Endothelin-1 down-regulates matrix metalloproteinase 14 and 15 expression in human first trimester trophoblasts via endothelin receptor type B
STUDY QUESTION Does endothelin-1 (ET-1) regulate matrix metalloproteinase (MMP) 14 and 15 production and invasion of human first trimester trophoblasts? SUMMARY ANSWER ET-1 in pathophysiological concentrations down-regulates MMP14 and MMP15 expression via endothelin receptor (ETR) type B and decreas...
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| Published in: | Human reproduction (Oxford) Vol. 32; no. 1; pp. 46 - 54 |
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| ISSN: | 0268-1161, 1460-2350 |
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| Abstract | STUDY QUESTION
Does endothelin-1 (ET-1) regulate matrix metalloproteinase (MMP) 14 and 15 production and invasion of human first trimester trophoblasts?
SUMMARY ANSWER
ET-1 in pathophysiological concentrations down-regulates MMP14 and MMP15 expression via endothelin receptor (ETR) type B and decreases trophoblast migration and invasion.
WHAT IS KNOWN ALREADY
MMP14 and MMP15 are involved in trophoblast invasion. Impairment of invasion has been linked to pregnancy complications such as pre-eclampsia (PE). ET-1 is up-regulated in PE.
STUDY DESIGN, SIZE, DURATION
In vitro study using primary human trophoblasts from 50 first trimester placentas (gestational week 7–12).
PARTICIPANTS/MATERIALS, SETTING, METHODS
Trophoblasts were cultured in the absence or presence of 10–100 nM ET-1. MMP14 and MMP15 mRNA and protein were quantified by RT-qPCR and Western blotting, respectively. Selective antagonists for ETRA (BQ-123) or ETRB (BQ-788) were used to identify ETR subtypes involved. Functional ET-1 effects were tested in first trimester chorionic villous explants and transwell invasion assays. The roles of tumor necrosis factor (TNF)-α (25 ng/ml) and oxygen (1%) in ET-1 regulation of MMP14 and 15 expression were assessed by Western blotting.
MAIN RESULTS AND THE ROLE OF CHANCE
ET-1 down-regulated MMP14 and MMP15 mRNA (−21% and −26%, respectively, P < 0.05) and protein levels (–18% and –22%, respectively, P < 0.05). This effect was mediated via ETRB. ET-1 decreased trophoblast outgrowth in placental explants (−24%, P < 0.05) and trophoblast invasion (−26%, P ≤ 0.01). TNF-α enhanced ET-1 mediated MMP15 down-regulation (by 10%, P < 0.05), whereas hypoxia abolished the effect of ET-1 on both MMPs.
LARGE SCALE DATA
N/A.
LIMITATIONS, REASONS FOR CAUTION
Only primary trophoblasts were used in this study. Since trophoblast yield from first trimester placental material is limited, further aspects of MMP14 and 15 regulation could not be characterized. Other anti-invasive factors may be altered by ET-1 in trophoblasts and, thus, contribute to the reduced invasion, but have not been investigated. Oxygen levels similar to those found in the decidua (5–8% O2) were not analyzed in this study.
WIDER IMPLICATIONS OF THE FINDINGS
ET-1 modifies placental function already during the first trimester of pregnancy, the time-window when the placental changes implicated in PE occur. Thus, our results improve the understanding of the placental mechanisms underlying trophoblast invasion and PE.
STUDY FUNDING/COMPETING INTEREST(S)
The study was funded by the Oesterreichische Nationalbank (Anniversary Fund, project number: 14796) and the Herzfelder'sche Familienstiftung (to J.P.; number: 00685). AMM received funding from the Austrian Science Fund FWF (W1241) and the Medical University Graz through the PhD Program Molecular Fundamentals of Inflammation (DK-MOLIN). The authors have no conflict of interest. |
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| AbstractList | Does endothelin-1 (ET-1) regulate matrix metalloproteinase (MMP) 14 and 15 production and invasion of human first trimester trophoblasts?
ET-1 in pathophysiological concentrations down-regulates MMP14 and MMP15 expression via endothelin receptor (ETR) type B and decreases trophoblast migration and invasion.
MMP14 and MMP15 are involved in trophoblast invasion. Impairment of invasion has been linked to pregnancy complications such as pre-eclampsia (PE). ET-1 is up-regulated in PE.
