Cargo-selective regulation of clathrin-mediated endocytosis by AMP-activated protein kinase

Summary: The cell surface abundance of many proteins is controlled by clathrin-mediated endocytosis (CME). CME is driven by the assembly of clathrin and other proteins on the inner leaflet of the plasma membrane into clathrin-coated pits (CCPs). Regulation of CCP dynamics allows for control of the f...

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Main Authors: Laura A. Orofiamma, Ralph Christian Delos Santos, Ayshin Mehrabi, Nikol Leshchyshyn, Geoffrey G. Hesketh, Sadia Rahmani, Aesha Patel, Farnaz Fekri, Rehman Ata, Colin D.H. Ratcliffe, Mathieu J.F. Crupi, Lois Mulligan, Morag Park, Anne-Claude Gingras, Costin N. Antonescu
Format: Article
Language:English
Published: Elsevier 2025-08-01
Series:iScience
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Online Access:http://www.sciencedirect.com/science/article/pii/S2589004225013926
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author Laura A. Orofiamma
Ralph Christian Delos Santos
Ayshin Mehrabi
Nikol Leshchyshyn
Geoffrey G. Hesketh
Sadia Rahmani
Aesha Patel
Farnaz Fekri
Rehman Ata
Colin D.H. Ratcliffe
Mathieu J.F. Crupi
Lois Mulligan
Morag Park
Anne-Claude Gingras
Costin N. Antonescu
author_facet Laura A. Orofiamma
Ralph Christian Delos Santos
Ayshin Mehrabi
Nikol Leshchyshyn
Geoffrey G. Hesketh
Sadia Rahmani
Aesha Patel
Farnaz Fekri
Rehman Ata
Colin D.H. Ratcliffe
Mathieu J.F. Crupi
Lois Mulligan
Morag Park
Anne-Claude Gingras
Costin N. Antonescu
author_sort Laura A. Orofiamma
collection DOAJ
description Summary: The cell surface abundance of many proteins is controlled by clathrin-mediated endocytosis (CME). CME is driven by the assembly of clathrin and other proteins on the inner leaflet of the plasma membrane into clathrin-coated pits (CCPs). Regulation of CCP dynamics allows for control of the function of specific cell surface proteins, impacting a range of cellular outcomes. AMP-activated protein kinase (AMPK) becomes activated upon metabolic insufficiency and facilitates cellular adaptation to nutrient stress. Here, we examined how AMPK regulates CME and the cell surface membrane traffic of β1-integrin. We find that AMPK controls CCP dynamics and regulates the abundance of the endocytic adaptor protein Dab2 within CCPs in a manner that requires the GTPase Arf6, thus selectively promoting the CCP recruitment and internalization of β1-integrin. This study reveals a signaling pathway for cargo-selective metabolic regulation of CME by AMPK that impacts the function of cell surface proteins such as integrins.
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issn 2589-0042
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publisher Elsevier
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series iScience
spelling doaj-art-3ff72307255c4639817cfdb9b261b0132025-08-20T04:00:34ZengElsevieriScience2589-00422025-08-0128811313110.1016/j.isci.2025.113131Cargo-selective regulation of clathrin-mediated endocytosis by AMP-activated protein kinaseLaura A. Orofiamma0Ralph Christian Delos Santos1Ayshin Mehrabi2Nikol Leshchyshyn3Geoffrey G. Hesketh4Sadia Rahmani5Aesha Patel6Farnaz Fekri7Rehman Ata8Colin D.H. Ratcliffe9Mathieu J.F. Crupi10Lois Mulligan11Morag Park12Anne-Claude Gingras13Costin N. Antonescu14Department of Chemistry and Biology, Toronto Metropolitan University, Toronto, ON, Canada; Graduate Program in Molecular Science, Toronto Metropolitan University, Toronto, ON, CanadaDepartment of Chemistry and Biology, Toronto Metropolitan University, Toronto, ON, Canada; Graduate Program in Molecular Science, Toronto Metropolitan University, Toronto, ON, CanadaDepartment of Chemistry and Biology, Toronto Metropolitan University, Toronto, ON, CanadaDepartment of Chemistry and Biology, Toronto Metropolitan University, Toronto, ON, Canada; Graduate Program in Molecular Science, Toronto Metropolitan University, Toronto, ON, CanadaCentre for Systems