Glial Lipid Droplets and ROS Induced by Mitochondrial Defects Promote Neurodegeneration

Reactive oxygen species (ROS) and mitochondrial defects in neurons are implicated in neurodegenerative disease. Here, we find that a key consequence of ROS and neuronal mitochondrial dysfunction is the accumulation of lipid droplets (LD) in glia. In Drosophila, ROS triggers c-Jun-N-terminal Kinase (...

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Published in	Cell Vol. 160; no. 1-2; pp. 177 - 190
Main Authors	Liu, Lucy, Zhang, Ke, Sandoval, Hector, Yamamoto, Shinya, Jaiswal, Manish, Sanz, Elisenda, Li, Zhihong, Hui, Jessica, Graham, Brett H., Quintana, Albert, Bellen, Hugo J.
Format	Journal Article
Language	English
Published	United States Elsevier Inc 15.01.2015
Subjects	Animals binding proteins carboxylic ester hydrolases droplets Drosophila Electron Transport Complex I - genetics Electron Transport Complex I - metabolism Lipid Droplets - metabolism lipid peroxidation lipids MAP Kinase Kinase 4 - metabolism Mice Mice, Knockout mitochondria Mitochondria - metabolism mitogen-activated protein kinase mutants neurodegenerative diseases Neurodegenerative Diseases - metabolism Neurodegenerative Diseases - pathology Neuroglia - metabolism Neuroglia - pathology neurons Neurons - pathology reactive oxygen species Reactive Oxygen Species - metabolism Sterol Regulatory Element Binding Proteins - metabolism
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Abstract	Reactive oxygen species (ROS) and mitochondrial defects in neurons are implicated in neurodegenerative disease. Here, we find that a key consequence of ROS and neuronal mitochondrial dysfunction is the accumulation of lipid droplets (LD) in glia. In Drosophila, ROS triggers c-Jun-N-terminal Kinase (JNK) and Sterol Regulatory Element Binding Protein (SREBP) activity in neurons leading to LD accumulation in glia prior to or at the onset of neurodegeneration. The accumulated lipids are peroxidated in the presence of ROS. Reducing LD accumulation in glia and lipid peroxidation via targeted lipase overexpression and/or lowering ROS significantly delays the onset of neurodegeneration. Furthermore, a similar pathway leads to glial LD accumulation in Ndufs4 mutant mice with neuronal mitochondrial defects, suggesting that LD accumulation following mitochondrial dysfunction is an evolutionarily conserved phenomenon, and represents an early, transient indicator and promoter of neurodegenerative disease. [Display omitted] •Lipid droplets (LD) are transient and occur prior to neurodegeneration in flies and mice•LD are present in glia and induced by neuronal increase of ROS, JNK, and SREBP•Reduction of ROS by antioxidants, lipases, or lower JNK or SREBP, delay degeneration•Neurodegeneration in mice with ROS/lipid droplets can be delayed with antioxidants Lipid droplet accumulation in glial cells, driven by mitochondrial defects and ROS in neurons, contribute to neurodegeneration in a Drosophila model, with evidence of a conserved mechanism in mice.
AbstractList	Reactive oxygen species (ROS) and mitochondrial defects in neurons are implicated in neurodegenerative disease. Here, we find that a key consequence of ROS and neuronal mitochondrial dysfunction is the accumulation of lipid droplets (LD) in glia. In Drosophila, ROS triggers c-Jun-N-terminal Kinase (JNK) and Sterol Regulatory Element Binding Protein (SREBP) activity in neurons leading to LD accumulation in glia prior to or at the onset of neurodegeneration. The accumulated lipids are peroxidated in the presence of ROS. Reducing LD accumulation in glia and lipid peroxidation via targeted lipase overexpression and/or lowering ROS significantly delays the onset of neurodegeneration. Furthermore, a similar pathway leads to glial LD accumulation in Ndufs4 mutant mice with neuronal mitochondrial defects, suggesting that LD accumulation following mitochondrial dysfunction is an evolutionarily conserved phenomenon, and represents an early, transient indicator and promoter of neurodegenerative disease.Reactive oxygen species (ROS) and mitochondrial defects in neurons are implicated in neurodegenerative disease. Here, we find that a key consequence of ROS and neuronal mitochondrial dysfunction is the accumulation of lipid droplets (LD) in glia. In Drosophila, ROS triggers c-Jun-N-terminal Kinase (JNK) and Sterol Regulatory Element Binding Protein (SREBP) activity in neurons leading to LD accumulation in glia prior to or at the onset of neurodegeneration. The accumulated lipids are peroxidated in the presence of ROS. Reducing LD accumulation in glia and lipid peroxidation via targeted lipase overexpression and/or lowering ROS significantly delays the onset of neurodegeneration. Furthermore, a similar pathway leads to glial LD accumulation in Ndufs4 mutant mice with neuronal mitochondrial defects, suggesting that LD accumulation following