ApoE influences amyloid-β (Aβ) clearance despite minimal apoE/Aβ association in physiological conditions
Apolipoprotein E gene (APOE) alleles may shift the onset of Alzheimer’s disease (AD) through apoE protein isoforms changing the probability of amyloid-β (Aβ) accumulation. It has been proposed that differential physical interactions of apoE isoforms with soluble Aβ (sAβ) in brain fluids influence th...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 110; no. 19; pp. E1807 - E1816 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
07.05.2013
National Acad Sciences |
| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Apolipoprotein E gene (APOE) alleles may shift the onset of Alzheimer’s disease (AD) through apoE protein isoforms changing the probability of amyloid-β (Aβ) accumulation. It has been proposed that differential physical interactions of apoE isoforms with soluble Aβ (sAβ) in brain fluids influence the metabolism of Aβ, providing a mechanism to account for how APOE influences AD risk. In contrast, we provide clear evidence that apoE and sAβ interactions occur minimally in solution and in the cerebrospinal fluid of human subjects, producing apoE3 and apoE4 isoforms as assessed by multiple biochemical and analytical techniques. Despite minimal extracellular interactions with sAβ in fluid, we find that apoE isoforms regulate the metabolism of sAβ by astrocytes and in the interstitial fluid of mice that received apoE infusions during brain Aβ microdialysis. We find that a significant portion of apoE and sAβ compete for the low-density lipoprotein receptor-related protein 1 (LRP1)–dependent cellular uptake pathway in astrocytes, providing a mechanism to account for apoE’s regulation of sAβ metabolism despite minimal evidence of direct interactions in extracellular fluids. We propose that apoE influences sAβ metabolism not through direct binding to sAβ in solution but through its actions with other interacting receptors/transporters and cell surfaces. These results provide an alternative frame work for the mechanistic explanations on how apoE isoforms influence the risk of AD pathogenesis. |
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| AbstractList | Apolipoprotein E gene (APOE) alleles may shift the onset of Alzheimer’s disease (AD) through apoE protein isoforms changing the probability of amyloid-β (Aβ) accumulation. It has been proposed that differential physical interactions of apoE isoforms with soluble Aβ (sAβ) in brain fluids influence the metabolism of Aβ, providing a mechanism to account for how APOE influences AD risk. In contrast, we provide clear evidence that apoE and sAβ interactions occur minimally in solution and in the cerebrospinal fluid of human subjects, producing apoE3 and apoE4 isoforms as assessed by multiple biochemical and analytical techniques. Despite minimal extracellular interactions with sAβ in fluid, we find that apoE isoforms regulate the metabolism of sAβ by astrocytes and in the interstitial fluid of mice that received apoE infusions during brain Aβ microdialysis. We find that a significant portion of apoE and sAβ compete for the low-density lipoprotein receptor-related protein 1 (LRP1)–dependent cellular uptake pathway in astrocytes, providing a mechanism to account for apoE’s regulation of sAβ metabolism despite minimal evidence of direct interactions in extracellular fluids. We propose that apoE influences sAβ metabolism not through direct binding to sAβ in solution but through its actions with other interacting receptors/transporters and cell surfaces. These results provide an alternative frame work for the mechanistic explanations on how apoE isoforms influence the risk of AD pathogenesis. It has been proposed that differential physical interactions of apolipoprotein E (apoE) isoforms with soluble amyloid-β (Aβ) in brain fluids influence the metabolism of Aβ, providing a major mechanism to account for how APOE influences Alzheimer’s disease risk. The current study challenges this proposal and clearly shows that lipoproteins containing apoE isoforms are unlikely to play a significant role in Aβ metabolism by binding directly to Aβ in physiological fluids such as cerebrospinal fluid or interstitial fluid. Our in vitro and in vivo results suggest that apoE isoforms influence Aβ metabolism