Monoclonal antibodies against Aβ42 fibrils distinguish multiple aggregation state polymorphisms in vitro and in Alzheimer disease brain

Journal of Biological Chemistry

Volumn 289, Issue 46, 2014, Pages 32131-32143

  Hatami, Asa ^a,c   Albay, Ricardo ^a   Monjazeb, Sanaz ^a   Milton, Saskia ^a   Glabe, Charles ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATES; EPITOPES; GLYCOPROTEINS; IMMUNE SYSTEM; MONOCLONAL ANTIBODIES; NEURODEGENERATIVE DISEASES; PROTEINS; SURFACE PLASMON RESONANCE;

AMYLOIDOGENIC PROTEINS; CONFORMATIONAL EPITOPES; HUMORAL IMMUNE RESPONSE; IMMUNOREACTIVITIES; N-TERMINAL DOMAINS; PATHOLOGICAL PROCESS; STRUCTURAL POLYMORPHISMS; THERAPEUTIC MONOCLONAL ANTIBODIES;

ANTIBODIES;

AMYLOID BETA PROTEIN[1-42]; EPITOPE; MONOCLONAL ANTIBODY; MONOMER; ALPHA SYNUCLEIN; AMYLOID; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (1-42); PEPTIDE FRAGMENT; PROTEIN BINDING;

ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ANTIGEN ANTIBODY REACTION; ARTICLE; HUMAN; HUMAN TISSUE; HUMORAL IMMUNITY; IMMUNOREACTIVITY; IN VITRO STUDY; MOUSE; NEUROFILAMENT; NONHUMAN; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN POLYMORPHISM; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; TRANSGENIC MOUSE; AMINO ACID SEQUENCE; AMYLOID PLAQUE; ANIMAL; BRAIN; CHEMISTRY; EPITOPE MAPPING; HEAT; HYDROGEN BOND; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; SEQUENCE HOMOLOGY;

MUS MUSCULUS; SOLENOIDEA;

ALPHA-SYNUCLEIN; ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYLOID; AMYLOID BETA-PEPTIDES; ANIMALS; ANTIBODIES, MONOCLONAL; BRAIN; EPITOPE MAPPING; EPITOPES; HOT TEMPERATURE; HUMANS; HYDROGEN BONDING; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PLAQUE, AMYLOID; PROTEIN BINDING; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84911453499     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.594846     Document Type: Article

References (46)

