Early embryo-maternal communication in the oviduct: A review.
embryo
embryo-maternal communication
female genital tract
oviduct
Journal
Molecular reproduction and development
ISSN: 1098-2795
Titre abrégé: Mol Reprod Dev
Pays: United States
ID NLM: 8903333
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
27
02
2020
revised:
05
05
2020
accepted:
10
05
2020
pubmed:
9
6
2020
medline:
23
7
2021
entrez:
8
6
2020
Statut:
ppublish
Résumé
An intact embryo-maternal communication is critical for the establishment of a successful pregnancy. To date, a huge number of studies have been performed describing the complex process of embryo-maternal signaling within the uterus. However, recent studies indicate that the early embryo communicates with the oviductal cells shortly after fertilizationand that this is important for the successful establishment of pregnancy. Only if the early embryo is capable to signal the mother within a precise timeframe and to garner a response, will the embryo be able to survive and reach the uterus. This review will give an overview of all the experimental designs which have investigated embryo-maternal interaction in the oviduct. In addition to that, it will provide a comprehensive analysis of the findings to date elucidating the morphological and molecular changes in the oviduct which are induced by the presence of the early embryo highlighting how the tubal responses affect embryo development and survival.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
650-662Informations de copyright
© 2020 Wiley Periodicals LLC.
Références
Abe, H., & Hoshi, H. (2008). Morphometric and ultrastructural changes in ciliated cells of the oviductal epithelium in prolific Chinese Meishan and large white pigs during the oestrous cycle. Reproduction in Domestic Animals, 43(1), 66-73. https://doi.org/10.1111/j.1439-0531.2007.00856.x
Absalon-Medina, V. A., Butler, W. R., & Gilbert, R. O. (2014). Preimplantation embryo metabolism and culture systems: Experience from domestic animals and clinical implications. Journal of Assisted Reproduction and Genetics, 31(4), 393-409. https://doi.org/10.1007/s10815-014-0179-2
Adachi, K., Kurachi, H., Homma, H., Adachi, H., Imai, T., Sakata, M., … Sakoyama, Y. (1995). Estrogen induces epidermal growth factor (EGF) receptor and its ligands in human fallopian tube: Involvement of EGF but not transforming growth factor-alpha in estrogen-induced tubal cell growth in vitro. Endocrinology, 136(5), 2110-2119. https://doi.org/10.1210/endo.136.5.7720660
Akira, S., Sanbuissho, A., Lin, Y. C., & Araki, T. (1993). Acceleration of embryo transport in superovulated adults rats. Life Sciences, 53(15), 1243-1251. https://doi.org/10.1016/0024-3205(93)90543-C
Alminana, C., Heath, P. R., Wilkinson, S., Sanchez-Osorio, J., Cuello, C., Parrilla, I., … Fazeli, A. (2012). Early developing pig embryos mediate their own environment in the maternal tract. PLoS One, 7(3):e33625. https://doi.org/10.1371/journal.pone.0033625
Alminana, C., Tsikis, G., Labas, V., Uzbekov, R., da Silveira, J. C., Bauersachs, S., & Mermillod, P. (2018). Deciphering the oviductal extracellular vesicles content across the estrous cycle: Implications for the gametes-oviduct interactions and the environment of the potential embryo. BMC Genomics, 19(1), 622. https://doi.org/10.1186/s12864-018-4982-5
Alonso, B. R., Sanchez, J. M., Hamdi, M., Besenfelder, U., Havlicek, V., Lonergan, P., & Rizos, D. (2018). Oviduct-embryo interaction in cattle: Effect of asynchrony between the embryo and the oviduct on subsequent embryo development. Human Reproduction, 33, 236-237.
