Home LiteratureArticle Details
PMID: 10816430 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

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

The Biochemical journal ·Vol. 348 Pt 2 ·2000-06-01 ·Pages 359-65

Tokuda T, Calero M, Matsubara E, Vidal R, Kumar A, Permanne B, Zlokovic B, Smith JD, Ladu MJ, Rostagno A, Frangione B, Ghiso J

Abstract

The inheritance of the apolipoprotein E (apoE) epsilon4 allele is a prevailing risk factor for sporadic and familial Alzheimer's disease (AD). ApoE isoforms bind directly to Alzheimer's amyloid beta (Abeta) peptides both in vitro and in vivo. Recent studies suggest that association of apoE with lipids may modulate its interaction with Abeta. We examined the binding of lipid-associated and delipidated apoE3 and apoE4 isoforms to Abeta utilizing a solid-phase binding assay and estimated the dissociation constants for the interaction of various apoE and Abeta species. Using native apoE isoforms from stably transfected RAW 264 and human embryonic kidney 293 cells, apoE3 had greater affinity than apoE4 for both Abeta1-40 and Abeta1-42. Delipidation of apoE decreased its affinity for Abeta peptides by 5-10-fold and abolished the isoform-specificity. Conversely, incorporation of apoE isoforms produced by baculovirus-infected Sf9 cells into reconstituted human high-density-lipoprotein lipoparticles restored the affinity values for Abeta peptides and resulted in preferential binding of apoE3. The data demonstrate that native lipid-associated apoE3 binds to Abeta peptides with 2-3-fold higher affinity than lipid-associated apoE4. Since the isoforms' binding efficiency correlate inversely with the risk of developing late-onset AD, the results suggest a possible involvement of apoE3 in the clearance or routing out of Abeta from the central nervous system as one of the mechanisms underlying the pathology of the disease.

