Effect of carbohydrates on lipid metabolism during porcine oocyte IVM
Jenna L. Lowe A , Roslyn Bathgate A and Christopher G. Grupen A BA Sydney School of Veterinary Science, Faculty of Science, The University of Sydney, 425 Werombi Road, Camden, NSW 2570, Australia.
B Corresponding author. Email: christopher.grupen@sydney.edu.au
Reproduction, Fertility and Development 31(3) 557-569 https://doi.org/10.1071/RD18043
Abstract
Porcine oocytes contain a large amount of endogenous lipid, which is thought to function as an intracellular source of energy. The aim of this study was to determine the effects of stimulating or inhibiting lipid metabolism using l-carnitine or etomoxir respectively on the IVM of porcine oocytes cultured in media of varying carbohydrate composition. In the presence of pyruvate and lactate, exclusion of glucose inhibited oocyte nuclear and cytoplasmic maturation compared with oocytes matured in media containing low (1.5 mM) and high (4.0 mM) concentrations of glucose. In the absence of pyruvate and lactate in low-glucose medium only, a greater proportion of l-carnitine-treated oocytes progressed to the MII stage compared with untreated oocytes. The inclusion of pyruvate and lactate significantly altered the distribution of cytoplasmic lipid droplets and elevated the ATP content of oocytes, whereas the l-carnitine treatment did not. Further, the inhibitory effect of etomoxir on nuclear maturation was decreased in high- compared with low-glucose medium. The results indicate that carbohydrate substrates are absolutely necessary for effective porcine oocyte maturation, and that l-carnitine supplementation can only partially compensate for deficiencies in carbohydrate provision.
Additional keywords: embryo, fatty acid.
References
Ali, A., and Sirard, M. A. (2002). Effect of the absence or presence of various protein supplements on further development of bovine oocytes during in vitro maturation. Biol. Reprod. 66, 901–905.| Effect of the absence or presence of various protein supplements on further development of bovine oocytes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar |
Alvarez, G. M., Dalvit, G. C., Achi, M. V., Miguez, M. S., and Cetica, P. D. (2009). Immature oocyte quality and maturational competence of porcine cumulus–oocyte complexes subpopulations. Biocell 33, 167–177.
Appeltant, R., Somfai, T., Nakai, M., Bodo, S., Maes, D., Kikuchi, K., and Van Soom, A. (2015). Interactions between oocytes and cumulus cells during in vitro maturation of porcine cumulus–oocyte complexes in a chemically defined medium: effect of denuded oocytes on cumulus expansion and oocyte maturation. Theriogenology 83, 567–576.
| Interactions between oocytes and cumulus cells during in vitro maturation of porcine cumulus–oocyte complexes in a chemically defined medium: effect of denuded oocytes on cumulus expansion and oocyte maturation.Crossref | GoogleScholarGoogle Scholar |
Bagg, M. A., Vassena, R., Papasso-Brambilla, E., Grupen, C. G., Armstrong, D. T., and Gandolfi, F. (2004). Changes in ovarian, follicular, and oocyte morphology immediately after the onset of puberty are not accompanied by an increase in oocyte developmental competence in the pig. Theriogenology 62, 1003–1011.
| Changes in ovarian, follicular, and oocyte morphology immediately after the onset of puberty are not accompanied by an increase in oocyte developmental competence in the pig.Crossref | GoogleScholarGoogle Scholar |
Bagg, M. A., Nottle, M. B., Armstrong, D. T., and Grupen, C. G. (2007). Relationship between follicle size and oocyte developmental competence in prepubertal and adult pigs. Reprod. Fertil. Dev. 19, 797–803.
| Relationship between follicle size and oocyte developmental competence in prepubertal and adult pigs.Crossref | GoogleScholarGoogle Scholar |
Bartolac, L. K., Lowe, J. L., Koustas, G., Sjöblom, C., and Grupen, C. G. (2015). A comparison of different vitrification devices and the effect of blastocoele collapse on the cryosurvival of in vitro produced porcine embryos. J. Reprod. Dev. 61, 525–531.