Arganaraz, M. E., Apichela, S. A., & Miceli, D. C. (2012). LEFTY2 expression and localization in rat oviduct during early pregnancy. Zygote, 20(1), 53-60. https://doi.org/10.1017/S0967199410000602
Barrera, D., Garcia, E. V., Sinowatz, F., Palma, G. A., Jimenez-Diaz, M. A., & Miceli, D. C. (2013). Expression of DNA methyltransferase genes in four-cell bovine embryos cultured in the presence of oviductal fluid. Anatomia, Histologia, Embryologia, 42(4), 312-315. https://doi.org/10.1111/ahe.12010
Bauersachs, S., Blum, H., Mallok, S., Wenigerkind, H., Rief, S., Prelle, K., & Wolf, E. (2003). Regulation of ipsilateral and contralateral bovine oviduct epithelial cell function in the postovulation period: A transcriptomics approach. Biology of Reproduction, 68(4), 1170-1177. https://doi.org/10.1095/biolreprod.102.010660
Bauersachs, S., Mitko, K., Ulbrich, S. E., Blum, H., & Wolf, E. (2008). Transcriptome studies of bovine endometrium reveal molecular profiles characteristic for specific stages of estrous cycle and early pregnancy. Experimental and Clinical Endocrinology & Diabetes, 116(7), 371-384. https://doi.org/10.1055/s-2008-1076714
Bauersachs, S., Rehfeld, S., Ulbrich, S. E., Mallok, S., Prelle, K., Wenigerkind, H., … Wolf, E. (2004). Monitoring gene expression changes in bovine oviduct epithelial cells during the oestrous cycle. Journal of Molecular Endocrinology, 32(2), 449-466. https://doi.org/10.1677/jme.0.0320449
Bousquet, D., Twagiramungu, H., Morin, N., Brisson, C., Carboneau, G., & Durocher, J. (1999). In vitro embryo production in the cow: An effective alternative to the conventional embryo production approach. Theriogenology, 51(1), 59-70. https://doi.org/10.1016/s0093-691x(98)00231-3
Briceag, I., Costache, A., Purcarea, V. L., Cergan, R., Dumitru, M., Briceag, I., … Ispas, A. T. (2015). Fallopian tubes-literature review of anatomy and etiology in female infertility. Journal of Medicine and Life, 8(2), 129-131. Retrieved from. https://www.ncbi.nlm.nih.gov/pubmed/25866566
Bridi, A., Perecin, F., & Silveira, J. C. D. (2020). Extracellular vesicles mediated early embryo-maternal interactions. International Journal of Molecular Sciences, 21(3), 1163. https://doi.org/10.3390/ijms21031163
Burkitt, M., Walker, D., Romano, D. M., & Fazeli, A. (2012). Using computational modeling to investigate sperm navigation and behavior in the female reproductive tract. Theriogenology, 77(4), 703-716. https://doi.org/10.1016/j.theriogenology.2011.11.011
Burns, G. W., Brooks, K. E., & Spencer, T. E. (2016). Extracellular vesicles originate from the conceptus and uterus during early pregnancy in sheep. Biology of Reproduction, 94(3), 56. https://doi.org/10.1095/biolreprod.115.134973
Cebrian-Serrano, A., Salvador, I., Garcia-Rosello, E., Pericuesta, E., Perez-Cerezales, S., Gutierrez-Adan, A., … Silvestre, M. A. (2013). Effect of the bovine oviductal fluid on in vitro fertilization, development and gene expression of in vitro-produced bovine blastocysts. Reproduction in Domestic Animals, 48(2), 331-338. https://doi.org/10.1111/j.1439-0531.2012.02157.x
Chegini, N., Zhao, Y., & McLean, F. W. (1994). Expression of messenger ribonucleic acid and presence of immunoreactive proteins for epidermal growth factor (EGF), transforming growth factor alpha (TGF alpha) and EGF/TGF alpha receptors and 125I-EGF binding sites in human fallopian tube. Biology of Reproduction, 50(5), 1049-1058. https://doi.org/10.1095/biolreprod50.5.1049
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. Biology of Reproduction, 89(3), 54. https://doi.org/10.1095/biolreprod.113.108829
Chen, S., Palma-Vera, S. E., Langhammer, M., Galuska, S. P., Braun, B. C., Krause, E., … Schoen, J. (2017). ). An air-liquid interphase approach for modeling the early embryo-maternal contact zone. Scientific Reports, 7, 42298. https://doi.org/10.1038/srep42298
Chen, Z., Hagen, D. E., Wang, J., Elsik, C. G., Ji, T., Siqueira, L. G., … Rivera, R. M. (2016). Global assessment of imprinted gene expression in the bovine conceptus by next generation sequencing. Epigenetics, 11(7), 501-516. https://doi.org/10.1080/15592294.2016.1184805
Chow, J. F., Lee, K. F., Chan, S. T., & Yeung, W. S. (2001). Quantification of transforming growth factor beta1 (TGFbeta1) mRNA expression in mouse preimplantation embryos and determination of TGFbeta receptor (type I and type II) expression in mouse embryos and reproductive tract. Molecular Human Reproduction, 7(11), 1047-1056. https://doi.org/10.1093/molehr/7.11.1047
Croxatto, H. B. (2002). Mechanisms that explain the contraceptive action of progestin implant for women. Contraception, 65(1), 21-27. https://doi.org/10.1016/S0010-7824(01)00294-3
Daliri, M., Rao, K. B. C. A., Kaur, G., Garg, S., Patil, S., & Totey, S. M. (1999). Expression of growth factor ligand and receptor genes in preimplantation stage water buffalo (Bubalus bubalis) embryos and oviduct epithelial cells. Journal of Reproduction and Fertility, 117(1), 61-70.
