Structural characterization of GNNQQNY amyloid fibrils by magic angle spinning NMR

Biochemistry

Volumn 49, Issue 44, 2010, Pages 9457-9469

  Van Der Wel, Patrick C A ^a,b   Lewandowski, Józef R ^a,c   Griffin, Robert G ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITÉ LYON 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHARACTERIZATION; CHEMICAL SHIFT; GLYCOPROTEINS; PEPTIDES;

CHEMICAL SHIFT ASSIGNMENT; COMPUTATIONAL ANALYSIS; CRYSTAL FORMATION; EXPERIMENTAL CHARACTERIZATION; INTERMOLECULAR CONTACTS; MAGIC ANGLE SPINNING NMR; PEPTIDE CONFORMATION; STRUCTURAL CHARACTERIZATION;

MAGIC ANGLE SPINNING;

AMYLOID;

ARTICLE; CRYSTALLIZATION; MAGIC ANGLE SPINNING NUCLEAR MAGNETIC RESONANCE; MECHANICAL TORSION; NUCLEAR MAGNETIC RESONANCE; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY;

EID: 78149340576     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100077x     Document Type: Article

References (99)

1. Chiti, F. and Dobson, C. M. (2006) Protein Misfolding, Functional Amyloid, and Human Disease Annu. Rev. Biochem. 75, 333-366
2. Langkilde, A. E. and Vestergaard, B. (2009) Methods for Structural Characterization of Prefibrillar Intermediates and Amyloid Fibrils FEBS Lett. 583, 2600-2609
3. Ma, B. and Nussinov, R. (2006) Simulations as Analytical Tools to Understand Protein Aggregation and Predict Amyloid Conformation Curr. Opin. Chem. Biol. 10, 445-452
4. Nelson, R., Sawaya, M. R., Balbirnie, M., Madsen, A. O., Riekel, C., Grothe, R., and Eisenberg, D. (2005) Structure of the Cross-Beta Spine of Amyloid-Like Fibrils Nature 435, 773-778
5. Sawaya, M. R., Sambashivan, S., Nelson, R., Ivanova, M. I., Sievers, S. A., Apostol, M. I., Thompson, M. J., Balbirnie, M., Wiltzius, J. J. W., McFarlane, H. T., Madsen, A. O., Riekel, C., and Eisenberg, D. (2007) Atomic Structures of Amyloid Cross-β Spines Reveal Varied Steric Zippers Nature 447, 453-457
6. Balbirnie, M., Grothe, R., and Eisenberg, D. S. (2001) An Amyloid-Forming Peptide from the Yeast Prion Sup35 Reveals a Dehydrated Beta-Sheet Structure for Amyloid Proc. Natl. Acad. Sci. U.S.A. 98, 2375-2380
7. Gsponer, J., Haberthür, U., and Caflisch, A. (2003) The Role of Side-Chain Interactions in the Early Steps of Aggregation: Molecular Dynamics Simulations of an Amyloid-Forming Peptide from the Yeast Prion Sup35 Proc. Natl. Acad. Sci. U.S.A. 100, 5154-5159
8. Cecchini, M., Rao, F., Seeber, M., and Caflisch, A. (2004) Replica Exchange Molecular Dynamics Simulations of Amyloid Peptide Aggregation J. Chem. Phys. 121, 10748-10756
9. Lipfert, J., Franklin, J., Wu, F., and Doniach, S. (2005) Protein Misfolding and Amyloid Formation for the Peptide GNNQQNY from Yeast Prion Protein Sup35: Simulation by Reaction Path Annealing J. Mol. Biol. 349, 648-658
10. Fernández, A. (2005) What Factor Drives the Fibrillogenic Association of Beta-Sheets? FEBS Lett. 579, 6635-6640
11. Zheng, J., Ma, B., Tsai, C.-J., and Nussinov, R. (2006) Structural Stability and Dynamics of an Amyloid-Forming Peptide GNNQQNY from the Yeast Prion Sup-35 Biophys. J. 91, 824-833
12. Esposito, L., Pedone, C., and Vitagliano, L. (2006) Molecular Dynamics Analyses of Cross-Beta-Spine Steric Zipper Models: Beta-Sheet Twisting and Aggregation Proc. Natl. Acad. Sci. U.S.A. 103, 11533-11538
