Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Expanded equine cumulus–oocyte complexes exhibit higher meiotic competence and lower glucose consumption than compact cumulus–oocyte complexes

L. González-Fernández A B , M. J. Sánchez-Calabuig C , M. G. Alves D , P. F. Oliveira D , S. Macedo A , A. Gutiérrez-Adán C , A. Rocha A and B. Macías-García A E F
+ Author Affiliations
- Author Affiliations

A Centro de Estudos de Ciência Animal/Instituto de Ciências, Tecnologias e Agroambiente; Instituto de Ciências Biomédicas Abel Salazar, University of Porto, Campus Agrario de Vairão, Rua Padre Armando Quintas, 4485-661 Vairão, Portugal.

B Research Group of Intracellular Signalling and Technology of Reproduction (SINTREP), School of Veterinary Medicine, University of Extremadura, Avda. de la universidad s/n, 10003, Cáceres, Spain.

C Department of Animal Reproduction, Instituto nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Ctra. De la Coruña, Km. 5.9, Madrid 28040, Spain.

D Department of Microscopy, Cell Biology Laboratory, Abel Salazar Institute of Biomedical Sciences and Unit for Multidisciplinary Research in Biomedicine (UMIB), University of Porto, Porto, Portugal.

E Assisted Reproduction Unit, Jesús Usón Minimally Invasive Surgery Centre (CCMIJU), Carretera N-521, km. 41,8. 10071, Cáceres, Spain.

F Corresponding author. Email: bea_macias@hotmail.com

Reproduction, Fertility and Development - https://doi.org/10.1071/RD16441
Submitted: 4 November 2016  Accepted: 6 June 2017   Published online: 6 July 2017

Abstract

Equine cumulus–oocyte complexes (COCs) are classified as compact (cCOC) or expanded (eCOC) and vary in their meiotic competence. This difference could be related to divergent glucose metabolism. To test this hypothesis in the present study, eCOCs, cCOCs and expanded or compact mural granulosa cells (EC and CC respectively) were matured in vitro for 30 h, at which time maturation rate, glucose metabolism and the expression of genes involved in glucose transport, glycolysis, apoptosis and meiotic competence were determined. There were significant differences between eCOCs and cCOCs in maturation rate (50% vs 21.7% (n = 192 and 46) respectively; P < 0.001), as well as mean (± s.e.m.) glucose consumption (1.8 ± 0.5 vs 27.9 ± 5.9 nmol per COC respectively) and pyruvate (0.09 ± 0.01 vs 2.4 ± 0.8 nmol per COC respectively) and lactate (4.7 ± 1.3 vs 64.1 ± 20.6 nmol per COC respectively; P < 0.05 for all) production. Glucose consumption in EC and CC did not differ significantly. Expression of hyaluronan-binding protein (tumour necrosis factor alpha induced protein 6; TNFAIP6) was increased in eCOCs and EC, and solute carrier family 2 member 1 (SLC2A1) expression was increased in eCOCs, but there were no differences in the expression of glycolysis-related enzymes and solute carrier family 2 member 3 (SLC2A3) between the COC or mural granulosa cell types. The findings of the present study demonstrate that metabolic and genomic differences exist between eCOCs and cCOCs and mural granulosa cells in the horse.

Additional keywords: glycolysis, horse, in vitro maturation, nuclear magnetic resonance.


References

Baumann, C. G., Morris, D. G., Sreenan, J. M., and Leese, H. J. (2007). The quiet embryo hypothesis: Molecular characteristics favoring viability. Mol. Reprod. Dev. 74, 1345–1353.
The quiet embryo hypothesis: Molecular characteristics favoring viability.CrossRef | 1:CAS:528:DC%2BD2sXhtVCmtr7O&md5=d37657a32a213fed86e7ee1fa9151e06CAS | open url image1

Bermejo-Álvarez, P., Rizos, D., Rath, D., Lonergan, P., and Gutierrez-Adan, A. (2008). Epigenetic differences between male and female bovine blastocysts produced in vitro. Physiol. Genomics 32, 264–272.
Epigenetic differences between male and female bovine blastocysts produced in vitro.CrossRef | open url image1

Billig, H., Hedin, L., and Magnusson, C. (1983). Gonadotrophins stimulate lactate production by rat cumulus and granulosa cells. Acta Endocrinol. (Copenh.) 103, 562–566.
| 1:CAS:528:DyaL3sXkvF2ks7c%3D&md5=e8868b62309c1f1b6b3233a812d5686aCAS | open url image1

