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Title: Solid-state NMR structure of a pathogenic fibril of full-length human α-synuclein

Abstract

Misfolded α-synuclein amyloid fibrils are the principal components of Lewy bodies and neurites, hallmarks of Parkinson's disease (PD). In this paper, we present a high-resolution structure of an α-synuclein fibril, in a form that induces robust pathology in primary neuronal culture, determined by solid-state NMR spectroscopy and validated by EM and X-ray fiber diffraction. Over 200 unique long-range distance restraints define a consensus structure with common amyloid features including parallel, in-register β-sheets and hydrophobic-core residues, and with substantial complexity arising from diverse structural features including an intermolecular salt bridge, a glutamine ladder, close backbone interactions involving small residues, and several steric zippers stabilizing a new orthogonal Greek-key topology. These characteristics contribute to the robust propagation of this fibril form, as supported by the structural similarity of early-onset-PD mutants. Finally, the structure provides a framework for understanding the interactions of α-synuclein with other proteins and small molecules, to aid in PD diagnosis and treatment.

Authors:
 [1];  [2];  [1];  [3];  [1];  [1];  [1];  [1];  [2];  [4];  [4];  [4];  [5];  [3];  [6];  [7]
+ Show Author Affiliations
  1. Univ. of Illinois, Urbana, IL (United States). Dept. of Chemistry
  2. Univ. of Illinois, Urbana, IL (United States). Center for Biophysics and Quantitative Biology
  3. Univ. of Pennsylvania, Philadelphia, PA (United States). School of Medicine. Dept. of Pathology and Lab. Medicine. Inst. on Aging. Center for Neurodegenerative Disease Research
  4. Vanderbilt Univ., Nashville, TN (United States). Dept. of Biological Sciences. Center for Structural Biology
  5. National Inst. of Health (NIH), Bethesda, MD (United States). Division of Computational Bioscience. Center for Information Technology
  6. Queen Mary Univ. of London (United Kingdom). Dept. of Biological and Experimental Psychology. School of Biological and Chemical Sciences
  7. Univ. of Illinois, Urbana, IL (United States). Dept. of Chemistry. Center for Biophysics and Quantitative Biology. Dept. of Biochemistry
Publication Date:
Research Org.:
Univ. of Illinois at Urbana-Champaign, IL (United States); Univ. of Pennsylvania, Philadelphia, PA (United States); Vanderbilt Univ., Nashville, TN (United States); National Institutes of Health (NIH), Bethesda, MD (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES); National Inst. of Health (NIH) (United States); National Science Foundation (NSF)
OSTI Identifier:
1467083
Grant/Contract Number:  
FG02-07ER46453; FG02-07ER46471; R01-GM073770; P50-NS053488; P01-AG002132; S10-RR025037; T32-GM008276; T32-AG000255; P41-EB2181; S10-RR011966
Resource Type:
Accepted Manuscript
Journal Name:
Nature Structural & Molecular Biology
Additional Journal Information:
Journal Volume: 23; Journal Issue: 5; Journal ID: ISSN 1545-9993
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; solid-state NMR; supramolecular assembly

Citation Formats

Tuttle, Marcus D., Comellas, Gemma, Nieuwkoop, Andrew J., Covell, Dustin J., Berthold, Deborah A., Kloepper, Kathryn D., Courtney, Joseph M., Kim, Jae K., Barclay, Alexander M., Kendall, Amy, Wan, William, Stubbs, Gerald, Schwieters, Charles D., Lee, Virginia M. Y., George, Julia M., and Rienstra, Chad M. Solid-state NMR structure of a pathogenic fibril of full-length human α-synuclein. United States: N. p., 2016. Web. doi:10.1038/nsmb.3194.
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Tuttle, Marcus D., Comellas, Gemma, Nieuwkoop, Andrew J., Covell, Dustin J., Berthold, Deborah A., Kloepper, Kathryn D., Courtney, Joseph M., Kim, Jae K., Barclay, Alexander M., Kendall, Amy, Wan, William, Stubbs, Gerald, Schwieters, Charles D., Lee, Virginia M. Y., George, Julia M., & Rienstra, Chad M. Solid-state NMR structure of a pathogenic fibril of full-length human α-synuclein. United States. https://doi.org/10.1038/nsmb.3194
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Tuttle, Marcus D., Comellas, Gemma, Nieuwkoop, Andrew J., Covell, Dustin J., Berthold, Deborah A., Kloepper, Kathryn D., Courtney, Joseph M., Kim, Jae K., Barclay, Alexander M., Kendall, Amy, Wan, William, Stubbs, Gerald, Schwieters, Charles D., Lee, Virginia M. Y., George, Julia M., and Rienstra, Chad M. Mon . "Solid-state NMR structure of a pathogenic fibril of full-length human α-synuclein". United States. https://doi.org/10.1038/nsmb.3194. https://www.osti.gov/servlets/purl/1467083.
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@article{osti_1467083,
title = {Solid-state NMR structure of a pathogenic fibril of full-length human α-synuclein},
author = {Tuttle, Marcus D. and Comellas, Gemma and Nieuwkoop, Andrew J. and Covell, Dustin J. and Berthold, Deborah A. and Kloepper, Kathryn D. and Courtney, Joseph M. and Kim, Jae K. and Barclay, Alexander M. and Kendall, Amy and Wan, William and Stubbs, Gerald and Schwieters, Charles D. and Lee, Virginia M. Y. and George, Julia M. and Rienstra, Chad M.},
abstractNote = {Misfolded α-synuclein amyloid fibrils are the principal components of Lewy bodies and neurites, hallmarks of Parkinson's disease (PD). In this paper, we present a high-resolution structure of an α-synuclein fibril, in a form that induces robust pathology in primary neuronal culture, determined by solid-state NMR spectroscopy and validated by EM and X-ray fiber diffraction. Over 200 unique long-range distance restraints define a consensus structure with common amyloid features including parallel, in-register β-sheets and hydrophobic-core residues, and with substantial complexity arising from diverse structural features including an intermolecular salt bridge, a glutamine ladder, close backbone interactions involving small residues, and several steric zippers stabilizing a new orthogonal Greek-key topology. These characteristics contribute to the robust propagation of this fibril form, as supported by the structural similarity of early-onset-PD mutants. Finally, the structure provides a framework for understanding the interactions of α-synuclein with other proteins and small molecules, to aid in PD diagnosis and treatment.},
doi = {10.1038/nsmb.3194},
journal = {Nature Structural & Molecular Biology},
number = 5,
volume = 23,
place = {United States},
year = {Mon Mar 28 00:00:00 EDT 2016},
month = {Mon Mar 28 00:00:00 EDT 2016}
}
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https://doi.org/10.1038/nsmb.3194
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  • Molecular Neurodegeneration, Vol. 10, Issue 1
  • DOI: 10.1186/s13024-015-0029-4

Site-Specific Perturbations of Alpha-Synuclein Fibril Structure by the Parkinson's Disease Associated Mutations A53T and E46K
journal, March 2013

Solid-state NMR sequential assignments of α-synuclein
text, January 2012

Lifting the veil on amyloid drug design
journal, July 2013

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