13. Zhang, Z., Chen, H., Bai, H., and Lai, L. (2007) Molecular Dynamics Simulations on the Oligomer-Formation Process of the GNNQQNY Peptide from Yeast Prion Protein Sup35 Biophys. J. 93, 1484-1492
14. Wu, C., Wang, Z., Lei, H., Zhang, W., and Duan, Y. (2007) Dual Binding Modes of Congo Red to Amyloid Protofibril Surface Observed in Molecular Dynamics Simulations J. Am. Chem. Soc. 129, 1225-1232
15. Tsemekhman, K., Goldschmidt, L., Eisenberg, D., and Baker, D. (2007) Cooperative Hydrogen Bonding in Amyloid Formation Protein Sci. 16, 761-764
16. Strodel, B., Whittleston, C. S., and Wales, D. J. (2007) Thermodynamics and Kinetics of Aggregation for the GNNQQNY Peptide J. Am. Chem. Soc. 129, 16005-16014
17. Knowles, T. P., Fitzpatrick, A. W., Meehan, S., Mott, H. R., Vendruscolo, M., Dobson, C. M., and Welland, M. E. (2007) Role of Intermolecular Forces in Defining Material Properties of Protein Nanofibrils Science 318, 1900-1903
18. Meli, M., Morra, G., and Colombo, G. (2008) Investigating the Mechanism of Peptide Aggregation: Insights from Mixed Monte Carlo-Molecular Dynamics Simulations Biophys. J. 94, 4414-4426
19. De Simone, A., Esposito, L., Pedone, C., and Vitagliano, L. (2008) Insights into Stability and Toxicity of Amyloid-Like Oligomers by Replica Exchange Molecular Dynamics Analyses Biophys. J. 95, 1965-1973
20. Wang, J., Tan, C., Chen, H.-F., and Luo, R. (2008) All-Atom Computer Simulations of Amyloid Fibrils Disaggregation Biophys. J. 95, 5037-5047
21. Esposito, L., Paladino, A., Pedone, C., and Vitagliano, L. (2008) Insights into Structure, Stability, and Toxicity of Monomeric and Aggregated Polyglutamine Models from Molecular Dynamics Simulations Biophys. J. 94, 4031-4040
22. Vitagliano, L., Esposito, L., Pedone, C., and De Simone, A. (2008) Stability of Single Sheet GNNQQNY Aggregates Analyzed by Replica Exchange Molecular Dynamics: Antiparallel versus Parallel Association Biochem. Biophys. Res. Commun. 377, 1036-1041
23. Periole, X., Rampioni, A., Vendruscolo, M., and Mark, A. E. (2009) Factors That Affect the Degree of Twist in Beta-Sheet Structures: A Molecular Dynamics Simulation Study of a Cross-Beta Filament of the GNNQQNY Peptide J. Phys. Chem. B 113, 1728-1737
24. Berryman, J. T., Radford, S. E., and Harris, S. A. (2009) Thermodynamic Description of Polymorphism in Q- and N-Rich Peptide Aggregates Revealed by Atomistic Simulation Biophys. J. 97, 1-11
25. Reddy, G., Straub, J. E., and Thirumalai, D. (2009) Dynamics of locking of peptides onto growing amyloid fibrils Proc. Natl. Acad. Sci. U.S.A. 106, 11948-11953
26. Brovchenko, I., Singh, G., and Winter, R. (2009) Aggregation of Amyloidogenic Peptides near Hydrophobic and Hydrophilic Surfaces Langmuir 25, 8111-8116
27. Park, J., Kahng, B., and Hwang, W. (2009) Thermodynamic Selection of Steric Zipper Patterns in the Amyloid Cross-β Spine PLoS Comput. Biol. 5, e1000492
28. Glabe, C. G. (2008) Structural Classification of Toxic Amyloid Oligomers J. Biol. Chem. 283, 29639-29643
29. Diaz-Avalos, R., Long, C., Fontano, E., Balbirnie, M., Grothe, R., Eisenberg, D., and Caspar, D. L. D. (2003) Cross-beta order and diversity in nanocrystals of an amyloid-forming peptide J. Mol. Biol. 330, 1165-1175
