Hostname: page-component-669899f699-b58lm Total loading time: 0 Render date: 2025-04-26T07:24:24.389Z Has data issue: false hasContentIssue false
  • English
  • Français

Fibrils with parallel in-register structure constitute a major class of amyloid fibrils: molecular insights from electron paramagnetic resonance spectroscopy

Published online by Cambridge University Press:  11 December 2008

Martin Margittai  and
Ralf Langen
Martin Margittai*
Affiliation:
Department of Chemistry and Biochemistry, University of Denver, Denver, CO, USA
Ralf Langen*
Affiliation:
Department of Biochemistry and Molecular Biology, Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
*
*Authors for correspondence: Dr. M. Margittai, Department of Chemistry and Biochemistry, University of Denver, Denver, CO80208, USA. Tel.: 303-871-4135; Fax: 303-871-2254; Email: [email protected]
Dr. R. Langen, Department of Biochemistry and Molecular Biology, Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA90033, USA. Tel.: 323-442-1323; Fax: 323-442-4404; Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The deposition of amyloid- and amyloid-like fibrils is the main pathological hallmark of numerous protein misfolding diseases including Alzheimer's disease, transmissible spongiform encephalopathy, and type 2 diabetes. Besides the well-established role in disease, recent work on a variety of organisms ranging from bacteria to humans suggests that amyloid fibrils can also convey biological functions. To better understand the molecular mechanisms by which amyloidogenic proteins misfold in disease or perform biological functions, structural information is essential. Although high-resolution structural analysis of amyloid fibrils has been challenging, a combination of biophysical approaches is beginning to unravel the various structural features of amyloid fibrils. Here we review these recent developments with particular emphasis on amyloid fibrils that have been studied using site-directed spin labeling and electron paramagnetic resonance spectroscopy. This approach has been used to define the precise location of fibril-forming core regions and identify local secondary structures within such core regions. Perhaps one of the most remarkable findings arrived at by site-directed spin labeling was that most fibrils that contain an extensive core region of ∼20 amino acids or more share a common parallel in-register arrangement of β strands. The preference for this arrangement can be explained on topological grounds and may be rationalized by the maximization of hydrophobic contact surface.

Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 41 , Issue 3-4 , November 2008 , pp. 265 - 297
Copyright
Copyright © 2008 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Aguzzi, A. & Polymenidou, M. (2004). Mammalian prion biology: one century of evolving concepts. Cell 116(2), 313–327.CrossRefGoogle ScholarPubMed
Altenbach, C., Greenhalgh, D. A., Khorana, H. G. & Hubbell, W. L. (1994). A collision gradient method to determine the immersion depth of nitroxides in lipid bilayers: application to spin-labeled mutants of bacteriorhodopsin. Proceedings of the National Academy of Sciences USA 91(5), 1667–1671.CrossRefGoogle ScholarPubMed
Altenbach, C., Oh, K. J., Trabanino, R. J., Hideg, K. & Hubbell, W. L. (2001). Estimation of inter-residue distances in spin labeled proteins at physiological temperatures: experimental strategies and practical limitations. Biochemistry 40(51), 15471–15482.CrossRefGoogle ScholarPubMed
Anderson, P. W. & Weiss, P. R. (1953). Exchange narrowing in paramagnetic resonance. Reviews of Modern Physics 25(1), 269–276.CrossRefGoogle Scholar
Anfinsen, C. B. (1973). Principles that govern the folding of protein chains. Science 181(96), 223–230.CrossRefGoogle ScholarPubMed
Antzutkin, O. N., Balbach, J. J., Leapman, R. D., Rizzo, N. W., Reed, J. & Tycko, R. (2000). Multiple quantum solid-state NMR indicates a parallel, not antiparallel, organization of beta-sheets in Alzheimer's beta-amyloid fibrils. Proceedings of the National Academy of Sciences USA 97(24), 13045–13050.CrossRefGoogle Scholar
Antzutkin, O. N., Balbach, J. J. & Tycko, R. (2003). Site-specific identification of non-beta-strand conformations in Alzheimer's beta-amyloid fibrils by solid-state NMR. Biophysical Journal 84(5), 3326–3335.CrossRefGoogle ScholarPubMed
Apostolidou, M., Jayasinghe, S. A. & Langen, R. (2008). Structure of alpha-helical membrane-bound hIAPP and its implications for membrane-mediated misfolding. Journal of Biological Chemistry 283(25), 17205–17210.CrossRefGoogle ScholarPubMed
Balbach, J. J., Ishii, Y., Antzutkin, O. N., Leapman, R. D., Rizzo, N. W., Dyda, F., Reed, J. & Tycko, R. (2000). Amyloid fibril formation by A beta 16–22, a seven-residue fragment of the Alzheimer's beta-amyloid peptide, and structural characterization by solid state NMR. Biochemistry 39(45), 13748–13759.CrossRefGoogle ScholarPubMed
Balbach, J. J., Petkova, A. T., Oyler, N. A., Antzutkin, O. N., Gordon, D. J., Meredith, S. C. & Tycko, R. (2002). Supramolecular structure in full-length Alzheimer's beta-amyloid fibrils: evidence for a parallel beta-sheet organization from solid-state nuclear magnetic resonance. Biophysical Journal 83(2), 1205–1216.CrossRefGoogle ScholarPubMed
