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

Maternal age affects oocyte developmental potential at both ends of the age spectrum

Rebecca L. Krisher
+ Author Affiliations
- Author Affiliations

Colorado Center for Reproductive Medicine, 10290 RidgeGate Circle, Lone Tree, CO 80124, USA. Email: rkrisher@FLColo.com

Reproduction, Fertility and Development 31(1) 1-9 https://doi.org/10.1071/RD18340
Published online: 3 December 2018

Abstract

Maternal age has a significant effect on oocyte developmental competence. Overall, evidence suggests that oocytes from both prepubertal females and reproductively aged females are inherently less competent. Reduced oocyte quality in both age groups is problematic for human medicine and agriculture. Some of the cellular mechanisms implicated in poor oocyte quality associated with maternal age are mitochondrial function and location, reduction of oxygen radicals, balance of metabolic pathways, regulation of maternal mRNAs and appropriate communication between the oocyte and cumulus cells. However, additional knowledge must be gained about the deficiencies present in prepubertal and reproductively aged oocytes that result in poor developmental potential before significant improvement can be achieved. This review discusses the evidence currently available regarding oocyte quality at both ends of the maternal age spectrum, what we know, or hypothesise, about the mechanisms involved and current thoughts regarding potential treatment for improvement.

Additional keywords: aging, gene expression, mitochondria, oocyte quality, prepubertal.


References

Al-Edani, T., Assou, S., Ferrieres, A., Bringer Deutsch, S., Gala, A., Lecellier, C. H., Ait-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 |

Andux, S., and Ellis, R. E. (2008). Apoptosis maintains oocyte quality in aging Caenorhabditis elegans females. PLoS Genet. 4, e1000295.
Apoptosis maintains oocyte quality in aging Caenorhabditis elegans females.Crossref | GoogleScholarGoogle Scholar |

Armstrong, D. T. (2001). Effects of maternal age on oocyte developmental competence. Theriogenology 55, 1303–1322.
Effects of maternal age on oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar |

Baldassarre, H., Currin, L., Michalovic, L., Bellefleur, A. M., Gutierrez, K., Mondadori, R. G., Glanzner, W. G., Schuermann, Y., Bohrer, R. C., Dicks, N., Lopez, R., Grand, F. X., Vigneault, C., Blondin, P., Gourdon, J., and Bordignon, V. (2018). Interval of gonadotropin administration for in vitro embryo production from oocytes collected from Holstein calves between 2 and 6 months of age by repeated laparoscopy. Theriogenology 116, 64–70.
Interval of gonadotropin administration for in vitro embryo production from oocytes collected from Holstein calves between 2 and 6 months of age by repeated laparoscopy.Crossref | GoogleScholarGoogle Scholar |

Bartmann, A. K., Romao, G. S., da Silveira Ramos, E., and Ferriani, R. A. (2004). Why do older women have poor implantation rates? A possible role of mitochondria. J. Assist. Reprod. Genet. 21, 79–83.
Why do older women have poor implantation rates? A possible role of mitochondria.Crossref | GoogleScholarGoogle Scholar |

Ben-Meir, A., Burstein, E., Borrego-Alvarez, A., Chong, J., Wong, E., Yavorska, T., Naranian, T., Chi, M., Wang, Y., Bentov, Y., Alexis, J., Meriano, J., Sung, H. K., Gasser, D. L., Moley, K. H., Hekimi, S., Casper, R. F., and Jurisicova, A. (2015). Coenzyme Q10 restores oocyte mitochondrial function and fertility during reproductive aging. Aging Cell 14, 887–895.
Coenzyme Q10 restores oocyte mitochondrial function and fertility during reproductive aging.Crossref | GoogleScholarGoogle Scholar |

Benadiva, C. A., Kligman, I., and Munne, S. (1996). Aneuploidy 16 in human embryos increases significantly with maternal age. Fertil. Steril. 66, 248–255.
Aneuploidy 16 in human embryos increases significantly with maternal age.Crossref | GoogleScholarGoogle Scholar |