30. Van der Wel, P. C. A., Lewandowski, J. R., and Griffin, R. G. (2007) Solid State NMR Study of Amyloid Nanocrystals and Fibrils Formed by the Peptide GNNQQNY from Yeast Prion Protein Sup35p J. Am. Chem. Soc. 129, 5117-5130
31. Jimenez, J. L., Guijarro, J. I., Orlova, E., Zurdo, J., Dobson, C. M., Sunde, M., and Saibil, H. R. (1999) Cryo-electron Microscopy Structure of an SH3 Amyloid Fibril and Model of the Molecular Packing EMBO J. 18, 815-821
32. Jimenez, J. L., Nettleton, E. J., Bouchard, M., Robinson, C. V., Dobson, C. M., and Saibil, H. R. (2002) The Protofilament Structure of Insulin Amyloid Fibrils Proc. Natl. Acad. Sci. U.S.A. 99, 9196-9201
33. Ferguson, N., Berriman, J., Petrovich, M., Sharpe, T. D., Finch, J. T., and Fersht, A. R. (2003) Rapid Amyloid Fiber Formation from the Fast-Folding WW Domain FBP28 Proc. Natl. Acad. Sci. U.S.A. 100, 9814-9819
34. Saiki, M., Honda, S., Kawasaki, K., Zhou, D., Kaito, A., Konakahara, T., and Morii, H. (2005) Higher-Order Molecular Packing in Amyloid-Like Fibrils Constructed with Linear Arrangements of Hydrophobic and Hydrogen-Bonding Side-Chains J. Mol. Biol. 348, 983-998
35. Petkova, A. T., Leapman, R. D., Guo, Z., Yau, W.-M., Mattson, M. P., and Tycko, R. (2005) Self-Propagating, Molecular-Level Polymorphism in Alzheimer's β-Amyloid Fibrils Science 307, 262-265
36. Luca, S., Yau, W. M., Leapman, R., and Tycko, R. (2007) Peptide Conformation and Supramolecular Organization in Amylin Fibrils: Constraints from Solid-State NMR Biochemistry 46, 13505-13522
37. Marshall, K. E., Hicks, M. R., Williams, T. L., Hoffmann, S. V., Rodger, A., Dafforn, T. R., and Serpell, L. C. (2010) Characterizing the Assembly of the Sup35 Yeast Prion Fragment, GNNQQNY: Structural Changes Accompany a Fiber-to-Crystal Switch Biophys. J. 98, 330-338
38. Tycko, R. (2006) Molecular Structure of Amyloid Fibrils: Insights from Solid-State NMR Q. Rev. Biophys. 39, 1-55
39. Heise, H. (2008) Solid-State NMR Spectroscopy of Amyloid Proteins ChemBioChem 9, 179-189
40. Costa, P. R., Gross, J. D., Hong, M., and Griffin, R. G. (1997) Solid-State NMR Measurement of ψ in Peptides: a NCCN 2Q-Heteronuclear Local Field Experiment Chem. Phys. Lett. 280, 95-103
41. Gregory, D. M., Mitchell, D. J., Stringer, J. A., Kiihne, S., Shiels, J. C., Callahan, J., Mehta, M. A., and Drobny, G. P. (1995) Windowless Dipolar Recoupling: The Detection of Weak Dipolar Couplings between Spin 1/2 Nuclei with Large Chemical Shift Anisotropies Chem. Phys. Lett. 246, 654-663
42. Gregory, D. M., Benzinger, T. L. S., Burkoth, T. S., Miller-Auer, H., Lynn, D. G., Meredith, S. C., and Botto, R. E. (1998) Dipolar Recoupling NMR of Biomolecular Self-Assemblies: Determining Inter- And Intrastrand Distances in Fibrilized Alzheimer's β-Amyloid Peptide Solid State Nucl. Magn. Reson. 13, 149-166
43. (10-35) Is Parallel β-Sheet with Residues in Exact Register Proc. Natl. Acad. Sci. U.S.A. 95, 13407-13412
44. Caporini, M. A., Bajaj, V. S., Veshtort, M., Fitzpatrick, A., MacPhee, C. E., Vendruscolo, M., Dobson, C. M., and Griffin, R. G. (2010) Accurate Determination of Interstrand Distances and Alignment in Amyloid Fibrils by Magic Angle Spinning NMR. J. Phys. Chem., in press.
