Hostname: page-component-cc8bf7c57-xrnlw Total loading time: 0 Render date: 2024-12-11T20:37:05.991Z Has data issue: false hasContentIssue false
  • English
  • Français

Frozen–thawed ampullary cell monolayer improves bovine embryo in vitro development and quality

Published online by Cambridge University Press:  13 August 2019

Anise Asaadi ,
Mojtaba Kafi Open the ORCID record for Mojtaba Kafi [Opens in a new window] ,
Hadi Atashi ,
Mehdi Azari  and
Miel Hostens
Anise Asaadi
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine, Shiraz University, Shiraz, Iran
Mojtaba Kafi*
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine, Shiraz University, Shiraz, Iran
Hadi Atashi
Affiliation:
Department of Animal Science, School of Agriculture, Shiraz University, Shiraz, Iran
Mehdi Azari
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine, Shiraz University, Shiraz, Iran
Miel Hostens
Affiliation:
Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
*
Address for correspondence: Mojtaba Kafi. Department of Animal Reproduction, School of Veterinary Medicine, Shiraz University, Shiraz, Iran. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The aim of this study was to evaluate the effects of different timing for frozen–thawed bovine ampullary epithelial cell (BAEC) and bovine oviductal epithelial cell (BOEC) co-culture on the development and quality of bovine embryos produced in vitro. Embryo development was assessed by day 8 blastocyst yield, whereas embryo quality was determined using blastocyst differential cell count, cryotolerance and the expression of selected genes related to embryo quality. The results showed that the presence of BAECs during the last 6 h of in vitro maturation (IVM) increased blastocyst yield and survival of the vitrified-warmed blastocysts. In addition, embryos produced in the presence of BAECs during the last 6 h of IVM or in the presence of BOECs during the first 4 days of in vitro culture (IVC) showed a greater number of trophectoderm cells and a greater inner cell mass. In terms of gene expression, IFN-T was downregulated and PLAC8, AQP3 and ATP1A1 were upregulated in the presence of the BAECs during the last 6 h of the IVM and/or in the presence of BOECs during the first 4 days of IVC. In conclusion, co-culturing bovine oocytes with a frozen–thawed ampullary cell monolayer during the last 6 h of maturation increased blastocyst yield and quality.

Keywords

AmpullaEmbryo productionGene expressionOocyte maturation
Type
Research Article
Information
Zygote , Volume 27 , Issue 5 , October 2019 , pp. 337 - 346
Copyright
© Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Austin, KJ, Ward, SK, Glaucia Teixeira, M, Dean, VC, Moore, DW and Hansen, TR (1996) Ubiquitin cross-reactive protein is released by the bovine uterus in response to interferon during early pregnancy. Biol Reprod 54, 600–6.CrossRefGoogle ScholarPubMed
Avilés, M, Gutierrez-Adán, A and Coy, P (2010) Oviductal secretions: will they be key factors for the future ARTs? Mol Hum Reprod 16, 896–906.CrossRefGoogle ScholarPubMed
Avilés, M, Coy, P and Rizos, D (2015) The oviduct: A key organ for the success of early reproductive events. Anim Front 5, 25–31.CrossRefGoogle Scholar
Azari, M, Kafi, M, Ebrahimi, B, Fatehi, R and Jamalzadeh, M (2017) Oocyte maturation, embryo development and gene expression following two different methods of bovine cumulus–oocyte complexes vitrification. Vet Res Commun 41, 49–56.CrossRefGoogle ScholarPubMed
