Active immunotherapy facilitates Aβ plaque removal following through microglial activation without obvious T cells infiltrating the CNS

Journal of Neuroimmunology

Volumn 274, Issue 1-2, 2014, Pages 62-70

  Sha, Sha ^a   Xing, Xiao Na ^b   Cao, Yun Peng ^c  

^a CHINA MEDICAL UNIVERSITY   (China)

^b Canton People's Provincial Hospital   (China)

^c First Affiliated Hospital of China Medical University   (China)

Author keywords

Alzheimer's disease; Amyloid protein; Microglial; T cell infiltration

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN ANTIBODY; AMYLOID BETA PROTEIN[1-42]; AMYLOID BETA PROTEIN[3-10]; DNA VACCINE; FREUND ADJUVANT; MELATONIN; UNCLASSIFIED DRUG;

ACTIVE IMMUNIZATION; ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL CELL; ANIMAL MODEL; ANTIBODY TITER; ARTICLE; BLOOD SAMPLING; BRAIN HEMORRHAGE; CELL ACTIVATION; CENTRAL NERVOUS SYSTEM; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ELECTROPORATION; ENCEPHALITIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FRONTAL CORTEX; HIPPOCAMPUS; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; IMMUNOGENICITY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LYMPHOCYTIC INFILTRATION; MICROGLIA; MOUSE; NONHUMAN; PHAGOCYTOSIS; PLASMID; PRIORITY JOURNAL; T LYMPHOCYTE; TANDEM REPEAT;

ALZHEIMER'S DISEASE; AMYLOID Β-PROTEIN; MICROGLIAL; T CELL INFILTRATION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; CENTRAL NERVOUS SYSTEM; CEREBRAL HEMORRHAGE; DISEASE MODELS, ANIMAL; ENCEPHALITIS; IMMUNOTHERAPY, ACTIVE; MICE; MICE, TRANSGENIC; MICROGLIA; PEPTIDE FRAGMENTS; PLAQUE, AMYLOID; RANDOM ALLOCATION; T-LYMPHOCYTES; VACCINES, DNA;

EID: 84906938689     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2014.06.008     Document Type: Article

References (39)

