Exacerbation of cerebral amyloid angiopathy-associated microhemorrhage in amyloid precursor protein transgenic mice by immunotherapy is dependent on antibody recognition of deposited forms of amyloid β

Journal of Neuroscience

Volumn 25, Issue 3, 2005, Pages 629-636

  Racke, Margaret M ^a   Boone, Laura I ^a   Hepburn, Deena L ^a   Parsadainian, Maia ^a   Bryan, Matthew T ^a   Ness, Daniel K ^a   Piroozi, Kathy S ^a   Jordan, William H ^a   Brown, Donna D ^a   Hoffman, Wherly P ^a   Holtzman, David M ^b   Bales, Kelly R ^a   Gitter, Bruce D ^a   May, Patrick C ^a   Paul, Steven M ^a   DeMattos, Ronald B ^a,c  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ELI LILLY AND COMPANY   (United States)

Author keywords

Alzheimer's disease; Amyloid; CAA; Immunotherapy; Microhemorrhage; Transgenic

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; PROTEIN ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; BINDING AFFINITY; BRAIN; CHEMICAL ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE EXACERBATION; DISEASE SEVERITY; IMMUNOTHERAPY; IN VITRO STUDY; IN VIVO STUDY; INCIDENCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; VASCULAR AMYLOIDOSIS;

AGING; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANTIBODY AFFINITY; CEREBRAL AMYLOID ANGIOPATHY; CEREBRAL HEMORRHAGE; FEMALE; IMMUNIZATION, PASSIVE; MALE; MICE; MICE, TRANSGENIC;

EID: 19944431509     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4337-04.2005     Document Type: Article

References (45)

