Human placental exosomes in gestational diabetes mellitus carry a specific set of miRNAs associated with skeletal muscle insulin sensitivity

There is increasing evidence that miRNAs, which are enriched in nanovesicles called exosomes, are important regulators of gene expression. When compared with normal pregnancies, pregnancies with gestational diabetes mellitus (GDM) are associated with skeletal muscle insulin resistance as well as inc...

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Published inClinical science (1979) Vol. 132; no. 22; pp. 2451 - 2467
Main Authors Nair, Soumyalekshmi, Jayabalan, Nanthini, Guanzon, Dominic, Palma, Carlos, Scholz-Romero, Katherin, Elfeky, Omar, Zuñiga, Felipe, Ormazabal, Valeska, Diaz, Emilio, Rice, Gregory E, Duncombe, Gregory, Jansson, Thomas, McIntyre, Harold David, Lappas, Martha, Salomon, Carlos
Format Journal Article
LanguageEnglish
Published England 30.11.2018
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Abstract There is increasing evidence that miRNAs, which are enriched in nanovesicles called exosomes, are important regulators of gene expression. When compared with normal pregnancies, pregnancies with gestational diabetes mellitus (GDM) are associated with skeletal muscle insulin resistance as well as increased levels of circulating placental exosomes. Here we investigated whether placental exosomes in GDM carry a specific set of miRNAs associated with skeletal muscle insulin sensitivity. Exosomes were isolated from chorionic villous (CV) explants from both women with Normal Glucose Tolerant (NGT) and GDM pregnancies. Using miRNA sequencing, we identified a specific set of miRNAs selectively enriched with exosomes and compared with their cells of origin indicating a specific packaging of miRNAs into exosomes. Gene target and ontology analysis of miRNA differentially expressed in exosomes secreted in GDM compared with NGT are associated with pathways regulating cell migration and carbohydrate metabolism. We determined the expression of a selected set of miRNAs in placenta, plasma, and skeletal muscle biopsies from NGT and GDM. Interestingly, the expression of these miRNAs varied in a consistent pattern in the placenta, in circulating exosomes, and in skeletal muscle in GDM. Placental exosomes from GDM pregnancies decreased insulin-stimulated migration and glucose uptake in primary skeletal muscle cells obtained from patients with normal insulin sensitivity. Interestingly, placental exosomes from NGT increase migration and glucose uptake in response to insulin in skeletal muscle from diabetic subjects. These findings suggest that placental exosomes might have a role in the changes on insulin sensitivity in normal and GDM pregnancies.
AbstractList There is increasing evidence that miRNAs, which are enriched in nanovesicles called exosomes, are important regulators of gene expression. When compared with normal pregnancies, pregnancies with gestational diabetes mellitus (GDM) are associated with skeletal muscle insulin resistance as well as increased levels of circulating placental exosomes. Here we investigated whether placental exosomes in GDM carry a specific set of miRNAs associated with skeletal muscle insulin sensitivity. Exosomes were isolated from chorionic villous (CV) explants from both women with Normal Glucose Tolerant (NGT) and GDM pregnancies. Using miRNA sequencing, we identified a specific set of miRNAs selectively enriched with exosomes and compared with their cells of origin indicating a specific packaging of miRNAs into exosomes. Gene target and ontology analysis of miRNA differentially expressed in exosomes secreted in GDM compared with NGT are associated with pathways regulating cell migration and carbohydrate metabolism. We determined the expression of a selected set of miRNAs in placenta, plasma, and skeletal muscle biopsies from NGT and GDM. Interestingly, the expression of these miRNAs varied in a consistent pattern in the placenta, in circulating exosomes, and in skeletal muscle in GDM. Placental exosomes from GDM pregnancies decreased insulin-stimulated migration and glucose uptake in primary skeletal muscle cells obtained from patients with normal insulin sensitivity. Interestingly, placental exosomes from NGT increase migration and glucose uptake in response to insulin in skeletal muscle from diabetic subjects. These findings suggest that placental exosomes might have a role in the changes on insulin sensitivity in normal and GDM pregnancies.
