Solvent microenvironments and copper binding alters the conformation and toxicity of a prion fragment

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Inayathullah, Mohammed ^a   Satheeshkumar, K S ^b,d   Malkovskiy, Andrey V ^a   Carre, Antoine L ^a   Sivanesan, Senthilkumar ^a   Hardesty, Jasper O ^c   Rajadas, Jayakumar ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CENTRAL LEATHER RESEARCH INSTITUTE   (India)

^c Stanford University   (United States)

^d Arignar Anna Government Arts College   (India)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER; PEPTIDE; PRION; PROTEIN BINDING;

ANIMAL; ASTROCYTE; CELL CULTURE; CHEMISTRY; METABOLISM; PATHOLOGY; PRION; PROTEIN SECONDARY STRUCTURE; RAT; WISTAR RAT;

ANIMALS; ASTROCYTES; CELLS, CULTURED; COPPER; PEPTIDES; PRIONS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RATS; RATS, WISTAR;

EID: 84893624731     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085160     Document Type: Article

References (87)

1. Costanzo M, Zurzolo C (2013) The cell biology of prion-like spread of protein aggregates: mechanisms and implication in neurodegeneration. Biochem J 452: 1-17. doi:10.1042/BJ20130484. PubMed: 23614720.
2. Jellinger KA (2012) Interaction between pathogenic proteins in neurodegenerative disorders. J Cell Mol Med 16: 1166-1183. doi:10.1111/j.1582- 4934.2011.01507.x. PubMed: 22176890.
3. Aguzzi A, Rajendran L (2009) The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 64: 783-790. doi:10.1016/j.neuron.2009. 12.016. PubMed: 20064386.
4. Fernandez-Funez P, Casas-Tinto S, Zhang Y, Gómez-Velazquez M, Morales-Garza MA et al. (2009) In vivo generation of neurotoxic prion protein: role for hsp70 in accumulation of misfolded isoforms. PLoS Genet 5: e1000507. PubMed: 19503596.
5. Caughey B, Chesebro B (1997) Prion protein and the transmissible spongiform encephalopathies. Trends Cell Biol 7: 56-62. doi:10.1016/S0962- 8924(96)10054-4. PubMed: 17708907. (Pubitemid 27075754)
6. Prusiner SB (1997) Prion diseases and the BSE crisis. Science 278: 245-251. doi:10.1126/science.278.5336.245. PubMed: 9323196.
7. De Armond SJ, Gonzales M, Mobley WC, Kon AA, Stern A et al. (1989) PrPSc in scrapie-infected hamster brain is spatially and temporally related to histopathology and infectivity titer. Prog Clin Biol Res 317: 601-618. PubMed: 2574872.
8. Ashe KH, Aguzzi A (2013) Prions, prionoids and pathogenic proteins in Alzheimer disease. Prion 7: 55-59. doi:10.4161/pri.23061. PubMed: 23208281.
9. Grenier C, Bissonnette C, Volkov L, Roucou X (2006) Molecular morphology and toxicity of cytoplasmic prion protein aggregates in neuronal and non-neuronal cells. J Neurochem 97: 1456-1466. doi:10.1111/j.1471-4159.2006. 03837.x. PubMed: 16696854. (Pubitemid 43725584)
10. Kristiansen M, Messenger MJ, Klöhn PC, Brandner S, Wadsworth JD et al. (2005) Disease-related prion protein forms aggresomes in neuronal cells leading to caspase activation and apoptosis. J Biol Chem 280: 38851-38861. doi:10.1074/jbc.M506600200. PubMed: 16157591. (Pubitemid 43853788)
11. Simoneau S, Rezaei H, Salès N, Kaiser-Schulz G, Lefebvre-Roque M et al. (2007) In vitro and in vivo neurotoxicity of prion protein oligomers. PLoS Pathog 3: e125. doi:10.1371/journal.ppat.0030125. PubMed: 17784787.
12. Kristiansen M, Deriziotis P, Dimcheff DE, Jackson GS, Ovaa H et al. (2007) Disease-associated prion protein oligomers inhibit the 26S proteasome. Mol Cell 26: 175-188. doi:10.1016/j.molcel.2007.04.001. PubMed: 17466621.
