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Article ; Online: Serotonin-estrogen interactions: What can we learn from pregnancy?

Hudon Thibeault, Andrée-Anne / Sanderson, J Thomas / Vaillancourt, Cathy

2019 Volume 161, Page(s) 88–108

Abstract: We have reviewed the scientific literature related to four diseases in which to serotonin (5-HT) is involved in the etiology, herein named 5-HT-linked diseases, and whose prevalence is influenced by estrogenic status: depression, migraine, irritable ... ...

Abstract	We have reviewed the scientific literature related to four diseases in which to serotonin (5-HT) is involved in the etiology, herein named 5-HT-linked diseases, and whose prevalence is influenced by estrogenic status: depression, migraine, irritable bowel syndrome and eating disorders. These diseases all have in common a sex-dimorphic prevalence, with women more frequently affected than men. The co-occurrence between these 5-HT-linked diseases suggests that they have common physiopathological mechanisms. In most 5-HT-linked diseases (except for anorexia nervosa and irritable bowel syndrome), a decrease in the serotonergic tone is observed and estrogens are thought to contribute to the improvement of symptoms by stimulating the serotonergic system. Human pregnancy is characterized by a unique 5-HT and estrogen synthesis by the placenta. Pregnancy-specific disorders, such as hyperemesis gravidarum, gestational diabetes mellitus and pre-eclampsia, are associated with a hyperserotonergic state and decreased estrogen levels. Fetal programming of 5-HT-linked diseases is a complex phenomenon that involves notably fetal-sex differences, which suggest the implication of sex steroids. From a mechanistic point of view, we hypothesize that estrogens regulate the serotonergic system, resulting in a protective effect against 5-HT-linked diseases, but that, in turn, 5-HT affects estrogen synthesis in an attempt to retrieve homeostasis. These two processes (5-HT and estrogen biosynthesis) are crucial for successful pregnancy outcomes, and thus, a disruption of this 5-HT-estrogen relationship may explain pregnancy-specific pathologies or pregnancy complications associated with 5-HT-linked diseases.
MeSH term(s)	Drug Interactions ; Estrogens/metabolism ; Female ; Humans ; Placenta/metabolism ; Placenta/physiopathology ; Pregnancy ; Pregnancy Complications/metabolism ; Pregnancy Complications/physiopathology ; Serotonin/metabolism
Chemical Substances	Estrogens ; Serotonin (333DO1RDJY)
Language	English
Publishing date	2019-04-01
Publishing country	France
Document type	Journal Article ; Review
ZDB-ID	120345-9
ISSN	1638-6183 ; 0300-9084
ISSN (online)	1638-6183
ISSN	0300-9084
DOI	10.1016/j.biochi.2019.03.023
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Article ; Online: Evaluating the effects on steroidogenesis of estragole and trans-anethole in a feto-placental co-culture model.

Yancu, Debbie / Vaillancourt, Cathy / Sanderson, J Thomas

Molecular and cellular endocrinology

2019 Volume 498, Page(s) 110583

Abstract: In this study, we determined whether estragole and its isomer trans-anethole interfered with feto-placental steroidogenesis in a human co-culture model composed of fetal-like adrenocortical (H295R) and placental trophoblast-like (BeWo) cells. Estragole ... ...

