Influence of LRP-1 and apolipoprotein E on Amyloid-β uptake and toxicity to cerebrovascular smooth muscle cells

Journal of Alzheimer's Disease

Volumn 33, Issue 1, 2013, Pages 95-110

  Ruzali, Wan Adriyani W ^a   Kehoe, Patrick G ^a   Love, Seth ^a  

^a FRENCHAY HOSPITAL   (United Kingdom)

Author keywords

Amyloid ; apolipoprotein E; cell death; cerebral amyloid angiopathy; low density lipoprotein receptor related protein 1; receptor associated protein; smooth muscle cell

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; APOLIPOPROTEIN E; APOLIPOPROTEIN E2; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; FLUORESCEIN; HIGH DENSITY LIPOPROTEIN; ISOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; SMOOTH MUSCLE ACTIN;

ARTICLE; BRAIN BLOOD VESSEL; CELL DEATH; CONTROLLED STUDY; CYTOTOXICITY; FETUS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN TRANSPORT; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

EID: 84872470182     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2012-121336     Document Type: Article

References (89)

1. Zlokovic BV (2005) Neurovascular mechanisms of Alzheimer's neurodegeneration. Trends Neurosci 28, 202-208. (Pubitemid 40445527)
2. Weller RO, Boche D, Nicoll JA (2009) Microvasculature changes and cerebral amyloid angiopathy in Alzheimer's disease and their potential impact on therapy. Acta Neuropathol 118, 87-102.
3. Weller RO, Massey A, Newman TA, Hutchings M, Kuo YM, RoherAE(1998) Cerebral amyloid angiopathy: Amyloid beta accumulates in putative interstitial fluid drainage pathways in Alzheimer's disease. Am J Pathol 153, 725-733. (Pubitemid 28419027)
4. Bell RD, Zlokovic BV (2009) Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer's disease. Acta Neuropathol 118, 103-113.
5. WellerRO, Preston SD, Subash M, CarareRO(2009) Cerebral amyloid angiopathy in the aetiology and immunotherapy of Alzheimer disease. Alzheimers Res Ther 1, 6.
6. WellerRO, Djuanda E,YowHY, CarareRO(2009) Lymphatic drainage of the brain and the pathophysiology of neurological disease. Acta Neuropathol 117, 1-14.
7. GaoW, Eisenhauer PB, Conn K, Lynch JA,Wells JM, Ullman MD,McKee A, Thatte HS, Fine RE (2004) Insulin degrading enzyme is expressed in the human cerebrovascular endothelium and in cultured human cerebrovascular endothelial cells. Neurosci Lett 371, 6-11. (Pubitemid 39410505)
8. Morelli L, Llovera RE, Mathov I, Lue LF, Frangione B, Ghiso J, Castano EM (2004) Insulin-degrading enzyme in brain microvessels: Proteolysis of amyloid beta vasculotropic variants and reduced activity in cerebral amyloid angiopathy. J Biol Chem 279, 56004-56013. (Pubitemid 40066608)
9. Carpentier M, Robitaille Y, DesGroseillers L, Boileau G, Marcinkiewicz M (2002) Declining expression of neprilysin in Alzheimer disease vasculature: Possible involvement in cerebral amyloid angiopathy. J Neuropathol Exp Neurol 61, 849-856.
10. Miners JS, Baig S, Palmer J, Palmer LE, Kehoe PG, Love S (2008) Abeta-degrading enzymes in Alzheimer's disease. Brain Pathol 18, 240-252.
11. Miners JS, Van Helmond Z, Chalmers K,Wilcock G, Love S, Kehoe PG (2006) Decreased expression and activity of neprilysin in Alzheimer disease are associated with cerebral amyloid angiopathy. J Neuropathol Exp Neurol 65, 1012-1021. (Pubitemid 44521802)
