Cytokine supplemented maturation medium improved development to term following somatic cell nuclear transfer (SCNT) in cattle
Jacob Keim A , Ying Liu A * , Misha Regouski A , Rusty Stott A , Galina N. Singina B , Kenneth L. White A and Irina A. Polejaeva A *A Department of Animal, Dairy and Veterinary Sciences, Utah State University, Logan, UT, USA.
B L. K. Ernst Federal Research Center for Animal Husbandry, Podolsk, Russia.
Reproduction, Fertility and Development 35(11) 575-588 https://doi.org/10.1071/RD23011
Published online: 13 June 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: In vitro maturation is an important process in the production of embryos. It has been shown that three cytokines, fibroblast growth factor 2, leukemia inhibitory factor and insulin-like growth factor 1 (FLI), increased efficiency of in vitro maturation, somatic cell nuclear transfer (SCNT) blastocyst production, and in vivo development of genetically engineered piglets.
Aims: Assess effects of FLI on oocyte maturation, quality of oocytes, and embryo development in bovine in vitro fertilisation (IVF) and SCNT.
Key results: Cytokine supplementation resulted in significant increases in maturation rates and decreased levels of reactive oxygen species. Oocytes matured in FLI had increased blastocyst rates when used in IVF (35.6% vs 27.3%, P < 0.05) and SCNT (40.6% vs 25.7%, P < 0.05). SCNT blastocysts contained significantly more inner cell mass and trophectodermal cells when compared to the control group. Importantly, SCNT embryos derived from oocytes matured in FLI medium resulted in a four-fold increase in full-term development compared to control medium (23.3% vs 5.3%, P < 0.05). Relative mRNA expression analysis of 37 genes associated with embryonic and fetal development revealed one gene had differential transcript abundance in metaphase II oocytes, nine genes at the 8-cell stage, 10 genes at the blastocyst stage in IVF embryos and four genes at the blastocyst stage in SCNT embryos.
Conclusions: Cytokine supplementation increased efficiency of in vitro production of IVF and SCNT embryos and in vivo development of SCNT embryos to term.
Implications: Cytokine supplementation is beneficial to embryo culture systems, which may shed light on requirements of early embryo development.
Keywords: cytokines, embryo development, gene expression, in vitro fertilisation, oocyte maturation, oocyte quality, somatic cell nuclear transfer.
References
Abazarikia, A, Zhandi, M, Towhidi, A, Shakeri, M, Yousefi, AR, and Aliyan, A (2021). Conjugated linoleic acid improves meiotic spindle morphology and developmental competence of heat-stressed bovine oocyte. Theriogenology 172, 67–72.| Conjugated linoleic acid improves meiotic spindle morphology and developmental competence of heat-stressed bovine oocyte.Crossref | GoogleScholarGoogle Scholar |
Akizawa, H, Nagatomo, H, Odagiri, H, Kohri, N, Yamauchi, N, Yanagawa, Y, Nagano, M, Takahashi, M, and Kawahara, M (2016). Conserved roles of fibroblast growth factor receptor 2 signaling in the regulation of inner cell mass development in bovine blastocysts. Molecular Reproduction and Development 83, 516–525.
| Conserved roles of fibroblast growth factor receptor 2 signaling in the regulation of inner cell mass development in bovine blastocysts.Crossref | GoogleScholarGoogle Scholar |
Anderson, JE, Matteri, RL, Abeydeera, LR, Day, BN, and Prather, RS (1999). Cyclin B1 transcript quantitation over the maternal to zygotic transition in both in vivo- and in vitro-derived 4-cell porcine embryos. Biology of Reproduction 61, 1460–1467.
| Cyclin B1 transcript quantitation over the maternal to zygotic transition in both in vivo- and in vitro-derived 4-cell porcine embryos.Crossref | GoogleScholarGoogle Scholar |
Auclair, S, Uzbekov, R, Elis, S, Sanchez, L, Kireev, I, Lardic, L, Dalbies-Tran, R, and Uzbekova, S (2013). Absence of cumulus cells during in vitro maturation affects lipid metabolism in bovine oocytes. American Journal of Physiology-Endocrinology and Metabolism 304, E599–E613.
| Absence of cumulus cells during in vitro maturation affects lipid metabolism in bovine oocytes.Crossref | GoogleScholarGoogle Scholar |
Barrière, C, Santamaría, D, Cerqueira, A, Galán, J, Martín, A, Ortega, S, Malumbres, M, Dubus, P, and Barbacid, M (2007). Mice thrive without Cdk4 and Cdk2. Molecular Oncology 1, 72–83.
| Mice thrive without Cdk4 and Cdk2.Crossref | GoogleScholarGoogle Scholar |
Bavister, BD, and Yanagimachi, R (1977). The effects of sperm extracts and energy sources on the motility and acrosome reaction of hamster spermatozoa in vitro. Biology of Reproduction 16, 228–237.