Barnhart, M. M. & Chapman, M. R. (2006). Curli biogenesis and function. Annual Review of Microbiology 60, 131–147.CrossRefGoogle ScholarPubMed
Bauer, H. H., Aebi, U., Haner, M., Hermann, R., Muller, M. & Merkle, H. P. (1995). Architecture and polymorphism of fibrillar supramolecular assemblies produced by in vitro aggregation of human calcitonin. Journal of Structural Biology 115(1), 1–15.CrossRefGoogle ScholarPubMed
Baxa, U., Cheng, N., Winkler, D. C., Chiu, T. K., Davies, D. R., Sharma, D., Inouye, H., Kirschner, D. A., Wickner, R. B. & Steven, A. C. (2005). Filaments of the Ure2p prion protein have a cross-beta core structure. Journal of Structural Biology 150(2), 170–179.CrossRefGoogle ScholarPubMed
Baxa, U., Taylor, K. L., Wall, J. S., Simon, M. N., Cheng, N., Wickner, R. B. & Steven, A. C. (2003). Architecture of Ure2p prion filaments: the N-terminal domains form a central core fiber. Journal of Biological Chemistry 278(44), 43717–43727.CrossRefGoogle Scholar
Baxa, U., Wickner, R. B., Steven, A. C., Anderson, D. E., Marekov, L. N., Yau, W. M. & Tycko, R. (2007). Characterization of beta-sheet structure in Ure2p1-89 yeast prion fibrils by solid-state nuclear magnetic resonance. Biochemistry 46(45), 13149–13162.CrossRefGoogle ScholarPubMed
Benzinger, T. L., Gregory, D. M., Burkoth, T. S., Miller-Auer, H., Lynn, D. G., Botto, R. E. & Meredith, S. C. (2000). Two-dimensional structure of beta-amyloid (10–35) fibrils. Biochemistry 39(12), 3491–3499.CrossRefGoogle ScholarPubMed
Beratan, D. N., Onuchic, J. N., Winkler, J. R. & Gray, H. B. (1992). Electron-tunneling pathways in proteins. Science 258(5089), 1740–1741.CrossRefGoogle ScholarPubMed
Berliner, L. J., Grunwald, J., Hankovszky, H. O. & Hideg, K. (1982). A novel reversible thiol-specific spin label: papain active-site labeling and inhibition. Analytical Biochemistry 119(2), 450–455.CrossRefGoogle ScholarPubMed
Berriman, J., Serpell, L. C., Oberg, K. A., Fink, A. L., Goedert, M. & Crowther, R. A. (2003). Tau filaments from human brain and from in vitro assembly of recombinant protein show cross-beta structure. Proceedings of the National Academy of Sciences USA 100(15), 9034–9038.CrossRefGoogle ScholarPubMed
Berson, J. F., Theos, A. C., Harper, D. C., Tenza, D., Raposo, G. & Marks, M. S. (2003). Proprotein convertase cleavage liberates a fibrillogenic fragment of a resident glycoprotein to initiate melanosome biogenesis. Journal of Cell Biology 161(3), 521–533.CrossRefGoogle ScholarPubMed
Borbat, P. P., Davis, J. H., Butcher, S. E. & Freed, J. H. (2004). Measurement of large distances in biomolecules using double-quantum filtered refocused electron spin-echoes. Journal of the American Chemical Society 126(25), 7746–7747.CrossRefGoogle ScholarPubMed
Borbat, P. P., Mchaourab, H. S. & Freed, J. H. (2002). Protein structure determination using long-distance constraints from double-quantum coherence ESR: study of T4 lysozyme. Journal of the American Chemical Society 124(19), 5304–5314.CrossRefGoogle ScholarPubMed
Bousset, L., Briki, F., Doucet, J. & Melki, R. (2003). The native-like conformation of Ure2p in fibrils assembled under physiologically relevant conditions switches to an amyloid-like conformation upon heat-treatment of the fibrils. Journal of Structural Biology 141(2), 132–142.CrossRefGoogle Scholar
Bousset, L., Redeker, V., Decottignies, P., Dubois, S., Le Marechal, P. & Melki, R. (2004). Structural characterization of the fibrillar form of the yeast Saccharomyces cerevisiae prion Ure2p. Biochemistry 43(17), 5022–5032.CrossRefGoogle ScholarPubMed
Bousset, L., Thomson, N. H., Radford, S. E. & Melki, R. (2002). The yeast prion Ure2p retains its native alpha-helical conformation upon assembly into protein fibrils in vitro. EMBO Journal 21(12), 2903–2911.CrossRefGoogle ScholarPubMed
Brack, A. & Orgel, L. E. (1975). Beta structures of alternating polypeptides and their possible prebiotic significance. Nature 256(5516), 383–387.CrossRefGoogle ScholarPubMed
Broome, B. M. & Hecht, M. H. (2000). Nature disfavors sequences of alternating polar and non-polar amino acids: implications for amyloidogenesis. Journal of Molecular Biology 296(4), 961–968.CrossRefGoogle ScholarPubMed
Bu, Z., Shi, Y., Callaway, D. J. & Tycko, R. (2007). Molecular alignment within beta-sheets in Abeta (14–23) fibrils: solid-state NMR experiments and theoretical predictions. Biophysical Journal 92(2), 594–602.CrossRefGoogle ScholarPubMed
Cage, B., Cevc, P., Blinc, R., Brunel, L. C. & Dalal, N. S. (1998). 1–370 GHz EPR linewidths for K3CrO8: a comprehensive test for the Anderson–Weiss model. Journal of Magnetic Resonance 135(1), 178–184.CrossRefGoogle ScholarPubMed
Chan, J. C., Oyler, N. A., Yau, W. M. & Tycko, R. (2005). Parallel beta-sheets and polar zippers in amyloid fibrils formed by residues 10–39 of the yeast prion protein Ure2p. Biochemistry 44(31), 10669–10680.CrossRefGoogle ScholarPubMed
Chapman, M. R., Robinson, L. S., Pinkner, J. S., Roth, R., Heuser, J., Hammar, M., Normark, S. & Hultgren, S. J. (2002). Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295(5556), 851–855.CrossRefGoogle ScholarPubMed