Biology, Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON, CanadaDepartment of Chemistry and Biology, Toronto Metropolitan University, Toronto, ON, Canada; Graduate Program in Molecular Science, Toronto Metropolitan University, Toronto, ON, CanadaDepartment of Chemistry and Biology, Toronto Metropolitan University, Toronto, ON, CanadaDepartment of Chemistry and Biology, Toronto Metropolitan University, Toronto, ON, Canada; Graduate Program in Molecular Science, Toronto Metropolitan University, Toronto, ON, CanadaDepartment of Chemistry and Biology, Toronto Metropolitan University, Toronto, ON, Canada; Graduate Program in Molecular Science, Toronto Metropolitan University, Toronto, ON, CanadaDepartment of Biochemistry, McGill University, Montreal, QC, Canada; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, QC, CanadaDivision of Cancer Biology and Genetics, Sinclair Cancer Research Institute, and Department of Pathology and Molecular Medicine, Queen’s University, Kingston, ON, CanadaDivision of Cancer Biology and Genetics, Sinclair Cancer Research Institute, and Department of Pathology and Molecular Medicine, Queen’s University, Kingston, ON, CanadaDepartment of Biochemistry, McGill University, Montreal, QC, Canada; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, QC, CanadaCentre for Systems Biology, Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON, Canada; Department of Molecular Genetics, University of Toronto, Toronto, ON, CanadaDepartment of Chemistry and Biology, Toronto Metropolitan University, Toronto, ON, Canada; Graduate Program in Molecular Science, Toronto Metropolitan University, Toronto, ON, Canada; Corresponding authorSummary: The cell surface abundance of many proteins is controlled by clathrin-mediated endocytosis (CME). CME is driven by the assembly of clathrin and other proteins on the inner leaflet of the plasma membrane into clathrin-coated pits (CCPs). Regulation of CCP dynamics allows for control of the function of specific cell surface proteins, impacting a range of cellular outcomes. AMP-activated protein kinase (AMPK) becomes activated upon metabolic insufficiency and facilitates cellular adaptation to nutrient stress. Here, we examined how AMPK regulates CME and the cell surface membrane traffic of β1-integrin. We find that AMPK controls CCP dynamics and regulates the abundance of the endocytic adaptor protein Dab2 within CCPs in a manner that requires the GTPase Arf6, thus selectively promoting the CCP recruitment and internalization of β1-integrin. This study reveals a signaling pathway for cargo-selective metabolic regulation of CME by AMPK that impacts the function of cell surface proteins such as integrins.http://www.sciencedirect.com/science/article/pii/S2589004225013926BiochemistryCell biology
spellingShingle Laura A. Orofiamma
Ralph Christian Delos Santos
Ayshin Mehrabi
Nikol Leshchyshyn
Geoffrey G. Hesketh
Sadia Rahmani
Aesha Patel
Farnaz Fekri
Rehman Ata
Colin D.H. Ratcliffe
Mathieu J.F. Crupi
Lois Mulligan
Morag Park
Anne-Claude Gingras
Costin N. Antonescu
Cargo-selective regulation of clathrin-mediated endocytosis by AMP-activated protein kinase
iScience
Biochemistry
Cell biology
title Cargo-selective regulation of clathrin-mediated endocytosis by AMP-activated protein kinase
title_full Cargo-selective regulation of clathrin-mediated endocytosis by AMP-activated protein kinase
title_fullStr Cargo-selective regulation of clathrin-mediated endocytosis by AMP-activated protein kinase
title_full_unstemmed Cargo-selective regulation of clathrin-mediated endocytosis by AMP-activated protein kinase
title_short Cargo-selective regulation of clathrin-mediated endocytosis by AMP-activated protein kinase
title_sort cargo selective regulation of clathrin mediated endocytosis by amp activated protein kinase
topic Biochemistry
Cell biology
url http://www.sciencedirect.com/science/article/pii/S2589004225013926
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