The βA4 amyloid peptide complexes to and enhances the uptake of β-very low density lipoproteins by the low density lipoprotein receptor-related protein and heparan sulfate proteoglycans pathway

Laboratory Investigation

Volumn 79, Issue 10, 1999, Pages 1271-1286

  Scharnagl, Hubert ^a,e   Tisljar, Ursula ^a   Winkler, Karl ^a   Hüttinger, Manfred ^b   Nauck, Matthias A ^a   Groß, Werner ^c   Wieland, Heinrich ^a   Ohm, Thomas G ^d   März, Winfried ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF VIENNA   (Austria)

^c GOETHE UNIVERSITY   (Germany)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 2 MACROGLOBULIN; AMYLOID BETA PROTEIN; AMYLOID PROTEIN; APOLIPOPROTEIN E; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; PROTEOHEPARAN SULFATE; VERY LOW DENSITY LIPOPROTEIN; LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; LIPOPROTEIN RECEPTOR-RELATED PROTEIN 6;

ARTICLE; CELL METABOLISM; CHO CELL; DEGENERATIVE DISEASE; ENDOCYTOSIS; FIBROBLAST; HIPPOCAMPUS; HUMAN; HUMAN CELL; INTERNALIZATION; PRIORITY JOURNAL; PROTEIN BINDING; SYNAPTOGENESIS; ANIMAL; ANIMAL FOOD; CELL CULTURE; CHEMISTRY; CHOLESTEROL INTAKE; CYTOLOGY; HAMSTER; METABOLISM; RABBIT; RAT; WISTAR RAT;

AMYLOID BETA-PROTEIN; ANIMAL FEED; ANIMALS; CELLS, CULTURED; CHO CELLS; CHOLESTEROL, DIETARY; CRICETINAE; FIBROBLASTS; HEPARAN SULFATE PROTEOGLYCANS; HIPPOCAMPUS; HUMANS; LIPOPROTEINS, VLDL; RABBITS; RATS; RATS, WISTAR; RECEPTORS, LDL;

EID: 0032590201     PISSN: 00236837     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (95)

1. Ali SM, Dunn E, Oostveen JA, Hall ED, and Carter DB (1996). Induction of apolipoprotein E mRNA in the hippocampus of the gerbil after transient global ischemia. Brain Res Mol Brain Res 38:37-44.
2. Argraves KM, Battey FD, MacCalman CD, McCrae KR, Gafvels M, Kozarsky KF, Chappell DA, Strauss JF III, and Strickland DK (1995). The very low density lipoprotein receptor mediates the cellular catabolism of lipoprotein lipase and urokinase-plasminogen activator inhibitor type I complexes. J Biol Chem 270:26550-26557.
3. 2-macroglobulin. J Cell Biol 110:1041-1048.
4. Beisiegel U, Weber W, lhrke G, Herz J, and Stanley KK (1989). The LDL-receptor-related protein, LRP, is an apolipoprotein E-binding protein. Nature 341:162-164.
5. Bellosta S, Nathan BP, Orth M, Dong LM, Mahley RW, and Pitas RE (1995). Stable expression and secretion of apolipoproteins E3 and E4 in mouse neuroblastoma cells produces differential effects on neurite outgrowth. J Biol Chem 270:27063-27071.
6. Biere AL, Ostaszewski B, Stimson ER, Hyman BT, Maggio JE, and Selkoe DJ (1996). Amyloid β-peptide is transported on lipoproteins and albumin in human plasma. J Biol Chem 271:32916-32922.
7. 2-macroglobulin receptor/low density lipoprotein receptor-related protein-dependent mechanism. J Biol Chem 270:6389-6395.
8. Boyles JK, Pitas RE, Wilson E, Mahley RW, and Taylor JM (1985). Apolipoprotein E associated with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system. J Clin Invest 76:1501-1513.
9. Brunden KR, Richter-Cook NJ, Chaturvedi N, and Frederickson RC (1993). pH-dependent binding of synthetic β-amyloid peptides to glycosaminoglycans. J Neurochem 61:2147-2154.
