Myosin VI drives arrestin-independent internalization and signaling of GPCRs

Abstract G protein-coupled receptor (GPCR) endocytosis is canonically associated with β-arrestins. Here, we delineate a β-arrestin-independent endocytic pathway driven by the cytoskeletal motor, myosin VI. Myosin VI engages GIPC, an adaptor protein that binds a PDZ sequence motif present at the C-te...

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Main Authors: Nishaben M. Patel, Léa Ripoll, Chloe J. Peach, Ning Ma, Emily E. Blythe, Nagarajan Vaidehi, Nigel W. Bunnett, Mark von Zastrow, Sivaraj Sivaramakrishnan
Format: Article
Language:English
Published: Nature Portfolio 2024-12-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-55053-9
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author Nishaben M. Patel
Léa Ripoll
Chloe J. Peach
Ning Ma
Emily E. Blythe
Nagarajan Vaidehi
Nigel W. Bunnett
Mark von Zastrow
Sivaraj Sivaramakrishnan
author_facet Nishaben M. Patel
Léa Ripoll
Chloe J. Peach
Ning Ma
Emily E. Blythe
Nagarajan Vaidehi
Nigel W. Bunnett
Mark von Zastrow
Sivaraj Sivaramakrishnan
author_sort Nishaben M. Patel
collection DOAJ
description Abstract G protein-coupled receptor (GPCR) endocytosis is canonically associated with β-arrestins. Here, we delineate a β-arrestin-independent endocytic pathway driven by the cytoskeletal motor, myosin VI. Myosin VI engages GIPC, an adaptor protein that binds a PDZ sequence motif present at the C-terminus of several GPCRs. Using the D2 dopamine receptor (D2R) as a prototype, we find that myosin VI regulates receptor endocytosis, spatiotemporal localization, and signaling. We find that access to the D2R C-tail for myosin VI-driven internalization is controlled by an interaction between the C-tail and the third intracellular loop of the receptor. Agonist efficacy, co-factors, and GIPC expression modulate this interaction to tune agonist trafficking. Myosin VI is differentially regulated by distinct GPCR C-tails, suggesting a mechanism to shape spatiotemporal signaling profiles in different ligand and physiological contexts. Our biophysical and structural insights may advance orthogonal therapeutic strategies for targeting GPCRs through cytoskeletal motor proteins.
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spelling doaj-art-3dee4150cd6f48cb81a29bb29098c7822025-08-20T02:31:19ZengNature PortfolioNature Communications2041-17232024-12-0115111510.1038/s41467-024-55053-9Myosin VI drives arrestin-independent internalization and signaling of GPCRsNishaben M. Patel0Léa Ripoll1Chloe J. Peach2Ning Ma3Emily E. Blythe4Nagarajan Vaidehi5Nigel W. Bunnett6Mark von Zastrow7Sivaraj Sivaramakrishnan8Department of Genetics, Cell Biology and Development, University of MinnesotaDepartment of Psychiatry and Behavioral Sciences, University of California, San FranciscoDepartment of Molecular Pathobiology, New York UniversityIrell and Manella Graduate School of Biological Sciences, Beckman Research Institute of the City of HopeDepartment of Psychiatry and Behavioral Sciences, University of California, San FranciscoIrell and Manella Graduate School of Biological Sciences, Beckman Research Institute of the City of HopeDepartment of Molecular Pathobiology, New York UniversityDepartment of Psychiatry and Behavioral Sciences, University of California, San FranciscoDepartment of Genetics, Cell Biology and Development, University of MinnesotaAbstract G protein-coupled receptor (GPCR) endocytosis is canonically associated with β-arrestins. Here, we delineate a β-arrestin-independent endocytic pathway driven by the cytoskeletal motor, myosin VI. Myosin VI engages GIPC, an adaptor protein that binds a PDZ sequence motif present at the C-terminus of several GPCRs. Using the D2 dopamine receptor (D2R) as a prototype, we find that myosin VI regulates receptor endocytosis, spatiotemporal localization, and signaling. We find that access to the D2R C-tail for myosin VI-driven internalization is controlled by an interaction between the C-tail and the third intracellular loop of the receptor. Agonist efficacy, co-factors, and GIPC expression modulate this interaction to tune agonist trafficking. Myosin VI is differentially regulated by distinct GPCR C-tails, suggesting a mechanism to shape spatiotemporal signaling profiles in different ligand and physiological contexts. Our biophysical and structural insights may advance orthogonal therapeutic strategies for targeting GPCRs through cytoskeletal motor proteins.https://doi.org/10.1038/s41467-024-55053-9
spellingShingle Nishaben M. Patel
Léa Ripoll
Chloe J. Peach
Ning Ma
Emily E. Blythe
Nagarajan Vaidehi
Nigel W. Bunnett
Mark von Zastrow
Sivaraj Sivaramakrishnan
Myosin VI drives arrestin-independent internalization and signaling of GPCRs
Nature Communications
title Myosin VI drives arrestin-independent internalization and signaling of GPCRs
title_full Myosin VI drives arrestin-independent internalization and signaling of GPCRs
title_fullStr Myosin VI drives arrestin-independent internalization and signaling of GPCRs
title_full_unstemmed Myosin VI drives arrestin-independent internalization and signaling of GPCRs
title_short Myosin VI drives arrestin-independent internalization and signaling of GPCRs
title_sort myosin vi drives arrestin independent internalization and signaling of gpcrs
url https://doi.org/10.1038/s41467-024-55053-9
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