Experimental investigation of antibody-mediated clearance mechanisms of amyloid-β in CNS of Tg-SwDI transgenic mice

Journal of Neuroscience

Volumn 27, Issue 49, 2007, Pages 13376-13383

  Vasilevko, Vitaly ^a   Xu, Feng ^c   Previti, Mary Lou ^c   Van Nostrand, William E ^c   Cribbs, David H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STONY BROOK UNIVERSITY   (United States)

Author keywords

amyloid; Alzheimer's disease; Blood brain barrier; Epitope vaccine; Immunotherapy; Peripheral sink; Transgenic animal model

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN D1; ANTIBODY; UNCLASSIFIED DRUG;

ARTICLE; BLOOD BRAIN BARRIER; BRAIN REGION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; IMMUNIZATION; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL;

AMYLOID BETA-PROTEIN; ANIMALS; ANTIBODIES; BLOOD-BRAIN BARRIER; CENTRAL NERVOUS SYSTEM; IMMUNOTHERAPY; METABOLIC CLEARANCE RATE; MICE; MICE, TRANSGENIC;

EID: 37149008108     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2788-07.2007     Document Type: Article

References (46)

1. Agadjanyan MG, Ghochikyan A, Petrushina I, Vasilevko V, Movsesyan N, Mkrtichyan M, Saing T, Cribbs DH (2005) 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 174:1580-1586.
2. Austin L, Arendash GW, Gordon MN, Diamond DM, DiCarlo G, Dickey C, Ugen K, Morgan D (2003) Short-term beta-amyloid vaccinations do not improve cognitive performance in cognitively impaired APP + PS1 mice. Behav Neurosci 117:478-484.
3. Bacskai BJ, Kajdasz ST, Christie RH, Carter C, Games D, Seubert P, Schenk D, Hyman BT (2001) Imaging of amyloid-beta deposits in brains of living mice permits direct observation of clearance of plaques with immunotherapy. Nat Med 7:369-372.
4. Bacskai BJ, Kajdasz ST, McLellan ME, Games D, Seubert P, Schenk D, Hyman BTN (2002) Non-Fc-mediated mechanisms are involved in clearance of amyloid-β in vivo by immunotherapy. J Neurosci 22:7873-7878.
5. Bard F, Cannon C, Barbour R, Burke RL, 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, et al. (2000) Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat Med 6:916-919.
6. Caccamo A, Oddo S, Sugarman MC, Akbari Y, LaFerla FM (2005) Age- and region-dependent alterations in Abeta-degrading enzymes: implications for Abeta-induced disorders. Neurobiol Aging 26:645-654.
7. Cribbs DH, Ghochikyan A, Tran M, Vasilevko V, Petrushina I, Sadzikava N, Kesslak P, Kieber-Emmons T, Cotman CW, Agadjanyan MG (2003) Adjuvant-dependent modulation of Th1 and Th2 responses to immunization with beta-amyloid. Int Immunol 15:505-514.
8. Das P, Murphy MP, Younkin LH, Younkin SG, Golde TE (2001) Reduced effectiveness of Abeta1-42 immunization in APP transgenic mice with significant amyloid deposition. Neurobiol Aging 22:721-727.
9. Davis J, Xu F, Deane R, Romanov G, Previti ML, Zeigler K, Zlokovic BV, Van Nostrand WE (2004) Early-onset and robust cerebral microvascular accumulation of amyloid beta-protein in transgenic mice expressing low levels of a vasculotropic Dutch/Iowa mutant form of amyloid beta-protein precursor. J Biol Chem 279:20296-20306.
10. Davis J, Xu F, Miao J, Previti ML, Romanov G, Ziegler K, Van Nostrand WE (2006) Deficient cerebral clearance of vasculotropic mutant Dutch/Iowa Double A beta in human A betaPP transgenic mice. Neurobiol Aging 27:946-954.
11. Deane R, Du Yan S, Submamaryan RK, LaRue B, Jovanovic S, Hogg E, Welch D, Manness L, Lin C, Yu J, Zhu H, Ghiso J, Frangione B, Stern A, Schmidt AM, Armstrong DL, Arnold B, Liliensiek B, Nawroth P, Hofman F, et al. (2003) RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain. Nat Med 9:907-913.
12. Deane R, Wu Z, Sagare A, Davis J, Du Yan S, Hamm K, Xu F, Parisi M, LaRue B, Hu HW, Spijkers P, Guo H, Song X, Lenting PJ, Van Nostrand WE, Zlokovic BV (2004) LRP/amyloid beta-peptide interaction mediates differential brain efflux of Abeta isoforms. Neuron 43:333-344.
