ApoE influences amyloid-β (Aβ) clearance despite minimal apoE/Aβ association in physiological conditions

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 19, 2013, Pages

  Verghese, Philip B ^a   Castellano, Joseph M ^a   Garai, Kanchan ^a   Wang, Yinong ^a   Jiang, Hong ^a   Shah, Aarti ^a   Bu, Guojun ^b   Frieden, Carl ^a   Holtzman, David M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

Cholesterol efflux; Neurodegeneration

Indexed keywords

AMYLOID BETA PROTEIN; APOLIPOPROTEIN E; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN;

ARTICLE; ASTROCYTE; CEREBROSPINAL FLUID; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN METABOLISM;

CHOLESTEROL EFFLUX; NEURODEGENERATION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; APOLIPOPROTEINS E; BRAIN; CELL LINE; CHOLESTEROL; GENE EXPRESSION REGULATION; HUMANS; MICE; MICE, KNOCKOUT; NEURODEGENERATIVE DISEASES; PROTEIN BINDING; PROTEIN ISOFORMS; TIME FACTORS;

EID: 84877326649     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1220484110     Document Type: Article

References (76)

1. Morris JC (1997) Clinical assessment of Alzheimer's disease. Neurology 49(3, Suppl 3): S7-S10.
2. Selkoe DJ (2002) Alzheimer's disease is a synaptic failure. Science 298(5594): 789-791.
3. Holtzman DM, Morris JC, Goate AM (2011) Alzheimer's disease: The challenge of the second century. Sci Transl Med 3(77):sr1.
4. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297(5580): 353-356.
5. Karran E, Mercken M, De Strooper B (2011) The amyloid cascade hypothesis for Alzheimer's disease: An appraisal for the development of therapeutics. Nat Rev Drug Discov 10(9): 698-712.
6. Golde TE, Dickson D, Hutton M (2006) Filling the gaps in the abeta cascade hypothesis of Alzheimer's disease. Curr Alzheimer Res 3(5): 421-430.
7. Tanzi RE, Bertram L (2005) Twenty years of the Alzheimer's disease amyloid hypothesis: A genetic perspective. Cell 120(4): 545-555.
8. Mahley RW, Rall SC, Jr. (2000) Apolipoprotein E: Far more than a lipid transport protein. Annu Rev Genomics Hum Genet 1: 507-537.
9. Corder EH, et al. (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261(5123): 921-923.
10. Strittmatter WJ, et al. (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 USA 90(5): 1977-1981.
11. Saunders AM, et al. (1993) Apolipoprotein E epsilon 4 allele distributions in late-onset Alzheimer's disease and in other amyloid-forming diseases. Lancet 342(8873): 710-711.
12. Verghese PB, Castellano JM, Holtzman DM (2011) Apolipoprotein E in Alzheimer's disease and other neurological disorders. Lancet Neurol 10(3): 241-252.
13. Kim J, Basak JM, Holtzman DM (2009) The role of apolipoprotein E in Alzheimer's disease. Neuron 63(3): 287-303.
14. Ma J, Yee A, Brewer HB, Jr., Das S, Potter H (1994) Amyloid-associated proteins alpha 1-antichymotrypsin and apolipoprotein E promote assembly of Alzheimer betaprotein into filaments. Nature 372(6501): 92-94.
15. Castano EM, et al. (1995) Fibrillogenesis in Alzheimer's disease of amyloid beta peptides and apolipoprotein E. Biochem J 306(Pt 2): 599-604.
16. Bales KR, et al. (1997) Lack of apolipoprotein E dramatically reduces amyloid betapeptide deposition. Nat Genet 17(3): 263-264.
17. Bales KR, et al. (1999) Apolipoprotein E is essential for amyloid deposition in the APP (V717F) transgenic mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 96(26): 15233-15238.