12. Miners JS,Kehoe P, Love S (2011) Neprilysin protects against cerebral amyloid angiopathy and Abeta-induced degeneration of cerebrovascular smooth muscle cells. Brain Pathol 21, 594-605.
13. 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.
14. Melchor JP, Van Nostrand WE (2000) Fibrillar amyloid betaprotein mediates the pathologic accumulation of its secreted precursor in human cerebrovascular smooth muscle cells. J Biol Chem 275, 9782-9791. (Pubitemid 30185213)
15. Miao J, Xu F, Davis J, Otte-Holler I, Verbeek MM, Van NostrandWE( 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. (Pubitemid 43026105)
16. Davis J, Cribbs DH, Cotman CW, Van Nostrand WE (1999) Pathogenic amyloid beta-protein induces apoptosis in cultured human cerebrovascular smooth muscle cells. Amyloid 6, 157-164. (Pubitemid 29483006)
17. 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. (Pubitemid 32038587)
18. Zheng G, Bachinsky DR, Stamenkovic I, Strickland DK, Brown D, Andres G, McCluskey RT (1994) Organ distribution in rats of two members of the low-density lipoprotein receptor gene family, gp330 and LRP/alpha 2MR, and the receptor-associated protein (RAP). J Histochem Cytochem 42, 531-542. (Pubitemid 24090013)
19. Bu G, Maksymovitch EA, Nerbonne JM, Schwartz AL (1994) Expression and function of the low density lipoprotein receptor-related protein (LRP) in mammalian central neurons. J Biol Chem 269, 18521-18528. (Pubitemid 24224088)
20. Rebeck GW, Harr SD, Strickland DK, Hyman BT (1995) Multiple, diverse senile plaque-associated proteins are ligands of an apolipoprotein E receptor, the alpha 2-macroglobulin receptor/low-density-lipoprotein receptorrelated protein. Ann Neurol 37, 211-217.
21. Hollister RD, Kisiel W, Hyman BT (1996) Immunohistochemical localization of tissue factor pathway inhibitor-1 (TFPI-1), a Kunitz proteinase inhibitor, in Alzheimer's disease. Brain Res 728, 13-19. (Pubitemid 26254951)
22. Arelin K, Kinoshita A, WhelanCM,IrizarryMC,RebeckGW, Strickland DK, Hyman BT (2002) LRP and senile plaques in Alzheimer's disease: Colocalization with apolipoprotein E and with activated astrocytes. Brain Res Mol Brain Res 104, 38-46. (Pubitemid 34765544)
23. Rebeck GW, Reiter JS, Strickland DK, Hyman BT (1993) Apolipoprotein E in sporadic Alzheimer's disease: Allelic variation and receptor interactions. Neuron 11, 575-580. (Pubitemid 23321768)
24. Cam JA, Bu G (2006) Modulation of beta-amyloid precursor protein trafficking and processing by the low density lipoprotein receptor family. Mol Neurodegener 1, 8.
25. Ulery PG, Beers J, Mikhailenko I, Tanzi RE, Rebeck GW, Hyman BT, Strickland DK (2000) Modulation of betaamyloid precursor protein processing by the low density lipoprotein receptor-related protein (LRP). Evidence thatLRP contributes to the pathogenesis of Alzheimer's disease. J Biol Chem 275, 7410-7415. (Pubitemid 30146296)
26. Pietrzik CU, BusseT, Merriam DE,Weggen S,KooEH(2002) The cytoplasmic domain of the LDL receptor-related protein regulates multiple steps inAPPprocessing.EMBOJ 21, 5691-5700. (Pubitemid 35315269)
27. Bu G (2009) Apolipoprotein E and its receptors in Alzheimer's disease: Pathways, pathogenesis and therapy. Nat Rev Neurosci 10, 333-344.
28. Aleshkov S, Abraham CR, Zannis VI (1997) Interaction of nascent ApoE2, ApoE3, and ApoE4 isoforms expressed in mammalian cells with amyloid peptide beta (1-40). Relevance to Alzheimer's disease. Biochemistry 36, 10571-10580. (Pubitemid 27374151)