13. Deane R, Sagare A, Hamm K, Parisi M, LaRue B, Guo H, Wu Z, Holtzman DM, Zlokovic BV (2005) IgG-assisted age-dependent clearance of Alzheimer's amyloid β peptide by the blood-brain barrier neonatal Fc receptor. J Neurosci 25:11495-11503.
14. Delmastro P, Meola A, Monaci P, Cortese R, Galfre G (1997) Immunogenicity of filamentous phage displaying peptide mimotopes after oral administration. Vaccine 15:1276-1285.
15. DeMattos RB, Bales KR, Cummins DJ, Dodart JC, Paul SM, Holtzman DM (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 USA 98:8850-8855.
16. DeMattos RB, Bales KR, Cummins DJ, Paul SM, Holtzman DM (2002a) Brain to plasma amyloid-beta efflux: a measure of brain amyloid burden in a mouse model of Alzheimer's disease. Science 295:2264-2267.
17. DeMattos RB, Bales KR, Parsadanian M, O'Dell MA, Foss EM, Paul SM, Holtzman DM (2002b) Plaque-associated disruption of CSF and plasma amyloid-b (Ab) equlibrium in a mouse model of Alzheimer's disease. J Neurochem 81:229-236.
18. Ferrer I, Rovira MB, Guerra MLS, Rey MJ, Costa-Jussa F (2004) Neuropathology and pathogenesis of encephalitis following amyloid-beta immunization in Alzheimer's disease. Brain Pathol 14:11-20.
19. Frenkel D, Balass M, Katchalski-Katzir E, Solomon B (1999) High affinity binding of monoclonal antibodies to the sequential epitope EFRH of beta-amyloid peptide is essential for modulation of fibrillar aggregation. J Neuroimmunol 95:136-142.
20. Holtzman DM, Bales KR, Paul SM, DeMattos RB (2002) Abeta immunization and anti-Abeta antibodies: potential therapies for the prevention and treatment of Alzheimer's disease. Adv Drug Deliv Rev 54:1603-1613.
21. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 274:99-102.
22. Johnson-Wood K, Lee M, Motter R, Hu K, Gordon G, Barbour R, Khan K, Gordon M, Tan H, Games D, Lieberburg I, Schenk D, Seubert P, McConlogue L (1997) Amyloid precursor protein processing and A beta42 deposition in a transgenic mouse model of Alzheimer disease. Proc Natl Acad Sci USA 94:1550-1555.
23. Kalback W, Esh C, Castano EM, Rahman A, Kokjohn T, Luehrs DC, Sue L, Cisneros R, Gerber F, Richardson C, Bohrmann B, Walker DG, Beach TG, Roher AE (2004) Atherosclerosis, vascular amyloidosis and brain hypoperfusion in the pathogenesis of sporadic Alzheimer's disease. Neurol Res 26:525-539.
24. Lemere C, Spooner ET, LaFrancois J, Malester B, Mori C, Leverone JF, Matsuoka Y, Taylor JW, DeMattos RB, Holtzman DM, Clements JD, Selkoe DJ, Duff K (2003) Evidence for peripheral clearance of cerebral Abeta protein following chronic, active Abeta immunization in PSAPP mice. Neurobiol Dis 14:10-18.
25. Levites Y, Smithson LA, Price RW, Dakin RS, Yuan B, Sierks MR, Kim J, McGowan E, Reed DK, Rosenberry TL, Das P, Golde TE (2006) Insights into the mechanisms of action of anti-Abeta antibodies in Alzheimer's disease mouse models. FASEB J 20:2576-2578.
26. Maggio JE, Stimson ER, Ghilardi JR, Allen CJ, Dahl CE, Whitcomb DC, Vigna SR, Vinters HV, Labenski ME, Mantyh PW (1992) Reversible in vitro growth of Alzheimer disease beta-amyloid plaques by deposition of labeled amyloid peptide. Proc Natl Acad Sci USA 89:5462-5466.
27. Masliah E, Hansen L, Adame A, Crews L, Bard F, Lee C, Seubert P, Games D, Kirby L, Schenk D (2005) Abeta vaccination effects on plaque pathology in the absence of encephalitis in Alzheimer disease. Neurology 64:129-131.
28. McLaurin J, Cecal R, Kierstead ME, Tian X, Phinney AL, Manea M, French JE, Lambermon MH, Darabie AA, Brown ME, Janus C, Chishti MA, Horne P, Westaway D, Fraser PE, Mount HT, 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.
