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Embryo co-culture with bovine amniotic membrane stem cells can enhance the cryo-survival of IVF-derived bovine blastocysts comparable with co-culture with bovine oviduct epithelial cells

Published online by Cambridge University Press:  20 October 2020

Shayan Nejat-Dehkordi ,
Ebrahim Ahmadi Open the ORCID record for Ebrahim Ahmadi [Opens in a new window] ,
Abolfazl Shirazi ,
Hassan Nazari  and
Naser Shams-Esfandabadi
Shayan Nejat-Dehkordi
Affiliation:
Department of Clinical Sciences, Faculty of Veterinary Medicine, Shahrekord University, Shahrekord, Iran
Ebrahim Ahmadi
Affiliation:
Research Institute of Animal Embryo Technology, Shahrekord University, Shahrekord, Iran
Abolfazl Shirazi*
Affiliation:
Department of Clinical Sciences, Faculty of Veterinary Medicine, Shahrekord University, Shahrekord, Iran Research Institute of Animal Embryo Technology, Shahrekord University, Shahrekord, Iran Reproductive Biotechnology Research Center, Avicenna Research Institute, ACECR, Tehran, Iran
Hassan Nazari
Affiliation:
Research Institute of Animal Embryo Technology, Shahrekord University, Shahrekord, Iran
Naser Shams-Esfandabadi
Affiliation:
Department of Clinical Sciences, Faculty of Veterinary Medicine, Shahrekord University, Shahrekord, Iran
*
Author for correspondence: Abolfazl Shirazi, Reproductive Biotechnology Research Center, Avicenna Research Institute, ACECR, Tehran, Iran and Research Institute of Animal Embryo Technology, Shahrekord University, Shahrekord, Iran. Tel: +98 21 2404144. Fax: +98 21 22404145. E-mail: [email protected]
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Summary

Culture conditions have a profound effect on the quality of in vitro-produced embryos. Co-culturing embryos with somatic cells has some beneficial effects on embryonic development. Considering the ability of stem cells to secrete a broad range of growth factors with different biological activities, we hypothesized that bovine amniotic membrane stem cells (bAMSCs) might be superior to bovine oviduct epithelial cells (BOECs) in supporting embryonic development and enhancing their cryo-survival. Bovine abattoir-derived oocytes were matured and fertilized in vitro. The resultant presumptive zygotes were then cultured up to the blastocyst stage in the following groups: (i) co-culture with bAMSCs, (ii) co-culture with BOECs, and (iii) cell-free culture (Con). Embryos that reached the blastocyst stage were vitrified and warmed, and their post-warming re-expansion, survival and hatching rates were evaluated after 72 h culture. Results showed that the cleavage, blastocyst, and 2 h post-warming re-expansion rates of embryos did not differ between groups. However, their survival rates in BOEC and bAMSC groups were significantly higher compared with the control (72.7, 75.6 and 37.5%, respectively, P < 0.05). In conclusion, our results showed that the cryo-survivability of IVF-derived bovine embryos could be improved through co-culturing with bAMSCs. Moreover, considering the possibility to provide multiple passages from bAMSCs compared with BOECs, due to their stemness properties and their ability to produce growth factors, the use of bAMSCs is a good alternative to BOECs in embryo co-culture systems.

Keywords

Adult stem cellsCulture systemEmbryo qualityFreezabilityVitrification
Type
Research Article
Information
Zygote , Volume 29 , Issue 2 , April 2021 , pp. 102 - 107
Copyright
© The Author(s), 2020. Published by Cambridge University Press