29. Hyman BT, Strickland D, RebeckGW(2000) Role of the lowdensity lipoprotein receptor-related protein in beta-amyloid metabolism and Alzheimer disease. Arch Neurol 57, 646-650. (Pubitemid 30252798)
30. Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J, Salvesen GS, Roses AD (1993) Apolipoprotein E: High-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc Natl Acad Sci U S A 90, 1977-1981. (Pubitemid 23069980)
31. Corder EH, Saunders AM, Risch NJ, Strittmatter WJ, Schmechel DE, Gaskell PC Jr, Rimmler JB, Locke PA, Conneally PM, Schmader KE et al. (1994) Protective effect of apolipoproteinEtype 2 allele for late onset Alzheimer disease. Nat Genet 7, 180-184. (Pubitemid 24174658)
32. 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. (Pubitemid 28182634)
33. Greenberg SM, Rebeck GW, Vonsattel JP, Gomez-Isla T, Hyman BT (1995) Apolipoprotein E epsilon 4 and cerebral hemorrhage associated with amyloid angiopathy. Ann Neurol 38, 254-259.
34. Chalmers K, Wilcock GK, Love S (2003) APOE epsilon 4 influences the pathological phenotype of Alzheimer's disease by favouring cerebrovascular over parenchymal accumulation of A beta protein. Neuropathol Appl Neurobiol 29, 231-238. (Pubitemid 36718171)
35. Love S, Nicoll JA, Hughes A,Wilcock GK (2003) APOE and cerebral amyloid angiopathy in the elderly. Neuroreport 14, 1535-1536. (Pubitemid 37083144)
36. McCarron MO, Nicoll JA (1998) High frequency of apolipoprotein E epsilon 2 allele is specific for patients with cerebral amyloid angiopathy-related haemorrhage. Neurosci Lett 247, 45-48. (Pubitemid 28231333)
37. Nicoll JA, Burnett C, Love S, Graham DI, Dewar D, Ironside JW, Stewart J, Vinters HV (1997) High frequency of apolipoprotein E epsilon 2 allele in hemorrhage due to cerebral amyloid angiopathy. Ann Neurol 41, 716-721. (Pubitemid 27249176)
38. Nicoll JA, Burnett C, Love S, Graham DI, IronsideJW,Vinters HV (1996) High frequency of apolipoprotein E epsilon 2 in patients with cerebral hemorrhage due to cerebral amyloid angiopathy. Ann Neurol 39, 682-683. (Pubitemid 26143609)
39. McCarron MO, Nicoll JA, Stewart J, Ironside JW,Mann DM, Love S, Graham DI, Dewar D (1999) The apolipoprotein E epsilon2 allele and the pathological features in cerebral amyloid angiopathy-related hemorrhage. J Neuropathol Exp Neurol 58, 711-718. (Pubitemid 29328500)
40. Greenberg SM, Vonsattel JP, Segal AZ, Chiu RI, Clatworthy AE, Liao A, Hyman BT, Rebeck GW (1998) Association of apolipoprotein E epsilon2 and vasculopathy in cerebral amyloid angiopathy. Neurology 50, 961-965. (Pubitemid 28212822)
41. Yang DS, Small DH, Seydel U, Smith JD, Hallmayer J, Gandy SE, Martins RN (1999) Apolipoprotein E promotes the binding and uptake of beta-amyloid into Chinese hamster ovary cells in an isoform-specific manner. Neuroscience 90, 1217-1226. (Pubitemid 29170140)
42. Fagan AM, Bu G, Sun Y, Daugherty A, HoltzmanDM(1996) Apolipoprotein E-containing high density lipoprotein promotes neurite outgrowth and is a ligand for the low density lipoprotein receptor-related protein. J Biol Chem 271, 30121-30125. (Pubitemid 26389653)
43. Elliott DA, Halliday GM, Garner B (2010) Apolipoprotein-E forms dimers in human frontal cortex and hippocampus.BMC Neurosci 11, 23.
