Immunogenicity of DNA- and recombinant protein-based Alzheimer Disease epitope vaccines

References

• Dementia WHO. key facts. http://www.who.int/mediacentre/factsheets/fs362/en/, 2012.
   Google Scholar
• Price DL, Sisodia SS. Cellular and molecular biology of Alzheimer’s disease and animal models. Annu Rev Med 1994; 45:435 - 46; http://dx.doi.org/10.1146/annurev.med.45.1.435; PMID: 8198393
   PubMed Web of Science ®Google Scholar
• Selkoe DJ. The molecular pathology of Alzheimer’s disease. Neuron 1991; 6:487 - 98; http://dx.doi.org/10.1016/0896-6273(91)90052-2; PMID: 1673054
   PubMed Web of Science ®Google Scholar
• Selkoe DJ. Alzheimer’s disease: a central role for amyloid. J Neuropathol Exp Neurol 1994; 53:438 - 47; http://dx.doi.org/10.1097/00005072-199409000-00003; PMID: 8083687
   PubMed Web of Science ®Google Scholar
• Esler WP, Wolfe MS. A portrait of Alzheimer secretases--new features and familiar faces. Science 2001; 293:1449 - 54; http://dx.doi.org/10.1126/science.1064638; PMID: 11520976
   PubMed Web of Science ®Google Scholar
• Orgogozo JM, Gilman S, Dartigues JF, Laurent B, Puel M, Kirby LC, Jouanny P, Dubois B, Eisner L, Flitman S, et al. Subacute meningoencephalitis in a subset of patients with AD after Abeta42 immunization. Neurology 2003; 61:46 - 54; http://dx.doi.org/10.1212/01.WNL.0000073623.84147.A8; PMID: 12847155
   PubMed Web of Science ®Google Scholar
• Imbimbo BP, Ottonello S, Frisardi V, Solfrizzi V, Greco A, Seripa D, Pilotto A, Panza F. Solanezumab for the treatment of mild-to-moderate Alzheimer’s disease. Expert Rev Clin Immunol 2012; 8:135 - 49; http://dx.doi.org/10.1586/eci.11.93; PMID: 22288451
   PubMed Web of Science ®Google Scholar
• Kerchner GA, Boxer AL. Bapineuzumab. Expert Opin Biol Ther 2010; 10:1121 - 30; http://dx.doi.org/10.1517/14712598.2010.493872; PMID: 20497044
   PubMed Web of Science ®Google Scholar
• Delrieu J, Ousset PJ, Vellas B. Gantenerumab for the treatment of Alzheimer’s disease. Expert Opin Biol Ther 2012; 12:1077 - 86; http://dx.doi.org/10.1517/14712598.2012.688022; PMID: 22583155
   PubMed Web of Science ®Google Scholar
• Lemere CA. Immunotherapy for Alzheimer’s disease: hoops and hurdles. Mol Neurodegener 2013; 8:36; http://dx.doi.org/10.1186/1750-1326-8-36; PMID: 24148220
   PubMed Web of Science ®Google Scholar
• Eli Lilly and Company Announcment. Eli Lilly and Company Announces Top-Line Results on Solanezumab Phase 3 Clinical Trials in Patients with Alzheimer's Disease. Available at http://newsroom.lilly.com/releasedetail.cfm?releaseid=702211, 2012.
   Google Scholar
• Sperling R, Salloway S, Raskind MA, Ferris S, Liu E, Yuen E, et al. A randomized double-blind, placebocontrolled clinical trila of intravenous bapineuzumab in patients with Alzheimer's disease who are apolipoprotein E ε4 carriers. 16th Congress of the European Federation of Neurological Societies. Stokholm, Sweden, 2012.
   Google Scholar
• Salloway S, Sperling R, Honig L, Porsteinsson A, Sabbagh M, Liu E, et al. A randomized double-blind, placebocontrolled clinical trila of intravenous bapineuzumab in patients with Alzheimer's disease who are apolipoprotein E ε4 non-carriers. 16th Congress of the European Federation of Neurological Societies. Stokholm, Sweden, 2012.
