Bovine oocyte developmental competence and gene expression following co-culturing with ampullary cells: An experimental study
Background: There is no sufficient information on the impact of bovine ampullary oviductal epithelial cells (BAOECs) on in vitro oocyte maturation competence and gene expression.
Objective: This study aimed to examine the oocyte developmental competence following co-culturing with a monolayer of fresh and frozen-thawed ampullary cells.
Materials and Methods: Bovine cumulus-oocyte complexes (COCs) were distributed into three groups: control group; where in COCs were cultured in cell-free media for 24 hr and FML and FTML groups in which the COCs were cultured in maturation media for 18 hr and then transferred into a media containing fresh and frozen-thawed BAOECs monolayer, respectively (BAOECs were extracted from the oviducts of slaughtered cattle and were then cultured freshly or frozen-thawed) for a further 6 hr. After 24 hr, the expanded COCs were evaluated for nuclear maturation, fertilization rate, and gene expression (GDF9, StAR, CASP3, and FSHr).
Results: Nuclear maturation rate in the FTML group was significantly higher than the control group (p = 0.02). The fertilization rate of FTML group was significantly higher than the control and FML groups (p = 0.05 and p = 0.03, respectively). In terms of gene expression, GDF9 were upregulated in the presence of the BAOECs during the last 6 hr of the in vitro maturation (p < 0.001). Furthermore, the expression of the StAR gene in the FTML group was higher than the other groups (p = 0.02).
Conclusion: Ampullary cells co-culturing (especially frozen-thawed cells) for in vitro maturation of bovine oocytes yields encourages the results and demonstrates the beneficial effect of co-culture on gene expression and developmental competence.
Key words: Ampulla, Bovine, Fertilization, Gene expression, IVM.
 Kölle S, Dubielzig S, Reese S, Wehrend A, König P, Kummer W. 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. Biol Reprod 2009; 81: 267–274.
 Coy P, Garcia-Vázquez FA, Visconti PE, Avilés M. Roles of the oviduct in mammalian fertilization. Reproduction 2012; 144: 649–660.
 Ghersevich S, Massa E, Zumoffen C. Oviductal secretion and gamete interaction. Reproduction 2015; 149: 1–14.
 Lopera-Vasquez R, Hamdi M, Maillo V, Gutierrez-Adan A, Bermejo-Alvarez P, Ramirez MA, et al. Effect of bovine oviductal extracellular vesicles on embryo development and quality in vitro. Reproduction 2017; 153: 461–470.
 Niżański W, Partyka A, Prochowska S. Evaluation of spermatozoal function-useful tools or just science. Reprod Domest Anim 2016; 51: 37–45.
 Coy P, Cánovas S, Mondéjar I, Saavedra MD, Romar R, Grullón L, et al. Oviduct-specific glycoprotein and heparin modulate sperm-zona pellucida interaction during fertilization and contribute to the control of polyspermy. Proc Natl Acad Sci U S A 2008; 105: 15809–15814.
 Nematollahi-mahani SN, Pahang H, Moshkdanian G, Nematollahi-mahani A. Effect of embryonic fibroblast cell co-culture on development of mouse embryos following exposure to visible light. J Assist Reprod Genet 2009; 26: 129–135.
 Park KS, Kim YS, Kim JH, Choi B, Kim SH, Tan AHK, et al. Trophic molecules derived from human mesenchymal stem cells enhance survival, function, and angiogenesis of isolated islets after transplantation. Transplantation 2010; 89: 509–517.
 Asgharzadeh S, Mirshokraei P, Hassanpour H, Ahmadi E, Nazari H. The effect of mesenchymal stem cells as coculture in in vitro nuclear maturation of ovine oocytes. Anim Sci Paper Report 2015; 33: 223–232.
 Lopera-Vásquez R, Hamdi M, Fernandez-Fuertes B, Maillo V, Beltrán-Breña P, Calle A, et al. Extracellular vesicles from BOEC in in vitro embryo development and quality. PLoS One 2016; 11: e0148083.
 Azari M, Kafi M, Ebrahimi B, Fatehi R, Jamalzadeh M. Oocyte maturation, embryo development and gene expression following two different methods of bovine cumulus-oocyte complexes vitrification. Vet Res Commun 2017; 41: 49–56.
