Summer heat stress (HS) negatively affects reproductive functions, including prostaglandin (PG) F2 α secretion in the endometrium, and decreases fertility in cattle. In the present study, we examined the effects of elevated temperatures on PG synthesis in oviductal epithelial cells. The epithelial cells obtained from the ampulla and isthmus of the oviduct were incubated at various temperatures (38.5, 39.5, 40.0, and 40.5 °C) for 24 h. In the ampulla, PGE2 concentration was higher at 40.5 °C than at 38.5 °C, while PGF2 α production was not affected by the temperatures in this range. The expressions of microsomal PGE synthase 1 (PTGES (m PGES 1)), cytosolic PGES (PTGES3 (cPGES)), and heat shock protein 90 (HSP90AA1 (HSP 90)) mRNAs and proteins were higher at 40.5 °C than at 38.5 °C in the ampullary epithelial cells. Seasonal changes in the expressions of PGES and HSP90AA1 mRNAs in oviductal tissues were also investigated. The expressions of PTGES3 and HSP90AA1 mRNAs were higher in the ampullary tissues in summer than in winter. In summary, elevated temperatures stimulated PGE2 production in the ampullary oviduct by increasing the expressions of PGESs and HSP90AA1, which can activate cPGES. The overall results suggest that HS upsets PG secretions and reduces oviductal smooth muscle motility, which in turn could decrease gamete/embryo transport through the oviduct.
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Yoshihiko Kobayashi, Kaori Wakamiya, Misa Kohka, Yuki Yamamoto, and Kiyoshi Okuda
Yoshihiko Kobayashi, Yuka Yoshimoto, Yuki Yamamoto, Koji Kimura, and Kiyoshi Okuda
Endothelins (EDNs) participate in various physiological events including smooth muscle contraction, nitric oxide (NO) synthesis, and embryonic development. In this study, we investigated the regional roles of EDNs produced by bovine oviductal epithelial cells in NO synthesis and smooth muscle motility. Quantification of mRNA expressions indicated that expression of EDN receptor B (EDNRB) in the ampullary region was higher after ovulation than before ovulation, whereas expression of EDNRA in the isthmic region was higher after ovulation than before ovulation. Immunohistochemistry revealed that the EDN receptors (EDNRA and EDNRB) were expressed in the epithelium, whereas smooth muscle showed positive staining only for EDNRA. The expressionsPlease suggest whether 'NOS2' can be treated as the updated symbol for 'iNOS' as per gene nomenclature. of inducible NO synthase (iNOS) protein and its mRNA (NOS2) in cultured epithelial cells isolated from the ampulla were stimulated by EDN1, but not by EDN2 or EDN3, after 1h of incubation. In isthmic epithelial cells, none of the EDNs affected the expression of NOS2. Isometric contraction tests indicated that spontaneous waves were strong in the isthmic region but weak in the ampullary region. EDN1 modulated smooth muscle motility in both the regions. The overall findings suggest that EDN1 plays region-specific roles in smooth muscle motility and epithelial NO synthesis, providing an optimal oviductal microenvironment for transport of gametes, fertilization, and development/transport of early embryo.
Yoshihiko Kobayashi, Yuki Yamamoto, Soichi Kageyama, Hiroki Hirayama, Koji Kimura, and Kiyoshi Okuda
Nitric oxide (NO) is a regulator of sperm motility, oocyte/embryo survival, and waves of contraction/relaxation in mammalian oviducts. As follicles control oviductal functions by two routes at least, (1) a systemic way via blood vessels before ovulation, (2) a direct way by entering of follicular fluid through fimbria at ovulation, we hypothesized that NO synthesis in the bovine oviduct is regulated by follicular steroids and prostaglandins (PGs). Quantification of mRNA expressions in the ampullary tissues showed that inducible NO synthase (NOS2) mRNA expression was highest on the day of ovulation (day 0). By contrast, NOS2 mRNA expression in the isthmus was highest on days 5–6 and lowest on days 19–21. Endothelial NOS (NOS3) mRNA expressions in either the ampulla or the isthmus did not change during the estrous cycle. PGE2 and PGF2α increased NOS2 mRNA expressions in cultured ampullary oviductal epithelial cells after 1-h incubation. These increases were suppressed by an antagonist of E-prostanoid receptor type 2, one of the PGE2 receptor. Estradiol-17β decreased the expression of NOS2 mRNA expression in cultured isthmic epithelial cells 24h after treatment. This effect was suppressed by an antagonist of estrogen receptorα(ESR1). Expression of ESR1 was highest on days 19–21 in the isthmic tissues. The overall findings indicate region-specific difference of NO synthesis in the oviduct. PGs flowed from ruptured follicle may up-regulate NO synthesis in the oviductal epithelium, whereas circulating E2 seems to inhibit NO synthesis via ESR1 in the isthmus at the follicular stage.