In vitro study using primary human trophoblasts from 50 first trimester placentas (gestational week 7-12).
Trophoblasts were cultured in the absence or presence of 10-100 nM ET-1. MMP14 and MMP15 mRNA and protein were quantified by RT-qPCR and Western blotting, respectively. Selective antagonists for ETRA (BQ-123) or ETRB (BQ-788) were used to identify ETR subtypes involved. Functional ET-1 effects were tested in first trimester chorionic villous explants and transwell invasion assays. The roles of tumor necrosis factor (TNF)-α (25 ng/ml) and oxygen (1%) in ET-1 regulation of MMP14 and 15 expression were assessed by Western blotting.
ET-1 down-regulated MMP14 and MMP15 mRNA (-21% and -26%, respectively, P < 0.05) and protein levels (-18% and -22%, respectively, P < 0.05). This effect was mediated via ETRB. ET-1 decreased trophoblast outgrowth in placental explants (-24%, P < 0.05) and trophoblast invasion (-26%, P ≤ 0.01). TNF-α enhanced ET-1 mediated MMP15 down-regulation (by 10%, P < 0.05), whereas hypoxia abolished the effect of ET-1 on both MMPs.
N/A.
Only primary trophoblasts were used in this study. Since trophoblast yield from first trimester placental material is limited, further aspects of MMP14 and 15 regulation could not be characterized. Other anti-invasive factors may be altered by ET-1 in trophoblasts and, thus, contribute to the reduced invasion, but have not been investigated. Oxygen levels similar to those found in the decidua (5-8% O
) were not analyzed in this study.
ET-1 modifies placental function already during the first trimester of pregnancy, the time-window when the placental changes implicated in PE occur. Thus, our results improve the understanding of the placental mechanisms underlying trophoblast invasion and PE.
The study was funded by the Oesterreichische Nationalbank (Anniversary Fund, project number: 14796) and the Herzfelder'sche Familienstiftung (to J.P.; number: 00685). AMM received funding from the Austrian Science Fund FWF (W1241) and the Medical University Graz through the PhD Program Molecular Fundamentals of Inflammation (DK-MOLIN). The authors have no conflict of interest. STUDY QUESTIONDoes endothelin-1 (ET-1) regulate matrix metalloproteinase (MMP) 14 and 15 production and invasion of human first trimester trophoblasts?SUMMARY ANSWERET-1 in pathophysiological concentrations down-regulates MMP14 and MMP15 expression via endothelin receptor (ETR) type B and decreases trophoblast migration and invasion.WHAT IS KNOWN ALREADYMMP14 and MMP15 are involved in trophoblast invasion. Impairment of invasion has been linked to pregnancy complications such as pre-eclampsia (PE). ET-1 is up-regulated in PE.STUDY DESIGN, SIZE, DURATIONIn vitro study using primary human trophoblasts from 50 first trimester placentas (gestational week 7-12).PARTICIPANTS/MATERIALS, SETTING, METHODSTrophoblasts were cultured in the absence or presence of 10-100 nM ET-1. MMP14 and MMP15 mRNA and protein were quantified by RT-qPCR and Western blotting, respectively. Selective antagonists for ETRA (BQ-123) or ETRB (BQ-788) were used to identify ETR subtypes involved. Functional ET-1 effects were tested in first trimester chorionic villous explants and transwell invasion assays. The roles of tumor necrosis factor (TNF)-α (25 ng/ml) and oxygen (1%) in ET-1 regulation of MMP14 and 15 expression were assessed by Western blotting.MAIN RESULTS AND THE ROLE OF CHANCEET-1 down-regulated MMP14 and MMP15 mRNA (-21% and -26%, respectively, P < 0.05) and protein levels (-18% and -22%, respectively, P < 0.05). This effect was mediated via ETRB. ET-1 decreased trophoblast outgrowth in placental explants (-24%, P < 0.05) and trophoblast invasion (-26%, P ≤ 0.01). TNF-α enhanced ET-1 mediated MMP15 down-regulation (by 10%, P < 0.05), whereas hypoxia abolished the effect of ET-1 on both MMPs.LARGE SCALE DATAN/A.LIMITATIONS, REASONS FOR CAUTIONOnly primary trophoblasts were used in this study. Since trophoblast yield from first trimester placental material is limited, further aspects of MMP14 and 15 