Research Paper Volume 14, Issue 21 pp 8595—8614

ESR1 dysfunction triggers neuroinflammation as a critical upstream causative factor of the Alzheimer’s disease process

Junying Liu1, *, , Shouli Yuan2, *, , Xinhui Niu3, , Robbie Kelleher4, , Helen Sheridan1, ,

  • 1 NatPro Center, School of Pharmacy and Pharmaceutical Sciences, Trinity College Dublin, Dublin 2, Ireland
  • 2 Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, China
  • 3 Department of Regenerative Medicine, School of Pharmaceutical Sciences, Jilin University, Changchun, China
  • 4 School of Medicine, Trinity College Dublin, Dublin 2, Ireland
* Equal contribution

Received: June 9, 2022       Accepted: October 14, 2022       Published: November 1, 2022      

https://doi.org/10.18632/aging.204359
How to Cite

Copyright: © 2022 Liu et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Abstract

Alzheimer's disease (AD) accounts for approximately 60% of dementia cases worldwide. Advanced age is the most significant risk factor for AD and approximately two-thirds of cases relate to women. While the previous meta-analysis suggests that estrogen receptor (ESR) genetic polymorphisms are closely associated with dementia, the implications of this observation on a molecular level are not entirely understood. Our study explores this intricate molecular puzzle through the use of a variety of bioinformatics tools. Initially, we attempted to elucidate mechanisms underlying breast cancer development by identifying the high-throughput dataset of ESR1-knockdown breast cancer tissue samples. Surprisingly, KEGG pathway enrichment showed that the most frequently occurring proteins were related to axonal guidance and inflammation-related gene markers. These observations were supported by an external high throughput dataset of AD inflammatory samples in vivo. Our results suggest that ESR1 is modulated by apolipoprotein E (APOE) through CEBPB/ATF4, mir-155-5p, or mir-1-3p. Moreover, sea hare-hydrolysates (SHH), as one of the axonal guidance molecules, could regulate the STAT3/PRDM1/CEBPB pathway and consequently induce cell death through pyroptosis signaling pathways, trigger the secretion of IL1β, leading to neuroinflammation and worsening AD pathogenesis. Molecular docking verification demonstrated that the predicted natural products scoulerine and genistein displayed strong binding affinities for BACE1 and ESR1, respectively. This strategy can be used to design novel, personalized therapeutic approaches to treatment and a first-in-class clinical lead for the personalised treatment of AD.

Abbreviations

AD: Alzheimer’s disease; AEP: asparagine endopeptidase; Aβ: amyloid-beta; APOE: apolipoprotein E; BACE1: Amyloid Precursor Protein Lyase 1; CADD: computer-aided drug design; C/EBPβ: CCAAT enhancer-binding protein β; CMap: Connectivity Map; DEGs: differentially expressed genes; ER: Endoplasmic Reticulum; ESR1: estrogen receptor-α gene; ETCM: Encyclopedia of Traditional Chinese Medicine; FPKM: fragments per kilo base per million mapped reads; FDR: false discovery rate; GSDMD: gasdermin D; GSEA: Gene Set Enrichment Analysis; GSK3β: glycogen synthase kinase-3 beta; GEO: Gene Expression Omnibus; HIF1α: hypoxia-inducible-1α; KEGG: Kyoto Encyclopedia of Genes and Genomes; MSigDB: Molecular Signatures Database; NFE2L2: Nuclear factor erythroid 2-related factor 2; NPT: number of particles, pressure, temperature; NVT: number of particles, volume, temperature; OPCs: oligodendrocyte progenitor cells; PCA: principal component analysis; PPI: protein-protein interaction; SHH: sea hare-hydrolysates; SEA: Similarity ensemble approaches; STAT3: signal transducers and activators of transcription 3; TF: transcription factors; TLR: toll-like receptor.