Barcroft, L, Moseley, A, Lingrel, J and Watson, A (2004) Deletion of the Na/K-ATPase α1-subunit gene (Atp1a1) does not prevent cavitation of the preimplantation mouse embryo. Mech Dev 121, 417–26.Google Scholar
Betts, D and King, W (2001) Genetic regulation of embryo death and senescence. Theriogenology 55, 171–91.CrossRefGoogle ScholarPubMed
Brackett, BG and Oliphant, G (1975) Capacitation of rabbit spermatozoa in vitro. Biol Reprod 12, 260–74.CrossRefGoogle ScholarPubMed
Buhi, WC (2002) Characterization and biological roles of oviduct-specific, oestrogen-dependent glycoprotein. Reproduction 123, 355–62.CrossRefGoogle ScholarPubMed
Corcoran, D, Rizos, D, Fair, T, Evans, AC and Lonergan, P (2007) Temporal expression of transcripts related to embryo quality in bovine embryos cultured from the two‐cell to blastocyst stage in vitro or in vivo. Mol Reprod Dev 74, 972–7.CrossRefGoogle ScholarPubMed
Cordova, A, Perreau, C, Uzbekova, S, Ponsart, C, Locatelli, Y and Mermillod, P (2014) Development rate and gene expression of IVP bovine embryos cocultured with bovine oviduct epithelial cells at early or late stage of preimplantation development. Theriogenology 81, 1163–73.CrossRefGoogle ScholarPubMed
Coy, P, Cánovas, S, Mondéjar, I, Saavedra, MD, Romar, R, Grullón, L, Matás, C and Avilés, M (2008) Oviduct-specific glycoprotein and heparin modulate sperm–zona pellucida interaction during fertilization and contribute to the control of polyspermy. Proc Natl Acad Sci 105, 15809–14.CrossRefGoogle ScholarPubMed
Coy, P, Lloyd, R, Romar, R, Satake, N, Matás, C, Gadea, J and Holt, WV (2010) Effects of porcine pre-ovulatory oviductal fluid on boar sperm function. Theriogenology 74, 632–42.CrossRefGoogle ScholarPubMed
Coy, P, Garcia-Vázquez, FA, Visconti, PE and Avilés, M (2012) Roles of the oviduct in mammalian fertilization. Reproduction 144, 649–60.CrossRefGoogle ScholarPubMed
Edashige, K, Yamaji, Y, Kleinhans, F and Kasai, M (2003) Artificial expression of aquaporin-3 improves the survival of mouse oocytes after cryopreservation. Biol Reprod 68, 87–94.CrossRefGoogle ScholarPubMed
Fazeli, A and Pewsey, E (2008) Maternal communication with gametes and embryos: a complex interactome. Brief Func Genomics Proteomics 7, 111–8.CrossRefGoogle ScholarPubMed
Ferraz, MA, Henning, HH, Stout, TA, Vos, PL and Gadella, BM (2017) Designing 3-dimensional in vitro oviduct culture systems to study mammalian fertilization and embryo production. Annals Biomed Eng 45, 1731–44.CrossRefGoogle ScholarPubMed
Freshney, RI (2015) Culture of Animal Cells: A Manual of Basic Technique and Specialized Applications, 7th edition. New Jersey, USA: John Wiley & Sons.Google Scholar
Gad, A, Hoelker, M, Besenfelder, U, Havlicek, V, Cinar, U, Rings, F, Held, E, Dufort, I, Sirard, M-A and Schellander, K (2012) Molecular mechanisms and pathways involved in bovine embryonic genome activation and their regulation by alternative in vivo and in vitro culture conditions. Biol Reprod 87, 100.CrossRefGoogle ScholarPubMed
Galaviz-Hernandez, C, Stagg, C, De Ridder, G, Tanaka, TS, Ko, MS, Schlessinger, D and Nagaraja, R (2003) Plac8 and Plac9, novel placental-enriched genes identified through microarray analysis. Gene 309, 81–9.CrossRefGoogle ScholarPubMed
Galli, C and Lazzari, G (1996) Practical aspects of IVM/IVF in cattle. Anim Reprod Sci 42, 371–9.CrossRefGoogle Scholar
Ghersevich, S, Massa, E and Zumoffen, C (2015) Oviductal secretion and gamete interaction. Reproduction 149, R1–R14.CrossRefGoogle ScholarPubMed
