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

Expression profiles of select genes in cumulus–oocyte complexes from young and aged mares

Lindsay Cox A , Dirk K. Vanderwall A B , Kate C. Parkinson A , Alexis Sweat A and S. Clay Isom A
+ Author Affiliations
- Author Affiliations

A Department of Animal, Dairy and Veterinary Sciences, 4815 Old Main Hill, Utah State University, Logan, UT 84322-4815, USA.

B Corresponding author. Email: dirk.vanderwall@usu.edu

Reproduction, Fertility and Development 27(6) 914-924 https://doi.org/10.1071/RD14446
Submitted: 16 November 2014  Accepted: 17 April 2015   Published: 15 May 2015

Abstract

There is compelling evidence that oocytes from mares >18 years of age have a high incidence of inherent defects that result in early embryonic loss. In women, an age-related decrease in oocyte quality is associated with an increased incidence of aneuploidy and it has recently been determined that the gene expression profile of human oocytes is altered with advancing age. We hypothesised that similar age-related aberrations in gene expression occur in equine oocytes. Therefore, the aim of the present study was to compare gene expression profiles of individual oocytes and cumulus cells from young and aged mares, specifically evaluating genes that have been identified as being differentially expressed with advancing maternal age and/or aneuploidy in human oocytes. Expression of 48 genes was compared between 14 cumulus–oocyte complexes (COCs) from mares aged 3–12 years and 10 COCs from mares ≥18 years of age. Three genes (mitochondrial translational initiation factor 3 (IF3), heat shock transcription factor 5 (HSF5) and Y box binding protein 2 (YBX2)) were differentially expressed in oocytes, with all being more abundant in oocytes from young mares. Three genes (ADP-ribosylation factor-like 6 interacting protein 6 (ARL6IP6), BCL2-associated X protein (BAX) and hypoxia upregulated 1 (HYOU1)) were differentially expressed in cumulus cells, with all being more abundant in aged mares. The results of the present study confirm there are age-related differences in gene expression in equine COCs, which may be associated with the lower quality and decreased developmental competence of oocytes from aged mares.

Additional keyword: equine.


References

Al-Edani, T., Assou, S., Ferrières, A., Bringer Deutsch, S., Gala, A., Lecellier, C. H., Aït-Ahmed, O., and Hamamah, S. (2014). Female aging alters expression of human cumulus cells genes that are essential for oocyte quality. BioMed. Res. Int. 2014, 964614.
Female aging alters expression of human cumulus cells genes that are essential for oocyte quality.Crossref | GoogleScholarGoogle Scholar | 25276836PubMed |

Allen, W. R., Brown, L., Wright, M., and Wilsher, S. (2007). Reproductive efficiency of flatrace and national hunt thoroughbred mares and stallions in England. Equine Vet. J. 39, 438–445.
Reproductive efficiency of flatrace and national hunt thoroughbred mares and stallions in England.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2srovFyntA%3D%3D&md5=0d152f353e184f1d73221ddf392a21cbCAS | 17910269PubMed |

Applied Biosystems. (2004). ‘Guide to Performing Relative Quantitation of Gene Expression Using Real-Time Quantitative PCR.’ (Applied Biosystems: Foster City, CA.)

Arya, R., Mallik, M., and Lakhotia, S. C. (2007). Heat shock genes-integrating cell survival and death. J. Biosci. 32, 595–610.
Heat shock genes-integrating cell survival and death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFalsrs%3D&md5=d823a6e252619642e940b7de127a8f78CAS | 17536179PubMed |

Ball, B. A., Little, T. V., Hillman, R. B., and Woods, G. L. (1986). Pregnancy rates at Days 2 and 14 and estimated embryonic loss rates prior to Day 14 in normal and subfertile mares. Theriogenology 26, 611–619.
Pregnancy rates at Days 2 and 14 and estimated embryonic loss rates prior to Day 14 in normal and subfertile mares.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvV2qsQ%3D%3D&md5=2d0e9096b6743dd8e03f51fc83e08137CAS | 16726227PubMed |