| A comparison of different vitrification devices and the effect of blastocoele collapse on the cryosurvival of in vitro produced porcine embryos.Crossref | GoogleScholarGoogle Scholar |
Bavister, B. D. (1989). A consistently successful procedure for in vitro fertilization of golden hamster eggs. Gamete Res. 23, 139–158.
| A consistently successful procedure for in vitro fertilization of golden hamster eggs.Crossref | GoogleScholarGoogle Scholar |
Bertoldo, M., Holyoake, P. K., Evans, G., and Grupen, C. G. (2010). Oocyte developmental competence is reduced in sows during the seasonal infertility period. Reprod. Fertil. Dev. 22, 1222–1229.
| Oocyte developmental competence is reduced in sows during the seasonal infertility period.Crossref | GoogleScholarGoogle Scholar |
Bertoldo, M. J., Holyoake, P. K., Evans, G., and Grupen, C. G. (2011). Seasonal effects on oocyte developmental competence in sows experiencing pregnancy loss. Anim. Reprod. Sci. 124, 104–111.
| Seasonal effects on oocyte developmental competence in sows experiencing pregnancy loss.Crossref | GoogleScholarGoogle Scholar |
Bertoldo, M. J., Nadal-Desbarats, L., Gerard, N., Dubois, A., Holyoake, P. K., and Grupen, C. G. (2013). Differences in the metabolomic signatures of porcine follicular fluid collected from environments associated with good and poor oocyte quality. Reproduction 146, 221–231.
| Differences in the metabolomic signatures of porcine follicular fluid collected from environments associated with good and poor oocyte quality.Crossref | GoogleScholarGoogle Scholar |
Biggers, J. D., Whitting, D. G., and Donahue, R. P. (1967). Pattern of energy metabolism in mouse oocyte and zygote. Proc. Natl Acad. Sci. USA 58, 560–567.
| Pattern of energy metabolism in mouse oocyte and zygote.Crossref | GoogleScholarGoogle Scholar |
Cetica, P., Pintos, L., Dalvit, G., and Beconi, M. (2002). Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro. Reproduction 124, 675–681.
| Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro.Crossref | GoogleScholarGoogle Scholar |
Chankitisakul, V., Somfai, T., Inaba, Y., Techakumphu, M., and Nagai, T. (2013). Supplementation of maturation medium with l-carnitine improves cryotolerance of bovine in vitro matured oocytes. Theriogenology 79, 590–598.
| Supplementation of maturation medium with l-carnitine improves cryotolerance of bovine in vitro matured oocytes.Crossref | GoogleScholarGoogle Scholar |
Downs, S. M., and Utecht, A. M. (1999). Metabolism of radiolabeled glucose by mouse oocytes and oocyte–cumulus cell complexes. Biol. Reprod. 60, 1446–1452.
| Metabolism of radiolabeled glucose by mouse oocytes and oocyte–cumulus cell complexes.Crossref | GoogleScholarGoogle Scholar |
Downs, S. M., Mosey, J. L., and Klinger, J. (2009). Fatty acid oxidation and meiotic resumption in mouse oocytes. Mol. Reprod. Dev. 76, 844–853.
| Fatty acid oxidation and meiotic resumption in mouse oocytes.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., Akison, L. K., Russell, D. L., Norman, R. J., and Robker, R. L. (2011). Increased beta-oxidation and improved oocyte developmental competence in response to l-carnitine during ovarian in vitro follicle development in mice. Biol. Reprod. 85, 548–555.
| Increased beta-oxidation and improved oocyte developmental competence in response to l-carnitine during ovarian in vitro follicle development in mice.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 |
Ferguson, E. M., and Leese, H. J. (1999). Triglyceride content of bovine oocytes and early embryos. J. Reprod. Fertil. 116, 373–378.