44. Weisgraber KH, Shinto LH (1991) Identification of the disulfide-linked homodimer of apolipoprotein E3 in plasma. Impact on receptor binding activity. J Biol Chem 266, 12029-12034. (Pubitemid 21907052)
45. Kanekiyo T, Bu G (2009) Receptor-associated protein interacts with amyloid-beta peptide and promotes its cellular uptake. J Biol Chem 284, 33352-33359.
46. Urmoneit B, Prikulis I,Wihl G, D'Urso D, Frank R, Heeren J, Beisiegel U, Prior R (1997) Cerebrovascular smooth muscle cells internalize Alzheimer amyloid beta protein via a lipoprotein pathway: Implications for cerebral amyloid angiopathy. Lab Invest 77, 157-166. (Pubitemid 27355912)
47. WilhelmusMM,Otte-Holler I, van Triel JJ,Veerhuis R, Maat-Schieman ML, Bu G, de Waal RM, Verbeek MM (2007) Lipoprotein receptor-related protein-1 mediates amyloidbeta-mediated cell death of cerebrovascular cells. Am J Pathol 171, 1989-1999.
48. Deane R,Wu Z, Sagare A, Davis J, Du Yan S, Hamm K, Xu F, Parisi M, LaRue B, HuHW, 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. (Pubitemid 39061126)
49. Qiu Z, Strickland DK, Hyman BT, Rebeck GW (1999) Alpha2-macroglobulin enhances the clearance of endogenous soluble beta-amyloid peptide via low-density lipoprotein receptor-related protein in cortical neurons. J Neurochem 73, 1393-1398. (Pubitemid 29440138)
50. Davis-Salinas J, Saporito-Irwin SM, Cotman CW, Van Nostrand WE (1995) Amyloid beta-protein induces its own production in cultured degenerating cerebrovascular smooth muscle cells. J Neurochem 65, 931-934.
51. Davis-Salinasx J, Van Nostrand WE (1995) Amyloid betaprotein aggregation nullifies its pathologic properties in cultured cerebrovascular smooth muscle cells. J Biol Chem 270, 20887-20890.
52. Subasinghe S, Unabia S, Barrow CJ, Mok SS, Aguilar MI, Small DH (2003) Cholesterol is necessary both for the toxic W.A.W. Ruzali et al. / LRP-1, ApoE and Aβ Smooth Muscle Toxicity 109 effect of Abeta peptides on vascular smooth muscle cells and for Abeta binding to vascular smooth muscle cell membranes. J Neurochem 84, 471-479. (Pubitemid 36182246)
53. Gwebu ET, Williams J, Mathis D, Warden JA, Selassie M, Richardson S, Gwebu NT (1997) Cytotoxicity of betaamyloid peptide 25-35 on vascular smooth muscle cells and attenuation by vitamin E. In Vitro Cell Dev Biol Anim 33, 672-673.
54. Wilhelmus MM, Otte-Holler I, Davis J, Van Nostrand WE, de Waal RM, Verbeek MM (2005) Apolipoprotein E genotype regulates amyloid-beta cytotoxicity. J Neurosci 25, 3621-3627.
55. Wang Z, Natte R, Berliner JA, van Duinen SG, Vinters HV (2000) Toxicity of Dutch (E22Q) and Flemish (A21G) mutant amyloid beta proteins to human cerebral microvessel and aortic smooth muscle cells. Stroke 31, 534-538. (Pubitemid 30078193)
56. Davis J, Van NostrandWE(1996) Enhanced pathologic properties of Dutch-type mutant amyloid beta-protein. Proc Natl Acad Sci U S A 93, 2996-3000. (Pubitemid 26114352)
57. Mazur-Kolecka B, Frackowiak J, Wisniewski HM (1995) Apolipoproteins E3 and E4 induce, and transthyretin prevents accumulation of the Alzheimer's beta-amyloid peptide in cultured vascular smooth-muscle cells. Brain Res 698, 217-222.
58. Deane R, Sagare A, Hamm K, Parisi M, Lane S, Finn MB, Holtzman DM, Zlokovic BV (2008) apoE isoform-specific disruption of amyloid beta peptide clearance from mouse brain. J Clin Invest 118, 4002-4013.
