Exosomal signaling during hypoxia mediates microvascular endothelial cell migration and vasculogenesis
Vasculogenesis and angiogenesis are critical processes in fetal circulation and placental vasculature development. Placental mesenchymal stem cells (pMSC) are known to release paracrine factors (some of which are contained within exosomes) that promote angiogenesis and cell migration. The aims of th...
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Published in | PloS one Vol. 8; no. 7; p. e68451 |
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Main Authors | , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Public Library of Science
08.07.2013
Public Library of Science (PLoS) |
Subjects | |
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Abstract | Vasculogenesis and angiogenesis are critical processes in fetal circulation and placental vasculature development. Placental mesenchymal stem cells (pMSC) are known to release paracrine factors (some of which are contained within exosomes) that promote angiogenesis and cell migration. The aims of this study were: to determine the effects of oxygen tension on the release of exosomes from pMSC; and to establish the effects of pMSC-derived exosomes on the migration and angiogenic tube formation of placental microvascular endothelial cells (hPMEC). pMSC were isolated from placental villi (8-12 weeks of gestation, n = 6) and cultured under an atmosphere of 1%, 3% or 8% O2. Cell-conditioned media were collected and exosomes (exo-pMSC) isolated by differential and buoyant density centrifugation. The dose effect (5-20 µg exosomal protein/ml) of pMSC-derived exosomes on hPMEC migration and tube formation were established using a real-time, live-cell imaging system (Incucyte™). The exosome pellet was resuspended in PBS and protein content was established by mass spectrometry (MS). Protein function and canonical pathways were identified using the PANTHER program and Ingenuity Pathway Analysis, respectively. Exo-pMSC were identified, by electron microscopy, as spherical vesicles, with a typical cup-shape and diameters around of 100 nm and positive for exosome markers: CD63, CD9 and CD81. Under hypoxic conditions (1% and 3% O2) exo-pMSC released increased by 3.3 and 6.7 folds, respectively, when compared to the controls (8% O2; p<0.01). Exo-pMSC increased hPMEC migration by 1.6 fold compared to the control (p<0.05) and increased hPMEC tube formation by 7.2 fold (p<0.05). MS analysis identified 390 different proteins involved in cytoskeleton organization, development, immunomodulatory, and cell-to-cell communication. The data obtained support the hypothesis that pMSC-derived exosomes may contribute to placental vascular adaptation to low oxygen tension under both physiological and pathological conditions. |
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AbstractList | Vasculogenesis and angiogenesis are critical processes in fetal circulation and placental vasculature development. Placental mesenchymal stem cells (pMSC) are known to release paracrine factors (some of which are contained within exosomes) that promote angiogenesis and cell migration. The aims of this study were: to determine the effects of oxygen tension on the release of exosomes from pMSC; and to establish the effects of pMSC-derived exosomes on the migration and angiogenic tube formation of placental microvascular endothelial cells (hPMEC). pMSC were isolated from placental villi (8–12 weeks of gestation, n = 6) and cultured under an atmosphere of 1%, 3% or 8% O2. Cell-conditioned media were collected and exosomes (exo-pMSC) isolated by differential and buoyant density centrifugation. The dose effect (5–20 µg exosomal protein/ml) of pMSC-derived exosomes on hPMEC migration and tube formation were established using a real-time, live-cell imaging system (Incucyte™). The exosome pellet was resuspended in PBS and protein content was established by mass spectrometry (MS). Protein function and canonical pathways were identified using the PANTHER program and Ingenuity Pathway Analysis, respectively. Exo-pMSC were identified, by electron microscopy, as spherical vesicles, with a typical cup-shape and diameters around of 100 nm and positive for exosome markers: CD63, CD9 and CD81. Under hypoxic conditions (1% and 3% O2) exo-pMSC released increased by 3.3 and 6.7 folds, respectively, when compared to the controls (8% O2; p<0.01). Exo-pMSC increased hPMEC migration by 1.6 fold compared to the control (p<0.05) and increased hPMEC tube formation by 7.2 fold (p<0.05). MS analysis identified 390 different proteins involved in cytoskeleton organization, development, immunomodulatory, and cell-to-cell communication. The data obtained support the hypothesis that pMSC-derived exosomes may contribute to placental vascular adaptation to low oxygen tension under both physiological and pathological conditions. Vasculogenesis and angiogenesis are critical processes in fetal circulation and placental vasculature development. Placental mesenchymal stem cells (pMSC) are known to release paracrine factors (some of which are contained within exosomes) that promote angiogenesis and cell migration. The aims of this study were: to determine the effects of oxygen tension on the release of exosomes from pMSC; and to establish the effects of pMSC-derived exosomes on the migration and angiogenic tube formation of placental microvascular endothelial cells (hPMEC). pMSC were isolated from placental villi (8-12 weeks of gestation, n = 6) and cultured under an atmosphere of 1%, 3% or 8% O.sub.2 . Cell-conditioned media were collected and exosomes (exo-pMSC) isolated by differential and buoyant density centrifugation. The dose effect (5-20 [micro]g exosomal protein/ml) of pMSC-derived exosomes on hPMEC migration and tube formation were established using a real-time, live-cell imaging system (Incucyte[TM]). The exosome pellet was resuspended in PBS and protein content was established by mass spectrometry (MS). Protein function and canonical pathways were identified using the PANTHER program and Ingenuity Pathway Analysis, respectively. Exo-pMSC