High-resolution MAS NMR analysis of PI3-SH3 amyloid fibrils: Backbone conformation and implications for protofilament assembly and structure

Biochemistry

Volumn 49, Issue 35, 2010, Pages 7474-7484

  Bayro, Marvin J ^a   Maly, Thorsten ^a   Birkett, Neil R ^b   MacPhee, Cait E ^c   Dobson, Christopher M ^b   Griffin, Robert G ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ELEMENTS; CONFORMATIONS; GLYCOPROTEINS; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYPEPTIDES; RESONANCE; SPIN DYNAMICS; STRUCTURAL ANALYSIS;

AMYLOID FIBRIL; CHEMICAL SHIFT ANALYSIS; CORE STRUCTURE; DEGREE OF STRUCTURAL ORDER; FIBRIL FORMATION; HIGH RESOLUTION; IN-VITRO; INFECTIOUS DISEASE; LOCAL DYNAMICS; MAGIC ANGLE SPINNING; MAS NMR; MECHANISM OF FORMATION; MODEL SYSTEM; MOLECULAR CONFORMATION; MOLECULAR MOTIONS; MOLECULAR PROPERTIES; NATIVE STATE; PI3-KINASE; POLYPEPTIDE CHAIN; PROTEIN SUBUNITS; PROTOFILAMENTS; RESONANCE ASSIGNMENTS; SECONDARY STRUCTURES; SITE-SPECIFIC; SOLID STATE NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SPIN SYSTEMS; STRUCTURAL DATA; STRUCTURAL SIMILARITY;

PROTEINS;

AMYLOID; PHOSPHATIDYLINOSITOL 3 KINASE;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CONFORMATIONAL TRANSITION; NITROGEN NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTON NUCLEAR MAGNETIC RESONANCE; CHEMICAL STRUCTURE; CHEMISTRY; NUCLEAR MAGNETIC RESONANCE; PROTEIN FOLDING; SRC HOMOLOGY DOMAIN;

AMYLOID; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN CONFORMATION; PROTEIN FOLDING; SRC HOMOLOGY DOMAINS;

EID: 77956158248     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100864t     Document Type: Article

References (97)