Abstract	In this study, we determined whether estragole and its isomer trans-anethole interfered with feto-placental steroidogenesis in a human co-culture model composed of fetal-like adrenocortical (H295R) and placental trophoblast-like (BeWo) cells. Estragole and trans-anethole are considered the biologically active compounds within basil and fennel seed essential oils, respectively. After a 24 h exposure of the co-culture to 2.5, 5.2 and 25 μM estragole or trans-anethole, hormone concentrations of estradiol, estrone, dehydroepiandrosterone, androstenedione, progesterone and estriol were significantly increased. Using RT-qPCR, estragole and trans-anethole were shown to significantly alter the expression of several key steroidogenic enzymes, such as those involved in cholesterol transport and steroid hormone biosynthesis, including StAR, CYP11A1, HSD3B1/2, SULT2A1, and HSD17B1, -4, and -5. Furthermore, we provided mechanistic insight into the ability of estragole and trans-anethole to stimulate promoter-specific expression of CYP19 through activation of the PKA pathway in H295R cells and the PKC pathway in BeWo cells, in both cases associated with increased cAMP levels. Moreover, we show new evidence suggesting a role for progesterone in regulating steroid hormone biosynthesis through regulation of the StAR gene.
MeSH term(s)	Adrenal Cortex Neoplasms/drug therapy ; Adrenal Cortex Neoplasms/metabolism ; Adrenal Cortex Neoplasms/pathology ; Adrenocortical Carcinoma/drug therapy ; Adrenocortical Carcinoma/metabolism ; Adrenocortical Carcinoma/pathology ; Anisoles/pharmacology ; Aromatase/genetics ; Aromatase/metabolism ; Cell Survival ; Choriocarcinoma/drug therapy ; Choriocarcinoma/metabolism ; Choriocarcinoma/pathology ; Coculture Techniques ; Estradiol Dehydrogenases/genetics ; Estradiol Dehydrogenases/metabolism ; Female ; Fetus/drug effects ; Fetus/metabolism ; Flavoring Agents/pharmacology ; Gene Expression Regulation, Neoplastic/drug effects ; Humans ; Oils, Volatile/pharmacology ; Placenta/drug effects ; Placenta/metabolism ; Pregnancy ; Steroids/metabolism ; Tumor Cells, Cultured
Chemical Substances	Anisoles ; Flavoring Agents ; Oils, Volatile ; Steroids ; estragole (9NIW07V3ET) ; Estradiol Dehydrogenases (EC 1.1.1.62) ; HSD17B1 protein, human (EC 1.1.1.62) ; Aromatase (EC 1.14.14.1) ; anethole (Q3JEK5DO4K)
Language	English
Publishing date	2019-09-16
Publishing country	Ireland
Document type	Evaluation Study ; Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	187438-x
ISSN	1872-8057 ; 0303-7207
ISSN (online)	1872-8057
ISSN	0303-7207
DOI	10.1016/j.mce.2019.110583
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Article: Evaluating the effects on steroidogenesis of estragole and trans-anethole in a feto-placental co-culture model

Yancu, Debbie / Sanderson, J. Thomas / Vaillancourt, Cathy

Molecular and cellular endocrinology. 2019 Dec. 01, v. 498

2019

Abstract	In this study, we determined whether estragole and its isomer trans-anethole interfered with feto-placental steroidogenesis in a human co-culture model composed of fetal-like adrenocortical (H295R) and placental trophoblast-like (BeWo) cells. Estragole and trans-anethole are considered the biologically active compounds within basil and fennel seed essential oils, respectively. After a 24 h exposure of the co-culture to 2.5, 5.2 and 25 μM estragole or trans-anethole, hormone concentrations of estradiol, estrone, dehydroepiandrosterone, androstenedione, progesterone and estriol were significantly increased. Using RT-qPCR, estragole and trans-anethole were shown to significantly alter the expression of several key steroidogenic enzymes, such as those involved in cholesterol transport and steroid hormone biosynthesis, including StAR, CYP11A1, HSD3B1/2, SULT2A1, and HSD17B1, -4, and -5. Furthermore, we provided mechanistic insight into the ability of estragole and trans-anethole to stimulate promoter-specific expression of CYP19 through activation of the PKA pathway in H295R cells and the PKC pathway in BeWo cells, in both cases associated with increased cAMP levels. Moreover, we show new evidence suggesting a role for progesterone in regulating steroid hormone biosynthesis through regulation of the StAR gene.
Keywords	androstenedione ; basil ; bioactive compounds ; biosynthesis ; cAMP-dependent protein kinase ; cholesterol ; coculture ; cyclic AMP ; essential oils ; estradiol ; estriol ; estrone ; fennel ; genes ; humans ; isomers ; methyl chavicol ; models ; prasterone ; progesterone ; protein kinase C ; quantitative polymerase chain reaction ; reverse transcriptase polymerase chain reaction ; steroid hormones ; steroidogenesis
Language	English
Dates of publication	2019-1201
Publishing place	Elsevier B.V.
Document type	Article
ZDB-ID	187438-x
ISSN	1872-8057 ; 0303-7207
ISSN (online)	1872-8057
ISSN	0303-7207
DOI	10.1016/j.mce.2019.110583
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Article ; Online: Effects of Neonicotinoid Pesticides on Promoter-Specific Aromatase (CYP19) Expression in Hs578t Breast Cancer Cells and the Role of the VEGF Pathway.