18. Holtzman DM, et al. (2000) Apolipoprotein E isoform-dependent amyloid deposition and neuritic degeneration in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 97(6): 2892-2897.
19. Schmechel DE, et al. (1993) Increased amyloid beta-peptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late-onset Alzheimer disease. Proc Natl Acad Sci USA 90(20): 9649-9653.
20. Rebeck GW, Reiter JS, Strickland DK, Hyman BT (1993) Apolipoprotein E in sporadic Alzheimer's disease: Allelic variation and receptor interactions. Neuron 11(4): 575-580.
21. Castellano JM, et al. (2011) Human apoE isoforms differentially regulate brain amyloid-β peptide clearance. Sci Transl Med 3(89):89ra57.
22. Namba Y, Tomonaga M, Kawasaki H, Otomo E, Ikeda K (1991) Apolipoprotein E immunoreactivity in cerebral amyloid deposits and neurofibrillary tangles in Alzheimer's disease and kuru plaque amyloid in Creutzfeldt-Jakob disease. Brain Res 541(1): 163-166.
23. Wisniewski T, Frangione B (1992) Apolipoprotein E: A pathological chaperone protein in patients with cerebral and systemic amyloid. Neurosci Lett 135(2): 235-238.
24. Strittmatter WJ, et al. (1993) Binding of human apolipoprotein E to synthetic amyloid beta peptide: Isoform-specific effects and implications for late-onset Alzheimer disease. Proc Natl Acad Sci USA 90(17): 8098-8102.
25. LaDu MJ, et al. (1994) Isoform-specific binding of apolipoprotein E to beta-amyloid. J Biol Chem 269(38): 23403-23406.
26. LaDu MJ, et al. (2012) Preferential interactions between ApoE-containing lipoproteins and Aβ revealed by a detection method that combines size exclusion chromatography with non-reducing gel-shift. Biochim Biophys Acta 1821(2): 295-302.
27. Koudinov AR, Koudinova NV, Kumar A, Beavis RC, Ghiso J (1996) Biochemical characterization of Alzheimer's soluble amyloid beta protein in human cerebrospinal fluid: Association with high density lipoproteins. Biochem Biophys Res Commun 223(3): 592-597.
28. Petrlova J, et al. (2011) A differential association of Apolipoprotein E isoforms with the amyloid-β oligomer in solution. Proteins 79(2): 402-416.
29. Zhou Z, Smith JD, Greengard P, Gandy S (1996) Alzheimer amyloid-beta peptide forms denaturant-resistant complex with type epsilon 3 but not type epsilon 4 isoform of native apolipoprotein E. Mol Med 2(2): 175-180.
30. Sanan DA, et al. (1994) Apolipoprotein E associates with beta amyloid peptide of Alzheimer's disease to form novel monofibrils. Isoform apoE4 associates more efficiently than apoE3. J Clin Invest 94(2): 860-869.
31. Bentley NM, Ladu MJ, Rajan C, Getz GS, Reardon CA (2002) Apolipoprotein E structural requirements for the formation of SDS-stable complexes with betaamyloid- (1-40): The role of salt bridges. Biochem J 366(Pt 1): 273-279.
32. Chan W, Fornwald J, Brawner M, Wetzel R (1996) Native complex formation between apolipoprotein E isoforms and the Alzheimer's disease peptide A beta. Biochemistry 35(22): 7123-7130.
33. Yang DS, Smith JD, Zhou Z, Gandy SE, Martins RN (1997) Characterization of the binding of amyloid-beta peptide to cell culture-derived native apolipoprotein E2, E3, and E4 isoforms and to isoforms from human plasma. J Neurochem 68(2): 721-725.
34. Tokuda T, et al. (2000) Lipidation of apolipoprotein E influences its isoform-specific interaction with Alzheimer's amyloid beta peptides. Biochem J 348(Pt 2): 359-365.
35. Hayek T, Oiknine J, Brook JG, Aviram M (1994) Role of HDL apolipoprotein E in cellular cholesterol efflux: Studies in apo E knockout transgenic mice. Biochem Biophys Res Commun 205(2): 1072-1078.