1. Akiyama H., Barger S., Barnum S., Bradt B., Bauer J., Cole G.M., Cooper N.R., Eikelenboom P., Emmerling M., Fiebich B.L., Finch C.E., Frautschy S., Griffin W.S., Hampel H., Hull M., Landreth G., Lue L., Mrak R., Mackenzie I.R., McGeer P.L., O'Banion M.K., Pachter J., Pasinetti G., Plata-Salaman C., Rogers J., Rydel R., Shen Y., Streit W., Strohmeyer R., Tooyoma I., Van Muiswinkel F.L., Veerhuis R., Walker D., Webster S., Wegrzyniak B., Wenk G., Wyss-Coray T. Inflammation and Alzheimer's disease. Neurobiol. Aging 2000, 21:383-421.
2. 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., Yednock T. Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat. Med. 2000, 6:916-919.
3. Bard F., Barbour R., Cannon C., Carretto R., Fox M., Games D., Guido T., Hoenow K., Hu K., Johnson-Wood K., Khan K., Kholodenko D., Lee C., Lee M., Motter R., Nguyen M., Reed A., Schenk D., Tang P., Vasquez N., Seubert P., Yednock T. Epitope and isotype specificities of antibodies to beta-amyloid peptide for protection against Alzheimer's disease-like neuropathology. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:2023-2028.
4. Cribbs D.H. Abeta DNA Vaccination for Alzheimer's Disease: Focus on Disease õPrevention. CNS Neurol. Disord. Drug Targets 2010, 9:207-216.
5. 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.
6. Dahlgren K.N., Manelli A.M., Stine W.B., Baker L.K., Krafft G.A., LaDu M.J. Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J. Biol. Chem. 2002, 277:32046-32053.
7. Das P., Murphy M.P., Younkin L.H., Younkin S.G., Golde T.E. Reduced effectiveness of Aβ1-42 immunization in APP transgenic mice with significant amyloid deposition. Neurobiol. Aging 2001, 22:721-727.
8. DeMattos R.B., Bales K.R., Cummins D.J., Dodart J.C., Paul S.M., Holtzman D.M. Peripheral anti-Aβ antibody alters CNS and plasma Aβ clearance and decreases brain Aβ burden in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:8850-8855.
9. Eikelenboom P., Veerhuis R. The role of complement and activated microglia in the pathogenesis of Alzheimer's disease. Neurobiol. Aging 1996, 17:673-680.
10. Fukuchi K., Pham D., Hart M., Li L., Lindsey J.R. Amyloid-beta deposition in skeletal muscle of transgenic mice: possible model of inclusion body myopathy. Am. J. Pathol. 1998, 153:1687-1693.
11. Ghochikyan A., Petrushina I., Lees A., Vasilevko V., Movsesyan N., Karapetyan A., Agadjanyan M.G., Cribbs D.H. Aβ-immunotherapy for Alzheimer's disease using mannan-amyloid-beta peptide immunoconjugates. DNA Cell Biol. 2006, 25:571-580.
12. Gilman S., Koller M., Black R.S., Jenkins L., Griffith S.G., Fox N.C., Eisner L., Kirby L., Rovira M., Boada, Forette F., Orgogozo J.M. Clinical effects of Abeta immunization (AN1792) in patients with AD in an interrupted trial. Neurology 2005, 64:1553-1562. AN1792(QS-21)-201 Study Team.
13. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress on the road to therapeutics. Science 2002, 297:353-356.
14. Harigaya Y., Saido T.C., Eckman C.B., Prada C.M., Shoji M., Younkin S.G. Amyloid beta protein starting pyroglutamate at position 3 is a major component of the amyloid deposits in the Alzheimers disease brain. Biochem. Biophys. Res. Commun. 2000, 276:422-427.
15. Hellstrand K., Hermodsson S. Monocyte-mediated suppression of IL-2-induced NK-cell activation: regulation by 5-HT1-type serotonin receptors. Scand. J. Immunol. 1990, 32:183-192.
16. Hock C., Konietzko U., Streffer J.R., Tracy J., Signorell A., Müller-Tillmanns B., Lemke U., Henke K., Moritz E., Garcia E., Wollmer M.A., Umbricht D., deQuervain D.J., Hofmann M., Maddalena A., Papassotiropoulos A., Nitsch R.M. Antibodies against beta-amyloid slow cognitive decline in Alzheimer's disease. Neuron 2003, 38:547-554.
17. Janus C., Pearson J., McLaurin J., Mathews P.M., Jiang Y., Schmidt S.D., Chishti M.A., Horne P., Heslin D., French J., Mount H.T., Nixon R.A., Mercken M., Bergeron C., Fraser P.E., StGeorge-Hyslop P., Westaway D. A beta peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature 2000, 408:979-982.
18. Lee E.B., Leng L.Z., Lee V.M., Trojanowski J.Q. Meningoencephalitis associated with passive immunization of a transgenic murine model of Alzheimer's amyloidosis. FEBS Lett. 2005, 579:2564-2568.
19. Lee E.B., Leng L.Z., Zhang B., Kwong L., Trojanowski J.Q., Abel T., Lee V.M. Targeting amyloid-beta peptide (Abeta) oligomers by passive immunization with a conformation selective monoclonal antibody improves learning and memory in Abeta precursor protein (APP) transgenic mice. J. Biol. Chem. 2006, 281:4292-4299.
20. Mamikonyan G., Necula M., Mkrtichyan M., Ghochikyan A., Petrushina I., Movsesyan N., Mina E., Kiyatkin A., Glabe C.G., Cribbs D.H. Agadjanyan Michael 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.
