Signaling by intracellular β2-adrenergic receptors regulates AMPA receptor trafficking and synaptic plasticity

Summary: Signaling by norepinephrine (NE) via adrenergic receptors (ARs) mediates attention, yet the underlying molecular mechanisms are largely unknown. AMPA receptors (AMPARs) form a complex with β2ARs, Gs, adenylyl cyclase, and protein kinase A (PKA) to augment AMPAR phosphorylation and, thereby,...

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Main Authors: Boram Lee, Xiaomin Xing, Erik A. Hammes, Zhuoer Zeng, Zoila M. Estrada-Tobar, Karam Kim, Kyle E. Ireton, Kwun Nok Mimi Man, Ariel A. Jacobi, Ruben A. Berumen, Justin C. Weiner, Ao Shen, Bing Xu, Joanne Wang, Paul J. Gasser, Manuel F. Navedo, Yang K. Xiang, Elva Díaz, Chao-Yin Chen, Mary C. Horne, Johannes W. Hell
Format: Article
Language:English
Published: Elsevier 2025-08-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S221112472500782X
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author Boram Lee
Xiaomin Xing
Erik A. Hammes
Zhuoer Zeng
Zoila M. Estrada-Tobar
Karam Kim
Kyle E. Ireton
Kwun Nok Mimi Man
Ariel A. Jacobi
Ruben A. Berumen
Justin C. Weiner
Ao Shen
Bing Xu
Joanne Wang
Paul J. Gasser
Manuel F. Navedo
Yang K. Xiang
Elva Díaz
Chao-Yin Chen
Mary C. Horne
Johannes W. Hell
author_facet Boram Lee
Xiaomin Xing
Erik A. Hammes
Zhuoer Zeng
Zoila M. Estrada-Tobar
Karam Kim
Kyle E. Ireton
Kwun Nok Mimi Man
Ariel A. Jacobi
Ruben A. Berumen
Justin C. Weiner
Ao Shen
Bing Xu
Joanne Wang
Paul J. Gasser
Manuel F. Navedo
Yang K. Xiang
Elva Díaz
Chao-Yin Chen
Mary C. Horne
Johannes W. Hell
author_sort Boram Lee
collection DOAJ
description Summary: Signaling by norepinephrine (NE) via adrenergic receptors (ARs) mediates attention, yet the underlying molecular mechanisms are largely unknown. AMPA receptors (AMPARs) form a complex with β2ARs, Gs, adenylyl cyclase, and protein kinase A (PKA) to augment AMPAR phosphorylation and, thereby, surface expression. We show that signaling by intracellular β2ARs is required for these effects and two different forms of long-term potentiation (LTP) that depend on β2AR signaling and phosphorylation of the AMPAR GluA1 subunit on S845. Inhibition of two NE transporters, the organic cation transporter 3 (OCT3) and the plasma membrane monoamine transporter (PMAT), impairs phosphorylation of the AMPAR GluA1 subunit on S845 by PKA, GluA1 surface insertion, both forms of LTP, and upregulation of miniature excitatory postsynaptic currents upon injection of NE into neurons. These results provide strong evidence for signaling by NE upon its transport into neurons in general and specifically in synaptic plasticity.
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spelling doaj-art-c2d07bd1704d4896b0d9cf01e5127aa82025-08-20T02:38:50ZengElsevierCell Reports2211-12472025-08-0144811601110.1016/j.celrep.2025.116011Signaling by intracellular β2-adrenergic receptors regulates AMPA receptor trafficking and synaptic plasticityBoram Lee0Xiaomin Xing1Erik A. Hammes2Zhuoer Zeng3Zoila M. Estrada-Tobar4Karam Kim5Kyle E. Ireton6Kwun Nok Mimi Man7Ariel A. Jacobi8Ruben A. Berumen9Justin C. Weiner10Ao Shen11Bing Xu12Joanne Wang13Paul J. Gasser14Manuel F. Navedo15Yang K. Xiang16Elva Díaz17Chao-Yin Chen18Mary C. Horne19Johannes W. Hell20Department of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USA; VA Northern California Health Care System, Mather, CA 95655, USADepartment of Pharmaceutics, University of Washington, Seattle, WA 98195-7280, USADepartment of Biomedical Sciences, Marquette University, Milwaukee, WI 53201-1881, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USA; VA Northern California Health Care System, Mather, CA 95655, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USADepartment of Pharmacology, University of California, Davis, Davis, CA 95616-8636, USA; Corresponding authorSummary: Signaling by norepinephrine (NE) via adrenergic receptors (ARs) mediates attention, yet the underlying molecular mechanisms are largely unknown. AMPA receptors (AMPARs) form a complex with β2ARs, Gs, adenylyl cyclase, and protein kinase A (PKA) to augment AMPAR phosphorylation and, thereby, surface expression. We show that signaling by intracellular β2ARs is required for these effects and two different forms of long-term potentiation (LTP) that depend on β2AR signaling and phosphorylation of the AMPAR GluA1 subunit on S845. Inhibition of two NE transporters, the organic cation transporter 3 (OCT3) and the plasma membrane monoamine transporter (PMAT), impairs phosphorylation of the AMPAR GluA1 subunit on S845 by PKA, GluA1 surface insertion, both forms of LTP, and upregulation of miniature excitatory postsynaptic currents upon injection of NE into neurons. These results provide strong evidence for signaling by NE upon its transport into neurons in general and specifically in synaptic plasticity.http://www.sciencedirect.com/science/article/pii/S221112472500782XCP: NeuroscienceCP: Cell biology
spellingShingle Boram Lee
Xiaomin Xing
Erik A. Hammes
Zhuoer Zeng
Zoila M. Estrada-Tobar
Karam Kim
Kyle E. Ireton
Kwun Nok Mimi Man
Ariel A. Jacobi
Ruben A. Berumen
Justin C. Weiner
Ao Shen
Bing Xu
Joanne Wang
Paul J. Gasser
Manuel F. Navedo
Yang K. Xiang
Elva Díaz
Chao-Yin Chen
Mary C. Horne
Johannes W. Hell
Signaling by intracellular β2-adrenergic receptors regulates AMPA receptor trafficking and synaptic plasticity
Cell Reports
CP: Neuroscience
CP: Cell biology
title Signaling by intracellular β2-adrenergic receptors regulates AMPA receptor trafficking and synaptic plasticity
title_full Signaling by intracellular β2-adrenergic receptors regulates AMPA receptor trafficking and synaptic plasticity
title_fullStr Signaling by intracellular β2-adrenergic receptors regulates AMPA receptor trafficking and synaptic plasticity
title_full_unstemmed Signaling by intracellular β2-adrenergic receptors regulates AMPA receptor trafficking and synaptic plasticity
title_short Signaling by intracellular β2-adrenergic receptors regulates AMPA receptor trafficking and synaptic plasticity
title_sort signaling by intracellular β2 adrenergic receptors regulates ampa receptor trafficking and synaptic plasticity
topic CP: Neuroscience
CP: Cell biology
url http://www.sciencedirect.com/science/article/pii/S221112472500782X
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