A combination of bovine serum albumin with insulin–transferrin–sodium selenite and/or epidermal growth factor as alternatives to fetal bovine serum in culture medium improves bovine embryo quality and trophoblast invasion by induction of matrix metalloproteinases
Ayman Mesalam A B , Kyeong-Lim Lee A , Imran Khan A C , M. M. R. Chowdhury A , Shimin Zhang A , Seok-Hwan Song A , Myeong-Don Joo A , Jae-Hoon Lee D , Jong-In Jin A E and Il-Keun Kong
A E F
+ Author Affiliations
- Author Affiliations
A Department of Animal Science, Division of Applied Life Science (BK21 Plus), Gyeongsang National University, Jinju 52828, Gyeongnam Province, Republic of Korea.
B Department of Theriogenology, Faculty of Veterinary Medicine, Zagazig University, Zagazig, 44519, Egypt.
C Department of Chemistry, Bacha Khan University, Charsadda, Khyber Pakhtunkhwa, 24420, Pakistan.
D Department of Veterinary Science, College of Veterinary Science, Gyeongsang National University, Jinju 52828, Gyeongnam Province, Republic of Korea.
E Institute of Agriculture and Life Science, Gyeongsang National University, Jinju 52828, Gyeongnam Province, Republic of Korea.
F Corresponding author. Email: ikong7900@gmail.com
Reproduction, Fertility and Development 31(2) 333-346 https://doi.org/10.1071/RD18162
Submitted: 30 November 2017 Accepted: 7 July 2018 Published: 8 August 2018
Abstract
This study investigated the use of bovine serum albumin (BSA) plus insulin–transferrin–sodium selenite (ITS) and/or epidermal growth factor (EGF) as alternatives to fetal bovine serum (FBS) in embryo culture medium. The developmental ability and quality of bovine embryos were determined by assessing their cell number, lipid content, gene expression and cryotolerance, as well as the invasion ability of trophoblasts. The percentage of embryos that underwent cleavage and formed a blastocyst was higher (P < 0.01) in medium containing ITS plus EGF and BSA than in medium containing FBS. Culture with ITS plus EGF and BSA also increased the hatching ability of blastocysts and the total cell number per blastocyst. Furthermore, the beneficial effects of BAS plus ITS and EGF on embryos were associated with a significantly reduced intracellular lipid content, which increased their cryotolerance. An invasion assay confirmed that culture with ITS plus EGF and BSA significantly improved the invasion ability of trophoblasts. Real-time quantitative polymerase chain reaction analysis showed that the mRNA levels of matrix metalloproteinase-2 (MMP2) and MMP9, acyl-CoA synthetase long-chain family member 3, acyl-coenzyme A dehydrogenase long-chain and hydroxymethylglutaryl-CoA reductase significantly increased upon culture with ITS plus EGF and BSA. Moreover, protein expression levels of matrix metalloproteinase-2 and -9 increased (P < 0.01) in medium supplemented with ITS plus EGF and BSA compared with medium supplemented with FBS. Taken together, these data suggest that supplementation of medium with ITS plus EGF and BSA improves in vitro bovine embryo production, cryotolerance and invasion ability of trophoblasts.
Additional keywords : cryotolerance, EGF, embryo culture, invasion ability, ITS, MMP2, MMP9.
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.| Accumulation of cytoplasmic lipid droplets in bovine embryos and cryotolerance of embryos developed in different culture systems using serum-free or serum-containing media.Crossref | GoogleScholarGoogle Scholar |
Antelman, J., Manandhar, G., Yi, Y. J., Li, R., Whitworth, K. M., Sutovsky, M., Agca, C., Prather, R. S., and Sutovsky, P. (2008). Expression of mitochondrial transcription factor A (TFAM) during porcine gametogenesis and preimplantation embryo development. J. Cell. Physiol. 217, 529–543.
| Expression of mitochondrial transcription factor A (TFAM) during porcine gametogenesis and preimplantation embryo development.Crossref | GoogleScholarGoogle Scholar |
Bavister, B. D. (1995). Culture of preimplantation embryos: facts and artifacts. Hum. Reprod. Update 1, 91–148.
| Culture of preimplantation embryos: facts and artifacts.Crossref | GoogleScholarGoogle Scholar |
Bernhard, E. J., Gruber, S. B., and Muschel, R. J. (1994). Direct evidence linking expression of matrix metalloproteinase 9 (92-kDa gelatinase/collagenase) to the metastatic phenotype in transformed rat embryo cells. Proc. Natl. Acad. Sci. USA 91, 4293–4297.
| Direct evidence linking expression of matrix metalloproteinase 9 (92-kDa gelatinase/collagenase) to the metastatic phenotype in transformed rat embryo cells.Crossref | GoogleScholarGoogle Scholar |
Bischof, P., Meisser, A., and Campana, A. (2000). Paracrine and autocrine regulators of trophoblast invasion – a review. Placenta 21, S55–60.