Bentov, Y., and Casper, R. F. (2013). The aging oocyte – can mitochondrial function be improved? Fertil. Steril. 99, 18–22.
The aging oocyte – can mitochondrial function be improved?Crossref | GoogleScholarGoogle Scholar |

Bentov, Y., Esfandiari, N., Burstein, E., and Casper, R. F. (2010). The use of mitochondrial nutrients to improve the outcome of infertility treatment in older patients. Fertil. Steril. 93, 272–275.
The use of mitochondrial nutrients to improve the outcome of infertility treatment in older patients.Crossref | GoogleScholarGoogle Scholar |

Bentov, Y., Yavorska, T., Esfandiari, N., Jurisicova, A., and Casper, R. F. (2011). The contribution of mitochondrial function to reproductive aging. J. Assist. Reprod. Genet. 28, 773–783.
The contribution of mitochondrial function to reproductive aging.Crossref | GoogleScholarGoogle Scholar |

Bentov, Y., Hannam, T., Jurisicova, A., Esfandiari, N., and Casper, R. F. (2014). Coenzyme Q10 supplementation and oocyte aneuploidy in women undergoing IVF-ICSI treatment. Clin. Med. Insights Reprod. Health 8, 31–36.
Coenzyme Q10 supplementation and oocyte aneuploidy in women undergoing IVF-ICSI treatment.Crossref | GoogleScholarGoogle Scholar |

Brevini-Gandolfi, T. A., Favetta, L. A., Mauri, L., Luciano, A. M., Cillo, F., and Gandolfi, F. (1999). Changes in poly(A) tail length of maternal transcripts during in vitro maturation of bovine oocytes and their relation with developmental competence. Mol. Reprod. Dev. 52, 427–433.
Changes in poly(A) tail length of maternal transcripts during in vitro maturation of bovine oocytes and their relation with developmental competence.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 |

Centers for Disease Control and Prevention, American Society for Reproductive Medicine, Society for Assisted Reproductive Technology (2015). Assisted reproductive technology national summary report. Atlanta (GA). US Department of Health and Human Services, Washington, D.C.

Chandra, A., Copen, C., and Stephen, E. (2013). ‘Infertility and Impaired Fecundity in the United States, 1982–2010: data from the National Survey of family growth.’ (National Center for Health Statistics: Hyattsville, MD.)

Chappel, S. (2013). The role of mitochondria from mature oocyte to viable blastocyst. Obstet. Gynecol. Int. 2013, 183024.
The role of mitochondria from mature oocyte to viable blastocyst.Crossref | GoogleScholarGoogle Scholar |

Cheng, J. M., Li, J., Tang, J. X., Hao, X. X., Wang, Z. P., Sun, T. C., Wang, X. X., Zhang, Y., Chen, S. R., and Liu, Y. X. (2017). Merotelic kinetochore attachment in oocyte meiosis II causes sister chromatids segregation errors in aged mice. Cell Cycle 16, 1404–1413.
Merotelic kinetochore attachment in oocyte meiosis II causes sister chromatids segregation errors in aged mice.Crossref | GoogleScholarGoogle Scholar |

Christopikou, D., Tsorva, E., Economou, K., Shelley, P., Davies, S., Mastrominas, M., and Handyside, A. H. (2013). Polar body analysis by array comparative genomic hybridization accurately predicts aneuploidies of maternal meiotic origin in cleavage stage embryos of women of advanced maternal age. Hum. Reprod. 28, 1426–1434.
Polar body analysis by array comparative genomic hybridization accurately predicts aneuploidies of maternal meiotic origin in cleavage stage embryos of women of advanced maternal age.Crossref | GoogleScholarGoogle Scholar |

Crosier, A. E., Comizzoli, P., Baker, T., Davidson, A., Munson, L., Howard, J., Marker, L. L., and Wildt, D. E. (2011). Increasing age influences uterine integrity, but not ovarian function or oocyte quality, in the cheetah (Acinonyx jubatus). Biol. Reprod. 85, 243–253.
Increasing age influences uterine integrity, but not ovarian function or oocyte quality, in the cheetah (Acinonyx jubatus).Crossref | GoogleScholarGoogle Scholar |

