Abstract
Two types of oviductal epithelial cells, secretory and ciliated, play crucial roles in the first days after fertilization in mammals. Secretory cells produce various molecules promoting embryo development, while ciliated cells facilitate transport of oocytes and zygotes by ciliary beating. The proportions of the two cell types change during the estrous cycle. The proportion of ciliated cells on the oviductal luminal surface is abundant at the follicular phase, whereas the proportion of secretory cells gradually increases with the formation of the corpus luteum. In the present study, we hypothesize that the proportions of ciliated and secretory epithelial cells are regulated by mitosis. The proportion of the cells being positive for FOXJ1 (a ciliated cell marker) or Ki67 (a mitosis marker) in epithelial cells during the estrous cycle were immunohistochemically examined. Ki67 and FOXJ1 or PAX8 (a secretory cell marker), were double-stained to clarify which types of epithelial cells undergo mitosis. In the ampulla, the percentage of FOXJ1-positive cells was highest at the day of ovulation (Day 0) and decreased by about 50 % by Days 8–12, while in the isthmus it did not change during the estrous cycle. The proportion of Ki67-positive cells was highest at around the time of ovulation in both the ampulla and isthmus. All the Ki67-positive cells were PAX8-positive and FOXJ1-negative in both the ampulla and isthmus. These findings suggest that epithelial remodeling, which is regulated by differentiation and/or proliferation of secretory cells of the oviduct, provides the optimal environment for gamete transport, fertilization and embryonic development.
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References
Abe H, Hoshi H (2007) Regional and cyclic variations in the ultrastructural features of secretory cells in the oviductal epithelium of the Chinese Meishan pig. Reprod Domest Anim 42:292–298
Abe H, Oikawa T (1993) Observations by scanning electron microscopy of oviductal epithelial cells from cows at follicular and luteal phases. Anat Rec 235:399–410
Afzelius BA (2004) Cilia-related diseases. J Pathol 204:470–477
Appino S, Vincenti L, Rota A, Pellegrini S, Chieppa MN, Cadoni V, Pregel P (2015) Chlamydia abortus in cows oviducts, occasional event or causal connection? Reprod Domest Anim 50:526–528
Arai M, Yoshioka S, Tasaki Y, Okuda K (2013) Remodeling of bovine endometrium throughout the estrous cycle. Anim Reprod Sci 142:1–9
Chen S, Einspanier R, Schoen J (2013) In vitro mimicking of estrous cycle stages in porcine oviduct epithelium cells: estradiol and progesterone regulate differentiation, gene expression, and cellular function. Biol Reprod 89:54
Chung D, Gao F, Jegga AG, Das SK (2015) Estrogen mediated epithelial proliferation in the uterus is directed by stromal Fgf10 and Bmp8a. Mol Cell Endocrinol 400:48–60
Cooke PS, Buchanan DL, Young P, Setiawan T, Brody J, Korach KS, Taylor J, Lubahn DB, Cunha GR (1997) Stromal estrogen receptors mediate mitogenic effects of estradiol on uterine epithelium. Proc Natl Acad Sci U S A 94:6535–6540
Croxatto HB (2002) Physiology of gamete and embryo transport through the fallopian tube. Reprod Biomed Online 4:160–169
Freeman D, Weber J, Geary R, Woods G (1991) Time of embryo transport through the mare oviduct. Theriogenology 36:823–830
Halbert SA, Tam PY, Blandau RJ (1976) Egg transport in the rabbit oviduct: the roles of cilia and muscle. Science 191:1052–1053
Hansen TR, Randel RD, Welsh TH Jr (1988) Granulosa cell steroidogenesis and follicular fluid steroid concentrations after the onset of oestrus in cows. J Reprod Fertil 84:409–416