Caron-Beaudoin, Élyse / Viau, Rachel / Sanderson, J Thomas

Environmental health perspectives

2018 Volume 126, Issue 4, Page(s) 47014

Abstract: Background: Aromatase (CYP19) is a key enzyme in estrogens biosynthesis. In the mammary gland, : Objective: We aimed to determine the effects of two neonicotinoids (thiacloprid and imidacloprid) on promoter-specific : Methods: Hs578t cells were ... ...

Abstract	Background: Aromatase (CYP19) is a key enzyme in estrogens biosynthesis. In the mammary gland, Objective: We aimed to determine the effects of two neonicotinoids (thiacloprid and imidacloprid) on promoter-specific Methods: Hs578t cells were exposed to various signaling pathway stimulants or neonicotinoids for 24 h. Promoter-specific expression of Results: To our knowledge, we are the first to demonstrate that the normal I.4 promoter and the breast cancer-relevant PII, I.3, and I.7 promoters of Conclusions: We demonstrated
MeSH term(s)	Aromatase/genetics ; Aromatase/metabolism ; Cell Line, Tumor ; Gene Expression Regulation, Neoplastic ; Humans ; Insecticides/toxicity ; Neonicotinoids/toxicity ; Nitro Compounds/toxicity ; Signal Transduction/drug effects ; Thiazines/toxicity ; Vascular Endothelial Growth Factor A/genetics ; Vascular Endothelial Growth Factor A/metabolism
Chemical Substances	Insecticides ; Neonicotinoids ; Nitro Compounds ; Thiazines ; VEGFA protein, human ; Vascular Endothelial Growth Factor A ; imidacloprid (3BN7M937V8) ; thiacloprid (DSV3A944A4) ; Aromatase (EC 1.14.14.1) ; CYP19A1 protein, human (EC 1.14.14.1)
Language	English
Publishing date	2018-04-26
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	195189-0
ISSN	1552-9924 ; 0091-6765 ; 1078-0475
ISSN (online)	1552-9924
ISSN	0091-6765 ; 1078-0475
DOI	10.1289/EHP2698
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Article ; Online: Profile of CYP19A1 mRNA expression and aromatase activity during syncytialization of primary human villous trophoblast cells at term.

Hudon Thibeault, Andrée-Anne / Vaillancourt, Cathy / Sanderson, J Thomas

Biochimie

2018 Volume 148, Page(s) 12–17

Abstract: Estrogen production by the human villous trophoblast is dependent on the biosynthetic enzyme aromatase (CYP19; CYP19A1) and is crucial for successful placental development and pregnancy outcome. Using villous cytotrophoblast cells (vCTs) freshly isolated ...