Diskin, M. G., & Morris, D. G. (2008). Embryonic and early fetal losses in cattle and other ruminants. Reproduction in Domestic Animals, 43(Suppl 2), 260-267. https://doi.org/10.1111/j.1439-0531.2008.01171.x
Downing, S. J., Maguiness, S. D., Tay, J. I., Watson, A., & Leese, H. J. (2002). Effect of platelet-activating factor on the electrophysiology of the human Fallopian tube: Early mediation of embryo-maternal dialog? Reproduction, 124(4), 523-529. https://doi.org/10.1530/rep.0.1240523
Eddie, S. L., Quartuccio, S. M., E, O. h, Moyle-Heyrman, G., Lantvit, D. D., Wei, J. J., … Burdette, J. E. (2015). Tumorigenesis and peritoneal colonization from fallopian tube epithelium. Oncotarget, 6(24), 20500-20512. https://doi.org/10.18632/oncotarget.3985
Emiliani, S., Delbaere, A., Devreker, F., & Englert, Y. (2005). Embryo-maternal interactive factors regulating the implantation process: Implications in assisted reproductive. Reproductive BioMedicine Online, 10(4), 527-540. https://doi.org/10.1016/s1472-6483(10)60831-0
Enright, B. P., Lonergan, P., Dinnyes, A., Fair, T., Ward, F. A., Yang, X., & Boland, M. P. (2000). Culture of in vitro produced bovine zygotes in vitro vs in vivo: Implications for early embryo development and quality. Theriogenology, 54(5), 659-673. https://doi.org/10.1016/S0093-691X(00)00381-2
Eyestone, W. H., & First, N. L. (1989). Co-culture of early cattle embryos to the blastocyst stage with oviducal tissue or in conditioned medium. Journal of Reproduction and Fertility, 85(2), 715-720. https://doi.org/10.1530/jrf.0.0850715
Fazeli, A. (2008). Maternal communication with gametes and embryos. Theriogenology, 70(8), 1182-1187. https://doi.org/10.1016/j.theriogenology.2008.06.010
Fazeli, A. (2011). Maternal communication with gametes and embryo: A personal opinion. Reproduction in Domestic Animals, 46(Suppl 2), 75-78. https://doi.org/10.1111/j.1439-0531.2011.01870.x
Ferraz, M., Henning, H. H. W., Costa, P. F., Malda, J., Melchels, F. P., Wubbolts, R., … Gadella, B. M. (2017). Improved bovine embryo production in an oviduct-on-a-chip system: Prevention of poly-spermic fertilization and parthenogenic activation. Lab Chip, 17(5), 905-916. https://doi.org/10.1039/c6lc01566b
Ferraz, M., Henning, H. H. W., Stout, T. A. E., Vos, P., & Gadella, B. M. (2017). Designing 3-dimensional in vitro oviduct culture systems to study mammalian fertilization and embryo production. Annals of Biomedical Engineering, 45(7), 1731-1744. https://doi.org/10.1007/s10439-016-1760-x
Freeman, D. A., Woods, G. L., Vanderwall, D. K., & Weber, J. A. (1992). Embryo-initiated oviductal transport in mares. Journal of Reproduction and Fertility, 95(2), 535-538. https://doi.org/10.1530/jrf.0.0950535
Gandolfi, F., & Moor, R. M. (1987). Stimulation of early embryonic development in the sheep by co-culture with oviduct epithelial cells. Journal of Reproduction and Fertility, 81(1), 23-28. https://doi.org/10.1530/jrf.0.0810023
Garcia, E. V., Hamdi, M., Barrera, A. D., Sanchez-Calabuig, M. J., Gutierrez-Adan, A., & Rizos, D. (2017). Bovine embryo-oviduct interaction in vitro reveals an early cross talk mediated by BMP signaling. Reproduction, 153(5), 631-643. https://doi.org/10.1530/REP-16-0654
Gardner, D. K., & Leese, H. J. (1990). Concentrations of nutrients in mouse oviduct fluid and their effects on embryo development and metabolism in vitro. Journal of Reproduction and Fertility, 88(1), 361-368. https://doi.org/10.1530/jrf.0.0880361
Gomez, E., & Munoz, M. (2015). Multiple-embryo transfer for studying very early maternal-embryo interactions in cattle. Reproduction, 150(2), R35-43. https://doi.org/10.1530/REP-14-0465
Gregoraszczuk, E. L., Cala, M., & Witkowska, E. (2000). Glycogen distribution in porcine fallopian tube epithelium during the estrus cycle. Folia Biol (Krakow), 48(3-4), 85-90. Retrieved from. https://www.ncbi.nlm.nih.gov/pubmed/11291545
Halbert, S. A., Tam, P. Y., & Blandau, R. J. (1976). Egg transport in the rabbit oviduct: The roles of cilia and muscle. Science, 191(4231), 1052-1053. https://doi.org/10.1126/science.1251215
Hamdi, M., Lopera-Vasquez, R., Maillo, V., Sanchez-Calabuig, M. J., Nunez, C., Gutierrez-Adan, A., & Rizos, D. (2018). Bovine oviductal and uterine fluid support in vitro embryo development. Reproduction, Fertility, and Development, 30(7), 935-945. https://doi.org/10.1071/RD17286
Hugentobler, S. A., Humpherson, P. G., Leese, H. J., Sreenan, J. M., & Morris, D. G. (2008). Energy substrates in bovine oviduct and uterine fluid and blood plasma during the oestrous cycle. Molecular Reproduction and Development, 75(3), 496-503. https://doi.org/10.1002/mrd.20760
Hugentobler, S. A., Sreenan, J. M., Humpherson, P. G., Leese, H. J., Diskin, M. G., & Morris, D. G. (2010). Effects of changes in the concentration of systemic progesterone on ions, amino acids, and energy substrates in cattle oviduct and uterine fluid and blood. Reproduction, Fertility, and Development, 22(4), 684-694. https://doi.org/10.1071/RD09129