Ball, B. A., Little, T. V., Weber, J. A., and Woods, G. L. (1989). Survival of Day-4 embryos from young, normal mares and aged, subfertile mares after transfer to normal recipient mares. J. Reprod. Fertil. 85, 187–194.
Survival of Day-4 embryos from young, normal mares and aged, subfertile mares after transfer to normal recipient mares.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M7isFCqsQ%3D%3D&md5=d13e755be6289e58a4c2554ff0ed42eaCAS | 2915352PubMed |

Battaglia, D. E., Goodwin, P., Klein, N. A., and Soules, M. R. (1996). Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum. Reprod. 11, 2217–2222.
Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s%2FpvV2itQ%3D%3D&md5=bc108b9e8bc1dda6d5897d8d627e1a12CAS | 8943533PubMed |

Boerjan, M. L., and de Boer, P. (1990). First cell cycle of zygotes of the mouse derived from oocytes aged postovulation in vivo and fertilized in vivo. Mol. Reprod. Dev. 25, 155–163.
First cell cycle of zygotes of the mouse derived from oocytes aged postovulation in vivo and fertilized in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhslantLY%3D&md5=b30fc150c31ba44fe259cb713ac54d59CAS | 2178641PubMed |

Brinsko, S. P., Ball, B. A., Miller, P. G., Thomas, P. G. A., and Ellington, J. E. (1994). In vitro development of Day 2 embryos obtained from young, fertile mares and aged, subfertile mares. J. Reprod. Fertil. 102, 371–378.
In vitro development of Day 2 embryos obtained from young, fertile mares and aged, subfertile mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjtFyns70%3D&md5=131e4d280580a57364b2f0e0f953c760CAS | 7861390PubMed |

Burton, A., Muller, J., Tu, S., Padilla-Longoria, P., Guccione, E., and Torres-Padilla, M. E. (2013). Single-cell profiling of epigenetic modifiers identifies PRDM14 as an inducer of cell fate in the mammalian embryo. Cell Reports 5, 687–701.
Single-cell profiling of epigenetic modifiers identifies PRDM14 as an inducer of cell fate in the mammalian embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslWmtr7P&md5=aa951de788959d2d9a99ad616d85768cCAS | 24183668PubMed |

Campos-Chillon, L. F., Clay, C. M., Altermatt, J. L., Bouma, G. J., and Carnevale, E. M. (2008). Differences in resumption of oocyte maturation in young and old mares. Reprod. Fertil. Dev. 20, 81.
Differences in resumption of oocyte maturation in young and old mares.Crossref | GoogleScholarGoogle Scholar |

Carnevale, E. M. (2008). The mare model for follicular maturation and reproductive aging in the woman. Theriogenology 69, 23–30.
The mare model for follicular maturation and reproductive aging in the woman.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVSmu7nN&md5=b1d730b243c0636c9f9498a2aecbc1f0CAS | 17976712PubMed |

Carnevale, E. M., and Ginther, O. J. (1992). Relationships of age to uterine function and reproductive efficiency in mares. Theriogenology 37, 1101–1115.
Relationships of age to uterine function and reproductive efficiency in mares.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvFyksw%3D%3D&md5=1d59d21e6ce65edf1bc2f7e3a516408aCAS | 16727108PubMed |

Carnevale, E. M., and Ginther, O. J. (1995). Defective oocytes as a cause of subfertility in old mares. Biol. Reprod. Monogr. 1, 209–214.

Carnevale, E. M., Bergfelt, D. R., and Ginther, O. J. (1993). Aging effects on follicular activity and concentrations of FSH, LH, and progesterone in mares. Anim. Reprod. Sci. 31, 287–299.
Aging effects on follicular activity and concentrations of FSH, LH, and progesterone in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltV2nsb0%3D&md5=447aae172b61b197d75fb8805cae2dfaCAS |

Carnevale, E. M., Maclellan, L. J., Ruggeri, E., and Albertini, D. F. (2012). Meiotic spindle configurations in metaphase II oocytes from young and old mares. J. Equine Vet. Sci. 32, 410–411.
Meiotic spindle configurations in metaphase II oocytes from young and old mares.Crossref | GoogleScholarGoogle Scholar |

Clanton, T. L. (2007). Hypoxia-induced reactive oxygen species formation in skeletal muscle. J. Appl. Physiol. 102, 2379–2388.
Hypoxia-induced reactive oxygen species formation in skeletal muscle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnsVKms7g%3D&md5=7e5514c3cc35c0843948224ce368467eCAS | 17289907PubMed |

Cummins, J. M. (2000). Mitochondrial dysfunction and ovarian aging. In: ‘Female Reproductive Aging’. (Eds E. R. te Velde, P. L. Pearson and F. J. Broekmans.) pp. 207–224. (The Parthenon Publishing Group: New York.)