13. Ma J, Wollmann R, Lindquist S (2002) Neurotoxicity and neurodegeneration when PrP accumulates in the cytosol. Science 298: 1781-1785. doi:10.1126/science.1073725. PubMed: 12386337. (Pubitemid 35404120)
14. Ferreiro E, Costa R, Marques S, Cardoso SM, Oliveira CR et al. (2008) Involvement of mitochondria in endoplasmic reticulum stress-induced apoptotic cell death pathway triggered by the prion peptide PrP(106-126). J Neurochem 104: 766-776. PubMed: 17995926.
15. Bate C, Boshuizen RS, Langeveld JP, Williams A (2002) Temporal and spatial relationship between the death of PrP-damaged neurones and microglial activation. Neuroreport 13: 1695-1700. doi:10.1097/00001756-200209160-00025. PubMed: 12352629.
16. Marella M, Chabry J (2004) Neurons and astrocytes respond to prion infection by inducing microglia recruitment. J Neurosci 24: 620-627. doi:10.1523/JNEUROSCI.4303-03.2004. PubMed: 14736847. (Pubitemid 38166487)
17. Moreno JA, Radford H, Peretti D, Steinert JR, Verity N et al. (2012) Sustained translational repression by eIF2alpha-P mediates prion neurodegeneration. Nature 485: 507-511. PubMed: 22622579.
18. Falsig J, Sonati T, Herrmann US, Saban D, Li B et al. (2012) Prion pathogenesis is faithfully reproduced in cerebellar organotypic slice cultures. PLoS Pathog 8: e1002985. PubMed: 23133383.
19. Simon D, Herva ME, Benitez MJ, Garrido JJ, Rojo AI et al. (2013) Dysfunction of the PI3K-Akt-GSK-3 pathway is a common feature in cell culture and in vivo models of prion disease. Neuropathol Appl Neurobiol: ([MedlinePgn:]) PubMed: 23741998.
20. Burns CS, Aronoff-Spencer E, Dunham CM, Lario P, Avdievich NI et al. (2002) Molecular features of the copper binding sites in the octarepeat domain of the prion protein. Biochemistry 41: 3991-4001. doi:10.1021/bi011922x. PubMed: 11900542. (Pubitemid 34251038)
21. Chattopadhyay M, Walter ED, Newell DJ, Jackson PJ, Aronoff-Spencer E et al. (2005) The octarepeat domain of the prion protein binds Cu(II) with three distinct coordination modes at pH 7.4. J Am Chem Soc 127: 12647-12656. doi:10.1021/ja053254z. PubMed: 16144413. (Pubitemid 41292182)
22. Millhauser GL (2007) Copper and the prion protein: methods, structures, function, and disease. Annu Rev Phys Chem 58: 299-320. doi:10.1146/annurev. physchem.58.032806.104657. PubMed: 17076634.
23. Whittal RM, Ball HL, Cohen FE, Burlingame AL, Prusiner SB et al. (2000) Copper binding to octarepeat peptides of the prion protein monitored by mass spectrometry. Protein Sci 9: 332-343. PubMed: 10716185. (Pubitemid 30127006)
24. Bocharova OV, Breydo L, Salnikov VV, Baskakov IV (2005) Copper(II) inhibits in vitro conversion of prion protein into amyloid fibrils. Biochemistry 44: 6776-6787. doi:10.1021/bi050251q. PubMed: 15865423. (Pubitemid 40637231)
25. Thakur AK, Srivastava AK, Srinivas V, Chary KV, Rao CM (2011) Copper alters aggregation behavior of prion protein and induces novel interactions between its N- and C-terminal regions. J Biol Chem 286: 38533-38545. doi:10.1074/jbc.M111.265645. PubMed: 21900252.
26. Singh A, Mohan ML, Isaac AO, Luo X, Petrak J et al. (2009) Prion protein modulates cellular iron uptake: a novel function with implications for prion disease pathogenesis. PLOS ONE 4: e4468. doi:10.1371/journal.pone.0004468. PubMed: 19212444.
27. Das D, Luo X, Singh A, Gu Y, Ghosh S et al. (2010) Paradoxical role of prion protein aggregates in redox-iron induced toxicity. PLOS ONE 5: e11420. doi:10.1371/journal.pone.0011420. PubMed: 20625431.