mitochondrial dysfunction is an evolutionarily conserved phenomenon, and represents an early, transient indicator and promoter of neurodegenerative disease. Reactive oxygen species (ROS) and mitochondrial defects in neurons are implicated in neurodegenerative disease. Here, we find that a key consequence of ROS and neuronal mitochondrial dysfunction is the accumulation of lipid droplets (LD) in glia. In Drosophila, ROS triggers c-Jun-N-terminal Kinase (JNK) and Sterol Regulatory Element Binding Protein (SREBP) activity in neurons leading to LD accumulation in glia prior to or at the onset of neurodegeneration. The accumulated lipids are peroxidated in the presence of ROS. Reducing LD accumulation in glia and lipid peroxidation via targeted lipase overexpression and/or lowering ROS significantly delays the onset of neurodegeneration. Furthermore, a similar pathway leads to glial LD accumulation in Ndufs4 mutant mice with neuronal mitochondrial defects, suggesting that LD accumulation following mitochondrial dysfunction is an evolutionarily conserved phenomenon, and represents an early, transient indicator and promoter of neurodegenerative disease. Reactive oxygen species (ROS) and mitochondrial defects in neurons are implicated in neurodegenerative disease. Here, we find that a key consequence of ROS and neuronal mitochondrial dysfunction is the accumulation of lipid droplets (LD) in glia. In Drosophila, ROS triggers c-Jun-N-terminal Kinase (JNK) and Sterol Regulatory Element Binding Protein (SREBP) activity in neurons leading to LD accumulation in glia prior to or at the onset of neurodegeneration. The accumulated lipids are peroxidated in the presence of ROS. Reducing LD accumulation in glia and lipid peroxidation via targeted lipase overexpression and/or lowering ROS significantly delays the onset of neurodegeneration. Furthermore, a similar pathway leads to glial LD accumulation in Ndufs4 mutant mice with neuronal mitochondrial defects, suggesting that LD accumulation following mitochondrial dysfunction is an evolutionarily conserved phenomenon, and represents an early, transient indicator and promoter of neurodegenerative disease. Reactive oxygen species (ROS) and mitochondrial defects in neurons are implicated in neurodegenerative disease. Here we find that a key consequence of ROS and neuronal mitochondrial dysfunction is the accumulation of lipid droplets (LD) in glia. In Drosophila , ROS triggers c-Jun-N-terminal Kinase (JNK) and Sterol Regulatory Element Binding Protein (SREBP) activity in neurons leading to LD accumulation in glia prior to or at the onset of neurodegeneration. The accumulated lipids are peroxidated in the presence of ROS. Reducing LD accumulation in glia and lipid peroxidation via targeted lipase overexpression and/or lowering ROS significantly delays the onset of neurodegeneration. Furthermore, a similar pathway leads to glial LD accumulation in Ndufs4 mutant mice with neuronal mitochondrial defects, suggesting that LD accumulation following mitochondrial dysfunction is an evolutionarily conserved phenomenon, and represents an early, transient indicator and promoter of neurodegenerative disease. Reactive oxygen species (ROS) and mitochondrial defects in neurons are implicated in neurodegenerative disease. Here, we find that a key consequence of ROS and neuronal mitochondrial dysfunction is the accumulation of lipid droplets (LD) in glia. In Drosophila, ROS triggers c-Jun-N-terminal Kinase (JNK) and Sterol Regulatory Element Binding Protein (SREBP) activity in neurons leading to LD accumulation in glia prior to or at the onset of neurodegeneration. The accumulated lipids are peroxidated in the presence of ROS. Reducing LD accumulation in glia and lipid peroxidation via targeted lipase overexpression and/or lowering ROS significantly delays the onset of neurodegeneration. Furthermore, a similar pathway leads to glial LD accumulation in Ndufs4 mutant mice with neuronal mitochondrial defects, suggesting that LD accumulation following mitochondrial dysfunction is an evolutionarily conserved phenomenon, and represents an early, transient indicator and promoter of neurodegenerative disease. [Display omitted] •Lipid droplets (LD) are transient and occur prior to neurodegeneration in flies and mice•LD are present in glia and induced by neuronal increase of ROS, JNK, and SREBP•Reduction of ROS by antioxidants, lipases, or lower JNK or SREBP, delay degeneration•Neurodegeneration in mice with ROS/lipid droplets can be delayed with antioxidants Lipid droplet accumulation in glial cells, driven by mitochondrial defects and ROS in neurons, contribute to neurodegeneration in a Drosophila model, with evidence of a conserved mechanism in mice.
Author	Zhang, Ke Graham, Brett H. Quintana, Albert Jaiswal, Manish Li, Zhihong Sanz, Elisenda Sandoval, Hector Yamamoto, Shinya Hui, Jessica Liu, Lucy Bellen, Hugo J.