59. Koistinaho M, Lin S, Wu X, Esterman M, Koger D, Hanson J, Higgs R, Liu F, Malkani S, Bales KR, Paul SM (2004) Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloid-beta peptides. Nat Med 10, 719-726. (Pubitemid 38937637)
60. Tokuda T, Calero M, Matsubara E, Vidal R, Kumar A, Permanne B, Zlokovic B, Smith JD, Ladu MJ, Rostagno A, Frangione B, Ghiso J (2000) Lipidation of apolipoprotein E influences its isoform-specific interaction with Alzheimer's amyloid beta peptides. Biochem J 348 (Pt 2), 359-365. (Pubitemid 30345209)
61. LaDu MJ, Falduto MT, Manelli AM, Reardon CA, Getz GS, Frail DE (1994) Isoform-specific binding of apolipoprotein E to beta-amyloid. J Biol Chem 269, 23403-23406.
62. Tamamizu-Kato S, Cohen JK, Drake CB, Kosaraju MG, Drury J, Narayanaswami V (2008) Interaction with amyloid beta peptide compromises the lipid binding function of apolipoprotein E. Biochemistry 47, 5225-5234. (Pubitemid 351620759)
63. Ruiz J,Kouiavskaia D, Migliorini M, Robinson S, Saenko EL, Gorlatova N, Li D, Lawrence D, Hyman BT,Weisgraber KH, Strickland DK (2005) The apoE isoform binding properties of the VLDL receptor reveal marked differences from LRP and the LDL receptor. J Lipid Res 46, 1721-1731. (Pubitemid 41099339)
64. Rolyan H, Feike AC, Upadhaya AR, Waha A, Van Dooren T, Haass C, Birkenmeier G, Pietrzik CU, Van Leuven F, Thal DR (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.
65. Urmoneit B, Prikulis I, Wihl G, Durso D, Frank R, Heeren J, Beisiegel U, Prior R (1997) Cerebrovascular smooth muscle cells internalize Alzheimer amyloid beta protein via a lipoprotein pathway: Implications for cerebral amyloid angiopathy. Lab Invest 77, 157-166. (Pubitemid 27355912)
66. Narita M, Holtzman DM, Schwartz AL, Bu G (1997) Alpha2-macroglobulin complexes with and mediates the endocytosis of beta-amyloid peptide via cell surface low-density lipoprotein receptor-related protein. J Neurochem 69, 1904-1911. (Pubitemid 27452736)
67. Whitson JS, Mims MP, Strittmatter WJ, Yamaki T, Morrisett JD, Appel SH (1994) Attenuation of the neurotoxic effect ofA beta amyloid peptide by apolipoprotein E. Biochem Biophys Res Commun 199, 163-170. (Pubitemid 24179929)
68. Puttfarcken PS, Manelli AM, Falduto MT, Getz GS, LaDu MJ (1997) Effect of apolipoprotein E on neurite outgrowth and beta-amyloid-induced toxicity in developing rat primary hippocampal cultures. J Neurochem 68, 760-769. (Pubitemid 27044741)
69. Miyata M, Smith JD (1996) Apolipoprotein E allele-specific antioxidant activity and effects on cytotoxicity by oxidative insults and beta-amyloid peptides. Nat Genet 14, 55-61. (Pubitemid 26301547)
70. Mazur-Kolecka B, Dickson D, Frackowiak J (2006) Induction of vascular amyloidosis-beta by oxidative stress depends on APOE genotype. Neurobiol Aging 27, 804-814.
71. Prior R, Wihl G, Urmoneit B (2000) Apolipoprotein E, smooth muscle cells and the pathogenesis of cerebral amyloid angiopathy: The potential role of impaired cerebrovascular A beta clearance. Ann N Y Acad Sci 903, 180-186. (Pubitemid 30251557)
72. Van Nostrand WE, Melchor JP, Ruffini L (1998) Pathologic amyloid beta-protein cell surface fibril assembly on cultured human cerebrovascular smooth muscle cells. J Neurochem 70, 216-223. (Pubitemid 28020846)