Campos-Chillon, F., Farmerie, T. A., Bouma, G. J., Clay, C. M., and Carnevale, E. M. (2015). Effects of aging on gene expression and mitochondrial DNA in the equine oocyte and follicle cells. Reprod. Fertil. Dev. 27, 925–933.
Effects of aging on gene expression and mitochondrial DNA in the equine oocyte and follicle cells.CrossRef | 1:CAS:528:DC%2BC2MXhtFOlsbnI&md5=2d848f98603e5b1b7a398cb4374df2d0CAS | open url image1

Donahue, R. P., and Stern, S. (1968). Follicular cell support of oocyte maturation: production of pyruvate in vitro. J. Reprod. Fertil. 17, 395–398.
Follicular cell support of oocyte maturation: production of pyruvate in vitro.CrossRef | 1:STN:280:DyaF1M%2FlsFagtQ%3D%3D&md5=8824ea4ae0f0b6826fe5f4319666b48aCAS | open url image1

Downs, S. M. (2015). Nutrient pathways regulating the nuclear maturation of mammalian oocytes. Reprod. Fertil. Dev. 27, 572–582.
Nutrient pathways regulating the nuclear maturation of mammalian oocytes.CrossRef | 1:CAS:528:DC%2BC2MXntVWnur8%3D&md5=321f416bea1b8bfa2ac97281d41f6c66CAS | open url image1

Downs, S. M., and Hudson, E. D. (2000). Energy substrates and the completion of spontaneous meiotic maturation. Zygote 8, 339–351.
Energy substrates and the completion of spontaneous meiotic maturation.CrossRef | 1:CAS:528:DC%2BD3cXovF2hsbs%3D&md5=20100cbe7e274c1c9e1f2cc1318aa472CAS | open url image1

Downs, S. M., and Mastropolo, A. M. (1994). The participation of energy substrates in the control of meiotic maturation in murine oocytes. Dev. Biol. 162, 154–168.
The participation of energy substrates in the control of meiotic maturation in murine oocytes.CrossRef | 1:CAS:528:DyaK2cXhvVyitLs%3D&md5=db59e6664410352c975b6e9dbb80f877CAS | open url image1

Downs, S. M., Humpherson, P. G., Martin, K. L., and Leese, H. J. (1996). Glucose utilization during gonadotropin-induced meiotic maturation in cumulus cell-enclosed mouse oocytes. Mol. Reprod. Dev. 44, 121–131.
Glucose utilization during gonadotropin-induced meiotic maturation in cumulus cell-enclosed mouse oocytes.CrossRef | 1:CAS:528:DyaK28XivV2mt7g%3D&md5=f6d34b7b5a7c332b09d15124ad3ddd1fCAS | open url image1

Downs, S. M., Humpherson, P. G., and Leese, H. J. (2002). Pyruvate utilization by mouse oocytes is influenced by meiotic status and the cumulus oophorus. Mol. Reprod. Dev. 62, 113–123.
Pyruvate utilization by mouse oocytes is influenced by meiotic status and the cumulus oophorus.CrossRef | 1:CAS:528:DC%2BD38XivVChu7s%3D&md5=88695a0a59c0bb315144c866fdb15bd3CAS | open url image1

Fladeby, C., Skar, R., and Serck-Hanssen, G. (2003). Distinct regulation of glucose transport and GLUT1/GLUT3 transporters by glucose deprivation and IGF-I in chromaffin cells. Biochim. Biophys. Acta 1593, 201–208.
Distinct regulation of glucose transport and GLUT1/GLUT3 transporters by glucose deprivation and IGF-I in chromaffin cells.CrossRef | 1:CAS:528:DC%2BD3sXhtVGiu7s%3D&md5=172172927c4c33f4a83bc52b05f23051CAS | open url image1

Gandolfi, F., and Brevini, T. A. L. (2010). RFD Award Lecture 2009. In vitro maturation of farm animal oocytes: a useful tool for investigating the mechanisms leading to full-term development. Reprod. Fertil. Dev. 22, 495–507.
RFD Award Lecture 2009. In vitro maturation of farm animal oocytes: a useful tool for investigating the mechanisms leading to full-term development.CrossRef | open url image1