Harada T, Kaponis A, Iwabe T, Taniguchi F, Makrydimas G, Sofikitis N, Paschopoulos M, Paraskevaidis E, Terakawa N (2004) Apoptosis in human endometrium and endometriosis. Hum Reprod Update 10:29–38
Jabbour HN, Kelly RW, Fraser HM, Critchley HO (2006) Endocrine regulation of menstruation. Endocr Rev 27:17–46
Jeoung M, Bridges PJ (2011) Cyclic regulation of apoptotic gene expression in the mouse oviduct. Reprod Fertil Dev 23:638–644
Jin Z, El-Deiry WS (2005) Overview of cell death signaling pathways. Cancer Biol Ther 4:139–163
Lau A, Kollara A, St John E, Tone AA, Virtanen C, Greenblatt EM, King WA, Brown TJ (2014) Altered expression of inflammation-associated genes in oviductal cells following follicular fluid exposure: implications for ovarian carcinogenesis. Exp Biol Med (Maywood) 239:24–32
Lonergan P, Carolan C, Van Langendonckt A, Donnay I, Khatir H, Mermillod P (1996) Role of epidermal growth factor in bovine oocyte maturation and preimplantation embryo development in vitro. Biol Reprod 54:1420–1429
Miyamoto Y, Skarzynski DJ, Okuda K (2000) Is tumor necrosis factor-α a trigger for the initiation of endometrial prostaglandin F2α release at luteolysis in cattle? Biol Reprod 62:1109–1115
Ohtani S, Okuda K, Nishimura K, Mohri S (1993) Histological changes in bovine endometrium during the estrous cycle. Theriogenology 39:1033–1042
Okuda K, Kito S, Sato K (1988) Study on the central cavity in the bovine corpus luteum. Vet Rec 123(7):180–183
Pardo-Saganta A, Law BM, Tata PR, Villoria J, Saez B, Mou H, Zhao R, Rajagopal J (2015) Injury induces direct lineage segregation of functionally distinct airway basal stem/progenitor cell subpopulations. Cell Stem Cell 16:184–197
Pier B, Kazanjian A, Gillette L, Strenge K, Burney RO (2013) Effect of cigarette smoking on human oviductal ciliation and ciliogenesis. Fertil Steril 99:199–205
Pushpakumara PG, Robinson RS, Demmers KJ, Mann GE, Sinclair KD, Webb R, Wathes DC (2002) Expression of the insulin-like growth factor (IGF) system in the bovine oviduct at oestrus and during early pregnancy. Reproduction 123:859–868
Sato T, Wang G, Hardy MP, Kurita T, Cunha GR, Cooke PS (2002) Role of systemic and local IGF-I in the effects of estrogen on growth and epithelial proliferation of mouse uterus. Endocrinology 143:2673–2679
Steinhauer N, Boos A, Günzel-Apel AR (2004) Morphological changes and proliferative activity in the oviductal epithelium during hormonally defined stages of the oestrous cycle in the bitch. Reprod Domest Anim 39:110–119
Wijayagunawardane MP, Miyamoto A, Cerbito WA, Acosta TJ, Takagi M, Sato K (1998) Local distributions of oviductal estradiol, progesterone, prostaglandins, oxytocin and endothelin-1 in the cyclic cow. Theriogenology 49:607–618
Wijayagunawardane MP, Kodithuwakku SP, Yamamoto D, Miyamoto A (2005) Vascular endothelial growth factor system in the cow oviduct: a possible involvement in the regulation of oviductal motility and embryo transport. Mol Reprod Dev 72:511–520
Acknowledgment
Con-focal microscopic images were obtained with the cooperation of the Department of Instrumental Analysis, Advanced Science Research Center, Okayama University, Okayama, Japan.
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The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the research reported.
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Yoshihiko Kobayashi is a Research Fellow of the Japan Society for the Promotion of Science (No. 26924).
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Ito, S., Kobayashi, Y., Yamamoto, Y. et al. Remodeling of bovine oviductal epithelium by mitosis of secretory cells. Cell Tissue Res 366, 403–410 (2016). https://doi.org/10.1007/s00441-016-2432-8
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DOI: https://doi.org/10.1007/s00441-016-2432-8