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PMID: 19474305 Published · ppublish English Journal Article

Human APOE isoform-dependent effects on brain beta-amyloid levels in PDAPP transgenic mice.

Bales KR, Liu F, Wu S, Lin S, Koger D, DeLong C, Hansen JC, Sullivan PM, Paul SM

Abstract

To investigate the role of human apolipoprotein E (apoE) on Abeta deposition in vivo, we crossed PDAPP mice lacking mouse Apoe to targeted replacement mice expressing human apoE (PDAPP/TRE2, PDAPP/TRE3, or PDAPP/TRE4). We then measured the levels of apoE protein and Abeta peptides in plasma, CSF, and brain homogenates in these mice at different ages. We also quantified the amount of brain Abeta and amyloid burden in 18-month-old mice. In young PDAPP/TRE4 mice that were analyzed at an age before brain Abeta deposition, we observed a significant decrease in the levels of apoE in CSF and brain when compared with age-matched mice expressing either human E2 or E3. The brain levels of Abeta42 in PDAPP/TRE4 mice were substantially elevated even at this very early time point. In older PDAPP/TRE4 mice, the levels of insoluble apoE protein increased in parallel to the dramatic rise in brain Abeta burden, and the majority of apoE was associated with Abeta. In TRE4 only mice, we also observed a significant decrease in the level of apoE in brain homogenates. Since the relative level of apoE mRNA was equivalent in PDAPP/TRE and TRE only mice, it appears that post-translational mechanisms influence the levels of apoE protein in brain (E4 < E3 << E2), resulting in early and dramatic apoE isoform-dependent effects on brain Abeta levels (E4 >> E3 > E2) that increase with age. Therapeutic strategies aimed at increasing the soluble levels of apoE protein, regardless of isoform, may effectively prevent and (or) treat Alzheimer's disease.