Brown, M. S., and Goldstein, J. L. (1990). Atherosclerosis. Scavenging for receptors. Nature 343, 508–509.
| Atherosclerosis. Scavenging for receptors.Crossref | GoogleScholarGoogle Scholar |
Chaddha, V., Viero, S., Huppertz, B., and Kingdom, J. (2004). Developmental biology of the placenta and the origins of placental insufficiency. Semin. Fetal Neonatal Med. 9, 357–369.
| Developmental biology of the placenta and the origins of placental insufficiency.Crossref | GoogleScholarGoogle Scholar |
Chang, W. L., Yang, Q., Zhang, H., Lin, H. Y., Zhou, Z., Lu, X., Zhu, C., Xue, L. Q., and Wang, H. (2014). Role of placenta-specific protein 1 in trophoblast invasion and migration. Reproduction 148, 343–352.
| Role of placenta-specific protein 1 in trophoblast invasion and migration.Crossref | GoogleScholarGoogle Scholar |
Chappel, S. (2013). The role of mitochondria from mature oocyte to viable blastocyst. Obstet. Gynecol. Int. 2013, 183024.
| The role of mitochondria from mature oocyte to viable blastocyst.Crossref | GoogleScholarGoogle Scholar |
Chia, C. M., Winston, R. M., and Handyside, A. H. (1995). EGF, TGF-alpha and EGFR expression in human preimplantation embryos. Development 121, 299–307.
Comiskey, M., and Warner, C. M. (2007). Spatio-temporal localization of membrane lipid rafts in mouse oocytes and cleaving preimplantation embryos. Dev. Biol. 303, 727–739.
| Spatio-temporal localization of membrane lipid rafts in mouse oocytes and cleaving preimplantation embryos.Crossref | GoogleScholarGoogle Scholar |
Cordova, B., Morato, R., Izquierdo, D., Paramio, T., and Mogas, T. (2010). Effect of the addition of insulin-transferrin-selenium and/or L-ascorbic acid to the in vitro maturation of prepubertal bovine oocytes on cytoplasmic maturation and embryo development. Theriogenology 74, 1341–1348.
| Effect of the addition of insulin-transferrin-selenium and/or L-ascorbic acid to the in vitro maturation of prepubertal bovine oocytes on cytoplasmic maturation and embryo development.Crossref | GoogleScholarGoogle Scholar |
Das, Z. C., Gupta, M. K., Uhm, S. J., and Lee, H. T. (2014). Supplementation of insulin-transferrin-selenium to embryo culture medium improves the in vitro development of pig embryos. Zygote 22, 411–418.
| Supplementation of insulin-transferrin-selenium to embryo culture medium improves the in vitro development of pig embryos.Crossref | GoogleScholarGoogle Scholar |
Dhali, A., Anchamparuthy, V. M., Butler, S. P., Mullarky, I. K., Pearson, R. E., and Gwazdauskas, F. C. (2011). Development and quality of bovine embryos produced in vitro using growth factor supplemented serum-free system. Open J. Anim. Sci. 1, 97–105.
| Development and quality of bovine embryos produced in vitro using growth factor supplemented serum-free system.Crossref | GoogleScholarGoogle Scholar |
Dilly, M., Hambruch, N., Haeger, J. D., and Pfarrer, C. (2010). Epidermal growth factor (EGF) induces motility and upregulates MMP-9 and TIMP-1 in bovine trophoblast cells. Mol. Reprod. Dev. 77, 622–629.
| Epidermal growth factor (EGF) induces motility and upregulates MMP-9 and TIMP-1 in bovine trophoblast cells.Crossref | GoogleScholarGoogle Scholar |
Dunning, K. R., Cashman, K., Russell, D. L., Thompson, J. G., Norman, R. J., and Robker, R. L. (2010). Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Biol. Reprod. 83, 909–918.
| Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development.Crossref | GoogleScholarGoogle Scholar |
Dunning, K. R., Anastasi, M. R., Zhang, V. J., Russell, D. L., and Robker, R. L. (2014). Regulation of fatty acid oxidation in mouse cumulus-oocyte complexes during maturation and modulation by PPAR agonists. PLoS One 9, e87327.
| Regulation of fatty acid oxidation in mouse cumulus-oocyte complexes during maturation and modulation by PPAR agonists.Crossref | GoogleScholarGoogle Scholar |
Fernandez-Gonzalez, R., Moreira, P., Bilbao, A., Jimenez, A., Perez-Crespo, M., Ramirez, M. A., Rodriguez De Fonseca, F., Pintado, B., and Gutierrez-Adan, A. (2004). Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior. Proc. Natl. Acad. Sci. USA 101, 5880–5885.
| Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior.Crossref | GoogleScholarGoogle Scholar |
Gao, F., Wei, P., Chen, X., Zhang, Z., and Liu, Y. (2002). Relationship between uterine expression of matrix metalloproteinases and their inhibitors and endometrial receptivity. Sci. China C Life Sci. 45, 406–411.
| Relationship between uterine expression of matrix metalloproteinases and their inhibitors and endometrial receptivity.Crossref | GoogleScholarGoogle Scholar |
George, F., Daniaux, C., Genicot, G., Verhaeghe, B., Lambert, P., and Donnay, I. (2008). Set up of a serum-free culture system for bovine embryos: embryo development and quality before and after transient transfer. Theriogenology 69, 612–623.
| Set up of a serum-free culture system for bovine embryos: embryo development and quality before and after transient transfer.Crossref | GoogleScholarGoogle Scholar |
Goovaerts, I. G., Leroy, J. L., Langbeen, A., Jorssen, E. P., Bosmans, E., and Bols, P. E. (2012). Unravelling the needs of singly in vitro-produced bovine embryos: from cumulus cell co-culture to semi-defined, oil-free culture conditions. Reprod. Fertil. Dev. 24, 1084–1092.
| Unravelling the needs of singly in vitro-produced bovine embryos: from cumulus cell co-culture to semi-defined, oil-free culture conditions.Crossref | GoogleScholarGoogle Scholar |
Hale, N. A., Yang, Y., and Rajagopalan, P. (2010). Cell migration at the interface of a dual chemical-mechanical gradient. ACS Appl. Mater. Interfaces 2, 2317–2324.
| Cell migration at the interface of a dual chemical-mechanical gradient.Crossref | GoogleScholarGoogle Scholar |
Herrler, A., Krusche, C. A., and Beier, H. M. (1998). Insulin and insulin-like growth factor-I promote rabbit blastocyst development and prevent apoptosis. Biol. Reprod. 59, 1302–1310.
| Insulin and insulin-like growth factor-I promote rabbit blastocyst development and prevent apoptosis.Crossref | GoogleScholarGoogle Scholar |
Holley, A. K., Dhar, S. K., and St Clair, D. K. (2010). Manganese superoxide dismutase vs. p53: regulation of mitochondrial ROS. Mitochondrion 10, 649–661.
| Manganese superoxide dismutase vs. p53: regulation of mitochondrial ROS.Crossref | GoogleScholarGoogle Scholar |
Holm, P., Booth, P. J., and Callesen, H. (2002). Kinetics of early in vitro development of bovine in vivo- and in vitro-derived zygotes produced and/or cultured in chemically defined or serum-containing media. Reproduction 123, 553–565.
| Kinetics of early in vitro development of bovine in vivo- and in vitro-derived zygotes produced and/or cultured in chemically defined or serum-containing media.Crossref | GoogleScholarGoogle Scholar |
Isobe, T., Ikebata, Y., Do, L. T., Tanihara, F., Taniguchi, M., and Otoi, T. (2015). In vitro development of OPU-derived bovine embryos cultured either individually or in groups with the silk protein sericin and the viability of frozen–thawed embryos after transfer. Anim. Sci. J. 86, 661–665.