| Triglyceride content of bovine oocytes and early embryos.Crossref | GoogleScholarGoogle Scholar |
Ferguson, E. M., and Leese, H. J. (2006). A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development. Mol. Reprod. Dev. 73, 1195–1201.
| A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development.Crossref | GoogleScholarGoogle Scholar |
Fu, X. W., Wu, G. Q., Li, J. J., Hou, Y. P., Zhou, G. B., Lun, S., Wang, Y. P., and Zhu, S. E. (2011). Positive effects of forskolin (stimulator of lipolysis) treatment on cryosurvival of in vitro matured porcine oocytes. Theriogenology 75, 268–275.
| Positive effects of forskolin (stimulator of lipolysis) treatment on cryosurvival of in vitro matured porcine oocytes.Crossref | GoogleScholarGoogle Scholar |
Funahashi, H., Koike, T., and Sakai, R. (2008). Effect of glucose and pyruvate on nuclear and cytoplasmic maturation of porcine oocytes in a chemically defined medium. Theriogenology 70, 1041–1047.
| Effect of glucose and pyruvate on nuclear and cytoplasmic maturation of porcine oocytes in a chemically defined medium.Crossref | GoogleScholarGoogle Scholar |
Gérard, N., Fahiminiya, S., Grupen, C. G., and Nadal-Desbarats, L. (2015). Reproductive physiology and ovarian folliculogenesis examined via 1H-NMR metabolomics signatures: a comparative study of large and small follicles in three mammalian species (Bos taurus, Sus scrofa domesticus and Equus ferus caballus). OMICS 19, 31–40.
| Reproductive physiology and ovarian folliculogenesis examined via 1H-NMR metabolomics signatures: a comparative study of large and small follicles in three mammalian species (Bos taurus, Sus scrofa domesticus and Equus ferus caballus).Crossref | GoogleScholarGoogle Scholar |
Gil, M. A., Ruiz, M., Vazquez, J. M., Roca, J., Day, B. N., and Martinez, E. A. (2004). Effect of short periods of sperm–oocyte coincubation during in vitro fertilization on embryo development in pigs. Theriogenology 62, 544–552.
| Effect of short periods of sperm–oocyte coincubation during in vitro fertilization on embryo development in pigs.Crossref | GoogleScholarGoogle Scholar |
Gonzales-Figueroa, H., and Gonzales-Molfino, H. M. (2005). Maturation of pig oocytes in vitro in a medium with pyruvate. Braz. J. Med. Biol. Res. 38, 869–872.
| Maturation of pig oocytes in vitro in a medium with pyruvate.Crossref | GoogleScholarGoogle Scholar |
Grupen, C. G. (2014). The evolution of porcine embryo in vitro production. Theriogenology 81, 24–37.
| The evolution of porcine embryo in vitro production.Crossref | GoogleScholarGoogle Scholar |
Grupen, C. G., and Armstrong, D. T. (2010). Relationship between cumulus cell apoptosis, progesterone production and porcine oocyte developmental competence: temporal effects of follicular fluid during IVM. Reprod. Fertil. Dev. 22, 1100–1109.
| Relationship between cumulus cell apoptosis, progesterone production and porcine oocyte developmental competence: temporal effects of follicular fluid during IVM.Crossref | GoogleScholarGoogle Scholar |
Grupen, C. G., McIlfatrick, S. M., Ashman, R. J., Boquest, A. C., Armstrong, D. T., and Nottle, M. B. (2003). Relationship between donor animal age, follicular fluid steroid content and oocyte developmental competence in the pig. Reprod. Fertil. Dev. 15, 81–87.
| Relationship between donor animal age, follicular fluid steroid content and oocyte developmental competence in the pig.Crossref | GoogleScholarGoogle Scholar |
Herrick, J. R., Brad, A. M., and Krisher, R. L. (2006). Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro. Reproduction 131, 289–298.
| Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro.Crossref | GoogleScholarGoogle Scholar |
Hiraga, K., Hoshino, Y., Tanemura, K., and Sato, E. (2013). Selection of in vitro-matured porcine oocytes based on localization patterns of lipid droplets to evaluate developmental competence. J. Reprod. Dev. 59, 405–408.
| Selection of in vitro-matured porcine oocytes based on localization patterns of lipid droplets to evaluate developmental competence.Crossref | GoogleScholarGoogle Scholar |
Jimenez, P. T., Frolova, A. I., Chi, M. M., Grindler, N. M., Willcockson, A. R., Reynolds, K. A., Zhao, Q. H., and Moley, K. H. (2013). DHEA-mediated inhibition of the pentose phosphate pathway alters oocyte lipid metabolism in mice. Endocrinology 154, 4835–4844.
| DHEA-mediated inhibition of the pentose phosphate pathway alters oocyte lipid metabolism in mice.Crossref | GoogleScholarGoogle Scholar |
Kikuchi, K., Ekwall, H., Tienthai, P., Kawai, Y., Noguchi, J., Kaneko, H., and Rodriguez-Martinez, H. (2002). Morphological features of lipid droplet transition during porcine oocyte fertilisation and early embryonic development to blastocyst in vivo and in vitro. Zygote 10, 355–366.
| Morphological features of lipid droplet transition during porcine oocyte fertilisation and early embryonic development to blastocyst in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar |
Krisher, R. L. (2013). In vivo and in vitro environmental effects on mammalian oocyte quality. Annu. Rev. Anim. Biosci. 1, 393–417.
| In vivo and in vitro environmental effects on mammalian oocyte quality.Crossref | GoogleScholarGoogle Scholar |
Krisher, R. L., and Bavister, B. D. (1998). Responses of oocytes and embryos to the culture environment. Theriogenology 49, 103–114.
| Responses of oocytes and embryos to the culture environment.Crossref | GoogleScholarGoogle Scholar |
Krisher, R. L., Brad, A. M., Herrick, J. R., Sparman, M. L., and Swain, J. E. (2007). A comparative analysis of metabolism and viability in porcine oocytes during in vitro maturation. Anim. Reprod. Sci. 98, 72–96.
| A comparative analysis of metabolism and viability in porcine oocytes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar |
Lowe, J. L., Bartolac, L. K., Bathgate, R., and Grupen, C. G. (2017a). Cryotolerance of porcine blastocysts is improved by treating in vitro matured oocytes with l-carnitine prior to fertilization. J. Reprod. Dev. 63, 263–270.
| Cryotolerance of porcine blastocysts is improved by treating in vitro matured oocytes with l-carnitine prior to fertilization.Crossref | GoogleScholarGoogle Scholar |
Lowe, J. L., Bartolac, L. K., Bathgate, R., and Grupen, C. G. (2017b). Supplementation of culture medium with l-carnitine improves the development and cryotolerance of in vitro-produced porcine embryos. Reprod. Fertil. Dev. 29, 2357–2366.
| Supplementation of culture medium with l-carnitine improves the development and cryotolerance of in vitro-produced porcine embryos.Crossref | GoogleScholarGoogle Scholar |
Luciano, A. M., Modina, S., Vassena, R., Milanesi, E., Lauria, A., and Gandolfi, F. (2004). Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte-cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte. Biol. Reprod. 70, 465–472.
| Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte-cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte.Crossref | GoogleScholarGoogle Scholar |
McEvoy, T. G., Coull, G. D., Broadbent, P. J., Hutchinson, J. S. M., and Speake, B. K. (2000). Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J. Reprod. Fertil. 118, 163–170.
| Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida.Crossref | GoogleScholarGoogle Scholar |
Motlik, J., and Fulka, J. (1976). Breakdown of germinal vesicle in pig oocytes in vivo and in vitro. J. Exp. Zool. 198, 155–162.
| Breakdown of germinal vesicle in pig oocytes in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar |
Paczkowski, M., Silva, E., Schoolcraft, W. B., and Krisher, R. L. (2013). Comparative importance of fatty acid beta-oxidation to nuclear maturation, gene expression, and glucose metabolism in mouse, bovine, and porcine cumulus oocyte complexes. Biol. Reprod. 88, 111.
