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Journal of Translational Medicine
Published in: Journal of Translational Medicine 1/2021

01-12-2021 | Insulins | Research

Extracellular vesicle-associated miRNAs are an adaptive response to gestational diabetes mellitus

Authors: Soumyalekshmi Nair, Dominic Guanzon, Nanthini Jayabalan, Andrew Lai, Katherin Scholz-Romero, Priyakshi Kalita de Croft, Valeska Ormazabal, Carlos Palma, Emilio Diaz, Elizabeth A. McCarthy, Alexis Shub, Jezid Miranda, Eduard Gratacós, Fátima Crispi, Gregory Duncombe, Martha Lappas, H. David McIntyre, Gregory Rice, Carlos Salomon

Published in: Journal of Translational Medicine | Issue 1/2021

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Abstract

Background

Gestational diabetes mellitus (GDM) is a serious public health issue affecting 9–15% of all pregnancies worldwide. Recently, it has been suggested that extracellular vesicles (EVs) play a role throughout gestation, including mediating a placental response to hyperglycaemia. Here, we investigated the EV-associated miRNA profile across gestation in GDM, assessed their utility in developing accurate, multivariate classification models, and determined the signaling pathways in skeletal muscle proteome associated with the changes in the EV miRNA profile.

Methods

Discovery: A retrospective, case–control study design was used to identify EV-associated miRNAs that vary across pregnancy and clinical status (i.e. GDM or Normal Glucose Tolerance, NGT). EVs were isolated from maternal plasma obtained at early, mid and late gestation (n = 29) and small RNA sequencing was performed. Validation: A longitudinal study design was used to quantify expression of selected miRNAs. EV miRNAs were quantified by real-time PCR (cases = 8, control = 14, samples at three times during pregnancy) and their individual and combined classification efficiencies were evaluated. Quantitative, data-independent acquisition mass spectrometry was use to establish the protein profile in skeletal muscle biopsies from normal and GDM.

Results

A total of 2822 miRNAs were analyzed using a small RNA library, and a total of 563 miRNAs that significantly changed (p < 0.05) across gestation and 101 miRNAs were significantly changed between NGT and GDM. Analysis of the miRNA changes in NGT and GDM separately identified a total of 256 (NGT-group), and 302 (GDM-group) miRNAs that change across gestation. A multivariate classification model was developed, based on the quantitative expression of EV-associated miRNAs, and the accuracy to correctly assign samples was > 90%. We identified a set of proteins in skeletal muscle biopsies from women with GDM associated with JAK-STAT signaling which could be targeted by the miRNA-92a-3p within circulating EVs. Interestingly, overexpression of miRNA-92a-3p in primary skeletal muscle cells increase insulin-stimulated glucose uptake.

Conclusions

During early pregnancy, differently-expressed, EV-associated miRNAs may be of clinical utility in identifying presymptomatic women who will subsequently develop GDM later in gestation. We suggest that miRNA-92a-3p within EVs might be a protected mechanism to increase skeletal muscle insulin sensitivity in GDM.
Appendix
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Metadata
Title
Extracellular vesicle-associated miRNAs are an adaptive response to gestational diabetes mellitus
Authors
Soumyalekshmi Nair
Dominic Guanzon
Nanthini Jayabalan
Andrew Lai
Katherin Scholz-Romero
Priyakshi Kalita de Croft
Valeska Ormazabal
Carlos Palma
Emilio Diaz
Elizabeth A. McCarthy
Alexis Shub
Jezid Miranda
Eduard Gratacós
Fátima Crispi
Gregory Duncombe
Martha Lappas
H. David McIntyre
Gregory Rice
Carlos Salomon
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2021
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-021-02999-9

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