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Architecture of androgen receptor pathways amplifying glucagon-like peptide-1 insulinotropic action in male pancreatic β cells

Published:30 May 2023 DOI: 10.1016/j.celrep.2023.112529 PMID: 37200193
Weiwei Xu,?M M Fahd Qadir,?Daniela Nasteska,?Paula Mota de Sa,?Caroline M Gorvin,?Manuel Blandino-Rosano,?Charles R Evans,?Thuong Ho,?Evgeniy Potapenko,?Rajakrishnan Veluthakal,?Fiona B Ashford,?Stavroula Bitsi,?Jia Fan,?Manika Bhondeley,?Kejing Song,?Venkata N Sure,?Siva S V P Sakamuri,?Lina Schiffer,?Wandy Beatty,?Rachael Wyatt,?Daniel E Frigo,?Xiaowen Liu,?Prasad V Katakam,?Wiebke Arlt,?Jochen Buck,?Lonny R Levin,?Tony Hu,?Jay Kolls,?Charles F Burant,?Alejandra Tomas,?Matthew J Merrins,?Debbie C Thurmond,?Ernesto Bernal-Mizrachi,?David J Hodson,?Franck Mauvais-Jarvis

Abstract

Male mice lacking the androgen receptor (AR) in pancreatic β cells exhibit blunted glucose-stimulated insulin secretion (GSIS), leading to hyperglycemia. Testosterone activates an extranuclear AR in β cells to amplify glucagon-like peptide-1 (GLP-1) insulinotropic action. Here, we examined the architecture of AR targets that regulate GLP-1 insulinotropic action in male β cells. Testosterone cooperates with GLP-1 to enhance cAMP production at the plasma membrane and endosomes via: (1) increased mitochondrial production of CO2, activating the HCO3--sensitive soluble adenylate cyclase; and (2) increased Gαs recruitment to GLP-1 receptor and AR complexes, activating transmembrane adenylate cyclase. Additionally, testosterone enhances GSIS in human islets via a focal adhesion kinase/SRC/phosphatidylinositol 3-kinase/mammalian target of rapamycin complex 2 actin remodeling cascade. We describe the testosterone-stimulated AR interactome, transcriptome, proteome, and metabolome that contribute to these effects. This study identifies AR genomic and non-genomic actions that enhance GLP-1-stimulated insulin exocytosis in male β cells.

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