| The effects of sperm extracts and energy sources on the motility and acrosome reaction of hamster spermatozoa in vitro.Crossref | GoogleScholarGoogle Scholar |
Bedzhov, I, Liszewska, E, Kanzler, B, and Stemmler, MP (2012). Igf1r signaling is indispensable for preimplantation development and is activated via a novel function of E-Cadherin. PLoS Genetics 8, e1002609.
| Igf1r signaling is indispensable for preimplantation development and is activated via a novel function of E-Cadherin.Crossref | GoogleScholarGoogle Scholar |
Berger, PS, and Wood, PA (2004). Disrupted blastocoele formation reveals a critical developmental role for long-chain Acyl-CoA dehydrogenase. Molecular Genetics and Metabolism 82, 266–272.
| Disrupted blastocoele formation reveals a critical developmental role for long-chain Acyl-CoA dehydrogenase.Crossref | GoogleScholarGoogle Scholar |
Betts, DH, and King, WA (2001). Genetic regulation of embryo death and senescence. Theriogenology 55, 171–191.
| Genetic regulation of embryo death and senescence.Crossref | GoogleScholarGoogle Scholar |
Bouniol-Baly, C, Hamraoui, L, Guibert, J, Beaujean, N, Szöllösi, MS, and Debey, P (1999). Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes. Biology of Reproduction 60, 580–587.
| Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes.Crossref | GoogleScholarGoogle Scholar |
Chaube, SK, Shrivastav, TG, Prasad, S, Tiwari, M, Tripathi, A, Pandey, AN, and Premkumar, KV (2014). Clomiphene citrate induces ROS-mediated apoptosis in mammalian oocytes. Open Journal of Apoptosis 03, 52–58.
| Clomiphene citrate induces ROS-mediated apoptosis in mammalian oocytes.Crossref | GoogleScholarGoogle Scholar |
Chowdhury, MMR, Mesalam, A, Khan, I, Joo, M-D, Lee, K-L, Xu, L, Afrin, F, and Kong, I-K (2018). Improved developmental competence in embryos treated with lycopene during in vitro culture system. Molecular Reproduction and Development 85, 46–61.
| Improved developmental competence in embryos treated with lycopene during in vitro culture system.Crossref | GoogleScholarGoogle Scholar |
Christians, E, Boiani, M, Garagna, S, Dessy, C, Redi, CA, Renard, JP, and Zuccotti, M (1999). Gene expression and chromatin organization during mouse oocyte growth. Developmental Biology 207, 76–85.
| Gene expression and chromatin organization during mouse oocyte growth.Crossref | GoogleScholarGoogle Scholar |
Chumakov, PM (2000). Function of the P53 gene: choice between life and death. Biochemistry (Moscow) 65, 28–40.
Coonrod, S (2006). Testis-specific lactate dehydrogenase (LDH-C4; Ldh3) in murine oocytes and preimplantation embryos. Journal of Andrology 27, 502–509.
| Testis-specific lactate dehydrogenase (LDH-C4; Ldh3) in murine oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar |
Cuthbert, JM, Russell, SJ, Polejaeva, IA, Meng, Q, White, KL, and Benninghoff, AD (2021). Comparing mRNA and sncRNA profiles during the maternal-to-embryonic transition in bovine IVF and scNT embryos. Biology of Reproduction 105, 1401–1415.
| Comparing mRNA and sncRNA profiles during the maternal-to-embryonic transition in bovine IVF and scNT embryos.Crossref | GoogleScholarGoogle Scholar |
Dalvit, GC, Cetica, PD, Pintos, LN, and Beconi, MT (2005). Brief note: reactive oxygen species in bovine embryo in vitro production. BIOCELL 29, 209–212.
| Brief note: reactive oxygen species in bovine embryo in vitro production.Crossref | GoogleScholarGoogle Scholar |
Dean, W, Santos, F, Stojkovic, M, Zakhartchenko, V, Walter, J, Wolf, E, and Reik, W (2001). Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proceedings of the National Academy of Sciences 98, 13734–13738.
| Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos.Crossref | GoogleScholarGoogle Scholar |
Deng, M, Liu, Z, Chen, B, Wan, Y, Yang, H, Zhang, Y, Cai, Y, Zhou, J, and Wang, F (2020). Aberrant DNA and histone methylation during zygotic genome activation in goat cloned embryos. Theriogenology 148, 27–36.
| Aberrant DNA and histone methylation during zygotic genome activation in goat cloned embryos.Crossref | GoogleScholarGoogle Scholar |
Devine, PJ, Perreault, SD, and Luderer, U (2012). Roles of reactive oxygen species and antioxidants in ovarian toxicity. Biology of Reproduction 86, 1–10.
