Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Endothelin as a local regulating factor in the bovine oviduct

Yuki Yamamoto A , Misa Kohka A , Yoshihiko Kobayashi A , Izabela Woclawek-Potocka B and Kiyoshi Okuda A C
+ Author Affiliations
- Author Affiliations

A Laboratory of Reproductive Physiology, Graduate School of Environmental and Life Science, Okayama University, 1-1-1 Tsushimanaka, Kita-ku, Okayama, Okayama, 700-8530, Japan.

B Department of Reproductive Immunology and Pathology, Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, 10–747 Olsztyn, Poland.

C Corresponding author. Email: kokuda@okayama-u.ac.jp

Reproduction, Fertility and Development 28(6) 673-681 https://doi.org/10.1071/RD14076
Submitted: 24 February 2014  Accepted: 8 September 2014   Published: 5 November 2014

Abstract

Endothelin (EDN) is a possible regulating factor of oviductal motility, which is important for the transport of gametes and embryo. To clarify the factors that control the secretion of EDN in the bovine oviduct, the expression of EDNs, EDN-converting enzymes (ECEs) and EDN receptors (EDNRs) were investigated. All isoforms of EDN (EDN1–3), ECE (ECE1 and ECE2) and EDNR (EDNRA and EDNRB) were immunolocalised in the epithelial cells of the ampulla and the isthmus. EDNRs were also immunolocalised in smooth-muscle cells. The mRNA expression of EDN2 and ECE2 was higher in cultured ampullary oviductal epithelial cells than in isthmic cells. The expression of EDN1, EDN2 and ECE2 in the ampullary tissue was highest on the day of ovulation. Oestradiol-17β increased EDN2 and ECE1 expression, while progesterone increased only ECE1 expression in cultured ampullary epithelial cells. These results indicate that EDNs are produced by epithelial cells and their target site is smooth-muscle and epithelial cells, and suggest that ovarian steroids are regulators of endothelin synthesis in ampullary oviductal epithelial cells.

Additional keywords: endothelin converting enzyme, endothelin receptor, epithelial cell, ovarian steroids, oviductal contraction and relaxation.


References

Acosta, T. J., Yoshioka, S., Komiyama, J., Lee, S. J., Grazul-Bilska, A. T., Skarzynski, D. J., and Okuda, K. (2007). Effects of storage and passage of bovine luteal endothelial cells on endothelin-1 and prostaglandin F2α production. J. Reprod. Dev. 53, 473–480.
Effects of storage and passage of bovine luteal endothelial cells on endothelin-1 and prostaglandin F2α production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosVyls7w%3D&md5=2dc4017428155d45f901827a26f29b38CAS | 17229995PubMed |

Al-Alem, L., Bridges, P. J., Su, W., Gong, M. C., Iglarz, M., and Ko, C. (2007). Endothelin-2 induces oviductal contraction via endothelin receptor subtype A in rats. J. Endocrinol. 193, 383–391.
Endothelin-2 induces oviductal contraction via endothelin receptor subtype A in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnt1CqtL4%3D&md5=57836dd4ed3b911da2faff8734307d13CAS | 17535876PubMed |

Arai, H., Hori, S., Aramori, I., Ohkubo, H., and Nakanishi, S. (1990). Cloning and expression of a cDNA encoding an endothelin receptor. Nature 348, 730–732.
Cloning and expression of a cDNA encoding an endothelin receptor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXktVaisb0%3D&md5=6821c6cb457dcbbe6f0a7478d3ffcb51CAS | 2175396PubMed |

Bridges, P., Cho, J., and Ko, C. (2011). Endothelins in regulating ovarian and oviductal function. Front. Biosci. (Schol. Ed.) 3, 145–155.
| 21196365PubMed |

Eberhardt, D. M., Jacobs, W. G., and Godkin, J. D. (1999). Steroid regulation of retinol-binding protein in the ovine oviduct. Biol. Reprod. 60, 714–720.
Steroid regulation of retinol-binding protein in the ovine oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsFektb0%3D&md5=63f08fd692d07e64781ce1eaa616036bCAS | 10026121PubMed |