Abstract	Estrogen production by the human villous trophoblast is dependent on the biosynthetic enzyme aromatase (CYP19; CYP19A1) and is crucial for successful placental development and pregnancy outcome. Using villous cytotrophoblast cells (vCTs) freshly isolated from normal term placenta, we characterized the promoter-specific expression of CYP19A1 mRNA (derived from promoters I.1, I.4, I.8 or total transcript) and aromatase activity during villous trophoblast syncytialization. CYP19A1 mRNA levels and aromatase activity in vCTs reached a maximum after about 48 h of culture. The cAMP inducer forskolin (10 μM) and protein kinase C stimulant phorbol myristate acetate (1 μM) increased CYP19A1 mRNA levels by 1.8- and 1.6-fold, respectively, as well as inducing aromatase catalytic activity. Dexamethasone (100 nM) and vascular endothelial growth factor (5 ng/mL) decreased CYP19A1 mRNA levels, while having no effect on aromatase activity. Our results emphasize the importance of not solely studying CYP19A1 regulation and function at the mRNA level but also considering posttranslational mechanisms that alter the final catalytic activity of aromatase.
MeSH term(s)	Aromatase/genetics ; Aromatase/metabolism ; Cell Differentiation ; Chorionic Villi/metabolism ; Gene Expression Regulation, Enzymologic ; Humans ; RNA, Messenger/genetics ; RNA, Messenger/metabolism ; Trophoblasts/cytology ; Trophoblasts/metabolism
Chemical Substances	RNA, Messenger ; Aromatase (EC 1.14.14.1) ; CYP19A1 protein, human (EC 1.14.14.1)
Language	English
Publishing date	2018-02-21
Publishing country	France
Document type	Journal Article
ZDB-ID	120345-9
ISSN	1638-6183 ; 0300-9084
ISSN (online)	1638-6183
ISSN	0300-9084
DOI	10.1016/j.biochi.2018.02.010
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Article: Placental and fetal steroidogenesis.

Sanderson, J Thomas

Methods in molecular biology (Clifton, N.J.)

2009 Volume 550, Page(s) 127–136

Abstract: Steroid hormones are essential for maintenance of pregnancy and fetal development. The expression and catalytic activity of the key steroidogenic enzymes involved in the production of progesterone and estrogens increase during pregnancy, and there is an ... ...

Abstract	Steroid hormones are essential for maintenance of pregnancy and fetal development. The expression and catalytic activity of the key steroidogenic enzymes involved in the production of progesterone and estrogens increase during pregnancy, and there is an intricate communication between the mother, the placenta, and the fetus in order to maintain a balanced supply of the steroid hormones essential for embryogenesis. This chapter describes methods for the measurement of the expression and catalytic activity of three key cytochrome P450 (CYP) enzymes involved in the production of progesterone and estrogens, aromatase (CYP19), steroid 17-hydroxylase/17,20-lyase (CYP17), and cholesterol side-chain cleavage (CYP11A).
MeSH term(s)	Aromatase/metabolism ; Base Sequence ; DNA Primers ; Female ; Fetus/metabolism ; Humans ; Placenta/metabolism ; Pregnancy ; RNA, Messenger/genetics ; Reverse Transcriptase Polymerase Chain Reaction ; Steroids/biosynthesis ; Steroids/metabolism ; Tumor Cells, Cultured
Chemical Substances	DNA Primers ; RNA, Messenger ; Steroids ; Aromatase (EC 1.14.14.1)
Language	English
Publishing date	2009
Publishing country	United States
Document type	Journal Article
ISSN	1064-3745
ISSN	1064-3745
DOI	10.1007/978-1-60327-009-0_7
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Article ; Online: Erratum: A Unique Co-Culture Model for Fundamental and Applied Studies of Human Fetoplacental Steroidogenesis and Interference by Environmental Chemicals.

Hudon Thibeault, Andrée-Anne / Deroy, Kathy / Vaillancourt, Cathy / Sanderson, J Thomas

Environmental health perspectives

2019 Volume 127, Issue 5, Page(s) 59003

Language	English
Publishing date	2019-05-31
Publishing country	United States
Document type	Journal Article ; Published Erratum
ZDB-ID	195189-0
ISSN	1552-9924 ; 0091-6765 ; 1078-0475
ISSN (online)	1552-9924
ISSN	0091-6765 ; 1078-0475
DOI	10.1289/EHP5506
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Article ; Online: Co-culture of H295R Adrenocortical Carcinoma and BeWo Choriocarcinoma Cells to Study Feto-placental Interactions: Focus on Estrogen Biosynthesis.

Thibeault, Andrée-Anne Hudon / Sanderson, J Thomas / Vaillancourt, Cathy

Methods in molecular biology (Clifton, N.J.)