Kawamura, K., Sato, N., Fukuda, J., Kodama, H., Kumagai, J., Tanikawa, H., … Tanaka, T. (2002). Leptin promotes the development of mouse preimplantation embryos in vitro. Endocrinology, 143(5), 1922-1931. https://doi.org/10.1210/endo.143.5.8818
Kaye, P. L., & Harvey, M. B. (1995). The role of growth factors in preimplantation development. Progress in Growth Factor Research, 6(1), 1-24. https://doi.org/10.1016/0955-2235(95)00001-1
Kolle, S. (2012). Live cell imaging of the oviduct. Methods in Enzymology, 506, 415-423. https://doi.org/10.1016/B978-0-12-391856-7.00045-7
Kolle, S., Dubielzig, S., Reese, S., Wehrend, A., Konig, P., & Kummer, W. (2009). Ciliary transport, gamete interaction, and effects of the early embryo in the oviduct: Ex vivo analyses using a new digital videomicroscopic system in the cow. Biology of Reproduction, 81(2), 267-274. https://doi.org/10.1095/biolreprod.108.073874
Kolle, S., Reese, S., & Kummer, W. (2010). New aspects of gamete transport, fertilization, and embryonic development in the oviduct gained by means of live cell imaging. Theriogenology, 73(6), 786-795. https://doi.org/10.1016/j.theriogenology.2009.11.002
Lai, Y. M., Wang, H. S., Lee, C. L., Lee, J. D., Huang, H. Y., Chang, F. H., … Soong, Y. K. (1996). Insulin-like growth factor-binding proteins produced by Vero cells, human oviductal cells and human endometrial cells, and the role of insulin-like growth factor-binding protein-3 in mouse embryo co-culture systems. Human Reproduction, 11(6), 1281-1286. https://doi.org/10.1093/oxfordjournals.humrep.a019372
Lavranos, T. C., Rathjen, P. D., & Seamark, R. F. (1995). Trophic effects of myeloid leukemia inhibitory factor (LIF) on mouse embryos. Journal of Reproduction and Fertility, 105(2), 331-338. https://doi.org/10.1530/jrf.0.1050331
Lazzari, G., Colleoni, S., Lagutina, I., Crotti, G., Turini, P., Tessaro, I., … Galli, C. (2010). Short-term and long-term effects of embryo culture in the surrogate sheep oviduct versus in vitro culture for different domestic species. Theriogenology, 73(6), 748-757. https://doi.org/10.1016/j.theriogenology.2009.08.001
Lee, J. M., Mhawech-Fauceglia, P., Lee, N., Parsanian, L. C., Lin, Y. G., Gayther, S. A., & Lawrenson, K. (2013). A three-dimensional microenvironment alters protein expression and chemosensitivity of epithelial ovarian cancer cells in vitro. Laboratory Investigation, 93(5), 528-542. https://doi.org/10.1038/labinvest.2013.41
Lee, K. F., Xu, J. S., Lee, Y. L., & Yeung, W. S. (2006). Demilune cell and parotid protein from murine oviductal epithelium stimulates preimplantation embryo development. Endocrinology, 147(1), 79-87. https://doi.org/10.1210/en.2005-0596
Lee, K. F., Xu, J. S., Lee, Y. L., & Yeung, W. S. (2006). Demilune cell and parotoid protein from murine oviductal epithelium stimulates preimplantation embryo development. Endocrinology, 147, 79-87.
Lee, K. F., Yao, Y. Q., Kwok, K. L., Xu, J. S., & Yeung, W. S. (2002). Early developing embryos affect the gene expression patterns in the mouse oviduct. Biochemical and Biophysical Research Communications, 292(2), 564-570. https://doi.org/10.1006/bbrc.2002.6676
Leese, H. J. (1988). The formation and function of oviduct fluid. Journal of Reproduction and Fertility, 82(2), 843-856. https://doi.org/10.1530/jrf.0.0820843
Levanon, K., Ng, V., Piao, H. Y., Zhang, Y., Chang, M. C., Roh, M. H., … Drapkin, R. (2010). Primary ex vivo cultures of human fallopian tube epithelium as a model for serous ovarian carcinogenesis. Oncogene, 29(8), 1103-1113. https://doi.org/10.1038/onc.2009.402
Li, S., Guo, X. C., Zhang, T., Wang, N., Li, J. Y., Xu, P. F., … Li, D. S. (2017). ). Fibroblast growth factor 21 ameliorates high glucose-induced fibrogenesis in mesangial cells through inhibiting STAT5 signaling pathway. Biomedicine & Pharmacotherapy, 93, 695-704. https://doi.org/10.1016/j.biopha.2017.06.100
Li, S., O'Neill, S. R. S., Zhang, Y., Holtzman, M. J., Takemaru, K. -I., Korach, K. S., & Winuthanyanon, W. (2017). Estrogen receptor α is required for oviductal transport of embryos. The Journal of the Federation of American Societies for Experimental Biology, 31(4), 1595-1607. https://doi.org/10.1096/fj.201601128R
Lighten, A. D., Moore, G. E., Winston, R. M., & Hardy, K. (1998). Routine addition of human insulin-like growth factor-I ligand could benefit clinical in-vitro fertilization culture. Human Reproduction, 13(11), 3144-3150. https://doi.org/10.1093/humrep/13.11.3144
Lloyd, R. E., Romar, R., Matas, C., Gutierrez-Adan, A., Holt, W. V., & Coy, P. (2009). Effects of oviductal fluid on the development, quality, and gene expression of porcine blastocysts produced in vitro. Reproduction, 137(4), 679-687. https://doi.org/10.1530/REP-08-0405
