Structural and Functional Evidence for Testosterone Activation of GPRC6A in Peripheral Tissues
Abstract
G protein-coupled receptor (GPCR) family C group 6 member A (GPRC6A) is a multiligand GPCR that is activated by cations, L-amino acids, and osteocalcin. GPRC6A plays an important role in the regulation of testosterone (T) production and energy metabolism in mice. T has rapid, transcription-independent (nongenomic) effects that are mediated by a putative GPCR. We previously found that T can activate GPRC6A in vitro, but the possibility that T is a ligand for GPRC6A remains controversial. Here, we demonstrate direct T binding to GPRC6A and construct computational structural models of GPRC6A that are used to identify potential binding poses of T. Mutations of the predicted binding site residues were experimentally found to block T activation of GPRC6A, in agreement with the modeling. Using Gpr6ca(-/-) mice, we confirmed that loss of GPRC6A resulted in loss of T rapid signaling responses and elucidated several biological functions regulated by GPRC6A-dependent T rapid signaling, including T stimulation of insulin secretion in pancreatic islets and enzyme expression involved in the biosynthesis of T in Leydig cells. Finally, we identified a stereo-specific effect of an R-isomer of a selective androgen receptor modulator that is predicted to bind to and shown to activate GPRC6A but not androgenmore »
- Authors:
-
- Univ. of Tennessee, Memphis, TN (United States). Health Science Center
- Univ. of Tennessee, Knoxville, TN (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1336593
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Molecular Endocrinology
- Additional Journal Information:
- Journal Volume: 29; Journal Issue: 12; Journal ID: ISSN 0888-8809
- Country of Publication:
- United States
- Language:
- English
Citation Formats
Pi, Min, Kapoor, Karan, Wu, Yunpeng, Ye, Ruisong, Senogles, Susan, Nishimoto, Satoru Kenneth, Hwang, Dong-Jin, Miller, Duane, Narayanan, Ramesh, Smith, Jeremy C., Baudry, Jerome, and Quarles, Leigh Darryl. Structural and Functional Evidence for Testosterone Activation of GPRC6A in Peripheral Tissues. United States: N. p., 2015.
Web. doi:10.1210/me.2015-1161.
Pi, Min, Kapoor, Karan, Wu, Yunpeng, Ye, Ruisong, Senogles, Susan, Nishimoto, Satoru Kenneth, Hwang, Dong-Jin, Miller, Duane, Narayanan, Ramesh, Smith, Jeremy C., Baudry, Jerome, & Quarles, Leigh Darryl. Structural and Functional Evidence for Testosterone Activation of GPRC6A in Peripheral Tissues. United States. https://doi.org/10.1210/me.2015-1161
Pi, Min, Kapoor, Karan, Wu, Yunpeng, Ye, Ruisong, Senogles, Susan, Nishimoto, Satoru Kenneth, Hwang, Dong-Jin, Miller, Duane, Narayanan, Ramesh, Smith, Jeremy C., Baudry, Jerome, and Quarles, Leigh Darryl. Thu .
"Structural and Functional Evidence for Testosterone Activation of GPRC6A in Peripheral Tissues". United States. https://doi.org/10.1210/me.2015-1161. https://www.osti.gov/servlets/purl/1336593.
@article{osti_1336593,
title = {Structural and Functional Evidence for Testosterone Activation of GPRC6A in Peripheral Tissues},
author = {Pi, Min and Kapoor, Karan and Wu, Yunpeng and Ye, Ruisong and Senogles, Susan and Nishimoto, Satoru Kenneth and Hwang, Dong-Jin and Miller, Duane and Narayanan, Ramesh and Smith, Jeremy C. and Baudry, Jerome and Quarles, Leigh Darryl},
abstractNote = {G protein-coupled receptor (GPCR) family C group 6 member A (GPRC6A) is a multiligand GPCR that is activated by cations, L-amino acids, and osteocalcin. GPRC6A plays an important role in the regulation of testosterone (T) production and energy metabolism in mice. T has rapid, transcription-independent (nongenomic) effects that are mediated by a putative GPCR. We previously found that T can activate GPRC6A in vitro, but the possibility that T is a ligand for GPRC6A remains controversial. Here, we demonstrate direct T binding to GPRC6A and construct computational structural models of GPRC6A that are used to identify potential binding poses of T. Mutations of the predicted binding site residues were experimentally found to block T activation of GPRC6A, in agreement with the modeling. Using Gpr6ca(-/-) mice, we confirmed that loss of GPRC6A resulted in loss of T rapid signaling responses and elucidated several biological functions regulated by GPRC6A-dependent T rapid signaling, including T stimulation of insulin secretion in pancreatic islets and enzyme expression involved in the biosynthesis of T in Leydig cells. Finally, we identified a stereo-specific effect of an R-isomer of a selective androgen receptor modulator that is predicted to bind to and shown to activate GPRC6A but not androgen receptor. Together, our data show that GPRC6A directly mediates the rapid signaling response to T and uncovers previously unrecognized endocrine networks.},
doi = {10.1210/me.2015-1161},
journal = {Molecular Endocrinology},
number = 12,
volume = 29,
place = {United States},
year = {Thu Jan 01 00:00:00 EST 2015},
month = {Thu Jan 01 00:00:00 EST 2015}
}
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