Graf, A, Krebs, S, Heininen-Brown, M, Zakhartchenko, V, Blum, H and Wolf, E (2014) Genome activation in bovine embryos: review of the literature and new insights from RNA sequencing experiments. Anim Reprod Sci 149, 46–58.CrossRefGoogle ScholarPubMed
Hanaue, M, Miwa, N, Uebi, T, Fukuda, Y, Katagiri, Y and Takamatsu, K (2011) Characterization of S100A11, a suppressive factor of fertilization, in the mouse female reproductive tract. Mol Reprod Dev 78, 91–103.CrossRefGoogle ScholarPubMed
Hosseini, S, Asgari, V, Ostadhosseini, S, Hajian, M, Ghanaei, H and Nasr-Esfahani, M (2015) Developmental competence of ovine oocytes after vitrification: differential effects of vitrification steps, embryo production methods, and parental origin of pronuclei. Theriogenology 83, 366–76.CrossRefGoogle ScholarPubMed
Huang, H-F, He, R-H, Sun, C-C, Zhang, Y, Meng, Q-X and Ma, Y-Y (2006) Function of aquaporins in female and male reproductive systems. Hum Reprod Update 12, 785–95.CrossRefGoogle ScholarPubMed
Hunter, R (1974) Chronological and cytological details of fertilization and early embryonic development in the domestic pig, Sus scrofa. Anatom Rec 178, 169–185.CrossRefGoogle ScholarPubMed
Jurisicova, A, Antenos, M, Varmuza, S, Tilly, JL and Casper, RF (2003) Expression of apoptosis-related genes during human preimplantation embryo development: potential roles for the Harakiri gene product and caspase-3 in blastomere fragmentation. MHR: Basic Sci Reprod Med 9, 133–41.Google ScholarPubMed
Kattal, N, Cohen, J and Barmat, LI (2008) Role of coculture in human in vitro fertilization: a meta-analysis. Fertil Steril 90, 1069–76.CrossRefGoogle ScholarPubMed
Leese, HJ, Hugentobler, SA, Gray, SM, Morris, DG, Sturmey, RG, Whitear, S-L and Sreenan, JM (2007) Female reproductive tract fluids: composition, mechanism of formation and potential role in the developmental origins of health and disease. Reprod Fertil Dev 20, 1–8.CrossRefGoogle Scholar
Lonergan, P and Fair, T (2008) In vitro-produced bovine embryos—dealing with the warts. Theriogenology 69, 17–22.CrossRefGoogle ScholarPubMed
Lonergan, P and Fair, T (2016) Maturation of oocytes in vitro. Ann Rev Anim Biosci 4, 255–68.CrossRefGoogle ScholarPubMed
Lonergan, P, Rizos, D, Kanka, J, Nemcova, L, Mbaye, A, Kingston, M, Wade, M, Duffy, P and Boland, M (2003) Temporal sensitivity of bovine embryos to culture environment after fertilization and the implications for blastocyst quality. Reproduction 126, 337–46.CrossRefGoogle ScholarPubMed
Lopera-Vásquez, R, Hamdi, M, Fernandez-Fuertes, B, Maillo, V, Beltrán-Breña, P, Calle, A, Redruello, A, López-Martín, S, Gutierrez-Adán, A and Yáñez-Mó, M (2016) Extracellular vesicles from BOEC in in vitro embryo development and quality. PLoS One 11, e0148083.CrossRefGoogle ScholarPubMed
Lopera-Vásquez, R, Hamdi, M, Maillo, V, Gutierrez-Adán, A, Bermejo-Alvarez, P, Ramirez, MA, Yáñez-Mó, M and Rizos, D (2017) Effect of bovine oviductal extracellular vesicles on embryo development and quality in vitro . Reproduction 153, 461–70.CrossRefGoogle ScholarPubMed
Marshall, OJ (2004) PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 20, 2471–2.CrossRefGoogle ScholarPubMed
Melka, M, Rings, F, Hölker, M, Tholen, E, Havlicek, V, Besenfelder, U, Schellander, K and Tesfaye, D (2010) Expression of apoptosis regulatory genes and incidence of apoptosis in different morphological quality groups of in vitro-produced bovine pre-implantation embryos. Reprod Domest Anim 45, 915–21.Google ScholarPubMed
