Synthetic dimeric Aβ(28-40) mimics the complex epitope of human anti-aβ autoantibodies against toxic Aβ oligomers

Journal of Biological Chemistry

Volumn 288, Issue 38, 2013, Pages 27638-27645

  Roeder, Andreas M ^a   Roettger, Yvonne ^a   Stündel, Anne ^a   Dodel, Richard ^a   Geyer, Armin ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONAL BEHAVIOR; CONFORMATIONAL EPITOPES; CONFORMATIONAL TRANSITIONS; HEXAFLUOROISOPROPANOL; HIGHLY COOPERATIVES; NATURALLY OCCURRING; PHYSIOLOGICAL ROLES; SYNTHETIC PEPTIDE EPITOPE;

DIMERS; GLYCOPROTEINS;

EPITOPES;

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN [28-40]; AMYLOID BETA PROTEIN ANTIBODY; AMYLOID BETA PROTEIN[1-40]; AUTOANTIBODY; DIMER; EPITOPE; HEXAFLUORO 2 PROPANOL; MINIAMYLOID DERIVATIVE; OLIGOMER; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

ALPHA HELIX; ANIMAL CELL; ANTIBODY AFFINITY; ARTICLE; BETA SHEET; BINDING KINETICS; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; MOLECULAR MIMICRY; MOUSE; NONHUMAN; PEPTIDE SYNTHESIS; PRIORITY JOURNAL;

ALZHEIMER DISEASE; AMYLOID; AUTOANTIBODIES; NEUROIMMUNOLOGY; NEUROLOGICAL DISEASES; PEPTIDE CHEMICAL SYNTHESIS; PEPTIDE CONFORMATION; PROTEIN AGGREGATION;

AMYLOID; AMYLOID BETA-PEPTIDES; ANIMALS; AUTOANTIBODIES; CELLS, CULTURED; CIRCULAR DICHROISM; EPITOPES; HUMANS; MICE; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY;

EID: 84884566044     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.463273     Document Type: Article

References (36)