10. Bu G, Maksymovitch EA, Geuze H, and Schwartz AL (1994). Subcellular localization and endocytic function of low density lipoprotein receptor-related protein in human glioblastoma cells. J Biol Chem 269:29874-29882.
11. Bu G and Rennke S (1996). Receptor-associated protein is a folding chaperone for low density lipoprotein receptor-related protein. J Biol Chem 271:22218-22224.
12. 2-macroglobulin receptor is an hepatic receptor for tissue-type plasminogen activator. Proc Natl Acad Sci USA 89:7427-7431.
13. Buee L, Ding W, Anderson JP, Narindrasorasak S, Kisilevsky R, Boyle NJ, Robakis NK, Delacourte A, Greenberg B, and Fillit HM (1993a). Binding of vascular heparan sulfate proteoglycan to Alzheimer's amyloid precursor protein is mediated in part by the N-terminal region of A4 peptide. Brain Res 627:199-204.
14. Buee L, Ding W, Delacourte A, and Fillit H (1993b). Binding of secreted human neuroblastoma proteoglycans to the Alzheimer's amyloid A4 peptide. Brain Res 601:154-163.
15. Cai XD, Golde TE, and Younkin SG (1993). Release of excess amyloid β protein from a mutant amyloid β protein precursor. Science 259:514-516.
16. Castaño EM, Prelli F, Wisniewski T, Golabek A, Kumar RA, Soto C, and Frangione B (1995). Fibrillogenesis in Alzheimer's disease of amyloid β peptides and apolipoprotein E. Biochem J 306:599-604.
17. Chan W, Fornwald J, Brawner M, and Wetzel R (1996). Native complex formation between apolipoprotein E isoforms and the Alzheimer's disease peptide A beta. Biochemistry 35: 7123-7130.
18. Chen H, Sottile J, Strickland DK, and Mosher DF (1996a). Binding and degradation of thrombospondin-1 mediated through heparan sulphate proteoglycans and low-density-lipoprotein receptor-related protein: Localization of the functional activity to the trimeric N-terminal heparin-binding region of thrombospondin-1. Biochem J 318:959-963.
19. Chen H, Strickland DK, and Mosher DF (1996b). Metabolism of thrombospondin 2: Binding and degradation by 3T3 cells and glycosaminoglycan-variant Chinese hamster ovary cells. J Biol Chem 271:15993-15999.
20. Citron M, Olterdorf T, Haass C, McConlogue L, Hung AY, Seubert P, Vigo-Pelfrey C, Lieberburg I, and Selkoe DJ (1992). Mutation of the β-amyloid precursor protein in familial Alzheimer's disease increases β-protein production. Nature 360:672-674.
21. de Knijff P, van den Maagdenberg AM, Frants RR, and Havekes LM (1994). Genetic heterogeneity of apolipoprotein E and its influence on plasma lipid and lipoprotein levels. Hum Mutat 4:178-194.
22. Elshourbagy NA, Liao WS, Mahley RW, and Taylor JM (1985). Apolipoprotein E mRNA is abundant in the brain and adrenals, as well as in the liver, and is present in other peripheral tissues of rats and marmosets. Proc Natl Acad Sci USA 82:203-207.
23. Esko JD, Rostand KS, and Weinke JL (1988). Tumor formation dependent on proteoglycan biosynthesis. Science 241: 1092-1096.
24. Esko JD, Stewart TE, and Taylor WH (1985). Animal cell mutants defective in glycosaminoglycan biosynthesis. Proc Natl Acad Sci USA 82:3197-3201.
25. Fagan AM, Bu G, Sun Y, Daugherty A, and Holtzman DM (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.
26. 212 → Lys): Increased binding to cell surface proteoglycans but decreased uptake and lysosomal degradation in cultured fibroblasts. J Lipid Res 37:1632-1645.
27. Gafvels ME, Paavola LG, Boyd CO, Nolan IM, Wittmaack F, Chawla A, Lazar MA, Bucan M, Angelin B, and Strauss JFI (1994). Cloning of a complementary deoxyribonucleic acid encoding the murine homolog of the very low density lipoprotein/apolipoprotein-E receptor: Expression pattern and assignment of the gene to mouse chromosome 19. Endocrinology 135:387-394.