28. Forloni G, Tagliavini F, Bugiani O, Salmona M (1996) Amyloid in Alzheimer's disease and prion-related encephalopathies: studies with synthetic peptides. Prog Neurobiol 49: 287-315. doi:10.1016/S0301-0082(96)00013-5. PubMed: 8888112. (Pubitemid 26305691)
29. Huang Z, Prusiner SB, Cohen FE (1996) Structures of prion proteins and conformational models for prion diseases. Curr Top Microbiol Immunol 207: 49-67. PubMed: 8575206.
30. Wille H, Michelitsch MD, Guenebaut V, Supattapone S, Serban A et al. (2002) Structural studies of the scrapie prion protein by electron crystallography. Proc Natl Acad Sci U S A 99: 3563-3568. doi:10.1073/pnas. 052703499. PubMed: 11891310. (Pubitemid 34252147)
31. Levy Y, Becker OM (2002) Conformational polymorphism of wild-type and mutant prion proteins: Energy landscape analysis. Proteins 47: 458-468. doi:10.1002/prot.10095.abs. PubMed: 12001224. (Pubitemid 34614725)
32. Pan KM, Baldwin M, Nguyen J, Gasset M, Serban A et al. (1993) Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc Natl Acad Sci U S A 90: 10962-10966. doi:10.1073/pnas.90.23. 10962. PubMed: 7902575.
33. Petchanikow C, Saborio GP, Anderes L, Frossard MJ, Olmedo MI et al. (2001) Biochemical and structural studies of the prion protein polymorphism. FEBS Lett 509: 451-456. doi:10.1016/S0014-5793(01)03147-7. PubMed: 11749972. (Pubitemid 34031977)
34. Prusiner SB, Scott MR, DeArmond SJ, Cohen FE (1998) Prion protein biology. Cell 93: 337-348. doi:10.1016/S0092-8674(00)81163-0. PubMed: 9590169.
35. Satheeshkumar KS, Jayakumar R (2003) Conformational polymorphism of the amyloidogenic peptide homologous to residues 113-127 of the prion protein. Biophys J 85: 473-483. doi:10.1016/S0006-3495(03)74492-0. PubMed: 12829502. (Pubitemid 36753651)
36. Baldwin MA, Cohen FE, Prusiner SB (1995) Prion protein isoforms, a convergence of biological and structural investigations. J Biol Chem 270: 19197-19200. doi:10.1074/jbc.270.33.19197. PubMed: 7642588.
37. De Gioia L, Selvaggini C, Ghibaudi E, Diomede L, Bugiani O et al. (1994) Conformational polymorphism of the amyloidogenic and neurotoxic peptide homologous to residues 106-126 of the prion protein. J Biol Chem 269: 7859-7862. PubMed: 7907586. (Pubitemid 24200181)
38. Tagliavini F, Prelli F, Porro M, Rossi G, Giaccone G et al. (1994) Amyloid fibrils in Gerstmann-Straussler-Scheinker disease (Indiana and Swedish kindreds) express only PrP peptides encoded by the mutant allele. Cell 79: 695-703. doi:10.1016/0092-8674(94)90554-1. PubMed: 7954833.
39. Tagliavini F, Prelli F, Verga L, Giaccone G, Sarma R et al. (1993) Synthetic peptides homologous to prion protein residues 106-147 form amyloid-like fibrils in vitro. Proc Natl Acad Sci U S A 90: 9678-9682. doi:10.1073/pnas.90.20.9678. PubMed: 8105481. (Pubitemid 23315849)
40. Donne DG, Viles JH, Groth D, Mehlhorn I, James TL et al. (1997) Structure of the recombinant full-length hamster prion protein PrP(29-231): the N terminus is highly flexible. Proc Natl Acad Sci U S A 94: 13452-13457. doi:10.1073/pnas.94.25.13452. PubMed: 9391046.