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References

Abe, H, Yamashita, S, Satoh, T and Hoshi, H (2002). Accumulation of cytoplasmic lipid droplets in bovine embryos and cryotolerance of embryos developed in different culture systems using serum-free or serum-containing media. Mol Reprod Dev 61, 57–66.CrossRefGoogle ScholarPubMed
Ascari, IJ, Martins, SC, Camargo, LSA, Mendez-Otero, R and Jasmin, J (2018). Development of bovine embryos in vitro in coculture with murine mesenchymal stem cells and embryonic fibroblasts. Mol Biol Rep 45, 1827–37CrossRefGoogle ScholarPubMed
Blazquez, R, Sanchez-Margallo, FM, Alvarez, V, Matilla, E, Hernandez, N, Marinaro, F, Gomez-Serrano, M, Jorge, I, Casado, JG and Macias-Garcia, B (2018). Murine embryos exposed to human endometrial MSCs-derived extracellular vesicles exhibit higher VEGF/PDGF AA release, increased blastomere count and hatching rates. PLoS One 13, e0196080.CrossRefGoogle ScholarPubMed
Dobrinsky, JR (2002). Advancements in cryopreservation of domestic animal embryos. Theriogenology 57, 285–302.CrossRefGoogle ScholarPubMed
Edwards, LJ, Batt, PA, Gandolfi, F and Gardner, DK (1997). Modifications made to culture medium by bovine oviduct epithelial cells: changes to carbohydrates stimulate bovine embryo development. Mol Reprod Dev 46, 146–54.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Gandolfi, F (1995). Functions of proteins secreted by oviduct epithelial cells. Microsc Res Tech 32, 1–12.CrossRefGoogle ScholarPubMed
Gandolfi, F and Moor, R (1987). Stimulation of early embryonic development in the sheep by co-culture with oviduct epithelial cells. J Reprod Infertil 81, 23–8.CrossRefGoogle ScholarPubMed
Gómez, E, Rodríguez, A, Muñoz, M, Caamaño, JN, Hidalgo, CO, Morán, E, Facal, N and Díez, C (2008). Serum free embryo culture medium improves in vitro survival of bovine blastocysts to vitrification. Theriogenology 69, 1013–21.CrossRefGoogle ScholarPubMed
Greve, T, Avery, B and Callesen, H (1993). Viability of in-vivo and in-vitro produced bovine embryos. Reprod Domest Anim 28, 164–9.CrossRefGoogle Scholar
Hardy, K and Spanos, S (2002). Growth factor expression and function in the human and mouse preimplantation embryo. J Endocrinol 172, 221–36.CrossRefGoogle ScholarPubMed
Harvey, MB, Arcellana-Panlilio, MY, Zhang, X, Schultz, GA and Watson, AJ (1995). Expression of genes encoding antioxidant enzymes in preimplantation mouse and cow embryos and primary bovine oviduct cultures employed for embryo coculture. Biol Reprod 53, 532–40.CrossRefGoogle ScholarPubMed
Jasmin, J, Peters, VM, Spray, DC and Mendez-Otero, R (2016). Effect of mesenchymal stem cells and mouse embryonic fibroblasts on the development of preimplantation mouse embryos. In Vitro Cell Dev Biol Anim 52, 497–506.CrossRefGoogle ScholarPubMed
Kim, EY, Lee, JB, Park, HY, Jeong, CJ, Riu, KZ and Park, SP (2011). The use of embryonic stem cell derived bioactive material as a new protein supplement for the in vitro culture of bovine embryos. J Reprod Dev 57, 346–54.CrossRefGoogle ScholarPubMed
Lange-Consiglio, A, Maggio, V, Pellegrino, L and Cremonesi, F (2012). Equine bone marrow mesenchymal or amniotic epithelial stem cells as feeder in a model for the in vitro culture of bovine embryos. Zygote 20, 45–51.CrossRefGoogle ScholarPubMed
Lee, SE, Moon, JJ, Kim, EY and Park, SP (2015). Stem cell-derived bioactive materials accelerate development of porcine in vitro-fertilized embryos. Cell Reprogram 17, 181–90.CrossRefGoogle ScholarPubMed
Leibo, SP and Loskutoff, NM (1993). Cryobiology of in vitro-derived bovine embryos. Theriogenology 39, 81–94.CrossRefGoogle Scholar
Lonergan, P, Rizos, D, Gutierrez-Adan, A, Fair, T and Boland, M (2003). Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns. Reprod Domest Anim 38, 259–67.CrossRefGoogle ScholarPubMed
Lopera-Vasquez, R, Hamdi, M, Fernandez-Fuertes, B, Maillo, V, Beltran-Brena, P, Calle, A, Redruello, A, Lopez-Martin, S, Gutierrez-Adan, A, Yanez-Mo, M, Ramirez, MA and Rizos, D (2016). Extracellular vesicles from BOEC in in vitro embryo development and quality. PLoS One 11, e0148083.CrossRefGoogle ScholarPubMed
Madrigal, M, Rao, KS and Riordan, NH (2014). A review of therapeutic effects of mesenchymal stem cell secretions and induction of secretory modification by different culture methods. J Transl Med 12, 260.CrossRefGoogle ScholarPubMed