MeSH Terms
Amyloid beta-Peptides/metabolism Animals Apolipoprotein E3 Apolipoprotein E4 Apolipoproteins E/metabolism Cell Line Humans Kidney Kinetics Macrophages Mice Protein Isoforms/metabolism Spodoptera Transfection
Chemicals
Amyloid beta-Peptides Apolipoprotein E3 Apolipoprotein E4 Apolipoproteins E Protein Isoforms
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Tokuda T
Department of Pathology, New York University School of Medicine, 550 First Avenue, New York, NY 10016, USA.
Calero M
Matsubara E
Vidal R
Kumar A
Permanne B
Zlokovic B
Smith J D
Ladu M J
Rostagno A
Frangione B
Ghiso J
References (47)
47 references, click to expand
  1. Self-associated tetramer of human apolipoprotein E does not lead to its accumulation on a lipid particle.
    Biochim Biophys Acta. 1990 Oct 22;1047(1):99-101 PMID: 2248966
  2. Apolipoprotein E immunoreactivity in cerebral amyloid deposits and neurofibrillary tangles in Alzheimer's disease and kuru plaque amyloid in Creutzfeldt-Jakob disease.
    Brain Res. 1991 Feb 8;541(1):163-6 PMID: 2029618
  3. Astrocytic apolipoprotein E mRNA and GFAP mRNA in hippocampus after entorhinal cortex lesioning.
    Brain Res Mol Brain Res. 1991 Sep;11(2):97-106 PMID: 1661818
  4. Apolipoprotein E: a pathological chaperone protein in patients with cerebral and systemic amyloid.
    Neurosci Lett. 1992 Feb 3;135(2):235-8 PMID: 1625800
  5. Isolation and quantification of soluble Alzheimer's beta-peptide from biological fluids.
    Nature. 1992 Sep 24;359(6393):325-7 PMID: 1406936
  6. Production of the Alzheimer amyloid beta protein by normal proteolytic processing.
    Science. 1992 Oct 2;258(5079):126-9 PMID: 1439760
  7. 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. 1993 Mar 1;90(5):1977-81 PMID: 8446617
  8. Apolipoprotein E: binding to soluble Alzheimer's beta-amyloid.
    Biochem Biophys Res Commun. 1993 Apr 30;192(2):359-65 PMID: 8484748
  9. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families.
    Science. 1993 Aug 13;261(5123):921-3 PMID: 8346443
  10. Association of apolipoprotein E allele epsilon 4 with late-onset familial and sporadic Alzheimer's disease.
    Neurology. 1993 Aug;43(8):1467-72 PMID: 8350998
  11. Binding of human apolipoprotein E to synthetic amyloid beta peptide: isoform-specific effects and implications for late-onset Alzheimer disease.
    Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):8098-102 PMID: 8367470
  12. Apolipoprotein E in sporadic Alzheimer's disease: allelic variation and receptor interactions.
    Neuron. 1993 Oct;11(4):575-80 PMID: 8398148
  13. Increased amyloid beta-peptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late-onset Alzheimer disease.
    Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9649-53 PMID: 8415756
  14. Characterization of beta-amyloid peptide from human cerebrospinal fluid.
    J Neurochem. 1993 Nov;61(5):1965-8 PMID: 8229004
  15. Differential effects of apolipoproteins E3 and E4 on neuronal growth in vitro.
    Science. 1994 May 6;264(5160):850-2 PMID: 8171342
  16. Soluble amyloid beta-protein is a marker of Alzheimer amyloid in brain but not in cerebrospinal fluid.
    Biochem Biophys Res Commun. 1994 May 16;200(3):1598-603 PMID: 8185615
  17. Relative abundance of Alzheimer A beta amyloid peptide variants in Alzheimer disease and normal aging.
    Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8378-82 PMID: 8078890
  18. Isoform-specific binding of apolipoprotein E to beta-amyloid.
    J Biol Chem. 1994 Sep 23;269(38):23403-6 PMID: 8089103
  19. 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. 1994 Dec 15;205(2):1164-71 PMID: 7802646
  20. Characterization of apolipoprotein J-Alzheimer's A beta interaction.
    J Biol Chem. 1995 Mar 31;270(13):7563-7 PMID: 7706304
  21. Is Alzheimer's disease an apolipoprotein E amyloidosis?
    Lancet. 1995 Apr 15;345(8955):956-8 PMID: 7715296
  22. Purification of apolipoprotein E attenuates isoform-specific binding to beta-amyloid.
    J Biol Chem. 1995 Apr 21;270(16):9039-42 PMID: 7721816
  23. Characterization of stable complexes involving apolipoprotein E and the amyloid beta peptide in Alzheimer's disease brain.
    Neuron. 1995 Jul;15(1):219-28 PMID: 7619525
  24. Clusterin (apoJ) alters the aggregation of amyloid beta-peptide (A beta 1-42) and forms slowly sedimenting A beta complexes that cause oxidative stress.
    Exp Neurol. 1995 Nov;136(1):22-31 PMID: 7589331
  25. Presence of soluble amyloid beta-peptide precedes amyloid plaque formation in Down's syndrome.
    Nat Med. 1996 Jan;2(1):93-5 PMID: 8564851
  26. Deposits of A beta fibrils are not toxic to cortical and hippocampal neurons in vitro.
    Neurobiol Aging. 1996 Jan-Feb;17(1):107-13 PMID: 8786792
  27. Alzheimer amyloid-beta peptide forms denaturant-resistant complex with type epsilon 3 but not type epsilon 4 isoform of native apolipoprotein E.
    Mol Med. 1996 Mar;2(2):175-80 PMID: 8726460
  28. Apolipoprotein E allele-specific antioxidant activity and effects on cytotoxicity by oxidative insults and beta-amyloid peptides.
    Nat Genet. 1996 Sep;14(1):55-61 PMID: 8782820
  29. Alzheimer's soluble amyloid beta is a normal component of human urine.
    FEBS Lett. 1997 May 12;408(1):105-8 PMID: 9180278
  30. Association of human, rat, and rabbit apolipoprotein E with beta-amyloid.
    J Neurosci Res. 1997 Jul 1;49(1):9-18 PMID: 9211985
  31. Interaction of nascent ApoE2, ApoE3, and ApoE4 isoforms expressed in mammalian cells with amyloid peptide beta (1-40). Relevance to Alzheimer's disease.
    Biochemistry. 1997 Aug 26;36(34):10571-80 PMID: 9265639
  32. Lack of apolipoprotein E dramatically reduces amyloid beta-peptide deposition.
    Nat Genet. 1997 Nov;17(3):263-4 PMID: 9354781
  33. Biology of A beta amyloid in Alzheimer's disease.
    Neurobiol Dis. 1997;4(5):313-28 PMID: 9440120
  34. Nascent astrocyte particles differ from lipoproteins in CSF.
    J Neurochem. 1998 May;70(5):2070-81 PMID: 9572293
  35. Functional and structural properties of lipid-associated apolipoprotein J (clusterin).
    Biochem J. 1999 Dec 1;344 Pt 2:375-83 PMID: 10567218
  36. Binding of arginine-rich (E) apoprotein after recombination with phospholipid vesicles to the low density lipoprotein receptors of fibroblasts.
    J Biol Chem. 1979 May 25;254(10):4186-90 PMID: 220235
  37. Human very low density lipoprotein apolipoprotein E isoprotein polymorphism is explained by genetic variation and posttranslational modification.
    Biochemistry. 1981 Feb 17;20(4):1033-41 PMID: 6260135
  38. Micellar complexes of human apolipoprotein A-I with phosphatidylcholines and cholesterol prepared from cholate-lipid dispersions.
    J Biol Chem. 1982 Apr 25;257(8):4535-40 PMID: 6802835
  39. Behavior of human apolipoprotein E in aqueous solutions and at interfaces.
    J Biol Chem. 1985 Dec 25;260(30):16375-82 PMID: 4066713
  40. Delipidation of plasma lipoproteins.
    Methods Enzymol. 1986;128:213-22 PMID: 3724503
  41. Electron microscopy of negatively stained lipoproteins.
    Methods Enzymol. 1986;128:442-57 PMID: 2425222
  42. Astrocytes synthesize apolipoprotein E and metabolize apolipoprotein E-containing lipoproteins.
    Biochim Biophys Acta. 1987 Jan 13;917(1):148-61 PMID: 3539206
  43. Expression of the human apolipoprotein E gene is regulated by multiple positive and negative elements.
    J Biol Chem. 1988 Jun 15;263(17):8300-8 PMID: 3372525
  44. Cross-linking of apoproteins in high density lipoprotein by dimethylsuberimidate inhibits specific lipoprotein binding to membranes.
    J Lipid Res. 1988 Mar;29(3):319-24 PMID: 3379343
  45. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins.
    Proc Natl Acad Sci U S A. 1998 May 26;95(11):6448-53 PMID: 9600986
  46. Expression of human apolipoprotein E reduces amyloid-beta deposition in a mouse model of Alzheimer's disease.
    J Clin Invest. 1999 Mar;103(6):R15-R21 PMID: 10079115
  47. Contribution of cysteine 158, the glycosylation site threonine 194, the amino- and carboxy-terminal domains of apolipoprotein E in the binding to amyloid peptide beta (1-40).
    Biochemistry. 1999 Jul 13;38(28):8918-25 PMID: 10413465
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
0264-6021
Published
2000-06-01
Pages
359-65
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1221074
Subset
IM
Grants
NIA NIH HHS · AG05891 · United States
NIA NIH HHS · AG10491 · United States
NINDS NIH HHS · NS38777 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com