| Roles of reactive oxygen species and antioxidants in ovarian toxicity.Crossref | GoogleScholarGoogle Scholar |
Dobbs, KB, Rodriguez, M, Sudano, MJ, Ortega, MS, Hansen, PJ, and Knott, JG (2013). Dynamics of DNA methylation during early development of the preimplantation bovine embryo. PLoS ONE 8, e66230.
| Dynamics of DNA methylation during early development of the preimplantation bovine embryo.Crossref | GoogleScholarGoogle Scholar |
Du, C, Davis, JS, Chen, C, Li, Z, Cao, Y, Sun, H, Shao, B-S, et al. (2021). FGF2/FGFR signaling promotes cumulus-oocyte complex maturation in vitro. Reproduction, October , .
| FGF2/FGFR signaling promotes cumulus-oocyte complex maturation in vitro.Crossref | GoogleScholarGoogle Scholar |
Duan, J, Zhu, L, Dong, H, Zheng, X, Jiang, Z, Chen, J, and Tian, XC (2019). Analysis of mRNA abundance for histone variants, histone- and DNA-modifiers in bovine in vivo and in vitro oocytes and embryos. Scientific Reports 9, 1217.
| Analysis of mRNA abundance for histone variants, histone- and DNA-modifiers in bovine in vivo and in vitro oocytes and embryos.Crossref | GoogleScholarGoogle Scholar |
Dumollard, R, Ward, Z, Carroll, J, and Duchen, MR (2007). Regulation of redox metabolism in the mouse oocyte and embryo. Development 134, 455–465.
| Regulation of redox metabolism in the mouse oocyte and embryo.Crossref | GoogleScholarGoogle Scholar |
Dunning, KR, Cashman, K, Russell, DL, Thompson, JG, Norman, RJ, and Robker, RL (2010). Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Biology of Reproduction 83, 909–918.
| Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development.Crossref | GoogleScholarGoogle Scholar |
Eckert, J, and Niemann, H (1998). mRNA expression of leukaemia inhibitory factor (LIF) and its receptor subunits glycoprotein 130 and LIF-receptor-beta in bovine embryos derived in vitro or in vivo. Molecular Human Reproduction 4, 957–965.
| mRNA expression of leukaemia inhibitory factor (LIF) and its receptor subunits glycoprotein 130 and LIF-receptor-beta in bovine embryos derived in vitro or in vivo.Crossref | GoogleScholarGoogle Scholar |
El-Sayed, A, Hoelker, M, Rings, F, Salilew, D, Jennen, D, Tholen, E, Sirard, M-A, Schellander, K, and Tesfaye, D (2006). Large-scale transcriptional analysis of bovine embryo biopsies in relation to pregnancy success after transfer to recipients. Physiological Genomics 28, 84–96.
| Large-scale transcriptional analysis of bovine embryo biopsies in relation to pregnancy success after transfer to recipients.Crossref | GoogleScholarGoogle Scholar |
Eppig, JJ, O’Brien, MJ, Wigglesworth, K, Nicholson, A, Zhang, W, and King, BA (2008). Effect of in vitro maturation of mouse oocytes on the health and lifespan of adult offspring. Human Reproduction 24, 922–928.
| Effect of in vitro maturation of mouse oocytes on the health and lifespan of adult offspring.Crossref | GoogleScholarGoogle Scholar |
Ferreira, EM, Vireque, AA, Adona, PR, Meirelles, FV, Ferriani, RA, and Navarro, PAAS (2009). Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71, 836–848.
| Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence.Crossref | GoogleScholarGoogle Scholar |
Furnus, CC, de Matos, DG, Picco, S, García, PP, Inda, AM, Mattioli, G, and Errecalde, AL (2008). Metabolic requirements associated with GSH synthesis during in vitro maturation of cattle oocytes. Animal Reproduction Science 109, 88–99.
| Metabolic requirements associated with GSH synthesis during in vitro maturation of cattle oocytes.Crossref | GoogleScholarGoogle Scholar |
Gandhi, AP (2000). A single medium supports development of bovine embryos throughout maturation, fertilization and culture. Human Reproduction 15, 395–401.
| A single medium supports development of bovine embryos throughout maturation, fertilization and culture.Crossref | GoogleScholarGoogle Scholar |
Ghisla, S, and Thorpe, C (2004). Acyl-CoA dehydrogenases. a mechanistic overview. European Journal of Biochemistry 271, 494–508.
| Acyl-CoA dehydrogenases. a mechanistic overview.Crossref | GoogleScholarGoogle Scholar |
Goissis, MD, and Cibelli, JB (2014). Functional characterization of SOX2 in bovine preimplantation embryos. Biology of Reproduction 90, 1–10.
| Functional characterization of SOX2 in bovine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar |
Goldstein, JL, and Brown, MS (1990). Regulation of the mevalonate pathway. Nature 343, 425–430.