28. Goldstein JL, Basu SK, and Brown MS (1983). Receptor-mediated endocytosis of low-density lipoprotein in cultured cells. Methods Enzymol 98:241-260.
29. Goldstein JL and Brown MS (1974). Binding and degradation of low density lipoproteins by cultured human fibroblasts: Comparison of cells from a normal subject and from a patient with homozygous familial hypercholesterolemia. J Biol Chem 249:5153-5162.
30. Gordon I, Grauer E, Genis I, Sehayek E, and Michaelson DM (1995). Memory deficits and cholinergic impairments in apolipoprotein E-deficient mice. Neurosci Lett 199:1-4.
31. Gretch DG, Sturley SL, Friesen PD, Beckage NE, and Attie AD (1991). Baculovirus-mediated expression of human apolipoprotein E in Manduca sexta larvae generates particles that bind to the low density lipoprotein receptor. Proc Natl Acad Sci USA 88:8530-8533.
32. Gupta-Bansal R, Frederickson RC, and Brunden KR (1995). Proteoglycan-mediated inhibition of Aβ proteolysis: A potential cause of senile plaque accumulation. J Biol Chem 270: 18666-18671.
33. Haass C and Selkoe DJ (1993). Cellular processing of β-amyloid precursor protein and the genesis of amyloid β-peptide. Cell 75:1039-1042.
34. 2-macroglobulin receptor. J Biol Chem 266:21232-21238.
35. Herz J, Hamann U, Rogne S, Myklebost O, Gausepohl H, and Stanley KK (1988). Surface location and high affinity for calcium of a 500-kd liver membrane protein closely related to the LDL-receptor suggest a physiological role as lipoprotein receptor. EMBO J 7:4119-4127.
36. Herz J, Kowal RC, Ho JK, Brown MS, and Goldstein JL (1990). Low density lipoprotein receptor-related protein mediates endocytosis of monoclonal antibodies in cultured cells and rabbit liver. J Biol Chem 265:21355-21362.
37. Hjalm G, Murray E, Crumley G, Harazim W, Lundgren S, Onyango I., Ek B, Larsson M, Juhlin C, Hellman P, Davis H, Akerstrom G, Rask L, and Morse B (1996). Cloning and sequencing of human gp330, a Ca(2+)-binding receptor with potential intracellular signaling properties. Eur J Biochem 239:132-137.
38. Holtzman DM, Pitas RE, Kilbridge J, Nathan B, Mahley RW, Bu G, and Schwartz AL (1995). Low density lipoprotein receptor-related protein mediates apolipoprotein E-dependent neurite outgrowth in a central nervous system-derived neuronal cell line. Proc Natl Acad Sci USA 92:9480-9484.
39. Horn IR, Moestrup SK, van den Berg BM, Pannekoek H, Nielsen MS, and Zonneveld AJ (1995). Analysis of the binding of pro-urokinase and urokinase-plasminogen activator inhibitor-1 complex to the low density lipoprotein receptor-related protein using a Fab fragment selected from a phage-displayed Fab library. J Biol Chem 270:11770-11775.
40. 2-macroglobulin receptor. J Biol Chem 266:13936-13940.
41. Ida N, Masters CL, and Beyreuther K (1996). Rapid cellular uptake of Alzheimer amyloid βA4 peptide by cultured human neuroblastoma cells. FEBS Lett 39:4174-4178.
42. Ignatius MJ, Gebicke-Haerter PJ, Skene JHP, Schilling JW, Weisgraber KH, Mahley RW, and Shooter EM (1986). Expression of apolipoprotein E during nerve degeneration and regeneration. Proc Natl Acad Sci USA 83:1125-1129.
43. Jacobsen L, Madsen P, Moestrup SK, Lund AH, Tommerup N, Nykjaer A, Sottrup-Jensen L, Gliemann J, and Petersen CM (1996). Molecular characterization of a novel human hybrid-type receptor that binds the alpha2-macroglobulin receptor-associated protein. J Biol Chem 271:31379-31383.