41. Selvaggini C, De Gioia L, Cantù L, Ghibaudi E, Diomede L et al. (1993) Molecular characteristics of a protease-resistant, amyloidogenic and neurotoxic peptide homologous to residues 106-126 of the prion protein. Biochem Biophys Res Commun 194: 1380-1386. doi:10.1006/bbrc.1993.1977. PubMed: 8102526. (Pubitemid 23255035)
42. Brown DR (1999) Prion protein peptide neurotoxicity can be mediated by astrocytes. J Neurochem 73: 1105-1113. PubMed: 10461901.
43. Ragg E, Tagliavini F, Malesani P, Monticelli L, Bugiani O et al. (1999) Determination of solution conformations of PrP106-126, a neurotoxic fragment of prion protein, by 1H NMR and restrained molecular dynamics. Eur J Biochem 266: 1192-1201. doi:10.1046/j.1432-1327.1999.00985.x. PubMed: 10583417. (Pubitemid 30010139)
44. Gasset M, Baldwin MA, Lloyd DH, Gabriel JM, Holtzman DM et al. (1992) Predicted alpha-helical regions of the prion protein when synthesized as peptides form amyloid. Proc Natl Acad Sci U S A 89: 10940-10944. doi:10.1073/pnas.89.22.10940. PubMed: 1438300.
45. Sreerama N, Woody RW (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem 287: 252-260. doi:10.1006/abio.2000.4880. PubMed: 11112271. (Pubitemid 32006234)
46. Andrews ME, Inayathullah NM, Jayakumar R, Malar EJP (2009) Conformational polymorphism and cellular toxicity of IAPP and beta AP domains. Journal of Structural Biology 166: 116-125.
47. Moses JP, Satheeshkumar KS, Murali J, Alli D, Jayakumar R (2003) Self-assembly of the synthetic polymer (Leu-Glu)(n): An amyloid-like structure formation. Langmuir 19: 3413-3418. doi:10.1021/la026661m.
48. Murali J, Jayakumar R (2005) Spectroscopic studies on native and protofibrillar insulin. J Struct Biol 150: 180-189. doi:10.1016/j.jsb.2005.02. 009. PubMed: 15866741. (Pubitemid 40615743)
49. Satheeshkumar KS, Murali J, Jayakumar R (2004) Assemblages of prion fragments: novel model systems for understanding amyloid toxicity. J Struct Biol 148: 176-193. doi:10.1016/j.jsb.2004.05.006. PubMed: 15477098.
50. Shanmugam G, Jayakumar R (2004) Structural analysis of amyloid beta peptide fragment (25-35) in different microenvironments. Biopolymers 76: 421-434. doi:10.1002/bip.20131. PubMed: 15468066. (Pubitemid 39540535)
51. Inayathullah M, Teplow DB (2011) Structural dynamics of the Delta E22 (Osaka) familial Alzheimer's disease-linked amyloid beta-protein. Amyloid-Journal of Protein Folding Disorders 18: 98-107. doi:10.3109/13506129. 2011.580399.
52. Maji SK, Loo RRO, Inayathullah M, Spring SM, Vollers SS et al. (2009) Amino Acid Position-specific Contributions to Amyloid beta-Protein Oligomerization. J Biol Chem 284: 23580-23591. doi:10.1074/jbc.M109.038133. PubMed: 19567875.
53. Chen SM, Ferrone FA, Wetzel R (2002) Huntington's disease age-ofonset linked to polyglutamine aggregation nucleation. Proc Natl Acad Sci U S A 99: 11884-11889. doi:10.1073/pnas.182276099. PubMed: 12186976. (Pubitemid 34994493)
54. Jaikaran ETAS, Higham CE, Serpell LC, Zurdo J, Gross M et al. (2001) Identification of a novel human islet amyloid polypeptide beta-sheet domain and factors influencing fibrillogenesis. J Mol Biol 308: 515-525. doi:10.1006/jmbi.2001.4593. PubMed: 11327784. (Pubitemid 33027616)
55. Di Natale G, Impellizzeri G, Pappalardo G (2005) Conformational properties of peptide fragments homologous to the 106-114 and 106-126 residues of the human prion protein: a CD and NMR spectroscopic study. Org Biomol Chem 3: 490-497. doi:10.1039/b407928k. PubMed: 15678187. (Pubitemid 40285715)
56. Jasanoff A, Fersht AR (1994) Quantitative determination of helical propensities from trifluoroethanol titration curves. Biochemistry 33: 2129-2135. doi:10.1021/bi00174a020. PubMed: 8117669.