| Regulation of the mevalonate pathway.Crossref | GoogleScholarGoogle Scholar |
Graf, A, Krebs, S, Zakhartchenko, V, Schwalb, B, Blum, H, and Wolf, E (2014). Fine mapping of genome activation in bovine embryos by RNA sequencing. Proceedings of the National Academy of Sciences 111, 4139–44.
| Fine mapping of genome activation in bovine embryos by RNA sequencing.Crossref | GoogleScholarGoogle Scholar |
Guerra, C, Koza, RA, Walsh, K, Kurtz, DM, Wood, PA, and Kozak, LP (1998). Abnormal nonshivering thermogenesis in mice with inherited defects of fatty acid oxidation. Journal of Clinical Investigation 102, 1724–1731.
| Abnormal nonshivering thermogenesis in mice with inherited defects of fatty acid oxidation.Crossref | GoogleScholarGoogle Scholar |
Haffner-Krausz, R, Gorivodsky, M, Chen, Y, and Lonai, P (1999). Expression of Fgfr2 in the early mouse embryo indicates its involvement in preimplantation development. Mechanisms of Development 85, 167–172.
| Expression of Fgfr2 in the early mouse embryo indicates its involvement in preimplantation development.Crossref | GoogleScholarGoogle Scholar |
Hartig, SM (2013). Basic image analysis and manipulation in ImageJ. Current Protocols in Molecular Biology 102, 14.15.1–14.15.12.
| Basic image analysis and manipulation in ImageJ.Crossref | GoogleScholarGoogle Scholar |
Hashimoto, S, Minami, N, Yamada, M, and Imai, H (2000). Excessive concentration of glucose during in vitro maturation impairs the developmental competence of bovine oocytes after in vitro fertilization: relevance to intracellular reactive oxygen species and glutathione contents. Molecular Reproduction and Development 56, 520–526.
| Excessive concentration of glucose during in vitro maturation impairs the developmental competence of bovine oocytes after in vitro fertilization: relevance to intracellular reactive oxygen species and glutathione contents.Crossref | GoogleScholarGoogle Scholar |
Hayes, MJ, Shao, D, Bailly, M, and Moss, SE (2006). Regulation of actin dynamics by annexin 2. The EMBO Journal 25, 1816–1826.
| Regulation of actin dynamics by annexin 2.Crossref | GoogleScholarGoogle Scholar |
Hu, B, Hu, S, Huang, H, Wei, Q, Ren, M, Huang, S, Tian, X, and Su, J (2019). Insecticides induce the co-expression of glutathione S-transferases through ROS/CncC pathway in Spodoptera exigua. Pesticide Biochemistry and Physiology 155, 58–71.
| Insecticides induce the co-expression of glutathione S-transferases through ROS/CncC pathway in Spodoptera exigua.Crossref | GoogleScholarGoogle Scholar |
Hunt, T (1989). Maturation promoting factor, cyclin and the control of M-phase. Current Opinion in Cell Biology 1, 268–274.
| Maturation promoting factor, cyclin and the control of M-phase.Crossref | GoogleScholarGoogle Scholar |
Javvaji, PK, Dhali, A, Francis, JR, Kolte, AP, Roy, SC, Selvaraju, S, Mech, A, and Sejian, V (2021). IGF-1 treatment during in vitro maturation improves developmental potential of ovine oocytes through the regulation of PI3K/Akt and apoptosis signaling. Animal Biotechnology 32, 798–805.
| IGF-1 treatment during in vitro maturation improves developmental potential of ovine oocytes through the regulation of PI3K/Akt and apoptosis signaling.Crossref | GoogleScholarGoogle Scholar |
Jiang, Z, Dong, H, Zheng, X, Marjani, SL, Donovan, DM, Chen, J, and Tian, X (2015). mRNA levels of imprinted genes in bovine in vivo oocytes, embryos and cross species comparisons with humans, mice and pigs. Scientific Reports 5, 17898.
| mRNA levels of imprinted genes in bovine in vivo oocytes, embryos and cross species comparisons with humans, mice and pigs.Crossref | GoogleScholarGoogle Scholar |
Jo, Y, Kim, SS, Garland, K, Fuentes, I, DiCarlo, LM, Ellis, JL, Fu, X, Booth, SL, Evers, BM, and DeBose-Boyd, RA (2020). Enhanced ER-associated degradation of HMG CoA reductase causes embryonic lethality associated with Ubiad1 deficiency. eLife 9, e54841.
| Enhanced ER-associated degradation of HMG CoA reductase causes embryonic lethality associated with Ubiad1 deficiency.Crossref | GoogleScholarGoogle Scholar |
Kafi, M, McGowan, MR, and Kirkland, PD (2002). In vitro maturation and fertilization of bovine oocytes and in vitro culture of presumptive zygotes in the presence of bovine pestivirus. Animal Reproduction Science 71, 169–179.