2017 Volume 1710, Page(s) 295–304

Abstract: Estrogens are produced in large amounts during pregnancy, as a result of a tightly regulated cooperation between the maternal and fetal adrenal cortex, which produce androgen precursors, and the placental villous trophoblast, which transforms these ... ...

Abstract	Estrogens are produced in large amounts during pregnancy, as a result of a tightly regulated cooperation between the maternal and fetal adrenal cortex, which produce androgen precursors, and the placental villous trophoblast, which transforms these precursors into estrogens. These estrogens play an important role in proper placental function, in adaptation of the mother to pregnancy, as well as in adequate fetal development. Disruption of estrogen production is associated with poor pregnancy outcomes and fetal malformation or altered fetal programming. Pregnant women may be exposed to endocrine disruptors from environmental sources or medications, and it is crucial to study the effects of such compounds on feto-placental steroidogenesis. The H295R/BeWo co-culture model offers the opportunity to study these interactions, by making it possible to evaluate the effects of chemical exposures on androgen and estrogen biosynthesis, as well as on various other aspects of feto-placental communication.
MeSH term(s)	Adrenocortical Carcinoma/metabolism ; Biosynthetic Pathways ; Cell Line, Tumor ; Choriocarcinoma/metabolism ; Coculture Techniques/methods ; Estrogens/metabolism ; Female ; Fetus/cytology ; Fetus/metabolism ; Humans ; Placenta/cytology ; Placenta/metabolism ; Pregnancy ; Trophoblasts/cytology ; Trophoblasts/metabolism
Chemical Substances	Estrogens
Language	English
Publishing date	2017-11-28
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-4939-7498-6_23
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Article ; Online: Effects of selective serotonin-reuptake inhibitors (SSRIs) in JEG-3 and HIPEC cell models of the extravillous trophoblast.

Clabault, Hélène / Cohen, Marie / Vaillancourt, Cathy / Sanderson, J Thomas

Placenta

2018 Volume 72-73, Page(s) 62–73

Abstract: Introduction: Between 2 and 10% of pregnant women are treated with selective serotonin-reuptake inhibitors (SSRIs) for depression. The extravillous trophoblasts (evTBs), which migrate and invade maternal tissues, are crucial for embryo implantation and ... ...

Abstract	Introduction: Between 2 and 10% of pregnant women are treated with selective serotonin-reuptake inhibitors (SSRIs) for depression. The extravillous trophoblasts (evTBs), which migrate and invade maternal tissues, are crucial for embryo implantation and remodeling of maternal spiral arteries. Poor migration/invasion of evTBs can cause serious pregnancy complications, yet the effects of SSRIs on these processes has never been studied. To determine the effects of five SSRIs (fluoxetine, norfluoxetine, citalopram, sertraline and venlafaxine) on migration/invasion, we used JEG-3 and HIPEC cells as evTB models. Methods: Cells were treated with increasing concentrations (0.03-10 μM) of SSRIs. Cell proliferation was monitored using an impedance-based system and cell cycle by flow cytometry. Migration was determined using a scratch test, and metalloproteinase (MMP) activities, by zymography. Invasion markers were determined by RT-qPCR. Results: Fluoxetine and sertraline (10 μM) significantly decreased cell proliferation by 94% and by 100%, respectively, in JEG-3 cells, and by 58.6% and 100%, respectively, in HIPEC cells. Norfluoxetine increased MMP-9 activity in JEG-3 cells by 2.0% at 0.03 μM and by 43.9% at 3 μM, but decreased MMP-9 activity in HIPEC cells by 63.7% at 3 μM. Sertraline at 0.03 μM increased mRNA level of TIMP-1 in JEG-3 cells by 36% and that of ADAM-10 by 85% and 115% at 0.3 and 3 μM, respectively. In HIPEC cells, venlafaxine at 0.03 and 0.3 μM, increased ADAM-10 mRNA levels by 156% and 167%, respectively. Discussion: This study shows that SSRIs may affect evTBs homeostasis at therapeutic levels and provides guidance for future research.
MeSH term(s)	ADAM10 Protein/genetics ; Amyloid Precursor Protein Secretases/genetics ; Cell Line ; Cell Line, Tumor ; Cell Movement/drug effects ; Cell Proliferation/drug effects ; Choriocarcinoma ; Female ; Fluoxetine/adverse effects ; Fluoxetine/analogs & derivatives ; Gene Expression/drug effects ; Humans ; Matrix Metalloproteinase 9/drug effects ; Matrix Metalloproteinase 9/metabolism ; Membrane Proteins/genetics ; Models, Biological ; Pregnancy ; RNA, Messenger/analysis ; Serotonin Uptake Inhibitors/adverse effects ; Serotonin Uptake Inhibitors/therapeutic use ; Sertraline/adverse effects ; Tissue Inhibitor of Metalloproteinase-1/genetics ; Trophoblasts/drug effects ; Trophoblasts/physiology ; Venlafaxine Hydrochloride/adverse effects
Chemical Substances	Membrane Proteins ; RNA, Messenger ; Serotonin Uptake Inhibitors ; Tissue Inhibitor of Metalloproteinase-1 ; Fluoxetine (01K63SUP8D) ; Venlafaxine Hydrochloride (7D7RX5A8MO) ; Amyloid Precursor Protein Secretases (EC 3.4.-) ; Matrix Metalloproteinase 9 (EC 3.4.24.35) ; ADAM10 Protein (EC 3.4.24.81) ; ADAM10 protein, human (EC 3.4.24.81) ; norfluoxetine (K8D70XE2F4) ; Sertraline (QUC7NX6WMB)
Language	English
Publishing date	2018-10-30
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	603951-0
ISSN	1532-3102 ; 0143-4004
ISSN (online)	1532-3102
ISSN	0143-4004
DOI	10.1016/j.placenta.2018.10.007
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Article: Serotonin-estrogen interactions: What can we learn from pregnancy?