 Manna PR, Dyson MT, Stocco DM. Regulation of the steroidogenic acute regulatory protein gene expression: Present and future perspectives. Mol Hum Reprod 2009; 15: 321–333.
 Freshney RI. Culture of animal cells: A manual of basic technique and specialized applications. 7th Ed. John Wiley & Sons, Hoboken, New Jersey; 2015.
 Asaadi A, Kafi M, Atashi H, Azari M, Hostens M. Frozenthawed ampullary cell monolayer improves bovine embryo in vitro development and quality. Zygote 2019; 27: 337– 346.
 Kafi M, Ashrafi M, Azari M, Jandarroodi B, Abouhamzeh B, Asl AR. Niacin improves maturation and cryo-tolerance of bovine in vitro matured oocytes: An experimental study. Int J Reprod Biomed 2019; 17: 621–628.
 Kafi M, Azari M, Chashnigir O, Gharibzadeh S, Aghabozorgi Z, Asaadi A, et al. Inherent inferior quality of follicular fluid in repeat breeder heifers as evidenced by low rates of in vitro production of bovine embryos. Theriogenology 2017; 102: 29–34.
 Dadashpour Davachi N, Kohram H, Zare Shahneh A, Zhandi M, Goudarzi A, Fallahi R, et al. The effect of conspecific ampulla oviductal epithelial cells during in vitro maturation on oocyte developmental competence and maturation-promoting factor (MPF) activity in sheep. Theriogenology 2017; 88: 207–214.
 Davachi ND, Shahneh AZ, Kohram H, Zhandi M, Shamsi H, Hajiyavand AM, et al. Differential influence of ampullary and isthmic derived epithelial cells on zona pellucida hardening and in vitro fertilization in ovine. Reprod Biol 2016; 16: 61–69.
 Lee SH, Oh HJ, Kim MJ, Kim GA, Choi YB, Jo YK, et al. Oocyte maturation-related gene expression in the canine oviduct, cumulus cells, and oocytes and effect of coculture with oviduct cells on in vitro maturation of oocytes. J Assist Reprod Genet 2017; 34: 929–938.
 No J, Zhao M, Lee S, Ock SA, Nam Y, Hur TY. Enhanced in vitro maturation of canine oocytes by oviduct epithelial cell co-culture. Theriogenology 2018; 105: 66–74.
 Lopes JS, Canha-Gouveia A, París-Oller E, Coy P. Supplementation of bovine follicular fluid during in vitro maturation increases oocyte cumulus expansion, blastocyst developmental kinetics, and blastocyst cell number. Theriogenology 2019; 126: 222–229.
 Fair T, Carter F, Park S, Evans ACO, Lonergan P. Global gene expression analysis during bovine oocyte in vitro maturation. Theriogenology 2007; 68: S91–S97.
 Katz-Jaffe MG, McCallie BR, Preis KA, Filipovits J, Gardner DK. Transcriptome analysis of in vivo and in vitro matured bovine MII oocytes. Theriogenology 2009; 71: 939–946.
 Assidi M, Sirard MA. Cumulus cell gene expression as a marker of oocyte quality. In: Coticchio G, Albertini DF, De Santis L. Oogenesis. London: Springer; 2013: 231–252.
 Wang XL, Wang K, Zhao S, Wu Y, Gao H, Zeng SM. Oocytesecreted growth differentiation factor 9 inhibits BCL-2- interacting mediator of cell death-extra long expression in porcine cumulus cell. Biol Reprod 2013; 89: 56.
 Nyholt de Prada JK, Kellam LD, Patel BG, Latham KE, VandeVoort CA. Growth hormone and gene expression of in vitro−matured rhesus macaque oocytes. Mol Reprod Dev 2010; 77: 353–362.
 Luo DY, Yang G, Liu JJ, Yang YR, Dong Q. Effects of varicocele on testosterone, apoptosis and expression of StAR mRNA in rat Leydig cells. Asian J Androl 2011; 13: 287–291.
 Hou L, Zhang Y, Yu B, Yang Y, Li B, Wu J. Oocyte-G1 promotes male germ cell apoptosis through activation of Caspase-3. Gene 2018; 670: 22–30.