Time-course full profiling of circulating miRNAs in neurologically deceased organ donors: a proof of concept study to understand the onset of the cytokine storm

Epigenetics. 2022 Nov;17(11):1546-1561. doi: 10.1080/15592294.2022.2076048. Epub 2022 May 21.

Abstract

Neurologically deceased organ donors (NDDs) generally display an immune response involving an intense production of pro-inflammatory cytokines referred to as the cytokine storm. The sudden surge of inflammatory mediators in circulation promotes tissue and organ damages and ultimately leads to poor transplant outcome. As microRNAs (miRNAs) are frequently proposed as key regulators of inflammation and are relatively stable in circulation, changes in their profiles could play a role in the onset of the cytokine storm in NDDs. In this proof-of-concept study, we sought to investigate differentially abundant circulating miRNAs in a temporal manner between neurological death and organ recovery and to assess the association between specific miRNAs and levels of inflammatory cytokines in blood. Plasma samples from five NDDs were obtained at multiple time points between organ donation consent and organ recovery. Using a time-course analysis and miRNA sequencing, we identified 32 plasma miRNAs fluctuating between consent and organ recovery (false discovery rate; q-value < 0.1). Eleven miRNAs relatively abundant (>100 reads) and detected in all samples were selected for further biological pathway analysis (miR-486-3p, miR-103a-3p, miR-106b-3p, miR-182-5p, miR-101-3p, miR-10a-5p, miR-125a-5p, miR-146b-5p, miR-26a-5p, miR-423-5p, miR-92b-3p). These miRNAs targeted genes such as c-JUN (TNF signalling pathway) and eEF2 (AMPK pathway), suggesting a potential role in regulation of inflammation. Our results contribute to a better understanding of the miRNAs dynamic after neurological death in organ donors and could potentially be used to predict the related early cytokine storm.Trial registration: ClinicalTrials.gov ID NCT03786991. Registered December 2018.

Keywords: Organ donation; circulating miRNAs; microRNAs; microtranscriptome; next-generation sequencing; transplantation.

Publication types

  • Clinical Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinases / genetics
  • AMP-Activated Protein Kinases / metabolism
  • Circulating MicroRNA* / genetics
  • Circulating MicroRNA* / metabolism
  • Cytokine Release Syndrome
  • Cytokines / genetics
  • Cytokines / metabolism
  • DNA Methylation
  • Gene Expression Profiling
  • Humans
  • Inflammation / genetics
  • Inflammation Mediators / metabolism
  • MicroRNAs* / metabolism
  • Proof of Concept Study
  • Tissue Donors

Substances

  • AMP-Activated Protein Kinases
  • Circulating MicroRNA
  • Cytokines
  • Inflammation Mediators
  • MicroRNAs

Associated data

  • ClinicalTrials.gov/NCT03786991

Grants and funding

The EPI-STORM study is funded by the Social Sciences and Humanities Research Councils, New Frontiers in Research Funds – Exploration program – NFRFE-2018-02115, by the Projet Structurant du Centre de recherche du Centre hospitalier universitaire de Sherbrooke (CR-CHUS) (grant #91314) and by the Fonds de Recherche du Québec – Santé (FRQ-S) (grant #36786). The granting agency was not involved in any part of the study. A-A.C. and CL were supported by a doctoral award formation from the Fonds de Recherche du Québec - Santé (FRQ-S). LB and FD are respectively senior and junior research scholars from the FRQ-S.