| In vitro maturation and fertilization of bovine oocytes and in vitro culture of presumptive zygotes in the presence of bovine pestivirus.Crossref | GoogleScholarGoogle Scholar |
Kang, M, Garg, V, and Hadjantonakis, A-K (2017). Lineage establishment and progression within the inner cell mass of the mouse blastocyst requires FGFR1 and FGFR2. Developmental Cell 41, 496–510.e5.
| Lineage establishment and progression within the inner cell mass of the mouse blastocyst requires FGFR1 and FGFR2.Crossref | GoogleScholarGoogle Scholar |
Khatib, H, Maltecca, C, Monson, RL, Schutzkus, V, Wang, X, and Rutledge, JJ (2008). The fibroblast growth factor 2 gene is associated with embryonic mortality in cattle. Journal of Animal Science 86, 2063–2067.
| The fibroblast growth factor 2 gene is associated with embryonic mortality in cattle.Crossref | GoogleScholarGoogle Scholar |
Kim, KS, Mitsumizo, N, Fujita, K, and Utsumi, K (1996). The effects of follicular fluid on in vitro maturation, oocyte fertilization and the development of bovine embryos. Theriogenology 45, 787–799.
| The effects of follicular fluid on in vitro maturation, oocyte fertilization and the development of bovine embryos.Crossref | GoogleScholarGoogle Scholar |
Koo, D-B, Kang, Y-K, Choi, Y-H, Park, JS, Kim, H-N, Oh, KB, Son, D-S, Park, H, Lee, K-K, and Han, Y-M (2002). Aberrant allocations of inner cell mass and trophectoderm cells in bovine nuclear transfer blastocysts. Biology of Reproduction 67, 487–492.
| Aberrant allocations of inner cell mass and trophectoderm cells in bovine nuclear transfer blastocysts.Crossref | GoogleScholarGoogle Scholar |
Kurtz, DM, Rinaldo, P, Rhead, WJ, Tian, L, Millington, DS, Vockley, J, Hamm, DA, et al. (1998). Targeted disruption of mouse long-chain acyl-CoA dehydrogenase gene reveals crucial roles for fatty acid oxidation. Proceedings of the National Academy of Sciences 95, 15592–97.
| Targeted disruption of mouse long-chain acyl-CoA dehydrogenase gene reveals crucial roles for fatty acid oxidation.Crossref | GoogleScholarGoogle Scholar |
Kwak, S-S, Cheong, S-A, Jeon, Y, Lee, E, Choi, K-C, Jeung, E-B, and Hyun, S-H (2012). The effects of resveratrol on porcine oocyte in vitro maturation and subsequent embryonic development after parthenogenetic activation and in vitro fertilization. Theriogenology 78, 86–101.
| The effects of resveratrol on porcine oocyte in vitro maturation and subsequent embryonic development after parthenogenetic activation and in vitro fertilization.Crossref | GoogleScholarGoogle Scholar |
Ledee-Bataille, N (2002). Concentration of leukaemia inhibitory factor (LIF) in uterine flushing fluid is highly predictive of embryo implantation. Human Reproduction 17, 213–218.
| Concentration of leukaemia inhibitory factor (LIF) in uterine flushing fluid is highly predictive of embryo implantation.Crossref | GoogleScholarGoogle Scholar |
Lim, KT, Jang, G, Ko, KH, Lee, WW, Park, HJ, Kim, JJ, Lee, SH, Hwang, WS, Lee, BC, and Kang, SK (2007). Improved in vitro bovine embryo development and increased efficiency in producing viable calves using defined media. Theriogenology 67, 293–302.
| Improved in vitro bovine embryo development and increased efficiency in producing viable calves using defined media.Crossref | GoogleScholarGoogle Scholar |
Liu, J-P, Baker, J, Perkins, AS, Robertson, EJ, and Efstratiadis, A (1993). Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 75, 59–72.
Liu, P, Begley, M, Michowski, W, Inuzuka, H, Ginzberg, M, Gao, D, Tsou, P, et al. (2014). Cell-cycle-regulated activation of Akt kinase by phosphorylation at its carboxyl terminus. Nature 508, 541–545.
| Cell-cycle-regulated activation of Akt kinase by phosphorylation at its carboxyl terminus.Crossref | GoogleScholarGoogle Scholar |
Livak, KJ, and Schmittgen, TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar |
Maimets, T, Neganova, I, Armstrong, L, and Lako, M (2008). Activation of p53 by nutlin leads to rapid differentiation of human embryonic stem cells. Oncogene 27, 5277–5287.
| Activation of p53 by nutlin leads to rapid differentiation of human embryonic stem cells.Crossref | GoogleScholarGoogle Scholar |
Markham, KE, and Kaye, PL (2003). Growth hormone, insulin-like growth factor I and cell proliferation in the mouse blastocyst. Reproduction 125, 327–336.
