The Effect of Glucose on the Release and Bioactivity of Exosomes From First Trimester Trophoblast Cells
Context: Hyperglycemia and hypoxia are risk factors of metabolic complication during pregnancy. The interactions between oxygen and glucose-sensing pathways that regulate exosome bioactivity from placental cells, however, have not been established. Objective: The aim of this study was to test the hy...
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Published in | The journal of clinical endocrinology and metabolism Vol. 100; no. 10; pp. E1280 - E1288 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Endocrine Society
01.10.2015
Copyright by The Endocrine Society |
Subjects | |
Online Access | Get full text |
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Abstract | Context:
Hyperglycemia and hypoxia are risk factors of metabolic complication during pregnancy. The interactions between oxygen and glucose-sensing pathways that regulate exosome bioactivity from placental cells, however, have not been established.
Objective:
The aim of this study was to test the hypothesis that exosomal signaling by placental cells (defined as the number of exosomes released per unit time and their bioactivity) is responsive to extracellular glucose concentration.
Methods:
First-trimester primary trophoblast cells were incubated with D-glucose (5 mM or 25 mM) under 1%, 3%, or 8% O2 for 48 hours. Exosomes were isolated from cell-conditioned media by differential and buoyant density centrifugation. The total number of exosome vesicles was determined by quantifying immunoreactive exosomal CD63. The effect of exosomes on cytokine (granulocyte macrophage colony-stimulating factor, IL-2, IL-4, IL-6. IL-8, IL-10, interferon-γ, and TNF-α) release from endothelial cells was established by a protein solution array analysis.
Results:
Glucose (25 mM) significantly increased the release of exosomes from trophoblast cells at all oxygen tensions tested (by approximately 2-fold when compared with controls, P < .001). Exosomes (100 μg/mL exosomal protein) released from trophoblast cells significantly increased (P < .05) the release of all cytokines from human umbilical vein endothelial cells when compared with the control (ie, cells without exosomes), with the exception of IL-2 and IL-10 (P > .05).
Conclusions:
The effects of high glucose on exosomes bioactivity may be recapitulated in vivo and is of clinical relevance in association with maternal insulin resistance (resulting in hyperglycemia) and preeclampsia (associated with placental insufficiency and hypoxia). |
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AbstractList | CONTEXTHyperglycemia and hypoxia are risk factors of metabolic complication during pregnancy. The interactions between oxygen and glucose-sensing pathways that regulate exosome bioactivity from placental cells, however, have not been established.OBJECTIVEThe aim of this study was to test the hypothesis that exosomal signaling by placental cells (defined as the number of exosomes released per unit time and their bioactivity) is responsive to extracellular glucose concentration.METHODSFirst-trimester primary trophoblast cells were incubated with D-glucose (5 mM or 25 mM) under 1%, 3%, or 8% O2 for 48 hours. Exosomes were isolated from cell-conditioned media by differential and buoyant density centrifugation. The total number of exosome vesicles was determined by quantifying immunoreactive exosomal CD63. The effect of exosomes on cytokine (granulocyte macrophage colony-stimulating factor, IL-2, IL-4, IL-6. IL-8, IL-10, interferon-γ, and TNF-α) release from endothelial cells was established by a protein solution array analysis.RESULTSGlucose (25 mM) significantly increased the release of exosomes from trophoblast cells at all oxygen tensions tested (by approximately 2-fold when compared with controls, P < .001). Exosomes (100 μg/mL exosomal protein) released from trophoblast cells significantly increased (P < .05) the release of all cytokines from human umbilical vein endothelial cells when compared with the control (ie, cells without exosomes), with the exception of IL-2 and IL-10 (P > .05).CONCLUSIONSThe effects of high glucose on exosomes bioactivity may be recapitulated in vivo and is of clinical relevance in association with maternal insulin resistance (resulting in hyperglycemia) and preeclampsia (associated with placental insufficiency and hypoxia). Hyperglycemia and hypoxia are risk factors of metabolic complication during pregnancy. The interactions between oxygen and glucose-sensing pathways that regulate exosome bioactivity from placental cells, however, have not been established. The aim