Currin, L., Michalovic, L., Bellefleur, A. M., Gutierrez, K., Glanzner, W., Schuermann, Y., Bohrer, R. C., Dicks, N., da Rosa, P. R., De Cesaro, M. P., Lopez, R., Grand, F. X., Vigneault, C., Blondin, P., Gourdon, J., Baldassarre, H., and Bordignon, V. (2017). The effect of age and length of gonadotropin stimulation on the in vitro embryo development of Holstein calf oocytes. Theriogenology 104, 87–93.
The effect of age and length of gonadotropin stimulation on the in vitro embryo development of Holstein calf oocytes.Crossref | GoogleScholarGoogle Scholar |

da Silveira, J. C., Veeramachaneni, D. N., Winger, Q. A., Carnevale, E. M., and Bouma, G. J. (2012). Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle. Biol. Reprod. 86, 71.
Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle.Crossref | GoogleScholarGoogle Scholar |

De La Fuente, R., and Eppig, J. J. (2001). Transcriptional activity of the mouse oocyte genome: companion granulosa cells modulate transcription and chromatin remodeling. Dev. Biol. 229, 224–236.
Transcriptional activity of the mouse oocyte genome: companion granulosa cells modulate transcription and chromatin remodeling.Crossref | GoogleScholarGoogle Scholar |

de Paz, P., Sánchez, A. J., De la Fuente, J., Chamorro, C. A., Alvarez, M., Anel, E., and Anel, L. (2001). Ultrastructural and cytochemical comparison between calf and cow oocytes. Theriogenology 55, 1107–1116.
Ultrastructural and cytochemical comparison between calf and cow oocytes.Crossref | GoogleScholarGoogle Scholar |

Dumollard, R., Duchen, M., and Carroll, J. (2007). The role of mitochondrial function in the oocyte and embryo. Curr. Top. Dev. Biol. 77, 21–49.
The role of mitochondrial function in the oocyte and embryo.Crossref | GoogleScholarGoogle Scholar |

Duncan, F. E., Chiang, T., Schultz, R. M., and Lampson, M. A. (2009). Evidence that a defective spindle assembly checkpoint is not the primary cause of maternal age-associated aneuploidy in mouse eggs. Biol. Reprod. 81, 768–776.
Evidence that a defective spindle assembly checkpoint is not the primary cause of maternal age-associated aneuploidy in mouse eggs.Crossref | GoogleScholarGoogle Scholar |

Eichenlaub-Ritter, U. (2012). Oocyte ageing and its cellular basis. Int. J. Dev. Biol. 56, 841–852.
Oocyte ageing and its cellular basis.Crossref | GoogleScholarGoogle Scholar |

Eichenlaub-Ritter, U., Vogt, E., Yin, H., and Gosden, R. (2004). Spindles, mitochondria and redox potential in ageing oocytes. Reprod. Biomed. Online 8, 45–58.
Spindles, mitochondria and redox potential in ageing oocytes.Crossref | GoogleScholarGoogle Scholar |

Eichenlaub-Ritter, U., Vogt, E., Yin, H., and Gosden, R. (2004). Spindles, mitochondria and redox potential in ageing oocytes. Reprod. Biomed. Online 8, 45–58.
Spindles, mitochondria and redox potential in ageing oocytes.Crossref | GoogleScholarGoogle Scholar |

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 |

Eppig, J. J., and Schroeder, A. C. (1989). Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biol. Reprod. 41, 268–276.
Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro.Crossref | GoogleScholarGoogle Scholar |

Eppig, J. J., Schultz, R. M., O’Brien, M., and Chesnel, F. (1994). Relationship between the developmental programs controlling nuclear and cytoplasmic maturation of mouse oocytes. Dev. Biol. 164, 1–9.
Relationship between the developmental programs controlling nuclear and cytoplasmic maturation of mouse oocytes.Crossref | GoogleScholarGoogle Scholar |

Eppig, J. J., Wigglesworth, K., and Pendola, F. L. (2002). The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc. Natl Acad. Sci. USA 99, 2890–2894.
The mammalian oocyte orchestrates the rate of ovarian follicular development.Crossref | GoogleScholarGoogle Scholar |

Fair, T., Hyttel, P., and Greve, T. (1995). Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol. Reprod. Dev. 42, 437–442.
Bovine oocyte diameter in relation to maturational competence and transcriptional activity.Crossref | GoogleScholarGoogle Scholar |

First, N. L., Leibfried-Rutledge, M. L., and Sirard, M. A. (1988). Cytoplasmic control of oocyte maturation and species differences in the development of maturational competence. Prog. Clin. Biol. Res. 267, 1–46.

