Tailoring the antibody response to aggregated aβ using novel Alzheimer-vaccines

PLoS ONE

Volumn 10, Issue 1, 2015, Pages

  Mandler, Markus ^a   Santic, Radmila ^a   Gruber, Petra ^a   Cinar, Yeliz ^b,c   Pichler, Dagmar ^a   Funke, Susanne Aileen ^b,d   Willbold, Dieter ^b   Schneeberger, Achim ^a   Schmidt, Walter ^a   Mattner, Frank ^a  

^a AFFiRiS GmbH   (Austria)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c ABBOTT GMBH AND CO KG   (Germany)

^d University of Applied Sciences and Arts   (Germany)

Author keywords

Max planck ring 2

Indexed keywords

AD01 PEPTIDE VACCINE; AD02 PEPTIDE VACCINE; AFFITOPE PEPTIDE VACCINE; ALZHEIMER DISEASE VACCINE; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR ALPHA PROTEIN; AMYLOID PRECURSOR PROTEIN; PEPTIDE VACCINE; UNCLASSIFIED DRUG; ANTIBODY; PEPTIDE LIBRARY;

AMYLOID NEUROPATHY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY DETECTION; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ARTICLE; BRAIN PROTECTION; CONTROLLED STUDY; DRUG RESPONSE; FEMALE; FUNCTIONAL ASSESSMENT; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOREACTIVITY; NONHUMAN; PROTEIN DETERMINATION; PROTEIN FUNCTION; T LYMPHOCYTE; VACCINATION; VACCINE PRODUCTION; ALZHEIMER DISEASE; ANIMAL; C57BL MOUSE; IMMUNOLOGY; MOUSE; PEPTIDE LIBRARY;

MUS MUSCULUS;

ALZHEIMER DISEASE; ALZHEIMER VACCINES; AMYLOID BETA-PEPTIDES; ANIMALS; ANTIBODIES; FEMALE; MICE; MICE, INBRED C57BL; PEPTIDE LIBRARY;

EID: 84921772464     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0115237     Document Type: Article

References (54)

