Cell-to-cell transmission of non-prion protein aggregates - PubMed (original) (raw)
Review
Cell-to-cell transmission of non-prion protein aggregates
Seung-Jae Lee et al. Nat Rev Neurol. 2010 Dec.
Erratum in
- Nat Rev Neurol. 2011 Jan;7(1):5
Abstract
Neurodegenerative disorders such as Alzheimer disease, Parkinson disease, frontotemporal dementia, Huntington disease and Creutzfeldt-Jakob disease (CJD) are characterized by progressive accumulation of protein aggregates in selected brain regions. Protein misfolding and templated assembly into aggregates might result from an imbalance between protein synthesis, aggregation and clearance. Although protein misfolding and aggregation occur in most neurodegenerative disorders, the concept of spreading and infectivity of aggregates in the CNS has, until now, been confined to prion diseases such as CJD and bovine spongiform encephalopathy. Emerging evidence, however, suggests that prion-like spreading, involving secreted proteins such as amyloid-β and cytosolic proteins such as tau, huntingtin and α-synuclein, can occur in other neurodegenerative disorders. The underlying molecular mechanisms and the therapeutic implications of the new data are discussed in this article.
Figures
Figure 1. Aggregate clearing activity, seed formation, and aggregate burden
The formation of misfolded/aggregated protein is an inevitable outcome of a protein's life and is normally cleared by the cellular quality control mechanisms. In situation such as aging and disease, the combined effects of accelerated production, due to elevated oxidative stress, and the reduced ability of cells to degrade damaged proteins, increse protein aggregation, Incomplete degradation of aggregated proteins may result in the production of smaller fragments that can serve as seeds for further aggregation thereby increasing the aggregate burden. Therefore, reduced function in proteing degradation systems plays a critical role in aggregate propagation in neurodegenerative diseases.
Figure 2. Models of cell-to-cell protein transmission
This diagram illustrates potential mechanisms by which misfolded/aggregated proteins are transmitted from one neuron to another. Proteins may be released from neurons via vesicle-mediated exocytosis (1) or simple leakage through damaged membranes (2), then internalize into neighboring neurons either via endocytosis or via direct penetration of the memebrane. Alternatively, as reported with the prion protein, proteins may be transmitted to the neighboring neurons by packaging into exosomes (3) or through tunneling nanotubes (4). Some or all of these mechanisms might work simultaneously, with a specific protein preferring a certain pathway to others. These mechanisms might act between the cell bodies, but could also occur trans-synaptically (5). Internalized aggregates (orange) might act as seeds for the aggregation of the endogenous native proteins (green). This seeded aggregation may produce toxic aggregate species during the course of dynamic aggregation process, which ultimately leads to the formation of pathological inclusion bodies.
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References
- Forman MS, Trojanowski JQ, Lee VM. Neurodegenerative diseases: a decade of discoveries paves the way for therapeutic breakthroughs. Nat Med. 2004;10:1055–1063. - PubMed
- Lansbury PT, Lashuel HA. A century-old debate on protein aggregation and neurodegeneration enters the clinic. Nature. 2006;443:774–779. - PubMed
- Aguzzi A, Baumann F, Bremer J. The prion's elusive reason for being. Annu Rev Neurosci. 2008;31:439–477. - PubMed
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