Lipidation of apolipoprotein E influences its isoform-specific interaction with Alzheimer's amyloid β peptides

Biochemical Journal

Volumn 348, Issue 2, 2000, Pages 359-365

  Tokuda, Takahiko ^a   Calero, Miguel ^a   Matsubara, Etsuro ^b   Vidal, Ruben ^a   Kumar, Asok ^a   Permanne, Bruno ^a   Zlokovic, Berislav ^c   Smith, Jonathan D ^d   Ladu, Mary Jo ^e   Rostagno, Agueda ^a   Frangione, Blas ^a   Ghiso, Jorge ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GUNMA UNIVERSITY   (Japan)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

^e ENH Research Institute   (United States)

Author keywords

A ; ApoE isoform; Dissociation constant; HDL; Lipid

Indexed keywords

AMYLOID BETA PROTEIN; APOLIPOPROTEIN E; HIGH DENSITY LIPOPROTEIN; ISOPROTEIN; LIPOSOME;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; BACULOVIRUS; DISSOCIATION CONSTANT; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING;

AMYLOID BETA-PROTEIN; ANIMALS; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; APOLIPOPROTEINS E; CELL LINE; HUMANS; KIDNEY; KINETICS; MACROPHAGES; MICE; PROTEIN ISOFORMS; SPODOPTERA; TRANSFECTION;

ANIMALIA; UNIDENTIFIED BACULOVIRUS;

EID: 0034214329     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/0264-6021:3480359     Document Type: Article

References (48)

