Protein transmission in neurodegenerative disease

Most neurodegenerative diseases are characterized by the intracellular or extracellular aggregation of misfolded proteins such as amyloid-β and tau in Alzheimer disease, α-synuclein in Parkinson disease, and TAR DNA-binding protein 43 in amyotrophic lateral sclerosis. Accumulating evidence from both...

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Published inNature reviews. Neurology Vol. 16; no. 4; pp. 199 - 212
Main Authors Peng, Chao, Trojanowski, John Q., Lee, Virginia M.-Y.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.04.2020
Nature Publishing Group
Subjects
Online AccessGet full text
ISSN1759-4758
1759-4766
1759-4766
DOI10.1038/s41582-020-0333-7

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Abstract Most neurodegenerative diseases are characterized by the intracellular or extracellular aggregation of misfolded proteins such as amyloid-β and tau in Alzheimer disease, α-synuclein in Parkinson disease, and TAR DNA-binding protein 43 in amyotrophic lateral sclerosis. Accumulating evidence from both human studies and disease models indicates that intercellular transmission and the subsequent templated amplification of these misfolded proteins are involved in the onset and progression of various neurodegenerative diseases. The misfolded proteins that are transferred between cells are referred to as ‘pathological seeds’. Recent studies have made exciting progress in identifying the characteristics of different pathological seeds, particularly those isolated from diseased brains. Advances have also been made in our understanding of the molecular mechanisms that regulate the transmission process, and the influence of the host cell on the conformation and properties of pathological seeds. The aim of this Review is to summarize our current knowledge of the cell-to-cell transmission of pathological proteins and to identify key questions for future investigation. In this Review, Peng et al. summarize the evidence for cell-to-cell transmission of pathological proteins in neurodegenerative diseases such as Alzheimer disease and Parkinson disease, and identify key questions for future investigation. Key points Cell-to-cell transmission and the subsequent amplification of pathological proteins is emerging as a common mechanism for the progression of various neurodegenerative diseases. Transmission within the CNS as well as from the peripheral nervous system to the CNS has been reported for multiple pathological proteins. Multiple molecular mechanisms involved in the secretion, uptake and transport of pathological seeds have been identified. Neurodegenerative disease-related pathological proteins are conformationally diverse. Various factors can modulate the transmission process, including neuronal activity, glial cells, genetic risk factors and interactions with other pathological proteins. Antibodies against pathological seeds, which are designed to block the transmission process, are currently in clinical trials.
AbstractList Most neurodegenerative diseases are characterized by the intracellular or extracellular aggregation of misfolded proteins such as amyloid-β and tau in Alzheimer disease, α-synuclein in Parkinson disease, and TAR DNA-binding protein 43 in amyotrophic lateral sclerosis. Accumulating evidence from both human studies and disease models indicates that intercellular transmission and the subsequent templated amplification of these misfolded proteins are involved in the onset and progression of various neurodegenerative diseases. The misfolded proteins that are transferred between cells are referred to as ‘pathological seeds’. Recent studies have made exciting progress in identifying the characteristics of different pathological seeds, particularly those isolated from diseased brains. Advances have also been made in our understanding of the molecular mechanisms that regulate the transmission process, and the influence of the host cell on the conformation and properties of pathological seeds. The aim of this Review is to summarize our current knowledge of the cell-to-cell transmission of pathological proteins and to identify key questions for future investigation.
Most neurodegenerative diseases are characterized by the intracellular or extracellular aggregation of misfolded proteins such as amyloid-[beta] and tau in Alzheimer disease, [alpha]-synuclein in Parkinson disease, and TAR DNA-binding protein 43 in amyotrophic lateral sclerosis. Accumulating evidence from both human studies and disease models indicates that intercellular transmission and the subsequent templated amplification of these misfolded proteins are involved in the onset and progression of various neurodegenerative diseases. The misfolded proteins that are transferred between cells are referred to as 'pathological seeds'. Recent studies have made exciting progress in identifying the characteristics of different pathological seeds, particularly those isolated from diseased brains. Advances have also been made in our understanding of the molecular mechanisms that regulate the transmission process, and the influence of the host cell on the conformation and properties of pathological seeds. The aim of this Review is to summarize our current knowledge of the cell-to-cell transmission of pathological proteins and to identify key questions for future investigation. In this Review, Peng et al. summarize the evidence for cell-to-cell transmission of pathological proteins in neurodegenerative diseases such as Alzheimer disease and Parkinson disease, and identify key questions for future investigation. Key points Cell-to-cell transmission and the subsequent amplification of pathological proteins is emerging as a common mechanism for the progression of various neurodegenerative diseases. Transmission within the CNS as well as from the peripheral nervous system to the CNS has been reported for multiple pathological proteins. Multiple molecular mechanisms involved in the secretion, uptake and transport of pathological seeds have been identified. Neurodegenerative disease-related pathological proteins are conformationally diverse. Various factors can modulate the transmission process, including neuronal activity, glial cells, genetic risk factors and interactions with other pathological proteins. Antibodies against pathological seeds, which are designed to block the transmission process, are currently in clinical trials.