Gérard, N., Loiseau, S., Duchamp, G., and Seguin, F. (2002). Analysis of the variations of follicular fluid composition during follicular growth and maturation in the mare using proton nuclear magnetic resonance (1H NMR). Reproduction 124, 241–248.
Analysis of the variations of follicular fluid composition during follicular growth and maturation in the mare using proton nuclear magnetic resonance (1H NMR).CrossRef | open url image1

Gérard, N., Fahiminiya, S., Grupen, C. G., and Nadal-Desbarats, L. (2014). 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 | open url image1

Geshi, M., Takenouchi, N., Yamauchi, N., and Nagai, T. (2000). Effects of sodium pyruvate in nonserum maturation medium on maturation, fertilization, and subsequent development of bovine oocytes with or without cumulus cells. Biol. Reprod. 63, 1730–1734.
Effects of sodium pyruvate in nonserum maturation medium on maturation, fertilization, and subsequent development of bovine oocytes with or without cumulus cells.CrossRef | 1:CAS:528:DC%2BD3cXosVKht70%3D&md5=513cf59e8ec4db88e650b82f7e5635faCAS | open url image1

González-Fernández, L., Macedo, S., Lopes, J. S., Rocha, A., and Macías-García, B. (2015). Effect of different media and protein source on equine gametes: potential impact during in vitro fertilization. Reprod. Domest. Anim. 50, 1039–1046.
Effect of different media and protein source on equine gametes: potential impact during in vitro fertilization.CrossRef | open url image1

Han, Z. B., Lan, G. C., Wu, Y. G., Han, D., Feng, W. G., Wang, J. Z., and Tan, J. H. (2006). Interactive effects of granulosa cell apoptosis, follicle size, cumulus–oocyte complex morphology, and cumulus expansion on the developmental competence of goat oocytes: a study using the well-in-drop culture system. Reproduction 132, 749–758.
Interactive effects of granulosa cell apoptosis, follicle size, cumulus–oocyte complex morphology, and cumulus expansion on the developmental competence of goat oocytes: a study using the well-in-drop culture system.CrossRef | 1:CAS:528:DC%2BD28XhtlWktbrE&md5=e932b404870e77ea4322b5ad53c336b8CAS | open url image1

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 | 1:CAS:528:DC%2BD28XisFalsLs%3D&md5=8b4c6722af37fcd377f0866edbac01e0CAS | open url image1

Hinrichs, K. (2010a). The equine oocyte: factors affecting meiotic and developmental competence. Mol. Reprod. Dev. 77, 651–661.
The equine oocyte: factors affecting meiotic and developmental competence.CrossRef | 1:CAS:528:DC%2BC3cXptFGnsb8%3D&md5=3deb506ff4ff9e0021f025296d49d820CAS | open url image1

Hinrichs, K. (2010b). In vitro production of equine embryos: state of the art. Reprod. Domest. Anim. 45, 3–8.
In vitro production of equine embryos: state of the art.CrossRef | open url image1

Hinrichs, K., and Schmidt, A. L. (2000). Meiotic competence in horse oocytes: interactions among chromatin configuration, follicle size, cumulus morphology, and season. Biol. Reprod. 62, 1402–1408.
Meiotic competence in horse oocytes: interactions among chromatin configuration, follicle size, cumulus morphology, and season.CrossRef | 1:CAS:528:DC%2BD3cXisl2htbc%3D&md5=664f4152520d90c4b59b97629b66faa9CAS | open url image1

Hourvitz, A., Yerushalmi, G. M., Maman, E., Raanani, H., Elizur, S., Brengauz, M., Orvieto, R., Dor, J., and Meirow, D. (2015). Combination of ovarian tissue harvesting and immature oocyte collection for fertility preservation increases preservation yield. Reprod. Biomed. Online 31, 497–505.
Combination of ovarian tissue harvesting and immature oocyte collection for fertility preservation increases preservation yield.CrossRef | 1:CAS:528:DC%2BC2MXhtF2ks7%2FO&md5=fca27f9aa1b6024b62400a94fe551578CAS | open url image1

Janicot, M., and Lane, M. D. (1989). Activation of glucose uptake by insulin and insulin-like growth factor I in Xenopus oocytes. Proc. Natl Acad. Sci. USA 86, 2642–2646.
Activation of glucose uptake by insulin and insulin-like growth factor I in Xenopus oocytes.CrossRef | 1:CAS:528:DyaL1MXitVKhsLs%3D&md5=28bc1c5dc87202a157a9e796f8b8d73fCAS | open url image1