of this study was to test the hypothesis that exosomal signaling by placental cells (defined as the number of exosomes released per unit time and their bioactivity) is responsive to extracellular glucose concentration. First-trimester primary trophoblast cells were incubated with D-glucose (5 mM or 25 mM) under 1%, 3%, or 8% O2 for 48 hours. Exosomes were isolated from cell-conditioned media by differential and buoyant density centrifugation. The total number of exosome vesicles was determined by quantifying immunoreactive exosomal CD63. The effect of exosomes on cytokine (granulocyte macrophage colony-stimulating factor, IL-2, IL-4, IL-6. IL-8, IL-10, interferon-γ, and TNF-α) release from endothelial cells was established by a protein solution array analysis. Glucose (25 mM) significantly increased the release of exosomes from trophoblast cells at all oxygen tensions tested (by approximately 2-fold when compared with controls, P < .001). Exosomes (100 μg/mL exosomal protein) released from trophoblast cells significantly increased (P < .05) the release of all cytokines from human umbilical vein endothelial cells when compared with the control (ie, cells without exosomes), with the exception of IL-2 and IL-10 (P > .05). The effects of high glucose on exosomes bioactivity may be recapitulated in vivo and is of clinical relevance in association with maternal insulin resistance (resulting in hyperglycemia) and preeclampsia (associated with placental insufficiency and hypoxia). CONTEXT:Hyperglycemia and hypoxia are risk factors of metabolic complication during pregnancy. The interactions between oxygen and glucose-sensing pathways that regulate exosome bioactivity from placental cells, however, have not been established. OBJECTIVE:The aim of this study was to test the hypothesis that exosomal signaling by placental cells (defined as the number of exosomes released per unit time and their bioactivity) is responsive to extracellular glucose concentration. METHODS:First-trimester primary trophoblast cells were incubated with D-glucose (5 mM or 25 mM) under 1%, 3%, or 8% O2 for 48 hours. Exosomes were isolated from cell-conditioned media by differential and buoyant density centrifugation. The total number of exosome vesicles was determined by quantifying immunoreactive exosomal CD63. The effect of exosomes on cytokine (granulocyte macrophage colony-stimulating factor, IL-2, IL-4, IL-6. IL-8, IL-10, interferon-γ, and TNF-α) release from endothelial cells was established by a protein solution array analysis. RESULTS:Glucose (25 mM) significantly increased the release of exosomes from trophoblast cells at all oxygen tensions tested (by approximately 2-fold when compared with controls, P < .001). Exosomes (100 μg/mL exosomal protein) released from trophoblast cells significantly increased (P < .05) the release of all cytokines from human umbilical vein endothelial cells when compared with the control (ie, cells without exosomes), with the exception of IL-2 and IL-10 (P > .05). CONCLUSIONS:The effects of high glucose on exosomes bioactivity may be recapitulated in vivo and is of clinical relevance in association with maternal insulin resistance (resulting in hyperglycemia) and preeclampsia (associated with placental insufficiency and hypoxia). Context: Hyperglycemia and hypoxia are risk factors of metabolic complication during pregnancy. The interactions between oxygen and glucose-sensing pathways that regulate exosome bioactivity from placental cells, however, have not been established. Objective: The aim of this study was to test the hypothesis that exosomal signaling by placental cells (defined as the number of exosomes released per unit time and their bioactivity) is responsive to extracellular glucose concentration. Methods: First-trimester primary trophoblast cells were incubated with D-glucose (5 mM or 25 mM) under 1%, 3%, or 8% O2 for 48 hours. Exosomes were isolated from cell-conditioned media by differential and buoyant density centrifugation. The total number of exosome vesicles was determined by quantifying immunoreactive exosomal CD63. The effect of exosomes on cytokine (granulocyte macrophage colony-stimulating factor, IL-2, IL-4, IL-6. IL-8, IL-10, interferon-γ, and TNF-α) release from endothelial cells was established by a protein solution array analysis. Results: Glucose (25 mM) significantly increased the release of exosomes from trophoblast cells at all oxygen tensions tested (by approximately 2-fold when compared with controls, P < .001). Exosomes (100 μg/mL exosomal protein) released from trophoblast cells significantly increased (P < .05) the release of all cytokines from human umbilical vein endothelial cells when compared with the control (ie, cells without exosomes), with the exception of IL-2 and IL-10 (P > .05). Conclusions: The effects of high glucose on exosomes bioactivity may be recapitulated in vivo and is of clinical relevance in association with maternal insulin resistance (resulting in hyperglycemia) and preeclampsia (associated with placental insufficiency and hypoxia). |