1. 1 Wisniewski, T., Ghiso, J. and Frangione, B. (1997) Biology of Aβ amyloid in Alzheimer's disease. Neurobiol. Dis. 4, 313-328
2. 2 Seubert, P., Vigo-Pelfrey, C., Esch, F., Lee, M., Dovey, H., Davis, D., Sinha, S., Schiossmacher, M., Whaley, J., Swindlehurst, C. et al. (1992) Isolation and quantification of soluble Alzheimer's β-peptide from biological fluids. Nature (London) 359, 325-327
3. 3 Shoji, M., Golde, T. E., Ghiso, J., Cheung, T. T., Estus, S., Shaffer, L. M., Cai, X. D., McKay, D. M., Tintner, R., Frangione, B. and Younkin, S. G. (1992) Production of the Alzheimer amyloid β protein by normal proteolytic processing. Science 258, 126-129
4. 4 Vigo-Pelfrey, C., Lee, D., Keim, P., Lieberburg, I. and Schenk, D. B. (1993) Characterization of β-amyloid peptide from human cerebrospinal fluid. J. Neurochem. 61, 1965-1968
5. 5 Ghiso, J., Calero, M., Matsubara, E., Governale, S., Chuba, J., Beavis, R., Wisniewski, T. and Frangione, B. (1997) Alzheimer's soluble amyloid β is a normal component of human urine. FEBS Lett. 408, 105-108
6. 6 Naslund, J., Schierhorn, A., Hellman, U., Lannfelt, L., Roses, A. D., Tjernberg, L. O., Silberring, J., Gandy, S. E., Winblad, B., Greengard, P. et al. (1994) Relative abundance of Alzheimer Aβ amyloid peptide variants in Alzheimer disease and normal aging. Proc. Natl. Acad. Sci. U.S.A. 91, 8378-8382
7. 7 Tabaton, M., Nunzi, M. G., Xue. R., Usiak, M., Autilio-Gambetti, L. and Gambetti, P. (1994) Soluble amyloid β-protein is a marker of Alzheimer amyloid in brain but not in cerebrospinal fluid. Biochem. Biophys. Res. Commun. 200, 1598-1603
8. 8 Teller, J. K., Russo, C., DeBusk, L. M., Angelini, G., Zaccheo, D., Dagna-Bricarelli, F., Scartezzini, S., Bertolini, S., Mann, D. M. A., Tabaton, M. and Gambetti, P. (1996) Presence of soluble amyloid β-peptide precedes amyloid plaque formation in Down's syndrome. Nat. Med. 2, 93-95
9. 9 Oda, T., Wals, P., Osterburg, H. H., Johnson, S. A., Pasinetti, G. M., Morgan, T. E., Rozovsky, I., Stine, W. B., Snyder, S. W., Holzman, T. F. et al. (1995) Clusterin (apoJ) alters the aggregation of amyloid β-peptide (Aβ 1-42) and forms slowly sedimenting Aβ complexes that cause oxidative stress. Exp. Neurol. 136, 22-31
10. 10 Wujek, J. R., Dority, M. D., Frederickson, R. C. and Brunden, K. R. (1996) Deposits of Aβ fibrils are not toxic to cortical and hippocampal neurons in vitro. Neurobiol. Aging 17, 107-113
11. 11 Lambert, M. P., Barlow, A. K., Chromy, B. A., Edwards, C., Freed, R., Liosatos, M., Morgan, T. E., Rozovsky, I., Trommer, B., Viola, K. L. et al. (1998) Diffusible, nonfibrillar ligands derived from Aβ1 -42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U.S.A. 95, 6448-6453
12. 12 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
13. 13 Wisniewski, T. and Frangione, B. (1992) Apolipoprotein E: a pathological chaperone protein in patients with cerebral and systemic amyloid. Neurosci. Lett. 135, 235-238
14. 14 Naslund, J., Thyberg, J , Tjernberg, L. O., Wernstedt, C., Karlstrom, A. R., Bogdanovic, N., Gandy, S. E., Lannfelt, L., Terenius, L. and Nordstedt, C. (1995) Characterization of stable complexes involving apolipoprotein E and the amyloid β peptide in Alzheimer's disease brain. Neuron 15, 219-228
15. 15 Wisniewski, T., Lalowski, M., Golabek, A., Vogel, T. and Frangione, B. (1995) Is Alzheimer's disease an apolipoprotein E amyloidosis? Lancet 345, 956-958
16. 16 Zannis, V. I. and Breslow, J. L. (1981) Human very low density lipoprotein apolipoprotein E isoprotein polymorphism is explained by genetic variation and posttranslational modification. Biochemistry 20, 1033-1041
17. 17 Saunders, A. M., Strittmatter, W. J , Schmechel, D., George-Hyslop, P. H., Pericak-Vance, M. A., Joo, S. H., Rosi, B. L., Gusella, J. F., Crapper-MacLachlan, D. R., Alberts, M. J. et al. (1993) Association of apolipoprotein E allele ε4 with late-onset familial and sporadic Alzheimer's disease. Neurology 43, 1467-1472
18. 18 Strittmatter, W. J., Saunders, A. M., Schmechel, D., Pericak-Vance, M., Enghild, J., Salvesen, G. S. and Roses, A. D. (1993) 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. U.S.A. 90, 1977-1981
19. 19 Corder, E. H., Saunders, A. M., Strittmatter, W. J., Schmechel, D. E., Gaskell, P. C., Small, G. W., Roses, A. D., Haines, J. L. and Pericak-Vance, M. A. (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261, 921-923
20. 20 Rebeck, G. W., Reiter, J. S., Strickland, D. K. and Hyman, B. T. (1993) Apolipoprotein E in sporadic Alzheimer's disease: allelic variation and receptor interactions. Neuron 11, 575-580
21. 21 Schmechel, D. E., Saunders, A. M., Strittmatter, W. J., Crain, B. J., Hulette, C. M., Joo, S. H., Pericak-Vance, M. A., Goldgaber, D. and Roses, A. D. (1993) Increased amyloid β-peptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late-onset Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 90, 9649-9653
22. 22 Strittmatter, W. J., Weisgraber, K. H., Huang, D. Y., Dong, L.-M., Salvesen, G. S., Pericak-Vance, M., Schmechel, D., Saunders, A. M., Goldgaber, D. and Roses, A. D. (1993) Binding of human apolipoprotein E to synthetic amyloid β peptide: isoform-specific effects and implications for late-onset Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 90, 8098-8102