44. Ji ZS, Brecht WJ, Miranda RD, Hussain MM, lnnerarity TL, and Mahley RW (1993). Role of heparan sulfate proteoglycans in the binding and uptake of apolipoprotein E-enriched remnant lipoproteins by cultured cells. J Biol Chem 268: 10160-10167.
45. Ji ZS and Mahley RW (1994). Lactoferrin binding to heparan sulfate proteoglycans and the LDL receptor-related protein: Further evidence supporting the importance of direct binding of remnant lipoproteins to HSPG. Arterioscler Thromb 14: 2025-2031.
46. Ji ZS, Fazio S, and Mahley RW (1994a). Variable heparan sulfate proteoglycan binding of apolipoprotein variants may modulate the expression of type III hyperlipoproteinemia. J Biol Chem 269:13421-13428.
47. Ji ZS, Fazio S, Lee YL, and Mahley RW (1994b). Secretion-capture role for apolipoprotein E in remnant lipoprotein metabolism involving cell surface heparan sulfate proteoglycans. J Biol Chem 269:2764-2772.
48. Kim DH, Iijima H, Goto K, Sakai J, Ishii H, Kün HJ, Suzuki H, Kondo H, Saeki S, and Yamamoto T (1996). Human apolipoprotein E receptor 2. J Biol Chem 271:8373-8380.
49. Koudinov A, Matsubra E, Frangione B, and Ghiso J (1994). The soluble form of Alzheimer's amyloid beta protein is complexed to high density lipoprotein 3 and very high density lipoprotein in normal human plasma. Biochem Biophys Res Commun 205:1164-1171.
50. Koudinov AR, Koudinova NV, Kumar A, Beavis RC, and 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 223:592-597.
51. 2-macroglobulin receptor and glycoprotein 330. J Biol Chem 267:21162-21166.
52. Kounnas MZ, Chappell DA, Wong H, Argraves WS, and Strickland DK (1995a). The cellular internalization and degradation of hepatic lipase is mediated by low density lipoprotein receptor-related protein and requires cell surface proteoglycans. J Biol Chem 270:9307-9312.
53. 1-antitrypsin-trypsin complexes is mediated by the low density lipoprotein receptor-related protein. J Biol Chem 271:6523-6529.
54. Kounnas MZ, Moir RD, Rebeck GW, Bush AI, Argraves WS, Tanzi RE, Hyman BT, and Strickland DK (1995b). LDL receptor-related protein, a multifunctional ApoE receptor, binds secreted β-amyloid precursor protein and mediates its degradation. Cell 82:331-340.
55. Kovanen PT, Brown MS, Basu SK, Bilheimer DW, and Goldstein JL (1981). Saturation and suppression of hepatic lipoprotein receptors: A mechanism for the hypercholesterolemia of cholesterol-fed rabbits. Proc Natl Acad Sci USA 78:1396-1400.
56. Kowal RC, Herz J, Goldstein JL, Esser V, and Brown MS (1989). Low density lipoprotein receptor-related protein mediates uptake of cholesteryl esters derived from apoprotein E-enriched lipoproteins. Proc Natl Acad Sci USA 86:5810-5814.
57. Kowal RC, Herz J, Weisgraber KH, Mahley RW, Brown MS, and Goldstein JL (1990). Opposing effects of apolipoprotein E and C on lipoprotein binding to low density lipoprotein receptor-related protein. J Biol Chem 265:10771-10779.
58. 2-macroglobulin receptor. FEBS Lett 276:151-155.
59. Laemmli UK (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
60. Lund H, Takahashi K, Hamilton RL, and Havel RJ (1989). Lipoprotein binding and endosomal itinerary of the low density lipoprotein receptor-related protein in rat liver. Proc Natl Acad Sci USA 86:9318-9322.
61. Mahley RW (1988). Apolipoprotein E: Cholesterol transport protein with expanding role in cell biology. Science 240:622-630.
