Effective DNA epitope chimeric vaccines for Alzheimer's disease using a toxin-derived carrier protein as a molecular adjuvant

Clinical Immunology

Volumn 149, Issue 1, 2013, Pages 11-24

  Yu, Yun Zhou ^a   Wang, Shuang ^a   Bai, Jie Ying ^b   Zhao, Meng ^a,c   Chen, Ao ^a,d   Wang, Wen Bin ^a   Chang, Qing ^a   Liu, Si ^a   Qiu, Wei Yi ^a   Pang, Xiao Bin ^d   Xu, Qing ^c   Sun, Zhi Wei ^a  

^a BEIJING INSTITUTE OF BIOTECHNOLOGY   (China)

^b BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^c BEIJING JIAOTONG UNIVERSITY   (China)

^d HENAN UNIVERSITY   (China)

Author keywords

Alzheimer's disease; Carrier protein; DNA vaccine; Immunotherapy; Toxin fragment

Indexed keywords

CARRIER PROTEIN; DNA VACCINE;

ADJUVANT THERAPY; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; DRUG EFFICACY; DRUG INHIBITION; DRUG SAFETY; FEMALE; IMMUNE RESPONSE; IMMUNOTHERAPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; T LYMPHOCYTE;

ALZHEIMER'S DISEASE; CARRIER PROTEIN; DNA VACCINE; IMMUNOTHERAPY; TOXIN FRAGMENT;

ALZHEIMER DISEASE; ALZHEIMER VACCINES; AMYLOID BETA-PEPTIDES; ANIMALS; EPITOPES; FEMALE; IMMUNOGLOBULIN G; IMMUNOTHERAPY; INTERFERON-GAMMA; INTERLEUKIN-4; MALARIA VACCINES; MAZE LEARNING; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; PEPTIDE FRAGMENTS; T-LYMPHOCYTES; VACCINES, DNA;

EID: 84880585765     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2013.05.016     Document Type: Article

References (40)

1. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356.
2. Pimplikar S.W. Reassessing the amyloid cascade hypothesis of Alzheimer's disease. Int. J. Biochem. Cell Biol. 2009, 41:1261-1268.
3. Haass C., Selkoe D.J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat. Rev. Mol. Cell Biol. 2007, 8:101-112.
4. Ghochikyan A. Rationale for peptide and DNA based epitope vaccines for Alzheimer's disease immunotherapy. CNS Neurol. Disord. Drug Targets 2009, 8:128-143.
5. Lemere C.A., Masliah E. Can Alzheimer disease be prevented by amyloid-beta immunotherapy?. Nat. Rev. Neurol. 2010, 6:108-119.
6. Bayer A.J., Bullock R., Jones R.W., Wilkinson D., Paterson K.R., Jenkins L., Millais S.B., Donoghue S. Evaluation of the safety and immunogenicity of synthetic Abeta42 (AN1792) in patients with AD. Neurology 2005, 64:94-101.
7. Gilman S., Koller M., Black R.S., Jenkins L., Griffith S.G., Fox N.C., Eisner L., Kirby L., Rovira M.B., Forette F., Orgogozo J.M. Clinical effects of Abeta immunization (AN1792) in patients with AD in an interrupted trial. Neurology 2005, 64:1553-1562.
8. Delrieu J., Ousset P.J., Caillaud C., Vellas B. 'Clinical trials in Alzheimer's disease': immunotherapy approaches. J. Neurochem. 2012, 120(Suppl. 1):186-193.
9. Orgogozo J.M., Gilman S., Dartigues J.F., Laurent B., Puel M., Kirby L.C., Jouanny P., Dubois B., Eisner L., Flitman S., Michel B.F., Boada M., Frank A., Hock C. Subacute meningoencephalitis in a subset of patients with AD after Abeta42 immunization. Neurology 2003, 61:46-54.
10. Cribbs D.H., Ghochikyan A., Vasilevko V., Tran M., Petrushina I., Sadzikava N., Babikyan D., Kesslak P., Kieber-Emmons T., Cotman C.W., Agadjanyan M.G. Adjuvant-dependent modulation of Th1 and Th2 responses to immunization with beta-amyloid. Int. Immunol. 2003, 15:505-514.
11. Cribbs D.H. Abeta DNA vaccination for Alzheimer's disease: focus on disease prevention. CNS Neurol. Disord. Drug Targets 2010, 9:207-216.
12. Patton R.L., Kalback W.M., Esh C.L., Kokjohn T.A., Van Vickle G.D., Luehrs D.C., Kuo Y.M., Lopez J., Bruno D., Ferrer I., Masliah E., Newel A.J., Beach T.G., Castano E.M., Roher A.E. Amyloid-beta peptide remnants in AN-1792-immunized Alzheimer's disease patients - a biochemical analysis. Am. J. Pathol. 2006, 169:1048-1063.
13. Shah S., Federoff H.J. Therapeutic potential of vaccines for Alzheimer's disease. Immunotherapy 2011, 3:287-298.
14. Agadjanyan M.G., Ghochikyan A., Petrushina I., Vasilevko V., Movsesyan N., Mkrtichyan M., Saing T., Cribbs D.H. 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, 174:1580-1586.
15. Mamikonyan G., Necula M., Mkrtichyan M., Ghochikyan A., Petrushina I., Movsesyan N., Mina E., Kiyatkin A., Glabe C.G., Cribbs D.H., Agadjanyan M.G. Anti-A beta 1-11 antibody binds to different beta-amyloid species, inhibits fibril formation, and disaggregates preformed fibrils but not the most toxic oligomers. J. Biol. Chem. 2007, 282:22376-22386.
16. Petrushina I., Ghochikyan A., Mktrichyan M., Mamikonyan G., Movsesyan N., Davtyan H., Patel A., Head E., Cribbs D.H., Agadjanyan M.G. Alzheimer's disease peptide epitope vaccine reduces insoluble but not soluble/oligomeric Abeta species in amyloid precursor protein transgenic mice. J. Neurosci. 2007, 27:12721-12731.
17. Movsesyan N., Mkrtichyan M., Petrushina I., Ross T.M., Cribbs D.H., Agadjanyan M.G., Ghochikyan A. DNA epitope vaccine containing complement component C3d enhances anti-amyloid-beta antibody production and polarizes the immune response towards a Th2 phenotype. J. Neuroimmunol. 2008, 205:57-63.
18. Movsesyan N., Ghochikyan A., Mkrtichyan M., Petrushina I., Davtyan H., Olkhanud P.B., Head E., Biragyn A., Cribbs D.H., Agadjanyan M.G. Reducing AD-like pathology in 3×Tg-AD mouse model by DNA epitope vaccine - a novel immunotherapeutic strategy. PLoS One 2008, 3:e2124.
19. Olkhanud P.B., Mughal M., Ayukawa K., Malchinkhuu E., Bodogai M., Feldman N., Rothman S., Lee J.H., Chigurupati S., Okun E., Nagashima K., Mattson M.P., Biragyn A. DNA immunization with HBsAg-based particles expressing a B cell epitope of amyloid beta-peptide attenuates disease progression and prolongs survival in a mouse model of Alzheimer's disease. Vaccine 2012, 30:1650-1658.
20. Yu Y.Z., Li N., Zhu H.Q., Wang R.L., Du Y., Wang S., Yu W.Y., Sun Z.W. The recombinant Hc subunit of Clostridium botulinum neurotoxin serotype A is an effective botulism vaccine candidate. Vaccine 2009, 27:2816-2822.
21. Yu Y.Z., Ma Y., Chen Y.X., Gong Z.W., Wang S., Yu W.Y., Sun Z.W. Binding activity and immunogenic characterization of recombinant C-terminal quarter and half of the heavy chain of botulinum neurotoxin serotype A. Hum. Vaccine 2011, 7:1090-1095.
