Reducing available soluble β-amyloid prevents progression of cerebral amyloid angiopathy in transgenic mice

Journal of Neuropathology and Experimental Neurology

Volumn 71, Issue 11, 2012, Pages 1009-1017

  Gregory, Julia L ^a   Prada, Claudia M ^a   Fine, Sara J ^a   Garcia Alloza, Monica ^a,b   Betensky, Rebecca A ^c   Arbel Ornath, Michal ^a   Greenberg, Steven M ^a   Bacskai, Brian J ^a   Frosch, Matthew P ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF CÁDIZ   (Spain)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Alzheimer; Amyloid; Cerebral amyloid angiopathy; Cerebrovasculature; Gamma secretase; Gelsolin; Imaging; Multiphoton

Indexed keywords

AMYLOID BETA PROTEIN; GAMMA SECRETASE; GELSOLIN; N2 [2 (3,5 DIFLUOROPHENYL) 2 HYDROXYACETYL] N1 (6,7 DIHYDRO 5 METHYL 6 OXO 5H DIBENZ[B,D]AZEPIN 7 YL)ALANINAMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CONTROLLED STUDY; DISEASE COURSE; ENZYME INHIBITION; FEMALE; IMMUNE RESPONSE; MALE; MOUSE; MULTIPHOTON MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE; VASCULAR AMYLOIDOSIS;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; CEREBRAL AMYLOID ANGIOPATHY; DISEASE PROGRESSION; FEMALE; MALE; MICE; MICE, TRANSGENIC; SOLUBILITY;

EID: 84871249596     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0b013e3182729845     Document Type: Article

References (44)