45. Caporini, M. A. (2008) Structural Studies of Amyloid Fibrils Using Solid-State NMR, Ph.D. Thesis, Massachusetts Institute of Technology, Cambridge, MA.
46. Bajaj, V. S. (2007) Dynamic Nuclear Polarization in Biomolecular Solid State NMR: Methods and Applications in Peptides and Membrane Proteins, Ph.D. Thesis, Massachusetts Institute of Technology, Cambridge, MA.
47. Costa, P. R., Sun, B., and Griffin, R. G. (2003) Rotational Resonance NMR: Separation of Dipolar Coupling and Zero Quantum Relaxation J. Magn. Reson. 164, 92-103
48. 13C-Labeled Peptides J. Am. Chem. Soc. 125, 15623-15629
49. Raleigh, D. P., Levitt, M. H., and Griffin, R. G. (1988) Rotational Resonance in Solid State NMR Chem. Phys. Lett. 146, 71-76
50. Colombo, M. G., Meier, B. H., and Ernst, R. R. (1988) Rotor-Driven Spin Diffusion in Natural-Abundance C-13 Spin Systems Chem. Phys. Lett. 146, 189
51. Levitt, M. H., Raleigh, D. P., Creuzet, F., and Griffin, R. G. (1990) Theory and Simulations of Homonuclear Spin Pair Systems in Rotating Solids J. Chem. Phys. 92, 6347-6364
52. 13C Distance Measurements in Uniformly Labeled Solids J. Chem. Phys. 124, 214107
53. 13C Distance Measurements in a Microcrystalline Protein via J-Decoupled Rotational Resonance Width Measurements ChemPhysChem 10, 1566-1663
54. Barnes, A. B., Andreas, L. B., Huber, M., Ramachandran, R., van der Wel, P. C. A., Veshtort, M., Griffin, R. G., and Mehta, M. A. (2009) High-Resolution Solid-State NMR Structure of Alanyl-Prolyl-Glycine J. Magn. Reson. 200, 95-100
55. Gullion, T. and Schaefer, J. (1989) Rotational-Echo Double-Resonance NMR J. Magn. Reson. 81, 196-200
56. Hing, A. W., Vega, S., and Schaefer, J. (1992) Transferred-Echo Double-Resonance NMR J. Magn. Reson. 96, 205-209
57. 15N-Labeled Solids J. Am. Chem. Soc. 124, 10728-10742
58. Madine, J., Jack, E., Stockley, P. G., Radford, S. E., Serpell, L. C., and Middleton, D. A. (2008) Structural Insights into the Polymorphism of Amyloid-Like Fibrils Formed by Region 20-29 of Amylin Revealed by Solid-State NMR and X-ray Fiber Diffraction J. Am. Chem. Soc. 130, 14990-15001
59. Gordon, D. J., Balbach, J. J., Tycko, R., and Meredith, S. C. (2004) Increasing the Amphiphilicity of an Amyloidogenic Peptide Changes the [Beta]-Sheet Structure in the Fibrils from Antiparallel to Parallel Biophys. J. 86, 428-434
60. Verel, R., Tomka, I. T., Bertozzi, C., Cadalbert, R., Kammerer, R. A., Steinmetz, M. O., and Meier, B. H. (2008) Polymorphism in an Amyloid-Like Fibril-Forming Model Peptide13 Angew. Chem., Intl. Ed. 47, 5842-5845
61. De Paëpe, G., Lewandowski, J. R., Loquet, A., Böckmann, A., and Griffin, R. G. (2008) Proton Assisted Recoupling and Protein Structure Determination J. Chem. Phys. 129, 245101
62. Stringer, J. A., Bronnimann, C. E., Mullen, C. G., Zhou, D. H., Stellfox, S. A., Li, Y., Williams, E. H., and Rienstra, C. M. (2005) Reduction of RF-Induced Sample Heating with a Scroll Coil Resonator Structure for Solid-State NMR Probes J. Magn. Reson. 173, 40-48
63. Takegoshi, K., Nakamura, S., and Terao, T. (2001) C-13-H-1 Dipolar-Assisted Rotational Resonance in Magic-Angle Spinning NMR Chem. Phys. Lett. 344, 631-637