21. McLaurin J., Cecal R., Kierstead M.E., Tian X., Phinney A.L., Manea M., French J.E., Lambermon M.H.L., Darabie A.A., Brown M.E., Janus C., Chishti M.A., Horne P., Westaway D., Fraser P.E., Mount H.T.J., Przybylski M., St.George-Hyslop P, 2002, Therapeutically effective antibodies against amyloid-beta peptide target amyloid-beta residues 4-10 and inhibit cytotoxicity and fibrillogenesis. Nat. Med. 8:1263-1269.
22. 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.
23. Morgan D., Diamond D.M., Gottschall P.E., Ugen K.E., Dickey C., Hardy J., Duff K., Jantzen P., DiCarlo G., Wilcock D., Connor K., Hatcher J., Hope C., Gordon M., Arendash G.W. A beta peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 2000, 408:982-985.
24. 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 3xTg-AD Mouse Model by DNA Epitope Vaccine- a Novel Immunotherapeutic Strategy. PLoS ONE 2008, 3:e2124.
25. 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-β antibody production and polarizes the immune response towards a Th2 phenotype. J. Neuroimmunol. 2008, 205:57-63.
26. 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.
27. Otten G., Schaefer M., Doe B., Liu H., Srivastava I., zur Megede J., O'Hagan D., Donnelly J., Widera G., Rabussay D., Lewis M.G., Barnett S., Ulmer J.B. Enhancement of DNA vaccine potency in rhesus macaques by electroporation. Vaccine 2004, 22:2489-2493.
28. Petrushina I., Ghochikyan A., Mkrichyan M., Mamikonyan G., Movsesyan N., Ajdari R., Vasilevko V., Karapetyan A., Lees A., Agadjanyan M.G., Cribbs D.H. Mannan-Abeta28 conjugate prevents Abeta-plaque deposition, but increases microhemorrhages in the brains of vaccinated Tg2576(APPsw) mice. J. Neuroinflammation 2008, 5:42.
29. Rabinovic G.D., Jagust W.J. Amyloid imaging in aging and dementia: testing the amyloid hypothesis in vivo. Behav. Neurol. 2009, 21:117-128.
30. Reiter R.J., Cabrera J., Sainz R.M., Mayo J.C., Manchester L.C., Tan D.X. Melatonin as a pharmacyological agent against neuronal loss in experimental models of Huntington's disease, Alzheimer's disease and parkinsonism. Ann. N. Y. Acad. Sci. 1999, 890:471-485.
31. Rinne J.O., Brooks D.J., Rossor M.N., Fox N.C., Bullock R., Klunk W.E., Mathis C.A., Blennow K., Barakos J., Okello A.A., Martinez Rodriguez, de Liano S., Liu E., Koller M., Gregg K.M., Schenk D., Black R., Grundman M. 11C-PiB PET assessment of change in fibrillar amyloid-β load in patients with Alzheimer's disease treated with bapineuzumab: a phase 2, double-blind, placebo-controlled, ascending-dose study. Lancet Neurol. 2010, 9:363-372.
32. Schenk D., Barbour R., Dunn W., Gordon G., Grajeda H., Guido T., Hu K., Huang J., Johnson-Wood K., Khan K., Kholodenko D., Lee M., Liao Z., Lieberburg I., Motter R., Mutter L., Soriano F., Shopp G., Vasquez N., Vandevert C., Walker S., Wogulis M., Yednock T., Games D., Seubert P. Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 1999, 400:173-177.
33. Schroeter S., Khan K., Barbour R., Doan M., Chen M., Guido T., Gill D., Basi G., Schenk D., Seubert P., Games D. Immunotherapy reduces vascular amyloid-beta in PDAPP mice. J. Neurosci. 2008, 28:6787-6793.
34. Sha S., Xing X.N., Guo W.S., Li Y., Zong L.X., Guo R., Cao Y.P. In vivo electroporation of a new gene vaccine encoding ten repeats of Aβ3-10 prevents brain Aβ deposition and delays cognitive impairment in young Tg-APPswe/PSEN1dE9 mice. Neurochem. Res. 2012, 1534-1544.
35. Solomon B., Koppel R., Frenkel D., Hanan-Aharon E. Disaggregation of Alzheimer beta-amyloid by site-directed monoclonal antibodies. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:4109-4112.
36. Thakker D.R., Weatherspoon M.R., Harrison J., Keene T.E., Lane D.S., Kaemmerer W.F., Stewart G.R., Shafer L.L. Intracerebroventricular amyloid-β antibodies reduce cerebral amyloid angiopathy and associated micro-hemorrhages in aged Tg2576 mice. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:4501-4506.
37. Wilcock D.M., Rojiani A., Rosenthal A., Levkowitz G., Subbarao S., Alamed J., Wilson D., Wilson N., Freeman M.J., Gordon M.N., Morgan D. Passive amyloid immunotherapy clears amyloid and transiently activates microglia in a transgenic mouse model of amyloid deposition. J. Neurosci. 2004, 24:6144-6151.
38. Wilcock D.M., Jantzen P.T., Li Q., Morgan D., Gordon M.N. Amyloid-beta vaccination, but not nitro-NSAID treatment, increases vascular amyloid and microhemorrhage while both reduce parenchymal amyloid. Neuroscience 2007, 144:950-960.
39. Xie Z., Wei M., Morgan T.E., Fabrizio P., Han D., Finch C.E., Longo V.D. Peroxynitrite mediates neurotoxicity of amyloid beta-peptide Aβ42 and lipopolysaccharide-activated microglia. J. Neurosci. 2002, 22:3484-3492.