Chen, M., Margittai, M., Chen, J. & Langen, R. (2007). Investigation of alpha-synuclein fibril structure by site-directed spin labeling. Journal of Biological Chemistry 282(34), 24970–24979.CrossRefGoogle ScholarPubMed
Cherny, I., Rockah, L., Levy-Nissenbaum, O., Gophna, U., Ron, E. Z. & Gazit, E. (2005). The formation of Escherichia coli curli amyloid fibrils is mediated by prion-like peptide repeats. Journal of Molecular Biology 352(2), 245–252.CrossRefGoogle ScholarPubMed
Chien, P., Weissman, J. S. & Depace, A. H. (2004). Emerging principles of conformation-based prion inheritance. Annual Review of Biochemistry 73, 617–656.CrossRefGoogle ScholarPubMed
Chimon, S., Shaibat, M. A., Jones, C. R., Calero, D. C., Aizezi, B. & Ishii, Y. (2007). Evidence of fibril-like beta-sheet structures in a neurotoxic amyloid intermediate of Alzheimer's beta-amyloid. Nature Structural & Molecular Biology 14(12), 1157–1164.CrossRefGoogle Scholar
Chiti, F. & Dobson, C. M. (2006). Protein misfolding, functional amyloid, and human disease. Annual Review of Biochemistry 75, 333–366.CrossRefGoogle ScholarPubMed
Chiti, F., Stefani, M., Taddei, N., Ramponi, G. & Dobson, C. M. (2003). Rationalization of the effects of mutations on peptide and protein aggregation rates. Nature 424(6950), 805–808.CrossRefGoogle ScholarPubMed
Cleveland, D. W., Hwo, S. Y. & Kirschner, M. W. (1977). Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly. Journal of Molecular Biology 116(2), 227–247.CrossRefGoogle ScholarPubMed
Closs, G. L., Piotrowiak, P., Macinnis, J. M. & Fleming, G. R. (1988). Determination of long-distance intramolecular triplet energy-transfer rates – a quantitative comparison with electron-transfer. Journal of the American Chemical Society 110(8), 2652–2653.CrossRefGoogle Scholar
Cobb, N. J., Sonnichsen, F. D., Mchaourab, H. & Surewicz, W. K. (2007). Molecular architecture of human prion protein amyloid: a parallel, in-register beta-structure. Proceedings of the National Academy of Sciences USA 104(48), 18946–18951.CrossRefGoogle ScholarPubMed
Cole, G. J. & Liu, I. H. (2006). Protein misfolding, aggregation and conformational diseases: Part A: protein aggregation and conformational diseases. In Protein Reviews (eds.Uversky, V. N. & Fink, A. L.), pp. 83–100. New York: Springer-Verlag.Google Scholar
Collinge, J. (2001). Prion diseases of humans and animals: their causes and molecular basis. Annual Review of Neuroscience 24, 519–550.CrossRefGoogle ScholarPubMed
Columbus, L. & Hubbell, W. L. (2002). A new spin on protein dynamics. Trends in Biochemical Sciences 27(6), 288–295.CrossRefGoogle ScholarPubMed
Columbus, L., Kalai, T., Jeko, J., Hideg, K. & Hubbell, W. L. (2001). Molecular motion of spin labeled side chains in alpha-helices: analysis by variation of side chain structure. Biochemistry 40(13), 3828–3846.CrossRefGoogle ScholarPubMed
Del Mar, C., Greenbaum, E. A., Mayne, L., Englander, S. W. & Woods, V. L. Jr., (2005). Structure and properties of alpha-synuclein and other amyloids determined at the amino acid level. Proceedings of the National Academy of Sciences USA 102(43), 15477–15482.CrossRefGoogle ScholarPubMed
DeMarco, M. L. & Daggett, V. (2004). From conversion to aggregation: protofibril formation of the prion protein. Proceedings of the National Academy of Sciences USA 101(8), 2293–2298.CrossRefGoogle ScholarPubMed
Der-Sarkissian, A., Jao, C. C., Chen, J. & Langen, R. (2003). Structural organization of alpha-synuclein fibrils studied by site-directed spin labeling. Journal of Biological Chemistry 278(39), 37530–37535.CrossRefGoogle ScholarPubMed
Eaglestone, S. S., Cox, B. S. & Tuite, M. F. (1999). Translation termination efficiency can be regulated in Saccharomyces cerevisiae by environmental stress through a prion-mediated mechanism. EMBO Journal 18(7), 1974–1981.CrossRefGoogle ScholarPubMed
Epstein, E. A. & Chapman, M. R. (2008). Polymerizing the fibre between bacteria and host cells: the biogenesis of functional amyloid fibres. Cell Microbiology 10(7), 1413–1420.CrossRefGoogle ScholarPubMed
Fandrich, M. & Dobson, C. M. (2002). The behaviour of polyamino acids reveals an inverse side chain effect in amyloid structure formation. EMBO Journal 21(21), 5682–5690.CrossRefGoogle ScholarPubMed
Fowler, D. M., Koulov, A. V., Balch, W. E. & Kelly, J. W. (2007). Functional amyloid – from bacteria to humans. Trends in Biochemical Sciences 32(5), 217–224.CrossRefGoogle ScholarPubMed
Giasson, B. I., Jakes, R., Goedert, M., Duda, J. E., Leight, S., Trojanowski, J. Q. & Lee, V. M. (2000). A panel of epitope-specific antibodies detects protein domains distributed throughout human alpha-synuclein in Lewy bodies of Parkinson's disease. Journal of Neuroscience Research 59(4), 528–533.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Goedert, M., Jakes, R., Spillantini, M. G., Hasegawa, M., Smith, M. J. & Crowther, R. A. (1996). Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans. Nature 383(6600), 550–553.CrossRefGoogle ScholarPubMed
