Mitochondria-localized AMPK responds to local energetics and contributes to exercise and energetic stress-induced mitophagy.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
14 09 2021
Historique:
accepted: 05 08 2021
received: 06 08 2021
entrez: 8 9 2021
pubmed: 9 9 2021
medline: 15 12 2021
Statut: ppublish

Résumé

Mitochondria form a complex, interconnected reticulum that is maintained through coordination among biogenesis, dynamic fission, and fusion and mitophagy, which are initiated in response to various cues to maintain energetic homeostasis. These cellular events, which make up mitochondrial quality control, act with remarkable spatial precision, but what governs such spatial specificity is poorly understood. Herein, we demonstrate that specific isoforms of the cellular bioenergetic sensor, 5' AMP-activated protein kinase (AMPKα1/α2/β2/γ1), are localized on the outer mitochondrial membrane, referred to as mitoAMPK, in various tissues in mice and humans. Activation of mitoAMPK varies across the reticulum in response to energetic stress, and inhibition of mitoAMPK activity attenuates exercise-induced mitophagy in skeletal muscle in vivo. Discovery of a mitochondrial pool of AMPK and its local importance for mitochondrial quality control underscores the complexity of sensing cellular energetics in vivo that has implications for targeting mitochondrial energetics for disease treatment.

Identifiants

pubmed: 34493662
pii: 2025932118
doi: 10.1073/pnas.2025932118
pmc: PMC8449344
pii:
doi:

Substances chimiques

AMPK alpha2 subunit, mouse EC 2.7.11.1
AMP-Activated Protein Kinases EC 2.7.11.31

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIAMS NIH HHS
ID : R01 AR050429
Pays : United States
Organisme : NIAMS NIH HHS
ID : R01 AR077440
Pays : United States
Organisme : NCRR NIH HHS
ID : S10 RR025616
Pays : United States
Organisme : NIA NIH HHS
ID : R00 AG057825
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG067048
Pays : United States
Organisme : NIA NIH HHS
ID : K99 AG057825
Pays : United States
Organisme : NHLBI NIH HHS
ID : R25 HL088724
Pays : United States
Organisme : Wellcome Trust
ID : 204766/Z/16/Z
Pays : United Kingdom
Organisme : NHLBI NIH HHS
ID : R01 HL136314
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : NIH HHS
ID : S10 OD016446
Pays : United States
Organisme : NHLBI NIH HHS
ID : T32 HL007284
Pays : United States

Informations de copyright

Copyright © 2021 the Author(s). Published by PNAS.

Déclaration de conflit d'intérêts

The authors declare no competing interest.

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Auteurs

Joshua C Drake (JC)

Center for Skeletal Muscle Research at Robert M. Berne Cardiovascular Research Center, University of Virginia School of Medicine, Charlottesville, VA 22908; zy3m@virginia.edu joshuacd@vt.edu.
Department of Human Nutrition, Foods, and Exercise, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061.

Rebecca J Wilson (RJ)

Center for Skeletal Muscle Research at Robert M. Berne Cardiovascular Research Center, University of Virginia School of Medicine, Charlottesville, VA 22908.
Department of Biochemistry and Molecular Genetics, University of Virginia School of Medicine, Charlottesville, VA 22908.

Rhianna C Laker (RC)

Center for Skeletal Muscle Research at Robert M. Berne Cardiovascular Research Center, University of Virginia School of Medicine, Charlottesville, VA 22908.

Yuntian Guan (Y)

Center for Skeletal Muscle Research at Robert M. Berne Cardiovascular Research Center, University of Virginia School of Medicine, Charlottesville, VA 22908.
Department of Pharmacology, University of Virginia School of Medicine, Charlottesville, VA 22908.

Hannah R Spaulding (HR)

Center for Skeletal Muscle Research at Robert M. Berne Cardiovascular Research Center, University of Virginia School of Medicine, Charlottesville, VA 22908.

Anna S Nichenko (AS)

Department of Human Nutrition, Foods, and Exercise, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061.

Wenqing Shen (W)

Center for Skeletal Muscle Research at Robert M. Berne Cardiovascular Research Center, University of Virginia School of Medicine, Charlottesville, VA 22908.

Huayu Shang (H)

Center for Skeletal Muscle Research at Robert M. Berne Cardiovascular Research Center, University of Virginia School of Medicine, Charlottesville, VA 22908.

Maya V Dorn (MV)

Center for Skeletal Muscle Research at Robert M. Berne Cardiovascular Research Center, University of Virginia School of Medicine, Charlottesville, VA 22908.