Franasiak, J. M., Forman, E. J., Hong, K. H., Werner, M. D., Upham, K. M., Treff, N. R., and Scott, R. T. (2014a). Aneuploidy across individual chromosomes at the embryonic level in trophectoderm biopsies: changes with patient age and chromosome structure. J. Assist. Reprod. Genet. 31, 1501–1509.
Aneuploidy across individual chromosomes at the embryonic level in trophectoderm biopsies: changes with patient age and chromosome structure.Crossref | GoogleScholarGoogle Scholar |

Franasiak, J. M., Forman, E. J., Hong, K. H., Werner, M. D., Upham, K. M., Treff, N. R., and Scott, R. T. (2014b). The nature of aneuploidy with increasing age of the female partner: a review of 15,169 consecutive trophectoderm biopsies evaluated with comprehensive chromosomal screening. Fertil. Steril 101, 656–663e1.
The nature of aneuploidy with increasing age of the female partner: a review of 15,169 consecutive trophectoderm biopsies evaluated with comprehensive chromosomal screening.Crossref | GoogleScholarGoogle Scholar |

Fujino, Y., Ozaki, K., Yamamasu, S., Ito, F., Matsuoka, I., Hayashi, E., Nakamura, H., Ogita, S., Sato, E., and Inoue, M. (1996). DNA fragmentation of oocytes in aged mice. Hum. Reprod. 11, 1480–1483.
DNA fragmentation of oocytes in aged mice.Crossref | GoogleScholarGoogle Scholar |

Gandolfi, F., Milanesi, E., Pocar, P., Luciano, A. M., Brevini, T. A., Acocella, F., Lauria, A., and Armstrong, D. T. (1998). Comparative analysis of calf and cow oocytes during in vitro maturation. Mol. Reprod. Dev. 49, 168–175.
Comparative analysis of calf and cow oocytes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar |

Gandolfi, F., Vassena, R., and Lauria, A. (2000). The developmental competence of the oocyte before puberty: is something missing? Reprod. Domest. Anim. 35, 66–71.

Ge, Z. J., Schatten, H., Zhang, C. L., and Sun, Q. Y. (2015). Oocyte ageing and epigenetics. Reproduction 149, R103–R114.
Oocyte ageing and epigenetics.Crossref | GoogleScholarGoogle Scholar |

Ghaffarilaleh, V., Fouladi-Nashta, A., and Paramio, M. T. (2014). Effect of alpha-linolenic acid on oocyte maturation and embryo development of prepubertal sheep oocytes. Theriogenology 82, 686–696.
Effect of alpha-linolenic acid on oocyte maturation and embryo development of prepubertal sheep oocytes.Crossref | GoogleScholarGoogle Scholar |

Grondahl, M. L., Yding Andersen, 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 |

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 |

Gupta, M. K., Uhm, S. J., and Lee, H. T. (2007). Sexual maturity and reproductive phase of oocyte donor influence the developmental ability and apoptosis of cloned and parthenogenetic porcine embryos. Anim. Reprod. Sci. 108, 107–121.