Johnson, M. T., Freeman, E. A., Gardner, D. K., and Hunt, P. A. (2007). Oxidative metabolism of pyruvate is required for meiotic maturation of murine oocytes in vivo. Biol. Reprod. 77, 2–8.
Oxidative metabolism of pyruvate is required for meiotic maturation of murine oocytes in vivo.CrossRef | 1:CAS:528:DC%2BD2sXntV2gsbw%3D&md5=1ec882fbd17f01f47f29057360d8c423CAS | open url image1

Keefe, D., Kumar, M., and Kalmbach, K. (2015). Oocyte competency is the key to embryo potential. Fertil. Steril. 103, 317–322.
Oocyte competency is the key to embryo potential.CrossRef | open url image1

Kidder, G. M., and Vanderhyden, B. C. (2010). Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence. Can. J. Physiol. Pharmacol. 88, 399–413.
Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence.CrossRef | 1:CAS:528:DC%2BC3cXlslCqsbY%3D&md5=8a3a63a15835d4dee9fd671a7ca2f01bCAS | open url image1

Kumar, P., Rajput, S., Verma, A., De, S., and Datta, T. K. (2013). Expression pattern of glucose metabolism genes in relation to development rate of buffalo (Bubalus bubalis) oocytes and in vitro-produced embryos. Theriogenology 80, 914–922.
Expression pattern of glucose metabolism genes in relation to development rate of buffalo (Bubalus bubalis) oocytes and in vitro-produced embryos.CrossRef | 1:CAS:528:DC%2BC3sXhtlCltLvK&md5=2554f401ee2e53bc00af60819592186eCAS | open url image1

Leese, H. J. (2002). Quiet please, do not disturb: a hypothesis of embryo metabolism and viability. BioEssays 24, 845–849.
Quiet please, do not disturb: a hypothesis of embryo metabolism and viability.CrossRef | open url image1

Len, J., McDowall, M., Anastasie, M., and Kleeman, D. (2016). Glucose uptake and lactate production of equine cumulus–oocyte complexes during in vitro maturation. J. Equine Vet. Sci. 41, 59. open url image1

Lewis, N., Hinrichs, K., Brison, D., Sturmey, R., Grove-White, D., Schnauffer, K., and McGregor-Argo, C. (2016). 184 Preliminary findings on carbohydrate metabolism of intact equine cumulus-oocyte complexes during in vitro maturation. Reprod. Fertil. Dev. 28, 223.
184 Preliminary findings on carbohydrate metabolism of intact equine cumulus-oocyte complexes during in vitro maturation.CrossRef | open url image1

Lin, Z. L., Li, Y. H., Xu, Y. N., Wang, Q. L., Namgoong, S., Cui, X. S., and Kim, N. H. (2014). Effects of growth differentiation factor 9 and bone morphogenetic protein 15 on the in vitro maturation of porcine oocytes. Reprod. Domest. Anim. 49, 219–227.
Effects of growth differentiation factor 9 and bone morphogenetic protein 15 on the in vitro maturation of porcine oocytes.CrossRef | 1:CAS:528:DC%2BC2cXktlKksb0%3D&md5=a46ce9f12b846421f00a3dfe13549498CAS | open url image1

Martino, N. A., Dell’Aquila, M. E., Filioli Uranio, M., Rutigliano, L., Nicassio, M., Lacalandra, G. M., and Hinrichs, K. (2014). Effect of holding equine oocytes in meiosis inhibitor-free medium before in vitro maturation and of holding temperature on meiotic suppression and mitochondrial energy/redox potential. Reprod. Biol. Endocrinol. 12, 99.
Effect of holding equine oocytes in meiosis inhibitor-free medium before in vitro maturation and of holding temperature on meiotic suppression and mitochondrial energy/redox potential.CrossRef | open url image1

Martins, A. D., Moreira, A. C., Sa, R., Monteiro, M. P., Sousa, M., Carvalho, R. A., Silva, B. M., Oliveira, P. F., and Alves, M. G. (2015). Leptin modulates human Sertoli cells acetate production and glycolytic profile: a novel mechanism of obesity-induced male infertility? Biochim. Biophys. Acta 1852, 1824–1832.
Leptin modulates human Sertoli cells acetate production and glycolytic profile: a novel mechanism of obesity-induced male infertility?CrossRef | 1:CAS:528:DC%2BC2MXhtVWru7fP&md5=ee9782665900867051329fd0c4b627beCAS | open url image1