57. Luidens MK, Figge J, Breese K, Vajda S (1996) Predicted and trifluoroethanol-induced alpha-helicity of polypeptides. Biopolymers 39: 367-376. doi:10.1002/(SICI)1097-0282(199609)39:3. PubMed: 8756516.
58. Nelson JW, Kallenbach NR (1986) Stabilization of the ribonuclease Speptide alpha-helix by trifluoroethanol. Proteins 1: 211-217. doi:10.1002/prot.340010303. PubMed: 3449856.
59. Chen H, Gu F, Huang Z (2006) Improved Chou-Fasman method for protein secondary structure prediction. BMC Bioinformatics 7 Suppl 4: S14. doi:10.1186/1471-2105-7-S5-S14. PubMed: 17217506.
60. Ronga L, Palladino P, Saviano G, Tancredi T, Benedetti E et al. (2007) NMR structure and CD titration with metal cations of human prion alpha2-helix-related peptides. Bioinorg Chem Appl: 10720: 10720. PubMed: 18274605.
61. Tizzano B, Palladino P, De Capua A, Marasco D, Rossi F et al. (2005) The human prion protein alpha2 helix: a thermodynamic study of its conformational preferences. Proteins 59: 72-79. doi:10.1002/prot.20395. PubMed: 15688445. (Pubitemid 40316479)
62. Tcherkasskaya O, Sanders W, Chynwat V, Davidson EA, Orser CS (2003) The role of hydrophobic interactions in amyloidogenesis: example of prion-related polypeptides. J Biomol Struct Dyn 21: 353-365. doi:10.1080/07391102.2003. 10506931. PubMed: 14616031. (Pubitemid 37549636)
63. Zhou GP, Huang RB (2013) The pH-Triggered Conversion of the PrP(c) to PrP(sc.). Curr Top Med Chem 13: 1152-1163. doi:10.2174/15680266113139990003. PubMed: 23647538.
64. Sureshbabu N, Kirubagaran R, Jayakumar R (2009) Surfactant-induced conformational transition of amyloid beta-peptide. Eur Biophys J 38: 355-367. doi:10.1007/s00249-008-0379-8. PubMed: 19005650.
65. Rapoport TA (1986) Protein translocation across and integration into membranes. CRC Crit Rev Biochem 20: 73-137. doi:10.3109/10409238609115901. PubMed: 3007024.
66. Wickner WT, Lodish HF (1985) Multiple mechanisms of protein insertion into and across membranes. Science 230: 400-407. doi:10.1126/science.4048938. PubMed: 4048938. (Pubitemid 16192554)
67. Reddy GL, Nagara R (1989) Circular dichroism studies on synthetic signal peptides indicate beta-conformation as a common structural feature in highly hydrophobic environment. J Biol Chem 264: 16591-16597. PubMed: 2777801. (Pubitemid 19243551)
68. Jobling MF, Huang X, Stewart LR, Barnham KJ, Curtain C et al. (2001) Copper and zinc binding modulates the aggregation and neurotoxic properties of the prion peptide PrP106-126. Biochemistry 40: 8073-8084. doi:10.1021/bi0029088. PubMed: 11434776. (Pubitemid 32641204)
69. Pan KM, Stahl N, Prusiner SB (1992) Purification and properties of the cellular prion protein from Syrian hamster brain. Protein Sci 1: 1343-1352. doi:10.1002/pro.5560011014. PubMed: 1363897. (Pubitemid 23009228)
70. Stöckel J, Safar J, Wallace AC, Cohen FE, Prusiner SB (1998) Prion protein selectively binds copper(II) ions. Biochemistry 37: 7185-7193. doi:10.1021/bi972827k. PubMed: 9585530. (Pubitemid 28235199)
71. Klewpatinond M, Viles JH (2007) Fragment length influences affinity for Cu2+ and Ni2+ binding to His96 or His111 of the prion protein and spectroscopic evidence for a multiple histidine binding only at low pH. Biochem J 404: 393-402. doi:10.1042/BJ20061893. PubMed: 17331076. (Pubitemid 46953913)
72. Brown DR, Schmidt B, Kretzschmar HA (1998) Effects of copper on survival of prion protein knockout neurons and glia. J Neurochem 70: 1686-1693. PubMed: 9523587. (Pubitemid 28136985)
73. Brown DR, Qin K, Herms JW, Madlung A, Manson J et al. (1997) The cellular prion protein binds copper in vivo. Nature 390: 684-687. PubMed: 9414160.
