Cholesterol and matrisome pathways dysregulated in human APOE ε4 glia
Posted on: 12 August 2019
Preprint posted on 25 July 2019
Back to the beginning in Alzheimer’s disease research: An extensive RNAseq study reveals that Apolipoprotein E isoforms differentially regulate lipid metabolism in human brain glia cells. Intriguing: discrepancies between human and mouse were found.
Selected by Theresa PohlkampCategories: bioinformatics, cell biology, genetics, immunology, neuroscience, pathology, physiology
Background
The highest genetic risk factor for Alzheimer’s disease (AD) is Apolipoprotein E (ApoE) isoform ε4 (APOE 4). Three major ApoE isoforms exist in the human population: APOE 2, APOE 3, and APOE 4. Whereas APOE 2 has protective features, APOE 4 increases the risk for the disease. Age is the highest general risk factor to develop AD; each APOE 4 allele decreases the age of disease onset by 3-5 years. However, it is not well understood how APOE 4 contributes to AD pathology. Since its discovery as genetic risk factor for AD in the mid-90s scientists attributed toxic and/or defective functions to APOE 4.
The general function of ApoE is to nurture cells with lipids like fat and cholesterol, the major components of the cell membranes. In the brain, astrocytes provide the major source of ApoE. Unless stressed, other cells like microglia, the immune cells of the brain, and neurons only produce small amounts of ApoE. The difference between APOE 3 and APOE 4, the two isoforms this preprint is focusing on, is a substitution of only one amino acid. This substitution affects the structure and biochemical properties of APOE with regard to lipidation, degradation, toxicity, and intracellular trafficking. To study APOE 3 and APOE 4 in vivo, human APOE 3 and APOE 4 targeted replacement mice (APOE 2-TR, APOE 3-TR, APOE 4-TR), as well as Apoe-knockout (Apoe KO) mice have been created and are used intensely in the AD-field (reviewed in Balu et al., 2019). This preprint reveals detailed insight into how human APOE 4 compared to APOE 3 affects the transcriptome of diverse brain cell types of human and mouse.
What was done?
The authors analyzed the transcriptome of up to three homologous APOE genotypes (APOE 3/APOE 3 = 33, APOE 4/APOE 4 = 44, and KO/KO) in up to four brain cell types derived from human or mouse. Thirteen (7xAPOE 33, 6xAPOE 44) human induced pluripotent stem cell (hiPSC) lines were differentiated into microglia, astrocytes, mixed cortical cells (neurons and 5-25% astrocytes), and brain microvascular endothelial cells (BMEC). Isogenic glia (astrocytes and microglia) lines were obtained by mutating APOE 44 hiPSC lines to APOE 33 by using CRISPR/Cas9. Isogenic lines were used for experimental studies. Mouse primary glia were cultured from cortical tissue of APOE 33-TR, APOE 44-TR, and Apoe KO pups. RNA sequencing (RNAseq) was performed on human and mouse cell lines. Publicly available transcriptomic data of AD brain samples derived from postmortem patients (APOE 33 and APOE 44) were used to compute cell-line specific transcriptomes following a deconvolution algorithm.
What was found?
Lipid metabolism related pathways are dysregulated in human but not mouse APOE 4 glia
RNAseq analysis of hiPSC-derived cell lines showed APOE genotype-dependent gene expression discrepancies in astrocytes, microglia, and mixed cortical cultures, but not brain microvascular endothelial cells. The authors found that specific pathways were differentially regulated in APOE 4 versus APOE 3 glia, with greatest discrepancies in lipid metabolism pathways. Differences in gene expression predicted an increase in cholesterol synthesis and metabolism in APOE 4 glia. A reduced lipid/cholesterol efflux, lysosomal accumulation of cholesterol, and a decrease in lipid clearance and catabolism were predicted for microglia (Figure), only. The deconvoluted glia transcriptome of human AD brain tissue supported these findings.
Figure: Functional pathway analysis of hiPSC-derived microglia. Red and orange colors are upregulated, green and blue are downregulated genes/functions in APOE 4 compared to APOE 3. Reproduced with permission from Figure 2g of the preprint.