| In vitro development of OPU-derived bovine embryos cultured either individually or in groups with the silk protein sericin and the viability of frozen–thawed embryos after transfer.Crossref | GoogleScholarGoogle Scholar |
Johnson, D. C., and Chatterjee, S. (1993). Epidermal growth factor (EGF) replaces estradiol for the initiation of embryo implantation in the hypophysectomized rat. Placenta 14, 429–438.
| Epidermal growth factor (EGF) replaces estradiol for the initiation of embryo implantation in the hypophysectomized rat.Crossref | GoogleScholarGoogle Scholar |
Li, M., Yee, D., Magnuson, T. R., Smithies, O., and Caron, K. M. (2006). Reduced maternal expression of adrenomedullin disrupts fertility, placentation, and fetal growth in mice. J. Clin. Invest. 116, 2653–2662.
| Reduced maternal expression of adrenomedullin disrupts fertility, placentation, and fetal growth in mice.Crossref | GoogleScholarGoogle Scholar |
Mesalam, A., Khan, I., Lee, K. L., Song, S. H., Chowdhury, M. M. R., Uddin, Z., Park, K. H., and Kong, I. K. (2017a). 2-Methoxystypandrone improves in vitro-produced bovine embryo quality through inhibition of IKBKB. Theriogenology 99, 10–20.
| 2-Methoxystypandrone improves in vitro-produced bovine embryo quality through inhibition of IKBKB.Crossref | GoogleScholarGoogle Scholar |
Mesalam, A., Kong, R., Khan, I., Chowdhury, M., Choi, B. H., Kim, S. W., Cho, K. W., Jin, J. I., and Kong, I. K. (2017b). Effect of charcoal:dextran stripped fetal bovine serum on in vitro development of bovine embryos. Reprod. Biol. 17, 312–319.
| Effect of charcoal:dextran stripped fetal bovine serum on in vitro development of bovine embryos.Crossref | GoogleScholarGoogle Scholar |
Mihalik, J., Rehak, P., and Koppel, J. (2000). The influence of insulin on the in vitro development of mouse and bovine embryos. Physiol. Res. 49, 347–354.
Murakami, M., Dong, Y. J., Suzuki, T., Taniguchi, M., Kaedei, Y., Sato, Y., Tanihara, F., and Otoi, T. (2011). Development and subsequent cryotolerance of domestic cat embryos cultured in serum-free and serum-containing media. Cryobiology 63, 170–174.
| Development and subsequent cryotolerance of domestic cat embryos cultured in serum-free and serum-containing media.Crossref | GoogleScholarGoogle Scholar |
Nagashima, H., Kashiwazaki, N., Ashman, R. J., Grupen, C. G., Seamark, R. F., and Nottle, M. B. (1994). Removal of cytoplasmic lipid enhances the tolerance of porcine embryos to chilling. Biol. Reprod. 51, 618–622.
| Removal of cytoplasmic lipid enhances the tolerance of porcine embryos to chilling.Crossref | GoogleScholarGoogle Scholar |
Nakayama, T., Fujiwara, H., Maeda, M., Inoue, T., Yoshioka, S., Mori, T., and Fujii, S. (2002). Human peripheral blood mononuclear cells (PBMC) in early pregnancy promote embryo invasion in vitro: HCG enhances the effects of PBMC. Hum. Reprod. 17, 207–212.
| Human peripheral blood mononuclear cells (PBMC) in early pregnancy promote embryo invasion in vitro: HCG enhances the effects of PBMC.Crossref | GoogleScholarGoogle Scholar |
Ou, X., Lee, M. R., Huang, X., Messina-Graham, S., and Broxmeyer, H. E. (2014). SIRT1 positively regulates autophagy and mitochondria function in embryonic stem cells under oxidative stress. Stem Cells 32, 1183–1194.
| SIRT1 positively regulates autophagy and mitochondria function in embryonic stem cells under oxidative stress.Crossref | GoogleScholarGoogle Scholar |
Pennington, K. A., Schlitt, J. M., and Schulz, L. C. (2012). Isolation of primary mouse trophoblast cells and trophoblast invasion assay. J. Vis. Exp. 3202, .
| Isolation of primary mouse trophoblast cells and trophoblast invasion assay.Crossref | GoogleScholarGoogle Scholar |
Pratt, H. P. (1982). Preimplantation mouse embryos synthesize membrane sterols. Dev. Biol. 89, 101–110.