Gordon, D. J., Tappe, R. & Meredith, S. C. (2002). Design and characterization of a membrane permeable N-methyl amino acid-containing peptide that inhibits Abeta1-40 fibrillogenesis. Journal of Peptide Research 60(1), 37–55.CrossRefGoogle ScholarPubMed
Gosal, W. S., Myers, S. L., Radford, S. E. & Thomson, N. H. (2006). Amyloid under the atomic force microscope. Protein and Peptide Letters 13(3), 261–270.CrossRefGoogle ScholarPubMed
Govaerts, C., Wille, H., Prusiner, S. B. & Cohen, F. E. (2004). Evidence for assembly of prions with left-handed beta-helices into trimers. Proceedings of the National Academy of Sciences USA 101(22), 8342–8347.CrossRefGoogle ScholarPubMed
Griffiths, J. M., Ashburn, T. T., Auger, M., Costa, P. R. & Griffin, R. G. (1995). Rotational resonance solid-state NMR elucidates a structural model of pancreatic amyloid. Journal of the American Chemical Society 117, 3539–3546.CrossRefGoogle Scholar
Gross, A., Columbus, L., Hideg, K., Altenbach, C. & Hubbell, W. L. (1999). Structure of the KcsA potassium channel from Streptomyces lividans: a site-directed spin labeling study of the second transmembrane segment. Biochemistry 38(32), 10324–10335.CrossRefGoogle ScholarPubMed
Guo, Z., Cascio, D., Hideg, K. & Hubbell, W. L. (2008). Structural determinants of nitroxide motion in spin-labeled proteins: solvent-exposed sites in helix B of T4 lysozyme. Protein Science 17(2), 228–239.CrossRefGoogle ScholarPubMed
Hamada, D., Yanagihara, I. & Tsumoto, K. (2004). Engineering amyloidogenicity towards the development of nanofibrillar materials. Trends in Biotechnology 22(2), 93–97.CrossRefGoogle ScholarPubMed
Hanson, P., Millhauser, G., Formaggio, F., Crisma, M. & Toniolo, C. (1996). ESR characterization of hexameric, helical peptides using double TOAC spin labeling. Journal of the American Chemical Society 118(32), 7618–7625.CrossRefGoogle Scholar
Heise, H., Hoyer, W., Becker, S., Andronesi, O. C., Riedel, D. & Baldus, M. (2005). Molecular-level secondary structure, polymorphism, and dynamics of full-length alpha-synuclein fibrils studied by solid-state NMR. Proceedings of the National Academy of Sciences USA 102(44), 15871–15876.CrossRefGoogle ScholarPubMed
Hoshino, M., Katou, H., Yamaguchi, K. & Goto, Y. (2007). Dimethylsulfoxide-quenched hydrogen/deuterium exchange method to study amyloid fibril structure. Biochimica et Biophysica Acta 1768(8), 1886–1899.CrossRefGoogle ScholarPubMed
Hubbell, W. L. & Altenbach, C. (1994). Investigation of structure and dynamics in membrane-proteins using site-directed spin-labeling. Current Opinion in Structural Biology 4(4), 566–573.CrossRefGoogle Scholar
Hubbell, W. L., Cafiso, D. S. & Altenbach, C. (2000). Identifying conformational changes with site-directed spin labeling. Nature Structural Biology 7(9), 735–739.CrossRefGoogle ScholarPubMed
Hubbell, W. L., Gross, A., Langen, R. & Lietzow, M. A. (1998). Recent advances in site-directed spin labeling of proteins. Current Opinion in Structural Biology 8(5), 649–656.CrossRefGoogle ScholarPubMed
Hubbell, W. L., Mchaourab, H. S., Altenbach, C. & Lietzow, M. A. (1996). Watching proteins move using site-directed spin labeling. Structure 4(7), 779–783.CrossRefGoogle ScholarPubMed
Isas, J. M., Langen, R., Haigler, H. T. & Hubbell, W. L. (2002). Structure and dynamics of a helical hairpin and loop region in annexin 12: a site-directed spin labeling study. Biochemistry 41(5), 1464–1473.CrossRefGoogle ScholarPubMed
Iwata, K., Fujiwara, T., Matsuki, Y., Akutsu, H., Takahashi, S., Naiki, H. & Goto, Y. (2006). 3D structure of amyloid protofilaments of beta2-microglobulin fragment probed by solid-state NMR. Proceedings of the National Academy of Sciences USA 103(48), 18119–18124.CrossRefGoogle ScholarPubMed
Jakes, R., Novak, M., Davison, M. & Wischik, C. M. (1991). Identification of 3- and 4-repeat tau isoforms within the PHF in Alzheimer's disease. EMBO J 10(10), 2725–2729.CrossRefGoogle ScholarPubMed
Jao, C. C., Der-Sarkissian, A., Chen, J. & Langen, R. (2004). Structure of membrane-bound alpha-synuclein studied by site-directed spin labeling. Proceedings of the National Academy of Sciences USA 101(22), 8331–8336.CrossRefGoogle ScholarPubMed
Jaroniec, C. P., Filip, C. & Griffin, R. G. (2002). 3D TEDOR NMR experiments for the simultaneous measurement of multiple carbon-nitrogen distances in uniformly (13)C,(15)N-labeled solids. Journal of the American Chemical Society 124(36), 10728–10742.CrossRefGoogle Scholar
Jaroniec, C. P., Macphee, C. E., Bajaj, V. S., Mcmahon, M. T., Dobson, C. M. & Griffin, R. G. (2004). High-resolution molecular structure of a peptide in an amyloid fibril determined by magic angle spinning NMR spectroscopy. Proceedings of the National Academy of Sciences USA 101(3), 711–716.CrossRefGoogle Scholar
Jayasinghe, S. A. & Langen, R. (2004). Identifying structural features of fibrillar islet amyloid polypeptide using site-directed spin labeling. Journal of Biological Chemistry 279(46), 48420–48425.CrossRefGoogle ScholarPubMed
Jayasinghe, S. A. & Langen, R. (2005). Lipid membranes modulate the structure of islet amyloid polypeptide. Biochemistry 44(36), 12113–12119.CrossRefGoogle ScholarPubMed
Jayasinghe, S. A. & Langen, R. (2007). Membrane interaction of islet amyloid polypeptide. Biochimica et Biophysica Acta 1768(8), 2002–2009.CrossRefGoogle ScholarPubMed
