Crystal structures of IAPP amyloidogenic segments reveal a novel packing motif of out-of-register beta sheets

Journal of Physical Chemistry B

Volumn 120, Issue 26, 2016, Pages 5810-5816

  Soriaga, Angela B ^a,b,c   Sangwan, Smriti ^a,b,c   MacDonald, Ramsay ^a,b   Sawaya, Michael R ^a,b,c   Eisenberg, David ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTALLOGRAPHY; GLYCOPROTEINS;

BETA-SHEET; ISLET AMYLOID POLYPEPTIDES; PACKING MOTIFS; STRUCTURAL MOTIFS; STRUCTURAL STUDIES; TOXIC SPECIES; TYPE-2 DIABETES;

X RAY CRYSTALLOGRAPHY;

AMYLIN; PEPTIDE; PROTEIN AGGREGATE;

AMINO ACID SEQUENCE; BETA SHEET; CHEMISTRY; HUMAN; MOLECULAR MODEL; PROTEIN DOMAIN; SOLUTION AND SOLUBILITY; SYNTHESIS; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; HUMANS; ISLET AMYLOID POLYPEPTIDE; MODELS, MOLECULAR; PEPTIDES; PROTEIN AGGREGATES; PROTEIN CONFORMATION, BETA-STRAND; PROTEIN INTERACTION DOMAINS AND MOTIFS; SOLUTIONS; THERMODYNAMICS;

EID: 84978036723     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/acs.jpcb.5b09981     Document Type: Article

References (44)

