Zearalenone (ZEN) disrupts the anti-inflammatory response of bovine oviductal epithelial cells to sperm in vitro

Mohamed S Yousef; Mitsuhiro Takagi; Anup K Talukder; Mohamed A Marey; Rasoul Kowsar; Abdel-Razek Kh Abdel-Razek; Takashi Shimizu; Johanna Fink-Gremmels; Akio Miyamoto

doi:10.1016/j.reprotox.2017.09.012

Zearalenone (ZEN) disrupts the anti-inflammatory response of bovine oviductal epithelial cells to sperm in vitro

Mohamed S Yousef, Mitsuhiro Takagi, Anup K Talukder, Mohamed A Marey, Rasoul Kowsar, Abdel-Razek Kh Abdel-Razek, Takashi Shimizu, Johanna Fink-Gremmels, Akio Miyamoto^*

^*Corresponding author for this work

Graduate School of Animal and Food Hygiene, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, 080-8555, Japan; Department of Theriogenology, Faculty of Veterinary Medicine, Assiut University, Assiut, Egypt.
Joint Faculty of Veterinary Medicine, Yamaguchi University, Yamaguchi, 1677-1, Japan.
Graduate School of Animal and Food Hygiene, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, 080-8555, Japan; Department of Gynecology, Obstetrics and Reproductive Health, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gaipur-1706, Bangladesh.
Graduate School of Animal and Food Hygiene, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, 080-8555, Japan; Department of Theriogenology, Faculty of Veterinary Medicine, Damanhur University, Behera, Egypt.
Department of Animal Science, College of Agriculture, Isfahan University of Technology, Isfahan, Iran.
Department of Theriogenology, Faculty of Veterinary Medicine, Assiut University, Assiut, Egypt.
Graduate School of Animal and Food Hygiene, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, 080-8555, Japan.
Utrecht University
Graduate School of Animal and Food Hygiene, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, 080-8555, Japan. Electronic address: [email protected].

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Dietary contamination by Zearalenone (ZEN) has a detrimental effect on bovine fertility. Recently, we showed a novel anti-inflammatory response of bovine oviductal epithelial cells (BOEC) to active sperm cells in vitro. The aim of the present study was to investigate the effect of ZEN exposure of BOEC on the immune-related cytokine expression in response to bovine sperm. At concentrations of 100 and 1000ng/mL, ZEN induced the expression of TNF and IL1B (pro-inflammatory cytokines) as well as IL8 (chemokine) in BOEC in a dose-dependent manner. Furthermore, ZEN induced PTGES expression and PGE2 secretion in BOEC. Sperm co-culture induced an anti-inflammatory response in BOEC with upregulation of TGFB, secretion of PGE2 and downregulation of TNF. Most importantly, ZEN at 1-1000ng/mL eliminated the response of BOEC to sperm. Estradiol-17β (5ng/mL) treatment did not produce the same effects as ZEN, suggesting that the response of BOEC to ZEN is, at least in part, not mediated by estrogen receptors. Taken together, ZEN can produce inflammatory effects on BOEC by stimulating the expressions of pro-inflammatory cytokines and disrupt the normal interaction between sperm and BOEC at the level of cytokine expressions and PGE2 production. Thus, exposure of the bovine oviduct to ZEN may negatively affect sperm survival and reduce fertility.

Original language	English
Pages (from-to)	158-163
Number of pages	6
Journal	Reproductive Toxicology
Volume	74
DOIs	https://doi.org/10.1016/j.reprotox.2017.09.012
Publication status	Published - Dec 2017

Keywords

Zearalenone
Oviduct
Sperm
Cytokine
Inflammation

Access to Document

10.1016/j.reprotox.2017.09.012

1-s2.0-S0890623817301612-mainFinal published version, 584 KBLicence: Taverne

Cite this

@article{a61c49e108d74cadb4137417ff3a060f,

title = "Zearalenone (ZEN) disrupts the anti-inflammatory response of bovine oviductal epithelial cells to sperm in vitro",

abstract = "Dietary contamination by Zearalenone (ZEN) has a detrimental effect on bovine fertility. Recently, we showed a novel anti-inflammatory response of bovine oviductal epithelial cells (BOEC) to active sperm cells in vitro. The aim of the present study was to investigate the effect of ZEN exposure of BOEC on the immune-related cytokine expression in response to bovine sperm. At concentrations of 100 and 1000ng/mL, ZEN induced the expression of TNF and IL1B (pro-inflammatory cytokines) as well as IL8 (chemokine) in BOEC in a dose-dependent manner. Furthermore, ZEN induced PTGES expression and PGE2 secretion in BOEC. Sperm co-culture induced an anti-inflammatory response in BOEC with upregulation of TGFB, secretion of PGE2 and downregulation of TNF. Most importantly, ZEN at 1-1000ng/mL eliminated the response of BOEC to sperm. Estradiol-17β (5ng/mL) treatment did not produce the same effects as ZEN, suggesting that the response of BOEC to ZEN is, at least in part, not mediated by estrogen receptors. Taken together, ZEN can produce inflammatory effects on BOEC by stimulating the expressions of pro-inflammatory cytokines and disrupt the normal interaction between sperm and BOEC at the level of cytokine expressions and PGE2 production. Thus, exposure of the bovine oviduct to ZEN may negatively affect sperm survival and reduce fertility.",