1. Chiti, F. and Dobson, C. M. (2006) Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75, 333-366
2. Sipe, J. D. (1992) Amyloidosis Annu. Rev. Biochem. 61, 947-975
3. Sunde, M. and Blake, C. C. (1998) From the globular to the fibrous state: Protein structure and structural conversion in amyloid formation Q. Rev. Biophys. 31, 1-39
4. Chiti, F. and Dobson, C. M. (2009) Amyloid formation by globular proteins under native conditions Nat. Chem. Biol. 5, 15-22
5. Sacchettini, J. C. and Kelly, J. W. (2002) Therapeutic Strategies for Human Amyloid Diseases Nat. Rev. Drug Discovery 1, 267-275
6. Dobson, C. M. (2003) Protein folding and misfolding Nature 426, 884-890
7. Si, K., Lindquist, S., and Kandel, E. R. (2003) A neuronal isoform of the aplysia CPEB has prion-like properties Cell 115, 879-891
8. Coustou, V., Deleu, C., Saupe, S., and Begueret, J. (1997) The protein product of the het-s heterokaryon incompatibility gene of the fungus Podospora anserina behaves as a prion analog Proc. Natl. Acad. Sci. U.S.A. 94, 9773-9778
9. Chapman, M. R., Robinson, L. S., Pinkner, J. S., Roth, R., Heuser, J., Hammar, M., Normark, S., and Hultgren, S. J. (2002) Role of Escherichia coli curli operons in directing amyloid fiber formation Science 295, 851-855
10. Berson, J. F., Theos, A. C., Harper, D. C., Tenza, D., Raposo, G., and Marks, M. S. (2003) Proprotein convertase cleavage liberates a fibrillogenic fragment of a resident glycoprotein to initiate melanosome biogenesis J. Cell Biol. 161, 521-533
11. 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
12. Uversky, V. N. and Fink, A. L. (2004) Conformational constraints for amyloid fibrillation: The importance of being unfolded Biochim. Biophys. Acta 1698, 131-153
13. Guijarro, J. I., Sunde, M., Jones, J. A., Campbell, I. D., and Dobson, C. M. (1998) Amyloid Fibril Formation by an SH3 Domain Proc. Natl. Acad. Sci. U.S.A. 95, 4224-4228
14. Liang, J., Chen, J. K., Schreiber, S. T., and Clardy, J. (1996) Crystal structure of PI3K SH3 domain at 2.0 angstroms resolution J. Mol. Biol. 257, 632-643
15. Booker, G. W., Gout, I., Downing, A. K., Driscoll, P. C., Boyd, J., Waterfield, M. D., and Campbell, I. D. (1993) Solution structure and ligand-binding site of the SH3 domain of the p85 α subunit of phosphatidylinositol 3-kinase Cell 73, 813-822
16. Koyama, S., Yu, H., Dalgarno, D. C., Shin, T. B., Zydowsky, L. D., and Schreiber, S. L. (1993) Structure of the PI3K SH3 domain and analysis of the SH3 family Cell 72, 945-952
17. 15N assignments and secondary structure of the PI3K SH3 domain FEBS Lett. 324, 93-98
18. Ahn, H. C., Le, Y. T., Nagchowdhuri, P. S., Derose, E. F., Putnam-Evans, C., London, R. E., Markley, J. L., and Lim, K. H. (2006) NMR characterizations of an amyloidogenic conformational ensemble of the PI3K SH3 domain Protein Sci. 15, 2552-2557
19. Zurdo, J., Guijarro, J. I., and Dobson, C. M. (2001) Preparation and characterization of purified amyloid fibrils J. Am. Chem. Soc. 123, 8141-8142
20. Jimenez, J., Guijarro, J., Orlova, E., Zurdo, J., Dobson, C., Sunde, M., and Saibil, H. (1999) Cryo-electron microscopy structure of an SH3 amyloid fibril and model of the molecular packing EMBO J. 18, 815-821
21. Zurdo, J., Guijarro, J. I., Jimenez, J. L., Saibil, H. R., and Dobson, C. M. (2001) Dependence on solution conditions of aggregation and amyloid formation by an SH3 domain J. Mol. Biol. 311, 325-340
22. Polverino de Laureto, P., Taddei, N., Frare, E., Capanni, C., Costantini, S., Zurdo, J., Chiti, F., Dobson, C. M., and Fontana, A. (2003) Protein aggregation and amyloid fibril formation by an SH3 domain probed by limited proteolysis J. Mol. Biol. 334, 129-141
23. Carulla, N., Caddy, G. L., Hall, D. R., Zurdo, J., Gairi, M., Feliz, M., Giralt, E., Robinson, C. V., and Dobson, C. M. (2005) Molecular recycling within amyloid fibrils Nature 436, 554-558
24. Sunde, M., Serpell, L. C., Bartlam, M., Fraser, P. E., Pepys, M. B., and Blake, C. C. (1997) Common core structure of amyloid fibrils by synchrotron X-ray diffraction J. Mol. Biol. 273, 729-739
25. Serpell, L. C., Sunde, M., Benson, M. D., Tennent, G. A., Pepys, M. B., and Fraser, P. E. (2000) The protofilament substructure of amyloid fibrils J. Mol. Biol. 300, 1033-1039