1. Wimo A, Prince M (2010) World Alzheimer Report 2010: The glocal economic impact of dementia.
2. Dubois B, Feldman HH, Jacova C, Cummings JL, Dekosky ST, et al. (2010) Revising the definition of Alzheimer's disease: a new lexicon. Lancet Neurol 9: 1118-1127. doi: 10.1016/S1474-4422(10) 70223-4 PMID: 20934914
3. Lyketsos CG, Colenda CC, Beck C, Blank K, Doraiswamy MP, et al. (2006) Position statement of the American Association for Geriatric Psychiatry regarding principles of care for patients with dementia resulting from Alzheimer disease. Am J Geriatr Psychiatry 14: 561-572. doi: 10.1097/01.JGP. 0000221334.65330.55 PMID: 16816009
4. Haass C, Koo EH, Mellon A, Hung AY, Selkoe DJ (1992) Targeting of cell-surface beta-amyloid precursor protein to lysosomes: alternative processing into amyloid-bearing fragments. Nature 357: 500-503. doi: 10.1038/357500a0 PMID: 1608449
5. Seubert P, Vigo-Pelfrey C, Esch F, Lee M, Dovey H, et al. (1992) Isolation and quantification of soluble Alzheimer's beta-peptide from biological fluids. Nature 359: 325-327. doi: 10.1038/359325a0 PMID: 1406936
6. Shoji M, Golde TE, Ghiso J, Cheung TT, Estus S, et al. (1992) Production of the Alzheimer amyloid beta protein by normal proteolytic processing. Science 258: 126-129. doi: 10.1126/science.1439760 PMID: 1439760
7. Tomic JL, Pensalfini A, Head E, Glabe CG (2009) Soluble fibrillar oligomer levels are elevated in Alzheimer's disease brain and correlate with cognitive dysfunction. Neurobiol Dis 35: 352-358. doi: 10.1016/ j.nbd.2009.05.024 PMID: 19523517
8. Benilova I, Karran E, De Strooper B (2012) The toxic Abeta oligomer and Alzheimer's disease: an emperor in need of clothes. Nat Neurosci 15: 349-357. doi: 10.1038/nn.3028 PMID: 22286176
9. Schneeberger A, Mandler M, Mattner F, Schmidt W. (2010) AFFITOME(R) technology in neurodegenerative diseases: the doubling advantage. Hum Vaccin 6: 948-952. doi: 10.4161/hv.6.11.13217 PMID: 20980801
10. Le Poole IC, Luiten RM (2008) Autoimmune etiology of generalized vitiligo. Curr Dir Autoimmun 10: 227-243. doi: 10.1159/000131485 PMID: 18460889
11. Orgogozo JM, Gilman S, Dartigues JF, Laurent B, Puel M, et al. (2003) Subacute meningoencephalitis in a subset of patients with AD after Abeta42 immunization. Neurology 61: 46-54. doi: 10.1212/01. WNL.0000073623.84147.A8 PMID: 12847155
12. Rosenfeld MR, Dalmau J. (2010) Update on paraneoplastic and autoimmune disorders of the central nervous system. Semin Neurol 30: 320-331. doi: 10.1055/s-0030-1255223 PMID: 20577938
13. Wiessner C, Wiederhold KH, Tissot AC, Frey P, Danner S, et al. (2011) The second-generation active Abeta immunotherapy CAD106 reduces amyloid accumulation in APP transgenic mice while minimizing potential side effects. J Neurosci 31: 9323-9331. doi: 10.1523/JNEUROSCI.0293-11.2011 PMID: 21697382
14. Muhs A, Hickman DT, Pihlgren M, Chuard N, Giriens V, et al. (2007) Liposomal vaccines with confor-mation-specific amyloid peptide antigens define immune response and efficacy in APP transgenic mice. Proc Natl Acad Sci U S A 104: 9810-9815. doi: 10.1073/pnas.0703137104 PMID: 17517595
15. Wang CY, Finstad CL, Walfield AM, Sia C, Sokoll KK, et al. (2007) Site-specific UBITh amyloid-beta vaccine for immunotherapy of Alzheimer's disease. Vaccine 25: 3041-3052. doi: 10.1016/j.vaccine. 2007.01.031 PMID: 17287052
16. Liu B, Frost JL, Sun J, Fu H, Grimes S, et al. (2013) MER5101, a novel Abeta1-15:DT conjugate vaccine, generates a robust anti-Abeta antibody response and attenuates Abeta pathology and cognitive deficits in APPswe/PS1DeltaE9 transgenic mice. J Neurosci 33: 7027-7037. doi: 10.1523/ JNEUROSCI.5924-12.2013 PMID: 23595760
17. Giuffrida ML, Caraci F, Pignataro B, Cataldo S, De Bona P, et al. (2009) Beta-amyloid monomers are neuroprotective. J Neurosci 29: 10582-10587. doi: 10.1523/JNEUROSCI.1736-09.2009 PMID: 19710311
18. Chen Y, Dong C (2009) Abeta40 promotes neuronal cell fate in neural progenitor cells. Cell Death Differ 16: 386-394. doi: 10.1038/cdd.2008.94 PMID: 18566600
19. Kamenetz F, Tomita T, Hsieh H, Seabrook G, Borchelt D, et al. (2003) APP processing and synaptic function. Neuron 37: 925-937. doi: 10.1016/S0896-6273(03)00124-7 PMID: 12670422
