Crystal structure of the amyloid-β p3 fragment provides a model for oligomer formation in Alzheimer's disease

Journal of Neuroscience

Volumn 31, Issue 4, 2011, Pages 1419-1426

  Streltsov, Victor A ^a   Varghese, Joseph N ^a   Masters, Colin L ^b   Nuttall, Stewart D ^a  

^a CSIRO   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; OLIGOMER; PROTEIN PRECURSOR; SECRETASE; TETRAMER;

ALZHEIMER DISEASE; ARTICLE; BETA RHYTHM; BRAIN; CRYSTAL STRUCTURE; INFORMATION; NONHUMAN; OLIGOMERIZATION; PRECURSOR; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN MOTIF; SHARK; SPECIES;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CRYSTALLOGRAPHY, X-RAY; IMMUNOGLOBULIN VARIABLE REGION; MODELS, MOLECULAR; MUTATION; PEPTIDE FRAGMENTS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, ANTIGEN; RECOMBINANT FUSION PROTEINS; SHARKS;

EID: 79251567055     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4259-10.2011     Document Type: Article

References (64)

1. Barghorn S, Nimmrich V, Striebinger A, Krantz C, Keller P, Janson B, Bahr M, Schmidt M, Bitner RS, Harlan J, Barlow E, Ebert U, Hillen H (2005) Globular amyloid β-peptide oligomer - a homogenous and stable neuropathological protein in Alzheimer's disease. J Neurochem 95:834-847. (Pubitemid 41567174)
2. Barnham KJ, Cappai R, Beyreuther K, Masters CL, Hill AF (2006) Delineating common molecular mechanisms in Alzheimer's and prion diseases. Trends Biochem Sci 31:465-472. (Pubitemid 44108660)
3. Baumketner A, Krone MG, Shea JE (2008) Role of the familial Dutch mutation E22Q in the folding and aggregation of the 15-28 fragment of the Alzheimer amyloid-β protein. Proc Natl Acad Sci U S A 105:6027-6032. (Pubitemid 351758393)
4. Betts V, Leissring MA, Dolios G, Wang R, Selkoe DJ, Walsh DM (2008) Aggregation and catabolism of disease-associated intra-Aβ mutations: reduced proteolysis of AβA21G by neprilysin. Neurobiol Dis 31:442-450.
5. Brünger AT (1992) Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355:472-475.
6. Caine J, Volitakis I, Cherny R, Varghese J, Macreadie I (2007) Aβ produced as a fusion to maltose binding protein can be readily purified and stably associates with copper and zinc. Protein Pept Lett 14:83-86. (Pubitemid 46046956)
7. Chimon S, Ishii Y (2005) Capturing intermediate structures of Alzheimer's β-amyloid, Aβ(1-40), by solid-state NMR spectroscopy. J Am Chem Soc 127:13472-13473. (Pubitemid 41401181)
8. Chimon S, Shaibat MA, Jones CR, Calero DC, Aizezi B, Ishii Y (2007) Evidence of fibril-like β-sheet structures in a neurotoxic amyloid intermediate of Alzheimer's β-amyloid. Nat Struct Mol Biol 14:1157-1164. (Pubitemid 350223342)
9. DeLano WL (2002) The PyMOL molecular graphics system. San Carlos, CA: DeLano Scientific.
10. Egnaczyk GF, Greis KD, Stimson ER, Maggio JE (2001) Photoaffinity cross-linking of Alzheimer's disease amyloid fibrils reveals interstrand contact regions between assembled β-amyloid peptide subunits. Biochemistry 40:11706-11714.
11. Gardberg AS, Dice LT, Ou S, Rich RL, Helmbrecht E, Ko J, Wetzel R, Myszka DG, Patterson PH, Dealwis C (2007) Molecular basis for passive immunotherapy of Alzheimer's disease. Proc Natl Acad Sci U S A 104:15659-15664.