26. Harper, J. D., Lieber, C. M., and Lansbury, P. T., Jr. (1997) Atomic force microscopic imaging of seeded fibril formation and fibril branching by the Alzheimer's disease amyloid-β protein Chem. Biol. 4, 951-959
27. Rienstra, C. M., Tucker-Kellogg, L., Jaroniec, C. P., Hohwy, M., Reif, B., McMahon, M. T., Tidor, B., Lozano-Perez, T., and Griffin, R. G. (2002) De novo determination of peptide structure with solid-state magic-angle spinning NMR spectroscopy Proc. Natl. Acad. Sci. U.S.A. 99, 10260-10265
28. Castellani, F., van Rossum, B., Diehl, A., Schubert, M., Rehbein, K., and Oschkinat, H. (2002) Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy Nature 420, 98-102
29. Zech, S. G., Wand, A. J., and McDermott, A. E. (2005) Protein structure determination by high-resolution solid-state NMR spectroscopy: Application to microcrystalline ubiquitin J. Am. Chem. Soc. 127, 8618-8626
30. Loquet, A., Bardiaux, B., Gardiennet, C., Blanchet, C., Baldus, M., Nilges, M., Malliavin, T., and Bockmann, A. (2008) 3D Structure Determination of the Crh Protein from Highly Ambiguous Solid-State NMR Restraints J. Am. Chem. Soc. 130, 3579-3589
31. 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
32. Jaroniec, C. P., MacPhee, C. E., Bajaj, V. S., McMahon, M. T., Dobson, C. M., and Griffin, R. G. (2004) High-resolution molecular structure of a peptide in an amyloid fibril determined by magic angle spinning NMR spectroscopy Proc. Natl. Acad. Sci. U.S.A. 101, 711-716
33. Heise, H., Hoyer, W., Becker, S., Andronesi, O. C., Riedel, D., and Baldus, M. (2005) Molecular-level secondary structure, polymorphism, and dynamics of full-length α-synuclein fibrils studied by solid-state NMR Proc. Natl. Acad. Sci. U.S.A. 102, 15871-15876
34. Balbach, J. J., Ishii, Y., Antzutkin, O. N., Leapman, R. D., Rizzo, N. W., Dyda, F., Reed, J., and Tycko, R. (2000) Amyloid fibril formation by Aβ16-22, a seven-residue fragment of the Alzheimer's β-amyloid peptide, and structural characterization by solid state NMR Biochemistry 39, 13748-13759
35. Antzutkin, O. N., Leapman, R. D., Balbach, J. J., and Tycko, R. (2002) Supramolecular structural constraints on Alzheimer's β-amyloid fibrils from electron microscopy and solid-state nuclear magnetic resonance Biochemistry 41, 15436-15450
36. 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
37. Paravastu, A. K., Petkova, A. T., and Tycko, R. (2006) Polymorphic fibril formation by residues 10-40 of the Alzheimer's β-amyloid peptide Biophys. J. 90, 4618-4629
38. Petkova, A. T., Yau, W. M., and Tycko, R. (2006) Experimental constraints on quaternary structure in Alzheimer's β-amyloid fibrils Biochemistry 45, 498-512
39. 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
40. Debelouchina, G. T., Platt, G. W., Bayro, M. J., Radford, S. E., and Griffin, R. G. (2010) Magic angle spinning NMR analysis of β2-microglobulin amyloid fibrils in two distinct morphologies J. Am. Chem. Soc. 132, 10414-10423
41. Siemer, A. B., Ritter, C., Ernst, M., Riek, R., and Meier, B. H. (2005) High-resolution solid-state NMR spectroscopy of the prion protein HET-s in its amyloid conformation Angew. Chem., Int. Ed. 44, 2441-2444
42. Chan, J. C., Oyler, N. A., Yau, W. M., and Tycko, R. (2005) Parallel β-sheets and polar zippers in amyloid fibrils formed by residues 10-39 of the yeast prion protein Ure2p Biochemistry 44, 10669-10680
43. Andronesi, O. C., Becker, S., Seidel, K., Heise, H., Young, H. S., and Baldus, M. (2005) Determination of membrane protein structure and dynamics by magic-angle-spinning solid-state NMR spectroscopy J. Am. Chem. Soc. 127, 12965-12974
44. Siemer, A. B., Arnold, A. A., Ritter, C., Westfeld, T., Ernst, M., Riek, R., and Meier, B. H. (2006) Observation of highly flexible residues in amyloid fibrils of the HET-s prion J. Am. Chem. Soc. 128, 13224-13228
45. Tycko, R. (2006) Molecular structure of amyloid fibrils: Insights from solid-state NMR Q. Rev. Biophys. 39, 1-55
46. Curtis-Fisk, J., Spencer, R. M., and Weliky, D. P. (2008) Native conformation at specific residues in recombinant inclusion body protein in whole cells determined with solid-state NMR spectroscopy J. Am. Chem. Soc. 130, 12568-12569
47. Sivertsen, A. C., Bayro, M. J., Belenky, M., Griffin, R. G., and Herzfeld, J. (2009) Solid-state NMR evidence for inequivalent GvpA subunits in gas vesicles J. Mol. Biol. 387, 1032-1039