Inoue, A., Yanagisawa, M., Kimura, S., Kasuya, Y., Miyauchi, T., Goto, K., and Masaki, T. (1989). The human endothelin family: three structurally and pharmacologically distinct isopeptides predicted by three separate genes. Proc. Natl. Acad. Sci. USA 86, 2863–2867.
The human endothelin family: three structurally and pharmacologically distinct isopeptides predicted by three separate genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkslahsLg%3D&md5=b188c3e20e5aafe29271f2a35991b5e5CAS | 2649896PubMed |

Jankovic, S. M., Jankovic, S. V., Lukic, G., Radonjic, V., Cupara, S., and Stefanovic, S. (2009). Contractile effects of endothelins on isolated ampullar segment of human oviduct in luteal phase of menstrual cycle. Pharmacol. Res. 59, 69–73.
Contractile effects of endothelins on isolated ampullar segment of human oviduct in luteal phase of menstrual cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjvFOjsQ%3D%3D&md5=b10caf35f0d4f7ffe3ed7ced96e1a185CAS | 18983921PubMed |

Jayaraman, A., Carroll, J. C., Morgan, T. E., Lin, S. R., Zhao, L. Q., Arimoto, J. M., Murphy, M. P., Beckett, T. L., Finch, C. E., Brinton, R. D., and Pike, C. J. (2012). 17 beta-oestradiol and progesterone regulate expression of beta-amyloid clearance factors in primary neuron cultures and female rat brain. Endocrinology 153, 5467–5479.
17 beta-oestradiol and progesterone regulate expression of beta-amyloid clearance factors in primary neuron cultures and female rat brain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1OnsLfO&md5=ebcc68ab3fa19436c77248ab50bbc60eCAS | 22962256PubMed |

Jeoung, M., Lee, S., Hawng, H. K., Cheon, Y. P., Jeong, Y. K., Gye, M. C., Iglarz, M., Ko, C., and Bridges, P. J. (2010). Identification of a novel role for endothelins within the oviduct. Endocrinology 151, 2858–2867.
Identification of a novel role for endothelins within the oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnsVyqtbo%3D&md5=6d1c1d11f18b222f245e4ddae58fc652CAS | 20357223PubMed |

Kawanabe, Y., and Nauli, S. M. (2011). Endothelin. Cell. Mol. Life Sci. 68, 195–203.
Endothelin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXis1ejsw%3D%3D&md5=f8593d0b607a3849840dfeb4add54fd2CAS | 20848158PubMed |

Kobayashi, Y., Wakamiya, K., Kohka, M., Yamamoto, Y., and Okuda, K. (2013). Summer heat stress affects prostaglandin synthesis in the bovine oviduct. Reproduction 146, 103–110.
Summer heat stress affects prostaglandin synthesis in the bovine oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlSnsb7P&md5=f78a7375611dafb6415d5ce502b2e0a6CAS | 23704311PubMed |

Kozuka, M., Ito, T., Hirose, S., Takahashi, K., and Hagiwara, H. (1989). Endothelin induces two types of contractions of rat uterus – phasic contractions by way of voltage-dependent calcium channels and developing contractions through a second type of calcium channel. Biochem. Biophys. Res. Commun. 159, 317–323.
Endothelin induces two types of contractions of rat uterus – phasic contractions by way of voltage-dependent calcium channels and developing contractions through a second type of calcium channel.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhsVyks7o%3D&md5=2308cd134fe0067cec4ed9b9b9bfbaadCAS | 2538125PubMed |

Ling, L., Maguire, J. J., and Davenport, A. P. (2013). Endothelin-2, the forgotten isoform: emerging role in the cardiovascular system, ovarian development, immunology and cancer. Br. J. Pharmacol. 168, 283–295.
Endothelin-2, the forgotten isoform: emerging role in the cardiovascular system, ovarian development, immunology and cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitFOgug%3D%3D&md5=bc3a1bdc26532810f0c70e2aa52ad002CAS | 22118774PubMed |

Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=224f15b9dfd00d92fda868e1cb065922CAS | 11846609PubMed |

Miyamoto, Y., Skarzynski, D. J., and Okuda, K. (2000). Is tumour necrosis factor alpha a trigger for the initiation of endometrial prostaglandin F2α release at luteolysis in cattle? Biol. Reprod. 62, 1109–1115.
Is tumour necrosis factor alpha a trigger for the initiation of endometrial prostaglandin F2α release at luteolysis in cattle?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisl2htr8%3D&md5=4109fe57528feee511845fc94598cb5eCAS | 10775155PubMed |