Mohammadi-Sangcheshmeh, A., Held, E., Rings, F., Ghanem, N., Salilew-Wondim, D., Tesfaye, D., Sieme, H., Schellander, K., and Hoelker, M. (2014). Developmental competence of equine oocytes: impacts of zona pellucida birefringence and maternally derived transcript expression. Reprod. Fertil. Dev. 26, 441–452.
Developmental competence of equine oocytes: impacts of zona pellucida birefringence and maternally derived transcript expression.CrossRef | 1:CAS:528:DC%2BC2cXktlelt70%3D&md5=1bd0eb20f4935a57524514aa9ca76329CAS | open url image1

Nel-Themaat, L., and Nagy, Z. P. (2011). A review of the promises and pitfalls of oocyte and embryo metabolomics. Placenta 32, S257–S263.
A review of the promises and pitfalls of oocyte and embryo metabolomics.CrossRef | 1:CAS:528:DC%2BC3MXhtFSqsrrO&md5=e64ed018c90a9989f18274969c6e0c43CAS | open url image1

Nishimoto, H., Matsutani, R., Yamamoto, S., Takahashi, T., Hayashi, K.-G., Miyamoto, A., Hamano, S., and Tetsuka, M. (2006). Gene expression of glucose transporter (GLUT) 1, 3 and 4 in bovine follicle and corpus luteum. J. Endocrinol. 188, 111–119.
Gene expression of glucose transporter (GLUT) 1, 3 and 4 in bovine follicle and corpus luteum.CrossRef | 1:CAS:528:DC%2BD28XhtVCisL8%3D&md5=c067a3b1c896441a1c500a8f262bb116CAS | open url image1

Pincus, G., and Enzmann, E. V. (1935). The comparative behavior of mammalian eggs in vivo and in vitro: I. The activation of ovarian eggs. J. Exp. Med. 62, 665–675.
The comparative behavior of mammalian eggs in vivo and in vitro: I. The activation of ovarian eggs.CrossRef | 1:STN:280:DC%2BC3crjs1agtA%3D%3D&md5=08ff0b428aa8ffb6c73c047728f67284CAS | open url image1

Romar, R., De Santis, T., Papillier, P., Perreau, C., Thelie, A., Dell’Aquila, M. E., Mermillod, P., and Dalbies-Tran, R. (2011). Expression of maternal transcripts during bovine oocyte in vitro maturation is affected by donor age. Reprod. Domest. Anim. 46, e23–e30.
Expression of maternal transcripts during bovine oocyte in vitro maturation is affected by donor age.CrossRef | 1:STN:280:DC%2BC3M7itlOhuw%3D%3D&md5=5061efe6df283f78a560d2b455ba7a11CAS | open url image1

Sayasith, K., Dore, M., and Sirois, J. (2007). Molecular characterization of tumor necrosis alpha-induced protein 6 and its human chorionic gonadotropin-dependent induction in theca and mural granulosa cells of equine preovulatory follicles. Reproduction 133, 135–145.
Molecular characterization of tumor necrosis alpha-induced protein 6 and its human chorionic gonadotropin-dependent induction in theca and mural granulosa cells of equine preovulatory follicles.CrossRef | 1:CAS:528:DC%2BD2sXjs1aju7g%3D&md5=97cab268feea19c4ccf30696cca34ce4CAS | open url image1

Sayasith, K., Lussier, J., Doré, M., and Sirois, J. (2013). Human chorionic gonadotropin-dependent up-regulation of epiregulin and amphiregulin in equine and bovine follicles during the ovulatory process. Gen. Comp. Endocrinol. 180, 39–47.
Human chorionic gonadotropin-dependent up-regulation of epiregulin and amphiregulin in equine and bovine follicles during the ovulatory process.CrossRef | 1:CAS:528:DC%2BC38XhvV2rsbjM&md5=1a2c879535f0c184ffd87cfa9a1375f9CAS | open url image1

Scarlet, D., Ille, N., Ertl, R., Alves, B. G., Gastal, G. D. A., Paiva, S. O., Gastal, M. O., Gastal, E. L., and Aurich, C. (2017). Glucocorticoid metabolism in equine follicles and oocytes. Domest. Anim. Endocrinol. 59, 11–22.
Glucocorticoid metabolism in equine follicles and oocytes.CrossRef | 1:CAS:528:DC%2BC28XhvVarsr7P&md5=ab64fd1ecfd54d0b529978a70d2ad9e1CAS | open url image1