1. Eisenberg, D.; Jucker, M. The Amyloid State of Proteins in Human Diseases Cell 2012, 148, 1188-1203 10.1016/j.cell.2012.02.022
2. Chiti, F.; Dobson, C. M. Protein Misfolding, Functional Amyloid, and Human Disease Annu. Rev. Biochem. 2006, 75, 333-366 10.1146/annurev.biochem.75.101304.123901
3. Xu, J.; Reumers, J.; Couceiro, J. R.; De Smet, F.; Gallardo, R.; Rudyak, S.; Cornelis, A.; Rozenski, J.; Zwolinska, A.; Marine, J.-C. et al. Gain of Function of Mutant p53 by Coaggregation with Multiple Tumor Suppressors Nat. Chem. Biol. 2011, 7, 285-295 10.1038/nchembio.546
4. Makin, O. S.; Serpell, L. C. Structures for Amyloid Fibrils: Structures for Amyloid Fibrils FEBS J. 2005, 272, 5950-5961 10.1111/j.1742-4658.2005.05025.x
5. Nelson, R.; Sawaya, M. R.; Balbirnie, M.; Madsen, A. Ø.; Riekel, C.; Grothe, R.; Eisenberg, D. Structure of the Cross-B Spine of Amyloid-like Fibrils Nature 2005, 435, 773-778 10.1038/nature03680
6. 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. et al. Atomic Structures of Amyloid Cross-B Spines Reveal Varied Steric Zippers Nature 2007, 447, 453-457 10.1038/nature05695
7. Glabe, C. G. Structural Classification of Toxic Amyloid Oligomers J. Biol. Chem. 2008, 283, 29639-29643 10.1074/jbc.R800016200
8. Haass, C.; Selkoe, D. J. Soluble Protein Oligomers in Neurodegeneration: Lessons from the Alzheimer's Amyloid B-Peptide Nat. Rev. Mol. Cell Biol. 2007, 8, 101-112 10.1038/nrm2101
9. Laganowsky, A.; Liu, C.; Sawaya, M. R.; Whitelegge, J. P.; Park, J.; Zhao, M.; Pensalfini, A.; Soriaga, A. B.; Landau, M.; Teng, P. K. et al. Atomic View of a Toxic Amyloid Small Oligomer Science 2012, 335, 1228-1231 10.1126/science.1213151
10. Liu, C.; Sawaya, M. R.; Cheng, P.-N.; Zheng, J.; Nowick, J. S.; Eisenberg, D. Characteristics of Amyloid-Related Oligomers Revealed by Crystal Structures of Macrocyclic B-Sheet Mimics J. Am. Chem. Soc. 2011, 133, 6736-6744 10.1021/ja200222n
11. Liu, C.; Zhao, M.; Jiang, L.; Cheng, P.-N.; Park, J.; Sawaya, M. R.; Pensalfini, A.; Gou, D.; Berk, A. J.; Glabe, C. G. et al. Out-of-Register -Sheets Suggest a Pathway to Toxic Amyloid Aggregates Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 20913-20918 10.1073/pnas.1218792109
12. Cheng, P.-N.; Liu, C.; Zhao, M.; Eisenberg, D.; Nowick, J. S. Amyloid B-Sheet Mimics That Antagonize Protein Aggregation and Reduce Amyloid Toxicity Nat. Chem. 2012, 4, 927-933 10.1038/nchem.1433
13. Cooper, G. J. S.; Willis, A. C.; Clark, A.; Turner, R. C.; Sim, R. B.; Reid, K. B. M. Purification and Characterization of a Peptide from Amyloid-Rich Pancreases of Type 2 Diabetic Patients Proc. Natl. Acad. Sci. U. S. A. 1987, 84, 8628-8632 10.1073/pnas.84.23.8628
14. Westermark, P.; Wernstedt, C.; Wilander, E.; Sletten, K. A Novel Peptide in the Calcitonin Gene Related Peptide Family as an Amyloid Fibril Protein in the Endocrine Pancreas Biochem. Biophys. Res. Commun. 1986, 140, 827-831 10.1016/0006-291X(86)90708-4
15. Kahn, S. E.; Andrikopoulos, S.; Verchere, C. B. Islet Amyloid: A Long-Recognized but Underappreciated Pathological Feature of Type 2 Diabetes Diabetes 1999, 48, 241-253 10.2337/diabetes.48.2.241
16. Cao, P.; Marek, P.; Noor, H.; Patsalo, V.; Tu, L.-H.; Wang, H.; Abedini, A.; Raleigh, D. P. Islet Amyloid: From Fundamental Biophysics to Mechanisms of Cytotoxicity FEBS Lett. 2013, 587, 1106-1118 10.1016/j.febslet.2013.01.046
17. Tenidis, K.; Waldner, M.; Bernhagen, J.; Fischle, W.; Bergmann, M.; Weber, M.; Merkle, M.-L.; Voelter, W.; Brunner, H.; Kapurniotu, A. Identification of a Penta- and Hexapeptide of Islet Amyloid Polypeptide (IAPP) with Amyloidogenic and Cytotoxic Properties J. Mol. Biol. 2000, 295, 1055-1071 10.1006/jmbi.1999.3422
18. Goldsbury, C. S.; Cooper, G. J. S.; Goldie, K. N.; Muller, S.; Saafi, E. L.; Gruijters, W. T. M.; Misur, M. P.; Engel, A.; Aebi, U.; Kistler, J. Polymorphic Fibrillar Assembly of Human Amylin J. Struct. Biol. 1997, 119, 17-27 10.1006/jsbi.1997.3858
19. Madine, J.; Jack, E.; Stockley, P. G.; Radford, S. E.; Serpell, L. C.; Middleton, D. A. 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. 2008, 130, 14990-15001 10.1021/ja802483d
20. Wiltzius, J. J. W.; Sievers, S. A.; Sawaya, M. R.; Cascio, D.; Popov, D.; Riekel, C.; Eisenberg, D. Atomic Structure of the Cross-B Spine of Islet Amyloid Polypeptide (amylin) Protein Sci. 2008, 17, 1467-1474 10.1110/ps.036509.108
21. Wiltzius, J. J. W.; Landau, M.; Nelson, R.; Sawaya, M. R.; Apostol, M. I.; Goldschmidt, L.; Soriaga, A. B.; Cascio, D.; Rajashankar, K.; Eisenberg, D. Molecular Mechanisms for Protein-Encoded Inheritance Nat. Struct. Mol. Biol. 2009, 16, 973-978 10.1038/nsmb.1643
