Sperm Binding to Oviduct Epithelial Cells Enhances TGFB1 and IL10 Expressions in Epithelial Cells as Well as Neutrophils In Vitro: Prostaglandin E2 As a Main Regulator of Anti-Inflammatory Response in the Bovine Oviduct.
Sperm are allogenic to the female genital tract; however, oviducts provide optimal conditions for survival and capacitation of these non-self cells until fertilization. Recently, we showed that oviduct-conditioned media and prostaglandin E2 (PGE2) suppress sperm phagocytosis by polymorphonuclear neutrophils (PMNs) under physiological conditions. We hypothesized that sperm binding to bovine oviduct epithelial cells (BOECs) could change the local innate immunity via PGE2. As the first step to obtain basic information, sub-confluent BOEC monolayers were co-cultured with swim-up sperm for 2 h. BOECs with viable bound sperm were cultured for an additional 3, 6, 12, or 24 h. Then, we confirmed the impact of the sperm-BOEC binding on both BOECs and PMN gene expression. Immunohistochemistry revealed that BOECs strongly express TGFB1 and IL10 in the oviduct. Sperm binding to BOECs in culture induced the anti-inflammatory cytokines (TGFB1 and IL10) and PGE2 production by BOECs. Exogenous PGE2 in vitro suppressed pro-inflammatory cytokine expression (TNF and IL1B) in BOECs. Moreover, pre-exposure of PMNs to BOEC-conditioned media suppressed the TNF expression, but the BOEC media co-cultured with sperm stimulated PMNs to express TGFB1 and IL10, with increasing PGE2 secretion. Of note, exogenous PGE2 led PMNs in vitro to decrease their TNF expression and increase anti-inflammatory cytokines expression. Our findings strongly suggest that BOECs provide an anti-inflammatory environment under physiological conditions and the sperm-BOEC binding further strengthens this milieu thus suppresses PMNs in the bovine oviduct. PGE2 is likely to drive this stable anti-inflammatory environment in the oviduct.
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.
Mohamed Samy
MS
Yousef
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.
Mohamed Ali
MA
Marey
Department of Anatomy, University of Veterinary Medicine Hannover, Hannover, D-30173, Germany.
Nina
N
Hambruch
Genetics Hokkaido Association, Shimizu-cho, 089-0103, Japan.
Hiroyuki
H
Hayakawa
Graduate School of Animal and Food Hygiene, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, 080-8555, Japan.
Takashi
T
Shimizu
Department of Theriogenology, Faculty of Veterinary Medicine, Assiut University, Assiut, Egypt.
Hassan Ali
HA
Hussien
Department of Theriogenology, Faculty of Veterinary Medicine, Assiut University, Assiut, Egypt.
Abdel-Razek Khalifa
AK
Abdel-Razek
Department of Anatomy, University of Veterinary Medicine Hannover, Hannover, D-30173, Germany.
Christiane
C
Pfarrer
Graduate School of Animal and Food Hygiene, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, 080-8555, Japan.
Akio
A
Miyamoto
Mol Reprod Dev. 1993 Nov;36(3):338-45
8286116
Anim Reprod Sci. 2001 Oct 31;68(1-2):121-31
11600280
Hum Immunol. 2008 Nov;69(11):708-14
18817827
J Androl. 1996 Mar-Apr;17(2):158-63
8723440
Reproduction. 2013 Dec 24;147(2):211-9
24255155
Methods. 2001 Dec;25(4):402-8
11846609
Hum Immunol. 2008 Nov;69(11):715-20
18817830
Mol Reprod Dev. 2005 Dec;72(4):511-20
16155957
J Reprod Fertil. 1968 Feb;15(1):127-30
5689141
Fertil Steril. 1994 Jul;62(1):186-8
8005288
Theriogenology. 1995 Oct 15;44(6):859-69
16727781
Br J Pharmacol. 1992 Nov;107(3):640-1
1282071
J Clin Immunol. 2007 Mar;27(2):152-62
17308869
Biol Reprod. 2007 Oct;77(4):590-8
17596562
J Immunol. 2004 Jul 1;173(1):559-65
15210817
Biotech Histochem. 1992 May;67(3):119-24
1377502
World J Gastroenterol. 2012 Nov 7;18(41):5848-61
23139600
Reprod Nutr Dev. 1984;24(4):461-8
6541363
J Reprod Dev. 2004 Feb;50(1):57-62
15007202
J Reprod Dev. 2013 Oct;59(5):470-8
23800958
Biol Reprod. 2004 Jul;71(1):60-5
14973272
Anim Reprod Sci. 2010 Jun;119(3-4):244-57
20171026
Arch Androl. 1993 Sep-Oct;31(2):79-86
8215695
Mol Reprod Dev. 1995 Oct;42(2):226-32
8562068
Theriogenology. 1998 Feb;49(3):607-18
10732039
J Immunol. 2005 Aug 1;175(3):1483-90
16034085
Reproduction. 2007 Jun;133(6):1087-94
17636163
J Proteomics. 2015 Jan 15;113:1-14
25281772
Eur Respir J Suppl. 1996 Aug;22:90s-94s
8871051
Anat Histol Embryol. 1990 Mar;19(1):16-36
2375508
Biol Reprod. 2001 Sep;65(3):799-804
11514344
Biol Reprod. 1991 Jan;44(1):102-7
2015341
Anal Biochem. 1987 Apr;162(1):156-9
2440339
World J Clin Oncol. 2014 Oct 10;5(4):753-63
25302175
J Proteome Res. 2007 Dec;6(12):4656-66
18004800
Theriogenology. 2016 Jan 1;85(1):105-12
26277704
Biol Reprod. 1997 May;56(5):1198-204
9160719