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. Biology of Reproduction, 54(6), 1420-1429. https://doi.org/10.1095/biolreprod54.6.1420
Lonergan, P., & Fair, T. (2008). In vitro-produced bovine embryos: Dealing with the warts. Theriogenology, 69(1), 17-22. https://doi.org/10.1016/j.theriogenology.2007.09.007
Lopera-Vasquez, R., Hamdi, M., Fernandez-Fuertes, B., Maillo, V., Beltran-Brena, P., Calle, A., … Rizos, D. (2016). Extracellular vesicles from BOEC in in vitro embryo development and quality. PLoS One, 11(2):e0148083. https://doi.org/10.1371/journal.pone.0148083
Lopera-Vasquez, R., Hamdi, M., Maillo, V., Gutierrez-Adan, A., Bermejo-Alvarez, P., Ramirez, M. A., … Rizos, D. (2017). Effect of bovine oviductal extracellular vesicles on embryo development and quality in vitro. Reproduction, 153(4), 461-470. https://doi.org/10.1530/REP-16-0384
Lopera-Vasquez, R., Hamdi, M., Mailo, V., Nunez, C., Yanez-Mo, M., Ramirez, M. A., … Rizos, D. (2015). Extracellular vesicles of bovine oviductal fluid modify the gene expression on bovine in vitro-derived embryos. Reproduction, Fertility, and Development, 28, 179. https://doi.org/10.1071/RDv28n2Ab99
Maillo, V., Gaora, P. O., Forde, N., Besenfelder, U., Havlicek, V., Burns, G. W., … Rizos, D. (2015). Oviduct-embryo interactions in cattle: Two-way traffic or a one-way street? Biology of Reproduction, 92(6), 144. https://doi.org/10.1095/biolreprod.115.127969
Maillo, V., Lopera-Vasquez, R., Hamdi, M., Gutierrez-Adan, A., Lonergan, P., & Rizos, D. (2016). Maternal-embryo interaction in the bovine oviduct: Evidence from in vivo and in vitro studies. Theriogenology, 86(1), 443-450. https://doi.org/10.1016/j.theriogenology.2016.04.060
McComb, P., Langley, L., Villalon, M., & Verdugo, P. (1986). The oviductal cilia and Kartagener's syndrome. Fertility and Sterility, 46(3), 412-416. Retrieved from. https://www.ncbi.nlm.nih.gov/pubmed/3488922
Mellisho, E. A., Velasquez, A. E., Nunez, M. J., Cabezas, J. G., Cueto, J. A., Fader, C., … Rodriguez-Alvarez, L. (2017). Identification and characteristics of extracellular vesicles from bovine blastocysts produced in vitro. PLoS One, 12(5):e0178306. https://doi.org/10.1371/journal.pone.0178306
Memili, E., Dominko, T., & First, N. L. (1998). Onset of transcription in bovine oocytes and preimplantation embryos. Molecular Reproduction and Development, 51(1), 36-41. https://doi.org/10.1002/(SICI)1098-2795(199809)51:1<36::AID-MRD4>3.0.CO;2-X
Miessen, K., Sharbati, S., Einspanier, R., & Schoen, J. (2011). Modeling the porcine oviduct epithelium: A polarized in vitro system suitable for long-term cultivation. Theriogenology, 76(5), 900-910. https://doi.org/10.1016/j.theriogenology.2011.04.021
Mokhtar, D. M. (2015). Microscopic and histochemical characterization of the bovine uterine tube during the follicular and luteal phases of estrous cycle. J Microsc Ultrastruct, 3(1), 44-52. https://doi.org/10.1016/j.jmau.2014.09.002
Nakamura, K., Kusama, K., Bai, R., Sakurai, T., Isuzugawa, K., Godkin, J. D., … Imakawa, K. (2016). Induction of IFNT-stimulated genes by conceptus-derived exosomes during the attachment period. PLoS One, 11(6):e0158278. https://doi.org/10.1371/journal.pone.0158278
Natale, D. R., De Sousa, P. A., Westhusin, M. E., & Watson, A. J. (2001). Sensitivity of bovine blastocyst gene expression patterns to culture environments assessed by differential display RT-PCR. Reproduction, 122(5), 687-693. Retrieved from. https://www.ncbi.nlm.nih.gov/pubmed/11690528
Noreikat, K., Wolff, M., Kummer, W., & Kolle, S. (2012). Ciliary activity in the oviduct of cycling, pregnant, and muscarinic receptor knockout mice. Biology of Reproduction, 86(4), 120. https://doi.org/10.1095/biolreprod.111.096339
O'Doherty, A. M., MacHugh, D. E., Spillane, C., & Magee, D. A. (2015). Genomic imprinting effects on complex traits in domesticated animal species. Frontiers in Genetics, 6, 156. https://doi.org/10.3389/fgene.2015.00156
O'Neill, C., Ryan, J. P., Collier, M., Saunders, D. M., Ammit, A. J., & Pike, I. L. (1989). Supplementation of in vitro fertilization culture medium with platelet activating factor. Lancet, 2(8666), 769-772. https://doi.org/10.1016/s0140-6736(89)90831-3
Ortiz, M. E., Bedregal, C., Carvajal, M. I., & Croxatto, H. B. (1986). Fertilized and unfertilized ova are transported at different rates by the hamster oviduct. Biology of Reproduction, 34(4), 777-781. https://doi.org/10.1095/biolreprod34.4.777
Ortiz, M. E., Llados, C., & Croxatto, H. B. (1989). Embryos of different ages transferred to the rat oviduct enter the uterus at different times. Biology of Reproduction, 41(3), 381-384. https://doi.org/10.1095/biolreprod41.3.381
Ovalle, W. K., Nahirney, P. C. (2013). Female reproductive system. In W. K. Ovalle & P. C. Nahirney (Eds.), Netter's essential histology (2 ed., pp. 403-429). Philadelphia: Elsevier Saunders.
