Amyloid-β pathology and APOE genotype modulate retinoid X receptor agonist activity in vivo

J Biol Chem. 2014 Oct 31;289(44):30538-30555. doi: 10.1074/jbc.M114.600833. Epub 2014 Sep 12.

Abstract

Previous data demonstrate that bexarotene (Bex), retinoid X receptor (RXR) agonist, reduces soluble and insoluble amyloid-β (Aβ) in Alzheimer disease (AD)-transgenic mice either by increasing the levels of mouse apolipoprotein E (apoE) or increasing ABCA1/ABCG1-induced apoE lipoprotein association/lipidation. However, although the mechanism of action of RXR agonists remains unclear, a major concern for their use is human (h)-APOE4, the greatest AD genetic risk factor. If APOE4 imparts a toxic gain-of-function, then increasing apoE4 may increase soluble Aβ, likely the proximal AD neurotoxin. If the APOE4 loss-of-function is lipidation of apoE4, then induction of ABCA1/ABCG1 may be beneficial. In novel EFAD-Tg mice (overexpressing h-Aβ42 with h-APOE), levels of soluble Aβ (Aβ42 and oligomeric Aβ) are highest in E4FAD hippocampus (HP) > E3FAD-HP > E4FAD cortex (CX) > E3FAD-CX, whereas levels of lipoprotein-associated/lipidated apoE have the opposite pattern (6 months). In E4FAD-HP, short-term RXR agonist treatment (Bex or LG100268; 5.75-6 months) increased ABCA1, apoE4 lipoprotein-association/lipidation, and apoE4/Aβ complex, decreased soluble Aβ, and increased PSD95. In addition, hydrogel delivery, which mimics low sustained release, was equally effective as gavage for Bex and LG100268. RXR agonists induced no beneficial effects in the E4FAD-HP in a prevention protocol (5-6 months) and actually increased soluble Aβ levels in E3FAD-CX and E4FAD-CX with the short-term protocol, possibly the result of systemic hepatomegaly. Thus, RXR agonists address the loss-of-function associated with APOE4 and exacerbated by Aβ pathology, i.e. low levels of apoE4 lipoprotein association/lipidation. Further studies are vital to address whether RXR agonists are an APOE4-specific AD therapeutic and the systemic side effects that limit translational application.

Keywords: ABCA1/ABCG1 Lipid Transporters; Alzheimer Disease; Amyloid-β (AB); ApoE/Aβ Complex; Apolipoprotein E (ApoE); Drug Action; Drug Delivery; Hepatomegaly; Oligomeric Aβ; RXR Agonists.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP Binding Cassette Transporter 1 / metabolism
  • ATP Binding Cassette Transporter, Subfamily G, Member 1
  • ATP-Binding Cassette Transporters / metabolism
  • Administration, Oral
  • Alzheimer Disease / drug therapy
  • Amyloid beta-Peptides / metabolism*
  • Animals
  • Apolipoproteins E / genetics*
  • Bexarotene
  • Disks Large Homolog 4 Protein
  • Drug Evaluation, Preclinical
  • Genotype
  • Guanylate Kinases / metabolism
  • Humans
  • Lipoproteins / metabolism
  • Liver / drug effects
  • Liver / pathology
  • Male
  • Membrane Proteins / metabolism
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Nicotinic Acids / administration & dosage*
  • Nicotinic Acids / adverse effects
  • Nicotinic Acids / pharmacokinetics
  • Organ Size / drug effects
  • Peptide Fragments / metabolism*
  • Retinoid X Receptors / agonists*
  • Retinoid X Receptors / metabolism
  • Solubility
  • Tetrahydronaphthalenes / administration & dosage*
  • Tetrahydronaphthalenes / adverse effects
  • Tetrahydronaphthalenes / pharmacokinetics

Substances

  • ABCA1 protein, mouse
  • ABCG1 protein, mouse
  • ATP Binding Cassette Transporter 1
  • ATP Binding Cassette Transporter, Subfamily G, Member 1
  • ATP-Binding Cassette Transporters
  • Amyloid beta-Peptides
  • Apolipoproteins E
  • Disks Large Homolog 4 Protein
  • Dlg4 protein, mouse
  • Lipoproteins
  • Membrane Proteins
  • Nicotinic Acids
  • Peptide Fragments
  • Retinoid X Receptors
  • Tetrahydronaphthalenes
  • amyloid beta-protein (1-42)
  • Bexarotene
  • Guanylate Kinases
  • LG 100268