Most neurodegenerative diseases are characterized by the intracellular or extracellular aggregation of misfolded proteins such as amyloid-β and tau in Alzheimer disease, α-synuclein in Parkinson disease, and TAR DNA-binding protein 43 in amyotrophic lateral sclerosis. Accumulating evidence from both human studies and disease models indicates that intercellular transmission and the subsequent templated amplification of these misfolded proteins are involved in the onset and progression of various neurodegenerative diseases. The misfolded proteins that are transferred between cells are referred to as 'pathological seeds'. Recent studies have made exciting progress in identifying the characteristics of different pathological seeds, particularly those isolated from diseased brains. Advances have also been made in our understanding of the molecular mechanisms that regulate the transmission process, and the influence of the host cell on the conformation and properties of pathological seeds. The aim of this Review is to summarize our current knowledge of the cell-to-cell transmission of pathological proteins and to identify key questions for future investigation.Most neurodegenerative diseases are characterized by the intracellular or extracellular aggregation of misfolded proteins such as amyloid-β and tau in Alzheimer disease, α-synuclein in Parkinson disease, and TAR DNA-binding protein 43 in amyotrophic lateral sclerosis. Accumulating evidence from both human studies and disease models indicates that intercellular transmission and the subsequent templated amplification of these misfolded proteins are involved in the onset and progression of various neurodegenerative diseases. The misfolded proteins that are transferred between cells are referred to as 'pathological seeds'. Recent studies have made exciting progress in identifying the characteristics of different pathological seeds, particularly those isolated from diseased brains. Advances have also been made in our understanding of the molecular mechanisms that regulate the transmission process, and the influence of the host cell on the conformation and properties of pathological seeds. The aim of this Review is to summarize our current knowledge of the cell-to-cell transmission of pathological proteins and to identify key questions for future investigation.
Most neurodegenerative diseases are characterized by the intracellular or extracellular aggregation of misfolded proteins such as amyloid-β and tau in Alzheimer disease, α-synuclein in Parkinson disease, and TAR DNA-binding protein 43 in amyotrophic lateral sclerosis. Accumulating evidence from both human studies and disease models indicates that intercellular transmission and the subsequent templated amplification of these misfolded proteins are involved in the onset and progression of various neurodegenerative diseases. The misfolded proteins that are transferred between cells are referred to as ‘pathological seeds’. Recent studies have made exciting progress in identifying the characteristics of different pathological seeds, particularly those isolated from diseased brains. Advances have also been made in our understanding of the molecular mechanisms that regulate the transmission process, and the influence of the host cell on the conformation and properties of pathological seeds. The aim of this Review is to summarize our current knowledge of the cell-to-cell transmission of pathological proteins and to identify key questions for future investigation.In this Review, Peng et al. summarize the evidence for cell-to-cell transmission of pathological proteins in neurodegenerative diseases such as Alzheimer disease and Parkinson disease, and identify key questions for future investigation.
Most neurodegenerative diseases are characterized by the intracellular or extracellular aggregation of misfolded proteins such as amyloid-[beta] and tau in Alzheimer disease, [alpha]-synuclein in Parkinson disease, and TAR DNA-binding protein 43 in amyotrophic lateral sclerosis. Accumulating evidence from both human studies and disease models indicates that intercellular transmission and the subsequent templated amplification of these misfolded proteins are involved in the onset and progression of various neurodegenerative diseases. The misfolded proteins that are transferred between cells are referred to as 'pathological seeds'. Recent studies have made exciting progress in identifying the characteristics of different pathological seeds, particularly those isolated from diseased brains. Advances have also been made in our understanding of the molecular mechanisms that regulate the transmission process, and the influence of the host cell on the conformation and properties of pathological seeds. The aim of this Review is to summarize our current knowledge of the cell-to-cell transmission of pathological proteins and to identify key questions for future investigation.