   Google Scholar
• Farlow M, Arnold SE, van Dyck CH, Aisen PS, Snider BJ, Porsteinsson AP, Friedrich S, Dean RA, Gonzales C, Sethuraman G, et al. Safety and biomarker effects of solanezumab in patients with Alzheimer’s disease. Alzheimers Dement 2012; 8:261 - 71; http://dx.doi.org/10.1016/j.jalz.2011.09.224; PMID: 22672770
   PubMed Web of Science ®Google Scholar
• NIH. Gantenerumab for Prodromal Alzheimer's Disease. http://www.nia.nih.gov/alzheimers/clinical-trials/gantenerumab-prodromal-alzheimers-disease.
   Google Scholar
• NIH. Dominantly Inherited Alzheimer Network Trial: An Opportunity to Prevent Dementia. A Study of Potential Disease Modifying Treatments in Individuals at Risk for or With a Type of Early Onset Alzheimer's Disease Caused by a Genetic Mutation. (DIAN TU). http://clinicaltrials.gov/ct2/show/NCT01760005.
   Google Scholar
• NIH. NIH-supported Alzheimer’s studies to focus on innovative treatments. http://www.nih.gov/news/health/jan2013/nia-14.htm. 2013.
   Google Scholar
• Agadjanyan MG, Ghochikyan A, Petrushina I, Vasilevko V, Movsesyan N, Mkrtichyan M, Saing T, Cribbs DH. Prototype Alzheimer’s disease vaccine using the immunodominant B cell epitope from beta-amyloid and promiscuous T cell epitope pan HLA DR-binding peptide. J Immunol 2005; 174:1580 - 6; PMID: 15661919
   PubMed Web of Science ®Google Scholar
• Ghochikyan A, Mkrtichyan M, Petrushina I, Movsesyan N, Karapetyan A, Cribbs DH, Agadjanyan MG. Prototype Alzheimer’s disease epitope vaccine induced strong Th2-type anti-Abeta antibody response with Alum to Quil A adjuvant switch. Vaccine 2006; 24:2275 - 82; http://dx.doi.org/10.1016/j.vaccine.2005.11.039; PMID: 16368167
   PubMed Web of Science ®Google Scholar
• Davtyan H, Mkrtichyan M, Movsesyan N, Petrushina I, Mamikonyan G, Cribbs DH, Agadjanyan MG, Ghochikyan A. DNA prime-protein boost increased the titer, avidity and persistence of anti-Abeta antibodies in wild-type mice. Gene Ther 2010; 17:261 - 71; http://dx.doi.org/10.1038/gt.2009.140; PMID: 19865176
   PubMed Web of Science ®Google Scholar
• Davtyan H, Ghochikyan A, Petrushina I, Hovakimyan A, Davtyan A, Poghosyan A, Marleau AM, Movsesyan N, Kiyatkin A, Rasool S, et al. Immunogenicity, efficacy, safety, and mechanism of action of epitope vaccine (Lu AF20513) for Alzheimer’s disease: prelude to a clinical trial. J Neurosci 2013; 33:4923 - 34; http://dx.doi.org/10.1523/JNEUROSCI.4672-12.2013; PMID: 23486963
   PubMed Web of Science ®Google Scholar
• Petrushina I, Ghochikyan A, Mktrichyan M, Mamikonyan G, Movsesyan N, Davtyan H, Patel A, Head E, Cribbs DH, Agadjanyan MG. Alzheimer’s disease peptide epitope vaccine reduces insoluble but not soluble/oligomeric Abeta species in amyloid precursor protein transgenic mice. J Neurosci 2007; 27:12721 - 31; http://dx.doi.org/10.1523/JNEUROSCI.3201-07.2007; PMID: 18003852
   PubMed Web of Science ®Google Scholar
• Delrieu J, Ousset PJ, Caillaud C, Vellas B. ‘Clinical trials in Alzheimer’s disease’: immunotherapy approaches. J Neurochem 2012; 120:Suppl 1 186 - 93; http://dx.doi.org/10.1111/j.1471-4159.2011.07458.x; PMID: 21883222