Jellinger, K. A. (2003). Alpha-synuclein pathology in Parkinson's and Alzheimer's disease brain: incidence and topographic distribution – a pilot study. Acta Neuropathologica 106(3), 191–201.CrossRefGoogle ScholarPubMed
Jenkins, J. & Pickersgill, R. (2001). The architecture of parallel beta-helices and related folds. Progress in Biophysics and Molecular Biology 77(2), 111–175.CrossRefGoogle ScholarPubMed
Jeschke, G. (2002). Distance measurements in the nanometer range by pulse EPR. Chemphyschem 3(11), 927–932.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Jeschke, G. & Polyhach, Y. (2007). Distance measurements on spin-labelled biomacromolecules by pulsed electron paramagnetic resonance. Physical Chemistry Chemical Physics 9(16), 1895–1910.CrossRefGoogle ScholarPubMed
Jones, E. M. & Surewicz, W. K. (2005). Fibril conformation as the basis of species- and strain-dependent seeding specificity of mammalian prion amyloids. Cell 121(1), 63–72.CrossRefGoogle ScholarPubMed
Kamihira, M., Naito, A., Tuzi, S., Nosaka, A. Y. & Saito, H. (2000). Conformational transitions and fibrillation mechanism of human calcitonin as studied by high-resolution solid-state 13C NMR. Protein Science 9(5), 867–877.CrossRefGoogle ScholarPubMed
Kamihira, M., Oshiro, Y., Tuzi, S., Nosaka, A. Y., Saito, H. & Naito, A. (2003). Effect of electrostatic interaction on fibril formation of human calcitonin as studied by high resolution solid state 13C NMR. Journal of Biological Chemistry 278(5), 2859–2865.CrossRefGoogle ScholarPubMed
Kajava, A. V., Baxa, U., Wickner, R. B. & Steven, A. C. (2004). A model for Ure2p prion filaments and other amyloids: the parallel superpleated beta-structure. Proceedings of the National Academy of Sciences USA 101(21), 7885–7890.CrossRefGoogle Scholar
Kheterpal, I. & Wetzel, R. (2006). Hydrogen/deuterium exchange mass spectrometry – a window into amyloid structure. Accounts of Chemical Research 39(9), 584–593.CrossRefGoogle ScholarPubMed
Kheterpal, I., Williams, A., Murphy, C., Bledsoe, B. & Wetzel, R. (2001). Structural features of the Abeta amyloid fibril elucidated by limited proteolysis. Biochemistry 40(39), 11757–11767.CrossRefGoogle ScholarPubMed
Kheterpal, I., Zhou, S., Cook, K. D. & Wetzel, R. (2000). Abeta amyloid fibrils possess a core structure highly resistant to hydrogen exchange. Proceedings of the National Academy of Sciences USA 97(25), 13597–13601.CrossRefGoogle ScholarPubMed
Khurana, R., Uversky, V. N., Nielsen, L. & Fink, A. L. (2001). Is Congo red an amyloid-specific dye? Journal of Biological Chemistry 276(25), 22715–22721.CrossRefGoogle ScholarPubMed
King, C. Y. & Diaz-Avalos, R. (2004). Protein-only transmission of three yeast prion strains. Nature 428(6980), 319–323.CrossRefGoogle ScholarPubMed
Kirschner, D. A., Abraham, C. & Selkoe, D. J. (1986). X-ray diffraction from intraneuronal paired helical filaments and extraneuronal amyloid fibers in Alzheimer disease indicates cross-beta conformation. Proceedings of the National Academy of Sciences USA 83(2), 503–507.CrossRefGoogle ScholarPubMed
Knight, J. D., Hebda, J. A. & Miranker, A. D. (2006). Conserved and cooperative assembly of membrane-bound alpha-helical states of islet amyloid polypeptide. Biochemistry 45(31), 9496–9508.CrossRefGoogle ScholarPubMed
Lajzerowicz-Bonneteau, J. (1976). Molecular structures of nitroxides. In Spin Labeling Theory and Applications (ed.Berliner, L. J.), pp. 239–272. New York: Academic Press.CrossRefGoogle Scholar
Langen, R., Chang, I. J., Germanas, J. P., Richards, J. H., Winkler, J. R. & Gray, H. B. (1995). Electron-tunneling in proteins: coupling through a beta-strand. Science 268(5218), 1733–1735.CrossRefGoogle ScholarPubMed
Langen, R., Isas, J. M., Luecke, H., Haigler, H. T. & Hubbell, W. L. (1998). Membrane-mediated assembly of annexins studied by site-directed spin labeling. Journal of Biological Chemistry 273(35), 22453–22457.CrossRefGoogle ScholarPubMed
Langen, R., Oh, K. J., Cascio, D. & Hubbell, W. L. (2000). Crystal structures of spin labeled T4 lysozyme mutants: implications for the interpretation of EPR spectra in terms of structure. Biochemistry 39(29), 8396–8405.CrossRefGoogle ScholarPubMed
Lansbury, P. T. Jr.,, Costa, P. R., Griffiths, J. M., Simon, E. J., Auger, M., Halverson, K. J., Kocisko, D. A., Hendsch, Z. S., Ashburn, T. T., Spencer, R. G., et al. (1995). Structural model for the beta-amyloid fibril based on interstrand alignment of an antiparallel-sheet comprising a C-terminal peptide. Nature Structural Biology 2(11), 990–998.CrossRefGoogle ScholarPubMed
Lee, V. M., Goedert, M. & Trojanowski, J. Q. (2001). Neurodegenerative tauopathies. Annual Review of Neuroscience 24, 1121–1159.CrossRefGoogle ScholarPubMed
Lee, V. M. & Trojanowski, J. Q. (2006). Mechanisms of Parkinson's disease linked to pathological alpha-synuclein: new targets for drug discovery. Neuron 52(1), 33–38.CrossRefGoogle ScholarPubMed
Legname, G., Baskakov, I. V., Nguyen, H. O., Riesner, D., Cohen, F. E., Dearmond, S. J. & Prusiner, S. B. (2004). Synthetic mammalian prions. Science 305(5684), 673–676.CrossRefGoogle ScholarPubMed