1. Querfurth, H. W., and La Ferla, F. M. (2010) Alzheimer's disease. N. Engl. J. Med. 362, 329-344
2. Hebert, L. E., Scherr, P. A., Bienias, J. L., Bennett, D. A., and Evans, D. A. (2003) Alzheimer disease in the US population: prevalence estimates using the 2000 census. Arch. Neurol. 60, 1119-1122
3. Katzman, R., and Saitoh, T. (1991) Advances in Alzheimer's disease. FASEB J. 5, 278-286
4. Serrano-Pozo, A., Frosch, M. P., Masliah, E., and Hyman, B. T. (2011) Neuropathological alterations in Alzheimer disease. Cold Spring Harbor Perspect. Med. 1, a006189
5. Hardy, J., and Selkoe, D. J. (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356
6. Haass, C., and Selkoe, D. J. (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β-peptide. Nat. Rev. Mol. Cell Biol. 8, 101-112
7. Yang, A. J., Knauer, M., Burdick, D. A., and Glabe, C. (1995) Intracellular Aβ1-42 aggregates stimulate the accumulation of stable, insoluble amyloidogenic fragments of the amyloid precursor protein in transfected cells. J. Biol. Chem. 270, 14786-14792
8. 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
9. Lambert, M. P., Viola, K. L., Chromy, B. A., Chang, L., Morgan, T. E., Yu, J., Venton, D. L., Krafft, G. A., Finch, C. E., and Klein, W. L. (2001) Vaccination with soluble Aβ oligomers generates toxicity-neutralizing antibodies. J. Neurochem. 79, 595-605
10. 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
11. Stroud, J. C., Liu, C., Teng, P. K., and Eisenberg, D. (2012) Toxic fibrillar oligomers of amyloid-β have cross-β structure. Proc. Natl. Acad. Sci. 109, 7717-7722
12. Yoshiike, Y., Kayed, R., Milton, S. C., Takashima, A., and Glabe, C. G. (2007) Pore-forming proteins share structural and functional homology with amyloid oligomers. Neuromolecular Med. 9, 270-275
13. Cerf, E., Sarroukh, R., Tamamizu-Kato, S., Breydo, L., Derclaye, S., Dufrêne, Y. F., Narayanaswami, V., Goormaghtigh, E., Ruysschaert, J. M., and Raussens, V. (2009) Antiparallel β-sheet: a signature structure of the oligomeric amyloid β-peptide. Biochem. J. 421, 415-423
14. 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
15. Head, E., Pop, V., Vasilevko, V., Hill, M., Saing, T., Sarsoza, F., Nistor, M., Christie, L. A., Milton, S., Glabe, C., Barrett, E., and Cribbs, D. (2008) A twoyear study with fibrillarβ-amyloid (Aβ) immunization in aged canines: effects on cognitive function and brain Aβ. J. Neurosci. 28, 3555-3566
16. Kayed, R., Canto, I., Breydo, L., Rasool, S., Lukacsovich, T., Wu, J., Albay, R., 3rd, Pensalfini, A., Yeung, S., Head, E., Marsh, J. L., and Glabe, C. (2010) Conformation dependent monoclonal antibodies distinguish different replicating strains or conformers of prefibrillar Aβ oligomers. Mol. Neurodegener. 5, 57
17. Kheterpal, I., Chen, M., Cook, K. D., and Wetzel, R. (2006) Structural differences in Aβ amyloid protofibrils and fibrils mapped by hydrogen exchange-mass spectrometry with on-line proteolytic fragmentation. J. Mol. Biol. 361, 785-795
18. Williams, A. D., Portelius, E., Kheterpal, I., Guo, J.-T., Cook, K. D., Xu, Y., and Wetzel, R. (2004) Mapping Aβ amyloid fibril secondary structure using scanning proline mutagenesis. J. Mol. Biol. 335, 833-842
19. Petkova, A. T., Yau, W.-M., and Tycko, R. (2006) Experimental constraints on quaternary structure in Alzheimer'sβ-amyloid fibrils. Biochemistry 45, 498-512
20. Goldsbury, C. S., Wirtz, S., Müller, S. A., Sunderji, S., Wicki, P., Aebi, U., and Frey, P. (2000) Studies on the in vitro assembly of Aβ1-40: implications for the search for a β fibril formation inhibitors. J. Struct. Biol. 130, 217-231
21. Benilova, I., Karran, E., and De Strooper, B. (2012) The toxic Aβ oligomer and Alzheimer's disease: an emperor in need of clothes. Nat. Neurosci. 15, 349-357
22. Campioni, S., Mannini, B., Zampagni, M., Pensalfini, A., Parrini, C., Evangelisti, E., Relini, A., Stefani, M., Dobson, C. M., Cecchi, C., and Chiti, F. (2010) A causative link between the structure of aberrant protein oligomers and their toxicity. Nat. Chem. Biol. 6, 140-147
23. Lee, M., Bard, F., Johnson-Wood, K., Lee, C., Hu, K., Griffith, S. G., Black, R. S., Schenk, D., and Seubert, P. (2005) Aβ42 immunization in Alzheimer's disease generates Aβ N-terminal antibodies. Ann. Neurol. 58, 430-435
24. Hock, C., Konietzko, U., Papassotiropoulos, A., Wollmer, A., Streffer, J., von Rotz, R. C., Davey, G., Moritz, E., and Nitsch, R. M. (2002) Generation of antibodies specific for β-amyloid by vaccination of patients with Alzheimer disease. Nat. Med. 8, 1270-1275
25. Nussbaum, J. M., Seward, M. E., and Bloom, G. S. (2013) Alzheimer disease: a tale of two prions. Prion 7, 14-19