64. Morcombe, C. R., Gaponenko, V., Byrd, R. A., and Zilm, K. W. (2004) Diluting Abundant Spins by Isotope Edited Radio Frequency Field Assisted Diffusion J. Am. Chem. Soc. 126, 7196-7197
65. Lewandowski, J., De Paëpe, G., and Griffin, R. G. (2007) Proton Assisted Insensitive Nuclei Cross Polarization J. Am. Chem. Soc. 129, 728-729
66. Schaefer, J., McKay, R. A., and Stejskal, E. O. (1979) Double-Cross-Polarization NMR of Solids J. Magn. Reson. 34, 443-447
67. Baldus, M., Petkova, A. T., Herzfeld, J., and Griffin, R. G. (1998) Cross Polarization in the Tilted Frame: Assignment and Spectral Simplification in Heteronuclear Spin Systems Mol. Phys. 95, 1197-1207
68. Petkova, A. T., Baldus, M., Belenky, M., Hong, M., Griffin, R. G., and Herzfeld, J. (2003) Backbone and Side Chain Assignment Strategies for Multiply Labeled Membrane Peptides and Proteins in the Solid State J. Magn. Reson. 160, 1-12
69. 15N] Labeled Membrane-Protein Complex at Ultra-High Magnetic Fields J. Biomol. NMR 19, 243-253
70. 15N Signal Assignments of the α-Spectrin SH3 Domain by Magic Angle Spinning Solid-State NMR at 17.6 T ChemBioChem 2, 272-281
71. Bennett, A. E., Rienstra, C. M., Auger, M., Lakshmi, K. V., and Griffin, R. G. (1995) Heteronuclear Decoupling in Rotating Solids J. Chem. Phys. 103, 6951-6957
72. Morcombe, C. R. and Zilm, K. W. (2003) Chemical Shift Referencing in MAS Solid State NMR J. Magn. Reson. 162, 479-486
73. Markley, J. L., Bax, A., Arata, Y., Hilbers, C. W., Kaptein, R., Sykes, B. D., Wright, P. E., and Wüthrich, K. (1998) Recommendations for the Presentation of NMR Structures of Proteins and Nucleic Acids Pure Appl. Chem. 70, 117-142 (Pubitemid 128484457)
74. Harris, R. K., Becker, E. D., Cabral de Menezes, S. M., Goodfellow, R., and Granger, P. (2002) NMR Nomenclature: Nuclear Spin Properties and Conventions for Chemical Shifts Solid State Nucl. Magn. Reson. 22, 458-483
75. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a Multidimensional Spectral Processing System Based on UNIX Pipes J. Biomol. NMR 6, 277-293
76. Goddard, T. D. and Kneller, D. G. (2006) SPARKY 3, University of California, San Francisco.
77. Vranken, W. F., Boucher, W., Stevens, T. J., Fogh, R. H., Pajon, A., Llinas, M., Ulrich, E. L., Markley, J. L., Ionides, J., and Laue, E. D. (2005) The CCPN Data Model for NMR Spectroscopy: Development of a Software Pipeline Proteins: Struct., Funct., Bioinf. 59, 687-696
78. Cornilescu, G., Delaglio, F., and Bax, A. (1999) Protein Backbone Angle Restraints from Searching a Database for Chemical Shift and Sequence Homology J. Biomol. NMR 13, 289-302
79. Feng, X., Lee, Y. K., Sandström, D., Eden, M., Maisel, H., Sebald, A., and Levitt, M. H. (1996) Direct Determination of a Molecular Torsional Angle by Solid-State NMR Chem. Phys. Lett. 257, 314-320
80. Hohwy, M., Rienstra, C. M., Jaroniec, C. P., and Griffin, R. G. (1999) Fivefold Symmetric Homonuclear Dipolar Recoupling in Rotating Solids: Application to Double Quantum Spectroscopy J. Chem. Phys. 110, 7983-7992
81. Veshtort, M. and Griffin, R. G. (2006) SPINEVOLUTION: A Powerful Tool for the Simulation of Solid and Liquid State NMR Experiments J. Magn. Reson. 178, 248-282
82. 13C Chemical-Shift Data J. Biomol. NMR 4, 171-180