   PubMedGoogle Scholar
• Lobello K, Ryan JM, Liu E, Rippon G, Black R. Targeting Beta amyloid: a clinical review of immunotherapeutic approaches in Alzheimer’s disease. Int J Alzheimers Dis 2012; 2012:628070; http://dx.doi.org/10.1155/2012/628070; PMID: 22292124
   PubMedGoogle Scholar
• Lemere CA, Masliah E. Can Alzheimer disease be prevented by amyloid-beta immunotherapy?. Nat Rev Neurol 2010; 6:108 - 19; http://dx.doi.org/10.1038/nrneurol.2009.219; PMID: 20140000
   PubMed Web of Science ®Google Scholar
• Hickman DT, López-Deber MP, Ndao DM, Silva AB, Nand D, Pihlgren M, Giriens V, Madani R, St-Pierre A, Karastaneva H, et al. Sequence-independent control of peptide conformation in liposomal vaccines for targeting protein misfolding diseases. J Biol Chem 2011; 286:13966 - 76; http://dx.doi.org/10.1074/jbc.M110.186338; PMID: 21343310
   PubMed Web of Science ®Google Scholar
• Muhs A, Hickman DT, Pihlgren M, Chuard N, Giriens V, Meerschman C, van der Auwera I, van Leuven F, Sugawara M, Weingertner MC, et al. Liposomal vaccines with conformation-specific amyloid peptide antigens define immune response and efficacy in APP transgenic mice. Proc Natl Acad Sci U S A 2007; 104:9810 - 5; http://dx.doi.org/10.1073/pnas.0703137104; PMID: 17517595
   PubMed Web of Science ®Google Scholar
• Goodman JLUS. Food and Drug Administration Workshop: Adjuvants and Adjuvanted Preventive and Therapeutic Vaccines for Infectious Disease Indications 2008. Available from: http://www.fda.gov/downloads/BiologicsBloodVaccines/NewsEvents/WorkshopsMeetingsConferences/UCM095732.pdf
   Google Scholar
• Baylor NW, Egan W, Richman P. Aluminum salts in vaccines--US perspective. Vaccine 2002; 20:Suppl 3 S18 - 23; http://dx.doi.org/10.1016/S0264-410X(02)00166-4; PMID: 12184360
   PubMed Web of Science ®Google Scholar
• Rappuoli R, Mandl CW, Black S, De Gregorio E. Vaccines for the twenty-first century society. Nat Rev Immunol 2011; 11:865 - 72; PMID: 22051890
   PubMed Web of Science ®Google Scholar
• Galimberti D, Ghezzi L, Scarpini E. Immunotherapy against amyloid pathology in Alzheimer’s disease. J Neurol Sci 2013; 333:50 - 4; http://dx.doi.org/10.1016/j.jns.2012.12.013; PMID: 23299047
   PubMed Web of Science ®Google Scholar
• Winblad B, Andreasen N, Minthon L, Floesser A, Imbert G, Dumortier T, Maguire RP, Blennow K, Lundmark J, Staufenbiel M, et al. Safety, tolerability, and antibody response of active Aβ immunotherapy with CAD106 in patients with Alzheimer’s disease: randomised, double-blind, placebo-controlled, first-in-human study. Lancet Neurol 2012; 11:597 - 604; http://dx.doi.org/10.1016/S1474-4422(12)70140-0; PMID: 22677258
   PubMed Web of Science ®Google Scholar
• Schneeberger A, Mandler M, Mattner F, Schmidt W. AFFITOME® technology in neurodegenerative diseases: the doubling advantage. Hum Vaccin 2010; 6:948 - 52; http://dx.doi.org/10.4161/hv.6.11.13217; PMID: 20980801
   PubMed Web of Science ®Google Scholar
• International WHO. Clinical Trials. In: GmbH NP, ed., http://apps.who.int/trialsearch/trial.aspx?trialid=EUCTR2009-012394-35-DE, 2010.