62. Mahley RW, Nathan BP, Bellosta S, and Pitas RE (1995). Apolipoprotein E: Impact of cytoskeletal stability in neurons and the relationship to Alzheimer's disease. Curr Opin Lipidol 6:86-91.
63. März W, Baumstark MW, Scharnagl H, Ruzicka V, Buxbaum S, Herwig J, Pohl T, Russ A, Schaaf L, Berg A, Böhles HJ, Usadel KH, and Groß W (1993). Accumulation of "small dense" low density lipoproteins (LDL) in a homozygous patient with familial defective apolipoprotein B-100 results from heterogeneous interaction of LDL subfractions with the LDL receptor. J Clin Invest 92:2922-2933.
64. Masliah E, Mallory M, Ge N, Alford M, Veinbergs I, and Roses AD (1995). Neurodegeneration in the central nervous system of apoE-deficient mice. Exp Neurol 136:107-122.
65. 2-macroglobulin receptor and transport to endosomes. FEBS Lett 360:70-74.
66. Namba Y, Tomonaga M, Kawasaki H, Otomo E, and 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 541:163-166.
67. Nathan BP, Bellosta S, Sanan DA, Weisgraber KH, Mahley RW, and Pitas RE (1994). Differential effects of apolipoprotein E3 and E4 on neuronal growth in vitro. Science 264:850-852.
68. Nathan BP, Chang KC, Bellosta S, Brisch E, Ge N, Mahley RW, and Pitas RE (1995). The inhibitory effect of apolipoprotein E4 on neurite outgrowth is associated with microtubule depolymerization. J Biol Chem 270:19791-19799.
69. 2-macroglobulin receptor/low density lipoprotein receptor-related protein. J Biol Chem 271:12909-12912.
70. 2-macroglobulin receptor/low density lipoprotein receptor-related protein: Evidence that lipoprotein lipase and the carboxyl-terminal domain of the receptor-associated protein bind to the same site. J Biol Chem 270:23713-23719.
71. Noorman F, Braat EA, and Rijken DC (1995). Degradation of tissue-type plasminogen activator by human monocyte-derived macrophages is mediated by the mannose receptor and by the low-density lipoprotein receptor-related protein. Blood 86:3421-3427.
72. Ohm TG, Kirca M, Bohl J, Scharnagl H, Groß W, and März W (1995). Apolipoprotein E polymorphism influences not only cerebral senile plaque load but also Alzheimer-type neurofibrillary tangle formation. Neuroscience 66:583-587.
73. 2-macroglobulin receptor. Proc Natl Acad Sci USA 89:7422-7426.
74. Pitas RE, Boyles JK, Lee SH, Foss D, and Mahley RW (1987a). Astrocytes synthesize apolipoprotein E and metabolize apolipoprotein E-containing lipoproteins. Biochim Biophys Acta 917:148-161.
75. Pitas RE, Boyles JK, Lee SH, Hui D, and Weisgraber KH (1987b). Lipoproteins and their receptors in the central nervous system: Characterization of the lipoproteins in cerebrospinal fluid and the identification of apolipoprotein B, E(LDL) receptors in the brain. J Biol Chem 262:14352-14360.
76. Sanan DA, Weisgraber KH, Russel SJ, Mahley RW, Huang D, Saunders A, Schmechel D, Wisniewski T, Frangione B, Roses AD, and Strittmatter WJ (1994). Apolipoprotein E associates with β-amyloid peptide of Alzheimer's disease to form novel monofibrils: Isoform apoE4 associates more efficiently than apoE3. J Clin Invest 94:860-869.
77. Selkoe DJ (1997). Alzheimer's disease: Genotypes, phenotypes, and treatments. Sciene 275:630-631.
78. Snow AD, Kinsella MG, Parks E, Sekiguchi RT, Miller JD, and Wight TN (1995). Differential binding of vascular cell-derived proteoglycans (perlecan, byglycan, decorin, and versican) to the beta-amyloid protein of Alzheimer's disease. Arch Biochem Biophys 320:84-95.