1. Jellinger KA. Alzheimer disease and cerebrovascular pathology: An update. J Neural Transm 2002;109:813-36
2. Vinters HV. Cerebral amyloid angiopathy: A critical review. Stroke 1987; 18:311-24
3. Zhang-Nunes S, Maat-Schieman M, van Duinan S, et al. The cerebral beta-amyloid angiopathies: Hereditary and sporadic. Brain Pathol 2006; 16:30-39
4. Nicoll JA, Wilkinson D, Holmes C, et al. Neuropathology of human Alzheimer disease after immunization with amyloid-beta peptide: A case report. Nat Med 2003;9:448-52
5. Salloway S, Sperling R, Gilman S, et al. A phase 2 multiple ascending dose trial of bapineuzumab in mild to moderate Alzheimer disease. Neurology 2009;73:2061-70
6. Sperling RA, Jack CR Jr., Black SE, et al. Amyloid-related imaging abnormalities in amyloid-modifying therapeutic trials: Recommendations from the Alzheimer's Association Research Roundtable Workgroup. Alzheimers Dement 2011;7:367-85
7. DeMattos RB, Bales KR, Cummins DJ, et al. 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 2001;98:8850-55
8. Matsuoka Y, Saito M, LaFrancois J, et al. Novel therapeutic approach for the treatment of Alzheimer's disease by peripheral administration of agents with an affinity to beta-amyloid. J Neurosci 2003;23:29-33
9. Dovey HF, John V, Anderson JP, et al. Functional gamma-secretase inhibitors reduce beta-amyloid peptide levels in brain. J Neurochem 2001; 76:173-81
10. Siemers ER, Quinn JF, Kaye J, et al. Effects of a {gamma}-secretase inhibitor in a randomized study of patients with Alzheimer disease. Neurology 2006;66:602-4
11. Lanz TA, Hosley JD, Adams WJ, et al. Studies of Abeta pharmacodynamics in the brain, cerebrospinal fluid, and plasma in young (plaque-free) Tg2576 mice using the gamma-secretase inhibitor N2-[(2S)-2-(3,5- difluorophenyl)-2- hydroxyethanoyl]-N1-[(7S)-5-methyl-6-oxo-6,7- dihydro-5H-dibenzo[b,d]azepin-7- yl]-L-alaninamide (LY-411575). J Pharmacol Exp Ther 2004;309:49-55
12. Hyde LA, McHugh NA, Chen J, et al. Studies to investigate the in vivo therapeutic window of the gamma-secretase inhibitor N2-[(2S)-2-(3,5- difluorophenyl)-2-hydroxyethanoyl]-N1-[(7S)-5-methyl-6-oxo-6,7- di hydro-5H-dibenzo[b,d]azepin-7-yl]-L-alaninamide (L-411575) in the CRND8 mouse. J Pharmacol Exp Ther 2006;319:1133-43
13. Garcia-Alloza M, Subramanian M, Thyssen D, et al. Existing plaques and neuritic abnormalities in APP:PS1 mice are not affected by administration of the gamma-secretase inhibitor LY-411575. Mol Neurodegener 2009;4:19
14. Domnitz SB, Robbins EM, Hoang AW, et al. Progression of cerebral amyloid angiopathy in transgenic mouse models of Alzheimer disease. J Neuropathol Exp Neurol 2005;64:588-94
15. Prada CM, Garcia-Alloza M, Betensky RA, et al. Antibody-mediated clearance of amyloid-beta peptide from cerebral amyloid angiopathy revealed by quantitative in vivo imaging. J Neurosci 2007;27:1973-80
16. Robbins EM, Betensky RA, Domnitz SB, et al. Kinetics of cerebral amyloid angiopathy progression in a transgenic mouse model of Alzheimer disease. J Neurosci 2006;26:365-71
17. Garcia-Alloza M, Robbins EM, Zhang-Nunes SX, et al. Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis 2006;24:516-24
18. Hsiao K, Chapman P, Nilsen S, et al. Correlative memory deficits, A beta elevation, and amyloid plaques in transgenic mice. Science 1996;274: 99-102
19. Fauq AH, Simpson K, Maharvi GM, et al. A multigram chemical synthesis of the gamma-secretase inhibitor L-411575 and its diastereoisomers. Bioorg Med Chem Lett 2007;17:6392-5
20. Kukar T, Murphy MP, Eriksen JL, et al. Diverse compounds mimic Alzheimer diseaseYcausing mutations by augmenting Abeta42 production. Nat Med 2005;11:545-50
21. Klunk WEMP, Bacskai BJP, Mathis CAP, et al. Imaging A[beta] plaques in living transgenic mice with multiphoton microscopy and methoxy-X04, a systemically administered Congo red derivative. J Neuropathol Exp Neurol 2002;61:797-805
22. Schenk D, Barbour R, Dunn W, et al. Immunization with amyloid-bold beta attenuates Alzheimer-diseaseYlike pathology in the PDAPP mouse. Nature 1999;400:173-77
23. Bacskai BJ, Kajdasz ST, Christie RH, et al. Imaging of amyloid-[beta] deposits in brains of living mice permits direct observation of clearance of plaques with immunotherapy. Nat Med 2001;7:369-72