were identified, by electron microscopy, as spherical vesicles, with a typical cup-shape and diameters around of 100 nm and positive for exosome markers: CD63, CD9 and CD81. Under hypoxic conditions (1% and 3% O.sub.2) exo-pMSC released increased by 3.3 and 6.7 folds, respectively, when compared to the controls (8% O.sub.2 ; p<0.01). Exo-pMSC increased hPMEC migration by 1.6 fold compared to the control (p<0.05) and increased hPMEC tube formation by 7.2 fold (p<0.05). MS analysis identified 390 different proteins involved in cytoskeleton organization, development, immunomodulatory, and cell-to-cell communication. The data obtained support the hypothesis that pMSC-derived exosomes may contribute to placental vascular adaptation to low oxygen tension under both physiological and pathological conditions. Vasculogenesis and angiogenesis are critical processes in fetal circulation and placental vasculature development. Placental mesenchymal stem cells (pMSC) are known to release paracrine factors (some of which are contained within exosomes) that promote angiogenesis and cell migration. The aims of this study were: to determine the effects of oxygen tension on the release of exosomes from pMSC; and to establish the effects of pMSC-derived exosomes on the migration and angiogenic tube formation of placental microvascular endothelial cells (hPMEC). pMSC were isolated from placental villi (8–12 weeks of gestation, n = 6) and cultured under an atmosphere of 1%, 3% or 8% O 2 . Cell-conditioned media were collected and exosomes (exo-pMSC) isolated by differential and buoyant density centrifugation. The dose effect (5–20 µg exosomal protein/ml) of pMSC-derived exosomes on hPMEC migration and tube formation were established using a real-time, live-cell imaging system (Incucyte™). The exosome pellet was resuspended in PBS and protein content was established by mass spectrometry (MS). Protein function and canonical pathways were identified using the PANTHER program and Ingenuity Pathway Analysis, respectively. Exo-pMSC were identified, by electron microscopy, as spherical vesicles, with a typical cup-shape and diameters around of 100 nm and positive for exosome markers: CD63, CD9 and CD81. Under hypoxic conditions (1% and 3% O 2 ) exo-pMSC released increased by 3.3 and 6.7 folds, respectively, when compared to the controls (8% O 2 ; p <0.01). Exo-pMSC increased hPMEC migration by 1.6 fold compared to the control ( p <0.05) and increased hPMEC tube formation by 7.2 fold ( p <0.05). MS analysis identified 390 different proteins involved in cytoskeleton organization, development, immunomodulatory, and cell-to-cell communication. The data obtained support the hypothesis that pMSC-derived exosomes may contribute to placental vascular adaptation to low oxygen tension under both physiological and pathological conditions. |
Audience | Academic |
Author | Kobayashi, Miharu Ryan, Jennifer Sobrevia, Luis Ashman, Keith Rice, Gregory E Mitchell, Murray Salomon, Carlos |
AuthorAffiliation | University of Bristol, United Kingdom 1 University of Queensland Centre for Clinical Research, Herston, Queensland, Australia 2 Cellular and Molecular Physiology Laboratory (CMPL), Division of Obstetrics and Gynaecology, School of Medicine, Faculty of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile |
AuthorAffiliation_xml | – name: 2 Cellular and Molecular Physiology Laboratory (CMPL), Division of Obstetrics and Gynaecology, School of Medicine, Faculty of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile – name: University of Bristol, United Kingdom – name: 1 University of Queensland Centre for Clinical Research, Herston, Queensland, Australia |
Author_xml | – sequence: 1 givenname: Carlos surname: Salomon fullname: Salomon, Carlos email: c.salomongallo@uq.edu.au organization: University of Queensland Centre for Clinical Research, Herston, Queensland, Australia. c.salomongallo@uq.edu.au – sequence: 2 givenname: Jennifer surname: Ryan fullname: Ryan, Jennifer – sequence: 3 givenname: Luis surname: Sobrevia fullname: Sobrevia, Luis – sequence: 4 givenname: Miharu surname: Kobayashi fullname: Kobayashi, Miharu – sequence: 5 givenname: Keith surname: Ashman fullname: Ashman, Keith – sequence: 6 givenname: Murray surname: Mitchell fullname: Mitchell, Murray – sequence: 7 givenname: Gregory E surname: Rice fullname: Rice, Gregory E |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23861904$$D View this record in MEDLINE/PubMed |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Competing Interests: The authors have declared that no competing interests exist. Conceived and designed the experiments: CS GR. Performed the experiments: CS JR MK. Analyzed the data: CS LS KA MM GR. Contributed reagents/materials/analysis tools: CS LS MM GR. Wrote the paper: CS GR. |
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SubjectTerms | Angiogenesis Biology Bone marrow Cancer CD63 antigen CD81 antigen CD9 antigen Cell adhesion & migration Cell Hypoxia - drug effects Cell interactions Cell migration Cell Movement - drug effects Centrifugation Conditioning Cytoskeleton Electron microscopy Endothelial cells Endothelial Cells - cytology Endothelial Cells - drug effects Endothelial Cells - metabolism Endothelium Exosomes Exosomes - drug effects Exosomes - metabolism Female Fetuses Gestation Humans Hypoxia Immunomodulation Kinases Kinetics Laboratories Mass Spectrometry Mass spectroscopy Media (differential) Medicine Mesenchymal Stromal Cells - cytology Mesenchymal Stromal Cells - drug effects Mesenchymal Stromal Cells - metabolism Mesenchyme Metastasis Microvasculature Microvessels - cytology Neovascularization, Physiologic - drug effects Oxygen Oxygen - pharmacology Oxygen tension Paracrine signalling Physiology Placenta Placenta - cytology Pregnancy Proteins Proteomics Signal Transduction - drug effects Software Stem cells Tension Transplants & implants |
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Title | Exosomal signaling during hypoxia mediates microvascular endothelial cell migration and vasculogenesis |
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