| Growth hormone, insulin-like growth factor I and cell proliferation in the mouse blastocyst.Crossref | GoogleScholarGoogle Scholar |
Massudi, H, Grant, R, Guillemin, GJ, and Braidy, N (2012). NAD+ metabolism and oxidative stress: the golden nucleotide on a crown of thorns. Redox Report 17, 28–46.
| NAD+ metabolism and oxidative stress: the golden nucleotide on a crown of thorns.Crossref | GoogleScholarGoogle Scholar |
McBride, D, Carré, W, Sontakke, SD, Hogg, CO, Law, A, Donadeu, FX, and Clinton, M (2012). Identification of miRNAs associated with the follicular–luteal transition in the ruminant ovary. Reproduction 144, 221–233.
| Identification of miRNAs associated with the follicular–luteal transition in the ruminant ovary.Crossref | GoogleScholarGoogle Scholar |
Milkovic, L, Cipak Gasparovic, A, Cindric, M, Mouthuy, P-A, and Zarkovic, N (2019). Short overview of ROS as cell function regulators and their implications in therapy concepts. Cells 8, 793.
| Short overview of ROS as cell function regulators and their implications in therapy concepts.Crossref | GoogleScholarGoogle Scholar |
Mo, X, Wu, G, Yuan, D, Jia, B, Liu, C, Zhu, S, and Hou, Y (2014). Leukemia inhibitory factor enhances bovine oocyte maturation and early embryo development: role of leukemia inhibitory factor in bovine oocyte maturation. Molecular Reproduction and Development 81, 608–618.
| Leukemia inhibitory factor enhances bovine oocyte maturation and early embryo development: role of leukemia inhibitory factor in bovine oocyte maturation.Crossref | GoogleScholarGoogle Scholar |
Molyneaux, KA, Schaible, K, and Wylie, C (2003). GP130, the shared receptor for the LIF/IL6 cytokine family in the mouse, is not required for early germ cell differentiation, but is required cell-autonomously in oocytes for ovulation. Development 130, 4287–4294.
| GP130, the shared receptor for the LIF/IL6 cytokine family in the mouse, is not required for early germ cell differentiation, but is required cell-autonomously in oocytes for ovulation.Crossref | GoogleScholarGoogle Scholar |
Nuttinck, F, Charpigny, G, Mermillod, P, Loosfelt, H, Meduri, G, Freret, S, Grimard, B, and Heyman, Y (2004). Expression of components of the insulin-like growth factor system and gonadotropin receptors in bovine cumulus–oocyte complexes during oocyte maturation. Domestic Animal Endocrinology 27, 179–195.
| Expression of components of the insulin-like growth factor system and gonadotropin receptors in bovine cumulus–oocyte complexes during oocyte maturation.Crossref | GoogleScholarGoogle Scholar |
Ohashi, K, Osuga, J-I, Tozawa, R, Kitamine, T, Yagyu, H, Sekiya, M, Tomita, S, et al. (2003). Early embryonic lethality caused by targeted disruption of the 3-hydroxy-3-methylglutaryl-CoA reductase gene. Journal of Biological Chemistry 278, 42936–42941.
| Early embryonic lethality caused by targeted disruption of the 3-hydroxy-3-methylglutaryl-CoA reductase gene.Crossref | GoogleScholarGoogle Scholar |
Okano, M, Bell, DW, Haber, DA, and Li, E (1999). DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247–257.
| DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development.Crossref | GoogleScholarGoogle Scholar |
Ono, R, Kobayashi, S, Wagatsuma, H, Aisaka, K, Kohda, T, Kaneko-Ishino, T, and Ishino, F (2001). A retrotransposon-derived gene, PEG10, is a novel imprinted gene located on human chromosome 7q21. Genomics 73, 232–237.
| A retrotransposon-derived gene, PEG10, is a novel imprinted gene located on human chromosome 7q21.Crossref | GoogleScholarGoogle Scholar |
Ono, R, Nakamura, K, Inoue, K, Naruse, M, Usami, T, Wakisaka-Saito, N, Hino, T, et al. (2006). Deletion of Peg10, an imprinted gene acquired from a retrotransposon, causes early embryonic lethality. Nature Genetics 38, 101–106.
| Deletion of Peg10, an imprinted gene acquired from a retrotransposon, causes early embryonic lethality.Crossref | GoogleScholarGoogle Scholar |
O’Hara, L, Forde, N, Kelly, AK, and Lonergan, P (2014). Effect of bovine blastocyst size at embryo transfer on day 7 on conceptus length on day 14: can supplementary progesterone rescue small embryos? Theriogenology 81, 1123–1128.