83. Zhang, H., Neal, S., and Wishart, D. S. (2003) RefDB: A Database of Uniformly Referenced Protein Chemical Shifts J. Biomol. NMR 25, 173-195
84. Jaroniec, C. P., MacPhee, C. E., Astrof, N. S., Dobson, C. M., and Griffin, R. G. (2002) Molecular Conformation of a Peptide Fragment of Transthyretin in an Amyloid Fibril Proc. Natl. Acad. Sci. U.S.A. 99, 16748-16753
85. 13C Chemical Shift Tensors for Intermolecular Shielding in 4,7-Di-t-butylacenaphthene versus 4,7-Di-t-butylacenaphthylene J. Phys. Chem. A 111, 2020-2027
86. Krissinel, E. and Henrick, K. (2004) Secondary-Structure Matching (SSM), a New Tool for Fast Protein Structure Alignment in Three Dimensions Acta Crystallogr. D 60, 2256-2268
87. Collaborative Computational Project Number 4 (1994) The CCP4 Suite: Programs for Protein Crystallography Acta Crystallogr. D 50, 760-763
88. Bajaj, V. S., van der Wel, P. C. A., and Griffin, R. G. (2008) Observation of a Low-Temperature, Dynamically Driven Structural Transition in a Polypeptide by Solid-State NMR Spectroscopy J. Am. Chem. Soc. 131, 118-128
89. Debelouchina, G. T., Bayro, M. J., Van Der Wel, P. C. A., Caporini, M. A., Barnes, A. B., Rosay, M., Maas, W. E., and Griffin, R. G. (2010) Dynamic Nuclear Polarization-Enhanced Solid-State NMR Spectroscopy of GNNQQNY Nanocrystals and Amyloid Fibrils Phys. Chem. Chem. Phys. 1-11
90. Cheung, M.-S., Maguire, M. L., Stevens, T. J., and Broadhurst, R. W. (2010) DANGLE: A Bayesian Inferential Method for Predicting Protein Backbone Dihedral Angles and Secondary Structure J. Magn. Reson. 202, 223-233
91. Richardson, J. S. and Richardson, D. C. (2002) Natural Beta-Sheet Proteins Use Negative Design to Avoid Edge-to-Edge Aggregation Proc. Natl. Acad. Sci. U.S.A. 99, 2754-2759
92. De Simone, A., Dodson, G. G., Fraternali, F., and Zagari, A. (2006) Water Molecules As Structural Determinants among Prions of Low Sequence Identity FEBS Lett. 580, 2488-2494
93. Nielsen, J. T., Bjerring, M., Jeppesen, M. D., Pedersen, R. O., Pedersen, J. M., Hein, Kim L., Vosegaard, T., Skrydstrup, T., Otzen, D. E., and Nielsen, N. C. (2009) Unique Identification of Supramolecular Structures in Amyloid Fibrils by Solid-State NMR Spectroscopy Angew. Chem., Intl. Ed. 48, 2118-2121
94. Shewmaker, F., Kryndushkin, D., Chen, B., Tycko, R., and Wickner, R. B. (2009) Two Prion Variants of Sup35p Have In-Register Parallel Beta-Sheet Structures, Independent of Hydration Biochemistry 48, 5074-5082
95. Wickner, R. B., Dyda, F., and Tycko, R. (2008) Amyloid of Rnq1p, the Basis of the [PIN+] Prion, Has a Parallel In-Register Beta-Sheet Structure Proc. Natl. Acad. Sci. U.S.A. 105, 2403-2408
96. Baxa, U., Wickner, R. B., Steven, A. C., Anderson, D. E., Marekov, L. N., Yau, W.-M., and Tycko, R. (2007) Characterization of Beta-Sheet Structure in Ure2p1-89 Yeast Prion Fibrils by Solid-State Nuclear Magnetic Resonance Biochemistry 46, 13149-13162
97. Shewmaker, F., Wickner, R. B., and Tycko, R. (2006) Amyloid of the Prion Domain of Sup35p Has an In-Register Parallel Beta-Sheet Structure Proc. Natl. Acad. Sci. U.S.A. 103, 19754-19759
98. Ross, E. D., Minton, A., and Wickner, R. B. (2005) Prion Domains: Sequences, Structures and Interactions Nat. Cell Biol. 7, 1039-1044
99. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.