Disruption of arterial perivascular drainage of amyloid-β from the brains of mice expressing the human APOE ε4 allele

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Hawkes, Cheryl A ^a   Sullivan, Patrick M ^b   Hands, Sarah ^c   Weller, Roy O ^a   Nicoll, James A R ^a   Carare, Roxana O ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b DUKE UNIVERSITY   (United States)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; APOLIPOPROTEIN E4; BASEMENT MEMBRANE PROTEIN; COLLAGEN TYPE 4; LAMININ; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

AGING; ALLELE; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOE EPSILON4 GENE; APOE4 GENE; ARTERIAL PERIVASCULAR DRAINAGE DISRUPTION; ARTICLE; BASEMENT MEMBRANE; BRAIN BLOOD VESSEL; BRAIN TISSUE; CEREBROVASCULAR DISEASE; CLEARANCE; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENETIC ASSOCIATION; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PROTEIN AGGREGATION; PROTEIN EXPRESSION; WESTERN BLOTTING; WILD TYPE;

ALLELES; AMYLOID BETA-PEPTIDES; ANIMALS; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; BASEMENT MEMBRANE; BRAIN; CEREBRAL ARTERIES; GENE EXPRESSION; GENOTYPE; HUMANS; MALE; MICE; PEPTIDE FRAGMENTS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY;

MUS;

EID: 84864691664     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041636     Document Type: Article

References (55)

