Disruption of Mitophagy Flux through the PARL-PINK1 Pathway by CHCHD10 Mutations or CHCHD10 Depletion
Coiled-coil-helix-coiled-coil-helix domain-containing 10 (CHCHD10) is a nuclear-encoded mitochondrial protein which is primarily mutated in the spectrum of familial and sporadic amyotrophic lateral sclerosis (ALS)-frontotemporal dementia (FTD). Endogenous CHCHD10 levels decline in the brains of ALS-...
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Published in | Cells (Basel, Switzerland) Vol. 12; no. 24; p. 2781 |
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Format | Journal Article |
Language | English |
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Abstract | Coiled-coil-helix-coiled-coil-helix domain-containing 10 (CHCHD10) is a nuclear-encoded mitochondrial protein which is primarily mutated in the spectrum of familial and sporadic amyotrophic lateral sclerosis (ALS)-frontotemporal dementia (FTD). Endogenous CHCHD10 levels decline in the brains of ALS-FTD patients, and the CHCHD10
mutation in
induces dominant toxicity together with PTEN-induced kinase 1 (PINK1), a protein critical for the induction of mitophagy. However, whether and how CHCHD10 variants regulate mitophagy flux in the mammalian brain is unknown. Here, we demonstrate through in vivo and in vitro models, as well as human FTD brain tissue, that ALS/FTD-linked CHCHD10 mutations (R15L and S59L) impair mitophagy flux and mitochondrial Parkin recruitment, whereas wild-type CHCHD10 (CHCHD10
) normally enhances these measures. Specifically, we show that CHCHD10
and CHCHD10
mutations reduce PINK1 levels by increasing PARL activity, whereas CHCHD10
produces the opposite results through its stronger interaction with PARL, suppressing its activity. Importantly, we also demonstrate that FTD brains with TAR DNA-binding protein-43 (TDP-43) pathology demonstrate disruption of the PARL-PINK1 pathway and that experimentally impairing mitophagy promotes TDP-43 aggregation. Thus, we provide herein new insights into the regulation of mitophagy and TDP-43 aggregation in the mammalian brain through the CHCHD10-PARL-PINK1 pathway. |
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AbstractList | Coiled-coil-helix-coiled-coil-helix domain-containing 10 (CHCHD10) is a nuclear-encoded mitochondrial protein which is primarily mutated in the spectrum of familial and sporadic amyotrophic lateral sclerosis (ALS)-frontotemporal dementia (FTD). Endogenous CHCHD10 levels decline in the brains of ALS-FTD patients, and the CHCHD10
mutation in
induces dominant toxicity together with PTEN-induced kinase 1 (PINK1), a protein critical for the induction of mitophagy. However, whether and how CHCHD10 variants regulate mitophagy flux in the mammalian brain is unknown. Here, we demonstrate through in vivo and in vitro models, as well as human FTD brain tissue, that ALS/FTD-linked CHCHD10 mutations (R15L and S59L) impair mitophagy flux and mitochondrial Parkin recruitment, whereas wild-type CHCHD10 (CHCHD10
) normally enhances these measures. Specifically, we show that CHCHD10
and CHCHD10
mutations reduce PINK1 levels by increasing PARL activity, whereas CHCHD10
produces the opposite results through its stronger interaction with PARL, suppressing its activity. Importantly, we also demonstrate that FTD brains with TAR DNA-binding protein-43 (TDP-43) pathology demonstrate disruption of the PARL-PINK1 pathway and that experimentally impairing mitophagy promotes TDP-43 aggregation. Thus, we provide herein new insights into the regulation of mitophagy and TDP-43 aggregation in the mammalian brain through the CHCHD10-PARL-PINK1 pathway. Coiled-coil-helix-coiled-coil-helix domain-containing 10 (CHCHD10) is a nuclear-encoded mitochondrial protein which is primarily mutated in the spectrum of familial and sporadic amyotrophic lateral sclerosis (ALS)–frontotemporal dementia (FTD). Endogenous CHCHD10 levels decline in the brains of ALS–FTD patients, and the CHCHD10S59L mutation in Drosophila induces dominant toxicity together with PTEN-induced kinase 1 (PINK1), a protein critical for the induction of mitophagy. However, whether and how CHCHD10 variants regulate mitophagy flux in the mammalian brain is unknown. Here, we demonstrate through in vivo and in vitro models, as well as human FTD brain tissue, that ALS/FTD-linked CHCHD10 mutations (R15L and S59L) impair mitophagy flux and mitochondrial Parkin recruitment, whereas wild-type CHCHD10 (CHCHD10WT) normally enhances these measures. Specifically, we show that CHCHD10R15L and CHCHD10S59L mutations reduce PINK1 levels by increasing PARL activity, whereas CHCHD10WT produces the opposite results through its stronger interaction with PARL, suppressing its activity. Importantly, we also demonstrate that FTD brains with TAR DNA-binding protein-43 (TDP-43) pathology demonstrate disruption of the PARL–PINK1 pathway and that experimentally impairing mitophagy promotes TDP-43 aggregation. Thus, we provide herein new insights into the regulation of mitophagy and TDP-43 aggregation in the mammalian brain through the CHCHD10–PARL–PINK1 pathway. Coiled-coil-helix-coiled-coil-helix