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ER-mitochondria distance is a critical parameter for efficient mitochondrial Ca2+ uptake and oxidative metabolism

by Ladds, Graham , Filigheddu, Nicoletta , Grilli, Mariagrazia , Fresu, Luigia G , Talmon, Maria , Mikoshiba, Katsuhiko , Cavaliere, Fabio , Malecka, Justyna , Pessolano, Emanuela , Ramos-Gonzalez, Paula , Brini, Marisa , Chrostek, Gabriela , Jekabsone, Aiste , Tonelli, Elisa , Lim, Dmitry , Calì, Tito , Dematteis, Giulia , Tapella, Laura , Distasi, Carla , Genazzani, Armando A , Casali, Claudio , Ariotti, Adele , Miggiano, Riccardo , Umbrasas, Danielius , Matute, Carlos , Biggiogera, Marco , Kulkovienė, Gabrielė , Reano, Simone

in Cell Biology

2024

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ER-mitochondria distance is a critical parameter for efficient mitochondrial Ca2+ uptake and oxidative metabolism

in Cell Biology

2024

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ER-mitochondria distance is a critical parameter for efficient mitochondrial Ca2+ uptake and oxidative metabolism

in Cell Biology

2024

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Paper

ER-mitochondria distance is a critical parameter for efficient mitochondrial Ca2+ uptake and oxidative metabolism

Ladds, Graham,

Filigheddu, Nicoletta,

Grilli, Mariagrazia,

Fresu, Luigia G,

Talmon, Maria,

Mikoshiba, Katsuhiko,

Cavaliere, Fabio,

Malecka, Justyna,

Pessolano, Emanuela,

Ramos-Gonzalez, Paula,

Brini, Marisa,

Chrostek, Gabriela,

Jekabsone, Aiste,

Tonelli, Elisa,

Lim, Dmitry,

Calì, Tito,

Dematteis, Giulia,

Tapella, Laura,

Distasi, Carla,

Genazzani, Armando A,

Casali, Claudio,

Ariotti, Adele,

Miggiano, Riccardo,

Umbrasas, Danielius,

Matute, Carlos,

Biggiogera, Marco,

Kulkovienė, Gabrielė,

Reano, Simone

2024

Overview

IP3 receptor (IP3R)-mediated Ca2+ transfer at the mitochondria-endoplasmic reticulum (ER) contact sites (MERCS) drives mitochondrial Ca2+ uptake and oxidative metabolism and is linked to different pathologies, including Parkinson’s disease (PD). The dependence of Ca2+ transfer efficiency on the ER-mitochondria distance remains unexplored. Employing molecular rulers that stabilize ER-mitochondrial distances at 5 nm resolution, and using genetically-encoded Ca2+ indicators targeting the ER lumen and the sub-mitochondrial compartments, we now show that a distance of ∼20 nm is optimal for Ca2+ transfer and mitochondrial oxidative metabolism due to enrichment of IP3R at MERCS. In human iPSC-derived astrocytes from PD patients, 20 nm MERCS were specifically reduced which correlated with a reduction of mitochondrial Ca2+ uptake. Our work determines with precision the optimal distance for Ca2+ flux between ER and mitochondria and suggests a new paradigm for fine control over mitochondrial function.

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Publisher

Cold Spring Harbor Laboratory

Subject

Cell Biology