Most neurodegenerative diseases are characterized by the intracellular or extracellular aggregation of misfolded proteins such as amyloid-β and tau in Alzheimer disease, α-synuclein in Parkinson disease, and TAR DNA-binding protein 43 in amyotrophic lateral sclerosis. Accumulating evidence from both human studies and disease models indicates that intercellular transmission and the subsequent templated amplification of these misfolded proteins are involved in the onset and progression of various neurodegenerative diseases. The misfolded proteins that are transferred between cells are referred to as ‘pathological seeds’. Recent studies have made exciting progress in identifying the characteristics of different pathological seeds, particularly those isolated from diseased brains. Advances have also been made in our understanding of the molecular mechanisms that regulate the transmission process, and the influence of the host cell on the conformation and properties of pathological seeds. The aim of this Review is to summarize our current knowledge of the cell-to-cell transmission of pathological proteins and to identify key questions for future investigation. In this Review, Peng et al. summarize the evidence for cell-to-cell transmission of pathological proteins in neurodegenerative diseases such as Alzheimer disease and Parkinson disease, and identify key questions for future investigation. Key points Cell-to-cell transmission and the subsequent amplification of pathological proteins is emerging as a common mechanism for the progression of various neurodegenerative diseases. Transmission within the CNS as well as from the peripheral nervous system to the CNS has been reported for multiple pathological proteins. Multiple molecular mechanisms involved in the secretion, uptake and transport of pathological seeds have been identified. Neurodegenerative disease-related pathological proteins are conformationally diverse. Various factors can modulate the transmission process, including neuronal activity, glial cells, genetic risk factors and interactions with other pathological proteins. Antibodies against pathological seeds, which are designed to block the transmission process, are currently in clinical trials.
Audience Academic
Author Trojanowski, John Q.
Lee, Virginia M.-Y.
Peng, Chao
AuthorAffiliation 1 Department of Neurology, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA
2 The Department of Pathology and Laboratory Medicine, Institute on Aging and Center for Neurodegenerative Disease Research, The Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, USA
AuthorAffiliation_xml – name: 2 The Department of Pathology and Laboratory Medicine, Institute on Aging and Center for Neurodegenerative Disease Research, The Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, USA
– name: 1 Department of Neurology, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA
Author_xml – sequence: 1
  givenname: Chao
  surname: Peng
  fullname: Peng, Chao
  organization: Department of Neurology, David Geffen School of Medicine, University of California Los Angeles
– sequence: 2
  givenname: John Q.
  orcidid: 0000-0002-9239-8794
  surname: Trojanowski
  fullname: Trojanowski, John Q.
  organization: The Department of Pathology and Laboratory Medicine, Institute on Aging and Center for Neurodegenerative Disease Research, The Perelman School of Medicine at the University of Pennsylvania
– sequence: 3
  givenname: Virginia M.-Y.
  orcidid: 0000-0003-3536-6902
  surname: Lee
  fullname: Lee, Virginia M.-Y.
  email: vmylee@upenn.edu
  organization: The Department of Pathology and Laboratory Medicine, Institute on Aging and Center for Neurodegenerative Disease Research, The Perelman School of Medicine at the University of Pennsylvania
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32203399$$D View this record in MEDLINE/PubMed
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ORCID 0000-0002-9239-8794
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OpenAccessLink https://proxy.k.utb.cz/login?url=https://www.ncbi.nlm.nih.gov/pmc/articles/9242841
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PublicationDate 2020-04-01
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  year: 2020
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PublicationTitle Nature reviews. Neurology
PublicationTitleAbbrev Nat Rev Neurol
PublicationTitleAlternate Nat Rev Neurol
PublicationYear 2020
Publisher Nature Publishing Group UK
Nature Publishing Group
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SubjectTerms 631/45/470/2284
692/699/375/365
alpha-Synuclein - metabolism
Alzheimer Disease - metabolism
Alzheimer Disease - pathology
Amyloid beta-Peptides - metabolism
Amyotrophic Lateral Sclerosis - metabolism
Amyotrophic Lateral Sclerosis - pathology
Axonal Transport
Biological transport
Brain - metabolism
Brain - pathology
Cell Communication
Cell interaction
Degeneration
DNA-Binding Proteins - metabolism
Endocytosis
Exosomes - metabolism
Genetic Predisposition to Disease
Health aspects
Humans
Huntingtin Protein - metabolism
Huntington Disease - metabolism
Huntington Disease - pathology
Medicine
Medicine & Public Health
Membrane Fusion
Nanotubes
Nervous system
Neurodegenerative Diseases - metabolism
Neurodegenerative Diseases - pathology
Neuroglia - metabolism
Neurological research
Neurology
Neurons - metabolism
Parkinson Disease - metabolism
Parkinson Disease - pathology
Parkinson's disease
Physiological aspects
Protein Aggregation, Pathological - metabolism
Protein Aggregation, Pathological - pathology
Protein metabolism
Protein Transport
Proteins
Review Article
tau Proteins - metabolism
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