20. Sotthibundhu A, Li QX, ThangniponW, Coulson EJ (2009) Abeta(1-42) stimulates adult SVZ neurogenesis through the p75 neurotrophin receptor. Neurobiol Aging 30: 1975-1985. doi: 10.1016/j. neurobiolaging.2008.02.004 PMID: 18374455
21. Freir DB, Fedriani R, Scully D, Smith IM, Selkoe DJ, et al. (2011) Abeta oligomers inhibit synapse remodelling necessary for memory consolidation. Neurobiol Aging 32: 2211-2218. doi: 10.1016/j. neurobiolaging.2010.01.001 PMID: 20097446
22. Hartley DM, Walsh DM, Ye CP, Diehl T, Vasquez S, et al. (1999) Protofibrillar intermediates of amyloid beta-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons. J Neurosci 19: 8876-8884. PMID: 10516307
23. Mucke L, Selkoe DJ (2012) Neurotoxicity of amyloid beta-protein: synaptic and network dysfunction. Cold Spring Harb Perspect Med 2: a006338. PMID: 22762015
24. Reed MN, Hofmeister JJ, Jungbauer L, Welzel AT, Yu C, et al. (2011) Cognitive effects of cell-derived and synthetically derived Abeta oligomers. Neurobiol Aging 32: 1784-1794. doi: 10.1016/j. neurobiolaging.2009.11.007 PMID: 20031278
25. Rogers DC, Jones DN, Nelson PR, Jones CM, Quilter CA, et al. (1999) Use of SHIRPA and discriminant analysis to characterise marked differences in the behavioural phenotype of six inbred mouse strains. Behav Brain Res 105: 207-217. doi: 10.1016/S0166-4328(99)00072-8 PMID: 10563494
26. Mandler M, Rockenstein E, Ubhi K, Hansen L, Adame A, et al. (2012) Detection of peri-synaptic amy-loid-beta pyroglutamate aggregates in early stages of Alzheimer' s disease and in AbetaPP transgenic mice using a novel monoclonal antibody. J Alzheimers Dis 28: 783-794. PMID: 22064070
27. Johansson AS, Berglind-Dehlin F, Karlsson G, Edwards K, Gellerfors P, et al. (2006) Physiochemical characterization of the Alzheimer's disease-related peptides A beta 1-42Arctic and A beta 1-42wt. FEBS J 273: 2618-2630. doi: 10.1111/j.1742-4658.2006.05263.x PMID: 16817891
28. Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11: 47-60. doi: 10.1016/0165-0270(84)90007-4 PMID: 6471907
29. Comery TA, Martone RL, Aschmies S, Atchison KP, Diamantidis G, et al. (2005) Acute gammasecretase inhibition improves contextual fear conditioning in the Tg2576 mouse model of Alzheimer's disease. J Neurosci 25: 8898-8902. doi: 10.1523/JNEUROSCI.2693-05.2005 PMID: 16192379
30. Hock C, Konietzko U, Streffer JR, Tracy J, Signorell A, et al. (2003) Antibodies against beta-amyloid slow cognitive decline in Alzheimer's disease. Neuron 38: 547-554. doi: 10.1016/S0896-6273(03) 00294-0 PMID: 12765607
31. DeMattos RB, Bales KR, Cummins DJ, Dodart JC, Paul SM, et al. (2001) Peripheral anti-A beta antibody alters CNS and plasma A beta clearance and decreases brain A beta burden in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 98: 8850-8855. doi: 10.1073/pnas.151261398 PMID: 11438712
32. DeMattos RB, Bales KR, Cummins DJ, Paul SM, Holtzman DM (2002) Brain to plasma amyloid-beta efflux: a measure of brain amyloid burden in a mouse model of Alzheimer 's disease. Science 295: 2264-2267. doi: 10.1126/science.1067568 PMID: 11910111
33. Lemere CA, Spooner ET, LaFrancois J, Malester B, Mori C, et al. (2003) Evidence for peripheral clearance of cerebral Abeta protein following chronic, active Abeta immunization in PSAPP mice. Neurobiol Dis 14: 10-18. doi: 10.1016/S0969-9961(03)00044-5 PMID: 13678662
34. Wilcock DM, Colton CA (2009) Immunotherapy, vascular pathology, and microhemorrhages in transgenic mice. CNS Neurol Disord Drug Targets 8: 50-64. doi: 10.2174/187152709787601858 PMID: 19275636
35. Oyarbide-Valencia K, van den Boorn JG, Denman CJ, Li M, Carlson JM, et al. (2006) Therapeutic implications of autoimmune vitiligo T cells. Autoimmun Rev 5: 486-492. doi: 10.1016/j.autrev.2006.03.012 PMID: 16920575
36. Fujinami RS, von Herrath MG, Christen U, Whitton JL (2006) Molecular mimicry, bystander activation, or viral persistence: infections and autoimmune disease. Clin Microbiol Rev 19: 80-94. doi: 10.1128/ CMR.19.1.80-94.2006 PMID: 16418524
37. Yankner BA, Caceres A, Duffy LK (1990) Nerve growth factor potentiates the neurotoxicity of beta amyloid. Proc Natl Acad Sci U S A 87: 9020-9023. doi: 10.1073/pnas.87.22.9020 PMID: 2174172
38. Heber S, Herms J, Gajic V, Hainfellner J, Aguzzi A, et al. (2000) Mice with combined gene knock-outs reveal essential and partially redundant functions of amyloid precursor protein family members. J Neurosci 20: 7951-7963. PMID: 11050115
