TDP-43 extracted from frontotemporal lobar degeneration subject brains displays distinct aggregate assemblies and neurotoxic effects reflecting disease progression rates

Accumulation of abnormally phosphorylated TDP-43 (pTDP-43) is the main pathology in affected neurons of people with amyotrophic lateral sclerosis (ALS) and frontotemporal lobar degeneration (FTLD). Morphological diversity and neuroanatomical distribution of pTDP-43 accumulations allowed classificati...

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Vydáno v:Nature neuroscience Ročník 22; číslo 1; s. 65 - 77
Hlavní autoři: Laferrière, Florent, Maniecka, Zuzanna, Pérez-Berlanga, Manuela, Hruska-Plochan, Marian, Gilhespy, Larissa, Hock, Eva-Maria, Wagner, Ulrich, Afroz, Tariq, Boersema, Paul J, Barmettler, Gery, Foti, Sandrine C, Asi, Yasmine T, Isaacs, Adrian M, Al-Amoudi, Ashraf, Lewis, Amanda, Stahlberg, Henning, Ravits, John, De Giorgi, Francesca, Ichas, François, Bezard, Erwan, Picotti, Paola, Lashley, Tammaryn, Polymenidou, Magdalini
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States Nature Publishing Group 01.01.2019
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ISSN:1097-6256, 1546-1726, 1546-1726
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Abstract Accumulation of abnormally phosphorylated TDP-43 (pTDP-43) is the main pathology in affected neurons of people with amyotrophic lateral sclerosis (ALS) and frontotemporal lobar degeneration (FTLD). Morphological diversity and neuroanatomical distribution of pTDP-43 accumulations allowed classification of FTLD cases into at least four subtypes, which are correlated with clinical presentations and genetic causes. To understand the molecular basis of this heterogeneity, we developed SarkoSpin, a new method for biochemical isolation of pathological TDP-43. By combining SarkoSpin with mass spectrometry, we revealed proteins beyond TDP-43 that become abnormally insoluble in a disease subtype-specific manner. We show that pTDP-43 extracted from brain forms stable assemblies of distinct densities and morphologies that are associated with disease subtypes. Importantly, biochemically extracted pTDP-43 assemblies showed differential neurotoxicity and seeding that were correlated with disease duration of FTLD subjects. Our data are consistent with the notion that disease heterogeneity could originate from alternate pathological TDP-43 conformations, which are reminiscent of prion strains.
AbstractList Accumulation of abnormally phosphorylated TDP-43 (pTDP-43) is the main pathology in affected neurons of people with amyotrophic lateral sclerosis (ALS) and frontotemporal lobar degeneration (FTLD). Morphological diversity and neuroanatomical distribution of pTDP-43 accumulations allowed classification of FTLD cases into at least four subtypes, which are correlated with clinical presentations and genetic causes. To understand the molecular basis of this heterogeneity, we developed SarkoSpin, a new method for biochemical isolation of pathological TDP-43. By combining SarkoSpin with mass spectrometry, we revealed proteins beyond TDP-43 that become abnormally insoluble in a disease subtype-specific manner. We show that pTDP-43 extracted from brain forms stable assemblies of distinct densities and morphologies that are associated with disease subtypes. Importantly, biochemically extracted pTDP-43 assemblies showed differential neurotoxicity and seeding that were correlated with disease duration of FTLD subjects. Our data are consistent with the notion that disease heterogeneity could originate from alternate pathological TDP-43 conformations, which are reminiscent of prion strains.Accumulation of abnormally phosphorylated TDP-43 (pTDP-43) is the main pathology in affected neurons of people with amyotrophic lateral sclerosis (ALS) and frontotemporal lobar degeneration (FTLD). Morphological diversity and neuroanatomical distribution of pTDP-43 accumulations allowed classification of FTLD cases into at least four subtypes, which are correlated with clinical presentations and genetic causes. To understand the molecular basis of this heterogeneity, we developed SarkoSpin, a new method for biochemical isolation of pathological TDP-43. By combining SarkoSpin with mass spectrometry, we revealed proteins beyond TDP-43 that become abnormally insoluble in a disease subtype-specific manner. We show that pTDP-43 extracted from brain forms stable assemblies of distinct densities and morphologies that are associated with disease subtypes. Importantly, biochemically extracted pTDP-43 assemblies showed differential neurotoxicity and seeding that were correlated with disease duration of FTLD subjects. Our data are consistent with the notion that disease heterogeneity could originate from alternate pathological TDP-43 conformations, which are reminiscent of prion strains.
Accumulation of abnormally phosphorylated TDP-43 (pTDP-43) is the main pathology in affected neurons of people with amyotrophic lateral sclerosis (ALS) and frontotemporal lobar degeneration (FTLD). Morphological diversity and neuroanatomical distribution of pTDP-43 accumulations allowed classification of FTLD cases into at least four subtypes, which are correlated with clinical presentations and genetic causes. To understand the molecular basis of this heterogeneity, we developed SarkoSpin, a new method for biochemical isolation of pathological TDP-43. By combining SarkoSpin with mass spectrometry, we revealed proteins beyond TDP-43 that become abnormally insoluble in a disease subtype-specific manner. We show that pTDP-43 extracted from brain forms stable assemblies of distinct densities and morphologies that are associated with disease subtypes. Importantly, biochemically extracted pTDP-43 assemblies showed differential neurotoxicity and seeding that were correlated with disease duration of FTLD subjects. Our data are consistent with the notion that disease heterogeneity could originate from alternate pathological TDP-43 conformations, which are reminiscent of prion strains.
