The conformational epitope for a new Aβ42 protofibril-selective antibody partially overlaps with the peptide N-terminal region

Journal of Neurochemistry

Volumn 143, Issue 6, 2017, Pages 736-749

  Colvin, Benjamin A ^a   Rogers, Victoria A ^a   Kulas, Joshua A ^b   Ridgway, Elizabeth A ^a   Amtashar, Fatima S ^a   Combs, Colin K ^b   Nichols, Michael R ^a  

^a UNIVERSITY OF MISSOURI ST LOUIS   (United States)

^b UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

amyloid beta; conformation selective antibody; protofibrils

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; ANTIBODY; ANTIBODY ST. LOUIS; EPITOPE; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (1-42); PEPTIDE FRAGMENT;

ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNIZATION; IN VITRO STUDY; LIMIT OF QUANTITATION; MICROGLIA; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; ANIMAL; ANTIBODY SPECIFICITY; BETA SHEET; C57BL MOUSE; CHEMISTRY; IMMUNOLOGY; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ANTIBODIES; ANTIBODY SPECIFICITY; EPITOPES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION, BETA-STRAND;

EID: 85034743014     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.14211     Document Type: Article

References (44)

1. Bradford M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254.
2. Cummings J., Morstorf T. and Lee G. (2016) Alzheimer's drug-development pipeline: 2016. Alzheimers Dement. 2, 222–232.
3. Deshpande A., Kawai H., Metherate R., Glabe C. G. and Busciglio J. (2009) A role for synaptic zinc in activity-dependent Aβ oligomer formation and accumulation at excitatory synapses. J. Neurosci. 29, 4004–4015.
4. Englund H., Sehlin D., Johansson A. S., Nilsson L. N., Gellerfors P., Paulie S., Lannfelt L. and Pettersson F. E. (2007) Sensitive ELISA detection of amyloid-beta protofibrils in biological samples. J. Neurochem. 103, 334–345.
5. Gardberg A. S., Dice L. T., Ou S., Rich R. L., Helmbrecht E., Ko J., Wetzel R., Myszka D. G., Patterson P. H. and Dealwis C. (2007) Molecular basis for passive immunotherapy of Alzheimer's disease. Proc. Natl Acad. Sci. USA 104, 15659–15664.
6. Gardberg A., Dice L., Pridgen K., Ko J., Patterson P., Ou S., Wetzel R. and Dealwis C. (2009) Structures of Aβ-related peptide-monoclonal antibody complexes. Biochemistry 48, 5210–5217.
7. Georganopoulou D. G., Chang L., Nam J. M., Thaxton C. S., Mufson E. J., Klein W. L. and Mirkin C. A. (2005) Nanoparticle-based detection in cerebral spinal fluid of a soluble pathogenic biomarker for Alzheimer's disease. Proc. Natl Acad. Sci. USA 102, 2273–2276.
8. Goure W. F., Krafft G. A., Jerecic J. and Hefti F. (2014) Targeting the proper amyloid-beta neuronal toxins: a path forward for Alzheimer's disease immunotherapeutics. Alzheimers Res. Ther. 6, 42.
9. Gouwens L. K., Makoni N. J., Rogers V. A. and Nichols M. R. (2016) Amyloid-β42 protofibrils are internalized by microglia more extensively than monomers. Brain Res. 1648, 485–495.
10. Gravina S. A., Ho L., Eckman C. B., Long K. E., Otvos L., Jr, Younkin L. H., Suzuki N. and Younkin S. G. (1995) Amyloid β protein (Aβ) in Alzheimer's disease brain. Biochemical and immunocytochemical analysis with antibodies specific for forms ending at Aβ40 or Aβ42(43). J. Biol. Chem. 270, 7013–7016.
11. 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.
12. Harper J. D., Wong S. S., Lieber C. M. and LansburyJr P. T. (1997) Observation of metastable Aβ amyloid protofibrils by atomic force microscopy. Chem. Biol. 4, 119–125.
13. Harper J. D., Wong S. S., Lieber C. M. and Lansbury P. T. Jr (1999) Assembly of Aβ amyloid peptides: an in vitro model for a possible early event in Alzheimer's disease. Biochemistry 38, 8972–8980.
14. Hatami A., Albay R., 3rd, Monjazeb S., Milton S. and Glabe C. (2014) Monoclonal antibodies against Aβ42 fibrils distinguish multiple aggregation state polymorphisms in vitro and in Alzheimer disease brain. J. Biol. Chem. 289, 32131–32143.
15. Jan A., Hartley D. M. and Lashuel H. A. (2010) Preparation and characterization of toxic Aβ aggregates for structural and functional studies in Alzheimer's disease research. Nat. Protoc. 5, 1186–1209.
16. Jankowsky J. L., Fadale D. J., Anderson J. et al. (2004) Mutant presenilins specifically elevate the levels of the 42 residue β-amyloid peptide in vivo: evidence for augmentation of a 42-specific γ secretase. Hum. Mol. Genet. 13, 159–170.
17. 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.
18. Kayed R., Head E., Sarsoza F. et al. (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.
19. Kheterpal I., Lashuel H. A., Hartley D. M., Walz T., Lansbury P. T., Jr and Wetzel R. (2003) Aβ protofibrils possess a stable core structure resistant to hydrogen exchange. Biochemistry 42, 14092–14098.
20. 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.