1. Haglund M, Kalaria R, Slade JY, Englund E, (2006) Differential deposition of amyloid beta peptides in cerebral amyloid angiopathy associated with Alzheimer's disease and vascular dementia. Acta Neuropathol 111: 430-435.
2. Miao J, Xu F, Davis J, Otte-Holler I, Verbeek MM, et al. (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.
3. Perlmutter LS, (1994) Microvascular pathology and vascular basement membrane components in Alzheimer's disease. Mol Neurobiol 9: 33-40.
4. Tian J, Shi J, Smallman R, Iwatsubo T, Mann DM, (2006) Relationships in Alzheimer's disease between the extent of Abeta deposition in cerebral blood vessel walls, as cerebral amyloid angiopathy, and the amount of cerebrovascular smooth muscle cells and collagen. Neuropathol Appl Neurobiol 32: 332-340.
5. Natte R, Maat-Schieman ML, Haan J, Bornebroek M, Roos RA, et al. (2001) Dementia in hereditary cerebral hemorrhage with amyloidosis-Dutch type is associated with cerebral amyloid angiopathy but is independent of plaques and neurofibrillary tangles. Ann Neurol 50: 765-772.
6. Pfeifer LA, White LR, Ross GW, Petrovitch H, Launer LJ, (2002) Cerebral amyloid angiopathy and cognitive function: the HAAS autopsy study. Neurology 58: 1629-1634.
7. Pfeifer M, Boncristiano S, Bondolfi L, Stalder A, Deller T, et al. (2002) Cerebral hemorrhage after passive anti-Abeta immunotherapy. Science 298: 1379.
8. Chung YA, Kim JY, Kim KJ, Ahn KJ, (2009) Hypoperfusion and ischemia in cerebral amyloid angiopathy documented by 99mTc-ECD brain perfusion SPECT. J Nucl Med 50: 1969-1974.
9. Shin HK, Jones PB, Garcia-Alloza M, Borrelli L, Greenberg SM, et al. (2007) Age-dependent cerebrovascular dysfunction in a transgenic mouse model of cerebral amyloid angiopathy. Brain 130: 2310-2319.
10. Farrer LA, Cupples LA, Haines JL, Hyman B, Kukull WA, et al. (1997) Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype and Alzheimer disease. A meta-analysis. APOE and Alzheimer Disease Meta Analysis Consortium. JAMA 278: 1349-1356.
11. Premkumar DR, Cohen DL, Hedera P, Friedland RP, Kalaria RN, (1996) Apolipoprotein E-epsilon4 alleles in cerebral amyloid angiopathy and cerebrovascular pathology associated with Alzheimer's disease. Am J Pathol 148: 2083-2095.
12. Mahley RW, Innerarity TL, (1983) Lipoprotein receptors and cholesterol homeostasis. Biochim Biophys Acta 737: 197-222.
13. Masliah E, Mallory M, Veinbergs I, Miller A, Samuel W, (1996) Alterations in apolipoprotein E expression during aging and neurodegeneration. Prog Neurobiol 50: 493-503.
14. Blacker D, Haines JL, Rodes L, Terwedow H, Go RC, et al. (1997) ApoE-4 and age at onset of Alzheimer's disease: the NIMH genetics initiative. Neurology 48: 139-147.
15. Fryer JD, Simmons K, Parsadanian M, Bales KR, Paul SM, et al. (2005) Human apolipoprotein E4 alters the amyloid-beta 40:42 ratio and promotes the formation of cerebral amyloid angiopathy in an amyloid precursor protein transgenic model. J Neurosci 25: 2803-2810.
16. Thal DR, Papassotiropoulos A, Saido TC, Griffin WS, Mrak RE, et al. (2010) Capillary cerebral amyloid angiopathy identifies a distinct APOE epsilon4-associated subtype of sporadic Alzheimer's disease. Acta Neuropathol 120: 169-183.
17. Weller RO, Subash M, Preston SD, Mazanti I, Carare RO, (2008) Perivascular drainage of amyloid-beta peptides from the brain and its failure in cerebral amyloid angiopathy and Alzheimer's disease. Brain Pathol 18: 253-266.
18. Mawuenyega KG, Sigurdson W, Ovod V, Munsell L, Kasten T, et al. (2010) Decreased Clearance of CNS β-Amyloid in Alzheimer's Disease. Science 330: 1774.
19. Bell RD, Zlokovic BV, (2009) Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer's disease. Acta Neuropathol 118: 103-113.
20. Weller RO, Cohen NR, Nicoll JA, (2004) Cerebrovascular disease and the pathophysiology of Alzheimer's disease. Implications for therapy. Panminerva Med 46: 239-251.
21. Cook DG, Leverenz JB, McMillan PJ, Kulstad JJ, Ericksen S, et al. (2003) Reduced hippocampal insulin-degrading enzyme in late-onset Alzheimer's disease is associated with the apolipoprotein E-epsilon4 allele. Am J Pathol 162: 313-319.
22. Du J, Chang J, Guo S, Zhang Q, Wang Z, (2009) ApoE 4 reduces the expression of Abeta degrading enzyme IDE by activating the NMDA receptor in hippocampal neurons. Neurosci Lett 464: 140-145.
23. Vitek MP, Brown CM, Colton CA, (2009) APOE genotype-specific differences in the innate immune response. Neurobiol Aging 30: 1350-1360.
24. Zhao L, Lin S, Bales KR, Gelfanova V, Koger D, et al. (2009) Macrophage-mediated degradation of beta-amyloid via an apolipoprotein E isoform-dependent mechanism. J Neurosci 29: 3603-3612.
25. Deane R, Sagare A, Hamm K, Parisi M, Lane S, et al. (2008) apoE isoform-specific disruption of amyloid beta peptide clearance from mouse brain. J Clin Invest 118: 4002-4013.
26. Couchman JR, Abrahamson DR, McCarthy KJ, (1993) Basement membrane proteoglycans and development. Kidney Int 43: 79-84.
27. Timpl R, (1996) Macromolecular organization of basement membranes. Curr Opin Cell Biol 8: 618-624.
28. Carare RO, Bernardes-Silva M, Newman TA, Page AM, Nicoll JA, et al. (2008) Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries and arteries: significance for cerebral amyloid angiopathy and neuroimmunology. Neuropathol Appl Neurobiol 34: 131-144.