1. Alonzo NC, Hyman BT, Rebeck GW, Greenberg SM (1998) Progression of cerebral amyloid angiopathy: accumulation of amyloid-beta40 in affected vessels. J Neuropathol Exp Neurol 57:353-359.
2. Anders KH, Wang ZZ, Kornfeld M, Gray F, Soontornniyomkij V, Reed LA, Hart MN, Menchine M, Secor DL, Vinters HV (1997) Giant cell arteritis in association with cerebral amyloid angiopathy: immunohistochemical and molecular studies. Hum Pathol 28:1237-1246.
3. Backsai BJ, Kajdasz ST, Christie RH, Carter C, Games D, Seubert P, Schenk D, Hyman BT (2001) Imaging of amyloid-β deposits in brains of living mice permits direct observation of clearance of plaques with immunotherapy. Nat Med 7:369-372.
4. 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 β-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer's disease. Nat Med 6:916-919.
5. Bard F, Barbour R, Cannon C, Carretto R, Fox M, Games D, Guido T, Hoenow K, Hu K, Johnson-Wood KL, Khan K, Kholodenko D, Lee M, Motter R, Nguyen M, Reed A, Schenk D, Tang P, Vasquez N, Seubert P, et al. (2003) Epitope and isotype specificities of antibodies to β-amyloid peptide for protection against Alzheimer's disease-like neuropathology. Proc Natl Acad Sci USA 100:2023-2028.
6. Calhoun ME, Burgermeister P, Phinney AL, Stalder M, Tolnay M, Wiederhold K-H, Abramowski D, Sturchler-Pierrat C, Sommer B, Staufenbiel M, Jucker M (1999) Neuronal overexpression of mutant amyloid precursor protein results in prominent deposition of cerebrovascular amyloid. Proc Natl Acad Sci USA 96:14088-14093.
7. DeMattos RB, Bales KR, Cummins DJ, Dodart J-C, Paul SM, Holtzman DM (2001) 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 USA 98:8850-8855.
8. DeMattos RB, Bales K, 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.
9. DeMattos RB, O'Dell MA, Parsadanian M, Taylor JW, Harmony JA, Bales KR, Paul SM, Aronow BJ, Holtzman DM (2002b) Clusterin promotes amyloid plaque formation and is critical for neuritic toxicity in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 99:10843-10848.
10. Dunnett CW (1964) New tables for multiple comparisons with a control. Biometrics 20:482-491.
11. Eng JA, Frosch MP, Choi K, Rebeck GW, Greenberg SM (2004) Clinical manifestations of cerebral amyloid angiopathy-related inflammation. Ann Neurol 55:250-256.
12. Ferrer I, Boada Rovira M, Sanchez Guerra ML, Rey MJ, Costa-Jussa F (2004) Neuropathology and pathogenesis of encephalitis following amyloid-beta immunization in Alzheimer's disease. Brain Pathol 14:11-20.
13. Frackowiak J, Zoltowska A, Wisniewski HM (1994) Non-fibrillar beta-amyloid protein is associated with smooth muscle cells of vessel walls in Alzheimer disease. J Neuropathol Exp Neurol 53:637-645.
14. Fryer JD, Taylor JW, DeMattos RB, Bales KR, Paul SM, Parsadanian M, Holtzman DM (2003) Apolipoprotein E markedly facilitates age-dependent cerebral amyloid angiopathy and spontaneous hemorrhage in amyloid precursor protein transgenic mice. J Neurosci 23:7889-7896.
15. Games D, Adams D, Alessandrini R, Barbour R, Berthelette P, Blackwell C, Carr T, Clemens J, Donaldson T, Gillespie F, Guido T, Hagopian S, Johnson-Wood K, Khan K, Lee M, Leibowitz P, Lieberburg I, Little S, Masliah E, McConlogue L, et al. (1995) Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature 373:523-527.
16. Grammas P, Ovase R (2001) Inflammatory factors are elevated in brain microvessels in Alzheimer's disease. Neurobiol Aging 22:837-842.
17. Hock C, Konietzko U, Papassotiropoulos A, Wollmer MA, Streffer J, von Rotz RC, Davey G, Moritz E, Nitsch RM (2002) Generation of antibodies specific for β-amyloid by vaccination of patients with Alzheimer's disease. Nat Med 8:1270-1275.
18. Hock C, Konietzko U, Streffer JR, Tracy J, Signorell A, Muller-Tillmanns B, Lemke U, Henke K, Moritz E, Garcia E, Wollmer MA, Umbricht D, deq Uervain DJ, Hofmann M, Maddalena A, Papassotiropoulos A, Nitsch RM (2003) Antibodies against beta-amyloid slow cognitive decline in Alzheimer's disease. Neuron 38:547-554.
19. Holtzman DM, Bales KR, Wu S, Bhat P, Parsadanian M, Fagan AM, Chang LK, Sun Y, Paul SM (1999) In vivo expression of apolipoprotein E reduces amyloid-β deposition in a mouse model of Alzheimers disease. J Clin Invest 103:R15-R21.
20. Holtzman DM, Fagan AM, Mackey B, Tenkova T, Sartorius L, Paul SM, Bales K, Ashe KH, Irizzary MC, Hyman BT (2000) ApoE facilitates neuritic and cerebrovascular plaque formation in the APPsw mouse model of Alzheimer's disease. Ann Neurol 47:739-747.
