Mitochondrial pathways of copper neurotoxicity: focus on mitochondrial dynamics and mitophagy

Copper (Cu) is essential for brain development and function, yet its overload induces neuronal damage and contributes to neurodegeneration and other neurological disorders. Multiple studies demonstrated that Cu neurotoxicity is associated with mitochondrial dysfunction, routinely assessed by reducti...

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Main Authors: Michael Aschner, Anatoly V. Skalny, Rongzhu Lu, Airton C. Martins, Yousef Tizabi, Sergey V. Nekhoroshev, Abel Santamaria, Anton I. Sinitskiy, Alexey A. Tinkov
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-12-01
Series:Frontiers in Molecular Neuroscience
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Online Access:https://www.frontiersin.org/articles/10.3389/fnmol.2024.1504802/full
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author Michael Aschner
Anatoly V. Skalny
Anatoly V. Skalny
Anatoly V. Skalny
Rongzhu Lu
Airton C. Martins
Yousef Tizabi
Sergey V. Nekhoroshev
Abel Santamaria
Abel Santamaria
Anton I. Sinitskiy
Alexey A. Tinkov
Alexey A. Tinkov
Alexey A. Tinkov
author_facet Michael Aschner
Anatoly V. Skalny
Anatoly V. Skalny
Anatoly V. Skalny
Rongzhu Lu
Airton C. Martins
Yousef Tizabi
Sergey V. Nekhoroshev
Abel Santamaria
Abel Santamaria
Anton I. Sinitskiy
Alexey A. Tinkov
Alexey A. Tinkov
Alexey A. Tinkov
author_sort Michael Aschner
collection DOAJ
description Copper (Cu) is essential for brain development and function, yet its overload induces neuronal damage and contributes to neurodegeneration and other neurological disorders. Multiple studies demonstrated that Cu neurotoxicity is associated with mitochondrial dysfunction, routinely assessed by reduction of mitochondrial membrane potential. Nonetheless, the role of alterations of mitochondrial dynamics in brain mitochondrial dysfunction induced by Cu exposure is still debatable. Therefore, the objective of the present narrative review was to discuss the role of mitochondrial dysfunction in Cu-induced neurotoxicity with special emphasis on its influence on brain mitochondrial fusion and fission, as well as mitochondrial clearance by mitophagy. Existing data demonstrate that, in addition to mitochondrial electron transport chain inhibition, membrane damage, and mitochondrial reactive oxygen species (ROS) overproduction, Cu overexposure inhibits mitochondrial fusion by down-regulation of Opa1, Mfn1, and Mfn2 expression, while promoting mitochondrial fission through up-regulation of Drp1. It has been also demonstrated that Cu exposure induces PINK1/Parkin-dependent mitophagy in brain cells, that is considered a compensatory response to Cu-induced mitochondrial dysfunction. However, long-term high-dose Cu exposure impairs mitophagy, resulting in accumulation of dysfunctional mitochondria. Cu-induced inhibition of mitochondrial biogenesis due to down-regulation of PGC-1α further aggravates mitochondrial dysfunction in brain. Studies from non-brain cells corroborate these findings, also offering additional evidence that dysregulation of mitochondrial dynamics and mitophagy may be involved in Cu-induced damage in brain. Finally, Cu exposure induces cuproptosis in brain cells due mitochondrial proteotoxic stress, that may also contribute to neuronal damage and pathogenesis of certain brain diseases. Based on these findings, it is assumed that development of mitoprotective agents, specifically targeting mechanisms of mitochondrial quality control, would be useful for prevention of neurotoxic effects of Cu overload.