Using a newly developed biochemical method for aggregated protein extraction, Laferrière and colleagues uncover different neurotoxic types of pathologic TDP-43 assemblies in the brains of subjects with distinct subtypes of frontotemporal dementia.
Author Pérez-Berlanga, Manuela
Hock, Eva-Maria
Wagner, Ulrich
Afroz, Tariq
Barmettler, Gery
Hruska-Plochan, Marian
Ravits, John
Bezard, Erwan
Picotti, Paola
Asi, Yasmine T
Lewis, Amanda
Isaacs, Adrian M
Stahlberg, Henning
Lashley, Tammaryn
Gilhespy, Larissa
Foti, Sandrine C
De Giorgi, Francesca
Maniecka, Zuzanna
Boersema, Paul J
Polymenidou, Magdalini
Laferrière, Florent
Al-Amoudi, Ashraf
Ichas, François
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  organization: Institute of Molecular Life Sciences, University of Zurich, Zurich, Switzerland
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  organization: Institute of Molecular Life Sciences, University of Zurich, Zurich, Switzerland
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  organization: Institute of Molecular Life Sciences, University of Zurich, Zurich, Switzerland
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  surname: Wagner
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  organization: Department of Pathology and Molecular Pathology, University Hospital Zurich, Zurich, Switzerland
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  surname: Afroz
  fullname: Afroz, Tariq
  organization: Institute of Molecular Life Sciences, University of Zurich, Zurich, Switzerland
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  organization: Institute of Biochemistry, Department of Biology, ETH Zurich (ETHZ), Zurich, Switzerland
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  givenname: Gery
  surname: Barmettler
  fullname: Barmettler, Gery
  organization: Center for Microscopy and Image Analysis, University of Zurich, Zurich, Switzerland
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  givenname: Sandrine C
  surname: Foti
  fullname: Foti, Sandrine C
  organization: Department of Neurodegenerative Disease, UCL Institute of Neurology, London, UK
– sequence: 12
  givenname: Yasmine T
  surname: Asi
  fullname: Asi, Yasmine T
  organization: Department of Neurodegenerative Disease, UCL Institute of Neurology, London, UK
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  givenname: Adrian M
  surname: Isaacs
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  organization: UK Dementia Research Institute at UCL, UCL Institute of Neurology, London, UK
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  givenname: Ashraf
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  organization: Center for Cellular Imaging and NanoAnalytics (C-CINA), Biozentrum, University of Basel, Basel, Switzerland
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  givenname: Henning
  orcidid: 0000-0002-1185-4592
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  givenname: Francesca
  surname: De Giorgi
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  organization: CNRS, Institut des Maladies Neurodégénératives, UMR 5293, Bordeaux, France
– sequence: 19
  givenname: François
  surname: Ichas
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  organization: CNRS, Institut des Maladies Neurodégénératives, UMR 5293, Bordeaux, France
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  orcidid: 0000-0002-0410-4638
  surname: Bezard
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  organization: CNRS, Institut des Maladies Neurodégénératives, UMR 5293, Bordeaux, France
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  surname: Polymenidou
  fullname: Polymenidou, Magdalini
  email: magdalini.polymenidou@imls.uzh.ch
  organization: Institute of Molecular Life Sciences, University of Zurich, Zurich, Switzerland. magdalini.polymenidou@imls.uzh.ch
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30559480$$D View this record in MEDLINE/PubMed
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Snippet Accumulation of abnormally phosphorylated TDP-43 (pTDP-43) is the main pathology in affected neurons of people with amyotrophic lateral sclerosis (ALS) and...
Using a newly developed biochemical method for aggregated protein extraction, Laferrière and colleagues uncover different neurotoxic types of pathologic TDP-43...
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SubjectTerms Aggregates
Amyotrophic lateral sclerosis
Anatomy
Animals
Assemblies
Brain
Brain - metabolism
Brain - pathology
Brain architecture
Degeneration
Dementia
Disease Progression
DNA-Binding Proteins - metabolism
Frontotemporal dementia
Frontotemporal Lobar Degeneration - metabolism
Frontotemporal Lobar Degeneration - pathology
HEK293 Cells
Heterogeneity
Humans
Inclusion Bodies - metabolism
Inclusion Bodies - pathology
Mass Spectrometry
Mass spectroscopy
Medical research
Mice
Morphology
Motor neurone disease
Mutation
Neurodegeneration
Neurology
Neurons - metabolism
Neurons - pathology
Neuropathology
Neurosciences
Neurotoxicity
Pathology
Phosphorylation
Physiology
Protein Aggregates - physiology
Protein seeding
Proteins
Scientific imaging
Semantics
Title TDP-43 extracted from frontotemporal lobar degeneration subject brains displays distinct aggregate assemblies and neurotoxic effects reflecting disease progression rates
URI https://www.ncbi.nlm.nih.gov/pubmed/30559480
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