21. Iwatsubo T, Saido TC, Mann DM, Lee VM, Trojanowski JQ (1996) Full-length amyloid-beta (1-42(43)) and amino-terminally modified and truncated amyloid-beta 42(43) deposit in diffuse plaques. Am J Pathol 149:1823-1830.
22. Jellinger KA (2002) Alzheimer disease and cerebrovascular pathology: an update. J Neural Transm 109:813-836.
23. 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 Aβ42 deposition in a transgenic mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 94:1550-1555.
24. Kawarabayashi T, Younkin LH, Saido TC, Shoji M, Ashe KH, Younkin SG (2001) Age-dependent changes in brain, CSF, and plasma amyloid β protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J Neurosci 21:372-381.
25. Kuo YM, Kokjohn TA, Beach TG, Sue LI, Brune D, Lopez JC, Kalback WM, Abramowski D, Sturchler-Pierrat C, Staufenbiel M, Roher AE (2001) Comparative analysis of amyloid-beta chemical structure and amyloid plaque morphology of transgenic mouse and Alzheimer's disease brains. J Biol Chem 276:12991-12998.
26. Lemere CA, Beierschmitt A, Iglesias M, Spooner ET, Bloom JK, Leverone JF, Zheng JB, Seabrook TJ, Louard D, Li D, Selkoe DJ, Palmour RM, Ervin FR (2004) Alzheimer's disease abeta vaccine reduces central nervous system abeta levels in a non-human primate, the Caribbean vervet. Am J Pathol 165:283-297.
27. Levene H (1960) Robust tests for equality of variances. In: Contributions to probability and statistics (Olkin I, Ghurye SG, Hoeffding W, Madow WG, Mann HB, eds), pp 278-292. Stanford, CA: Stanford UP.
28. McCarron MO, Nicoll JA, Stewart J, Cole GM, Yang F, Ironside JW, Mann DM, Love S, Graham DI (2000) Amyloid beta-protein length and cerebral amyloid angiopathy-related haemorrhage. NeuroReport 11:937-940.
29. 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-β peptide target amyloid-β residues 4-10 and inhibit cytotoxicity and fibrillogenesis. Nat Med 8:1263-1269.
30. Nicoll JA, Wilkinson D, Holmes C, Steart P, Markham H, Weller RO (2003) Neuropathology of human Alzheimer disease after immunization with amyloid-β peptide: a case report. Nat Med 9:448-452.
31. Oh U, Gupta R, Krakauer JW, Khandji AG, Chin SS, Elkind MSV (2004) Reversible leukoencephalopathy associated with cerebral amyloid angiopathy. Neurology 62:494-497.
32. Orgogozo JM, Gilman S, Dartigues JF, Laurent B, Puel M, Kirby LC, Jouanny P, Dubois B, Eisner L, Flitman S, Michel BF, Boada M, Frank A, Hock C (2003) Subacute meningoencephalitis in a subset of patients with AD after Aβ42 immunization. Neurology 61:46-54.
33. Pfeifer M, Boncristiano S, Bondolfi L, Stalder A, Deller T, Staufenbiel M, Mathews PM, Jucker M (2002) Cerebral hemorrhage after passive anti-beta amyloid immunotherapy. Science 298:1379.
34. Rensink AA, de Waal RM, Kremer B, Verbeek MM (2003) Pathogenesis of cerebral amyloid angiopathy. Brain Res Brain Res Rev 43:207-223.
35. 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.
36. Selkoe DJ (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81:741-766.
37. Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591-611.
38. Spooner ET, Desai RV, Mori C, Leverone JF, Lemere CA (2002) The generation and characterization of potentially therapeutic Aβ antibodies in mice: differences according to strain and immunization protocol. Vaccine 21:290-297.
39. Sturchler-Pierrat C, Abramowski D, Duke M, Wiederhold KH, Mistl C, Rothacher S, Ledermann B, Burki K, Frey P, Paganetti PA, Waridel C, Calhoun ME, Jucker M, Probst A, Staufenbiel M, Sommer B (1997) Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc Natl Acad Sci USA 94:13287-13292.
40. Suzuki N, Iwatsubo T, Odaka A, Ishibashi Y, Kitada C, Ihara Y (1994) High tissue content of soluble beta 1-40 is linked to cerebral amyloid angiopathy. Am J Pathol 145:452-460.
41. Van Nostrand WE, Melchor JP, Romanov G, Zeigler K, Davis J (2002) Pathogenic effects of cerebral amyloid angiopathy mutations in the amyloid beta-protein precursor. Ann NY Acad Sci 977:258-265.
42. Vinters HV (1987) Cerebral amyloid angiopathy: a critical review. Stroke 18:311-324.
43. Walker LC (1997) Animal models of cerebral beta-amyloid angiopathy. Brain Res Brain Res Rev 25:70-84.
44. Wikock DM, Rojiani A, Rosenthal A, Alamed J, Wilson D, Wilson N, Freeman MJ, Gordon MN, Morgan D (2004) Passive immunization with anti-Aβ antibodies reduces amyloid burden while producing a brief activation of microglia in a transgenic mouse model of amyloid deposition. Neurobiol Aging 25:579.
45. Winkler DT, Bondolfi L, Herzig MC, Jann L, Calhoun ME, Wiederhold KH, Tolnay M, Staufenbiel M, Jucker M (2001) Spontaneous hemorrhagic stroke in a mouse model of cerebral amyloid angiopathy. J Neurosci 21:1619-1627.