Kian Huang (K)

Center for Skeletal Muscle Research at Robert M. Berne Cardiovascular Research Center, University of Virginia School of Medicine, Charlottesville, VA 22908.

Mei Zhang (M)

Center for Skeletal Muscle Research at Robert M. Berne Cardiovascular Research Center, University of Virginia School of Medicine, Charlottesville, VA 22908.
Department of Medicine, University of Virginia School of Medicine, Charlottesville, VA 22908.

Aloka B Bandara (AB)

Department of Human Nutrition, Foods, and Exercise, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061.

Matthew H Brisendine (MH)

Department of Human Nutrition, Foods, and Exercise, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061.

Jennifer A Kashatus (JA)

Department of Microbiology, Immunology and Cancer Biology, University of Virginia School of Medicine, Charlottesville, VA 22908.

Poonam R Sharma (PR)

Department of Biomedical Engineering, University of Virginia School of Medicine, Charlottesville, VA 22908.

Alexander Young (A)

Center for Skeletal Muscle Research at Robert M. Berne Cardiovascular Research Center, University of Virginia School of Medicine, Charlottesville, VA 22908.

Jitendra Gautam (J)

Department of Nephrology, University of Virginia School of Medicine, Charlottesville, VA 22908.

Ruofan Cao (R)

W. M. Keck Center for Cellular Imaging, University of Virginia, Charlottesville, VA 22904.

Horst Wallrabe (H)

W. M. Keck Center for Cellular Imaging, University of Virginia, Charlottesville, VA 22904.
Department of Biology, University of Virginia, Charlottesville, VA 22904.

Paul A Chang (PA)

Department of Cardiothoracic Surgery, Stanford University School of Medicine, Stanford, CA 94305.

Michael Wong (M)

Department of Cardiothoracic Surgery, Stanford University School of Medicine, Stanford, CA 94305.

Eric M Desjardins (EM)

Centre for Metabolism, Obesity and Diabetes Research, Department of Medicine, McMaster University, Hamilton ON L8N 3Z5, Canada.
Department of Medicine, McMaster University, Hamilton ON L8N 3Z5, Canada.

Simon A Hawley (SA)

Division of Cell Signaling and Immunology, School of Life Sciences, University of Dundee, DD1 5EH Scotland, United Kingdom.

George J Christ (GJ)

Department of Biomedical Engineering, University of Virginia School of Medicine, Charlottesville, VA 22908.
Department of Orthopaedic Surgery, University of Virginia School of Medicine, Charlottesville, VA 22908.

David F Kashatus (DF)

Department of Microbiology, Immunology and Cancer Biology, University of Virginia School of Medicine, Charlottesville, VA 22908.

Clint L Miller (CL)

Department of Biochemistry and Molecular Genetics, University of Virginia School of Medicine, Charlottesville, VA 22908.
Department of Biomedical Engineering, University of Virginia School of Medicine, Charlottesville, VA 22908.
Department of Public Health Sciences, University of Virginia School of Medicine, Charlottesville, VA 22908.
Center for Public Health Genomics, University of Virginia School of Medicine, Charlottesville, VA 22908.

Matthew J Wolf (MJ)

Center for Skeletal Muscle Research at Robert M. Berne Cardiovascular Research Center, University of Virginia School of Medicine, Charlottesville, VA 22908.
Department of Medicine, University of Virginia School of Medicine, Charlottesville, VA 22908.

Ammasi Periasamy (A)

W. M. Keck Center for Cellular Imaging, University of Virginia, Charlottesville, VA 22904.
Department of Biology, University of Virginia, Charlottesville, VA 22904.

Gregory R Steinberg (GR)

Centre for Metabolism, Obesity and Diabetes Research, Department of Medicine, McMaster University, Hamilton ON L8N 3Z5, Canada.
Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton ON L8N 3Z5, Canada.

D Grahame Hardie (DG)

Division of Cell Signaling and Immunology, School of Life Sciences, University of Dundee, DD1 5EH Scotland, United Kingdom.

Zhen Yan (Z)

Center for Skeletal Muscle Research at Robert M. Berne Cardiovascular Research Center, University of Virginia School of Medicine, Charlottesville, VA 22908; zy3m@virginia.edu joshuacd@vt.edu.
Department of Pharmacology, University of Virginia School of Medicine, Charlottesville, VA 22908.
Department of Medicine, University of Virginia School of Medicine, Charlottesville, VA 22908.
Department of Molecular Physiology and Biological Physics, University of Virginia School of Medicine, Charlottesville, VA 22908.

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