   Google Scholar
• Genetic Engineering and Biotechnology News. AFFiRiS Invests in Public-Funded Lab to Develop Vaccine Against Diabetes and Cardiometabolic Diseases. http://www.genengnews.com/keywordsandtools/print/4/23255/.
   Google Scholar
• NIH. Study to Evaluate Safety, Tolerability and Immunogenicity of Vaccine (UB 311) in Subjects With Alzheimer's Disease. http://clinicaltrials.gov/ct2/show/NCT00965588.
   Google Scholar
• Savage MJ, Wu GY, McCampbell A, Wessner KR, Citron M, Liang X, et al. A novel multivalent Abeta peptide vaccine with preclinical evidence of a central immune response that generates antisera recognizing a wide range of abeta peptide species. Alzheimers Dement 2010; 6:S142; http://dx.doi.org/10.1016/j.jalz.2010.05.437
   Google Scholar
• Davtyan H, Ghochikyan A, Petrushina I, Hovakimyan A, Davtyan A, Cribbs DH, Agadjanyan MG. The MultiTEP platform-based Alzheimer’s disease epitope vaccine activates a broad repertoire of T helper cells in nonhuman primates. Alzheimers Dement 2014; Forthcoming http://dx.doi.org/10.1016/j.jalz.2013.12.003; PMID: 24560029
   PubMed Web of Science ®Google Scholar
• H. Lundbeck A/S. Lundbeck and Otsuka to co-develop a vaccine, Lu AF20513, their third collaborative development project to tackle Alzheimer's disease. http://investor.lundbeck.com/releasedetail.cfm?ReleaseID=813105. 2013.
   Google Scholar
• Mura T, Proust-Lima C, Jacqmin-Gadda H, Akbaraly TN, Touchon J, Dubois B, Berr C. Measuring cognitive change in subjects with prodromal Alzheimer’s disease. J Neurol Neurosurg Psychiatry 2013; Forthcoming http://dx.doi.org/10.1136/jnnp-2013-305078; PMID: 23840054
   PubMed Web of Science ®Google Scholar
• Babiuk LA, Pontarollo R, Babiuk S, Loehr B, van Drunen Littel-van den Hurk S. Induction of immune responses by DNA vaccines in large animals. Vaccine 2003; 21:649 - 58; http://dx.doi.org/10.1016/S0264-410X(02)00574-1; PMID: 12531334
   PubMed Web of Science ®Google Scholar
• Li L, Saade F, Petrovsky N. The future of human DNA vaccines. J Biotechnol 2012; 162:171 - 82; http://dx.doi.org/10.1016/j.jbiotec.2012.08.012; PMID: 22981627
   PubMed Web of Science ®Google Scholar
• Ferraro B, Morrow MP, Hutnick NA, Shin TH, Lucke CE, Weiner DB. Clinical applications of DNA vaccines: current progress. Clin Infect Dis 2011; 53:296 - 302; http://dx.doi.org/10.1093/cid/cir334; PMID: 21765081
   PubMed Web of Science ®Google Scholar
• Gregersen JP. DNA vaccines. Naturwissenschaften 2001; 88:504 - 13; http://dx.doi.org/10.1007/s00114-001-0270-2; PMID: 11824223
   PubMed Web of Science ®Google Scholar
• Ghochikyan A, Vasilevko V, Petrushina I, Movsesyan N, Babikyan D, Tian W, Sadzikava N, Ross TM, Head E, Cribbs DH, et al. Generation and characterization of the humoral immune response to DNA immunization with a chimeric beta-amyloid-interleukin-4 minigene. Eur J Immunol 2003; 33:3232 - 41; http://dx.doi.org/10.1002/eji.200324000; PMID: 14635031