79. Stefansson S, Lawrence DA, and Argraves WS (1996). Plasminogen activator inhibitor-1 and vitronectin promote the cellular clearance of thrombin by low density lipoprotein receptor-related proteins 1 and 2. J Biol Chem 271:8215-8220.
80. 2-macroglobulin receptor and low density lipoprotein receptor-related protein suggests that this molecule is a multifunctional receptor. J Biol Chem 265:17401-17404.
81. Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J, Salvesan GS, and Roses AD (1993a). Apolipoprotein E: High-avidity binding to β-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc Natl Acad Sci USA 90:1977-1981.
82. Strittmatter WJ, Weisgraber KH, Huang DY, Dong LM, Salvesen GS, Pericak-Vance M, Schmechel D, Saunders AM, Goldgaber D, and Roses AD (1993b). Binding of human apolipoprotein E to synthetic amyloid β peptide: Isoform-specific effects and implications for late-onset Alzheimer disease. Proc Natl Acad Sci USA 90:8098-8102.
83. Talafous J, Marcinowski KJ, Klopman G, and Zagorski MG (1994). Solution structure of residues 1-28 of the amyloid β-peptide. Biochemistry 33:7788-7796.
84. Urmoneit B, Prikulis I, Wihl G, D'Urso D, Frank R, Heeren J, Beisiegel U, and 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.
85. Vassiliou G and Stanley KK (1994). Exogenous receptor-associated protein binds to two distinct sites on human fibroblasts but does not bind to the glycosaminoglycan residues of heparan sulfate proteoglycans. J Biol Chem 269:15172-15178.
86. Warshawsky I, Herz J, Broze GJ Jr, and Schwartz AL (1996). The low density lipoprotein receptor-related protein can function independently from heparan sulfate proteoglycans in tissue factor pathway inhibitor endocytosis. J Biol Chem 271:25873-25879.
87. Willnow TE, Armstrong SA, Hammer RE, and Herz J (1995). Functional expression of low density lipoprotein receptor-related protein is controlled by receptor-associated protein in vivo. Proc Natl Acad Sci USA 92:4537-4541.
88. Willnow TE, Goldstein JL, Orth K, Brown MS, and Herz J (1992). Low density lipoprotein receptor-related protein and gp330 bind similar ligands, including plasminogen activator-inhibitor complexes and lactoferrin, an inhibitor of chylomicron remnant clearance. J Biol Chem 267:26172-26180.
89. Willnow TE and Herz J (1994). Genetic deficiency in low density lipoprotein receptor-related protein confers cellular resistance to Pseudomonas exotoxin A: Evidence that this protein is required for uptake and degradation of multiple ligands. J Cell Sci 107:719-726.
90. Willnow TE, Rohlmann A, Horton J, Otani H, Braun JR, Hammer RE, and Herz J (1996). RAP, a specialized chaperone, prevents ligand-induced ER retention and degradation of LDL receptor-related endocytic receptors. EMBO J 15: 2632-2639.
91. Winkler K, Scharnagl H, Tisljar U, Hoschützky H, Friedrich I, Hoffmann MM, Huttinger M, Wieland H, and März W (1999). Competition of Aβ amyloid peptide and apolipoprotein E for receptor-mediated endocytosis. J Lipid Res 40:447-455.
92. Wisniewski T, Golabek A, Matsubra E, Ghiso J, and Frangione B (1993). Apolipoprotein E: Binding to soluble Alzheimer's β-amyloid. Biochem Biophys Res Commun 192:359-362.
93. Yamazaki H, Bujo H, Kusonoki J, Seirniya K, Kanaki T, Morisaki N, Schneider WJ, and Saito Y (1996). Elements of neural adhesion molecules and a yeast vacuolar protein sorting receptor are present in a novel mammalian low density lipoprotein receptor family member. J Biol Chem 271:25761-25768.
94. Yang DS, Smith JD, Zhou Z, Gandy SE, and 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 68:721-725.
95. Zhou Z, Smith JD, Greengard P, and Gandy S (1996). Alzheimer amyloid-β peptide forms denaturant-resistant complex with type epsilon 3 but not type epsilon 4 isoforms of native apolipoprotein E. Mol Med 2:175-180