74. Chacón MA, Barría MI, Lorca R, Huidobro-Toro JP, Inestrosa NC (2003) A human prion protein peptide (PrP(59-91)) protects against copper neurotoxicity. Mol Psychiatry 8: 835-862, 10.1038/sj.mp.4001400. PubMed: 14515136.
75. Rivillas-Acevedo L, Grande-Aztatzi R, Lomelí I, García JE, Barrios E et al. (2011) Spectroscopic and electronic structure studies of copper(II) binding to His111 in the human prion protein fragment 106-115: evaluating the role of protons and methionine residues. Inorg Chem 50: 1956-1972. doi:10.1021/ic102381j. PubMed: 21261254.
76. Kawahara M, Koyama H, Nagata T, Sadakane Y (2011) Zinc, copper, and carnosine attenuate neurotoxicity of prion fragment PrP106-126. Metallomics 3: 726-734. doi:10.1039/c1mt00015b. PubMed: 21442127.
77. Ono K, Condron MM, Ho L, Wang J, Zhao W et al. (2008) Effects of grape seed-derived polyphenols on amyloid beta-protein self-assembly and cytotoxicity. J Biol Chem 283: 32176-32187. doi:10.1074/jbc.M806154200. PubMed: 18815129.
78. Ono K, Condron MM, Teplow DB (2009) Structure-neurotoxicity relationships of amyloid beta-protein oligomers. Proc Natl Acad Sci U S A 106: 14745-14750. doi:10.1073/pnas.0905127106. PubMed: 19706468.
79. Viles JH, Klewpatinond M, Nadal RC (2008) Copper and the structural biology of the prion protein. Biochem Soc Trans 36: 1288-1292. doi:10.1042/BST0361288. PubMed: 19021542.
80. You H, Tsutsui S, Hameed S, Kannanayakal TJ, Chen L et al. (2012) Abeta neurotoxicity depends on interactions between copper ions, prion protein, and N-methyl-D-aspartate receptors. Proc Natl Acad Sci U S A 109: 1737-1742. doi:10.1073/pnas.1110789109. PubMed: 22307640.
81. Bodanszky M, Bodanszky A (1984) The practice of peptide synthesis. Berlin; New York: Springer-Verlag. xvii, 284 pp.
82. Stewart JM, Young JD (1984). Solid phase peptide synthesis. Rockford, Ill.: Pierce Chemical Co. xvi, 176 p.
83. Jao SC, Ma K, Talafous J, Orlando R, Zagorski MG (1997) Trifluoroacetic acid pretreatment reproducibly disaggregates the amyloid beta-peptide. Amyloid-International Journal of Experimental and Clinical Investigation 4: 240-252. (Pubitemid 127716141)
84. Chun YS, Ha K, Lee YJ, Lee JS, Kim HS et al. (2002) Diisocyanates as novel molecular binders for monolayer assembly of zeolite crystals on glass. Chem Commun (Camb): 1846-1847. PubMed: 12271638. (Pubitemid 36138970)
85. Abe K, Saito H (1996) Menadione toxicity in cultured rat cortical astrocytes. Jpn J Pharmacol 72: 299-306. doi:10.1254/jjp.72.299. PubMed: 9015738.
86. Masilamoni JG, Jesudason EP, Bharathi SN, Jayakumar R (2005) The protective effect of alpha-crystallin against acute inflammation in mice. Biochim Biophys Acta 1740: 411-420. doi:10.1016/j.bbadis.2004.11.002. PubMed: 15949709. (Pubitemid 40804754)
87. Fezoui Y, Hartley DM, Walsh DM, Selkoe DJ, Osterhout JJ et al. (2000) A de novo designed helix-turn-helix peptide forms nontoxic amyloid fibrils. Nat Struct Biol 7: 1095-1099. doi:10.1038/81937. PubMed: 11101888.