| Effect of bovine blastocyst size at embryo transfer on day 7 on conceptus length on day 14: can supplementary progesterone rescue small embryos?Crossref | GoogleScholarGoogle Scholar |
Perisse, IV, Fan, Z, Singina, GN, White, KL, and Polejaeva, IA (2021). Improvements in gene editing technology boost its applications in livestock. Frontiers in Genetics 11, 614688.
| Improvements in gene editing technology boost its applications in livestock.Crossref | GoogleScholarGoogle Scholar |
Petrussa, L, Van de Velde, H, and De Rycke, M (2014). Dynamic regulation of DNA methyltransferases in human oocytes and preimplantation embryos after assisted reproductive technologies. Molecular Human Reproduction 20, 861–874.
| Dynamic regulation of DNA methyltransferases in human oocytes and preimplantation embryos after assisted reproductive technologies.Crossref | GoogleScholarGoogle Scholar |
Redel, BK, Spate, LD, Yuan, Y, Murphy, CN, Roberts, RM, and Prather, RS (2021). Neither gonadotropin nor cumulus cell expansion is needed for the maturation of competent porcine oocytes in vitro. Biology of Reproduction 105, 533–542.
| Neither gonadotropin nor cumulus cell expansion is needed for the maturation of competent porcine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar |
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. Molecular Reproduction and Development 61, 234–248.
| Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality.Crossref | GoogleScholarGoogle Scholar |
Sharpley, MS, Chi, F, Hoeve, J, and Banerjee, U (2021). Metabolic plasticity drives development during mammalian embryogenesis. Developmental Cell 56, 2329–2347.e6.
| Metabolic plasticity drives development during mammalian embryogenesis.Crossref | GoogleScholarGoogle Scholar |
Sirotkin, AV, Dukesová, J, Makarevich, AV, Kubek, A, and Bulla, J (2000). Evidence that growth factors IGF-I, IGF-II and EGF can stimulate nuclear maturation of porcine oocytes via intracellular protein kinase A. Reproduction Nutrition Development 40, 559–569.
| Evidence that growth factors IGF-I, IGF-II and EGF can stimulate nuclear maturation of porcine oocytes via intracellular protein kinase A.Crossref | GoogleScholarGoogle Scholar |
Stoecklein, KS, Ortega, MS, Spate, LD, Murphy, CN, and Prather, RS (2021). Improved cryopreservation of in vitro produced bovine embryos using FGF2, LIF, and IGF1. PLoS ONE 16, e0243727.
| Improved cryopreservation of in vitro produced bovine embryos using FGF2, LIF, and IGF1.Crossref | GoogleScholarGoogle Scholar |
Tai, C-I, and Ying, Q-L (2013). Gbx2, a LIF/Stat3 target, promotes reprogramming to and retention of the pluripotent ground state. Journal of Cell Science 126, 1093–1098.
| Gbx2, a LIF/Stat3 target, promotes reprogramming to and retention of the pluripotent ground state.Crossref | GoogleScholarGoogle Scholar |
Thélie, A, Papillier, P, Pennetier, S, Perreau, C, Traverso, JM, Uzbekova, S, Mermillod, P, Joly, C, Humblot, P, and Dalbiès-Tran, R (2007). Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo. BMC Developmental Biology 7, 125.
| Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo.Crossref | GoogleScholarGoogle Scholar |
Tian, H, Qi, Q, Yan, F, Wang, C, Hou, F, Ren, W, Zhang, L, and Hou, J (2021). Enhancing the developmental competence of prepubertal lamb oocytes by supplementing the in vitro maturation medium with sericin and the fibroblast growth factor 2 – leukemia inhibitory factor – insulin-like growth factor 1 combination. Theriogenology 159, 13–19.
| Enhancing the developmental competence of prepubertal lamb oocytes by supplementing the in vitro maturation medium with sericin and the fibroblast growth factor 2 – leukemia inhibitory factor – insulin-like growth factor 1 combination.Crossref | GoogleScholarGoogle Scholar |
Tscherner, A, Brown, AC, Stalker, L, Kao, J, Dufort, I, Sirard, M-A, and LaMarre, J (2018). STAT3 signaling stimulates miR-21 expression in bovine cumulus cells during in vitro oocyte maturation. Scientific Reports 8, 11527.
| STAT3 signaling stimulates miR-21 expression in bovine cumulus cells during in vitro oocyte maturation.Crossref | GoogleScholarGoogle Scholar |
Uysal, F, Cinar, O, and Can, A (2021). Knockdown of Dnmt1 and Dnmt3a gene expression disrupts preimplantation embryo development through global DNA methylation. Journal of Assisted Reproduction and Genetics 38, 3135–3144.