Papanikolaou, E. G., Kolibianakis, E. M., Tournaye, H., Venetis, C. A., Fatemi, H., Tarlatzis, B., & Devroey, P. (2008). Live birth rates after transfer of equal number of blastocysts or cleavage-stage embryos in IVF. A systematic review and meta-analysis. Human Reproduction, 23(1), 91-99. https://doi.org/10.1093/humrep/dem339
Paria, B. C., & Dey, S. K. (1990). Preimplantation embryo development in vitro: Cooperative interactions among embryos and role of growth factors. Proceedings of the National Academy of Sciences of the United States of America, 87(12), 4756-4760. https://doi.org/10.1073/pnas.87.12.4756
Pfeifer, T. L., & Chegini, N. (1994). Immunohistochemical Localization of Insulin-Like Growth-Factor (Igf-I), Igf-I Receptor, and Igf Binding-Proteins-1-4 in Human Fallopian-Tube at Various Reproductive Stages. Biology of Reproduction, 50(2), 281-289. https://doi.org/10.1095/biolreprod50.2.281
Ponsuksili, S., Tesfaye, D., El-Halawany, N., Schellander, K., & Wimmers, K. (2002). Stage-specific expressed sequence tags obtained during preimplantation bovine development by differential display RT-PCR and suppression subtractive hybridization. Prenatal Diagnosis, 22(12), 1135-1142. https://doi.org/10.1002/pd.501
Pontes, J. H., Silva, K. C., Basso, A. C., Rigo, A. G., Ferreira, C. R., Santos, G. M., … Seneda, M. M. (2010). Large-scale in vitro embryo production and pregnancy rates from Bos taurus, Bos indicus, and indicus-taurus dairy cows using sexed sperm. Theriogenology, 74(8), 1349-1355. https://doi.org/10.1016/j.theriogenology.2010.06.004
Pope, W. F. (1994). Embryonic mortality in swine. In R. D. Geisert (Ed.), Embryonic mortality in domestic species (pp. 53-77). Boca Raton: CRC Press.
Reischl, J., Prelle, K., Schol, H., Neumuller, C., Einspanier, R., Sinowatz, F., & Wolf, E. (1999). Factors affecting proliferation and dedifferentiation of primary bovine oviduct epithelial cells in vitro. Cell and Tissue Research, 296(2), 371-383. https://doi.org/10.1007/s004410051297
Rezvani, M., & Shaaban, A. M. (2011). Fallopian tube disease in the nonpregnant patient. Radiographics, 31(2), 527-548. https://doi.org/10.1148/rg.312105090
Rizos, D., Maillo, V., Sanchez-Calabuig, M. J., & Lonergan, P. (2017). The consequences of maternal-embryonic cross talk during the periconception period on subsequent embryonic development. Advances in Experimental Medicine and Biology, 1014, 69-86. https://doi.org/10.1007/978-3-319-62414-3_4
Rizos, D., Ramirez, M. A., Pintado, B., Longeran, P., & Gutierrez-Adan, A. (2010). Culture of bovine embryos in intermediate host oviducts with emphasis on the isolated mouse oviduct. Theriogenology, 73(6), 777-785. https://doi.org/10.1016/j.theriogenology.2009.10.001
Rizos, D., Ward, F., Duffy, P., Boland, M. P., & Lonergan, P. (2002). Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: Implications for blastocyst yield and blastocyst quality. Molecular Reproduction and Development, 61(2), 234-248. https://doi.org/10.1002/mrd.1153
Roberts, C., O'Neill, C., & Wright, L. (1993). Platelet activating factor (PAF) enhances mitosis in preimplantation mouse embryos. Reproduction, Fertility, and Development, 5(3), 271-279. https://doi.org/10.1071/rd9930271
Rodriguez-Alonso, B., Hamdi, M., Sanchez, J. M., Maillo, V., Gutierrez-Adan, A., Lonergan, P., & Rizos, D. (2019). An approach to study the local embryo effect on gene expression in the bovine oviduct epithelium in vivo. Reproduction in Domestic Animals, 54(12), 1516-1523. https://doi.org/10.1111/rda.13558
Rodriguez-Alonso, B., Hamdi, M., Sanchez, J. M., Gutierrez-Adan, A., Lonergan, P., & Rizos, D. (2018). In vivo transcriptomic response of bovine oviduct epithelial cells to the early embryo. Reproduction, Fertility, and Development, 30(197), 197.