AuthorAffiliation	1 Department of Neuroscience, Baylor College of Medicine 6 Howard Hughes Medical Institute, Baylor College of Medicine, Houston, TX 77030, USA 8 Center for Developmental Therapeutics, University of Washington, Seattle, WA, 98195, USA 3 Department of Molecular and Human Genetics, Baylor College of Medicine Department of Neurology, Johns Hopkins University School of Medicine 4 Program in Developmental Biology, Baylor College of Medicine 2 Structural and Computational Biology & Molecular Biophysics Graduate Program, Baylor College of Medicine 5 Jan and Dan Duncan Neurological Research Institute at Texas Children’s Hospital, Houston, TX 77030 7 Center for Integrative Brain Research, Seattle Children’s Research Institute 9 Department of Pediatrics, University of Washington, Seattle, WA, 98195, USA
AuthorAffiliation_xml	– name: 3 Department of Molecular and Human Genetics, Baylor College of Medicine – name: 1 Department of Neuroscience, Baylor College of Medicine – name: 7 Center for Integrative Brain Research, Seattle Children’s Research Institute – name: 6 Howard Hughes Medical Institute, Baylor College of Medicine, Houston, TX 77030, USA – name: 5 Jan and Dan Duncan Neurological Research Institute at Texas Children’s Hospital, Houston, TX 77030 – name: 9 Department of Pediatrics, University of Washington, Seattle, WA, 98195, USA – name: Department of Neurology, Johns Hopkins University School of Medicine – name: 8 Center for Developmental Therapeutics, University of Washington, Seattle, WA, 98195, USA – name: 4 Program in Developmental Biology, Baylor College of Medicine – name: 2 Structural and Computational Biology & Molecular Biophysics Graduate Program, Baylor College of Medicine
Author_xml	– sequence: 1 givenname: Lucy surname: Liu fullname: Liu, Lucy organization: Department of Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA – sequence: 2 givenname: Ke surname: Zhang fullname: Zhang, Ke organization: Structural and Computational Biology & Molecular Biophysics Graduate Program, Baylor College of Medicine, Houston, TX 77030, USA – sequence: 3 givenname: Hector surname: Sandoval fullname: Sandoval, Hector organization: Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA – sequence: 4 givenname: Shinya surname: Yamamoto fullname: Yamamoto, Shinya organization: Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA – sequence: 5 givenname: Manish surname: Jaiswal fullname: Jaiswal, Manish organization: Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA – sequence: 6 givenname: Elisenda surname: Sanz fullname: Sanz, Elisenda organization: Center for Integrative Brain Research, Seattle Children’s Research Institute, Seattle, WA 98101, USA – sequence: 7 givenname: Zhihong surname: Li fullname: Li, Zhihong organization: Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA – sequence: 8 givenname: Jessica surname: Hui fullname: Hui, Jessica organization: Center for Developmental Therapeutics, University of Washington, Seattle, WA, 98195, USA – sequence: 9 givenname: Brett H. surname: Graham fullname: Graham, Brett H. organization: Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA – sequence: 10 givenname: Albert surname: Quintana fullname: Quintana, Albert organization: Center for Integrative Brain Research, Seattle Children’s Research Institute, Seattle, WA 98101, USA – sequence: 11 givenname: Hugo J. surname: Bellen fullname: Bellen, Hugo J. email: hbellen@bcm.edu organization: Department of Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/25594180$$D View this record in MEDLINE/PubMed
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Snippet	Reactive oxygen species (ROS) and mitochondrial defects in neurons are implicated in neurodegenerative disease. Here, we find that a key consequence of ROS and... Reactive oxygen species (ROS) and mitochondrial defects in neurons are implicated in neurodegenerative disease. Here, we find that a key consequence of ROS and... Reactive oxygen species (ROS) and mitochondrial defects in neurons are implicated in neurodegenerative disease. Here we find that a key consequence of ROS and...
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SubjectTerms	Animals binding proteins carboxylic ester hydrolases droplets Drosophila Electron Transport Complex I - genetics Electron Transport Complex I - metabolism Lipid Droplets - metabolism lipid peroxidation lipids MAP Kinase Kinase 4 - metabolism Mice Mice, Knockout mitochondria Mitochondria - metabolism mitogen-activated protein kinase mutants neurodegenerative diseases Neurodegenerative Diseases - metabolism Neurodegenerative Diseases - pathology Neuroglia - metabolism Neuroglia - pathology neurons Neurons - pathology reactive oxygen species Reactive Oxygen Species - metabolism Sterol Regulatory Element Binding Proteins - metabolism
Title	Glial Lipid Droplets and ROS Induced by Mitochondrial Defects Promote Neurodegeneration
URI	https://dx.doi.org/10.1016/j.cell.2014.12.019 https://www.ncbi.nlm.nih.gov/pubmed/25594180 https://www.proquest.com/docview/1652389217 https://www.proquest.com/docview/2000214212 https://pubmed.ncbi.nlm.nih.gov/PMC4377295
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