Atomic structures of corkscrew‐forming segments of SOD1 reveal varied oligomer conformations

Sangwan, Smriti; Sawaya, Michael R.; Murray, Kevin A.; Hughes, Michael P.; Eisenberg, David S.

doi:10.1002/pro.3391

Atomic structures of corkscrew‐forming segments of SOD1 reveal varied oligomer conformations

Journal Article · Sat Mar 10 00:00:00 EST 2018 · Protein Science

DOI:https://doi.org/10.1002/pro.3391· OSTI ID:1425503

Sangwan, Smriti ^[1]; Sawaya, Michael R. ^[1]; Murray, Kevin A. ^[1]; Hughes, Michael P. ^[1]; Eisenberg, David S. ^[1]

Department of Biological Chemistry Los Angeles Howard Hughes Medical Institute, UCLA‐DOE and Molecular Biology Institute California

Abstract

The aggregation cascade of disease‐related amyloidogenic proteins, terminating in insoluble amyloid fibrils, involves intermediate oligomeric states. The structural and biochemical details of these oligomers have been largely unknown. Here we report crystal structures of variants of the cytotoxic oligomer‐forming segment residues 28–38 of the ALS‐linked protein, SOD1. The crystal structures reveal three different architectures: corkscrew oligomeric structure, nontwisting curved sheet structure and a steric zipper proto‐filament structure. Our work highlights the polymorphism of the segment 28–38 of SOD1 and identifies the molecular features of amyloidogenic entities.

View Accepted Manuscript (Publisher)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1425503

Alternate ID(s):: OSTI ID: 1459975

Journal Information:: Protein Science, Journal Name: Protein Science Journal Issue: 7 Vol. 27; ISSN 0961-8368

Publisher:: Wiley Blackwell (John Wiley & Sons)Copyright Statement

Country of Publication:: United Kingdom

Language:: English

References (40)

