The University of Southampton
University of Southampton Institutional Repository

Mitochondrial calcium uptake declines during aging and is directly activated by oleuropein to boost energy metabolism and skeletal muscle performance

Mitochondrial calcium uptake declines during aging and is directly activated by oleuropein to boost energy metabolism and skeletal muscle performance
Mitochondrial calcium uptake declines during aging and is directly activated by oleuropein to boost energy metabolism and skeletal muscle performance

Mitochondrial calcium (mtCa2+) uptake via the mitochondrial calcium uniporter (MCU) couples calcium homeostasis and energy metabolism. mtCa2+ uptake via MCU is rate-limiting for mitochondrial activation during muscle contraction, but its pathophysiological role and therapeutic application remain largely uncharacterized. By profiling human muscle biopsies, patient-derived myotubes, and preclinical models, we discovered a conserved downregulation of mitochondrial calcium uniporter regulator 1 (MCUR1) during skeletal muscle aging that associates with human sarcopenia and impairs mtCa2+ uptake and mitochondrial respiration. Through a screen of 5,000 bioactive molecules, we identify the natural polyphenol oleuropein as a specific MCU activator that stimulates mitochondrial respiration via mitochondrial calcium uptake 1 (MICU1) binding. Oleuropein activates mtCa2+ uptake and energy metabolism to enhance endurance and reduce fatigue in young and aged mice but not in muscle-specific MCU knockout (KO) mice. Our work demonstrates that impaired mtCa2+ uptake contributes to mitochondrial dysfunction during aging and establishes oleuropein as a novel food-derived molecule that specifically targets MCU to stimulate mitochondrial bioenergetics and muscle performance.

1550-4131
Gherardi, Gaia
8317ec8f-dd2b-49c1-b560-344deced9947
Weiser, Anna
d33c4244-d677-46c8-9088-9eeacd49c418
Bermont, Flavien
857332e4-48c6-4830-b16d-6a4226e156fb
Migliavacca, Eugenia
eda5ed6b-ec9d-4f00-9308-6fa2cfbad9d2
Brinon, Benjamin
984aa766-3caf-4a5d-8659-a8334fc4f056
Jacot, Guillaume E
19a4480f-f1ff-4f18-a800-b9bda002af4d
Hermant, Aurélie
a19e6e12-a1d1-4d2c-b1eb-724b6cabab23
Sturlese, Mattia
4bcc9f66-8306-4b02-84aa-27af9f5d9350
Nogara, Leonardo
ecf3ec91-6c2a-471b-8213-37ed09ee10d3
Vascon, Filippo
4215fd54-165e-471c-afab-a5c2313a6948
De Mario, Agnese
aa7ced61-f965-462b-b3ce-0c8a25ceb4ce
Mattarei, Andrea
265445cf-6afc-4143-a4f0-5d500f3559d8
Garratt, Emma
51598847-7206-4945-89cb-d495e99659f3
Burton, Mark
250319ad-90dc-4651-b118-d5dbe5eaafa6
Lillycrop, Karen
eeaaa78d-0c4d-4033-a178-60ce7345a2cc
Godfrey, Keith M.
0931701e-fe2c-44b5-8f0d-ec5c7477a6fd
Cendron, Laura
cfafef5e-0af3-4815-b8a2-f6f9e0a7ef99
Barron, Denis
45159d53-d83f-4bdf-9a7d-2392b7c39ad5
Moro, Stefano
f0487234-9165-4386-94d7-0f767d26b959
Blaauw, Bert
34d8bcdf-aad7-4159-bed0-acecbed2679b
Rizzuto, Rosario
1f91fc0f-e0da-4eb7-b40f-611771269ef8
Feige, Jerome N.
ed6ba764-f562-4314-b823-c6aff0d7fa47
Mammucari, Cristina
51ccd2a8-c8c0-4d02-8380-517cddeae2fa
De Marchi, Umberto
b1ab57ae-a796-4e31-98c7-22719fd588e0
Gherardi, Gaia
8317ec8f-dd2b-49c1-b560-344deced9947
Weiser, Anna
d33c4244-d677-46c8-9088-9eeacd49c418
Bermont, Flavien
857332e4-48c6-4830-b16d-6a4226e156fb
Migliavacca, Eugenia
eda5ed6b-ec9d-4f00-9308-6fa2cfbad9d2
Brinon, Benjamin
984aa766-3caf-4a5d-8659-a8334fc4f056
Jacot, Guillaume E
19a4480f-f1ff-4f18-a800-b9bda002af4d
Hermant, Aurélie
a19e6e12-a1d1-4d2c-b1eb-724b6cabab23
Sturlese, Mattia
4bcc9f66-8306-4b02-84aa-27af9f5d9350
Nogara, Leonardo
ecf3ec91-6c2a-471b-8213-37ed09ee10d3
Vascon, Filippo
4215fd54-165e-471c-afab-a5c2313a6948
De Mario, Agnese
aa7ced61-f965-462b-b3ce-0c8a25ceb4ce
Mattarei, Andrea
265445cf-6afc-4143-a4f0-5d500f3559d8
Garratt, Emma
51598847-7206-4945-89cb-d495e99659f3
Burton, Mark
250319ad-90dc-4651-b118-d5dbe5eaafa6
Lillycrop, Karen
eeaaa78d-0c4d-4033-a178-60ce7345a2cc
Godfrey, Keith M.
0931701e-fe2c-44b5-8f0d-ec5c7477a6fd
Cendron, Laura
cfafef5e-0af3-4815-b8a2-f6f9e0a7ef99
Barron, Denis
45159d53-d83f-4bdf-9a7d-2392b7c39ad5
Moro, Stefano
f0487234-9165-4386-94d7-0f767d26b959
Blaauw, Bert
34d8bcdf-aad7-4159-bed0-acecbed2679b
Rizzuto, Rosario
1f91fc0f-e0da-4eb7-b40f-611771269ef8
Feige, Jerome N.
ed6ba764-f562-4314-b823-c6aff0d7fa47
Mammucari, Cristina
51ccd2a8-c8c0-4d02-8380-517cddeae2fa
De Marchi, Umberto
b1ab57ae-a796-4e31-98c7-22719fd588e0

