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Profiling Small RNA From Brain Extracellular Vesicles in Individuals With Depression

Ibrahim, Pascal, Denniston, Ryan, Mitsuhashi, Haruka, Yang, Jennie, Fiori, Laura M, Żurawek, Dariusz, Mechawar, Naguib, Nagy, Corina, Turecki, Gustavo·2024·International Journal of Neuropsychopharmacology
DOI 10.1093/ijnp/pyae013PMC PMC10946232
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Abstract

Background: Major depressive disorder (MDD) is a leading cause of disability with significant mortality risk. Despite progress in our understanding of the etiology of MDD, the underlying molecular changes in the brain remain poorly understood. Extracellular vesicles (EVs) are lipid-bound particles that can reflect the molecular signatures of the tissue of origin. We aimed to optimize a streamlined EV isolation protocol from postmortem brain tissue and determine whether EV RNA cargo, particularly microRNAs (miRNAs), have an MDD-specific profile. Methods: EVs were isolated from postmortem human brain tissue. Quality was assessed using western blots, transmission electron microscopy, and microfluidic resistive pulse sensing. EV RNA was extracted and sequenced on Illumina platforms. Functional follow-up was performed in silico. Results: Quality assessment showed an enrichment of EV markers, as well as a size distribution of 30 to 200 nm in diameter, and no contamination with cellular debris. Small RNA profiling indicated the presence of several RNA biotypes, with miRNAs and transfer RNAs being the most prominent. Exploring miRNA levels between groups revealed decreased expression of miR-92a-3p and miR-129-5p, which was validated by qPCR and was specific to EVs and not seen in bulk tissue. Finally, in silico functional analyses indicate potential roles for these 2 miRNAs in neurotransmission and synaptic plasticity. Conclusion: We provide a streamlined isolation protocol that yields EVs of high quality that are suitable for molecular follow-up. Our findings warrant future investigations into brain EV miRNA dysregulation in MDD.

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Figure 1. Schematic diagram representing study workflow. CTRL, control; F1, fraction 1; F2, fraction 2; MDD, major depressive disorder. Figure was created using BioRender.
Figure 1. Schematic diagram representing study workflow. CTRL, control; F1, fraction 1; F2, fraction 2; MDD, major depressive disorder. Figure was created using BioRender.CC BY · PubMed Central
Figure 2. Quality assessment of EV isolation. (A) Left: Representative stain-free image showing total protein loading for western blot. Right: Representative western blot for Calnexin, BiP, VDAC, CD9, and TSG101 in F1, F2, WB, and PC. (B) Average distribution of particle size from 20 subjects (5 M-CTRL, 5 M-MDD, 5 F-CTRL, 5 F-MDD). (C) Graph showing RNA biotype precent distribution in CTRL and MDD groups. (D) Top: Negative stain TEM images of F1. Bottom: TEM images of EVs immunolabelled with anti-CD81. White rectangles are a zoomed in image of labelled EVs, while white arrows indicate electron-dense gold particles, which are seen as black dots, labeling CD81 on the surface of EVs. Scale: red bar = 200 nm; black bar = 100 nm. F1, fraction 1 (EV fraction); F2, fraction 2 (protein fraction); LD, ladder; PC, pellet with collagenase; WB, whole brain homogenate.
Figure 2. Quality assessment of EV isolation. (A) Left: Representative stain-free image showing total protein loading for western blot. Right: Representative western blot for Calnexin, BiP, VDAC, CD9, and TSG101 in F1, F2, WB, and PC. (B) Average distribution of particle size from 20 subjects (5 M-CTRL, 5 M-MDD, 5 F-CTRL, 5 F-MDD). (C) Graph showing RNA biotype precent distribution in CTRL and MDD groups. (D) Top: Negative stain TEM images of F1. Bottom: TEM images of EVs immunolabelled with anti-CD81. White rectangles are a zoomed in image of labelled EVs, while white arrows indicate electron-dense gold particles, which are seen as black dots, labeling CD81 on the surface of EVs. Scale: red bar = 200 nm; black bar = 100 nm. F1, fraction 1 (EV fraction); F2, fraction 2 (protein fraction); LD, ladder; PC, pellet with collagenase; WB, whole brain homogenate.CC BY · PubMed Central
Figure 3. Comparative analysis of EV miRNAs in males and females. (A) Volcano plots showing altered miRNA expression for males (blue) and females (orange) at a cut-off of P value ≤ .05. (B) Correlation plots between normalized sequencing counts and qPCR expression of the 3 top miRNAs for males (blue) and females (orange). (C) Boxplots showing differences in normalized qPCR expression levels between CTRL and MDD for miR-129-5p in males and miR-92a-3p in females. (D) Correlation plots between normalized sequencing counts from bulk tissue from Fiori et al. (2021) and normalized sequencing counts from overlapping subjects. Results for miR-129-5p (blue) and miR-92a-3p (orange) are shown. CTRL, control; GEO, geometric; MDD, major depressive disorder; SEQ, sequencing.
Figure 3. Comparative analysis of EV miRNAs in males and females. (A) Volcano plots showing altered miRNA expression for males (blue) and females (orange) at a cut-off of P value ≤ .05. (B) Correlation plots between normalized sequencing counts and qPCR expression of the 3 top miRNAs for males (blue) and females (orange). (C) Boxplots showing differences in normalized qPCR expression levels between CTRL and MDD for miR-129-5p in males and miR-92a-3p in females. (D) Correlation plots between normalized sequencing counts from bulk tissue from Fiori et al. (2021) and normalized sequencing counts from overlapping subjects. Results for miR-129-5p (blue) and miR-92a-3p (orange) are shown. CTRL, control; GEO, geometric; MDD, major depressive disorder; SEQ, sequencing.CC BY · PubMed Central

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Metadata

Authors
Ibrahim, P., Denniston, R., Mitsuhashi, H., Yang, J., Fiori, L. M., Żurawek, D., Mechawar, N., Nagy, C., & Turecki, G.
Affiliations
  • Integrated Program in Neuroscience, McGill University , Montreal, Quebec , Canada
  • McGill Group for Suicide Studies, Douglas Mental Health University Institute , Verdun, Quebec , Canada
ORCID
Venue
International Journal of Neuropsychopharmacology
Publisher
Oxford University Press (OUP)
Published
2024-03-01
Volume
27
Issue
3
ISSN
  • 1461-1457
  • 1469-5111
DOI
10.1093/ijnp/pyae013
PMC
PMC10946232
Cited by
29
References
5
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor, 7 d)
Funders
Canadian Institute of Health Research (FDN148374, ENP161427)

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Ibrahim, P., Denniston, R., Mitsuhashi, H., Yang, J., Fiori, L. M., Żurawek, D., Mechawar, N., Nagy, C., & Turecki, G. (2024). Profiling Small RNA From Brain Extracellular Vesicles in Individuals With Depression. International Journal of Neuropsychopharmacology. https://doi.org/10.1093/ijnp/pyae013