36. Dietschy JM, Turley SD (2001) Cholesterol metabolism in the brain. Curr Opin Lipidol 12(2): 105-112.
37. De Strooper B (2007) Loss-of-function presenilin mutations in Alzheimer disease. Talking Point on the role of presenilin mutations in Alzheimer disease. EMBO Rep 8(2): 141-146.
38. Fagan AM, et al. (2009) Decreased cerebrospinal fluid Abeta(42) correlates with brain atrophy in cognitively normal elderly. Ann Neurol 65(2): 176-183.
39. Morikawa M, et al. (2005) Production and characterization of astrocyte-derived human apolipoprotein E isoforms from immortalized astrocytes and their interactions with amyloid-beta. Neurobiol Dis 19(1-2): 66-76.
40. DeMattos RB, et al. (2001) Purification and characterization of astrocyte-secreted apolipoprotein E and J-containing lipoproteins from wild-type and human apoE transgenic mice. Neurochem Int 39(5-6): 415-425.
41. Fagan AM, et al. (2000) Differences in the Abeta40/Abeta42 ratio associated with cerebrospinal fluid lipoproteins as a function of apolipoprotein E genotype. Ann Neurol 48(2): 201-210.
42. Rellin L, Heeren J, Beisiegel U (2008) Recycling of apolipoprotein E is not associated with cholesterol efflux in neuronal cells. Biochim Biophys Acta 1781(5): 232-238.
43. Cruchaga C, et al.; Alzheimer's Disease Neuroimaging Initiative (2012) Cerebrospinal fluid APOE levels: An endophenotype for genetic studies for Alzheimer's disease. Hum Mol Genet 21(20): 4558-4571.
44. Shankar GM, Welzel AT, McDonald JM, Selkoe DJ, Walsh DM (2011) Isolation of low-n amyloid β-protein oligomers from cultured cells, CSF, and brain. Methods Mol Biol 670: 33-44.
45. Tamamizu-Kato S, et al. (2008) Interaction with amyloid beta peptide compromises the lipid binding function of apolipoprotein E. Biochemistry 47(18): 5225-5234.
46. Magde D, Elson EL, Webb WW (1974) Fluorescence correlation spectroscopy. II. An experimental realization. Biopolymers 13(1): 29-61.
47. Basak JM, Verghese PB, Yoon H, Kim J, Holtzman DM (2012) Low-density lipoprotein receptor represents an apolipoprotein E-independent pathway of Aβ uptake and degradation by astrocytes. J Biol Chem 287(17): 13959-13971.
48. Wyss-Coray T, et al. (2003) Adult mouse astrocytes degrade amyloid-beta in vitro and in situ. Nat Med 9(4): 453-457.
49. Koistinaho M, et al. (2004) Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloid-beta peptides. Nat Med 10(7): 719-726.
50. Kanekiyo T, et al. (2011) Heparan sulphate proteoglycan and the low-density lipoprotein receptor-related protein 1 constitute major pathways for neuronal amyloid-beta uptake. J Neurosci 31(5): 1644-1651.
51. Sagare A, et al. (2007) Clearance of amyloid-beta by circulating lipoprotein receptors. Nat Med 13(9): 1029-1031.
52. Castellano JM, et al. (2012) Low-density lipoprotein receptor overexpression enhances the rate of brain-to-blood Aβ clearance in a mouse model of β-amyloidosis. Proc Natl Acad Sci USA 109(38): 15502-15507.
53. Deane R, Sagare A, Zlokovic BV (2008) The role of the cell surface LRP and soluble LRP in blood-brain barrier Abeta clearance in Alzheimer's disease. Curr Pharm Des 14(16): 1601-1605.
54. Katsouri L, Georgopoulos S (2011) Lack of LDL receptor enhances amyloid deposition and decreases glial response in an Alzheimer's disease mouse model. PLoS ONE 6(7): e21880.