1. Jakob-Roetne, R., and Jacobsen, H. (2009) Alzheimer's Disease: From Pathology to Therapeutic Approaches. Angew. Chem. Int. Ed. 48, 3030-3059
2. Selkoe, D. J. (2011) Alzheimer's Disease. Cold Spring Harb. Perspect. Biol. 3, a004457
3. Du, Y., Dodel, R., Hampel, H., Buerger, K., Lin, S., Eastwood, B., Bales, K., Gao, F., Moeller, H. J., Oertel, W., Farlow, M., and Paul, S. (2001) Reduced levels of amyloid b-peptide antibody in Alzheimer disease. Neurology 57, 801-805
4. Du, Y., Wei, X., Dodel, R., Sommer, N., Hampel, H., Gao, F., Ma, Z., Zhao, L., Oertel, W. H., and Farlow, M. (2003) Human anti-β-amyloid antibodies block β-amyloid fibril formation and prevent β-amyloid-induced neurotoxicity. Brain 126, 1935-1939
5. Dodel, R. C., Du, Y., Depboylu, C., Hampel, H., Frölich, L., Haag, A., Hemmeter, U., Paulsen, S., Teipel, S. J., Brettschneider, S., Spottke, A., Nölker, C., Möller, H. J., Wei, X., Farlow, M., Sommer, N., and Oertel, W. H. (2004) Intravenous immunoglobulins containing antibodies against β-amyloid for the treatment of Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 75, 1472-1474
6. Dodel, R., Balakrishnan, K., Keyvani, K., Deuster, O., Neff, F., Andrei-Selmer, L. C., Röskam, S., Stüer, C., Al-Abed, Y., Noelker, C., Balzer-Geldsetzer, M., Oertel, W., Du, Y., and Bacher, M. (2011) Naturally occurring autoantibodies against β-amyloid: investigating their role in transgenic animal and in vitro models of Alzheimer's disease. J. Neurosci. 31, 5847-5854
7. Kayed, R., Head, E., Sarsoza, F., Saing, T., Cotman, C. W., Necula, M., Margol, L., Wu, J., Breydo, L., Thompson, J. L., Rasool, S., Gurlo, T., Butler, P., and Glabe, C. G. (2007) Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers. Mol. Neurodegener. 2, 18
8. Morgan, C., Colombres, M., Nuñez, M. T., and Inestrosa, N. C. (2004) Structure and function of amyloid in Alzheimer's disease. Prog. Neurobiol. 74, 323-349
9. Takano, K. (2008) Amyloid conformation in aqueous environment. Curr. Alzheimer Res. 5, 540-547
10. Vivekanandan, S., Brender, J. R., Lee, S. Y., and Ramamoorthy, A. (2011) A partially folded structure of amyloid-β (1-40) in an aqueous environment. Biochem. Biophys. Res. Commun. 411, 312-316
11. Takano, K., Endo, S., Mukaiyama, A., Chon, H., Matsumura, H., Koga, Y., and Kanaya, S. (2006) Structure of amyloid b fragments in aqueous environments. FEBS J. 273, 150-158
12. Hoyer, W., Grönwall, C., Jonsson, A., Ståhl, S., and Härd, T. (2008) Stabilization of a β-hairpin in monomeric Alzheimer's amyloid-β peptide inhibits amyloid formation. Proc. Natl. Acad. Sci. U. S. A. 105, 5099-5104
13. Jin, M., Shepardson, N., Yang, T., Chen, G., Walsh, D., and Selkoe, D. J. (2011) Soluble amyloid b-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration. Proc. Natl. Acad. Sci. U. S. A. 108, 5819-5824
14. Roychaudhuri, R., Yang, M., Hoshi, M. M., and Teplow, D. B. (2009) Amyloid b-protein assembly and Alzheimer disease. J. Biol. Chem. 284, 4749-4753
15. Schmechel, A., Zentgraf, H., Scheuermann, S., Fritz, G., Pipkorn, R., Reed, J., Beyreuther, K., Bayer, T. A., and Multhaup, G. (2003) Alzheimer b-Amyloid homodimers facilitate Ab fibrillization and the generation of conformational antibodies. J. Biol. Chem. 278, 35317-35324
16. Yamaguchi, T., Yagi, H., Goto, Y., Matsuzaki, K., and Hoshino, M. (2010) A disulfide-linked amyloid-b peptide dimer forms a protofibril-like oligomer through a distinct pathway from amyloid fibril formation. Biochemistry 49, 7100-7107
17. Müller-Schiffmann, A., Andreyeva, A., Horn, A. H., Gottmann, K., Korth, C., and Sticht, H. (2011) Molecular engineering of a secreted, highly homogeneous, and neurotoxic Ab dimer. ACS Chem. Neurosci. 2, 242-248
18. Kok, W. M., Scanlon, D. B., Karas, J. A., Miles, L. A., Tew, D. J., Parker, M. W., Barnham, K. J., and Hutton, C. A. (2009) Solid-phase synthesis of homodimeric peptides: preparation of covalently-linked dimers of amyloid b peptide. Chem. Commun. (Camb.) 12, 6228-6230
19. Lührs, T., Ritter, C., Adrian, M., Riek-Loher, D., Bohrmann, B., Döbeli, H., Schubert, D., and Riek, R. (2005) 3D structure of Alzheimer's amyloid-b-(1-42) fibrils. Proc. Natl. Acad. Sci. U. S. A. 102, 17342-17347