Devonshire, A. S., Elaswarapu, R., and Foy, C. A. (2011). Applicability of RNA standards for evaluating RT-qPCR assays and platforms. BMC Genomics 12, 118.
Applicability of RNA standards for evaluating RT-qPCR assays and platforms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXivVensLg%3D&md5=f332bc996d17f4ae7d2858985442cf99CAS | 21332979PubMed |

Eichenlaub-Ritter, U., Wieczorek, M., Luke, S., and Seidel, T. (2011). Age related changes in mitochondrial function and new approaches to study redox regulation in mammalian oocytes in response to age or maturation conditions. Mitochondrion 11, 783–796.
Age related changes in mitochondrial function and new approaches to study redox regulation in mammalian oocytes in response to age or maturation conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVWrsr%2FF&md5=be81660b4e365615908ca88a3002ef97CAS | 20817047PubMed |

Ennen, M., Keime, C., Kobi, D., Mengus, G., Lipsker, D., Thibault-Carpentier, C., and Davidson, I. (2014). Single-cell gene expression signatures reveal melanoma cell heterogeneity. Oncogene 0, 18.

Fragouli, E., Bianchi, V., Patrizio, P., Obradors, A., Huang, Z., Borini, A., Delhanty, J. D., and Wells, D. (2010). Transcriptomic profiling of human oocytes: association of meiotic aneuploidy and altered oocyte gene expression. Mol. Hum. Reprod. 16, 570–582.
Transcriptomic profiling of human oocytes: association of meiotic aneuploidy and altered oocyte gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptlegt7g%3D&md5=ff74ce42a6c7cad608564e4140341751CAS | 20444854PubMed |

Franceschi, C., Monti, D., Cossarizza, A., Tomasi, A., Sola, P., and Zannotti, M. (1990). Oxidative stress, poly(ADP)ribosylation and aging: in vitro studies on lymphocytes from normal and Down’s syndrome subjects of different age and from patients with Alzheimer’s dementia. Adv. Exp. Med. Biol. 264, 499–502.
Oxidative stress, poly(ADP)ribosylation and aging: in vitro studies on lymphocytes from normal and Down’s syndrome subjects of different age and from patients with Alzheimer’s dementia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltFajtro%3D&md5=eadec271e0587b5583cffa10a1455e39CAS | 2173880PubMed |

Ginther, O. J. (2012). The mare: a 1000 pound guinea pig for study of the ovulatory follicular wave in women. Theriogenology 77, 818–828.
The mare: a 1000 pound guinea pig for study of the ovulatory follicular wave in women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivFOmtr0%3D&md5=70b0fd61b4e52fe96ad3b2cd47244b16CAS | 22115815PubMed |

Ginther, O. J., Carnevale, E. M., and Bergfelt, D. R. (1993). Delay in emergence of the ovulatory follicular wave in old mares. J. Equine Vet. Sci. 13, 75–79.
Delay in emergence of the ovulatory follicular wave in old mares.Crossref | GoogleScholarGoogle Scholar |

Grøndahl, M. L., Yding, A. C., Bogstad, J., Nielsen, F. C., Meinertz, H., and Borup, R. (2010). Gene expression profiles of single human mature oocytes in relation to age. Hum. Reprod. 25, 957–968.
Gene expression profiles of single human mature oocytes in relation to age.Crossref | GoogleScholarGoogle Scholar | 20147335PubMed |

Hamatani, T., Falco, G., Carter, M. G., Akutsu, H., Stagg, C. A., Sharov, A. A., Dudekula, D. B., VanBuren, V., and Ko, M. S. (2004). Age-associated alteration of gene expression patterns in mouse oocytes. Hum. Mol. Genet. 13, 2263–2278.
Age-associated alteration of gene expression patterns in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXns1Onu7k%3D&md5=7b188ed580c78f36aa6e957827fae7eaCAS | 15317747PubMed |