keywords = "Zearalenone, Oviduct, Sperm, Cytokine, Inflammation",

author = "Yousef, {Mohamed S} and Mitsuhiro Takagi and Talukder, {Anup K} and Marey, {Mohamed A} and Rasoul Kowsar and Abdel-Razek, {Abdel-Razek Kh} and Takashi Shimizu and Johanna Fink-Gremmels and Akio Miyamoto",

year = "2017",

month = dec,

doi = "10.1016/j.reprotox.2017.09.012",

language = "English",

volume = "74",

pages = "158--163",

journal = "Reproductive Toxicology",

issn = "0890-6238",

publisher = "Elsevier Inc.",

}

TY - JOUR

T1 - Zearalenone (ZEN) disrupts the anti-inflammatory response of bovine oviductal epithelial cells to sperm in vitro

AU - Yousef, Mohamed S

AU - Takagi, Mitsuhiro

AU - Talukder, Anup K

AU - Marey, Mohamed A

AU - Kowsar, Rasoul

AU - Abdel-Razek, Abdel-Razek Kh

AU - Shimizu, Takashi

AU - Fink-Gremmels, Johanna

AU - Miyamoto, Akio

PY - 2017/12

Y1 - 2017/12

N2 - Dietary contamination by Zearalenone (ZEN) has a detrimental effect on bovine fertility. Recently, we showed a novel anti-inflammatory response of bovine oviductal epithelial cells (BOEC) to active sperm cells in vitro. The aim of the present study was to investigate the effect of ZEN exposure of BOEC on the immune-related cytokine expression in response to bovine sperm. At concentrations of 100 and 1000ng/mL, ZEN induced the expression of TNF and IL1B (pro-inflammatory cytokines) as well as IL8 (chemokine) in BOEC in a dose-dependent manner. Furthermore, ZEN induced PTGES expression and PGE2 secretion in BOEC. Sperm co-culture induced an anti-inflammatory response in BOEC with upregulation of TGFB, secretion of PGE2 and downregulation of TNF. Most importantly, ZEN at 1-1000ng/mL eliminated the response of BOEC to sperm. Estradiol-17β (5ng/mL) treatment did not produce the same effects as ZEN, suggesting that the response of BOEC to ZEN is, at least in part, not mediated by estrogen receptors. Taken together, ZEN can produce inflammatory effects on BOEC by stimulating the expressions of pro-inflammatory cytokines and disrupt the normal interaction between sperm and BOEC at the level of cytokine expressions and PGE2 production. Thus, exposure of the bovine oviduct to ZEN may negatively affect sperm survival and reduce fertility.

AB - Dietary contamination by Zearalenone (ZEN) has a detrimental effect on bovine fertility. Recently, we showed a novel anti-inflammatory response of bovine oviductal epithelial cells (BOEC) to active sperm cells in vitro. The aim of the present study was to investigate the effect of ZEN exposure of BOEC on the immune-related cytokine expression in response to bovine sperm. At concentrations of 100 and 1000ng/mL, ZEN induced the expression of TNF and IL1B (pro-inflammatory cytokines) as well as IL8 (chemokine) in BOEC in a dose-dependent manner. Furthermore, ZEN induced PTGES expression and PGE2 secretion in BOEC. Sperm co-culture induced an anti-inflammatory response in BOEC with upregulation of TGFB, secretion of PGE2 and downregulation of TNF. Most importantly, ZEN at 1-1000ng/mL eliminated the response of BOEC to sperm. Estradiol-17β (5ng/mL) treatment did not produce the same effects as ZEN, suggesting that the response of BOEC to ZEN is, at least in part, not mediated by estrogen receptors. Taken together, ZEN can produce inflammatory effects on BOEC by stimulating the expressions of pro-inflammatory cytokines and disrupt the normal interaction between sperm and BOEC at the level of cytokine expressions and PGE2 production. Thus, exposure of the bovine oviduct to ZEN may negatively affect sperm survival and reduce fertility.

KW - Zearalenone

KW - Oviduct

KW - Sperm

KW - Cytokine

KW - Inflammation

U2 - 10.1016/j.reprotox.2017.09.012

DO - 10.1016/j.reprotox.2017.09.012

M3 - Article

C2 - 28966149

SN - 0890-6238

VL - 74

SP - 158

EP - 163

JO - Reproductive Toxicology

JF - Reproductive Toxicology

ER -

Zearalenone (ZEN) disrupts the anti-inflammatory response of bovine oviductal epithelial cells to sperm in vitro

Abstract

Keywords

Access to Document

Fingerprint

Cite this