29. Miao J, Xu F, Davis J, Otte-Holler I, Verbeek MM, Van Nostrand WE (2005) Cerebral microvascular amyloid beta protein deposition induces vascular degeneration and neuroinflammation in transgenic mice expressing human vasculotropic mutant amyloid beta precursor protein. Am J Pathol 167:505-515.
30. Nicoll JA, Wilkinson D, Holmes C, Steart P, Markham H, Weller RO (2003) Neuropathology of human Alzheimer disease after immunization with amyloid-beta peptide: a case report. Nat Med 9:448-452.
31. Oddo S, Billings L, Kesslak JP, Cribbs DH, LaFerla FM (2004) Abeta immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome. Neuron 43:321-332.
32. Oddo S, Caccamo A, Smith IF, Green KN, LaFerla FM (2006) A dynamic relationship between intracellular and extracellular pools of Abeta. Am J Pathol 168:184-194.
33. Roher AE, Kuo YM, Esh C, Knebel C, Weiss N, Kalback W, Luehrs DC, Childress JL, Beach TG, Weller RO, Kokjohn TA (2003) Cortical and leptomeningeal cerebrovascular amyloid and white matter pathology in Alzheimer's disease. Mol Med 9:112-122.
34. 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, et al. (1999) Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 400:173-177.
35. Schenk D, Hagen M, Seubert P (2004) Current progress in beta-amyloid immunotherapy. Curr Opin Immunol 16:599-606.
36. Shibata M, Yamada S, Kumar SR, Calero M, Bading J, Frangione B, Holtzman DM, Miller CA, Strickland DK, Ghiso J, Zlokovic BV (2000) Clearance of Alzheimer's amyloid-ss(1-40) peptide from brain by LDL receptor-related protein-1 at the blood-brain barrier. J Clin Invest 106:1489-1499.
37. Shinall H, Song ES, Hersh LB (2005) Susceptibility of amyloid beta peptide degrading enzymes to oxidative damage: a potential Alzheimer's disease spiral. Biochemistry 44:15345-15350.
38. Sigurdsson EM, Knudsen E, Asuni A, Fitzer-Attas C, Sage D, Quartermain D, Goni F, Frangione B, Wisniewski T (2004) An attenuated immune response is sufficient to enhance cognition in an Alzheimer's disease mouse model immunized with amyloid-β derivatives. J Neurosci 24:6277-6282.
39. Solomon B, Koppel R, Hanan E, Katzav T (1996) Monoclonal antibodies inhibit in vitro fibrillar aggregation of the Alzheimer beta-amyloid peptide. Proc Natl Acad Sci USA 93:452-455.
40. Solomon B, Koppel R, Frankel D, Hanan-Aharon E (1997) Disaggregation of Alzheimer beta-amyloid by site-directed mAb. Proc Natl Acad Sci USA 94:4109-4112.
41. Thomas CE, Schiedner G, Kochanek S, Castro MG, Lowenstein PR (2001) Preexisting antiadenoviral immunity is not a barrier to efficient and stable transduction of the brain, mediated by novel high-capacity adenovirus vectors. Hum Gene Ther 12:839-846.
42. Tseng BP, Esler WP, Clish CB, Stimson ER, Ghilardi JR, Vinters HV, Mantyh PW, Lee JP, Maggio JE (1999) Deposition of monomeric, not oligomeric, Abeta mediates growth of Alzheimer's disease amyloid plaques in human brain preparations. Biochemistry 38:10424-10431.
43. Vasilevko V, Cribbs DH (2006) Novel approaches for immunotherapeutic intervention in Alzheimer's disease. Neurochem Int 49:113-126.
44. Wang DS, Lipton RB, Katz MJ, Davies P, Buschke H, Kuslansky G, Verghese J, Younkin SG, Eckman C, Dickson DW (2005) Decreased neprilysin immunoreactivity in Alzheimer disease, but not in pathological aging. J Neuropathol Exp Neurol 64:378-385.
45. Wilcock DM, DiCarlo G, Henderson D, Jackson J, Clarke K, Ugen KE, Gordon MN, Morgan D (2003) Intracranially administered anti-Aβ antibodies reduce β-amyloid deposition by mechanisms both independent of and associated with microglial activation. J Neurosci 23:3745-3751.
46. Zhou J, Fonseca MI, Kayed R, Hernandez I, Webster SD, Yazan O, Cribbs DH, Glabe CG, Tenner AJ (2005) Novel Abeta peptide immunogens modulate plaque pathology and inflammation in a murine model of Alzheimer's disease. J Neuroinflammation 2:28.