Rottmayer, R., Ulbrich, S. E., Kolle, S., Prelle, K., Neumueller, C., Sinowatz, F., … Hiendleder, S. (2006). A bovine oviduct epithelial cell suspension culture system suitable for studying embryo-maternal interactions: Morphological and functional characterization. Reproduction, 132(4), 637-648. https://doi.org/10.1530/rep.1.01136
Sakkas, D., & Trounson, A. O. (1990). Co-culture of mouse embryos with oviduct and uterine cells prepared from mice at different days of pseudopregnancy. Journal of Reproduction and Fertility, 90(1), 109-118. https://doi.org/10.1530/jrf.0.0900109
Salilew-Wondim, D., Fournier, E., Hoelker, M., Saeed-Zidane, M., Tholen, E., Looft, C., … Tesfaye, D. (2015). Genome-wide DNA methylation patterns of bovine blastocysts developed in vivo from embryos completed different stages of development in vitro. PLoS One, 10(11):e0140467. doi:ARTN e014046710.1371/journal.pone.0140467
Sathananthan, A. H., & Trounson, A. O. (2000). Mitochondrial morphology during preimplantational human embryogenesis. Human Reproduction, 15(Suppl 2), 148-159. https://doi.org/10.1093/humrep/15.suppl_2.148
Simintiras, C. A., & Forde, N. (2017). Understanding the uterine environment in early pregnancy in cattle: How have the omics enhanced our knowledge? Animal Reproduction, 14(3), 538-546. https://doi.org/10.21451/1984-3143-Ar997
Simon, C., Greening, D. W., Bolumar, D., Balaguer, N., Salamonsen, L. A., & Vilella, F. (2018). Extracellular vesicles in human reproduction in health and disease. Endocrine Reviews, 39(3), 292-332. https://doi.org/10.1210/er.2017-00229
Sjoblom, C., Roberts, C. T., Wikland, M., & Robertson, S. A. (2005). Granulocyte-macrophage colony-stimulating factor alleviates adverse consequences of embryo culture on fetal growth trajectory and placental morphogenesis. Endocrinology, 146(5), 2142-2153. https://doi.org/10.1210/en.2004-1260
Smits, K., De Coninck, D. I., Van Nieuwerburgh, F., Govaere, J., Van Poucke, M., Peelman, L., … Van Soom, A. (2016). The equine embryo influences immune-related gene expression in the oviduct. Biology of Reproduction, 94(2), 36. https://doi.org/10.1095/biolreprod.115.136432
Smits, K., Willems, S., Van Steendam, K., Van De Velde, M., De Lange, V., Ververs, C., … Van Soom, A. (2018). Proteins involved in embryo-maternal interaction around the signaling of maternal recognition of pregnancy in the horse. Scientific Reports, 8(1), 5249. https://doi.org/10.1038/s41598-018-23537-6
Sponchiado, M., Gomes, N. S., Fontes, P. K., Martins, T., Del Collado, M., Pastore, A. A., … Binelli, M. (2017). Pre-hatching embryo-dependent and -independent programming of endometrial function in cattle. PLoS One, 12(4):e0175954. https://doi.org/10.1371/journal.pone.0175954
Sturmey, R. G., Reis, A., Leese, H. J., & McEvoy, T. G. (2009). Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reproduction in Domestic Animals, 44(Suppl 3), 50-58. https://doi.org/10.1111/j.1439-0531.2009.01402.x
Suarez, S. S. (1987). Sperm transport and motility in the mouse oviduct: Observations in situ. Biology of Reproduction, 36(1), 203-210. https://doi.org/10.1095/biolreprod36.1.203
Suarez, S. S., & Pacey, A. A. (2006). Sperm transport in the female reproductive tract. Human Reproduction Update, 12(1), 23-37. https://doi.org/10.1093/humupd/dmi047
Sutton-McDowall, M. L., Feil, D., Robker, R. L., Thompson, J. G., & Dunning, K. R. (2012). Ultilization of endogenous fatty acid stores for energy production in bovine preimplantation embryos. Theriogenology, 77(8), 1632-1641. https://doi.org/10.1016/j.theriogenology.2011.12.008
Talbot, P., Geiske, C., & Knoll, M. (1999). Oocyte pickup by the mammalian oviduct. Molecular Biology of the Cell, 10(1), 5-8. https://doi.org/10.1091/mbc.10.1.5
Thibodeaux, J. K., Menezo, Y., Roussel, J. D., Hansel, W., Goodeaux, L. L., Thompson, D. L., Jr., & Godke, R. A. (1992). Coculture of in vitro fertilized bovine embryos with oviductal epithelial cells originating from different stages of the estrous cycle. Journal of Dairy Science, 75(6), 1448-1455. https://doi.org/10.3168/jds.S0022-0302(92)77900-4
Thompson, J. G., Partridge, R. J., Houghton, F. D., Kennedy, C. J., Pullar, D., & Leese, H. J. (1996). Oxygen consumption by day 7 bovine blastocysts: Determination of ATP production. Animal Reproduction Science, 43(4), 241-247. https://doi.org/10.1016/0378-4320(96)01477-7