| Comparative importance of fatty acid beta-oxidation to nuclear maturation, gene expression, and glucose metabolism in mouse, bovine, and porcine cumulus oocyte complexes.Crossref | GoogleScholarGoogle Scholar |
Paczkowski, M., Schoolcraft, W. B., and Krisher, R. L. (2014). Fatty acid metabolism during maturation affects glucose uptake and is essential to oocyte competence. Reproduction 148, 429–439.
| Fatty acid metabolism during maturation affects glucose uptake and is essential to oocyte competence.Crossref | GoogleScholarGoogle Scholar |
Petters, R. M., and Wells, K. D. (1993). Culture of pig embryos. J. Reprod. Fertil. Suppl. 48, 61–73.
Qian, Y., Shi, W. Q., Ding, J. T., Sha, J. H., and Fan, B. Q. (2003). Predictive value of the area of expanded cumulus mass on development of porcine oocytes matured and fertilized in vitro. J. Reprod. Dev. 49, 167–174.
| Predictive value of the area of expanded cumulus mass on development of porcine oocytes matured and fertilized in vitro.Crossref | GoogleScholarGoogle Scholar |
Romek, M., Gajda, B., Krzysztofowicz, E., Kepczynski, M., and Smorag, Z. (2011). New technique to quantify the lipid composition of lipid droplets in porcine oocytes and pre-implantation embryos using Nile red fluorescent probe. Theriogenology 75, 42–54.
| New technique to quantify the lipid composition of lipid droplets in porcine oocytes and pre-implantation embryos using Nile red fluorescent probe.Crossref | GoogleScholarGoogle Scholar |
Somfai, T., Kikuchi, K., Onishi, A., Iwamoto, M., Fuchimoto, D., Papp, A. B., Sato, E., and Nagai, T. (2004). Relationship between the morphological changes of somatic compartment and the kinetics of nuclear and cytoplasmic maturation of oocytes during in vitro maturation of porcine follicular oocytes. Mol. Reprod. Dev. 68, 484–491.
| Relationship between the morphological changes of somatic compartment and the kinetics of nuclear and cytoplasmic maturation of oocytes during in vitro maturation of porcine follicular oocytes.Crossref | GoogleScholarGoogle Scholar |
Somfai, T., Kaneda, M., Akagi, S., Watanabe, S., Haraguchi, S., Mizutani, E., Dang-Nguyen, T. Q., Geshi, M., Kikuchi, K., and Nagai, T. (2011). Enhancement of lipid metabolism with l-carnitine during in vitro maturation improves nuclear maturation and cleavage ability of follicular porcine oocytes. Reprod. Fertil. Dev. 23, 912–920.
| Enhancement of lipid metabolism with l-carnitine during in vitro maturation improves nuclear maturation and cleavage ability of follicular porcine oocytes.Crossref | GoogleScholarGoogle Scholar |
Stojkovic, M., Machado, S. A., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Goncalves, P. B., and Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 64, 904–909.
| Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture.Crossref | GoogleScholarGoogle Scholar |
Sturmey, R. G., and Leese, H. J. (2003). Energy metabolism in pig oocytes and early embryos. Reproduction 126, 197–204.
| Energy metabolism in pig oocytes and early embryos.Crossref | GoogleScholarGoogle Scholar |
Sturmey, R. G., O’Toole, P. J., and Leese, H. J. (2006). Fluorescence resonance energy transfer analysis of mitochondrial: lipid association in the porcine oocyte. Reproduction 132, 829–837.
| Fluorescence resonance energy transfer analysis of mitochondrial: lipid association in the porcine oocyte.Crossref | GoogleScholarGoogle Scholar |
Sun, Q. Y., Wu, G. M., Lai, L., Park, K. W., Cabot, R., Cheong, H. T., Day, B. N., Prather, R. S., and Schatten, H. (2001). Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction 122, 155–163.
| Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro.Crossref | GoogleScholarGoogle Scholar |
Sutton, M. L., Cetica, P. D., Beconi, M. T., Kind, K. L., Gilchrist, R. B., and Thompson, J. G. (2003). Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes. Reproduction 126, 27–34.
| Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes.Crossref | GoogleScholarGoogle Scholar |
Sutton-McDowall, M. L., Gilchrist, R. B., and Thompson, J. G. (2010). The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 139, 685–695.
| The pivotal role of glucose metabolism in determining oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar |
Swain, J. E., Bormann, C. L., Clark, S. G., Walters, E. A., Wheeler, M. B., and Krisher, R. L. (2002). Use of energy substrates by various stage preimplantation pig embryos produced in vivo and in vitro. Reproduction 123, 253–260.
| Use of energy substrates by various stage preimplantation pig embryos produced in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar |
Tsuzuki, Y., Ugajin, M., and Ashizawa, K. (2008). Effect of adding glucose to maturation medium on the nuclear maturation and ATP content of porcine oocytes. J. Mamm. Ova Res. 25, 172–176.
| Effect of adding glucose to maturation medium on the nuclear maturation and ATP content of porcine oocytes.Crossref | GoogleScholarGoogle Scholar |
Tubman, L., Peter, A., and Krisher, R. (2005). Effect of energy substrates on metabolism, nuclear maturation, and development of gilt and sow oocytes during in vitro maturation. Reprod. Fertil. Dev. 17, 301.
| Effect of energy substrates on metabolism, nuclear maturation, and development of gilt and sow oocytes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar |
Van Blerkom, J., Davis, P. W., and Lee, J. (1995). ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo-transfer. Hum. Reprod. 10, 415–424.
| ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo-transfer.Crossref | GoogleScholarGoogle Scholar |
Vanderhyden, B. C., Caron, P. J., Buccione, R., and Eppig, J. J. (1990). Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev. Biol. 140, 307–317.
| Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation.Crossref | GoogleScholarGoogle Scholar |
Wang, Q., Chi, M. M., Schedl, T., and Moley, K. H. (2012). An intercellular pathway for glucose transport into mouse oocytes. Am. J. Physiol. Endocrinol. Metab. 302, E1511–E1518.
| An intercellular pathway for glucose transport into mouse oocytes.Crossref | GoogleScholarGoogle Scholar |
Wu, G. Q., Jia, B. Y., Li, J. J., Fu, X. W., Zhou, G. B., Hou, Y. P., and Zhu, S. E. (2011). l-Carnitine enhances oocyte maturation and development of parthenogenetic embryos in pigs. Theriogenology 76, 785–793.
| l-Carnitine enhances oocyte maturation and development of parthenogenetic embryos in pigs.Crossref | GoogleScholarGoogle Scholar |
Yoshioka, K., Suzuki, C., Tanaka, A., Anas, I. M. K., and Iwamura, S. (2002). Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol. Reprod. 66, 112–119.
| Birth of piglets derived from porcine zygotes cultured in a chemically defined medium.Crossref | GoogleScholarGoogle Scholar |
Yoshioka, K., Suzuki, C., and Onishi, A. (2008). Defined system for in vitro production of porcine embryos using a single basic medium. J. Reprod. Dev. 54, 208–213.
| Defined system for in vitro production of porcine embryos using a single basic medium.Crossref | GoogleScholarGoogle Scholar |
You, J., Lee, J., Hyun, S. H., and Lee, E. (2012). l-Carnitine treatment during oocyte maturation improves in vitro development of cloned pig embryos by influencing intracellular glutathione synthesis and embryonic gene expression. Theriogenology 78, 235–243.
| l-Carnitine treatment during oocyte maturation improves in vitro development of cloned pig embryos by influencing intracellular glutathione synthesis and embryonic gene expression.Crossref | GoogleScholarGoogle Scholar |