Hassold, T. J., and Jacobs, P. A. (1984). Trisomy in man. Annu. Rev. Genet. 18, 69–97.
Trisomy in man.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M7kslKhtQ%3D%3D&md5=5f8a7b09b8ecfed01753be52025e0853CAS | 6241455PubMed |

Hemberg, E., Lundeheim, N., and Einarsson, S. (2004). Reproductive performance of thoroughbred mares in Sweden. Reprod. Domest. Anim. 39, 81–85.
Reproductive performance of thoroughbred mares in Sweden.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c7ntlClsg%3D%3D&md5=71657391b60592b72ce327bce1665340CAS | 15065988PubMed |

Jasnos, L., and Sawado, T. (2014). Determining cell division symmetry through the dissection of dividing cells using single-cell expression analysis. Nat. Protoc. 9, 505–516.
Determining cell division symmetry through the dissection of dividing cells using single-cell expression analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVektrc%3D&md5=171326ea8ee0e0f3240ec1ae3c29b79fCAS | 24504476PubMed |

Jiao, Z. X., Xu, M., and Woodruff, T. K. (2012). Age-associated alteration of oocyte-specific gene expression in polar bodies: potential markers of oocyte competence. Fertil. Steril. 98, 480–486.
Age-associated alteration of oocyte-specific gene expression in polar bodies: potential markers of oocyte competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnslOjsLY%3D&md5=94d6f480fc29009e5863f27add8c40dfCAS | 22633262PubMed |

Kaneko, T., Saito, H., Takahashi, T., Ohta, N., Saito, T., and Hiroi, M. (2000). Effects of controlled ovarian hyperstimulation on oocyte quality in terms of the incidence of apoptotic granulosa cells. J. Assist. Reprod. Genet. 17, 580–585.
Effects of controlled ovarian hyperstimulation on oocyte quality in terms of the incidence of apoptotic granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M3jt1GmsA%3D%3D&md5=d4a2701ffaf8f67d8e036cc68fffdac1CAS | 11209539PubMed |

Keefe, D. L., Niven-Fairchild, T., Powell, S., and Buradagunta, S. (1995). Mitochondrial deoxyribonucleic acid deletions in oocytes and reproductive aging in women. Fertil. Steril. 64, 577–583.
| 1:STN:280:DyaK2MzmvFGjsA%3D%3D&md5=706b4e59c9aabb6963fdaee0690deb2fCAS | 7641914PubMed |

Lai, L., and Prather, R. S. (2003). Production of cloned pigs by using somatic cells as donor. Cloning Stem Cells 5, 233–241.
Production of cloned pigs by using somatic cells as donor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXislaqtw%3D%3D&md5=f3afc3c5476ac49108bca6d2378532f5CAS | 14733743PubMed |

Li, Y., Guo, X., Xue, Q., Zhu, M., Gao, L., and Wang, Y. (2013). Single cell gene profiling revealed heterogeneity of paracrine effects of bone marrow cells in mouse infarcted hearts. PLoS One 8, e68270.
Single cell gene profiling revealed heterogeneity of paracrine effects of bone marrow cells in mouse infarcted hearts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFOmtLrN&md5=0fd0edd36d62ac002845d025cdaaf466CAS | 23861876PubMed |

Lord, T., and Aitken, R. J. (2013). Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction 146, R217–R227.
Oxidative stress and ageing of the post-ovulatory oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFynt7zF&md5=601884617f1f560291118468a7c2f118CAS | 23950493PubMed |

Medvedev, S., Yang, J., Hecht, N. B., and Schultz, R. M. (2008). CDC2A (CDK1)-mediated phosphorylation of MSY2 triggers maternal mRNA degradation during mouse oocyte maturation. Dev. Biol. 321, 205–215.
CDC2A (CDK1)-mediated phosphorylation of MSY2 triggers maternal mRNA degradation during mouse oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVSgtLzE&md5=88ae64d68974a2024a1db879dcda62e4CAS | 18606161PubMed |