MeSH Terms
Age Factors Amyloid beta-Peptides/metabolism Amyloid beta-Protein Precursor/genetics Analysis of Variance Animals Apolipoproteins E/classification,genetics,metabolism Brain/metabolism Humans Mice Mice, Inbred C57BL Mice, Transgenic Mutation Peptide Fragments/metabolism Protein Isoforms/metabolism
Chemicals
Amyloid beta-Peptides Amyloid beta-Protein Precursor Apolipoproteins E Peptide Fragments Protein Isoforms amyloid beta-protein (1-42)
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Bales Kelly R
Neuroscience Discovery Research, Eli Lilly and Company, Indianapolis, Indiana 46285, USA. [email protected]
Liu Feng
Wu Su
Lin Suizhen
Koger Deanna
DeLong Cynthia
Hansen Jeffrey C
Sullivan Patrick M
Paul Steven M
References (51)
51 references, click to expand
  1. Influence of the apolipoprotein E genotype on amyloid deposition and neurofibrillary tangle formation in Alzheimer's disease.
    Neuroscience. 1995 Dec;69(3):757-61 PMID: 8596645
  2. Apolipoprotein E epsilon4 and the risk of dementia with stroke. A population-based investigation.
    JAMA. 1997 Mar 12;277(10):818-21 PMID: 9052712
  3. Amyloid precursor protein processing and A beta42 deposition in a transgenic mouse model of Alzheimer disease.
    Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1550-5 PMID: 9037091
  4. Nascent astrocyte particles differ from lipoproteins in CSF.
    J Neurochem. 1998 May;70(5):2070-81 PMID: 9572293
  5. Apolipoprotein E epsilon 2 allele promotes longevity and protects patients with Down's syndrome from dementia.
    Neuroreport. 1994 Dec 20;5(18):2583-5 PMID: 7696609
  6. Overexpression of ABCA1 reduces amyloid deposition in the PDAPP mouse model of Alzheimer disease.
    J Clin Invest. 2008 Feb;118(2):671-82 PMID: 18202749
  7. Isoform-specific effects of ApoE on HSV immediate early gene expression and establishment of latency.
    Neurobiol Aging. 2008 Jan;29(1):71-7 PMID: 17101197
  8. Amyloid beta-protein, APOE genotype and head injury.
    Ann N Y Acad Sci. 1996 Jan 17;777:271-5 PMID: 8624097
  9. Apolipoprotein E dose-dependent modulation of beta-amyloid deposition in a transgenic mouse model of Alzheimer's disease.
    J Mol Neurosci. 2004;23(3):255-62 PMID: 15181254
  10. The absence of ABCA1 decreases soluble ApoE levels but does not diminish amyloid deposition in two murine models of Alzheimer disease.
    J Biol Chem. 2005 Dec 30;280(52):43243-56 PMID: 16207707
  11. APOE genotype predicts when--not whether--one is predisposed to develop Alzheimer disease.
    Nat Genet. 1998 Aug;19(4):321-2 PMID: 9697689
  12. ABCA1 is required for normal central nervous system ApoE levels and for lipidation of astrocyte-secreted apoE.
    J Biol Chem. 2004 Sep 24;279(39):40987-93 PMID: 15269217
  13. Apolipoprotein E associated with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system.
    J Clin Invest. 1985 Oct;76(4):1501-13 PMID: 3932467
  14. Apolipoprotein A-I stimulates secretion of apolipoprotein E by foam cell macrophages.
    J Biol Chem. 1999 Sep 24;274(39):27925-33 PMID: 10488140
  15. Apolipoprotein E and beta-amyloid levels in the hippocampus and frontal cortex of Alzheimer's disease subjects are disease-related and apolipoprotein E genotype dependent.
    Brain Res. 1999 Oct 2;843(1-2):87-94 PMID: 10528114
  16. Genetics of the apolipoprotein E system in man.
    Am J Hum Genet. 1980 May;32(3):339-47 PMID: 7386461
  17. Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype and Alzheimer disease. A meta-analysis. APOE and Alzheimer Disease Meta Analysis Consortium.
    JAMA. 1997 Oct 22-29;278(16):1349-56 PMID: 9343467
  18. Targeted replacement of the mouse apolipoprotein E gene with the common human APOE3 allele enhances diet-induced hypercholesterolemia and atherosclerosis.
    J Biol Chem. 1997 Jul 18;272(29):17972-80 PMID: 9218423
  19. Impact of apolipoprotein E (ApoE) polymorphism on brain ApoE levels.
    J Neurosci. 2008 Nov 5;28(45):11445-53 PMID: 18987181
  20. Cerebral amyloid angiopathy: amyloid beta accumulates in putative interstitial fluid drainage pathways in Alzheimer's disease.
    Am J Pathol. 1998 Sep;153(3):725-33 PMID: 9736023
  21. Amyloid precursor protein regulates brain apolipoprotein E and cholesterol metabolism through lipoprotein receptor LRP1.
    Neuron. 2007 Oct 4;56(1):66-78 PMID: 17920016
  22. Effect of domain interaction on apolipoprotein E levels in mouse brain.
    J Neurosci. 2005 Nov 16;25(46):10658-63 PMID: 16291938
  23. Apolipoprotein E: far more than a lipid transport protein.
    Annu Rev Genomics Hum Genet. 2000;1:507-37 PMID: 11701639
  24. 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