Lietzow, M. A. & Hubbell, W. L. (2004). Motion of spin label side chains in cellular retinol-binding protein: correlation with structure and nearest-neighbor interactions in an antiparallel beta-sheet. Biochemistry 43(11), 3137–3151.CrossRefGoogle Scholar
Luca, S., Yau, W. M., Leapman, R. & Tycko, R. (2007). Peptide conformation and supramolecular organization in amylin fibrils: constraints from solid-state NMR. Biochemistry 46(47), 13505–13522.CrossRefGoogle ScholarPubMed
Luhrs, T., Ritter, C., Adrian, M., Riek-Loher, D., Bohrmann, B., Dobeli, H., Schubert, D. & Riek, R. (2005). 3D structure of Alzheimer's amyloid-beta(1–42) fibrils. Proceedings of the National Academy of Sciences USA 102(48), 17342–17347.CrossRefGoogle ScholarPubMed
Luo, X., Tang, Z., Xia, G., Wassmann, K., Matsumoto, T., Rizo, J. & Yu, H. (2004). The Mad2 spindle checkpoint protein has two distinct natively folded states. Nature Structural & Molecular Biology 11(4), 338–345.CrossRefGoogle ScholarPubMed
Makin, O. S., Atkins, E., Sikorski, P., Johansson, J. & Serpell, L. C. (2005). Molecular basis for amyloid fibril formation and stability. Proceedings of the National Academy of Sciences USA 102(2), 315–320.CrossRefGoogle Scholar
Margittai, M., Fasshauer, D., Pabst, S., Jahn, R. & Langen, R. (2001). Homo- and heterooligomeric SNARE complexes studied by site-directed spin labeling. Journal of Biological Chemistry 276(16), 13169–13177.CrossRefGoogle ScholarPubMed
Margittai, M. & Langen, R. (2004). Template-assisted filament growth by parallel stacking of tau. Proceedings of the National Academy of Sciences USA 101(28), 10278–10283.CrossRefGoogle ScholarPubMed
Margittai, M. & Langen, R. (2006a). Side chain-dependent stacking modulates tau filament structure. Journal of Biological Chemistry 281(49), 37820–37827.CrossRefGoogle ScholarPubMed
Margittai, M. & Langen, R. (2006b). Spin labeling analysis of amyloids and other protein aggregates. Methods in Enzymology 413, 122–139.CrossRefGoogle ScholarPubMed
Mchaourab, H. S., Lietzow, M. A., Hideg, K. & Hubbell, W. L. (1996). Motion of spin-labeled side chains in T4 lysozyme. Correlation with protein structure and dynamics. Biochemistry 35(24), 7692–7704.CrossRefGoogle ScholarPubMed
Mchaourab, H. S., Oh, K. J., Fang, C. J. & Hubbell, W. L. (1997). Conformation of T4 lysozyme in solution. Hinge-bending motion and the substrate-induced conformational transition studied by site-directed spin labeling. Biochemistry 36(2), 307–316.CrossRefGoogle ScholarPubMed
Merkel, J. S., Sturtevant, J. M. & Regan, L. (1999). Sidechain interactions in parallel beta sheets: the energetics of cross-strand pairings. Structure 7(11), 1333–1343.CrossRefGoogle ScholarPubMed
Molin, Y. N., Salikhov, K. M. & Zamaraev, K. I. (1980). Spin Exchange. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Monsellier, E., Ramazzotti, M., De Laureto, P. P., Tartaglia, G. G., Taddei, N., Fontana, A., Vendruscolo, M. & Chiti, F. (2007). The distribution of residues in a polypeptide sequence is a determinant of aggregation optimized by evolution. Biophysical Journal 93(12), 4382–4391.CrossRefGoogle Scholar
Muller, S. A. & Engel, A. (2001). Structure and mass analysis by scanning transmission electron microscopy. Micron 32(1), 21–31.CrossRefGoogle ScholarPubMed
Nelson, R., Sawaya, M. R., Balbirnie, M., Madsen, A. O., Riekel, C., Grothe, R. & Eisenberg, D. (2005). Structure of the cross-beta spine of amyloid-like fibrils. Nature 435(7043), 773–778.CrossRefGoogle ScholarPubMed
Nilsson, M. R. (2004). Techniques to study amyloid fibril formation in vitro. Methods 34(1), 151–160.CrossRefGoogle ScholarPubMed
Onuchic, J. N., Beratan, D. N., Winkler, J. R. & Gray, H. B. (1992). Pathway analysis of protein electron-transfer reactions. Annual Review of Biophysics and Biomolecular Structure 21, 349–377.CrossRefGoogle ScholarPubMed
Padmavathi, P. V. & Steinhoff, H. J. (2008). Conformation of the closed channel state of colicin A in proteoliposomes: an umbrella model. Journal of Molecular Biology 378(1), 204–214.CrossRefGoogle ScholarPubMed
Paravastu, A. K., Petkova, A. T. & Tycko, R. (2006). Polymorphic fibril formation by residues 10–40 of the Alzheimer's beta-amyloid peptide. Biophysical Journal 90(12), 4618–4629.CrossRefGoogle ScholarPubMed
Pawar, A. P., Dubay, K. F., Zurdo, J., Chiti, F., Vendruscolo, M. & Dobson, C. M. (2005). Prediction of ‘aggregation-prone’ and ‘aggregation-susceptible’ regions in proteins associated with neurodegenerative diseases. Journal of Molecular Biology 350(2), 379–392.CrossRefGoogle ScholarPubMed
Pedersen, J. S., Dikov, D., Flink, J. L., Hjuler, H. A., Christiansen, G. & Otzen, D. E. (2006). The changing face of glucagon fibrillation: structural polymorphism and conformational imprinting. Journal of Molecular Biology 355(3), 501–523.CrossRefGoogle ScholarPubMed
Perozo, E., Cortes, D. M. & Cuello, L. G. (1998). Three-dimensional architecture and gating mechanism of a K+ channel studied by EPR spectroscopy. Nature Structural Biology 5(6), 459–469.CrossRefGoogle Scholar