12. Grant MA, Lazo ND, Lomakin A, Condron MM, Arai H, Yamin G, Rigby AC, Teplow DB (2007) Familial Alzheimer's disease mutations alter the stability of the amyloid β-protein monomer folding nucleus. Proc Natl Acad Sci U S A 104:16522-16527.
13. Grimaldi M, Scrima M, Esposito C, Vitiello G, Ramunno A, Limongelli V, D'Errico G, Novellino E, D'Ursi AM (2010) Membrane charge dependent states of the β-amyloid fragment Aβ(16-35) with differently charged micelle aggregates. Biochim Biophys Acta 1798:660-671.
14. Harada T, Kuroda R (2011) CD measurements of β-amyloid (1-40) and (1-42) in the condensed phase. Biopolymers 95:127-134.
15. Henderson KA, Streltsov VA, Coley AM, Dolezal O, Hudson PJ, Batchelor AH, Gupta A, Bai T, Murphy VJ, Anders RF, Foley M, Nuttall SD (2007) Structure of an IgNAR-AMA1 complex: targeting a conserved hydrophobic cleft broadens malarial strain recognition. Structure 15:1452-1466.
16. Higgins LS, Murphy GM Jr, Forno LS, Catalano R, Cordell B (1996) P3 β-amyloid peptide has a unique and potentially pathogenic immunohistochemical profile in Alzheimer's disease brain. Am J Pathol 149:585-596. (Pubitemid 26256346)
17. Hou L, Shao H, Zhang Y, Li H, Menon NK, Neuhaus EB, Brewer JM, Byeon IJ, Ray DG, Vitek MP, Iwashita T, Makula RA, Przybyla AB, Zagorski MG (2004) Solution NMR studies of the Aβ(1-40) and Aβ(1-42) peptides establish that the Met35 oxidation state affects the mechanism of amyloid formation. J Am Chem Soc 126:1992-2005.
18. Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14:33-38, 27-28.
19. Jang H, Arce FT, Ramachandran S, Capone R, Azimova R, Kagan BL, Nussinov R, Lal R (2010) Truncated β-amyloid peptide channels provide an alternative mechanism for Alzheimer's disease and Down syndrome. Proc Natl Acad Sci U S A 107:6538-6543.
20. Kajava AV, Squire JM, Parry DA (2006) β-Structures in fibrous proteins. Adv Protein Chem 73:1-15.
21. Kienlen-Campard P, Tasiaux B, Van Hees J, Li M, Huysseune S, Sato T, Fei JZ, Aimoto S, Courtoy PJ, Smith SO, Constantinescu SN, Octave JN (2008) Amyloidogenic processing but not amyloid precursor protein (APP) intracellular C-terminal domain production requires a precisely oriented APP dimer assembled by transmembrane GXXXG motifs. J Biol Chem 283:7733-7744.
22. Lalowski M, Golabek A, Lemere CA, Selkoe DJ, Wisniewski HM, Beavis RC, Frangione B, Wisniewski T (1996) The "nonamyloidogenic" p3 fragment (amyloid β17-42) is a major constituent of Down's syndrome cerebellar preamyloid. J Biol Chem 271:33623-33631.
23. Lawrence MC, Colman PM (1993) Shape complementarity at protein/protein interfaces. J Mol Biol 234:946-950.
24. Losic D, Martin LL, Mechler A, Aguilar MI, Small DH (2006) High resolution scanning tunnelling microscopy of the β-amyloid protein (Aβ1-40) of Alzheimer's disease suggests a novel mechanism of oligomer assembly. J Struct Biol 155:104-110. (Pubitemid 43867319)
25. Lührs T, Ritter C, Adrian M, Riek-Loher D, Bohrmann B, Döbeli H, Schubert D, Riek R (2005) 3D structure of Alzheimer's amyloid-β(1-42) fibrils. Proc Natl Acad Sci U S A 102:17342-17347.
26. Lynn DG, Meredith SC (2000) Review: model peptides and the physicochemical approach to β-amyloids. J Struct Biol 130:153-173.
27. Malinchik SB, Inouye H, Szumowski KE, Kirschner DA (1998) Structural analysis of Alzheimer's β(1-40) amyloid: protofilament assembly of tubular fibrils. Biophys J 74:537-545.