| Knockdown of Dnmt1 and Dnmt3a gene expression disrupts preimplantation embryo development through global DNA methylation.Crossref | GoogleScholarGoogle Scholar |
Wang, F, Tian, XZ, Zhang, L, He, CJ, Ji, PY, Li, Y, Tan, DX, and Liu, GS (2014). Beneficial effect of resveratrol on bovine oocyte maturation and subsequent embryonic development after in vitro fertilization. Fertility and Sterility 101, 577–586.e1.
| Beneficial effect of resveratrol on bovine oocyte maturation and subsequent embryonic development after in vitro fertilization.Crossref | GoogleScholarGoogle Scholar |
Wasielak, M, and Bogacki, M (2007). Apoptosis inhibition by insulin-like growth factor (IGF)-I during in vitro maturation of bovine oocytes. Journal of Reproduction and Development 53, 419–426.
| Apoptosis inhibition by insulin-like growth factor (IGF)-I during in vitro maturation of bovine oocytes.Crossref | GoogleScholarGoogle Scholar |
Webb, R, and Campbell, BK (2007). Development of the dominant follicle: mechanisms of selection and maintenance of oocyte quality. Reproduction in Domestic Ruminants 6, 141–163.
| Development of the dominant follicle: mechanisms of selection and maintenance of oocyte quality.Crossref | GoogleScholarGoogle Scholar |
Whitty, A, Kind, KL, Dunning, KR, and Thompson, JG (2021). Effect of oxygen and glucose availability during in vitro maturation of bovine oocytes on development and gene expression. Journal of Assisted Reproduction and Genetics 38, 1349–1362.
| Effect of oxygen and glucose availability during in vitro maturation of bovine oocytes on development and gene expression.Crossref | GoogleScholarGoogle Scholar |
Wright, J, and Mapletoft, R (2022). Appendix 1: photographic illustrations of in vivo- derived embryo developmental stage and quality codes. Manual of the International Embryo Transfer Society 2, 1–4.
Yang, MY, and Rajamahendran, R (2002). Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro. Animal Reproduction Science 70, 159–169.
| Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar |
Yang, J, Zhang, D, Yu, Y, Zhang, R-J, Hu, X-L, Huang, H-F, and Lu, Y-C (2015). Binding of FGF2 to FGFR2 in an autocrine mode in trophectoderm cells is indispensable for mouse blastocyst formation through PKC-p38 pathway. Cell Cycle 14, 3318–3330.
| Binding of FGF2 to FGFR2 in an autocrine mode in trophectoderm cells is indispensable for mouse blastocyst formation through PKC-p38 pathway.Crossref | GoogleScholarGoogle Scholar |
Yao, H, and Ye, J (2008). Long chain Acyl-CoA synthetase 3-mediated phosphatidylcholine synthesis is required for assembly of very low density lipoproteins in human hepatoma Huh7 cells. Journal of Biological Chemistry 283, 849–854.
| Long chain Acyl-CoA synthetase 3-mediated phosphatidylcholine synthesis is required for assembly of very low density lipoproteins in human hepatoma Huh7 cells.Crossref | GoogleScholarGoogle Scholar |
Yuan, Y, Spate, LD, Redel, BK, Tian, Y, Zhou, J, Prather, RS, and Roberts, RM (2017). Quadrupling efficiency in production of genetically modified pigs through improved oocyte maturation. Proceedings of the National Academy of Sciences 114, E5796–5804.
| Quadrupling efficiency in production of genetically modified pigs through improved oocyte maturation.Crossref | GoogleScholarGoogle Scholar |
Zhang, K, and Ealy, AD (2012). Supplementing fibroblast growth factor 2 during bovine oocyte in vitro maturation promotes subsequent embryonic development. Open Journal of Animal Sciences 02, 119–126.
| Supplementing fibroblast growth factor 2 during bovine oocyte in vitro maturation promotes subsequent embryonic development.Crossref | GoogleScholarGoogle Scholar |
Zhang, K, Hansen, PJ, and Ealy, AD (2010). Fibroblast growth factor 10 enhances bovine oocyte maturation and developmental competence in vitro. Reproduction 140, 815–826.
| Fibroblast growth factor 10 enhances bovine oocyte maturation and developmental competence in vitro.Crossref | GoogleScholarGoogle Scholar |
Zhang, Y, Xiang, Y, Yin, Q, Du, Z, Peng, X, Wang, Q, Fidalgo, M, et al. (2018). Dynamic epigenomic landscapes during early lineage specification in mouse embryos. Nature Genetics 50, 96–105.
| Dynamic epigenomic landscapes during early lineage specification in mouse embryos.Crossref | GoogleScholarGoogle Scholar |
Zhou, J, Bievre, M, and Bondy, CA (2000). Reduced GLUT1 expression in Igf1–/– null oocytes and follicles. Growth Hormone & IGF Research 10, 111–117.
| Reduced GLUT1 expression in Igf1–/– null oocytes and follicles.Crossref | GoogleScholarGoogle Scholar |