Author Jansson, Thomas
Jayabalan, Nanthini
Rice, Gregory E
Lappas, Martha
Ormazabal, Valeska
McIntyre, Harold David
Guanzon, Dominic
Palma, Carlos
Duncombe, Gregory
Scholz-Romero, Katherin
Elfeky, Omar
Nair, Soumyalekshmi
Diaz, Emilio
Zuñiga, Felipe
Salomon, Carlos
Author_xml – sequence: 1
  givenname: Soumyalekshmi
  surname: Nair
  fullname: Nair, Soumyalekshmi
  organization: Exosome Biology Laboratory, Centre for Clinical Diagnostics, University of Queensland Centre for Clinical Research, Royal Brisbane and Women's Hospital, The University of Queensland, Brisbane, QLD 4029, Australia
– sequence: 2
  givenname: Nanthini
  surname: Jayabalan
  fullname: Jayabalan, Nanthini
  organization: Exosome Biology Laboratory, Centre for Clinical Diagnostics, University of Queensland Centre for Clinical Research, Royal Brisbane and Women's Hospital, The University of Queensland, Brisbane, QLD 4029, Australia
– sequence: 3
  givenname: Dominic
  surname: Guanzon
  fullname: Guanzon, Dominic
  organization: Exosome Biology Laboratory, Centre for Clinical Diagnostics, University of Queensland Centre for Clinical Research, Royal Brisbane and Women's Hospital, The University of Queensland, Brisbane, QLD 4029, Australia
– sequence: 4
  givenname: Carlos
  surname: Palma
  fullname: Palma, Carlos
  organization: Exosome Biology Laboratory, Centre for Clinical Diagnostics, University of Queensland Centre for Clinical Research, Royal Brisbane and Women's Hospital, The University of Queensland, Brisbane, QLD 4029, Australia
– sequence: 5
  givenname: Katherin
  surname: Scholz-Romero
  fullname: Scholz-Romero, Katherin
  organization: Department of Clinical Biochemistry and Immunology, Faculty of Pharmacy, University of Concepción, Concepción, Chile
– sequence: 6
  givenname: Omar
  surname: Elfeky
  fullname: Elfeky, Omar
  organization: Exosome Biology Laboratory, Centre for Clinical Diagnostics, University of Queensland Centre for Clinical Research, Royal Brisbane and Women's Hospital, The University of Queensland, Brisbane, QLD 4029, Australia
– sequence: 7
  givenname: Felipe
  surname: Zuñiga
  fullname: Zuñiga, Felipe
  organization: Department of Clinical Biochemistry and Immunology, Faculty of Pharmacy, University of Concepción, Concepción, Chile
– sequence: 8
  givenname: Valeska
  surname: Ormazabal
  fullname: Ormazabal, Valeska
  organization: Department of Pharmacology, Faculty of Biological Sciences, University of Concepcion, Chile
– sequence: 9
  givenname: Emilio
  surname: Diaz
  fullname: Diaz, Emilio
  organization: Faculty of Medicine, University of Concepcion, Concepcion, Chile
– sequence: 10
  givenname: Gregory E
  surname: Rice
  fullname: Rice, Gregory E
  organization: Exosome Biology Laboratory, Centre for Clinical Diagnostics, University of Queensland Centre for Clinical Research, Royal Brisbane and Women's Hospital, The University of Queensland, Brisbane, QLD 4029, Australia
– sequence: 11
  givenname: Gregory
  surname: Duncombe
  fullname: Duncombe, Gregory
  organization: Exosome Biology Laboratory, Centre for Clinical Diagnostics, University of Queensland Centre for Clinical Research, Royal Brisbane and Women's Hospital, The University of Queensland, Brisbane, QLD 4029, Australia
– sequence: 12
  givenname: Thomas
  surname: Jansson
  fullname: Jansson, Thomas
  organization: Department of Obstetrics and Gynecology, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, U.S.A
– sequence: 13
  givenname: Harold David
  surname: McIntyre
  fullname: McIntyre, Harold David
  organization: Mater Research, Faculty of Medicine, The University of Queensland, Brisbane, QLD, Australia
– sequence: 14
  givenname: Martha
  surname: Lappas
  fullname: Lappas, Martha
  organization: Obstetrics, Nutrition and Endocrinology Group, Department of Obstetrics and Gynaecology, University of Melbourne, Victoria, Australia; Mercy Perinatal Research Centre, Mercy Hospital for Women, Victoria, Australia
– sequence: 15
  givenname: Carlos
  orcidid: 0000-0003-4474-0046
  surname: Salomon
  fullname: Salomon, Carlos
  email: c.salomongallo@uq.edu.au
  organization: Department of Clinical Biochemistry and Immunology, Faculty of Pharmacy, University of Concepción, Concepción, Chile
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Keywords microRNA
type 2 diabetes
Insulin sensitivity
exosomes
pregnancy
Language English
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Snippet There is increasing evidence that miRNAs, which are enriched in nanovesicles called exosomes, are important regulators of gene expression. When compared with...
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Title Human placental exosomes in gestational diabetes mellitus carry a specific set of miRNAs associated with skeletal muscle insulin sensitivity
URI https://www.ncbi.nlm.nih.gov/pubmed/30254065
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