22. Yu Y.Z., Gong Z.W., Ma Y., Zhang S.M., Zhu H.Q., Wang W.B., Du Y., Wang S., Yu W.Y., Sun Z.W. Co-expression of tetanus toxin fragment C in Escherichia coli with thioredoxin and its evaluation as an effective subunit vaccine candidate. Vaccine 2011, 29:5978-5985.
23. Zhang J., Wu X., Qin C., Qi J., Ma S., Zhang H., Kong Q., Chen D., Ba D., He W. A novel recombinant adeno-associated virus vaccine reduces behavioral impairment and beta-amyloid plaques in a mouse model of Alzheimer's disease. Neurobiol. Dis. 2003, 14:365-379.
24. Wiessner C., Wiederhold K.H., Tissot A.C., Frey P., Danner S., Jacobson L.H., Jennings G.T., Luond R., Ortmann R., Reichwald J., Zurini M., Mir A., Bachmann M.F., Staufenbiel M. The second-generation active Abeta immunotherapy CAD106 reduces amyloid accumulation in APP transgenic mice while minimizing potential side effects. J. Neurosci. 2011, 31:9323-9331.
25. Barghorn S., Nimmrich V., Striebinger A., Krantz C., Keller P., Janson B., Bahr M., Schmidt M., Bitner R.S., Harlan J., Barlow E., Ebert U., Hillen H. Globular amyloid beta-peptide oligomer - a homogenous and stable neuropathological protein in Alzheimer's disease. J. Neurochem. 2005, 95:834-847.
26. Hoogerhout P., Kamphuis W., Brugghe H.F., Sluijs J.A., Timmermans H.A., Westdijk J., Zomer G., Boog C.J., Hol E.M., van den Dobbelsteen G.P. A cyclic undecamer peptide mimics a turn in folded Alzheimer amyloid beta and elicits antibodies against oligomeric and fibrillar amyloid and plaques. PLoS One 2011, 6:e19110.
27. Simpson L.L., Maksymowych A.B., Kiyatkin N. Botulinum toxin as a carrier for oral vaccines. Cell Mol. Life Sci. 1999, 56:47-61.
28. Diethelm-Okita B.M., Okita D.K., Banaszak L., Conti-Fine B.M. Universal epitopes for human CD4+ cells on tetanus and diphtheria toxins. J. Infect. Dis. 2000, 181:1001-1009.
29. Baraldo K., Mori E., Bartoloni A., Petracca R., Giannozzi A., Norelli F., Rappuoli R., Grandi G., Del Giudice G. N19 polyepitope as a carrier for enhanced immunogenicity and protective efficacy of meningococcal conjugate vaccines. Infect. Immun. 2004, 72:4884-4887.
30. King C.A., Spellerberg M.B., Zhu D., Rice J., Sahota S.S., Thompsett A.R., Hamblin T.J., Radl J., Stevenson F.K. DNA vaccines with single-chain Fv fused to fragment C of tetanus toxin induce protective immunity against lymphoma and myeloma. Nat. Med. 1998, 4:1281-1286.
31. Yu Y.Z., Zhang S.M., Sun Z.W., Wang S., Yu W.Y. Enhanced immune responses using plasmid DNA replicon vaccine encoding the Hc domain of Clostridium botulinum neurotoxin serotype A. Vaccine 2007, 25:8843-8850.
32. Wisniewski T., Boutajangout A. Vaccination as a therapeutic approach to Alzheimer's disease, Mt. Sinai. J. Med. 2010, 77:17-31.
33. Venkitaramani D.V., Chin J., Netzer W.J., Gouras G.K., Lesne S., Malinow R., Lombroso P.J. Beta-amyloid modulation of synaptic transmission and plasticity. J. Neurosci. 2007, 27:11832-11837.
34. Selkoe D.J. Soluble oligomers of the amyloid beta-protein impair synaptic plasticity and behavior. Behav. Brain Res. 2008, 192:106-113.
35. Ghochikyan A., Vasilevko V., Petrushina I., Movsesyan N., Babikyan D., Tian W., Sadzikava N., Ross T., Head E., Cribbs D.H., Agadjanyan M.G. Generation and characterization of the humoral immune response to DNA immunization with a chimeric β-amyloid-interleukin-4 minigene. Eur. J. Immunol. 2003, 33:3232-3241.
36. Movsesyan N., Davtyan H., Mkrtichyan M., Petrushina I., Tiraturyan T., Ross T., Agadjanyan M.G., Ghochikyan A., Cribbs D.H. Low concentrations of anti-Ab antibodies generated in Tg2576 mice by DNA epitope vaccine fused with 3C3d molecular adjuvant do not affect AD pathology. Hum. Gene Ther. 2010, 21:1569-1576.
37. Chen G.Q., Chen K.S., Kobayashi D., Barbour R., Motter R., Games D., Martin S.J., Morris R.G.M. Active beta-amyloid immunization restores spatial learning in PDAPP mice displaying very low levels of beta-amyloid. J. Neurosci. 2007, 27:2654-2662.
38. Savelyeva N., King C.A., Vitetta E.S., Stevenson F.K. Inhibition of a vaccine-induced anti-tumor B cell response by soluble protein antigen in the absence of continuing T cell help. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:10987-10992.
39. Keitel W.A., Kester K.E., Atmar R.L., White A.C., Bond N.H., Holland C.A., Krzych U., Palmer D.R., Egan A., Diggs C., Ballou W.R., Hall B.F., Kaslow D. Phase I trial of two recombinant vaccines containing the 19kd carboxy terminal fragment of Plasmodium falciparum merozoite surface protein 1 (msp-1(19)) and T helper epitopes of tetanus toxoid. Vaccine 1999, 18:531-539.
40. Monsonego A., Maron R., Zota V., Selkoe D.J., Weiner H.L. Immune hyporesponsiveness to amyloid beta-peptide in amyloid precursor protein transgenic mice: implications for the pathogenesis and treatment of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:10273-10278.