22. Kabsch, W. Automatic Processing of Rotation Diffraction Data from Crystals of Initially Unknown Symmetry and Cell Constants J. Appl. Crystallogr. 1993, 26, 795-800 10.1107/S0021889893005588
23. The CCP4 Suite: Programs for Protein Crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 1994, 50, 760-763 10.1107/S0907444994003112.
24. Read, R. J. Pushing the Boundaries of Molecular Replacement with Maximum Likelihood Acta Crystallogr., Sect. D: Biol. Crystallogr. 2001, 57, 1373-1382 10.1107/S0907444901012471
25. Adams, P. D.; Afonine, P. V.; Bunkóczi, G.; Chen, V. B.; Davis, I. W.; Echols, N.; Headd, J. J.; Hung, L.-W.; Kapral, G. J.; Grosse-Kunstleve, R. W. et al. PHENIX: A Comprehensive Python-Based System for Macromolecular Structure Solution Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010, 66, 213-221 10.1107/S0907444909052925
26. Emsley, P.; Cowtan, K. Coot: Model-Building Tools for Molecular Graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60, 2126-2132 10.1107/S0907444904019158
27. The PyMOL Molecular Graphics System, version 1.5.0.4, Schrödinger, LLC.
28. Goldschmidt, L.; Teng, P. K.; Riek, R.; Eisenberg, D. Identifying the Amylome, Proteins Capable of Forming Amyloid-like Fibrils Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 3487-3492 10.1073/pnas.0915166107
29. Mehta, A. K.; Lu, K.; Childers, W. S.; Liang, Y.; Dublin, S. N.; Dong, J.; Snyder, J. P.; Pingali, S. V.; Thiyagarajan, P.; Lynn, D. G. Facial Symmetry in Protein Self-Assembly J. Am. Chem. Soc. 2008, 130, 9829-9835 10.1021/ja801511n
30. Liang, Y.; Pingali, S. V.; Jogalekar, A. S.; Snyder, J. P.; Thiyagarajan, P.; Lynn, D. G. Cross-Strand Pairing and Amyloid Assembly Biochemistry 2008, 47, 10018-10026 10.1021/bi801081c
31. Prusiner, S. B. A Unifying Role for Prions in Neurodegenerative Diseases Science 2012, 336, 1511-1513 10.1126/science.1222951
32. Brundin, P.; Melki, R.; Kopito, R. Prion-like Transmission of Protein Aggregates in Neurodegenerative Diseases Nat. Rev. Mol. Cell Biol. 2010, 11, 301-307 10.1038/nrm2873
33. Lu, J.-X.; Qiang, W.; Yau, W.-M.; Schwieters, C. D.; Meredith, S. C.; Tycko, R. Molecular Structure of B-Amyloid Fibrils in Alzheimer's Disease Brain Tissue Cell 2013, 154, 1257-1268 10.1016/j.cell.2013.08.035
34. Masuda-Suzukake, M.; Nonaka, T.; Hosokawa, M.; Oikawa, T.; Arai, T.; Akiyama, H.; Mann, D. M. A.; Hasegawa, M. Prion-like Spreading of Pathological -Synuclein in Brain Brain 2013, 136, 1128-1138 10.1093/brain/awt037
35. Sanders, D. W.; Kaufman, S. K.; DeVos, S. L.; Sharma, A. M.; Mirbaha, H.; Li, A.; Barker, S. J.; Foley, A. C.; Thorpe, J. R.; Serpell, L. C. et al. Distinct Tau Prion Strains Propagate in Cells and Mice and Define Different Tauopathies Neuron 2014, 82, 1271-1288 10.1016/j.neuron.2014.04.047
36. Marshall, K. E.; Serpell, L. C. Fibres, Crystals and Polymorphism: The Structural Promiscuity of Amyloidogenic Peptides Soft Matter 2010, 6, 2110 10.1039/b926623b
37. Ashburn, T. T.; Auger, M.; Lansbury, P. T. The Structural Basis of Pancreatic Amyloid Formation: Isotope-Edited Spectroscopy in the Solid State J. Am. Chem. Soc. 1992, 114, 790-791 10.1021/ja00028a073
38. Griffiths, J. M.; Ashburn, T. T.; Auger, M.; Costa, P. R.; Griffin, R. G.; Lansbury, P. T. Rotational Resonance Solid-State NMR Elucidates a Structural Model of Pancreatic Amyloid J. Am. Chem. Soc. 1995, 117, 3539-3546 10.1021/ja00117a023
39. Lansbury, P. T.; 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. S. et al. Structural Model for the B-Amyloid Fibril Based on Interstrand Alignment of an Antiparallel-Sheet Comprising a C-Terminal Peptide Nat. Struct. Biol. 1995, 2, 990-998 10.1038/nsb1195-990
40. Colletier, J.-P.; Laganowsky, A.; Landau, M.; Zhao, M.; Soriaga, A. B.; Goldschmidt, L.; Flot, D.; Cascio, D.; Sawaya, M. R.; Eisenberg, D. Molecular Basis for Amyloid-B Polymorphism Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 16938-16943 10.1073/pnas.1112600108
41. Qiang, W.; Yau, W.-M.; Luo, Y.; Mattson, M. P.; Tycko, R. Antiparallel -Sheet Architecture in Iowa-Mutant -Amyloid Fibrils Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 4443-4448 10.1073/pnas.1111305109
42. Berthelot, K.; Ta, H. P.; Géan, J.; Lecomte, S.; Cullin, C. In Vivo and In Vitro Analyses of Toxic Mutants of HET-S: FTIR Antiparallel Signature Correlates with Amyloid Toxicity J. Mol. Biol. 2011, 412, 137-152 10.1016/j.jmb.2011.07.009
43. Lee, B.; Richards, F. M. The Interpretation of Protein Structures: Estimation of Static Accessibility J. Mol. Biol. 1971, 55, 379-IN4 10.1016/0022-2836(71)90324-X
44. Lawrence, M. C.; Colman, P. M. Shape Complementarity at Protein/Protein Interfaces J. Mol. Biol. 1993, 234, 946-950 10.1006/jmbi.1993.1648