Hammami, S., Morato, R., Romaguera, R., Roura, M., Catala, M. G., Paramio, M. T., Mogas, T., and Izquierdo, D. (2013). Developmental competence and embryo quality of small oocytes from pre-pubertal goats cultured in IVM medium supplemented with low level of hormones, insulin–transferrin–selenium and ascorbic acid. Reprod. Domest. Anim. 48, 339–344.
Developmental competence and embryo quality of small oocytes from pre-pubertal goats cultured in IVM medium supplemented with low level of hormones, insulin–transferrin–selenium and ascorbic acid.Crossref | GoogleScholarGoogle Scholar |

Herrick, J. R., Brad, A. M., Krisher, R. L., and Pope, W. F. (2003). Intracellular adenosine triphosphate and glutathione concentrations in oocytes from first estrous, multi-estrous, and testosterone-treated gilts. Anim. Reprod. Sci. 78, 123–131.
Intracellular adenosine triphosphate and glutathione concentrations in oocytes from first estrous, multi-estrous, and testosterone-treated gilts.Crossref | GoogleScholarGoogle Scholar |

Hodgman, R., Tay, J., Mendez, R., and Richter, J. D. (2001). CPEB phosphorylation and cytoplasmic polyadenylation are catalyzed by the kinase IAK1/Eg2 in maturing mouse oocytes. Development 128, 2815–2822.

Ito, M., Muraki, M., Takahashi, Y., Imai, M., Tsukui, T., Yamakawa, N., Nakagawa, K., Ohgi, S., Horikawa, T., Iwasaki, W., Iida, A., Nishi, Y., Yanase, T., Nawata, H., Miyado, K., Kono, T., Hosoi, Y., and Saito, H. (2008). Glutathione S-transferase theta 1 expressed in granulosa cells as a biomarker for oocyte quality in age-related infertility. Fertil. Steril. 90, 1026–1035.
Glutathione S-transferase theta 1 expressed in granulosa cells as a biomarker for oocyte quality in age-related infertility.Crossref | GoogleScholarGoogle Scholar |

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 | GoogleScholarGoogle Scholar |

Kauffold, J., Am, H. A., Bergfeld, U., Weber, W., and Sobiraj, A. (2005). The in vitro developmental competence of oocytes from juvenile calves is related to follicular diameter. J. Reprod. Dev. 51, 325–332.
The in vitro developmental competence of oocytes from juvenile calves is related to follicular diameter.Crossref | GoogleScholarGoogle Scholar |

Khatir, H., Lonergan, P., Carolan, C., and Mermillod, P. (1996). Prepubertal bovine oocyte: a negative model for studying oocyte developmental competence. Mol. Reprod. Dev. 45, 231–239.
Prepubertal bovine oocyte: a negative model for studying oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar |

Khatir, H., Lonergan, P., Touze, J. L., and Mermillod, P. (1998). The characterization of bovine embryos obtained from prepubertal calf oocytes and their viability after non surgical embryo transfer. Theriogenology 50, 1201–1210.
The characterization of bovine embryos obtained from prepubertal calf oocytes and their viability after non surgical embryo transfer.Crossref | GoogleScholarGoogle Scholar |

Lampinen, R., Vehvilainen-Julkunen, K., and Kankkunen, P. (2009). A review of pregnancy in women over 35 years of age. Open Nurs. J. 3, 33–38.
A review of pregnancy in women over 35 years of age.Crossref | GoogleScholarGoogle Scholar |

Lechniak, D., Warzych, E., Pers-Kamczyc, E., Sosnowski, J., Antosik, P., and Rubes, J. (2007). Gilts and sows produce similar rate of diploid oocytes in vitro whereas the incidence of aneuploidy differs significantly. Theriogenology 68, 755–762.
Gilts and sows produce similar rate of diploid oocytes in vitro whereas the incidence of aneuploidy differs significantly.Crossref | GoogleScholarGoogle Scholar |

Lee, M. S., Liu, C. H., Lee, T. H., Wu, H. M., Huang, C. C., Huang, L. S., Chen, C. M., and Cheng, E. H. (2010). Association of creatin kinase B and peroxiredoxin 2 expression with age and embryo quality in cumulus cells. J. Assist. Reprod. Genet. 27, 629–639.
Association of creatin kinase B and peroxiredoxin 2 expression with age and embryo quality in cumulus cells.Crossref | GoogleScholarGoogle Scholar |