Schmittgen, T. D., and Livak, K. J. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101–1108.
Analyzing real-time PCR data by the comparative C(T) method.CrossRef | 1:CAS:528:DC%2BD1cXmvVemt7c%3D&md5=c158bd79247a48891822495d3f4249a2CAS | open url image1

Sessions-Bresnahan, D. R., and Carnevale, E. M. (2015). Age-associated changes in granulosa cell transcript abundance in equine preovulatory follicles. Reprod. Fertil. Dev. 27, 906–913.
Age-associated changes in granulosa cell transcript abundance in equine preovulatory follicles.CrossRef | 1:CAS:528:DC%2BC2MXhtFOlsbnJ&md5=0acec4c5653af25b6b408834e1726c14CAS | open url image1

Sessions-Bresnahan, D. R., Schauer, K. L., Heuberger, A. L., and Carnevale, E. M. (2016). Effect of obesity on the preovulatory follicle and lipid fingerprint of equine oocytes. Biol. Reprod. 94, 15.
Effect of obesity on the preovulatory follicle and lipid fingerprint of equine oocytes.CrossRef | open url image1

Singh, R., and Sinclair, K. D. (2007). Metabolomics: approaches to assessing oocyte and embryo quality. Theriogenology 68, S56–S62.
Metabolomics: approaches to assessing oocyte and embryo quality.CrossRef | 1:CAS:528:DC%2BD2sXotlaiuro%3D&md5=0f1f9272b1bfe78f2d3b7a0db86e0650CAS | open url image1

Songsasen, N., Spindler, R. E., and Wildt, D. E. (2007). Requirement for, and patterns of, pyruvate and glutamine metabolism in the domestic dog oocyte in vitro. Mol. Reprod. Dev. 74, 870–877.
Requirement for, and patterns of, pyruvate and glutamine metabolism in the domestic dog oocyte in vitro.CrossRef | 1:CAS:528:DC%2BD2sXmtlKlsbY%3D&md5=809bee5961740ed8701325e69b9a7e9fCAS | open url image1

Sugiura, K., Pendola, F. L., and Eppig, J. J. (2005). Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism. Dev. Biol. 279, 20–30.
Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism.CrossRef | 1:CAS:528:DC%2BD2MXhtlemtb4%3D&md5=278f468004c19e4f5270b95fbe877a44CAS | open url image1

Sutton, M. L., Gilchrist, R. B., and Thompson, J. G. (2003). Effects of in-vivo and in-vitro environments on the metabolism of the cumulus–oocyte complex and its influence on oocyte developmental capacity. Hum. Reprod. Update 9, 35–48.
Effects of in-vivo and in-vitro environments on the metabolism of the cumulus–oocyte complex and its influence on oocyte developmental capacity.CrossRef | 1:CAS:528:DC%2BD3sXjtVelt7Y%3D&md5=473ece3b9c541a7afa871571d18ed002CAS | open url image1

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 | 1:CAS:528:DC%2BC3cXltFajtr0%3D&md5=01128e9462420c39f1187a653b345471CAS | open url image1

Xie, H.-L., Wang, Y.-B., Jiao, G.-Z., Kong, D.-L., Li, Q., Li, H., Zheng, L.-L., and Tan, J.-H. (2016). Effects of glucose metabolism during in vitro maturation on cytoplasmic maturation of mouse oocytes. Sci. Rep. 6, 20764.
Effects of glucose metabolism during in vitro maturation on cytoplasmic maturation of mouse oocytes.CrossRef | 1:CAS:528:DC%2BC28XisVant7w%3D&md5=d2e4400cf6c95a6ae3a8f642df31850cCAS | open url image1

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 | 1:CAS:528:DC%2BC3MXhtValtbnE&md5=5c9e57352eac108b6278a4220225704dCAS | open url image1

Zheng, P., Vassena, R., and Latham, K. E. (2007). Effects of in vitro oocyte maturation and embryo culture on the expression of glucose transporters, glucose metabolism and insulin signaling genes in rhesus monkey oocytes and preimplantation embryos. Mol. Hum. Reprod. 13, 361–371.
Effects of in vitro oocyte maturation and embryo culture on the expression of glucose transporters, glucose metabolism and insulin signaling genes in rhesus monkey oocytes and preimplantation embryos.CrossRef | 1:CAS:528:DC%2BD2sXnvFCqu7s%3D&md5=80451d771772661570ead8837c953a4fCAS | open url image1



Supplementary MaterialSupplementary Material (175 KB) Export Citation

View Altmetrics