Intriguingly, the mouse primary cortical glia transcriptomes revealed different results. Whereas extracellular matrix and inflammation associated pathways were upregulated in mouse APOE 4 glia, no significant difference was observed in lipid metabolism pathways. In general, higher discrepancies were found in Apoe KO glia: most strikingly lipid metabolism pathways were upregulated, but also inflammation and extracellular matrix (ECM) related pathways were increased. Thus, dysregulations in Apoe KO are distinct from those linked to APOE 4.
APOE 4-mediated upregulation of matrisome pathways in glia requires the presence of neurons
The matrisome is an ensemble of ECM proteins and associated factors involved in cell-cell communication. Within the hiPSC-derived mixed cortical culture, matrisome related genes involved in chemotaxis, inflammation, and lipid-synthesis pathways were upregulated in APOE 4. Similar findings for APOE 4 compared to APOE 3 genotype were obtained in glia from cell-type deconvoluted RNAseq data of human AD brain tissue. The authors concluded that specific ApoE-isoform dependent communication pathways in glia are only activated in the presence of neurons. A transcriptome comparison across APOE 33 carriers, grouped by various criteria of AD related phenotypes, showed that matrisome pathways were enriched in AD. This enrichment pattern was independent of APOE genotype and also found in APOE 44 carriers. Hence, the matrisome seems to be upregulated by APOE 4 and other AD factors.
Experimental validation and mechanistic findings: decoupled lipid metabolism and increased inflammation in APOE 4 versus APOE 3 glia
To validate the RNAseq findings experimentally, hiPSC-derived, isogenic APOE 44 and APOE 33 glia were used to study cholesterol metabolism. APOE 4 astrocytes had increased free cholesterol levels but no changes in cholesteryl ester. After applying excess LDL to the cultures, cholesterol accumulated more intracellularly. This defective cholesterol accumulation was found in lysosomes of APOE 4 astrocytes. Intracellular and secreted APOE levels, as well as ABCA1 were much lower in APOE 4 than APOE 3 astrocytes. ABCA1 is the APOE lipidating transporter protein, also known as the cholesterol efflux regulatory protein, thus, these findings indicate a decreased cholesterol efflux. In total this suggests a decoupling of lipid synthesis and catabolism in APOE 4 astrocytes. In addition, APOE 4 astrocytes secreted higher amounts of proinflammatory chemokines, cytokines, and growth factors.
Overall, the findings suggest that restoring lipid homeostasis in glia by targeting the structure and/or function of APOE 4 provide a promising AD-treatment approach.
What I like about this paper
The study demonstrates that the involvement of APOE 4 in AD pathology likely falls back to the key role of ApoE in lipid metabolism and discovered a novel gene set/pathway called “matrisome” in APOE 4 and AD case. These findings are of tremendous importance to the field, since they make us researchers think why APOE-isoforms contribute to coronary artery disease, myocardial infarction, and AD in the same isoform specific stepwise pattern: APOE 4>APOE 3>APOE 2. Whereas this work demonstrates potential drawbacks of animal models for complex human diseases, it suggests that hiPSC-derived mixed cortical cultures provide a translatable in vitro model to study APOE 4-dysregulated pathways in AD.
Questions and future directions
(1) The Apoe gene promoter and the 5’UTR have not been replaced in APOE-TR mice, likely causing differences in gene regulation (Maloney et al., 2007) of human APOE isoforms in human versus mouse. Do you think this is causing the discrepancies in your study when you compare mouse and human glia?
(2) APOE expression was highest in BMEC, which was surprising to me. With regard to the high APOE-expression it is also surprising that these cells show the smallest changes in differentially expressed genes dependent on APOE isoforms, did you expect that?
(3) Did you compute the neuronal transcriptome? How does APOE affect transcription in neurons?
(4) Future studies could test whether (frequent) medium exchange between APOE 3 and APOE 4 glia can reverse the differences seen in lipid metabolism.
(5) Future studies could also investigate the effect of APOE-loss and APOE 2 in hiPSC-derived isogenic glia.
References
doi: https://doi.org/10.1242/prelights.13086
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5 years
Theresa Pohlkamp
I am very excited for the authors! The paper is now available on the SneakPeek server of Cell:
https://papers.ssrn.com/sol3/papers.cfm?abstract_id=3435267
It does contain additional data, especially in the last figure!