55. Zhong N, Ramaswamy G, Weisgraber KH (2009) Apolipoprotein E4 domain interaction induces endoplasmic reticulum stress and impairs astrocyte function. J Biol Chem 284(40): 27273-27280.
56. Cash JG, et al. (2012) Apolipoprotein E4 impairs macrophage efferocytosis and potentiates apoptosis by accelerating endoplasmic reticulum stress. J Biol Chem 287(33): 27876-27884.
57. Cirrito JR, et al. (2003) In vivo assessment of brain interstitial fluid with microdialysis reveals plaque-associated changes in amyloid-beta metabolism and half-life. J Neurosci 23(26): 8844-8853.
58. Mawuenyega KG, et al. (2010) Decreased clearance of CNS beta-amyloid in Alzheimer's disease. Science 330(6012):1774.
59. Bateman RJ, et al. (2006) Human amyloid-beta synthesis and clearance rates as measured in cerebrospinal fluid in vivo. Nat Med 12(7): 856-861.
60. Biere AL, et al. (1996) Amyloid beta-peptide is transported on lipoproteins and albumin in human plasma. J Biol Chem 271(51): 32916-32922.
61. Takamura A, et al. (2011) Dissociation of β-amyloid from lipoprotein in cerebrospinal fluid from Alzheimer's disease accelerates β-amyloid-42 assembly. J Neurosci Res 89(6): 815-821.
62. Shuvaev VV, Siest G (1996) Interaction between human amphipathic apolipoproteins and amyloid beta-peptide: Surface plasmon resonance studies. FEBS Lett 383(1-2): 9-12.
63. Bell RD, 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(5): 909-918.
64. Deane R, et al. (2008) apoE isoform-specific disruption of amyloid beta peptide clearance from mouse brain. J Clin Invest 118(12): 4002-4013.
65. Iliff JJ, et al. (2012) A Paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci Transl Med 4(147):147ra111.
66. Kim J, et al. (2011) Haploinsufficiency of human APOE reduces amyloid deposition in a mouse model of amyloid-β amyloidosis. J Neurosci 31(49): 18007-18012.
67. Bien-Ly N, Gillespie AK, Walker D, Yoon SY, Huang Y (2012) Reducing human apolipoprotein E levels attenuates age-dependent Aβ accumulation in mutant human amyloid precursor protein transgenic mice. J Neurosci 32(14): 4803-4811.
68. Winkler K, et al. (1999) Competition of Abeta amyloid peptide and apolipoprotein E for receptor-mediated endocytosis. J Lipid Res 40(3): 447-455.
69. Ho YY, et al. (2000) Endogenously expressed apolipoprotein E has different effects on cell lipid metabolism as compared to exogenous apolipoprotein E carried on triglyceride-rich particles. Biochemistry 39(16): 4746-4754.
70. Chen Y, Durakoglugil MS, Xian X, Herz J (2010) ApoE4 reduces glutamate receptor function and synaptic plasticity by selectively impairing ApoE receptor recycling. Proc Natl Acad Sci USA 107(26): 12011-12016.
71. Heeren J, et al. (2004) Impaired recycling of apolipoprotein E4 is associated with intracellular cholesterol accumulation. J Biol Chem 279(53): 55483-55492.
72. Bu G (2009) Apolipoprotein E and its receptors in Alzheimer's disease: Pathways, pathogenesis and therapy. Nat Rev Neurosci 10(5): 333-344.
73. Deane R, et al. (2004) LRP/amyloid beta-peptide interaction mediates differential brain efflux of Abeta isoforms. Neuron 43(3): 333-344.
74. Bell RD, et al. (2009) SRF and myocardin regulate LRP-mediated amyloid-beta clearance in brain vascular cells. Nat Cell Biol 11(2): 143-153.
75. Kanekiyo T, Liu CC, Shinohara M, Li J, Bu G (2012) LRP1 in brain vascular smooth muscle cells mediates local clearance of Alzheimer's amyloid-β. J Neurosci 32(46): 16458-16465.
76. DeMattos RB, et al. (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(15): 8850-8855.