Tiemann, U., Neels, P., Kuchenmeister, U., Walzel, H., & Spitschak, M. (1996). Effect of ATP and platelet-activating factor on intracellular calcium concentrations of cultured oviductal cells from cows. Journal of Reproduction and Fertility, 108(1), 1-9. https://doi.org/10.1530/jrf.0.1080001
Tiemann, U., Tomek, W., Schneider, F., Wollenhaupt, K., Kanitz, W., Becker, F., & Pohland, R. (2001). Platelet-activating factor (PAF)-like activity, localization of PAF receptor (PAF-R) and PAF-acetylhydrolase (PAF-AH) activity in bovine endometrium at different stages of the estrous cycle and early pregnancy. Prostaglandins & Other Lipid Mediators, 65(2-3), 125-141. https://doi.org/10.1016/S0090-6980(01)00130-7
Tienthai, P., Sajjarengpong, K., & Techakumphu, M. (2009). Light and scanning electron microscopic studies of oviductal epithelium in Thai swamp buffalo (Bubalus bubalis) at the follicular and luteal phases. Reproduction in Domestic Animals, 44(3), 450-455. https://doi.org/10.1111/j.1439-0531.2008.01111.x
Ulbrich, S. E., Zitta, K., Hiendleder, S., & Wolf, E. (2010). In vitro systems for intercepting early embryo-maternal cross-talk in the bovine oviduct. Theriogenology, 73(6), 802-816. https://doi.org/10.1016/j.theriogenology.2009.09.036
Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J. J., & Lotvall, J. O. (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature Cell Biology, 9(6), 654-659. https://doi.org/10.1038/ncb1596
Velasquez, L. A., Maisey, K., Fernandez, R., Valdes, D., Cardenas, H., Imarai, M., … Croxatto, H. B. (2001). PAF receptor and PAF acetylhydrolase expression in the endosalpinx of the human fallopian tube: Possible role of embryo-derived PAF in the control of embryo transport to the uterus. Human Reproduction, 16(8), 1583-1587. https://doi.org/10.1093/humrep/16.8.1583
Vigneault, C., Gravel, C., Vallee, M., McGraw, S., & Sirard, M. A. (2009). Unveiling the bovine embryo transcriptome during the maternal-to-embryonic transition. Reproduction, 137(2), 245-257. https://doi.org/10.1530/REP-08-0079
Walter, I. (1995). Culture of bovine oviduct epithelial cells (BOEC). Anatomical Record, 243(3), 347-356. https://doi.org/10.1002/ar.1092430309
Weber, J. A., Woods, G. L., Freeman, D. A., & Vanderwall, D. K. (1992). Prostaglandin E2-specific binding to the equine oviduct. Prostaglandins, 43(1), 61-65. https://doi.org/10.1016/0090-6980(92)90065-2
Wang, S., & Larina, I. V. (2018). In vivo imaging of the mouse reproductive organs, embryo transfer, and oviduct cilia dynamics using optical coherence tomography. In P. Delgado-Olguin (Ed.), Mouse embryogenesis: Methods in molecular biology. New York, NY: Humana Press. https://doi.org/10.1007/978-1-4939-7714-7_5
White, K. L., Hehnke, K., Rickords, L. F., Southern, L. L., Thompson, D. L., Jr., & Wood, T. C. (1989). Early embryonic development in vitro by coculture with oviductal epithelial cells in pigs. Biology of Reproduction, 41(3), 425-430. https://doi.org/10.1095/biolreprod41.3.425
Wolf, E., Arnold, G. J., Bauersachs, S., Beier, H. M., Blum, H., Einspanier, R., … Sinowatz, F. (2003). Embryo-maternal communication in bovine-strategies for deciphering a complex cross-talk. Reproduction in Domestic Animals, 38(4), 276-289. https://doi.org/10.1046/j.1439-0531.2003.00435.x
Xu, J. S., Lee, Y. L., Lee, K. F., Kwok, K. L., Lee, W. M., Luk, J. M., & Yeung, W. S. (2004). Embryotrophic factor-3 from human oviductal cells enhances proliferation, suppresses apoptosis and stimulates the expression of the beta1 subunit of sodium-potassium ATPase in mouse embryos. Human Reproduction, 19(12), 2919-2926. https://doi.org/10.1093/humrep/deh497
Yao, Y., Li, W., Wu, J., Germann, U.A., Su, M.S.S., Kuida, K., & Boucher, D.M. (2003). Extracellular signal-regulated kinase 2 is necessary for mesoderm differentiation. Proceedings of the National Academy for Sciences of the United States of America, 100(22), 12759-12764. https://doi.org/10.1073/pnas.2134254100
Yeung, W. S., Ho, P. C., Lau, E. Y., & Chan, S. T. (1992). Improved development of human embryos in vitro by a human oviductal cell co-culture system. Human Reproduction, 7(8), 1144-1149. https://doi.org/10.1093/oxfordjournals.humrep.a137810
Zinaman, M. J., Clegg, E. D., Brown, C. C., O'Connor, J., & Selevan, S. G. (1996). Estimates of human fertility and pregnancy loss. Fertility and Sterility, 65(3), 503-509. Retrieved from. https://www.ncbi.nlm.nih.gov/pubmed/8774277