20. 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 bamyloid fibrils based on experimental constraints from solid state NMR. Proc. Natl. Acad. Sci. U. S. A. 99, 16742-16747
21. Petkova, A. T., Yau, W. M., and Tycko, R. (2006) Experimental constraints on quaternary structure in Alzheimer's b-amyloid fibrils. Biochemistry 45, 498-512
22. Sato, T., Kienlen-Campard, P., Ahmed, M., Liu, W., Li, H., Elliott, J. I., Aimoto, S., Constantinescu, S. N., Octave, J. N., and Smith, S. O. (2006) Inhibitors of Amyloid Toxicity Based on b-sheet Packing of Ab40 and Ab42. Biochemistry 45, 5503-5516
23. Ahmed, M., Davis, J., Aucoin, D., Sato, T., Ahuja, S., Aimoto, S., Elliott, J. I., Van Nostrand, W. E., and Smith, S. O. (2010) Structural conversion of neurotoxic amyloid-b1-42 oligomers to fibrils. Nat. Struct. Mol. Biol. 17, 561-567
24. Scheidt, H. A., Morgado, I., Rothemund, S., Huster, D., and Fändrich, M. (2011) Solid-state NMR spectroscopic investigation of Ab protofibrils: implication of a b-sheet remodeling upon maturation into terminal amyloid fibrils. Angew. Chem. Int. Ed. 50, 2837-2840
25. Fradinger, E. A., Monien, B. H., Urbanc, B., Lomakin, A., Tan, M., Li, H., Spring, S. M., Condron, M. M., Cruz, L., Xie, C. W., Benedek, G. B., and Bitan, G. (2008) C-terminal peptides coassemble into Ab42 oligomers and protect neurons against Ab42-induced neurotoxicity. Proc. Natl. Acad. Sci. U. S. A. 105, 14175-14180
26. Walsh, D. M., Hartley, D. M., Kusumoto, Y., Fezoui, Y., Condron, M. M., Lomakin, A., Benedek, G. B., Selkoe, D. J., and Teplow, D. B. (1999) Amyloid b-Protein Fibrillogenesis. J. Biol. Chem. 274, 25945-25952
27. Barrow, C. J., Yasuda, A., Kenny, P. T., and Zagorski, M. G. (1992) Solution conformations and aggregational properties of synthetic amyloid b-peptides of Alzheimer's disease: Analysis of circular dichroism spectra. J. Mol. Biol. 225, 1075-1093
28. Fezoui, Y., and Teplow, D. B. (2002) Kinetic studies of amyloid b-protein fibril assembly. J. Biol. Chem. 277, 36948-36954
29. Tomaselli, S., Esposito, V., Vangone, P., Van Nuland, N. A., Bonvin, A. M., Guerrini, R., Tancredi, T., Temussi, P. A., and Picone, D. (2006) The a-to-b conformational transition of Alzheimer's Ab-(1-42) peptide in aqueous media is reversible: a step by step conformational analysis suggests the location of b conformation seeding. ChemBioChem 7, 257-267
30. Greenfield, N. J. (2006) Using circular dichroism collected as a function of temperature to determine the thermodynamics of protein unfolding and binding interactions. Nat. Protoc. 1, 2527-2535
31. Kayed, R., Head, E., Thompson, J. L., McIntire, T. M., Milton, S. C., Cotman, C. W., and Glabe, C. G. (2003) Common Structure of Soluble Amyloid Oligomers Implies Common Mechanism of Pathogenesis. Science 300, 486-489
32. Laganowsky, A., Liu, C., Sawaya, M. R., Whitelegge, J. P., Park, J., Zhao, M., Pensalfini, A., Soriaga, A. B., Landau, M., Teng, P. K., Cascio, D., Glabe, C., and Eisenberg, D. (2012) Atomic view of a toxic amyloid small oligomer. Science 335, 1228-1231
33. Yu, L., Edalji, R., Harlan, J. E., Holzman, T. F., Lopez, A. P., Labkovsky, B., Hillen, H., Barghorn, S., Ebert, U., Richardson, P. L., Miesbauer, L., Solomon, L., Bartley, D., Walter, K., Johnson, R. W., Hajduk, P. J., and Olejniczak, E. T. (2009) Structural characterization of a soluble amyloidβ-peptide oligomer. Biochemistry 48, 1870-1877
34. Bleiholder, C., Dupuis, N. F., Wyttenbach, T., and Bowers, M. T. (2011) Ion mobility-mass spectrometry reveals a conformational conversion from random assembly to β-sheet in amyloid fibril formation. Nat. Chem. 3, 172-177
35. Fezoui, Y., Hartley, D. M., Walsh, D. M., Selkoe, D. J., Osterhout, J. J., and Teplow, D. B. (2000) A de novo designed helix-turn-helix peptide forms nontoxic amyloid fibrils. Nat. Struct. Biol. 7, 1095-1099
36. Hauser, C. A., Deng, R., Mishra, A., Loo, Y., Khoe, U., Zhuang, F., Cheong, D. W., Accardo, A., Sullivan, M. B., Riekel, C., Ying, J. Y., and Hauser, U. A. (2011) Natural tri-to hexapeptides self-assemble in water to amyloid β-type fiber aggregates by unexpected β-helical intermediate structures. Proc. Natl. Acad. Sci. USA 108, 1361-1366