regulation could not be characterized. Other anti-invasive factors may be altered by ET-1 in trophoblasts and, thus, contribute to the reduced invasion, but have not been investigated. Oxygen levels similar to those found in the decidua (5-8% O2) were not analyzed in this study.WIDER IMPLICATIONS OF THE FINDINGSET-1 modifies placental function already during the first trimester of pregnancy, the time-window when the placental changes implicated in PE occur. Thus, our results improve the understanding of the placental mechanisms underlying trophoblast invasion and PE.STUDY FUNDING/COMPETING INTERESTSThe study was funded by the Oesterreichische Nationalbank (Anniversary Fund, project number: 14796) and the Herzfelder'sche Familienstiftung (to J.P.; number: 00685). AMM received funding from the Austrian Science Fund FWF (W1241) and the Medical University Graz through the PhD Program Molecular Fundamentals of Inflammation (DK-MOLIN). The authors have no conflict of interest. STUDY QUESTION Does endothelin-1 (ET-1) regulate matrix metalloproteinase (MMP) 14 and 15 production and invasion of human first trimester trophoblasts? SUMMARY ANSWER ET-1 in pathophysiological concentrations down-regulates MMP14 and MMP15 expression via endothelin receptor (ETR) type B and decreases trophoblast migration and invasion. WHAT IS KNOWN ALREADY MMP14 and MMP15 are involved in trophoblast invasion. Impairment of invasion has been linked to pregnancy complications such as pre-eclampsia (PE). ET-1 is up-regulated in PE. STUDY DESIGN, SIZE, DURATION In vitro study using primary human trophoblasts from 50 first trimester placentas (gestational week 7–12). PARTICIPANTS/MATERIALS, SETTING, METHODS Trophoblasts were cultured in the absence or presence of 10–100 nM ET-1. MMP14 and MMP15 mRNA and protein were quantified by RT-qPCR and Western blotting, respectively. Selective antagonists for ETRA (BQ-123) or ETRB (BQ-788) were used to identify ETR subtypes involved. Functional ET-1 effects were tested in first trimester chorionic villous explants and transwell invasion assays. The roles of tumor necrosis factor (TNF)-α (25 ng/ml) and oxygen (1%) in ET-1 regulation of MMP14 and 15 expression were assessed by Western blotting. MAIN RESULTS AND THE ROLE OF CHANCE ET-1 down-regulated MMP14 and MMP15 mRNA (−21% and −26%, respectively, P < 0.05) and protein levels (–18% and –22%, respectively, P < 0.05). This effect was mediated via ETRB. ET-1 decreased trophoblast outgrowth in placental explants (−24%, P < 0.05) and trophoblast invasion (−26%, P ≤ 0.01). TNF-α enhanced ET-1 mediated MMP15 down-regulation (by 10%, P < 0.05), whereas hypoxia abolished the effect of ET-1 on both MMPs. LARGE SCALE DATA N/A. LIMITATIONS, REASONS FOR CAUTION Only primary trophoblasts were used in this study. Since trophoblast yield from first trimester placental material is limited, further aspects of MMP14 and 15 regulation could not be characterized. Other anti-invasive factors may be altered by ET-1 in trophoblasts and, thus, contribute to the reduced invasion, but have not been investigated. Oxygen levels similar to those found in the decidua (5–8% O2) were not analyzed in this study. WIDER IMPLICATIONS OF THE FINDINGS ET-1 modifies placental function already during the first trimester of pregnancy, the time-window when the placental changes implicated in PE occur. Thus, our results improve the understanding of the placental mechanisms underlying trophoblast invasion and PE. STUDY FUNDING/COMPETING INTEREST(S) The study was funded by the Oesterreichische Nationalbank (Anniversary Fund, project number: 14796) and the Herzfelder'sche Familienstiftung (to J.P.; number: 00685). AMM received funding from the Austrian Science Fund FWF (W1241) and the Medical University Graz through the PhD Program Molecular Fundamentals of Inflammation (DK-MOLIN). The authors have no conflict of interest. |
| Author | Burton, Graham J. Knöfler, Martin Hiden, Ursula Majali-Martinez, Alejandro Tabrizi-Wizsy, Nassim Ghaffari Velicky, Philipp Pollheimer, Jürgen Desoye, Gernot Dieber-Rotheneder, Martina Yung, Hong wa Lang, Uwe |