Sulfonated dyes attenuate the toxic effects of β-amyloid in a structure-specific fashion Pollack, Scott J.; Sadler, Isobel I. J.; Hawtin, Stuart R. Neuroscience Letters, Vol. 197, Issue 3 https://doi.org/10.1016/0304-3940(95)11939-T	journal	September 1995
An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria Wong, Philip C.; Pardo, Carlos A.; Borchelt, David R. Neuron, Vol. 14, Issue 6 https://doi.org/10.1016/0896-6273(95)90259-7	journal	June 1995
Small molecule probes of protein aggregation Young, Lydia M.; Ashcroft, Alison E.; Radford, Sheena E. Current Opinion in Chemical Biology, Vol. 39 https://doi.org/10.1016/j.cbpa.2017.06.008	journal	August 2017
The Amyloid State of Proteins in Human Diseases Eisenberg, David; Jucker, Mathias Cell, Vol. 148, Issue 6 https://doi.org/10.1016/j.cell.2012.02.022	journal	March 2012
Functional amyloid – from bacteria to humans Fowler, Douglas M.; Koulov, Atanas V.; Balch, William E. Trends in Biochemical Sciences, Vol. 32, Issue 5 https://doi.org/10.1016/j.tibs.2007.03.003	journal	May 2007
Crystal Structures of IAPP Amyloidogenic Segments Reveal a Novel Packing Motif of Out-of-Register Beta Sheets Soriaga, Angela B.; Sangwan, Smriti; Macdonald, Ramsay The Journal of Physical Chemistry B, Vol. 120, Issue 26 https://doi.org/10.1021/acs.jpcb.5b09981	journal	January 2016
Characteristics of Amyloid-Related Oligomers Revealed by Crystal Structures of Macrocyclic β-Sheet Mimics Liu, Cong; Sawaya, Michael R.; Cheng, Pin-Nan Journal of the American Chemical Society, Vol. 133, Issue 17 https://doi.org/10.1021/ja200222n	journal	May 2011
Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis Rosen, Daniel R.; Siddique, Teepu; Patterson, David Nature, Vol. 362, Issue 6415 https://doi.org/10.1038/362059a0	journal	March 1993
Structure of the cross-β spine of amyloid-like fibrils Nelson, Rebecca; Sawaya, Michael R.; Balbirnie, Melinda Nature, Vol. 435, Issue 7043 https://doi.org/10.1038/nature03680	journal	June 2005
Atomic structures of amyloid cross-β spines reveal varied steric zippers Sawaya, Michael R.; Sambashivan, Shilpa; Nelson, Rebecca Nature, Vol. 447, Issue 7143 https://doi.org/10.1038/nature05695	journal	April 2007
The activities of amyloids from a structural perspective Riek, Roland; Eisenberg, David S. Nature, Vol. 539, Issue 7628 https://doi.org/10.1038/nature20416	journal	November 2016
Amyloid-β protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease Bernstein, Summer L.; Dupuis, Nicholas F.; Lazo, Noel D. Nature Chemistry, Vol. 1, Issue 4 https://doi.org/10.1038/nchem.247	journal	June 2009
Ligand binding and aggregation of pathogenic SOD1 Wright, Gareth S. A.; Antonyuk, Svetlana V.; Kershaw, Neil M. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms2750	journal	April 2013
Amyloid-like filaments and water-filled nanotubes formed by SOD1 mutant proteins linked to familial ALS Elam, Jennifer Stine; Taylor, Alexander B.; Strange, Richard Nature Structural & Molecular Biology, Vol. 10, Issue 6 https://doi.org/10.1038/nsb935	journal	May 2003
EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers Ehrnhoefer, Dagmar E.; Bieschke, Jan; Boeddrich, Annett Nature Structural & Molecular Biology, Vol. 15, Issue 6 https://doi.org/10.1038/nsmb.1437	journal	May 2008
Toxic prefibrillar α-synuclein amyloid oligomers adopt a distinctive antiparallel β-sheet structure Celej, María Soledad; Sarroukh, Rabia; Goormaghtigh, Erik Biochemical Journal, Vol. 443, Issue 3 https://doi.org/10.1042/BJ20111924	journal	April 2012
Dimer destabilization in superoxide dismutase may result in disease-causing properties: Structures of motor neuron disease mutants Hough, M. A.; Grossmann, J. G.; Antonyuk, S. V. Proceedings of the National Academy of Sciences, Vol. 101, Issue 16 https://doi.org/10.1073/pnas.0305143101	journal	March 2004
Misfolded CuZnSOD and amyotrophic lateral sclerosis Valentine, J. S.; Hart, P. J. Proceedings of the National Academy of Sciences, Vol. 100, Issue 7 https://doi.org/10.1073/pnas.0730423100	journal	March 2003
Identifying the amylome, proteins capable of forming amyloid-like fibrils Goldschmidt, Lukasz; Teng, Poh K.; Riek, Roland Proceedings of the National Academy of Sciences, Vol. 107, Issue 8 https://doi.org/10.1073/pnas.0915166107	journal	February 2010
An over-oxidized form of superoxide dismutase found in sporadic amyotrophic lateral sclerosis with bulbar onset shares a toxic mechanism with mutant SOD1 Guareschi, S.; Cova, E.; Cereda, C. Proceedings of the National Academy of Sciences, Vol. 109, Issue 13 https://doi.org/10.1073/pnas.1115402109	journal	March 2012
Out-of-register -sheets suggest a pathway to toxic amyloid aggregates Liu, C.; Zhao, M.; Jiang, L. Proceedings of the National Academy of Sciences, Vol. 109, Issue 51 https://doi.org/10.1073/pnas.1218792109	journal	December 2012