Mandawala, AA, Harvey, SC, Roy, TK and Fowler, KE (2016). Cryopreservation of animal oocytes and embryos: current progress and future prospects. Theriogenology 86, 1637–44.CrossRefGoogle ScholarPubMed
Mantikou, E, Youssef, MAFM, van Wely, M, van der Veen, F, Al-Inany, HG, Repping, S and Mastenbroek, S (2013). Embryo culture media and IVF/ICSI success rates: a systematic review. Hum Reprod Update 19, 210–20.CrossRefGoogle ScholarPubMed
Massip, A and Leibo, S (2002). Factors influencing cryopreservation of domestic animal embryos. In Assessment of Mammalian Embryo Quality (eds Van Soom, A and Boerjan, M). Springer, pp. 121–38.CrossRefGoogle Scholar
Miranda, MS, Nascimento, HS, Costa, MP, Costa, NN, Brito, KN, Lopes, CT, Santos, SS, Cordeiro, MS and Ohashi, OM (2016). Increasing of blastocyst rate and gene expression in co-culture of bovine embryos with adult adipose tissue-derived mesenchymal stem cells. J Assist Reprod Genet 33, 1395–403.CrossRefGoogle ScholarPubMed
Moshkdanian, G, Nematollahi-Mahani, SN, Pouya, F and Nematollahi-Mahani, A (2011). Antioxidants rescue stressed embryos at a rate comparable with co-culturing of embryos with human umbilical cord mesenchymal cells. J Assist Reprod Genet 28, 343–9.CrossRefGoogle Scholar
Mucci, N, Aller, J, Kaiser, GG, Hozbor, F, Cabodevila, J and Alberio, RH (2006). Effect of estrous cow serum during bovine embryo culture on blastocyst development and cryotolerance after slow freezing or vitrification. Theriogenology 65, 1551–62.CrossRefGoogle ScholarPubMed
Nazari, H, Shirazi, A, Shams-Esfandabadi, N, Afzali, A and Ahmadi, E (2016). The effect of amniotic membrane stem cells as donor nucleus on gene expression in reconstructed bovine oocytes. Int J Dev Biol 60, 95–102.CrossRefGoogle ScholarPubMed
Park, HY, Kim, EY, Lee, SE, Choi, HY, Moon, JJ, Park, MJ, Son, YJ, Lee, JB, Jeong, CJ, Lee, DS, Riu, KJ and Park, SP (2013). Effect of human adipose tissue-derived mesenchymal-stem-cell bioactive materials on porcine embryo development. Mol Reprod Dev 80, 1035–47.CrossRefGoogle ScholarPubMed
Rizos, D, Gutierrez-Adan, A, Perez-Garnelo, S, De La Fuente, J, Boland, MP and Lonergan, P (2003). Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance, and messenger RNA expression. Biol Reprod 68, 236–43.CrossRefGoogle ScholarPubMed
Rizos, D, Ward, F, Boland, MP 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
Rodrigues-Cunha, MC, Mesquita, LG, Bressan, F, del Collado, M, Balieiro, JC, Schwarz, KR, de Castro, FC, Watanabe, OY, Watanabe, YF and de Alencar Coelho, L (2016). Effects of melatonin during IVM in defined medium on oocyte meiosis, oxidative stress, and subsequent embryo development. Theriogenology 86, 1685–94.CrossRefGoogle ScholarPubMed
Saragusty, J and Arav, A (2011). Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification. Reproduction 141, 1–19.CrossRefGoogle ScholarPubMed
Schmaltz-Panneau, B, Locatelli, Y, Uzbekova, S, Perreau, C and Mermillod, P (2015). Bovine oviduct epithelial cells dedifferentiate partly in culture, while maintaining their ability to improve early embryo development rate and quality. Reprod Domest Anim 50, 719–29.CrossRefGoogle ScholarPubMed
Shirazi, A, Nazari, H, Ahmadi, E, Heidari, B and Shams-Esfandabadi, N (2009). Effect of culture system on survival rate of vitrified bovine embryos produced in vitro . Cryobiology 59, 285–90.CrossRefGoogle ScholarPubMed
Shirazi, A, Soleimani, M, Karimi, M, Nazari, H, Ahmadi, E and Heidari, B (2010). Vitrification of in vitro produced ovine embryos at various developmental stages using two methods. Cryobiology 60, 204–10.CrossRefGoogle ScholarPubMed
Van der Elst, J (2002). Embryo quality and freezing tolerance: cryopreservation of human embryos. In Assessment of Mammalian Embryo Quality (eds Van Soom, A and Boerjan, M). Springer, pp. 95–120.CrossRefGoogle Scholar
Wydooghe, E, Heras, S, Dewulf, J, Piepers, S, Van den Abbeel, E, De Sutter, P, Vandaele, L and Van Soom, A (2014). Replacing serum in culture medium with albumin and insulin, transferrin and selenium is the key to successful bovine embryo development in individual culture. Reprod Fertil Dev 26, 717–24.CrossRefGoogle ScholarPubMed
Yoshioka, K (2011). Development and application of a chemically defined medium for the in vitro production of porcine embryos. J Reprod Dev 57, 9–16.CrossRefGoogle ScholarPubMed
Young, LE, Sinclair, KD and Wilmut, I (1998). Large offspring syndrome in cattle and sheep. Rev Reprod 3, 155–63.CrossRefGoogle ScholarPubMed