Yuki Yamamoto, Maho Kurokawa, Taiji Ogawa, Sayaka Kubota, and Koji Kimura
Spontaneous contraction of oviductal smooth muscle is essential for gamete transport to the fertilization site in mammals. This study sheds light on the mechanism of elevated contraction amplitude in the bovine oviductal isthmus just before ovulation.
Rhythmic contraction of the oviducts is essential for transporting gametes and embryos at peri-ovulation; however, its regulatory mechanism during the estrous cycle is unclear. Meanwhile, it is reported that ion currents regulate muscle contraction. Our study aimed to clarify the involvement of ion channels and gap junctions in regulating oviductal motility during the estrous cycle in cattle. The isthmic sections of bovine oviducts collected just after ovulation (0–4 days after ovulation), at the mid-late luteal stage (10–17 days), and at the follicular stage (1–3 days before ovulation) were used in the experiments. The frequency and amplitude of contraction of the oviductal strips in the longitudinal direction were examined using the Magnus system. The frequency was not different among the estrous stages. Conversely, the amplitude was significantly higher at the follicular stage. The blockers of voltage-dependent calcium channels, both IP3 receptor and ryanodine receptors, chloride channel, and gap junction reduced the amplitude. Additionally, mRNA and protein expression of GJA1, a component of the gap junction, in the smooth muscle tissues of the oviductal isthmus were significantly higher in the follicular stage. In addition, estradiol-17β (E2; 1.0 ng/mL) significantly increased GJA1 mRNA expression in cultured smooth muscle tissues after 24 h and GJA1 protein expression in cultured smooth muscle cells after 48 h. These results suggest that local levels of E2 in the oviductal isthmus ipsilateral to an ovary with a dominant follicle support the increased contraction amplitude of bovine ipsilateral oviducts by elevating the gap junction expression.
Keisuke Kozai, Shota Tokuyama, Anna Z Szóstek, Yuko Toishi, Nobuo Tsunoda, Kazuyoshi Taya, Miki Sakatani, Masashi Takahashi, Yasuo Nambo, Dariusz J Skarzynski, Yuki Yamamoto, Koji Kimura, and Kiyoshi Okuda
In mares, prostaglandin F2α (PGF2α) secreted from the endometrium is a major luteolysin. Some domestic animals have an auto-amplification system in which PGF2α can stimulate its own production. Here, we investigated whether this is also the case in mares. In an in vivo study, mares at the mid-luteal phase (days 6–8 of estrous cycle) were injected i.m. with cloprostenol (250 µg) and blood samples were collected at fixed intervals until 72 h after treatment. Progesterone (P4) concentrations started decreasing 45 min after the injection and continued to decrease up to 24 h (P < 0.05). In turn, 13,14-dihydro-15-keto-PGF2α (PGFM) metabolite started to increase 4h after an injection and continued to increase up to 72 h (P < 0.05). PGF receptor (PTGFR) mRNA expression in the endometrium was significantly higher in the late luteal phase than in the early and regressed luteal phases (P < 0.05). In vitro, PGF2α significantly stimulated (P < 0.05) PGF2α production by endometrial tissues and endometrial epithelial and stromal cells and significantly increased (P < 0.05) the mRNA expression of prostaglandin-endoperoxide synthase-2 (PTGS2), an enzyme involved in PGF2α synthesis in endometrial cell. These findings strongly suggest the existence of an endometrial PGF2α auto-amplification system in mares.