26. Nussbaum, J. M., Schilling, S., Cynis, H., Silva, A., Swanson, E., Wangsanut, T., Tayler, K., Wiltgen, B., Hatami, A., Rönicke, R., Reymann, K., Hutter-Paier, B., Alexandru, A., Jagla, W., Graubner, S., Glabe, C. G., Demuth, H.-U., and Bloom, G. S. (2012) Prion-like behaviour and tau-dependent cytotoxicity of pyroglutamylated amyloid-β. Nature 485, 651-655
27. Reineke, U., and Sabat, R. (2009) in Epitope Mapping Protocols (Schutkowski, M., and Reineke, U., eds) pp. 145-177, Humana Press Inc., Totowa, NJ
28. Khoury, M. K., Parker, I., and Aswad, D. W. (2010) Acquisition of chemiluminescent signals from immunoblots with a digital single-lens reflex camera. Anal. Biochem. 397, 129-131
29. Murphy, K., Travers, P., and Walport, M. (2010) in Janeway's Immunobiology (Lawrence, E., ed) 8th Ed., Taylor & Francis, Inc., New York
30. Fanning, L. J., Connor, A. M., and Wu, G. E. (1996) Development of the immunoglobulin repertoire. Clin. Immunol. Immunopathol. 79, 1-14
31. Spooner, E. T., Desai, R. V., Mori, C., Leverone, J. F., and Lemere, C. A. (2002) The generation and characterization of potentially therapeutic Aβ antibodies in mice: differences according to strain and immunization protocol. Vaccine 21, 290-297
32. Winton, M. J., Lee, E. B., Sun, E., Wong, M. M., Leight, S., Zhang, B., Trojanowski, J. Q., and Lee, V. M. (2011) Intraneuronal APP, not free Aβ peptides in 3xTg-AD mice: implications for tau versus Aβ-mediated Alzheimer neurodegeneration. J. Neurosci. 31, 7691-7699
33. McLean, D., Cooke, M. J., Albay, R., 3rd, Glabe, C., and Shoichet, M. S. (2013) Positron emission tomography imaging of fibrillar parenchymal and vascular amyloid-β in TgCRND8 mice. ACS Chem. Neurosci. 4, 613-623
34. 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
35. Paravastu, A. K., Leapman, R. D., Yau, W.-M., and Tycko, R. (2008) Molecular structural basis for polymorphism in Alzheimer'sβ-amyloid fibrils. Proc. Natl. Acad. Sci. 105, 18349-18354
36. Whittemore, N. A., Mishra, R., Kheterpal, I., Williams, A. D., Wetzel, R., and Serpersu, E. H. (2005) Hydrogen-deuterium (H/D) exchange mapping of Aβ 1-40 amyloid fibril secondary structure using nuclear magnetic resonance spectroscopy. Biochemistry 44, 4434-4441
37. Kim, K. S., Miller, D. L., Sapienza, V. J., Chen, C. M. J., Bai, C., Grundke-Iqbal, I., Currie, J. R., and Wisniewski, H. M. (1988) Production and characterization of monoclonal antibodies reactive to synthetic cerebrovascular amyloid protein. Neurosci. Res. Commun. 2, 121-130
38. Bard, F., Cannon, C., Barbour, R., Burke, R. L., Games, D., Grajeda, H., Guido, T., Hu, K., Huang, J., Johnson-Wood, K., Khan, K., Kholodenko, D., Lee, M., Lieberburg, I., Motter, R., Nguyen, M., Soriano, F., Vasquez, N., Weiss, K., Welch, B., Seubert, P., Schenk, D., and Yednock, T. (2000) Peripherally administered antibodies against amyloid β-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat. Med. 6, 916-919
39. Schroeter, S., Khan, K., Barbour, R., Doan, M., Chen, M., Guido, T., Gill, D., Basi, G., Schenk, D., Seubert, P., and Games, D. (2008) Immunotherapy reduces vascular amyloid-β in PDAPP mice. J. Neurosci. 28, 6787-6793
40. Mattson, M. P., and Chan, S. L. (2003) Good and bad amyloid antibodies. Science 301, 1847-1849
41. Morgan, D., Diamond, D. M., Gottschall, P. E., Ugen, K. E., Dickey, C., Hardy, J., Duff, K., Jantzen, P., Di Carlo, G., Wilcock, D., Connor, K., Hatcher, J., Hope, C., Gordon, M., and Arendash, G. W. (2000) Aβ peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 408, 982-985
42. Wilcock, D. M., Rojiani, A., Rosenthal, A., Subbarao, S., Freeman, M. J., Gordon, M. N., and Morgan, D. (2004) Passive immunotherapy against Aβ in aged APP transgenic mice reverses cognitive deficits and depletes parenchymal amyloid deposits in spite of increased vascular amyloid and microhemorrhage. J. Neuroinflammation 1, 24
43. Neff, F., Wei, X., Nölker, C., Bacher, M., Du, Y., and Dodel, R. (2008) Immunotherapy and naturally occurring autoantibodies in neurodegenerative disorders. Autoimmun. Rev. 7, 501-507
44. Dodart, J. C., Bales, K. R., Gannon, K. S., Greene, S. J., De Mattos, R. B., Mathis, C., De Long, C. A., Wu, S., Wu, X., Holtzman, D. M., and Paul, S. M. (2002) Immunization reverses memory deficits without reducing brain Aβ burden in Alzheimer's disease model. Nat. Neurosci. 5, 452-457
45. Rasool, S., Albay, R., 3rd, Martinez-Coria, H., Breydo, L., Wu, J., Milton, S., Misra, S., Tran, A., Pensalfini, A., Laferla, F., Kayed, R., and Glabe, C. G. (2012) Vaccination with a non-human random sequence amyloid oligomer mimic results in improved cognitive function and reduced plaque deposition and micro hemorrhage in Tg2576 mice. Mol. Neurodegener. 7, 37
46. Goñi, F., Prelli, F., Ji, Y., Scholtzova, H., Yang, J., Sun, Y., Liang, F. X., Kascsak, R., Kascsak, R., Mehta, P., and Wisniewski, T. (2010) Immunomodulation targeting abnormal protein conformation reduces pathology in a mouse model of Alzheimer's disease. PLoS One 5, e13391