73. Chafekar SM, Baas F, Scheper W (2008) Oligomer-specific Abeta toxicity in cell models is mediated by selective uptake. Biochim Biophys Acta 1782, 523-531.
74. Balcells M, Wallins JS, Edelman ER (2008) Amyloid beta toxicity dependent upon endothelial cell state. Neurosci Lett 441, 319-322.
75. Lehtimaki T, Pirttila T, Mehta PD, Wisniewski HM, Frey H, Nikkari T (1995) Apolipoprotein E (apoE) polymorphism and its influence on ApoE concentrations in the cerebrospinal fluid in Finnish patients with Alzheimer's disease. Hum Genet 95, 39-42.
76. Nakamura T, Shoji M, Harigaya Y, Watanabe M, Hosoda K, Cheung TT, Shaffer LM, Golde TE,Younkin LH,Younkin SG et al. (1994) Amyloid beta protein levels in cerebrospinal fluid are elevated in early-onset Alzheimer's disease. Ann Neurol 36, 903-911.
77. Mehta PD, Pirttila T, Patrick BA, Barshatzky M, Mehta SP (2001) Amyloid beta protein 1-40 and 1-42 levels in matched cerebrospinal fluid and plasma from patients with Alzheimer disease. Neurosci Lett 304, 102-106. (Pubitemid 32377212)
78. Brody DL, Magnoni S, Schwetye KE, Spinner ML, Esparza TJ, Stocchetti N, Zipfel GJ, Holtzman DM (2008) Amyloidbeta dynamics correlate with neurological status in the injured human brain. Science 321, 1221-1224.
79. Jung SS, Van Nostrand WE (2003) Humanin rescues human cerebrovascular smooth muscle cells from Abeta-induced toxicity. J Neurochem 84, 266-272. (Pubitemid 36182268)
80. Cam JA, Zerbinatti CV, Li Y, Bu G (2005) Rapid endocytosis of the low density lipoprotein receptor-related protein modulates cell surface distribution and processing of the beta-amyloid precursor protein. J Biol Chem 280, 15464-15470. (Pubitemid 40562905)
81. Veinbergs I, Van Uden E, Mallory M, Alford M, McGiffert C, DeTeresa R, Orlando R, Masliah E (2001) Role of apolipoprotein E receptors in regulating the differential in vivo neurotrophic effects of apolipoprotein E. Exp Neurol 170, 15-26. (Pubitemid 32641770)
82. XuG, Karch C, Li N, Lin N, Fromholt D, GonzalesV, Borchelt DR (2008) Receptor-associated protein (RAP) plays a central role in modulating Abeta deposition in APP/PS1 transgenic mice. PLoS One 3, e3159.
83. Deane R, Wu Z, Zlokovic BV (2004) RAGE (yin) versus LRP (yang) balance regulates alzheimer amyloid beta-peptide clearance through transport across the blood-brain barrier. Stroke 35, 2628-2631. 110 W.A.W. Ruzali et al. / LRP-1, ApoE and Aβ Smooth Muscle Toxicity (Pubitemid 39458354)
84. Sagare A, Deane R, Bell RD, Johnson B, Hamm K, Pendu R, Marky A, Lenting PJ, Wu Z, Zarcone T, Goate A, Mayo K, Perlmutter D, Coma M, Zhong Z, Zlokovic BV (2007) Clearance of amyloid-beta by circulating lipoprotein receptors. Nat Med 13, 1029-1031. (Pubitemid 47517512)
85. Soffer D (2006) Cerebral amyloid angiopathy-a disease or age-related condition. Isr Med Assoc J 8, 803-806. (Pubitemid 44842652)
86. 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. (Pubitemid 351430402)
87. Okazaki H, Reagan TJ, Campbell RJ (1979) Clinicopathologic studies of primary cerebral amyloid angiopathy. Mayo Clin Proc 54, 22-31. (Pubitemid 9116377)
88. Vinters HV (1987) Cerebral amyloid angiopathy. A critical review. Stroke 18, 311-324. (Pubitemid 17059655)
89. Gray F, Dubas F, Roullet E, Escourolle R (1985) Leukoencephalopathy in diffuse hemorrhagic cerebral amyloid angiopathy. Ann Neurol 18, 54-59. (Pubitemid 15025414)