   PubMed Web of Science ®Google Scholar
• Qu B, Rosenberg RN, Li L, Boyer PJ, Johnston SA. Gene vaccination to bias the immune response to amyloid-beta peptide as therapy for Alzheimer disease. Arch Neurol 2004; 61:1859 - 64; http://dx.doi.org/10.1001/archneur.61.12.1859; PMID: 15596606
   PubMed Web of Science ®Google Scholar
• Matsumoto Y, Niimi N, Kohyama K. Development of a new DNA vaccine for Alzheimer disease targeting a wide range of aβ species and amyloidogenic peptides. PLoS One 2013; 8:e75203; http://dx.doi.org/10.1371/journal.pone.0075203; PMID: 24086465
   PubMedGoogle Scholar
• Lambracht-Washington D, Qu BX, Fu M, Anderson LD Jr., Eagar TN, Stüve O, Rosenberg RN. A peptide prime-DNA boost immunization protocol provides significant benefits as a new generation Aβ42 DNA vaccine for Alzheimer disease. J Neuroimmunol 2013; 254:63 - 8; http://dx.doi.org/10.1016/j.jneuroim.2012.09.008; PMID: 23036592
   PubMed Web of Science ®Google Scholar
• Qu BX, Xiang Q, Li L, Johnston SA, Hynan LS, Rosenberg RN. Abeta42 gene vaccine prevents Abeta42 deposition in brain of double transgenic mice. J Neurol Sci 2007; 260:204 - 13; http://dx.doi.org/10.1016/j.jns.2007.05.012; PMID: 17574274
   PubMed Web of Science ®Google Scholar
• Subramanian S, Divya Shree AN. Enhanced Th2 immunity after DNA prime-protein boost immunization with amyloid beta (1-42) plus CpG oligodeoxynucleotides in aged rats. Neurosci Lett 2008; 436:219 - 22; http://dx.doi.org/10.1016/j.neulet.2008.03.024; PMID: 18394801
   PubMed Web of Science ®Google Scholar
• Movsesyan N, Ghochikyan A, Mkrtichyan M, Petrushina I, Davtyan H, Olkhanud PB, Head E, Biragyn A, Cribbs DH, Agadjanyan MG. Reducing AD-like pathology in 3xTg-AD mouse model by DNA epitope vaccine - a novel immunotherapeutic strategy. PLoS One 2008; 3:e2124; http://dx.doi.org/10.1371/journal.pone.0002124; PMID: 18461171
   PubMed Web of Science ®Google Scholar
• Davtyan H, Ghochikyan A, Movsesyan N, Ellefsen B, Petrushina I, Cribbs DH, Hannaman D, Evans CF, Agadjanyan MG. Delivery of a DNA vaccine for Alzheimer’s disease by electroporation versus gene gun generates potent and similar immune responses. Neurodegener Dis 2012; 10:261 - 4; http://dx.doi.org/10.1159/000333359; PMID: 22301697
   PubMed Web of Science ®Google Scholar
• Olkhanud PB, Mughal M, Ayukawa K, Malchinkhuu E, Bodogai M, Feldman N, Rothman S, Lee JH, Chigurupati S, Okun E, et al. DNA immunization with HBsAg-based particles expressing a B cell epitope of amyloid β-peptide attenuates disease progression and prolongs survival in a mouse model of Alzheimer’s disease. Vaccine 2012; 30:1650 - 8; http://dx.doi.org/10.1016/j.vaccine.2011.12.136; PMID: 22248819
   PubMed Web of Science ®Google Scholar
• Kim HD, Jin JJ, Maxwell JA, Fukuchi K. Enhancing Th2 immune responses against amyloid protein by a DNA prime-adenovirus boost regimen for Alzheimer’s disease. Immunol Lett 2007; 112:30 - 8; http://dx.doi.org/10.1016/j.imlet.2007.06.006; PMID: 17686533