48. Han, Y., Ahn, J., Concel, J., Byeon, I. L., Gronenborn, A. M., Yang, J., and Polenova, T. (2010) Solid-State NMR Studies of HIV-1 Capsid Protein Assemblies J. Am. Chem. Soc. 132, 1976-1987
49. 13C NMR relaxation analysis J. Am. Chem. Soc. 118, 9255-9264
50. Hong, M. and Jakes, K. (1999) Selective and extensive C-13 labeling of a membrane protein for solid-state NMR investigations J. Biomol. NMR 14, 71-74
51. 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, 6951-6958
52. Bennett, A. E., Griffin, R. G., Ok, J. H., and Vega, S. (1992) Chemical shift correlation spectroscopy in rotating solids: Radio frequency-driven dipolar recoupling and longitudinal exchange J. Chem. Phys. 96, 8624-8627
53. Bennett, A. E., Rienstra, C. M., Griffiths, J. M., Zhen, W., Lansbury, P. T., Jr., and Griffin, R. G. (1998) Homonuclear radio frequency-driven recoupling in rotating solids J. Chem. Phys. 108, 9463-9479
54. Bayro, M. J., Ramachandran, R., Caporini, M. A., Eddy, M. T., and Griffin, R. G. (2008) Radio frequency-driven recoupling at high magic-angle spinning frequencies: Homonuclear recoupling sans heteronuclear decoupling J. Chem. Phys. 128, 052321
55. Verel, R., Ernst, M., and Meier, B. H. (2001) Adiabatic dipolar recoupling in solid-state NMR: The DREAM scheme J. Magn. Reson. 150, 81-99
56. De Paëpe, G., Bayro, M. J., Lewandowski, J., and Griffin, R. G. (2006) Broadband homonuclear correlation spectroscopy at high magnetic fields and MAS frequencies J. Am. Chem. Soc. 128, 1776-1777
57. 13C cross polarization-magic-angle spinning J. Magn. Reson. 47, 462-475
58. 13C Nuclei in Protein MAS NMR Spectroscopy Angew. Chem., Int. Ed. 48, 5708-5710
59. 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
60. Hing, A. W., Vega, S., and Schaefer, J. (1992) Transferred-echo double-resonance NMR J. Magn. Reson. 96, 205-209
61. Michal, C. A. and Jelinski, L. W. (1997) REDOR 3D: Heteronuclear distance measurements in uniformly labeled and natural abundance solids J. Am. Chem. Soc. 119, 9059-9060
62. 15N-Labeled Solids J. Am. Chem. Soc. 124, 10728-10742
63. Morcombe, C. R. and Zilm, K. W. (2003) Chemical shift referencing in MAS solid state NMR J. Magn. Reson. 162, 479-486
64. Harris, R. K., Becker, E. D., Cabral de Menezes, S. M., Goodfellow, R., and Granger, P. (2001) NMR nomenclature. Nuclear spin properties and conventions for chemical shifts (IUPAC Recommendations 2001) Pure Appl. Chem. 73, 1795-1818
65. 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
66. 13C chemical-shift data J. Biomol. NMR 4, 171-180
67. Zhang, H., Neal, S., and Wishart, D. S. (2003) RefDB: A database of uniformly referenced protein chemical shifts J. Biomol. NMR 25, 173-195
68. 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
69. Helmus, J. J., Surewicz, K., Nadaud, P. S., Surewicz, W. K., and Jaroniec, C. P. (2008) Molecular conformation and dynamics of the Y145Stop variant of human prion protein in amyloid fibrils Proc. Natl. Acad. Sci. U.S.A. 105, 6284-6289
70. Igumenova, T. I., McDermott, A. E., Zilm, K. W., Martin, R. W., Paulson, E. K., and Wand, A. J. (2004) Assignments of carbon NMR resonances for microcrystalline ubiquitin J. Am. Chem. Soc. 126, 6720-6727
71. 13C chemical shift assignments and conformational analysis J. Am. Chem. Soc. 127, 12291-12305
72. Bockmann, A., Lange, A., Galinier, A., Luca, S., Giraud, N., Juy, M., Heise, H., Montserret, R., Penin, F., and Baldus, M. (2003) Solid state NMR sequential resonance assignments and conformational analysis of the 2 - 10.4 kDa dimeric form of the Bacillus subtilis protein Crh J. Biomol. NMR 27, 323-339
73. 15N resonance assignment of parts of the HET-s prion protein in its amyloid form J. Biomol. NMR 34, 75-87
74. Petkova, A. T., Ishii, Y., Balbach, J. J., Antzutkin, O. N., Leapman, R. D., Delaglio, F., and Tycko, R. (2002) A structural model for Alzheimer's β-amyloid fibrils based on experimental constraints from solid state NMR Proc. Natl. Acad. Sci. U.S.A. 99, 16742-16747
75. Seidel, K., Lange, A., Becker, S., Hughes, C. E., Heise, H., and Baldus, M. (2004) Protein solid-state NMR resonance assignments from (C-13, C-13) correlation spectroscopy Phys. Chem. Chem. Phys. 6, 5090-5093
76. Bayro, M. J., Huber, M., Ramachandran, R., Davenport, T. C., Meier, B. H., Ernst, M., and Griffin, R. G. (2009) Dipolar truncation in magic-angle spinning NMR recoupling experiments J. Chem. Phys. 130, 114506