Author | Kobayashi, Miharu Sweeney, Emma Duncombe, Gregory Mitchell, Murray D Scholz-Romero, Katherin Rice, Gregory E Peiris, Hassendrini Salomon, Carlos |
AuthorAffiliation | Exosome Biology Laboratory, Centre for Clinical Diagnostics, University of Queensland Centre for Clinical Research, Royal Brisbane and Womenʼs Hospital, Brisbane 4029, Queensland, Australia |
AuthorAffiliation_xml | – name: Exosome Biology Laboratory, Centre for Clinical Diagnostics, University of Queensland Centre for Clinical Research, Royal Brisbane and Womenʼs Hospital, Brisbane 4029, Queensland, Australia |
Author_xml | – sequence: 1 givenname: Gregory E surname: Rice fullname: Rice, Gregory E – sequence: 2 givenname: Katherin surname: Scholz-Romero fullname: Scholz-Romero, Katherin – sequence: 3 givenname: Emma surname: Sweeney fullname: Sweeney, Emma – sequence: 4 givenname: Hassendrini surname: Peiris fullname: Peiris, Hassendrini – sequence: 5 givenname: Miharu surname: Kobayashi fullname: Kobayashi, Miharu – sequence: 6 givenname: Gregory surname: Duncombe fullname: Duncombe, Gregory – sequence: 7 givenname: Murray D surname: Mitchell fullname: Mitchell, Murray D – sequence: 8 givenname: Carlos surname: Salomon fullname: Salomon, Carlos email: c.salomongallo@uq.edu.au |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26241326$$D View this record in MEDLINE/PubMed |
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Notes | C.S. was in receipt of a University of Queensland Fellowship. G.E.R. was in receipt of a National Health and Medical Research Council Principal Research Fellowship. The International Organization for Standardization (ISO) 17025-accredited research facility was supported by grants from Therapeutics Innovation Australia and the National Collaborative Research Infrastructure Strategy. This study was partially funded by the Royal Brisbane Foundation. ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
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invasiveness is associated with discordant exosomal sequestration of Let-7 miRNA and miR-200 publication-title: J Transl Med doi: 10.1186/1479-5876-12-4 contributor: fullname: Kobayashi – volume: 12 start-page: 747 year: 2006 ident: 2020071617570422400_B2 article-title: Placental-related diseases of pregnancy: Involvement of oxidative stress and implications in human evolution publication-title: Hum Reprod Update doi: 10.1093/humupd/dml016 contributor: fullname: Jauniaux – volume: 33 start-page: 949 year: 2012 ident: 2020071617570422400_B18 article-title: A high-throughput colorimetric-assay for monitoring glucose consumption by cultured trophoblast cells and placental tissue publication-title: Placenta doi: 10.1016/j.placenta.2012.08.001 contributor: fullname: Hulme |
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Snippet | Context:
Hyperglycemia and hypoxia are risk factors of metabolic complication during pregnancy. The interactions between oxygen and glucose-sensing pathways... CONTEXT:Hyperglycemia and hypoxia are risk factors of metabolic complication during pregnancy. The interactions between oxygen and glucose-sensing pathways... Hyperglycemia and hypoxia are risk factors of metabolic complication during pregnancy. The interactions between oxygen and glucose-sensing pathways that... CONTEXTHyperglycemia and hypoxia are risk factors of metabolic complication during pregnancy. The interactions between oxygen and glucose-sensing pathways that... |
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StartPage | E1280 |
SubjectTerms | Cytokines - metabolism Exosomes - drug effects Exosomes - metabolism Female Glucose - pharmacology Human Umbilical Vein Endothelial Cells - drug effects Human Umbilical Vein Endothelial Cells - metabolism Humans Pregnancy Pregnancy Trimester, First - metabolism Trophoblasts - drug effects Trophoblasts - metabolism |
Title | The Effect of Glucose on the Release and Bioactivity of Exosomes From First Trimester Trophoblast Cells |
URI | http://dx.doi.org/10.1210/jc.2015-2270 http://ovidsp.ovid.com/ovidweb.cgi?T=JS&NEWS=n&CSC=Y&PAGE=fulltext&D=ovft&AN=00004678-201510000-00047 https://www.ncbi.nlm.nih.gov/pubmed/26241326 https://search.proquest.com/docview/1720452974 |
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