| Author_xml | – sequence: 1 givenname: Alejandro surname: Majali-Martinez fullname: Majali-Martinez, Alejandro organization: 1 Department of Obstetrics and Gynecology, Medical University of Graz, Auenbruggerplatz 14, Graz 8036, Austria – sequence: 2 givenname: Philipp surname: Velicky fullname: Velicky, Philipp organization: 2 Department of Obstetrics and Fetal-Maternal Medicine, Medical University of Vienna, Währinger Gürtel 18-20, Vienna 1090, Austria – sequence: 3 givenname: Jürgen surname: Pollheimer fullname: Pollheimer, Jürgen organization: 2 Department of Obstetrics and Fetal-Maternal Medicine, Medical University of Vienna, Währinger Gürtel 18-20, Vienna 1090, Austria – sequence: 4 givenname: Martin surname: Knöfler fullname: Knöfler, Martin organization: 2 Department of Obstetrics and Fetal-Maternal Medicine, Medical University of Vienna, Währinger Gürtel 18-20, Vienna 1090, Austria – sequence: 5 givenname: Hong wa surname: Yung fullname: Yung, Hong wa organization: 3 Department of Physiology, Development and Neuroscience, Centre for Trophoblast Research, University of Cambridge, Downing Street, Cambridge CB2 3 EG, UK – sequence: 6 givenname: Graham J. surname: Burton fullname: Burton, Graham J. organization: 3 Department of Physiology, Development and Neuroscience, Centre for Trophoblast Research, University of Cambridge, Downing Street, Cambridge CB2 3 EG, UK – sequence: 7 givenname: Nassim Ghaffari surname: Tabrizi-Wizsy fullname: Tabrizi-Wizsy, Nassim Ghaffari organization: 4 Institute of Pathophysiology and Immunology, SFL Chicken CAM Lab, Medical University of Graz, Heinrichstrasse 31a, Graz 8010, Austria – sequence: 8 givenname: Uwe surname: Lang fullname: Lang, Uwe organization: 1 Department of Obstetrics and Gynecology, Medical University of Graz, Auenbruggerplatz 14, Graz 8036, Austria – sequence: 9 givenname: Ursula surname: Hiden fullname: Hiden, Ursula email: ursula.hiden@medunigraz.at organization: 1 Department of Obstetrics and Gynecology, Medical University of Graz, Auenbruggerplatz 14, Graz 8036, Austria – sequence: 10 givenname: Gernot surname: Desoye fullname: Desoye, Gernot organization: 1 Department of Obstetrics and Gynecology, Medical University of Graz, Auenbruggerplatz 14, Graz 8036, Austria – sequence: 11 givenname: Martina surname: Dieber-Rotheneder fullname: Dieber-Rotheneder, Martina organization: 1 Department of Obstetrics and Gynecology, Medical University of Graz, Auenbruggerplatz 14, Graz 8036, Austria |
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| Keywords | hypoxia invasion inflammation MMPs pre-eclampsia endothelin-1 trophoblast |
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| Snippet | STUDY QUESTION
Does endothelin-1 (ET-1) regulate matrix metalloproteinase (MMP) 14 and 15 production and invasion of human first trimester trophoblasts?... Does endothelin-1 (ET-1) regulate matrix metalloproteinase (MMP) 14 and 15 production and invasion of human first trimester trophoblasts? ET-1 in... STUDY QUESTIONDoes endothelin-1 (ET-1) regulate matrix metalloproteinase (MMP) 14 and 15 production and invasion of human first trimester trophoblasts?SUMMARY... |
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| SubjectTerms | Cell Proliferation - drug effects Dose-Response Relationship, Drug Down-Regulation - drug effects Endothelin-1 - pharmacology Female Humans Matrix Metalloproteinase 14 - genetics Matrix Metalloproteinase 14 - metabolism Matrix Metalloproteinase 15 - genetics Matrix Metalloproteinase 15 - metabolism Placenta - drug effects Placenta - metabolism Pregnancy Pregnancy Trimester, First - metabolism Receptor, Endothelin B - genetics Receptor, Endothelin B - metabolism Trophoblasts - drug effects Trophoblasts - metabolism Tumor Necrosis Factor-alpha - pharmacology |
| Title | Endothelin-1 down-regulates matrix metalloproteinase 14 and 15 expression in human first trimester trophoblasts via endothelin receptor type B |
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