Petkova, A. T., Buntkowsky, G., Dyda, F., Leapman, R. D., Yau, W. M. & Tycko, R. (2004). Solid state NMR reveals a pH-dependent antiparallel beta-sheet registry in fibrils formed by a beta-amyloid peptide. Journal of Molecular Biology 335(1), 247–260.CrossRefGoogle ScholarPubMed
Petkova, A. T., Ishii, Y., Balbach, J. J., Antzutkin, O. N., Leapman, R. D., Delaglio, F. & Tycko, R. (2002). A structural model for Alzheimer's beta-amyloid fibrils based on experimental constraints from solid state NMR. Proceedings of the National Academy of Sciences USA 99(26), 16742–16747.CrossRefGoogle ScholarPubMed
Petkova, A. T., Leapman, R. D., Guo, Z., Yau, W. M., Mattson, M. P. & Tycko, R. (2005). Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils. Science 307(5707), 262–265.CrossRefGoogle ScholarPubMed
Petkova, A. T., Yau, W. M. & Tycko, R. (2006). Experimental constraints on quaternary structure in Alzheimer's beta-amyloid fibrils. Biochemistry 45(2), 498–512.CrossRefGoogle ScholarPubMed
Prusiner, S. B. (1998). Prions. Proceedings of the National Academy of Sciences USA 95(23), 13363–13383.CrossRefGoogle ScholarPubMed
Rabenstein, M. D. & Shin, Y. K. (1995). Determination of the distance between 2 spin labels attached to a macromolecule. Proceedings of the National Academy of Sciences USA 92(18), 8239–8243.CrossRefGoogle Scholar
Ritter, C., Maddelein, M. L., Siemer, A. B., Luhrs, T., Ernst, M., Meier, B. H., Saupe, S. J. & Riek, R. (2005). Correlation of structural elements and infectivity of the HET-s prion. Nature 435(7043), 844–848.CrossRefGoogle ScholarPubMed
Rizzu, P., Van Swieten, J. C., Joosse, M., Hasegawa, M., Stevens, M., Tibben, A., Niermeijer, M. F., Hillebrand, M., Ravid, R., Oostra, B. A., Goedert, M., Van Duijn, C. M. & Heutink, P. (1999). High prevalence of mutations in the microtubule-associated protein tau in a population study of frontotemporal dementia in the Netherlands. American Journal of Human Genetics 64(2), 414–421.CrossRefGoogle Scholar
Rochet, J. C. & Lansbury, P. T. Jr., (2000). Amyloid fibrillogenesis: themes and variations. Current Opinion in Structural Biology 10(1), 60–68.CrossRefGoogle ScholarPubMed
Ross, E. D., Edskes, H. K., Terry, M. J. & Wickner, R. B. (2005a). Primary sequence independence for prion formation. Proceedings of the National Academy of Sciences USA 102(36), 12825–12830.CrossRefGoogle ScholarPubMed
Ross, E. D., Minton, A. & Wickner, R. B. (2005b). Prion domains: sequences, structures and interactions. Nature Cell Biology 7(11), 1039–1044.CrossRefGoogle ScholarPubMed
Sackmann, E. & Träuble, H. (1972). Studies of crystalline–liquid crystalline phase-transition of lipid model membranes. 2. Analysis of electron-spin resonance spectra of steroid labels incorporated into lipid-membranes. Journal of the American Chemical Society 94(13), 4492–4498.CrossRefGoogle Scholar
Sawaya, M. R., Sambashivan, S., Nelson, R., Ivanova, M. I., Sievers, S. A., Apostol, M. I., Thompson, M. J., Balbirnie, M., Wiltzius, J. J., McFarlane, H. T., Madsen, A. O., Riekel, C. & Eisenberg, D. (2007). Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 447(7143), 453–457.CrossRefGoogle ScholarPubMed
Schweers, O., Schonbrunn-Hanebeck, E., Marx, A. & Mandelkow, E. (1994). Structural studies of tau protein and Alzheimer paired helical filaments show no evidence for beta-structure. Journal of Biological Chemistry 269(39), 24290–24297.CrossRefGoogle ScholarPubMed
Selkoe, D. J. (2003). Folding proteins in fatal ways. Nature 426(6968), 900–904.CrossRefGoogle ScholarPubMed
Serag, A. A., Altenbach, C., Gingery, M., Hubbell, W. L. & Yeates, T. O. (2002). Arrangement of subunits and ordering of beta-strands in an amyloid sheet. Nature Structural Biology 9(10), 734–739.CrossRefGoogle Scholar
Serpell, L. C., Sunde, M., Benson, M. D., Tennent, G. A., Pepys, M. B. & Fraser, P. E. (2000). The protofilament substructure of amyloid fibrils. Journal of Molecular Biology 300(5), 1033–1039.CrossRefGoogle ScholarPubMed
Shewmaker, F., Ross, E. D., Tycko, R. & Wickner, R. B. (2008). Amyloids of shuffled prion domains that form prions have a parallel in-register beta-sheet structure. Biochemistry 47(13), 4000–4007.CrossRefGoogle ScholarPubMed
Shewmaker, F., Wickner, R. B. & Tycko, R. (2006). Amyloid of the prion domain of Sup35p has an in-register parallel beta-sheet structure. Proceedings of the National Academy of Sciences USA 103(52), 19754–19759.CrossRefGoogle ScholarPubMed
Sipe, J. D. & Cohen, A. S. (2000). Review: history of the amyloid fibril. Journal of Structural Biology 130(2–3), 88–98.CrossRefGoogle ScholarPubMed
Smith, C. K. & Regan, L. (1995). Guidelines for protein design: the energetics of beta sheet side chain interactions. Science 270(5238), 980–982.CrossRefGoogle ScholarPubMed
Steinmetz, M. O., Gattin, Z., Verel, R., Ciani, B., Stromer, T., Green, J. M., Tittmann, P., Schulze-Briese, C., Gross, H., Van Gunsteren, W. F., Meier, B. H., Serpell, L. C., Muller, S. A. & Kammerer, R. A. (2008). Atomic models of de novo designed cc beta-Met amyloid-like fibrils. Journal of Molecular Biology 376(3), 898–912.CrossRefGoogle ScholarPubMed
Sunde, M. & Blake, C. (1997). The structure of amyloid fibrils by electron microscopy and X-ray diffraction. Advances in Protein Chemistry 50, 123–159.CrossRefGoogle ScholarPubMed