Okuda, K., Kito, S., Sumi, N., and Sato, K. (1988). A study of the central cavity in the bovine corpus luteum. Vet. Rec. 123, 180–183.
A study of the central cavity in the bovine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M7hsV2qsA%3D%3D&md5=51d6c16b54b5f48e163ac09ed84dd929CAS | 3218058PubMed |

Priyadarsana, M., Wijayagunawardane, B., and Miyamoto, A. (2004). Endothelin-1 system in the bovine oviduct: a regulator of local contraction and gamete transport. J. Cardiovasc. Pharmacol. 44, S248–S251.
Endothelin-1 system in the bovine oviduct: a regulator of local contraction and gamete transport.Crossref | GoogleScholarGoogle Scholar | 15838292PubMed |

Rodrigo, M. C., Martin, D. S., and Eyster, K. M. (2003). Vascular ECE-1 mRNA expression decreases in response to oestrogens. Life Sci. 73, 2973–2983.
Vascular ECE-1 mRNA expression decreases in response to oestrogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXns12rtbs%3D&md5=3ab8e222151627bf7159546dd12536b0CAS | 14519446PubMed |

Rosselli, M., Imthurn, B., Macas, E., Keller, P., and Dubey, R. (1994). Endogenous nitric oxide modulates endothelin-1 induced contraction of bovine oviduct. Biochem. Biophys. Res. Commun. 201, 143–148.
Endogenous nitric oxide modulates endothelin-1 induced contraction of bovine oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXktVWqsbs%3D&md5=f87512d131aa9903ac119739f314779cCAS | 7515230PubMed |

Sakamoto, M., Sakamoto, S., Kubota, T., Aso, T., and Azuma, H. (2001). Localisation and role of endothelin-1 and endothelin receptors in the human Fallopian tube. Mol. Hum. Reprod. 7, 1057–1063.
Localisation and role of endothelin-1 and endothelin receptors in the human Fallopian tube.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXovVKjtrw%3D&md5=daeeabefa931abecb9d55608769033c9CAS | 11675472PubMed |

Sakumoto, R., Komatsu, T., Kasuya, E., Saito, T., and Okuda, K. (2006). Expression of mRNAs for interleukin-4, interleukin-6 and their receptors in porcine corpus luteum during the oestrous cycle. Domest. Anim. Endocrinol. 31, 246–257.
Expression of mRNAs for interleukin-4, interleukin-6 and their receptors in porcine corpus luteum during the oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpsVWltbg%3D&md5=ede2a8c5d88090c684ff23d4b615aaf8CAS | 16332426PubMed |

Sakurai, T., Yanagisawa, M., Takuwa, Y., Miyazaki, H., Kimura, S., Goto, K., and Masaki, T. (1990). Cloning of a cDNA encoding a non-isopeptide-selective subtype of the endothelin receptor. Nature 348, 732–735.
Cloning of a cDNA encoding a non-isopeptide-selective subtype of the endothelin receptor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXktVaisbo%3D&md5=5b433b6e4a90ee09b7acfa289ce50fb2CAS | 2175397PubMed |

Siemieniuch, M. J., Woclawek-Potocka, I., Deptula, K., Okuda, K., and Skarzynski, D. J. (2009). Effects of tumour necrosis factor-α and nitric oxide on prostaglandin secretion by the bovine oviduct differ in the isthmus and ampulla and depend on the phase of the oestrous cycle. Exp. Biol. Med. (Maywood) 234, 1056–1066.
Effects of tumour necrosis factor-α and nitric oxide on prostaglandin secretion by the bovine oviduct differ in the isthmus and ampulla and depend on the phase of the oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFWjs77E&md5=c92c14a439a426f2dd7adf27c99ad5d8CAS | 19596830PubMed |

Szóstek, A. Z., Siemieniuch, M. J., Deptula, K., Woclawek-Potocka, I., Majewska, M., Okuda, K., and Skarzynski, D. J. (2011). Ovarian steroids modulate tumour necrosis factor-α and nitric oxide-regulated prostaglandin secretion by cultured bovine oviductal epithelial cells. Domest. Anim. Endocrinol. 41, 14–23.
Ovarian steroids modulate tumour necrosis factor-α and nitric oxide-regulated prostaglandin secretion by cultured bovine oviductal epithelial cells.Crossref | GoogleScholarGoogle Scholar | 21420267PubMed |