Medvedev, S., Pan, H., and Schultz, R. M. (2011). Absence of MSY2 in mouse oocytes perturbs oocyte growth and maturation, RNA stability, and the transcriptome. Biol. Reprod. 85, 575–583.
Absence of MSY2 in mouse oocytes perturbs oocyte growth and maturation, RNA stability, and the transcriptome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtV2gtLjL&md5=e0e9949f35a5f0cb2c3b727eda2c12a0CAS | 21613634PubMed |

Mohammadi-Sangcheshmeh, A., Held, E., Ghanem, N., Rings, F., Salilew-Wondim, D., Tesfaye, D., Sieme, H., Schellander, K., and Hoelker, M. (2011). G6PDH-activity in equine oocytes correlates with morphology, expression of candidate genes for viability, and preimplantative in vitro development. Theriogenology 76, 1215–1226.
G6PDH-activity in equine oocytes correlates with morphology, expression of candidate genes for viability, and preimplantative in vitro development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtF2htbbK&md5=b18dd4afa31996bdb84577b75f17aa0fCAS | 21820165PubMed |

Morel, M. C. G., Newcombe, J. R., and Swindlehurst, J. C. (2005). The effect of age on multiple ovulation rates, multiple pregnancy rates and embryonic vesicle diameter in the mare. Theriogenology 63, 2482–2493.
The effect of age on multiple ovulation rates, multiple pregnancy rates and embryonic vesicle diameter in the mare.Crossref | GoogleScholarGoogle Scholar |

Nakahara, K., Saito, H., Saito, T., Ito, M., Ohta, N., Takahashi, T., and Hiroi, M. (1997). The incidence of apoptotic bodies in membrana granulosa can predict prognosis of ova from patients participating in in vitro fertilization programs. Fertil. Steril. 68, 312–317.
The incidence of apoptotic bodies in membrana granulosa can predict prognosis of ova from patients participating in in vitro fertilization programs.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szosVGqtg%3D%3D&md5=8efb54302b6a4f51a46bbbc2db3b3ce0CAS | 9240262PubMed |

Pocar, P., Nestler, D., Risch, M., and Fischer, B. (2005). Apoptosis in bovine cumulus–oocyte complexes after exposure to polychlorinated biphenyl mixtures during in vitro maturation. Reproduction 130, 857–868.
Apoptosis in bovine cumulus–oocyte complexes after exposure to polychlorinated biphenyl mixtures during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xkt12ntA%3D%3D&md5=d3f2204f0a674775e01c4bf14565d363CAS | 16322545PubMed |

Rambags, B. P. B., Krijtenburg, P. J., Van Drie, H. F., Lazzari, G., Galli, C., Pearson, P. L., Colenbrander, B., and Stout, T. A. E. (2005). Numerical chromosomal abnormalities in equine embryos produced in vivo and in vitro. Mol. Reprod. Dev. 72, 77–87.
Numerical chromosomal abnormalities in equine embryos produced in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntlClsL4%3D&md5=1bef0fdd69e6a6a4d68533a79897d616CAS |

Russell, D. L., and Robker, R. L. (2007). Molecular mechanisms of ovulation: co-ordination through the cumulus complex. Hum. Reprod. Update 13, 289–312.
Molecular mechanisms of ovulation: co-ordination through the cumulus complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtlCisbc%3D&md5=1e06188007ef054c9e97ae3f7cf6eae2CAS | 17242016PubMed |

Saeed, A. I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T., Thiagarajan, M., Sturn, A., Snuffin, M., Rezantsev, A., Popov, D., Ryltsov, A., Kostukovich, E., Borisovsky, I., Liu, Z., Vinsavich, A., Trush, V., and Quackenbush, J. (2003). TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34, 374–378.
| 1:CAS:528:DC%2BD3sXhtlCiur4%3D&md5=68281ca0c4b61555d6307234aae094a1CAS | 12613259PubMed |

Schon, E. A., Kim, S. H., Ferreira, J. C., Magelhaes, P., Grace, M., Warburton, D., and Gross, S. J. (2000). Chromosomal non-disjunction in human oocytes: is there a mitochondrial connection? Hum. Reprod. 15, 160–172.
Chromosomal non-disjunction in human oocytes: is there a mitochondrial connection?Crossref | GoogleScholarGoogle Scholar | 11041522PubMed |