29. van Horssen J, Otte-Holler I, David G, Maat-Schieman ML, van den Heuvel LP, et al. (2001) Heparan sulfate proteoglycan expression in cerebrovascular amyloid beta deposits in Alzheimer's disease and hereditary cerebral hemorrhage with amyloidosis (Dutch) brains. Acta Neuropathol 102: 604-614.
30. Hawkes CA, Hartig W, Kacza J, Schliebs R, Weller RO, et al. (2011) Perivascular drainage of solutes is impaired in the ageing mouse brain and in the presence of cerebral amyloid angiopathy. Acta Neuropathol 121: 431-443.
31. Cotman SL, Halfter W, Cole GJ, (2000) Agrin binds to beta-amyloid (Abeta), accelerates abeta fibril formation, and is localized to Abeta deposits in Alzheimer's disease brain. Mol Cell Neurosci 15: 183-198.
32. Castillo GM, Ngo C, Cummings J, Wight TN, Snow AD, (1997) Perlecan binds to the beta-amyloid proteins (A beta) of Alzheimer's disease, accelerates A beta fibril formation, and maintains A beta fibril stability. J Neurochem 69: 2452-2465.
33. Kiuchi Y, Isobe Y, Fukushima K, Kimura M, (2002) Disassembly of amyloid beta-protein fibril by basement membrane components. Life Sci 70: 2421-2431.
34. Bronfman FC, Alvarez A, Morgan C, Inestrosa NC, (1998) Laminin blocks the assembly of wild-type A beta and the Dutch variant peptide into Alzheimer's fibrils. Amyloid 5: 16-23.
35. Huang DY, Weisgraber KH, Strittmatter WJ, Matthew WD, (1995) Interaction of apolipoprotein E with laminin increases neuronal adhesion and alters neurite morphology. Exp Neurol 136: 251-257.
36. Monji A, Tashiro K, Yoshida I, Hayashi Y, Tashiro N, (1998) Laminin inhibits A beta 40 fibril formation promoted by apolipoprotein E4 in vitro. Brain Res 796: 171-175.
37. Rolyan H, Feike AC, Upadhaya AR, Waha A, Van Dooren T, et al. (2011) Amyloid-beta protein modulates the perivascular clearance of neuronal apolipoprotein E in mouse models of Alzheimer's disease. J Neural Transm 118: 699-712.
38. Thal DR, Larionov S, Abramowski D, Wiederhold KH, Van Dooren T, et al. (2007) Occurrence and co-localization of amyloid beta-protein and apolipoprotein E in perivascular drainage channels of wild-type and APP-transgenic mice. Neurobiol Aging 28: 1221-1230.
39. Salloway S, Gur T, Berzin T, Tavares R, Zipser B, et al. (2002) Effect of APOE genotype on microvascular basement membrane in Alzheimer's disease. J Neurol Sci 203-204: 183-187.
40. Castellano JM, Kim J, Stewart FR, Jiang H, Demattos RB, et al. (2011) Human apoE Isoforms Differentially Regulate Brain Amyloid-{beta} Peptide Clearance. Sci Transl Med 3: 89ra57.
41. Kuhnke D, Jedlitschky G, Grube M, Krohn M, Jucker M, et al. (2007) MDR1-P-Glycoprotein (ABCB1) Mediates Transport of Alzheimer's amyloid-beta peptides-implications for the mechanisms of Abeta clearance at the blood-brain barrier. Brain Pathol 17: 347-353.
42. Mandrekar S, Jiang Q, Lee CY, Koenigsknecht-Talboo J, Holtzman DM, et al. (2009) Microglia mediate the clearance of soluble Abeta through fluid phase macropinocytosis. J Neurosci 29: 4252-4262.
43. Kandimalla KK, Scott OG, Fulzele S, Davidson MW, Poduslo JF, (2009) Mechanism of neuronal versus endothelial cell uptake of Alzheimer's disease amyloid beta protein. PLoS One 4: e4627.
44. Sullivan PM, Mace BE, Estrada JC, Schmechel DE, Alberts MJ, (2008) Human apolipoprotein E4 targeted replacement mice show increased prevalence of intracerebral hemorrhage associated with vascular amyloid deposition. J Stroke Cerebrovasc Dis 17: 303-311.
45. Filippini N, Ebmeier KP, MacIntosh BJ, Trachtenberg AJ, Frisoni GB, et al. (2011) Differential effects of the APOE genotype on brain function across the lifespan. Neuroimage 54: 602-610.
46. Kok E, Haikonen S, Luoto T, Huhtala H, Goebeler S, et al. (2009) Apolipoprotein E-dependent accumulation of Alzheimer disease-related lesions begins in middle age. Ann Neurol 65: 650-657.
47. Bell RD, Sagare AP, Friedman AE, Bedi GS, Holtzman DM, et al. (2007) Transport pathways for clearance of human Alzheimer's amyloid beta-peptide and apolipoproteins E and J in the mouse central nervous system. J Cereb Blood Flow Metab 27: 909-918.
48. Deane R, Zlokovic BV, (2007) Role of the blood-brain barrier in the pathogenesis of Alzheimer's disease. Curr Alzheimer Res 4: 191-197.
49. Hawkes CA, McLaurin J, (2009) Selective targeting of perivascular macrophages for clearance of beta-amyloid in cerebral amyloid angiopathy. Proc Natl Acad Sci U S A 106: 1261-1266.
50. Wu Z, Guo H, Chow N, Sallstrom J, Bell RD, et al. (2005) Role of the MEOX2 homeobox gene in neurovascular dysfunction in Alzheimer disease. Nat Med 11: 959-965.
51. Bell RD, Deane R, Chow N, Long X, Sagare A, et al. (2009) SRF and myocardin regulate LRP-mediated amyloid-beta clearance in brain vascular cells. Nat Cell Biol 11: 143-153.
52. Sullivan PM, Han B, Liu F, Mace BE, Ervin JF, et al. (2011) Reduced levels of human apoE4 protein in an animal model of cognitive impairment. Neurobiol Aging 32: 791-801.
53. Salloway S, Sperling R, Gilman S, Fox NC, Blennow K, et al. (2009) A phase 2 multiple ascending dose trial of bapineuzumab in mild to moderate Alzheimer disease. Neurology 73: 2061-2070.
54. Boche D, Zotova E, Weller RO, Love S, Neal JW, et al. (2008) Consequence of Abeta immunization on the vasculature of human Alzheimer's disease brain. Brain 131: 3299-3310.
55. Sullivan PM, Mezdour H, Aratani Y, Knouff C, Najib J, et al. (1997) Targeted replacement of the mouse apolipoprotein E gene with the common human APOE3 allele enhances diet-induced hypercholesterolemia and atherosclerosis. J Biol Chem 272: 17972-17980.