Gherardi, Gaia, Weiser, Anna, Bermont, Flavien, Migliavacca, Eugenia, Brinon, Benjamin, Jacot, Guillaume E, Hermant, Aurélie, Sturlese, Mattia, Nogara, Leonardo, Vascon, Filippo, De Mario, Agnese, Mattarei, Andrea, Garratt, Emma, Burton, Mark, Lillycrop, Karen, Godfrey, Keith M., Cendron, Laura, Barron, Denis, Moro, Stefano, Blaauw, Bert, Rizzuto, Rosario, Feige, Jerome N., Mammucari, Cristina and De Marchi, Umberto (2024) Mitochondrial calcium uptake declines during aging and is directly activated by oleuropein to boost energy metabolism and skeletal muscle performance. Cell Metabolism. (doi:10.1016/j.cmet.2024.10.021).

Record type: Article

Abstract

Mitochondrial calcium (mtCa2+) uptake via the mitochondrial calcium uniporter (MCU) couples calcium homeostasis and energy metabolism. mtCa2+ uptake via MCU is rate-limiting for mitochondrial activation during muscle contraction, but its pathophysiological role and therapeutic application remain largely uncharacterized. By profiling human muscle biopsies, patient-derived myotubes, and preclinical models, we discovered a conserved downregulation of mitochondrial calcium uniporter regulator 1 (MCUR1) during skeletal muscle aging that associates with human sarcopenia and impairs mtCa2+ uptake and mitochondrial respiration. Through a screen of 5,000 bioactive molecules, we identify the natural polyphenol oleuropein as a specific MCU activator that stimulates mitochondrial respiration via mitochondrial calcium uptake 1 (MICU1) binding. Oleuropein activates mtCa2+ uptake and energy metabolism to enhance endurance and reduce fatigue in young and aged mice but not in muscle-specific MCU knockout (KO) mice. Our work demonstrates that impaired mtCa2+ uptake contributes to mitochondrial dysfunction during aging and establishes oleuropein as a novel food-derived molecule that specifically targets MCU to stimulate mitochondrial bioenergetics and muscle performance.

Text
1-s2.0-S1550413124004170-main - Proof
Available under License Creative Commons Attribution.
Download (4MB)

More information

Accepted/In Press date: 23 October 2024
e-pub ahead of print date: 26 November 2024

Identifiers

Local EPrints ID: 496474
URI: http://eprints.soton.ac.uk/id/eprint/496474
ISSN: 1550-4131
PURE UUID: 2840929b-cec8-4bb0-b177-738c59950db4
ORCID for Mark Burton: ORCID iD orcid.org/0000-0002-7117-8151
ORCID for Karen Lillycrop: ORCID iD orcid.org/0000-0001-7350-5489
ORCID for Keith M. Godfrey: ORCID iD orcid.org/0000-0002-4643-0618

Catalogue record

Date deposited: 16 Dec 2024 17:43
Last modified: 17 Dec 2024 02:52

Export record

Altmetrics

Contributors

Author: Gaia Gherardi
Author: Anna Weiser
Author: Flavien Bermont
Author: Eugenia Migliavacca
Author: Benjamin Brinon
Author: Guillaume E Jacot
Author: Aurélie Hermant
Author: Mattia Sturlese
Author: Leonardo Nogara
Author: Filippo Vascon
Author: Agnese De Mario
Author: Andrea Mattarei
Author: Emma Garratt
Author: Mark Burton ORCID iD
Author: Karen Lillycrop ORCID iD
Author: Laura Cendron
Author: Denis Barron
Author: Stefano Moro
Author: Bert Blaauw
Author: Rosario Rizzuto
Author: Jerome N. Feige
Author: Cristina Mammucari
Author: Umberto De Marchi

Download statistics

Downloads from ePrints over the past year. Other digital versions may also be available to download e.g. from the publisher's website.

View more statistics

Atom RSS 1.0 RSS 2.0

Contact ePrints Soton: eprints@soton.ac.uk

ePrints Soton supports OAI 2.0 with a base URL of http://eprints.soton.ac.uk/cgi/oai2

This repository has been built using EPrints software, developed at the University of Southampton, but available to everyone to use.

We use cookies to ensure that we give you the best experience on our website. If you continue without changing your settings, we will assume that you are happy to receive cookies on the University of Southampton website.

×