Shomper, M., Lappa, C., and FitzHarris, G. (2014). Kinetochore microtubule establishment is defective in oocytes from aged mice. Cell Cycle 13, 1171–1179.
Kinetochore microtubule establishment is defective in oocytes from aged mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFWgs7nF&md5=adf770823c0faa6837b57a87fe649420CAS | 24553117PubMed |

Takahashi, T., Takahashi, E., Igarashi, H., Tezuka, N., and Kurachi, H. (2003). Impact of oxidative stress in aged mouse oocytes on calcium oscillations at fertilization. Mol. Reprod. Dev. 66, 143–152.
Impact of oxidative stress in aged mouse oocytes on calcium oscillations at fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnt1Wntr4%3D&md5=f467fd5ca6d85dade8e475bdf6da0adeCAS | 12950101PubMed |

Tarín, J. J., Vendrell, F. J., Ten, J., and Cano, A. (1998). Antioxidant therapy counteracts the disturbing effects of diamide and maternal ageing on meiotic division and chromosomal segregation in mouse oocytes. Mol. Hum. Reprod. 4, 281–288.
Antioxidant therapy counteracts the disturbing effects of diamide and maternal ageing on meiotic division and chromosomal segregation in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 9570274PubMed |

Tatone, C., Di Emidio, G., Barbaro, R., Vento, M., Ciriminna, R., and Artini, P. G. (2011). Effects of reproductive aging and postovulatory aging on the maintenance of biological competence after oocyte vitrification: insights from the mouse model. Theriogenology 76, 864–873.
Effects of reproductive aging and postovulatory aging on the maintenance of biological competence after oocyte vitrification: insights from the mouse model.Crossref | GoogleScholarGoogle Scholar | 21705053PubMed |

Thouas, G. A., Trounson, A. O., and Jones, G. M. (2005). Effect of female age on mouse oocyte developmental competence following mitochondrial injury. Biol. Reprod. 73, 366–373.
Effect of female age on mouse oocyte developmental competence following mitochondrial injury.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXms1yqsLc%3D&md5=7b20deaa17050daf109217658fded419CAS | 15843494PubMed |

Van Blerkom, J., Antczak, M., and Schrader, R. (1997). The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: association with vascular endothelial growth factor levels and perifollicular blood flow characteristics. Hum. Reprod. 12, 1047–1055.
The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: association with vascular endothelial growth factor levels and perifollicular blood flow characteristics.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szjsl2qsQ%3D%3D&md5=4ea35fa1baad266c7c5bab053cb260b0CAS | 9194664PubMed |

Vanderwall, D. K. (2008). Early embryonic loss in the mare. J. Equine Vet. Sci. 28, 691–702.
Early embryonic loss in the mare.Crossref | GoogleScholarGoogle Scholar |

Vanderwall, D. K., Hyde, K. J., and Woods, G. L. (2006). Effect of repeated transvaginal ultrasound-guided follicle aspiration on fertility in mares. J. Am. Vet. Med. Assoc. 228, 248–250.
Effect of repeated transvaginal ultrasound-guided follicle aspiration on fertility in mares.Crossref | GoogleScholarGoogle Scholar | 16426200PubMed |

Vanderwall, D. K., Baumann, C., Viveiros, M., Sertich, P. L., Kelleman, A. A., Maenhoudt, C., Jacobson, C. C., and De La Fuente, R. (2010). Characterizing the meiotic spindle configuration and chromosome complement of in vivo matured equine oocytes. Anim. Reprod. Sci. 121S, S234–S236.

Vincent, J. J., Li, Z., Lee, S. A., Liu, X., Etter, M. O., Diaz-Perez, S. V., Taylor, S. K., Gkountela, S., Lindgren, A. G., and Clark, A. T. (2011). Single cell analysis facilitates staging of Blimp1-dependent primordial germ cells derived from mouse embryonic stem cells. PLoS One 6, e28960.
Single cell analysis facilitates staging of Blimp1-dependent primordial germ cells derived from mouse embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xis1Wrsw%3D%3D&md5=24abf5152025972adb550daf1436fd9aCAS | 22194959PubMed |