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spelling doaj-art-fbc937a95d8b45a780b9ee0ca974fe862025-08-20T02:18:57ZengFrontiers Media S.A.Frontiers in Molecular Neuroscience1662-50992024-12-011710.3389/fnmol.2024.15048021504802Mitochondrial pathways of copper neurotoxicity: focus on mitochondrial dynamics and mitophagyMichael Aschner0Anatoly V. Skalny1Anatoly V. Skalny2Anatoly V. Skalny3Rongzhu Lu4Airton C. Martins5Yousef Tizabi6Sergey V. Nekhoroshev7Abel Santamaria8Abel Santamaria9Anton I. Sinitskiy10Alexey A. Tinkov11Alexey A. Tinkov12Alexey A. Tinkov13Department of Molecular Pharmacology, Albert Einstein College of Medicine, Bronx, NY, United StatesInstitute of Bioelementology, Orenburg State University, Orenburg, RussiaCenter of Bioelementology and Human Ecology, IM Sechenov First Moscow State Medical University (Sechenov University), Moscow, RussiaDepartment of Medical Elementology, Peoples’ Friendship University of Russia (RUDN University), Moscow, RussiaDepartment of Preventive Medicine and Public Health Laboratory Science, School of Medicine, Jiangsu University, Zhenjiang, ChinaDepartment of Molecular Pharmacology, Albert Einstein College of Medicine, Bronx, NY, United StatesDepartment of Pharmacology, Howard University College of Medicine, Washington, DC, United StatesProblem Research Laboratory, Khanty-Mansiysk State Medical Academy, Khanty-Mansiysk, RussiaFacultad de Ciencias, Universidad Nacional Autónoma de México, Mexico City, MexicoLaboratorio de Nanotecnología y Nanomedicina, Departamento de Atención a la Salud, Universidad Autónoma Metropolitana-Xochimilco, Mexico City, Mexico0Department of Biochemistry, South Ural State Medical University, Chelyabinsk, RussiaInstitute of Bioelementology, Orenburg State University, Orenburg, RussiaCenter of Bioelementology and Human Ecology, IM Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia1Laboratory of Ecobiomonitoring and Quality Control and Department of Physical Education, Yaroslavl State University, Yaroslavl, RussiaCopper (Cu) is essential for brain development and function, yet its overload induces neuronal damage and contributes to neurodegeneration and other neurological disorders. Multiple studies demonstrated that Cu neurotoxicity is associated with mitochondrial dysfunction, routinely assessed by reduction of mitochondrial membrane potential. Nonetheless, the role of alterations of mitochondrial dynamics in brain mitochondrial dysfunction induced by Cu exposure is still debatable. Therefore, the objective of the present narrative review was to discuss the role of mitochondrial dysfunction in Cu-induced neurotoxicity with special emphasis on its influence on brain mitochondrial fusion and fission, as well as mitochondrial clearance by mitophagy. Existing data demonstrate that, in addition to mitochondrial electron transport chain inhibition, membrane damage, and mitochondrial reactive oxygen species (ROS) overproduction, Cu overexposure inhibits mitochondrial fusion by down-regulation of Opa1, Mfn1, and Mfn2 expression, while promoting mitochondrial fission through up-regulation of Drp1. It has been also demonstrated that Cu exposure induces PINK1/Parkin-dependent mitophagy in brain cells, that is considered a compensatory response to Cu-induced mitochondrial dysfunction. However, long-term high-dose Cu exposure impairs mitophagy, resulting in accumulation of dysfunctional mitochondria. Cu-induced inhibition of mitochondrial biogenesis due to down-regulation of PGC-1α further aggravates mitochondrial dysfunction in brain. Studies from non-brain cells corroborate these findings, also offering additional evidence that dysregulation of mitochondrial dynamics and mitophagy may be involved in Cu-induced damage in brain. Finally, Cu exposure induces cuproptosis in brain cells due mitochondrial proteotoxic stress, that may also contribute to neuronal damage and pathogenesis of certain brain diseases. Based on these findings, it is assumed that development of mitoprotective agents, specifically targeting mechanisms of mitochondrial quality control, would be useful for prevention of neurotoxic effects of Cu overload.https://www.frontiersin.org/articles/10.3389/fnmol.2024.1504802/fullcoppermitophagymitochondrial fusionfissioncuproptosis
spellingShingle Michael Aschner
Anatoly V. Skalny
Anatoly V. Skalny
Anatoly V. Skalny
Rongzhu Lu
Airton C. Martins
Yousef Tizabi
Sergey V. Nekhoroshev
Abel Santamaria
Abel Santamaria
Anton I. Sinitskiy
Alexey A. Tinkov
Alexey A. Tinkov
Alexey A. Tinkov
Mitochondrial pathways of copper neurotoxicity: focus on mitochondrial dynamics and mitophagy
Frontiers in Molecular Neuroscience
copper
mitophagy
mitochondrial fusion
fission
cuproptosis
title Mitochondrial pathways of copper neurotoxicity: focus on mitochondrial dynamics and mitophagy
title_full Mitochondrial pathways of copper neurotoxicity: focus on mitochondrial dynamics and mitophagy
title_fullStr Mitochondrial pathways of copper neurotoxicity: focus on mitochondrial dynamics and mitophagy
title_full_unstemmed Mitochondrial pathways of copper neurotoxicity: focus on mitochondrial dynamics and mitophagy
title_short Mitochondrial pathways of copper neurotoxicity: focus on mitochondrial dynamics and mitophagy
title_sort mitochondrial pathways of copper neurotoxicity focus on mitochondrial dynamics and mitophagy
topic copper
mitophagy
mitochondrial fusion
fission
cuproptosis
url https://www.frontiersin.org/articles/10.3389/fnmol.2024.1504802/full
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