21. Koffie R. M., Meyer-Luehmann M., Hashimoto T. et al. (2009) Oligomeric amyloid β associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc. Natl Acad. Sci. USA 106, 4012–4017.
22. Kukar T., Murphy M. P., Eriksen J. L. et al. (2005) Diverse compounds mimic Alzheimer disease-causing mutations by augmenting Aβ42 production. Nat. Med. 11, 545–550.
23. 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.
24. Lannfelt L., Moller C., Basun H., Osswald G., Sehlin D., Satlin A., Logovinsky V. and Gellerfors P. (2014) Perspectives on future Alzheimer therapies: amyloid-β protofibrils - a new target for immunotherapy with BAN2401 in Alzheimer's disease. Alzheimers Res. Ther. 6, 16.
25. Lee E. B., Leng L. Z., Zhang B., Kwong L., Trojanowski J. Q., Abel T. and Lee V. M. (2006) Targeting amyloid-β peptide (Aβ) oligomers by passive immunization with a conformation-selective monoclonal antibody improves learning and memory in Aβ precursor protein (APP) transgenic mice. J. Biol. Chem. 281, 4292–4299.
26. Lesne S., Koh M. T., Kotilinek L., Kayed R., Glabe C. G., Yang A., Gallagher M. and Ashe K. H. (2006) A specific amyloid-β protein assembly in the brain impairs memory. Nature 440, 352–357.
27. 40-specific mAbs attenuate amyloid deposition in an Alzheimer disease mouse model. J. Clin. Invest. 116, 193–201.
28. Logovinsky V., Satlin A., Lai R., Swanson C., Kaplow J., Osswald G., Basun H. and Lannfelt L. (2016) Safety and tolerability of BAN2401 - a clinical study in Alzheimer's disease with a protofibril selective Aβ antibody. Alzheimers Res. Ther. 8, 14.
29. Masters C. L., Bateman R., Blennow K., Rowe C. C., Sperling R. A. and Cummings J. L. (2016) Alzheimer's disease. Nat. Rev. Dis. Primers 1, 15056.
30. Meli G., Visintin M., Cannistraci I. and Cattaneo A. (2009) Direct in vivo intracellular selection of conformation-sensitive antibody domains targeting Alzheimer's amyloid-β oligomers. J. Mol. Biol. 387, 584–606.
31. Nichols M. R., Moss M. A., Reed D. K., Lin W. L., Mukhopadhyay R., Hoh J. H. and Rosenberry T. L. (2002) Growth of β-amyloid(1-40) protofibrils by monomer elongation and lateral association. Characterization of distinct products by light scattering and atomic force microscopy. Biochemistry 41, 6115–6127.
32. Nichols M. R., Colvin B. A., Hood E. A., Paranjape G. S., Osborn D. C. and Terrill-Usery S. E. (2015) Biophysical comparison of soluble amyloid-β(1-42) protofibrils, oligomers, and protofilaments. Biochemistry 54, 2193–2204.
33. O'Nuallain B., Freir D. B., Nicoll A. J., Risse E., Ferguson N., Herron C. E., Collinge J. and Walsh D. M. (2010) Amyloid β-protein dimers rapidly form stable synaptotoxic protofibrils. J. Neurosci. 30, 14411–14419.
34. Paranjape G. S., Gouwens L. K., Osborn D. C. and Nichols M. R. (2012) Isolated amyloid-β(1-42) protofibrils, but not isolated fibrils, are robust stimulators of microglia. ACS Chem. Neurosci. 3, 302–311.
35. Paranjape G. S., Terrill S. E., Gouwens L. K., Ruck B. M. and Nichols M. R. (2013) Amyloid-β(1-42) protofibrils formed in modified artificial cerebrospinal fluid bind and activate microglia. J. Neuroimmune Pharmacol. 8, 312–322.
36. Selkoe D. J., Podlisny M. B., Joachim C. L., Vickers E. A., Lee G., Fritz L. C. and Oltersdorf T. (1988) β-Amyloid precursor protein of Alzheimer disease occurs as 110- to 135-kilodalton membrane-associated proteins in neural and nonneural tissues. Proc. Natl Acad. Sci. USA 85, 7341–7345.
37. Seubert P., Vigo-Pelfrey C., Esch F. et al. (1992) Isolation and quantification of soluble Alzheimer's β-peptide from biological fluids. Nature 359, 325–327.
38. Terrill-Usery S. E., Mohan M. J. and Nichols M. R. (2014) Amyloid-β(1-42) protofibrils stimulate a quantum of secreted IL-1β despite significant intracellular IL-1β accumulation in microglia. Biochim. Biophys. Acta 1842, 2276–2285.
39. Terrill-Usery S. E., Colvin B. A., Davenport R. E. and Nichols M. R. (2016) Aβ40 has a subtle effect on Aβ42 protofibril formation, but to a lesser degree than Aβ42 concentration, in Aβ42/Aβ40 mixtures. Arch. Biochem. Biophys. 597, 1–11.
40. Walsh D. M., Lomakin A., Benedek G. B., Condron M. M. and Teplow D. B. (1997) Amyloid β-protein fibrillogenesis: detection of a protofibrillar intermediate. J. Biol. Chem. 272, 22364–22372.
41. 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 β-protein fibrillogenesis: structure and biological activity of protofibrillar intermediates. J. Biol. Chem. 274, 25945–25952.
42. Wong C. W., Quaranta V. and Glenner G. G. (1985) Neuritic plaques and cerebrovascular amyloid in Alzheimer disease are antigenically related. Proc. Natl Acad. Sci. USA 82, 8729–8732.
43. Ye C. P., Selkoe D. J. and Hartley D. M. (2003) Protofibrils of amyloid β-protein inhibit specific K+ currents in neocortical cultures. Neurobiol. Dis. 13, 177–190.
44. Zheng H., Jiang M., Trumbauer M. E. et al. (1995) β-Amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity. Cell 81, 525–531.