Mondéjar, I, Acuna, O, Izquierdo-Rico, M, Coy, P and Avilés, M (2012) The oviduct: functional genomic and proteomic approach. Reprod Domest Anim 47, 22–9.CrossRefGoogle ScholarPubMed
Moore, K, Rodríguez-Sallaberry, C, Kramer, J, Johnson, S, Wroclawska, E, Goicoa, S and Niasari-Naslaji, A (2007) In vitro production of bovine embryos in medium supplemented with a serum replacer: effects on blastocyst development, cryotolerance and survival to term. Theriogenology 68, 1316–25.CrossRefGoogle ScholarPubMed
Mugnier, S, Kervella, M, Douet, C, Canepa, S, Pascal, G, Deleuze, S, Duchamp, G, Monget, P and Goudet, G (2009) The secretions of oviduct epithelial cells increase the equine in vitro fertilization rate: are osteopontin, atrial natriuretic peptide A and oviductin involved? Reprod Biol Endocrinol 7, 129.CrossRefGoogle ScholarPubMed
Pontes, J, Nonato-Junior, I, Sanches, B, Ereno-Junior, J, Uvo, S, Barreiros, T, Oliveira, J, Hasler, J and Seneda, M (2009) Comparison of embryo yield and pregnancy rate between in vivo and in vitro methods in the same Nelore (Bos indicus) donor cows. Theriogenology 71, 690–7.CrossRefGoogle ScholarPubMed
R Core Team (2017) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria.Google Scholar
Rizos, D, Ward, F, Boland, M and Lonergan, P (2001) Effect of culture system on the yield and quality of bovine blastocysts as assessed by survival after vitrification. Theriogenology 56, 1–16.CrossRefGoogle ScholarPubMed
Rizos, D, Ward, F, Duffy, P, Boland, MP and 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. Mol Reprod Dev 61, 234–48.CrossRefGoogle ScholarPubMed
Rizos, D, Clemente, M, Bermejo‐Alvarez, P, de La Fuente, J, Lonergan, P and Gutiérrez‐Adán, A (2008) Consequences of in vitro culture conditions on embryo development and quality. Reprod Domest Anim 43, 44–50.CrossRefGoogle ScholarPubMed
Rodriguez-Martinez, H (2007) Role of the oviduct in sperm capacitation. Theriogenology 68, S138–46.CrossRefGoogle ScholarPubMed
Schmaltz-Panneau, B, Cordova, A, Dhorne-Pollet, S, Hennequet-Antier, C, Uzbekova, S, Martinot, E, Doret, S, Martin, P, Mermillod, P and Locatelli, Y (2014) Early bovine embryos regulate oviduct epithelial cell gene expression during in vitro co-culture. Anim Reprod Sci 149, 103–16.CrossRefGoogle ScholarPubMed
Stallock, J, Molyneaux, K, Schaible, K, Knudson, CM and Wylie, C (2003) The pro-apoptotic gene Bax is required for the death of ectopic primordial germ cells during their migration in the mouse embryo. Development 130, 6589–97.CrossRefGoogle ScholarPubMed
Steinhauer, N, Boos, A and 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, 110–9.CrossRefGoogle ScholarPubMed
Strachan, T and Read, A (2018) Human Molecular Genetics, 5th edition. Taylor, Francis Group, Bosa Roca, USA: Garland Science.CrossRefGoogle Scholar
Tanghe, S, Van Soom, A, Nauwynck, H, Coryn, M and de Kruif, A (2002) Minireview: Functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev 61, 414–24.CrossRefGoogle ScholarPubMed
Thouas, G, Korfiatis, N, French, A, Jones, G and Trounson, A (2001) Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod Biomed Online 3, 25–9.CrossRefGoogle ScholarPubMed
Way, A, Schuler, A and Killian, G (1997) Influence of bovine ampullary and isthmic oviductal fluid on sperm–egg binding and fertilization in vitro . J Reprod Fertil 109, 95–101.CrossRefGoogle ScholarPubMed