by competing for the same clearance pathways within the brain. Apolipoprotein E gene ( APOE ) alleles may shift the onset of Alzheimer’s disease (AD) through apoE protein isoforms changing the probability of amyloid-β (Aβ) accumulation. It has been proposed that differential physical interactions of apoE isoforms with soluble Aβ (sAβ) in brain fluids influence the metabolism of Aβ, providing a mechanism to account for how APOE influences AD risk. In contrast, we provide clear evidence that apoE and sAβ interactions occur minimally in solution and in the cerebrospinal fluid of human subjects, producing apoE3 and apoE4 isoforms as assessed by multiple biochemical and analytical techniques. Despite minimal extracellular interactions with sAβ in fluid, we find that apoE isoforms regulate the metabolism of sAβ by astrocytes and in the interstitial fluid of mice that received apoE infusions during brain Aβ microdialysis. We find that a significant portion of apoE and sAβ compete for the low-density lipoprotein receptor-related protein 1 (LRP1)–dependent cellular uptake pathway in astrocytes, providing a mechanism to account for apoE’s regulation of sAβ metabolism despite minimal evidence of direct interactions in extracellular fluids. We propose that apoE influences sAβ metabolism not through direct binding to sAβ in solution but through its actions with other interacting receptors/transporters and cell surfaces. These results provide an alternative frame work for the mechanistic explanations on how apoE isoforms influence the risk of AD pathogenesis. Apolipoprotein E gene (APOE) alleles may shift the onset of Alzheimer's disease (AD) through apoE protein isoforms changing the probability of amyloid-β (Aβ) accumulation. It has been proposed that differential physical interactions of apoE isoforms with soluble Aβ (sAβ) in brain fluids influence the metabolism of Aβ, providing a mechanism to account for how APOE influences AD risk. In contrast, we provide clear evidence that apoE and sAβ interactions occur minimally in solution and in the cerebrospinal fluid of human subjects, producing apoE3 and apoE4 isoforms as assessed by multiple biochemical and analytical techniques. Despite minimal extracellular interactions with sAβ in fluid, we find that apoE isoforms regulate the metabolism of sAβ by astrocytes and in the interstitial fluid of mice that received apoE infusions during brain Aβ microdialysis. We find that a significant portion of apoE and sAβ compete for the low-density lipoprotein receptor-related protein 1 (LRP1)-dependent cellular uptake pathway in astrocytes, providing a mechanism to account for apoE's regulation of sAβ metabolism despite minimal evidence of direct interactions in extracellular fluids. We propose that apoE influences sAβ metabolism not through direct binding to sAβ in solution but through its actions with other interacting receptors/transporters and cell surfaces. These results provide an alternative frame work for the mechanistic explanations on how apoE isoforms influence the risk of AD pathogenesis.Apolipoprotein E gene (APOE) alleles may shift the onset of Alzheimer's disease (AD) through apoE protein isoforms changing the probability of amyloid-β (Aβ) accumulation. It has been proposed that differential physical interactions of apoE isoforms with soluble Aβ (sAβ) in brain fluids influence the metabolism of Aβ, providing a mechanism to account for how APOE influences AD risk. In contrast, we provide clear evidence that apoE and sAβ interactions occur minimally in solution and in the cerebrospinal fluid of human subjects, producing apoE3 and apoE4 isoforms as assessed by multiple biochemical and analytical techniques. Despite minimal extracellular interactions with sAβ in fluid, we find that apoE isoforms regulate the metabolism of sAβ by astrocytes and in the interstitial fluid of mice that received apoE infusions during brain Aβ microdialysis. We find that a significant portion of apoE and sAβ compete for the low-density lipoprotein receptor-related protein 1 (LRP1)-dependent cellular uptake pathway in astrocytes, providing a mechanism to account for apoE's regulation of sAβ metabolism despite minimal evidence of direct interactions in extracellular fluids. We propose that apoE influences sAβ metabolism not through direct binding to sAβ in solution but through its actions with other interacting receptors/transporters and cell surfaces. These results provide an alternative frame work for the mechanistic explanations on how apoE isoforms influence the risk of AD pathogenesis. |