  25. Lack of apolipoprotein E dramatically reduces amyloid beta-peptide deposition.
    Nat Genet. 1997 Nov;17(3):263-4 PMID: 9354781
  26. Production and characterization of astrocyte-derived human apolipoprotein E isoforms from immortalized astrocytes and their interactions with amyloid-beta.
    Neurobiol Dis. 2005 Jun-Jul;19(1-2):66-76 PMID: 15837562
  27. Apolipoprotein E is essential for amyloid deposition in the APP(V717F) transgenic mouse model of Alzheimer's disease.
    Proc Natl Acad Sci U S A. 1999 Dec 21;96(26):15233-8 PMID: 10611368
  28. Purification and characterization of astrocyte-secreted apolipoprotein E and J-containing lipoproteins from wild-type and human apoE transgenic mice.
    Neurochem Int. 2001 Nov-Dec;39(5-6):415-25 PMID: 11578777
  29. Association of apolipoprotein E polymorphism with outcome after head injury.
    Lancet. 1997 Oct 11;350(9084):1069-71 PMID: 10213549
  30. Potential role of apoE in structural plasticity in the nervous system; implications for disorders of the central nervous system.
    Trends Cardiovasc Med. 1998 Aug;8(6):250-5 PMID: 14987560
  31. Apolipoprotein E represents a potent gene-based therapeutic target for the treatment of sporadic Alzheimer's disease.
    Alzheimers Dement. 2008 Jan;4(1 Suppl 1):S91-7 PMID: 18632009
  32. Apolipoprotein (apo) E4 enhances amyloid beta peptide production in cultured neuronal cells: apoE structure as a potential therapeutic target.
    Proc Natl Acad Sci U S A. 2005 Dec 20;102(51):18700-5 PMID: 16344478
  33. Human and murine ApoE markedly alters A beta metabolism before and after plaque formation in a mouse model of Alzheimer's disease.
    Neurobiol Dis. 2002 Apr;9(3):305-18 PMID: 11950276
  34. Apolipoprotein E modulates gamma-secretase cleavage of the amyloid precursor protein.
    J Neurochem. 2004 Sep;90(5):1132-43 PMID: 15312168
  35. Apolipoprotein (apo) E4 enhances HIV-1 cell entry in vitro, and the APOE epsilon4/epsilon4 genotype accelerates HIV disease progression.
    Proc Natl Acad Sci U S A. 2008 Jun 24;105(25):8718-23 PMID: 18562290
  36. Cognitive change and the APOE epsilon 4 allele.
    Nature. 2002 Aug 29;418(6901):932 PMID: 12198535
  37. Human apolipoprotein E4 alters the amyloid-beta 40:42 ratio and promotes the formation of cerebral amyloid angiopathy in an amyloid precursor protein transgenic model.
    J Neurosci. 2005 Mar 16;25(11):2803-10 PMID: 15772340
  38. Apolipoprotein E expression by neurons surviving excitotoxic stress.
    Neurobiol Dis. 1999 Dec;6(6):508-14 PMID: 10600406
  39. The recycling of apolipoprotein E in macrophages: influence of HDL and apolipoprotein A-I.
    J Lipid Res. 2005 Jul;46(7):1433-9 PMID: 15805547
  40. 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
  41. Apolipoprotein E4 promotes the early deposition of Abeta42 and then Abeta40 in the elderly.
    Acta Neuropathol. 2000 Jul;100(1):36-42 PMID: 10912918
  42. Protective effect of apolipoprotein E type 2 allele for late onset Alzheimer disease.
    Nat Genet. 1994 Jun;7(2):180-4 PMID: 7920638
  43. Deletion of Abca1 increases Abeta deposition in the PDAPP transgenic mouse model of Alzheimer disease.
    J Biol Chem. 2005 Dec 30;280(52):43236-42 PMID: 16207708
  44. apoE isoform-specific disruption of amyloid beta peptide clearance from mouse brain.
    J Clin Invest. 2008 Dec;118(12):4002-13 PMID: 19033669
  45. Apolipoprotein E: structure-function relationships.
    Adv Protein Chem. 1994;45:249-302 PMID: 8154371
  46. Apolipoprotein E isoform-dependent amyloid deposition and neuritic degeneration in a mouse model of Alzheimer's disease.
    Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2892-7 PMID: 10694577
  47. ApoE promotes the proteolytic degradation of Abeta.
    Neuron. 2008 Jun 12;58(5):681-93 PMID: 18549781
  48. 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
  49. Characterization of four lipoprotein classes in human cerebrospinal fluid.
    J Lipid Res. 2001 Jul;42(7):1143-51 PMID: 11441143
  50. Desialylation of human apolipoprotein E decreases its binding to human high-density lipoprotein and its ability to deliver esterified cholesterol to the liver.
    Metabolism. 1999 Sep;48(9):1184-92 PMID: 10484062
  51. Apolipoprotein E4: a causative factor and therapeutic target in neuropathology, including Alzheimer's disease.
    Proc Natl Acad Sci U S A. 2006 Apr 11;103(15):5644-51 PMID: 16567625
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2009-05-27
Pages
6771-9
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6665579
Subset
IM
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