| Preimplantation mouse embryos synthesize membrane sterols.Crossref | GoogleScholarGoogle Scholar |
Ramalho-Santos, J., Varum, S., Amaral, S., Mota, P. C., Sousa, A. P., and Amaral, A. (2009). Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells. Hum. Reprod. Update 15, 553–572.
| Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells.Crossref | GoogleScholarGoogle Scholar |
Rauch, C., Feifel, E., Amann, E. M., Spotl, H. P., Schennach, H., Pfaller, W., and Gstraunthaler, G. (2011). Alternatives to the use of fetal bovine serum: human platelet lysates as a serum substitute in cell culture media. ALTEX 28, 305–316.
| Alternatives to the use of fetal bovine serum: human platelet lysates as a serum substitute in cell culture media.Crossref | GoogleScholarGoogle Scholar |
Ribeiro, M. L., Farina, M., Aisemberg, J., and Franchi, A. (2003). Effects of in vivo administration of epidermal growth factor (EGF) on uterine contractility, prostaglandin production and timing of parturition in rats. Reproduction 126, 459–468.
| Effects of in vivo administration of epidermal growth factor (EGF) on uterine contractility, prostaglandin production and timing of parturition in rats.Crossref | GoogleScholarGoogle Scholar |
Schulz, L. C., and Widmaier, E. P. (2004). The effect of leptin on mouse trophoblast cell invasion. Biol. Reprod. 71, 1963–1967.
| The effect of leptin on mouse trophoblast cell invasion.Crossref | GoogleScholarGoogle Scholar |
Seidel, G. E. (2006). Modifying oocytes and embryos to improve their cryopreservation. Theriogenology 65, 228–235.
| Modifying oocytes and embryos to improve their cryopreservation.Crossref | GoogleScholarGoogle Scholar |
Shahbazi, M. N., Jedrusik, A., Vuoristo, S., and Recher, G. (2016). Self-organization of the human embryo in the absence of maternal tissues. Nat. Cell Biol. 18, 700–708.
| Self-organization of the human embryo in the absence of maternal tissues.Crossref | GoogleScholarGoogle Scholar |
Sirisathien, S., Hernandez-Fonseca, H. J., and Brackett, B. G. (2003). Influences of epidermal growth factor and insulin-like growth factor-I on bovine blastocyst development in vitro. Anim. Reprod. Sci. 77, 21–32.
| Influences of epidermal growth factor and insulin-like growth factor-I on bovine blastocyst development in vitro.Crossref | GoogleScholarGoogle Scholar |
Smith, S. R., Ghosh, M. C., Ollivierre-Wilson, H., Hang Tong, W., and Rouault, T. A. (2006). Complete loss of iron regulatory proteins 1 and 2 prevents viability of murine zygotes beyond the blastocyst stage of embryonic development. Blood Cells Mol. Dis. 36, 283–287.
| Complete loss of iron regulatory proteins 1 and 2 prevents viability of murine zygotes beyond the blastocyst stage of embryonic development.Crossref | GoogleScholarGoogle Scholar |
Stetler-Stevenson, W. G., Liotta, L. A., and Kleiner, D. E. (1993). Extracellular matrix 6: role of matrix metalloproteinases in tumor invasion and metastasis. FASEB J. 7, 1434–1441.
| Extracellular matrix 6: role of matrix metalloproteinases in tumor invasion and metastasis.Crossref | GoogleScholarGoogle Scholar |
Sudano, M. J., Paschoal, D. M., Rascado Tda, S., Magalhaes, L. C., Crocomo, L. F., de Lima-Neto, J. F., and Landim-Alvarenga Fda, C. (2011). Lipid content and apoptosis of in vitro-produced bovine embryos as determinants of susceptibility to vitrification. Theriogenology 75, 1211–1220.
| Lipid content and apoptosis of in vitro-produced bovine embryos as determinants of susceptibility to vitrification.Crossref | GoogleScholarGoogle Scholar |
Van Soom, A., Vandaele, L., Goossens, K., de Kruif, A., and Peelman, L. (2007). Gamete origin in relation to early embryo development. Theriogenology 68, S131–S137.
