mugdha
Chari, Venkatesh
Dakshnamurthy, Selvakumar
McFall, Thomas
Saxton, Janice
Kidder, Benjamin L.
Shaw, Peter E.
Ratnam, Manohar
author_sort Rosati, Rayna
building Nottingham Research Data Repository
collection Online Access
description The ETS domain transcription factor ELK1 is in a repressive association with growth genes and is transiently activated through phosphorylation by ERK1/2. In prostate cancer (PCa) cells the androgen receptor (AR) is recruited by ELK1, via its amino-terminal domain (A/B), as a transcriptional co-activator, without ELK1 hyper-phosphorylation. Here we elucidate the structural basis of the interaction of AR with ELK1. The ELK1 polypeptide motifs required for co-activation by AR versus those required for activation of ELK1 by ERK were systematically mapped using a mammalian two-hybrid system and confirmed using a co-immunoprecipitation assay. The mapping precisely identified the two ERK-docking sites in ELK1, the D-box and the DEF (docking site for ERK, FXFP) motif, as the essential motifs for its cooperation with AR(A/B) or WTAR. In contrast, the transactivation domain in ELK1 was only required for activation by ERK. ELK1-mediated transcriptional activity of AR(A/B) was optimal in the absence of ELK1 binding partners, ERK1/2 and serum-response factor. Purified ELK1 and AR bound with a dissociation constant of 1.9 × 10−8 m. A purified mutant ELK1 in which the D-box and DEF motifs were disrupted did not bind AR. An ELK1 mutant with deletion of the D-box region had a dominant-negative effect on androgen-dependent growth of PCa cells that were insensitive to MEK inhibition. This novel mechanism in which a nuclear receptor impinges on a signaling pathway by co-opting protein kinase docking sites to constitutively activate growth genes could enable rational design of a new class of targeted drug interventions.
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spelling nottingham-411592020-05-04T18:26:47Z https://eprints.nottingham.ac.uk/41159/ The amino-terminal domain of the androgen receptor co-opts extracellular signal-regulated kinase (ERK) docking sites in ELK1 protein to induce sustained gene activation that supports prostate cancer cell growth Rosati, Rayna Patki, Mugdha Chari, Venkatesh Dakshnamurthy, Selvakumar McFall, Thomas Saxton, Janice Kidder, Benjamin L. Shaw, Peter E. Ratnam, Manohar The ETS domain transcription factor ELK1 is in a repressive association with growth genes and is transiently activated through phosphorylation by ERK1/2. In prostate cancer (PCa) cells the androgen receptor (AR) is recruited by ELK1, via its amino-terminal domain (A/B), as a transcriptional co-activator, without ELK1 hyper-phosphorylation. Here we elucidate the structural basis of the interaction of AR with ELK1. The ELK1 polypeptide motifs required for co-activation by AR versus those required for activation of ELK1 by ERK were systematically mapped using a mammalian two-hybrid system and confirmed using a co-immunoprecipitation assay. The mapping precisely identified the two ERK-docking sites in ELK1, the D-box and the DEF (docking site for ERK, FXFP) motif, as the essential motifs for its cooperation with AR(A/B) or WTAR. In contrast, the transactivation domain in ELK1 was only required for activation by ERK. ELK1-mediated transcriptional activity of AR(A/B) was optimal in the absence of ELK1 binding partners, ERK1/2 and serum-response factor. Purified ELK1 and AR bound with a dissociation constant of 1.9 × 10−8 m. A purified mutant ELK1 in which the D-box and DEF motifs were disrupted did not bind AR. An ELK1 mutant with deletion of the D-box region had a dominant-negative effect on androgen-dependent growth of PCa cells that were insensitive to MEK inhibition. This novel mechanism in which a nuclear receptor impinges on a signaling pathway by co-opting protein kinase docking sites to constitutively activate growth genes could enable rational design of a new class of targeted drug interventions. American Society for Biochemistry and Molecular Biology 2016-12-09 Article PeerReviewed Rosati, Rayna, Patki, Mugdha, Chari, Venkatesh, Dakshnamurthy, Selvakumar, McFall, Thomas, Saxton, Janice, Kidder, Benjamin L., Shaw, Peter E. and Ratnam, Manohar (2016) The amino-terminal domain of the androgen receptor co-opts extracellular signal-regulated kinase (ERK) docking sites in ELK1 protein to induce sustained gene activation that supports prostate cancer cell growth. Journal of Biological Chemistry, 291 (50). pp. 25983-25998. ISSN 1083-351X Androgen receptor ETS transcription factor family Extracellular signal-regulated kinase (ERK) Prostate cancer Transcription https://doi.org/10.1074/jbc.M116.745596 doi:10.1074/jbc.M116.745596 doi:10.1074/jbc.M116.745596
spellingShingle Androgen receptor
ETS transcription factor family
Extracellular signal-regulated kinase (ERK)
Prostate cancer
Transcription
Rosati, Rayna
Patki, Mugdha
Chari, Venkatesh
Dakshnamurthy, Selvakumar
McFall, Thomas
Saxton, Janice
Kidder, Benjamin L.
Shaw, Peter E.
Ratnam, Manohar
The amino-terminal domain of the androgen receptor co-opts extracellular signal-regulated kinase (ERK) docking sites in ELK1 protein to induce sustained gene activation that supports prostate cancer cell growth
title The amino-terminal domain of the androgen receptor co-opts extracellular signal-regulated kinase (ERK) docking sites in ELK1 protein to induce sustained gene activation that supports prostate cancer cell growth
title_full The amino-terminal domain of the androgen receptor co-opts extracellular signal-regulated kinase (ERK) docking sites in ELK1 protein to induce sustained gene activation that supports prostate cancer cell growth
title_fullStr The amino-terminal domain of the androgen receptor co-opts extracellular signal-regulated kinase (ERK) docking sites in ELK1 protein to induce sustained gene activation that supports prostate cancer cell growth
title_full_unstemmed The amino-terminal domain of the androgen receptor co-opts extracellular signal-regulated kinase (ERK) docking sites in ELK1 protein to induce sustained gene activation that supports prostate cancer cell growth
title_short The amino-terminal domain of the androgen receptor co-opts extracellular signal-regulated kinase (ERK) docking sites in ELK1 protein to induce sustained gene activation that supports prostate cancer cell growth
title_sort amino-terminal domain of the androgen receptor co-opts extracellular signal-regulated kinase (erk) docking sites in elk1 protein to induce sustained gene activation that supports prostate cancer cell growth
topic Androgen receptor
ETS transcription factor family
Extracellular signal-regulated kinase (ERK)
Prostate cancer
Transcription
url https://eprints.nottingham.ac.uk/41159/
https://eprints.nottingham.ac.uk/41159/
https://eprints.nottingham.ac.uk/41159/