28. Mastrangelo IA, Ahmed M, Sato T, Liu W, Wang C, Hough P, Smith SO (2006) High-resolution atomic force microscopy of soluble Aβ42 oligomers. J Mol Biol 358:106-119.
29. McRee DE (1999) XtalView/Xfit - a versatile program for manipulating atomic coordinates and electron density. J Struct Biol 125:156-165.
30. Miles LA, Wun KS, Crespi GA, Fodero-Tavoletti MT, Galatis D, Bagley CJ, Beyreuther K, Masters CL, Cappai R, McKinstry WJ, Barnham KJ, Parker MW (2008) Amyloid-β-anti-amyloid-β complex structure reveals an extended conformation in the immunodominant B-cell epitope. J Mol Biol 377:181-192.
31. Munter LM, Voigt P, Harmeier A, Kaden D, Gottschalk KE, Weise C, Pipkorn R, Schaefer M, Langosch D, Multhaup G (2007) GxxxG motifs within the amyloid precursor protein transmembrane sequence are critical for the etiology of Aβ42. EMBO J 26:1702-1712.
32. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53:240-255.
33. Nag S, Chen J, Irudayaraj J, Maiti S (2010) Measurement of the attachment and assembly of small amyloid-β oligomers on live cell membranes at physiological concentrations using single-molecule tools. Biophys J 99:1969-1975.
34. Nelson R, Eisenberg D (2006) Recent atomic models of amyloid fibril structure. Curr Opin Struct Biol 16:260-265.
35. Nuttall SD, Irving RA, Hudson PJ (2000) Immunoglobulin VH domains and beyond: design and selection of single-domain binding and targeting reagents. Curr Pharm Biotechnol 1:253-263.
36. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-326. (Pubitemid 27085611)
37. Paravastu AK, Qahwash I, Leapman RD, Meredith SC, Tycko R (2009) Seeded growth of β-amyloid fibrils from Alzheimer's brain-derived fibrils produces a distinct fibril structure. Proc Natl Acad Sci U S A 106:7443-7448.
38. Petkova AT, Ishii Y, Balbach JJ, Antzutkin ON, Leapman RD, Delaglio F, 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.
39. Petkova AT, Leapman RD, Guo Z, Yau WM, Mattson MP, Tycko R (2005) Self-propagating, molecular-level polymorphism in Alzheimer's β-amyloid fibrils. Science 307:262-265. (Pubitemid 40116242)
40. Petkova AT, Yau WM, Tycko R (2006) Experimental constraints on quaternary structure in Alzheimer's β-amyloid fibrils. Biochemistry 45:498-512. (Pubitemid 43100415)
41. Querfurth HW, LaFerla FM (2010) Alzheimer's disease. N Engl J Med 362:329-344.
42. Rand RP (1971) Structural studies by X-ray diffraction of model lipidprotein membranes of serum albumin-lecithin-cardiolipin. Biochim Biophys Acta 241:823-834.
43. Rauk A (2008) Why is the amyloid βpeptide of Alzheimer's disease neurotoxic? Dalton Trans 10:1273-1282.
44. Ryan DA, Narrow WC, Federoff HJ, Bowers WJ (2010) An improved method for generating consistent soluble amyloid-beta oligomer preparations for in vitro neurotoxicity studies. J Neurosci Methods 190:171-179.
45. Sachse C, Fändrich M, Grigorieff N (2008) Paired β-sheet structure of an Aβ(1-40) amyloid fibril revealed by electron microscopy. Proc Natl Acad Sci U S A 105:7462-7466.
46. Sato T, Kienlen-Campard P, Ahmed M, Liu W, Li H, Elliott JI, Aimoto S, Constantinescu SN, Octave JN, Smith SO (2006) Inhibitors of amyloid toxicity based on β-sheet packing of Aβ40 and Aβ42. Biochemistry 45:5503-5516.