Aggregation-triggering segments of SOD1 fibril formation support a common pathway for familial and sporadic ALS Ivanova, M. I.; Sievers, S. A.; Guenther, E. L. Proceedings of the National Academy of Sciences, Vol. 111, Issue 1 https://doi.org/10.1073/pnas.1320786110	journal	December 2013
Atomic structure of a toxic, oligomeric segment of SOD1 linked to amyotrophic lateral sclerosis (ALS) Sangwan, Smriti; Zhao, Anni; Adams, Katrina L. Proceedings of the National Academy of Sciences, Vol. 114, Issue 33 https://doi.org/10.1073/pnas.1705091114	journal	July 2017
Insights into the Role of the Unusual Disulfide Bond in Copper-Zinc Superoxide Dismutase Sea, Kevin; Sohn, Se Hui; Durazo, Armando Journal of Biological Chemistry, Vol. 290, Issue 4 https://doi.org/10.1074/jbc.M114.588798	journal	November 2014
Prefibrillar Amyloid Protein Aggregates Share Common Features of Cytotoxicity Bucciantini, Monica; Calloni, Giulia; Chiti, Fabrizio Journal of Biological Chemistry, Vol. 279, Issue 30 https://doi.org/10.1074/jbc.M400348200	journal	May 2004
Curcumin Inhibits Formation of Amyloid β Oligomers and Fibrils, Binds Plaques, and Reduces Amyloid in Vivo Yang, Fusheng; Lim, Giselle P.; Begum, Aynun N. Journal of Biological Chemistry, Vol. 280, Issue 7 https://doi.org/10.1074/jbc.M404751200	journal	December 2004
Small Molecule Inhibitors of Aggregation Indicate That Amyloid β Oligomerization and Fibrillization Pathways Are Independent and Distinct Necula, Mihaela; Kayed, Rakez; Milton, Saskia Journal of Biological Chemistry, Vol. 282, Issue 14 https://doi.org/10.1074/jbc.M608207200	journal	February 2007
Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants Kabsch, W. Journal of Applied Crystallography, Vol. 26, Issue 6 https://doi.org/10.1107/S0021889893005588	journal	December 1993
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
REFMAC 5 dictionary: organization of prior chemical knowledge and guidelines for its use Vagin, Alexei A.; Steiner, Roberto A.; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/S0907444904023510	journal	November 2004
Congo red and thioflavin-T analogs detect Aβ oligomers Maezawa, Izumi; Hong, Hyun-Seok; Liu, Ruiwu Journal of Neurochemistry, Vol. 0, Issue 0 https://doi.org/10.1111/j.1471-4159.2007.04972.x	journal	October 2007
Inhibition of Amyloid Fibril Formation by Polyphenols: Structural Similarity and Aromatic Interactions as a Common Inhibition Mechanism Porat, Yair; Abramowitz, Adel; Gazit, Ehud Chemical Biology Drug Design, Vol. 67, Issue 1 https://doi.org/10.1111/j.1747-0285.2005.00318.x	journal	January 2006
Common Structure of Soluble Amyloid Oligomers Implies Common Mechanism of Pathogenesis Kayed, R. Science, Vol. 300, Issue 5618 https://doi.org/10.1126/science.1079469	journal	April 2003
Atomic View of a Toxic Amyloid Small Oligomer Laganowsky, Arthur; Liu, Cong; Sawaya, Michael R. Science, Vol. 335, Issue 6073 https://doi.org/10.1126/science.1213151	journal	March 2012
Structural Studies of Amyloid Proteins at the Molecular Level Eisenberg, David S.; Sawaya, Michael R. Annual Review of Biochemistry, Vol. 86, Issue 1 https://doi.org/10.1146/annurev-biochem-061516-045104	journal	June 2017
Protein Misfolding, Functional Amyloid, and Human Disease Chiti, Fabrizio; Dobson, Christopher M. Annual Review of Biochemistry, Vol. 75, Issue 1 https://doi.org/10.1146/annurev.biochem.75.101304.123901	journal	June 2006
Towards a Pharmacophore for Amyloid Landau, Meytal; Sawaya, Michael R.; Faull, Kym F. PLoS Biology, Vol. 9, Issue 6 https://doi.org/10.1371/journal.pbio.1001080	journal	June 2011
Perspective on SOD1 mediated toxicity in Amyotrophic Lateral Sclerosis Sangwan, Smriti; Eisenberg, David S. Postępy Biochemii, Vol. 62, Issue 3 https://doi.org/10.18388/pb.2016_37	journal	November 2016
Susceptibility of Mutant SOD1 to Form a Destabilized Monomer Predicts Cellular Aggregation and Toxicity but Not In vitro Aggregation Propensity McAlary, Luke; Aquilina, J. Andrew; Yerbury, Justin J. Frontiers in Neuroscience, Vol. 10 https://doi.org/10.3389/fnins.2016.00499	journal	November 2016
Atomic structures of fibrillar segments of hIAPP suggest tightly mated β-sheets are important for cytotoxicity Krotee, Pascal; Rodriguez, Jose A.; Sawaya, Michael R. eLife, Vol. 6 https://doi.org/10.7554/eLife.19273	journal	January 2017

Similar Records

Atomic structure of a toxic, oligomeric segment of SOD1 linked to amyotrophic lateral sclerosis (ALS)

Journal Article · Sun Jul 30 20:00:00 EDT 2017 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1390865

Atomic View of a Toxic Amyloid Small Oligomer

Journal Article · Mon Apr 30 00:00:00 EDT 2012 · Science · OSTI ID:1037487

Characteristics of Amyloid-Related Oligomers Revealed by Crystal Structures of Macrocyclic [beta]-Sheet Mimics

Journal Article · Tue Sep 20 00:00:00 EDT 2011 · J. Am. Chem. Soc. · OSTI ID:1023676

Atomic structures of corkscrew‐forming segments of SOD1 reveal varied oligomer conformations

Citation Formats

References (40)

Similar Records

Related Subjects