77. Luca, S., Filippov, D. V., van Boom, J. H., Oschkinat, H., de Groot, H. J., and Baldus, M. (2001) Secondary chemical shifts in immobilized peptides and proteins: A qualitative basis for structure refinement under magic angle spinning J. Biomol. NMR 20, 325-331
78. Long, J. R., Sun, B. Q., Bowen, A., and Griffin, R. G. (1994) Molecular Dynamics and Magic Angle Spinning NMR J. Am. Chem. Soc. 116, 11950-11956
79. 6] J. Am. Chem. Soc. 118, 5665-5671
80. Carulla, N., Zhou, M., Arimon, M., Gairí, M., Giralt, E., Robinson, C. V., and Dobson, C. M. (2009) Experimental characterization of disordered and ordered aggregates populated during the process of amyloid fibril formation Proc. Natl. Acad. Sci. U.S.A. 106, 7828-7833
81. Blake, C. and Serpell, L. (1996) Synchrotron X-ray studies suggest that the core of the transthyretin amyloid fibril is a continuous β-sheet helix Structure 4, 989-998
82. Ventura, S., Lacroix, E., and Serrano, L. (2002) Insights into the origin of the tendency of the PI3-SH3 domain to form amyloid fibrils J. Mol. Biol. 322, 1147-1158
83. Ventura, S., Zurdo, J., Narayanan, S., Parreño, M., Mangues, R., Reif, B., Chiti, F., Giannoni, E., Dobson, C. M., Aviles, F. X., and Serrano, L. (2004) Short amino acid stretches can mediate amyloid formation in globular proteins: The Src homology 3 SH3 case Proc. Natl. Acad. Sci. U.S.A. 101, 7258-7263
84. Chiti, F., Stefani, M., Taddei, N., Ramponi, G., and Dobson, C. M. (2003) Rationalization of the effects of mutations on peptide and protein aggregation rates Nature 424, 805-808
85. Buell, A. K., Tartaglia, G. G., Birkett, N. R., Waudby, C. A., Vendruscolo, M., Salvatella, X., Welland, M. E., Dobson, C. M., and Knowles, T. P. (2009) Position-dependent electrostatic protection against protein aggregation ChemBioChem 10, 1309-1312
86. Tartaglia, G. G., Pawar, A. P., Campioni, S., Dobson, C. M., Chiti, F., and Vendruscolo, M. (2008) Prediction of aggregation-prone regions in structured proteins J. Mol. Biol. 380, 425-436
87. Tartaglia, G. G. and Vendruscolo, M. (2008) The Zyggregator method for predicting protein aggregation propensities Chem. Soc. Rev. 37, 1395-1401
88. Otzen, D. E. and Oliveberg, M. (1999) Salt-induced detour through compact regions of the protein folding landscape Proc. Natl. Acad. Sci. U.S.A. 96, 11746-11751
89. Matysiak, S. and Clementi, C. (2006) Minimalist protein model as a diagnostic tool for misfolding and aggregation J. Mol. Biol. 363, 297-308
90. Serio, T. R., Cashikar, A. G., Kowal, A. S., Sawicki, G. J., Moslehi, J. J., Serpell, L., Arnsdorf, M. F., and Lindquist, S. L. (2000) Nucleated conformational conversion and the replication of conformational information by a prion determinant Science 289, 1317-1321
91. Orte, A., Birkett, N. R., Clarke, R. W., Devlin, G. L., Dobson, C. M., and Klenerman, D. (2008) Direct characterization of amyloidogenic oligomers by single-molecule fluorescence Proc. Natl. Acad. Sci. U.S.A. 105, 14424-14429
92. West, M. W., Wang, W. X., Patterson, J., Mancias, J. D., Beasley, J. R., and Hecht, M. H. (1999) De novo amyloid proteins from designed combinatorial libraries Proc. Natl. Acad. Sci. U.S.A. 96, 11211-11216
93. Broome, B. M. and Hecht, M. H. (2000) Nature disfavors sequences of alternating polar and non-polar amino acids: Implications for amyloidogenesis J. Mol. Biol. 296, 961-968
94. Bader, R., Bamford, R., Zurdo, J., Luisi, B. F., and Dobson, C. M. (2006) Probing the mechanism of amyloidogenesis through a tandem repeat of the PI3-SH3 domain suggests a generic model for protein aggregation and fibril formation J. Mol. Biol. 356, 189-208
95. Wasmer, C., Lange, A., Van Melckebeke, H., Siemer, A. B., Riek, R., and Meier, B. H. (2008) Amyloid fibrils of the HET-s(218-289) prion form a β solenoid with a triangular hydrophobic core Science 319, 1523-1526
96. Iwata, K., Fujiwara, T., Matsuki, Y., Akutsu, H., Takahashi, S., Naiki, H., and Goto, Y. (2006) 3D structure of amyloid protofilaments of β2-microglobulin fragment probed by solid-state NMR Proc. Natl. Acad. Sci. U.S.A. 103, 18119-18124
97. Robustelli, P., Cavalli, A., and Vendruscolo, M. (2008) Determination of protein structures in the solid state from NMR chemical shifts Structure 16, 1764-1769