47. Sawaya MR, Sambashivan S, Nelson R, Ivanova MI, Sievers SA, Apostol MI, Thompson MJ, Balbirnie M, Wiltzius JJ, McFarlane HT, Madsen AØ, Riekel C, Eisenberg D (2007) Atomic structures of amyloid cross-β spines reveal varied steric zippers. Nature 447:453-457.
48. Schmechel A, Zentgraf H, Scheuermann S, Fritz G, Pipkorn R, Reed J, Beyreuther K, Bayer TA, Multhaup G (2003) Alzheimer β-amyloid homodimers facilitate Aβ fibrillization and the generation of conformational antibodies. J Biol Chem 278:35317-35324.
49. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe DJ (2008) Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14:837-842.
50. Shen Y, Joachimiak A, Rosner MR, Tang WJ (2006) Structures of human insulin-degrading enzyme reveal a new substrate recognition mechanism. Nature 443:870-874. (Pubitemid 44622699)
51. Sorimachi K, Craik DJ, Lloyd EJ, Beyreuther K, Masters CL (1990) Identification of a β-turn in the tertiary structure of a peptide fragment of the Alzheimer amyloid protein. Biochem Int 22:447-454.
52. Soscia SJ, Kirby JE, Washicosky KJ, Tucker SM, Ingelsson M, Hyman B, Burton MA, Goldstein LE, Duong S, Tanzi RE, Moir RD (2010) The Alzheimer's disease-associated amyloid β-protein is an antimicrobial peptide. PLoS One 5:e9505.
53. Streltsov V (2008) X-ray absorption and diffraction studies of the metal binding sites in amyloid β-peptide. Eur Biophys J 37:257-263.
54. Streltsov VA, Varghese JN, Carmichael JA, Irving RA, Hudson PJ, Nuttall SD (2004) Structural evidence for evolution of shark Ig new antigen receptor variable domain antibodies from a cell-surface receptor. Proc Natl Acad Sci U S A 101:12444-12449.
55. Streltsov VA, Titmuss SJ, Epa VC, Barnham KJ, Masters CL, Varghese JN (2008) The structure of the amyloid-β peptide high-affinity copper II binding site in Alzheimer disease. Biophys J 95:3447-3456.
56. Takano K, Endo S, Mukaiyama A, Chon H, Matsumura H, Koga Y, Kanaya S (2006) Structure of amyloid-β fragments in aqueous environments. FEBS J 273:150-158.
57. Tycko R (2001) Solid-state nuclear magnetic resonance techniques for structural studies of amyloid fibrils. Methods Enzymol 339:390-413.
58. Urbanc B, Betnel M, Cruz L, Bitan G, Teplow DB (2010) Elucidation of amyloid β-protein oligomerization mechanisms: discrete molecular dynamics study. J Am Chem Soc 132:4266-4280.
59. Vagin A, Teplyakov A (1997) MOLREP: an automated program for molecular replacement. J Appl Crystallogr 30:1022-1025. (Pubitemid 127485985)
60. Walsh DM, Selkoe DJ (2007) Aβ oligomers - a decade of discovery. J Neurochem 101:1172-1184.
61. Winn MD, Isupov MN, Murshudov GN (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr D Biol Crystallogr 57:122-133.
62. Wurth C, Guimard NK, Hecht MH (2002) Mutations that reduce aggregation of the Alzheimer's Aβ42 peptide: an unbiased search for the sequence determinants of Aβ amyloidogenesis. J Mol Biol 319:1279-1290. (Pubitemid 34729435)
63. Yoda M, Miura T, Takeuchi H (2008) Non-electrostatic binding and selfassociation of amyloid β-peptide on the surface of tightly packed phosphatidylcholine membranes. Biochem Biophys Res Commun 376:56-59.
64. Yu L, Edalji R, Harlan JE, Holzman TF, Lopez AP, Labkovsky B, Hillen H, Barghorn S, Ebert U, Richardson PL, Miesbauer L, Solomon L, Bartley D, Walter K, Johnson RW, Hajduk PJ, Olejniczak ET (2009) Structural characterization of a soluble amyloid β-peptide oligomer. Biochemistry 48:1870-1877.