24. Boche D, Zotova E, Weller RO, et al. Consequence of Abeta immunization on the vasculature of human Alzheimer's disease brain. Brain 2008; 131:3299-310
25. Yohrling GJ, Felsenstein KM, Conway KA, et al. A comparative analysis of brain and plasma Abeta levels in eight common non-transgenic mouse strains: Validation of a specific immunoassay for total rodent Abeta. Curr Alzheimer Res 2007;4:297-303
26. Abramowski D, Wiederhold KH, Furrer U, et al. Dynamics of Abeta turnover and deposition in different beta-amyloid precursor protein transgenic mouse models following gamma-secretase inhibition. J Pharmacol Exp Ther 2008;327:411-24
27. Best JD, Jay MT, Otu F, et al. Quantitative measurement of changes in amyloid-beta(40) in the rat brain and cerebrospinal fluid following treatment with the gamma-secretase inhibitor LY-411575 [N2-[(2S)-2-(3,5- difluorophenyl)-2-hydroxyethanoyl]-N1-[(7S)-5-methyl-6-oxo-6,7-d ihydro-5H-dibenzo[b,d]azepin-7-yl]-L-alaninamide]. J Pharmacol Exp Ther 2005;313:902-8
28. Siemers ER, Dean RA, Friedrich S, et al. Safety, tolerability, and effects on plasma and cerebrospinal fluid amyloid-beta after inhibition of gamma-secretase. Clin Neuropharmacol 2007;30:317-25
29. Schor NF. What the halted phase III gamma-secretase inhibitor trial may (or may not) be telling us. Ann Neurol 2011;69:237-39
30. Mitani Y, Yarimizu J, Saita K, et al. Differential effects between gammasecretase inhibitors and modulators on cognitive function in amyloid precursor protein-transgenic and nontransgenic mice. J Neurosci 2012; 32:2037-50
31. Barten DM, Guss VL, Corsa JA, et al. Dynamics of {beta}-amyloid reductions in brain, cerebrospinal fluid, and plasma of {beta}-amyloid precursor protein transgenic mice treated with a {gamma}-secretase inhibitor. J Pharmacol Exp Ther 2005;312:635-43
32. Wen D, Corina K, Chow EP, et al. The plasma and cytoplasmic forms of human gelsolin differ in disulfide structure. Biochemistry 1996;35: 9700-9
33. Chauhan V, Ray I, Chauhan A, et al. Binding of gelsolin, a secretory protein, to amyloid [beta]-protein. Biochem Biophys Res Commun 1999; 258:241-46
34. Ray I, Chauhan A, Wegiel J, et al. Gelsolin inhibits the fibrillization of amyloid beta-protein and also defibrillizes its preformed fibrils. Brain Res 2000;853:344-51
35. Antequera D, Vargas T, Ugalde C, et al. Cytoplasmic gelsolin increases mitochondrial activity and reduces A[beta] burden in a mouse model of Alzheimer's disease. Neurobiol Dis 2009;36:42-50
36. Schroeter S, Khan K, Barbour R, et al. Immunotherapy reduces vascular amyloid-beta in PDAPP mice. J Neurosci 2008;28:6787-93
37. Bacskai BJ, Kajdasz ST, McLellan ME, et al. Non-FcYmediated mechanisms are involved in clearance of amyloid-beta in vivo by immunotherapy. J Neurosci 2002;22:7873-78
38. Christie RH, Bacskai BJ, Zipfel WR, et al. Growth arrest of individual senile plaques in a model of Alzheimer's disease observed by in vivo multiphoton microscopy. J Neurosci 2001;21:858-64
39. Hirko AC, Meyer EM, King MA, et al. Peripheral transgene expression of plasma gelsolin reduces amyloid in transgenic mouse models of Alzheimer's disease. Mol Ther 2007;15:1623-29
40. Choo-Smith LP, Garzon-Rodriguez W, Glabe CG, Surewicz WK. Acceleration of amyloid fibril formation by specific binding of Abeta-(1-40) peptide to ganglioside-containing membrane vesicles. J Biol Chem 1997; 272:22987-90
41. Orgogozo JM, Gilman S, Dartigues JF, et al. Subacute meningoencephalitis in a subset of patients with AD after Abeta42 immunization. Neurology 2003;61:46-54
42. Pfeifer M, Boncristiano S, Bondolfi L, et al. Cerebral hemorrhage after passive anti-Abeta immunotherapy. Science 2002;298:1379
43. Racke MM, Boone LI, Hepburn DL, et al. Exacerbation of cerebral amyloid angiopathyYassociated microhemorrhage in amyloid precursor protein transgenic mice by immunotherapy is dependent on antibody recognition of deposited forms of amyloid beta. J Neurosci 2005;25: 629-36
44. Wilcock DM, Rojiani A, Rosenthal A, et al. Passive amyloid immunotherapy clears amyloid and transiently activates microglia in a transgenic mouse model of amyloid deposition. J Neurosci 2004;24:6144-51