| Gamete origin in relation to early embryo development.Crossref | GoogleScholarGoogle Scholar |
van Wagtendonk-de Leeuw, A. M., Mullaart, E., de Roos, A. P., Merton, J. S., den Daas, J. H., Kemp, B., and de Ruigh, L. (2000). Effects of different reproduction techniques: AI MOET or IVP, on health and welfare of bovine offspring. Theriogenology 53, 575–597.
| Effects of different reproduction techniques: AI MOET or IVP, on health and welfare of bovine offspring.Crossref | GoogleScholarGoogle Scholar |
Wang, C., Niu, Y., Chi, D., Zeng, Y., Liu, H., Dai, Y., and Li, J. (2015). Influence of delipation on the energy metabolism in pig parthenogenetically activated embryos. Reprod. Domest. Anim. 50, 826–833.
| Influence of delipation on the energy metabolism in pig parthenogenetically activated embryos.Crossref | GoogleScholarGoogle Scholar |
Weathers, J. D., and Prien, S. D. (2014). Estimation of weight and lipid composition in preimplantation embryos from Jersey and beef breeds of cattle. Open Journal of Veterinary Medicine 4, 51301.
| Estimation of weight and lipid composition in preimplantation embryos from Jersey and beef breeds of cattle.Crossref | GoogleScholarGoogle Scholar |
Wei, Z., Park, K. W., Day, B. N., and Prather, R. S. (2001). Effect of epidermal growth factor on preimplantation development and its receptor expression in porcine embryos. Mol. Reprod. Dev. 60, 457–462.
| Effect of epidermal growth factor on preimplantation development and its receptor expression in porcine embryos.Crossref | GoogleScholarGoogle Scholar |
Wilding, M., Coppola, G., Dale, B., and Di Matteo, L. (2009). Mitochondria and human preimplantation embryo development. Reproduction 137, 619–624.
| Mitochondria and human preimplantation embryo development.Crossref | GoogleScholarGoogle Scholar |
Wydooghe, E., Vandaele, L., Beek, J., Favoreel, H., Heindryckx, B., De Sutter, P., and Van Soom, A. (2011). Differential apoptotic staining of mammalian blastocysts based on double immunofluorescent CDX2 and active caspase-3 staining. Anal. Biochem. 416, 228–230.
| Differential apoptotic staining of mammalian blastocysts based on double immunofluorescent CDX2 and active caspase-3 staining.Crossref | GoogleScholarGoogle 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, 717–724.
| Replacing serum in culture medium with albumin and insulin, transferrin and selenium is the key to successful bovine embryo development in individual culture.Crossref | GoogleScholarGoogle Scholar |
Yang, Y. P., Ma, H., Starchenko, A., Huh, W. J., Li, W., Hickman, F. E., Zhang, Q., Franklin, J. L., Mortlock, D. P., Fuhrmann, S., Carter, B. D., Ihrie, R. A., and Coffey, R. J. (2017). A chimeric Egfr protein reporter mouse reveals Egfr localization and trafficking in vivo. Cell Reports 19, 1257–1267.
| A chimeric Egfr protein reporter mouse reveals Egfr localization and trafficking in vivo.Crossref | GoogleScholarGoogle Scholar |
Yu, Y., Ding, C., Wang, E., Chen, X., Li, X., Zhao, C., Fan, Y., Wang, L., Beaujean, N., Zhou, Q., Jouneau, A., and Ji, W. (2007). Piezo-assisted nuclear transfer affects cloning efficiency and may cause apoptosis. Reproduction 133, 947–954.
| Piezo-assisted nuclear transfer affects cloning efficiency and may cause apoptosis.Crossref | GoogleScholarGoogle Scholar |
Yuan, Y., Ida, J. M., Paczkowski, M., and Krisher, R. L. (2011). Identification of developmental competence-related genes in mature porcine oocytes. Mol. Reprod. Dev. 78, 565–575.
| Identification of developmental competence-related genes in mature porcine oocytes.Crossref | GoogleScholarGoogle Scholar |
Zhao, X. M., Hao, H. S., Du, W. H., Zhao, S. J., Wang, H. Y., Wang, N., Wang, D., Liu, Y., Qin, T., and Zhu, H. B. (2016). Melatonin inhibits apoptosis and improves the developmental potential of vitrified bovine oocytes. J. Pineal Res. 60, 132–141.
| Melatonin inhibits apoptosis and improves the developmental potential of vitrified bovine oocytes.Crossref | GoogleScholarGoogle Scholar |