Tsukahara, H., Ende, H., Magazine, H., Bahou, W. F., and Goligorsky, M. S. (1994). Molecular and functional characterisation of the non-isopeptide-selective ETB receptor in endothelial cells. Receptor coupling to nitric oxide synthase. J. Biol. Chem. 269, 21 778–21 785.
| 1:CAS:528:DyaK2cXlsV2kurg%3D&md5=0bc50d3edc7de6eee503ce0f37bd5e61CAS |

Turner, A. J., and Murphy, L. J. (1996). Molecular pharmacology of endothelin-converting enzymes. Biochem. Pharmacol. 51, 91–102.
Molecular pharmacology of endothelin-converting enzymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltFOguw%3D%3D&md5=e8226379f44a61adb06bc1a312db4328CAS | 8615890PubMed |

Tykocki, N. R., Gariepy, C. E., and Watts, S. W. (2009). Endothelin ETB receptors in arteries and veins: multiple actions in the vein. J. Pharmacol. Exp. Ther. 329, 875–881.
Endothelin ETB receptors in arteries and veins: multiple actions in the vein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1ehtbk%3D&md5=2fead2bceb84b0855ff515f298cb0b59CAS | 19297422PubMed |

Wijayagunawardane, M. P. B., Miyamoto, A., and Sato, K. (1999a). Prostaglandin E2, prostaglandin F2α and endothelin-1 production by cow oviductal epithelial cell monolayers: effect of progesterone, oestradiol 17β, oxytocin and luteinising hormone. Theriogenology 52, 791–801.
Prostaglandin E2, prostaglandin F2α and endothelin-1 production by cow oviductal epithelial cell monolayers: effect of progesterone, oestradiol 17β, oxytocin and luteinising hormone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns1Ohtbk%3D&md5=c92bb72c76917b9820a03012ee6a92b0CAS |

Wijayagunawardane, M. P. B., Choi, Y. H., Miyamoto, A., Kamishita, H., Fujimoto, S., Takagi, M., and Sato, K. (1999b). Effect of ovarian steroids and oxytocin on the production of prostaglandin E2, prostaglandin F2α and endothelin-1 from cow oviductal epithelial cell monolayers in vitro. Anim. Reprod. Sci. 56, 11–17.
Effect of ovarian steroids and oxytocin on the production of prostaglandin E2, prostaglandin F2α and endothelin-1 from cow oviductal epithelial cell monolayers in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsVSlsbg%3D&md5=7ddddfa80ee5fa994198b856a029400cCAS |

Wijayagunawardane, M. P. B., Miyamoto, A., Taquahashi, Y., Gabler, C., Acosta, T. J., Nishimura, M., Killian, G., and Sato, K. (2001). In vitro regulation of local secretion and contraction of the bovine oviduct: stimulation by luteinising hormone, endothelin-1 and prostaglandins, and inhibition by oxytocin. J. Endocrinol. 168, 117–130.
In vitro regulation of local secretion and contraction of the bovine oviduct: stimulation by luteinising hormone, endothelin-1 and prostaglandins, and inhibition by oxytocin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotVKjtg%3D%3D&md5=3d16b15ff5ed69d425808e9ec152c197CAS |

Yanagisawa, M., Inoue, A., Ishikawa, T., Kasuya, Y., Kimura, S., Kumagaye, S. I., Nakajima, K., Watanabe, T. X., Sakakibara, S., Goto, K., and Masaki, T. (1988). Primary structure, synthesis and biological-activity of rat endothelin, an endothelium-derived vasoconstrictor peptide. Proc. Natl. Acad. Sci. USA 85, 6964–6967.
Primary structure, synthesis and biological-activity of rat endothelin, an endothelium-derived vasoconstrictor peptide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXmtVGjsL8%3D&md5=f8a7e5973fbca38ccea531bb7095f471CAS | 3045827PubMed |

Ziecik, A. J., Kaczmarek, M. M., Blitek, A., Kowalczyk, A. E., Li, X. D., and Rahman, N. A. (2007). Novel biological and possible applicable roles of LH/hCG receptor. Mol. Cell. Endocrinol. 269, 51–60.
Novel biological and possible applicable roles of LH/hCG receptor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjslSqsbw%3D&md5=3f75c4a9ae982210d5f44417646dd05eCAS | 17367919PubMed |