Vincent, J. J., Huang, Y., Chen, P. Y., Feng, S., Calvopiña, J. H., Nee, K., Lee, S. A., Le, T., Yoon, A. J., Faull, K., Fan, G., Rao, A., Jacobsen, S. E., Pellegrini, M., and Clark, A. T. (2013). Stage-specific roles for Tet1 and Tet2 in DNA demethylation in primordial germ cells. Cell Stem Cell 12, 470–478.
Stage-specific roles for Tet1 and Tet2 in DNA demethylation in primordial germ cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXis1Ontbo%3D&md5=f8ca7c90d47f7a56df75a1231c4a4f88CAS | 23415914PubMed |

Vogelsang, S. G., and Vogelsang, M. M. (1989). Influence of donor parity and age on the success of commercial equine embryo transfer. Equine Vet. J. Suppl. 8, 71–72.

Wang, Q., Frolova, A. I., Purcell, S., Adastra, K., Schoeller, E., Chi, M. M., Schedl, T., and Moley, K. H. (2010). Mitochondrial dysfunction and apoptosis in cumulus cells of type I diabetic mice. PLoS One 5, e15901.
Mitochondrial dysfunction and apoptosis in cumulus cells of type I diabetic mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlslyqtw%3D%3D&md5=bf25ee94c4bf7f703173fffaaa1aa080CAS | 21209947PubMed |

Westerheide, S. D., Raynes, R., Powell, C., Xue, B., and Uversky, V. N. (2012). HSF transcription factor family, heat shock response, and protein intrinsic disorder. Curr. Protein Pept. Sci. 13, 86–103.
| 1:CAS:528:DC%2BC38XkvFamtLo%3D&md5=d85e7e6ec3eaa522d1827eba2f3e8514CAS | 22044151PubMed |

Woods, G. L., Hillman, R. B., and Schlafer, D. H. (1986). Recovery and evaluation of embryos from normal and infertile mares. Cornell Vet. 76, 386–394.
| 1:STN:280:DyaL2s%2FgtlGmug%3D%3D&md5=016b5a0211fbc1cf487429def653cc28CAS | 3757521PubMed |

Woods, G. L., Baker, C. B., Baldwin, J. L., Ball, B. A., Bilinski, J., Cooper, W. L., Ley, W. B., Mank, E. C., and Erb, H. N. (1987). Early pregnancy loss in brood mares. J. Reprod. Fertil. Suppl 35, 455–459.

Woods, G. L., Weber, J. A., Vanderwall, D. K., and Freeman, D. A. (1991). Selective oviductal transport and fertilization rate of equine embryos. In ‘Proceedings of the 37th Annual Convention of the American Association of Equine Practitioners’. pp. 197–201. (American Association of Equine Practitioners: Lexington, KY.)

Wu, Y., Wang, X. L., Liu, J. H., Bao, Z. J., Tang, D. W., Wu, Y., and Zeng, S. M. (2011). BIM EL-mediated apoptosis in cumulus cells contributes to degenerative changes in aged porcine oocytes via a paracrine action. Theriogenology 76, 1487–1495.
BIM EL-mediated apoptosis in cumulus cells contributes to degenerative changes in aged porcine oocytes via a paracrine action.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht12isbnN&md5=378770dc56d54f7779ba158671648707CAS | 21835451PubMed |

Yoshida, M., Ishigaki, K., Nagai, T., Chikyu, M., and Pursel, V. G. (1993). Glutathione concentration during maturation and after fertilization in pig oocytes: relevance to the ability of oocytes to form male pronucleus. Biol. Reprod. 49, 89–94.
Glutathione concentration during maturation and after fertilization in pig oocytes: relevance to the ability of oocytes to form male pronucleus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXkvFahtLY%3D&md5=69d76b153ad02cec7e49e6cf85fe8b18CAS | 8353194PubMed |

Zheng, P., Patel, B., McMenamin, M., Moran, E., Paprocki, A. M., Kihara, M., Schramm, R. D., and Latham, K. E. (2005). Effects of follicle size and oocyte maturation conditions on maternal messenger RNA regulation and gene expression in Rhesus monkey oocytes and embryos. Biol. Reprod. 72, 890–897.
Effects of follicle size and oocyte maturation conditions on maternal messenger RNA regulation and gene expression in Rhesus monkey oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXis12hs7s%3D&md5=a0205b30a70a6533e23f7425b218dd5eCAS | 15590902PubMed |