Sunde, M. & Blake, C. C. (1998). From the globular to the fibrous state: protein structure and structural conversion in amyloid formation. Quarterly Review of Biophyics 31(1), 1–39.CrossRefGoogle Scholar
Tanaka, M., Chien, P., Naber, N., Cooke, R. & Weissman, J. S. (2004). Conformational variations in an infectious protein determine prion strain differences. Nature 428(6980), 323–328.CrossRefGoogle Scholar
Thomas, D., Schultz, P., Steven, A. C. & Wall, J. S. (1994). Mass analysis of biological macromolecular complexes by STEM. Biology of the Cell 80(2–3), 181–192.CrossRefGoogle ScholarPubMed
Tofaris, G. K. & Spillantini, M. G. (2007). Physiological and pathological properties of alpha-synuclein. Cellular and Molecular Life Sciences 64(17), 2194–2201.CrossRefGoogle ScholarPubMed
Torok, M., Milton, S., Kayed, R., Wu, P., McIntire, T., Glabe, C. G. & Langen, R. (2002). Structural and dynamic features of Alzheimer's Abeta peptide in amyloid fibrils studied by site-directed spin labeling. Journal of Biological Chemistry 277(43), 40810–40815.CrossRefGoogle ScholarPubMed
Toyama, B. H., Kelly, M. J., Gross, J. D. & Weissman, J. S. (2007). The structural basis of yeast prion strain variants. Nature 449(7159), 233–237.CrossRefGoogle ScholarPubMed
True, H. L., Berlin, I. & Lindquist, S. L. (2004). Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 431(7005), 184–187.CrossRefGoogle ScholarPubMed
True, H. L. & Lindquist, S. L. (2000). A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407(6803), 477–483.CrossRefGoogle ScholarPubMed
Tuinstra, R. L., Peterson, F. C., Kutlesa, S., Elgin, E. S., Kron, M. A. & Volkman, B. F. (2008). Interconversion between two unrelated protein folds in the lymphotactin native state. Proceedings of the National Academy of Sciences USA 105(13), 5057–5062.CrossRefGoogle ScholarPubMed
Tycko, R. (2006). Molecular structure of amyloid fibrils: insights from solid-state NMR. Quarterly Reviews of Biophysics 39(1), 1–55.CrossRefGoogle ScholarPubMed
Uptain, S. M. & Lindquist, S. (2002). Prions as protein-based genetic elements. Annual Review of Microbiology 56, 703–741.CrossRefGoogle ScholarPubMed
Von Bergen, M., Barghorn, S., Li, L., Marx, A., Biernat, J., Mandelkow, E. M. & Mandelkow, E. (2001). Mutations of tau protein in frontotemporal dementia promote aggregation of paired helical filaments by enhancing local beta-structure. Journal of Biological Chemistry 276(51), 48165–48174.CrossRefGoogle ScholarPubMed
Wang, S. S., Tobler, S. A., Good, T. A. & Fernandez, E. J. (2003). Hydrogen exchange-mass spectrometry analysis of beta-amyloid peptide structure. Biochemistry 42(31), 9507–9514.CrossRefGoogle ScholarPubMed
Wasmer, C., Lange, A., Van Melckebeke, H., Siemer, A. B., Riek, R. & Meier, B. H. (2008). Amyloid fibrils of the HET-s(218–289) prion form a beta solenoid with a triangular hydrophobic core. Science 319(5869), 1523–1526.CrossRefGoogle Scholar
Wenger, O. S., Leigh, B. S., Villahermosa, R. M., Gray, H. B. & Winkler, J. R. (2005). Electron tunneling through organic molecules in frozen glasses. Science 307(5706), 99–102.CrossRefGoogle ScholarPubMed
West, M. W., Wang, W., Patterson, J., Mancias, J. D., Beasley, J. R. & Hecht, M. H. (1999). De novo amyloid proteins from designed combinatorial libraries. Proceedings of the National Academy of Sciences USA 96(20), 11211–11216.CrossRefGoogle ScholarPubMed
Westermark, P., Benson, M. D., Buxbaum, J. N., Cohen, A. S., Frangione, B., Ikeda, S., Masters, C. L., Merlini, G., Saraiva, M. J. & Sipe, J. D. (2007). A primer of amyloid nomenclature. Amyloid 14(3), 179–183.CrossRefGoogle ScholarPubMed
Whittemore, N. A., Mishra, R., Kheterpal, I., Williams, A. D., Wetzel, R. & Serpersu, E. H. (2005). Hydrogen–deuterium (H/D) exchange mapping of Abeta 1–40 amyloid fibril secondary structure using nuclear magnetic resonance spectroscopy. Biochemistry 44(11), 4434–4441.CrossRefGoogle ScholarPubMed
Wickner, R. B., Dyda, F. & Tycko, R. (2008). Amyloid of Rnq1p, the basis of the [PIN+] prion, has a parallel in-register beta-sheet structure. Proceedings of the National Academy of Sciences USA 105(7), 2403–2408.CrossRefGoogle Scholar
Williams, A. D., Portelius, E., Kheterpal, I., Guo, J. T., Cook, K. D., Xu, Y. & Wetzel, R. (2004). Mapping abeta amyloid fibril secondary structure using scanning proline mutagenesis. Journal of Molecular Biology 335(3), 833–842.CrossRefGoogle ScholarPubMed
Williamson, J. A. & Miranker, A. D. (2007). Direct detection of transient alpha-helical states in islet amyloid polypeptide. Protein Science 16(1), 110–117.CrossRefGoogle ScholarPubMed
Wischik, C. M., Novak, M., Thogersen, H. C., Edwards, P. C., Runswick, M. J., Jakes, R., Walker, J. E., Milstein, C., Roth, M. & Klug, A. (1988). Isolation of a fragment of tau derived from the core of the paired helical filament of Alzheimer disease. Proceedings of the National Academy of Sciences USA 85(12), 4506–4510.CrossRefGoogle ScholarPubMed
Zhang, S. & Rich, A. (1997). Direct conversion of an oligopeptide from a beta-sheet to an alpha-helix: a model for amyloid formation. Proceedings of the National Academy of Sciences USA 94(1), 23–28.CrossRefGoogle Scholar