| Author | Yinong Wang Joseph M. Castellano Kanchan Garai Aarti Shah David M. Holtzman Philip B. Verghese Hong Jiang Guojun Bu Carl Frieden |
| Author_xml | – sequence: 1 givenname: Philip B. surname: Verghese fullname: Verghese, Philip B. organization: Departments of aNeurology,, Hope Center for Neurological Disorders, and, The Charles F. and Joanne Knight Alzheimer’s Disease Research Center, Washington University School of Medicine, St. Louis, MO 63110; and – sequence: 2 givenname: Joseph M. surname: Castellano fullname: Castellano, Joseph M. organization: Departments of aNeurology,, Hope Center for Neurological Disorders, and, The Charles F. and Joanne Knight Alzheimer’s Disease Research Center, Washington University School of Medicine, St. Louis, MO 63110; and – sequence: 3 givenname: Kanchan surname: Garai fullname: Garai, Kanchan organization: Biochemistry and Molecular Biophysics, and, Hope Center for Neurological Disorders, and, The Charles F. and Joanne Knight Alzheimer’s Disease Research Center, Washington University School of Medicine, St. Louis, MO 63110; and – sequence: 4 givenname: Yinong surname: Wang fullname: Wang, Yinong organization: Biomedical Engineering,, Hope Center for Neurological Disorders, and – sequence: 5 givenname: Hong surname: Jiang fullname: Jiang, Hong organization: Departments of aNeurology,, Hope Center for Neurological Disorders, and, The Charles F. and Joanne Knight Alzheimer’s Disease Research Center, Washington University School of Medicine, St. Louis, MO 63110; and – sequence: 6 givenname: Aarti surname: Shah fullname: Shah, Aarti organization: Departments of aNeurology,, Hope Center for Neurological Disorders, and, The Charles F. and Joanne Knight Alzheimer’s Disease Research Center, Washington University School of Medicine, St. Louis, MO 63110; and – sequence: 7 givenname: Guojun surname: Bu fullname: Bu, Guojun organization: Department of Neuroscience, Mayo Clinic, Jacksonville, FL 32224 – sequence: 8 givenname: Carl surname: Frieden fullname: Frieden, Carl organization: Biochemistry and Molecular Biophysics, and, Hope Center for Neurological Disorders, and, The Charles F. and Joanne Knight Alzheimer’s Disease Research Center, Washington University School of Medicine, St. Louis, MO 63110; and – sequence: 9 givenname: David M. surname: Holtzman fullname: Holtzman, David M. organization: Departments of aNeurology,, Hope Center for Neurological Disorders, and, The Charles F. and Joanne Knight Alzheimer’s Disease Research Center, Washington University School of Medicine, St. Louis, MO 63110; and |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23620513$$D View this record in MEDLINE/PubMed |
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| Snippet | Apolipoprotein E gene (APOE) alleles may shift the onset of Alzheimer’s disease (AD) through apoE protein isoforms changing the probability of amyloid-β (Aβ)... It has been proposed that differential physical interactions of apolipoprotein E (apoE) isoforms with soluble amyloid-β (Aβ) in brain fluids influence the... Apolipoprotein E gene (APOE) alleles may shift the onset of Alzheimer's disease (AD) through apoE protein isoforms changing the probability of amyloid-β (Aβ)... |
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| SubjectTerms | alleles Alzheimer disease Alzheimer Disease - diagnosis Alzheimer Disease - genetics Amyloid beta-Peptides - metabolism analytical methods Animals apolipoprotein E Apolipoproteins E - metabolism astrocytes Biological Sciences brain Brain - pathology Cell Line cerebrospinal fluid Cholesterol - metabolism extracellular fluids Gene Expression Regulation Humans low density lipoprotein metabolism Mice Mice, Knockout microdialysis Neurodegenerative Diseases - metabolism pathogenesis PNAS Plus Protein Binding protein isoforms Protein Isoforms - metabolism receptors risk Time Factors transporters |
| Title | ApoE influences amyloid-β (Aβ) clearance despite minimal apoE/Aβ association in physiological conditions |
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