Hudon Thibeault, Andrée-Anne / Sanderson, J. Thomas / Vaillancourt, Cathy

Biochimie. 2019 June, v. 161

2019

Abstract	We have reviewed the scientific literature related to four diseases in which to serotonin (5-HT) is involved in the etiology, herein named 5-HT-linked diseases, and whose prevalence is influenced by estrogenic status: depression, migraine, irritable bowel syndrome and eating disorders. These diseases all have in common a sex-dimorphic prevalence, with women more frequently affected than men. The co-occurrence between these 5-HT-linked diseases suggests that they have common physiopathological mechanisms. In most 5-HT-linked diseases (except for anorexia nervosa and irritable bowel syndrome), a decrease in the serotonergic tone is observed and estrogens are thought to contribute to the improvement of symptoms by stimulating the serotonergic system. Human pregnancy is characterized by a unique 5-HT and estrogen synthesis by the placenta. Pregnancy-specific disorders, such as hyperemesis gravidarum, gestational diabetes mellitus and pre-eclampsia, are associated with a hyperserotonergic state and decreased estrogen levels. Fetal programming of 5-HT-linked diseases is a complex phenomenon that involves notably fetal-sex differences, which suggest the implication of sex steroids. From a mechanistic point of view, we hypothesize that estrogens regulate the serotonergic system, resulting in a protective effect against 5-HT-linked diseases, but that, in turn, 5-HT affects estrogen synthesis in an attempt to retrieve homeostasis. These two processes (5-HT and estrogen biosynthesis) are crucial for successful pregnancy outcomes, and thus, a disruption of this 5-HT-estrogen relationship may explain pregnancy-specific pathologies or pregnancy complications associated with 5-HT-linked diseases.
Keywords	anorexia nervosa ; biosynthesis ; estrogens ; etiology ; gestational diabetes ; homeostasis ; humans ; irritable bowel syndrome ; men ; migraine ; placenta ; pre-eclampsia ; pregnancy outcome ; protective effect ; serotonin ; women
Language	English
Dates of publication	2019-06
Size	p. 88-108.
Publishing place	Elsevier B.V.
Document type	Article
ZDB-ID	120345-9
ISSN	0300-9084
ISSN	0300-9084
DOI	10.1016/j.biochi.2019.03.023
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