   PubMed Web of Science ®Google Scholar
• Yu YZ, Wang S, Bai JY, Zhao M, Chen A, Wang WB, Chang Q, Liu S, Qiu WY, Pang XB, et al. Effective DNA epitope chimeric vaccines for Alzheimer’s disease using a toxin-derived carrier protein as a molecular adjuvant. Clin Immunol 2013; 149:11 - 24; http://dx.doi.org/10.1016/j.clim.2013.05.016; PMID: 23886550
   PubMed Web of Science ®Google Scholar
• Ghochikyan A, Davtyan H, Petrushina I, Hovakimyan A, Movsesyan N, Davtyan A, Kiyatkin A, Cribbs DH, Agadjanyan MG. Refinement of a DNA based Alzheimer’s disease epitope vaccine in rabbits. Hum Vaccin Immunother 2013; 9:1002 - 10; http://dx.doi.org/10.4161/hv.23875; PMID: 23399748
   PubMed Web of Science ®Google Scholar
• Evans CF, Davtyan H, Petrushina I, Hovakimyan A, Davtyan A, Hannaman D, Cribbs DH, Agadjanyan MG, Ghochikyan A. Epitope-based DNA vaccine for Alzheimer’s disease: Translational study in macaques. Alzheimers Dement 2013; Forthcoming http://dx.doi.org/10.1016/j.jalz.2013.04.505; PMID: 23916838
   PubMed Web of Science ®Google Scholar
• Banga AK, Prausnitz MR. Assessing the potential of skin electroporation for the delivery of protein- and gene-based drugs. Trends Biotechnol 1998; 16:408 - 12; http://dx.doi.org/10.1016/S0167-7799(98)01238-4; PMID: 9807837
   PubMed Web of Science ®Google Scholar
• Widera G, Austin M, Rabussay D, Goldbeck C, Barnett SW, Chen M, Leung L, Otten GR, Thudium K, Selby MJ, et al. Increased DNA vaccine delivery and immunogenicity by electroporation in vivo. J Immunol 2000; 164:4635 - 40; PMID: 10779767
   PubMed Web of Science ®Google Scholar
• Rizzuto G, Cappelletti M, Maione D, Savino R, Lazzaro D, Costa P, Mathiesen I, Cortese R, Ciliberto G, Laufer R, et al. Efficient and regulated erythropoietin production by naked DNA injection and muscle electroporation. Proc Natl Acad Sci U S A 1999; 96:6417 - 22; http://dx.doi.org/10.1073/pnas.96.11.6417; PMID: 10339602
   PubMed Web of Science ®Google Scholar
• Gregoriadis G, Bacon A, Caparros-Wanderley W, McCormack B. A role for liposomes in genetic vaccination. Vaccine 2002; 20:Suppl 5 B1 - 9; http://dx.doi.org/10.1016/S0264-410X(02)00514-5; PMID: 12477411
   PubMed Web of Science ®Google Scholar
• Laing P, Bacon A, McCormack B, Gregoriadis G, Frisch B, Schuber F. The ‘co-delivery’ approach to liposomal vaccines: application to the development of influenza-A and hepatitis-B vaccine candidates. J Liposome Res 2006; 16:229 - 35; http://dx.doi.org/10.1080/08982100600880432; PMID: 16952877
   PubMed Web of Science ®Google Scholar
• Espuelas S, Thumann C, Heurtault B, Schuber F, Frisch B. Influence of ligand valency on the targeting of immature human dendritic cells by mannosylated liposomes. Bioconjug Chem 2008; 19:2385 - 93; http://dx.doi.org/10.1021/bc8002524; PMID: 19053315
   PubMed Web of Science ®Google Scholar