39. Herms J, Anliker B, Heber S, Ring S, Fuhrmann M, et al. (2004) Cortical dysplasia resembling human type 2 lissencephaly in mice lacking all three APP family members. EMBO J 23: 4106-4115. doi: 10. 1038/sj.emboj.7600390 PMID: 15385965
40. Leyssen M, Ayaz D, Hebert SS, Reeve S, De Strooper B, et al. (2005) Amyloid precursor protein promotes post-developmental neurite arborization in the Drosophila brain. EMBO J 24: 2944-2955. doi: 10.1038/sj.emboj.7600757 PMID: 16052209
41. Wang P, Yang G, Mosier DR, Chang P, Zaidi T, et al. (2005) Defective neuromuscular synapses in mice lacking amyloid precursor protein (APP) and APP-Like protein 2. J Neurosci 25: 1219-1225. doi: 10.1523/JNEUROSCI.4660-04.2005 PMID: 15689559
42. Priller C, Bauer T, Mitteregger G, Krebs B, Kretzschmar HA, et al. (2006) Synapse formation and function is modulated by the amyloid precursor protein. J Neurosci 26: 7212-7221. doi: 10.1523/ JNEUROSCI.1450-06.2006 PMID: 16822978
43. Hayashi Y, Kashiwagi K, Ohta J, Nakajima M, Kawashima T, et al. (1994) Alzheimer amyloid protein precursor enhances proliferation of neural stem cells from fetal rat brain. Biochem Biophys Res Commun 205: 936-943. doi: 10.1006/bbrc.1994.2755 PMID: 7999135
44. Small DH, Nurcombe V, Reed G, Clarris H, Moir R, et al. (1994) A heparin-binding domain in the amyloid protein precursor of Alzheimer's disease is involved in the regulation of neurite outgrowth. J Neurosci 14: 2117-2127. PMID: 8158260
45. Ohsawa I, Takamura C, Morimoto T, Ishiguro M, Kohsaka S (1999) Amino-terminal region of secreted form of amyloid precursor protein stimulates proliferation of neural stem cells. Eur J Neurosci 11: 1907-1913. doi: 10.1046/j.1460-9568.1999.00601.x PMID: 10336659
46. Caille I, Allinquant B, Dupont E, Bouillot C, Langer A, et al. (2004) Soluble form of amyloid precursor protein regulates proliferation of progenitors in the adult subventricular zone. Development 131: 2173-2181. doi: 10.1242/dev.01103 PMID: 15073156
47. Taylor CJ, Ireland DR, Ballagh I, Bourne K, Marechal NM, et al. (2008) Endogenous secreted amyloid precursor protein-alpha regulates hippocampal NMDA receptor function, long-term potentiation and spatial memory. Neurobiol Dis 31: 250-260. doi: 10.1016/j.nbd.2008.04.011 PMID: 18585048
48. Ishida A, Furukawa K, Keller JN, Mattson MP (1997) Secreted form of beta-amyloid precursor protein shifts the frequency dependency for induction of LTD, and enhances LTP in hippocampal slices. Neuroreport 8: 2133-2137. doi: 10.1097/00001756-199707070-00009 PMID: 9243598
49. Roch JM, Masliah E, Roch-Levecq AC, Sundsmo MP, Otero DA, et al. (1994) Increase of synaptic density and memory retention by a peptide representing the trophic domain of the amyloid beta/A4 protein precursor. Proc Natl Acad Sci U S A 91: 7450-7454. doi: 10.1073/pnas.91.16.7450 PMID: 8052602
50. Meziane H, Dodart JC, Mathis C, Little S, Clemens J, et al. (1998) Memory-enhancing effects of secreted forms of the beta-amyloid precursor protein in normal and amnestic mice. Proc Natl Acad Sci U S A 95: 12683-12688. doi: 10.1073/pnas.95.21.12683 PMID: 9770546
51. Pride M, Seubert P, Grundman M, Hagen M, Eldridge J, et al. (2008) Progress in the active immunotherapeutic approach to Alzheimer's disease: clinical investigations into AN1792-associated meningoencephalitis. Neurodegener Dis 5: 194-196. doi: 10.1159/000113700 PMID: 18322388
52. Wilcock DM, Gharkholonarehe N, Van Nostrand WE, Davis J, Vitek MP, et al. (2009) Amyloid reduction by amyloid-beta vaccination also reduces mouse tau pathology and protects from neuron loss in two mouse models of Alzheimer's disease. J Neurosci 29: 7957-7965. doi: 10.1523/JNEUROSCI.1339-09.2009 PMID: 19553436
53. Wilcock DM, Jantzen PT, Li Q, Morgan D, Gordon MN (2007) Amyloid-beta vaccination, but not nitrononsteroidal anti-inflammatory drug treatment, increases vascular amyloid and microhemorrhage while both reduce parenchymal amyloid. Neuroscience 144: 950-960. doi: 10.1016/j.neuroscience.2006.10. 020 PMID: 17137722
54. Mandler M, Valera E, Rockenstein E, Weninger H, Patrick C, et al. (2014) Next-generation active immunization approach for synucleinopathies: implications for Parkinson's disease clinical trials. Acta Neuropathol 127(6): 861-79. doi: 10.1007/s00401-014-1256-4 PMID: 24525765