domain-containing 10 (CHCHD10) is a nuclear-encoded mitochondrial protein which is primarily mutated in the spectrum of familial and sporadic amyotrophic lateral sclerosis (ALS)–frontotemporal dementia (FTD). Endogenous CHCHD10 levels decline in the brains of ALS–FTD patients, and the CHCHD10[sup.S59L] mutation in Drosophila induces dominant toxicity together with PTEN-induced kinase 1 (PINK1), a protein critical for the induction of mitophagy. However, whether and how CHCHD10 variants regulate mitophagy flux in the mammalian brain is unknown. Here, we demonstrate through in vivo and in vitro models, as well as human FTD brain tissue, that ALS/FTD-linked CHCHD10 mutations (R15L and S59L) impair mitophagy flux and mitochondrial Parkin recruitment, whereas wild-type CHCHD10 (CHCHD10[sup.WT] ) normally enhances these measures. Specifically, we show that CHCHD10[sup.R15L] and CHCHD10[sup.S59L] mutations reduce PINK1 levels by increasing PARL activity, whereas CHCHD10[sup.WT] produces the opposite results through its stronger interaction with PARL, suppressing its activity. Importantly, we also demonstrate that FTD brains with TAR DNA-binding protein-43 (TDP-43) pathology demonstrate disruption of the PARL–PINK1 pathway and that experimentally impairing mitophagy promotes TDP-43 aggregation. Thus, we provide herein new insights into the regulation of mitophagy and TDP-43 aggregation in the mammalian brain through the CHCHD10–PARL–PINK1 pathway. |
Audience | Academic |
Author | Zhu, Zexi Ermekbaeva, Aizara Kee, Teresa R Kumaraguru, Pavan Gorthi, Viraj Bukhari, Mohammed Zaheen Woo, Jung-A Alexa Wetzel, Liam Yan, Yan Liu, Tian Kang, David E Jeon, Hanna |
Author_xml | – sequence: 1 givenname: Tian surname: Liu fullname: Liu, Tian organization: Department of Pathology, School of Medicine, Case Western Reserve University, Cleveland, OH 44106, USA – sequence: 2 givenname: Liam surname: Wetzel fullname: Wetzel, Liam organization: Department of Pathology, School of Medicine, Case Western Reserve University, Cleveland, OH 44106, USA – sequence: 3 givenname: Zexi surname: Zhu fullname: Zhu, Zexi organization: Department of Pathology, School of Medicine, Case Western Reserve University, Cleveland, OH 44106, USA – sequence: 4 givenname: Pavan surname: Kumaraguru fullname: Kumaraguru, Pavan organization: Department of Pathology, School of Medicine, Case Western Reserve University, Cleveland, OH 44106, USA – sequence: 5 givenname: Viraj surname: Gorthi fullname: Gorthi, Viraj organization: Department of Pathology, School of Medicine, Case Western Reserve University, Cleveland, OH 44106, USA – sequence: 6 givenname: Yan surname: Yan fullname: Yan, Yan organization: Byrd Alzheimer's Center & Research Institute, Department of Molecular Medicine, USF Health Morsani College of Medicine, Tampa, FL 33613, USA – sequence: 7 givenname: Mohammed Zaheen surname: Bukhari fullname: Bukhari, Mohammed Zaheen organization: Byrd Alzheimer's Center & Research Institute, Department of Molecular Medicine, USF Health Morsani College of Medicine, Tampa, FL 33613, USA – sequence: 8 givenname: Aizara surname: Ermekbaeva fullname: Ermekbaeva, Aizara organization: Byrd Alzheimer's Center & Research Institute, Department of Molecular Medicine, USF Health Morsani College of Medicine, Tampa, FL 33613, USA – sequence: 9 givenname: Hanna surname: Jeon fullname: Jeon, Hanna organization: Department of Pathology, School of Medicine, Case Western Reserve University, Cleveland, OH 44106, USA – sequence: 10 givenname: Teresa R orcidid: 0000-0003-4140-6341 surname: Kee fullname: Kee, Teresa R organization: Byrd Alzheimer's Center & Research Institute, Department of Molecular Medicine, USF Health Morsani College of Medicine, Tampa, FL 33613, USA – sequence: 11 givenname: Jung-A Alexa surname: Woo fullname: Woo, Jung-A Alexa organization: Department of Pathology, School of Medicine, Case Western Reserve University, Cleveland, OH 44106, USA – sequence: 12 givenname: David E surname: Kang fullname: Kang, David E organization: Louis Stokes Cleveland VA Medical Center, Cleveland, OH 44106, USA |
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SubjectTerms | Amyotrophic lateral sclerosis Amyotrophic Lateral Sclerosis - metabolism Analysis Animals Antibodies Autophagy (Cytology) Cellulose acetate CHCHD10 Degeneration Dementia disorders DNA binding proteins DNA-binding protein DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism Frontotemporal dementia Frontotemporal Dementia - genetics Frontotemporal Dementia - pathology Gene mutations Health aspects Humans Kinases Laboratories Mammals - metabolism Metalloproteases - genetics Mitochondria Mitochondrial Proteins - genetics Mitochondrial Proteins - metabolism Mitophagy Mitophagy - genetics Mutation Mutation - genetics Nervous system PARL PINK1 Protein Kinases - genetics Proteins PTEN protein PTEN-induced putative kinase TDP-43 Toxicity Transgenic animals |
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Title | Disruption of Mitophagy Flux through the PARL-PINK1 Pathway by CHCHD10 Mutations or CHCHD10 Depletion |
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