23. 23 Wisniewski, T., Golabek, A., Matsubara, E., Ghiso, J. and Frangione, B. (1993)) Apolipoprotein E: binding to soluble Alzheimer's β-amyloid. Biochem. Biophys. Res. Commun. 192, 359-365
24. 24 LaDu, M. J., Falduto, M. T., Manelli, A. M., Reardon, C. A., Getz, G. S. and Frail, D. E. (1994) Isoform-specific binding of apolipoprotein E to β-amyloid. J. Biol. Chem. 269, 23403-23406
25. 25 LaDu, M. J., Pederson, T. M., Frail, D. E., Reardon, C. A., Getz, G. S. and Falduto, M. T. (1995) Purification of apolipoprotein E attenuates isoform-specific binding to β-amyloid. J. Biol. Chem. 270, 9039-9042
26. 26 Zhou, Z., Smith, J. D., Greengard, P. and Gandy, S. (1996) Alzheimer amyloid-β peptide forms denaturant-resistant complex with type ε3 but not type ε4 isoform of native apolipoprotein E. Mol. Med. 2, 175-180
27. 27 LaDu, M. J., Lukens, J. R., Reardon, C. A. and Getz, G. S. (1997) Association of human, rat, and rabbit apolipoprotein E with β-amyloid. J. Neurosci. Res. 49, 9-18
28. 28 Aleshkov, S., Abraham, C. R. and Zannis, V. I. (1997) Interaction of nascent ApoE2, ApoES, and ApoE4 isoforms expressed in mammalian cells with amyloid peptide β (1-40). Relevance to Alzheimer's disease. Biochemistry 36, 10571-10580
29. 29 Smith, J. D., Melian, A., Left, T. and Breslow, J. (1988) Expression of the human apolipoprotein E gene is regulated by multiple positive and negative elements. J. Biol Chem. 263, 8300-8308
30. 30 Miyata, M. and Smith, J. D. (1996) Apolipoprotein E allele-specific antioxidant activity and effects on cytotoxicity by oxidative insults and beta-amyloid peptides. Nat. Genet. 14, 55-61
31. 31 LaDu, M. J., Gilligan, S. M., Lukens, J. R., Cabana, V. G., Reardon, C. A., Van Eldik, L. J. and Holtzman, D. M. (1998) Nascent astrocyte particles differ from lipoproteins in CSF. J. Neurochem. 70, 2070-2081
32. 32 Osborne, J. R. (1986) Delipidation of plasma lipoproteins. Methods Enzymol. 128, 213-222
33. 33 Koudinov, A., Matsubara, E., Frangione, B. and Ghiso, J. (1994) The soluble form of Alzheimer's amyloid β protein is complexed to high density lipoprotein 3 and very high density lipoprotein in normal human plasma. Biochem. Biophys. Res. Commun. 205, 1164-1171
34. 34 Matz, C. E. and Jonas, A. (1982) Micellar complexes of human apolipoprotein A-1 with phosphatidylcholines and cholesterol prepared from cholate-lipid dispersions. J. Biol. Chem. 257, 4535-4540
35. 35 Forte, T. M. and Nordhausen, R. W. (1986) Electron microscopy of negatively stained lipoproteins. Methods Enzymol. 128, 442-457
36. 36 Calero, M., Tokuda, T., Rostagno, A., Kumar, A., Zlokovic, B., Frangione, B. and Ghiso, J. (1999) Functional and structural properties of lipid-associated apolipoprotein J (clusterin). Biochem. J. 344, 375-383
37. 37 Chacko, G. K., Mahlberg, F. H. and Johnson, W. J. (1988) Cross-linking of apoproteins in high density lipoprotein by dimethylsuberimidate inhibits specific lipoprotein binding to membranes. J. Lipid. Res. 29, 319-324
38. 38 Matsubara, E., Frangione, B. and Ghiso, J. (1995) Characterization of apolipoprotein J-Alzheimer's A beta interaction. J. Biol. Chem. 270, 7563-7567
39. 39 Yokoyama, S., Kawai, Y., Tajima, S. and Yamamoto, A. (1985) Behavior of human apolipoprotein E in aqueous solutions and at interfaces. J. Biol. Chem 260, 16375-16382
40. 40 Yokoyama, S. (1990) Self-associated tetramer of human apolipoprotein E does not lead to its accumulation on a lipid particle. Biochim. Biophys. Acta 1047, 99-101
41. 41 Aleskov, S. B., Lavrentiadou, Z. N. and Zannis, V. I. (1999) Contribution of Cysteine 158, the glycosylation site Threonine 194, the amino-and carboxy-terminal domains of apolipoprotein E in the binding to amyloid peptide β (1-40). Biochemistry 38, 8918-8925
42. 42 Pitas, R. E., Boyles, J. K., Lee, S. H., Foss, D. and Mahley, R. W. (1987) Astrocytes synthesize apolipoprotein E and metabolize apolipoprotein E-containing lipoproteins. Biochim. Biophys. Acta 917, 148-161
43. 43 Poirier, J., Hess, M., May, P. C. and Finch, C. E. (1991) Astrocytic apolipoprotein E mRNA and GFAP mRNA in hippocampus after entorhinal cortex lesioning. Mol. Brain Res. 11, 97-106
44. 44 Rebeck, G. W. and Hyman, B. T. (1999) Lipoprotein receptors in brain. In Clusterin in Normal Brain Functions and during Neurodegeneration (Finch, C. E., ed.), pp. 49-59, R. G. Landes Co., Austin
45. 45 Innerarity, T. L., Pitas, E. and Mahley, R. W. (1979) Binding of arginine-rich (E) apoprotein after recombination with phospholipid vesicles to the low density lipoprotein receptors of fibroblasts. J. Biol. Chem. 254, 4186-4190
46. 46 Nathan, B. P., Bellosta, S., Sanan, D. A., Weisgraber, K. H., Mahley, R. W. and Pitas, R. E. (1994). Differential effects of apolipoproteins E3 and E4 on neuronal growth in vitro. Science 264, 850-852
47. 47 Bales, K. R., Verina, T., Dodel, R. C., Du, Y., Alstiel, L., Bender, M., Hyslop, P., Johnstone, E. M., Little, S. P., Cummins, D. J. et al. (1997) Lack of apolipoprotein E dramatically reduces amyloid beta-peptide deposition. Nat. Genet. 17, 263-264
48. 48 Holtzman, D. M., Bales, K. R., Wu, S., Priyanka, B., Parsadanian, M., Fagan, A. M., Chang, L. K., Sun, Y. and Paul, S. M. (1999) Expression of human apolipoprotein E reduces amyloid-beta deposition in a mouse model of Alzheimer's disease. J. Clin. Invest. 103, R15-R21