Lehmann, P., Velez, M. P., Saumet, J., Lapensee, L., Jamal, W., Bissonnette, F., Phillips, S., and Kadoch, I. J. (2014). Anti-Mullerian hormone (AMH): a reliable biomarker of oocyte quality in IVF. J. Assist. Reprod. Genet. 31, 493–498.
Anti-Mullerian hormone (AMH): a reliable biomarker of oocyte quality in IVF.Crossref | GoogleScholarGoogle Scholar |

Leoni, G. G., Succu, S., Berlinguer, F., Rosati, I., Bebbere, D., Bogliolo, L., Ledda, S., and Naitana, S. (2006). Delay on the in vitro kinetic development of prepubertal ovine embryos. Anim. Reprod. Sci. 92, 373–383.
Delay on the in vitro kinetic development of prepubertal ovine embryos.Crossref | GoogleScholarGoogle Scholar |

Leoni, G. G., Bebbere, D., Succu, S., Berlinguer, F., Mossa, F., Galioto, M., Bogliolo, L., Ledda, S., and Naitana, S. (2007). Relations between relative mRNA abundance and developmental competence of ovine oocytes. Mol. Reprod. Dev. 74, 249–257.
Relations between relative mRNA abundance and developmental competence of ovine oocytes.Crossref | GoogleScholarGoogle Scholar |

Leoni, G. G., Succu, S., Satta, V., Paolo, M., Bogliolo, L., Bebbere, D., Spezzigu, A., Madeddu, M., Berlinguer, F., Ledda, S., and Naitana, S. (2009). In vitro production and cryotolerance of prepubertal and adult goat blastocysts obtained from oocytes collected by laparoscopic oocyte-pick-up (LOPU) after FSH treatment. Reprod. Fertil. Dev. 21, 901–908.
In vitro production and cryotolerance of prepubertal and adult goat blastocysts obtained from oocytes collected by laparoscopic oocyte-pick-up (LOPU) after FSH treatment.Crossref | GoogleScholarGoogle Scholar |

Lie Fong, S., Baart, E. B., Martini, E., Schipper, I., Visser, J. A., Themmen, A. P., de Jong, F. H., Fauser, B. J., and Laven, J. S. (2008). Anti-Mullerian hormone: a marker for oocyte quantity, oocyte quality and embryo quality? Reprod. Biomed. Online 16, 664–670.
Anti-Mullerian hormone: a marker for oocyte quantity, oocyte quality and embryo quality?Crossref | GoogleScholarGoogle Scholar |

Lonergan, P., and Fair, T. (2008). In vitro-produced bovine embryos: dealing with the warts. Theriogenology 69, 17–22.
In vitro-produced bovine embryos: dealing with the warts.Crossref | GoogleScholarGoogle Scholar |

Lonergan, P., Rizos, D., Gutierrez-Adan, A., Fair, T., and Boland, M. P. (2003). Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns. Reprod. Domest. Anim. 38, 259–267.
Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns.Crossref | GoogleScholarGoogle Scholar |

Marchal, R., Feugang, J. M., Perreau, C., Venturi, E., Terqui, M., and Mermillod, P. (2001). Meiotic and developmental competence of prepubertal and adult swine oocytes. Theriogenology 56, 17–29.
Meiotic and developmental competence of prepubertal and adult swine oocytes.Crossref | GoogleScholarGoogle Scholar |

Martin-Montalvo, A., and de Cabo, R. (2013). Mitochondrial metabolic reprogramming induced by calorie restriction. Antioxid. Redox Signal. 19, 310–320.
Mitochondrial metabolic reprogramming induced by calorie restriction.Crossref | GoogleScholarGoogle Scholar |

Masala, L., Ariu, F., Bogliolo, L., Bellu, E., Ledda, S., and Bebbere, D. (2018). Delay in maternal transcript degradation in ovine embryos derived from low competence oocytes. Mol. Reprod. Dev. 85, 427–439.
Delay in maternal transcript degradation in ovine embryos derived from low competence oocytes.Crossref | GoogleScholarGoogle Scholar |

Matthews, T. J., and Hamilton, B. E. (2014). First births to older women continue to rise. NCHS Data Brief 152, 1–8.

May-Panloup, P., Chretien, M. F., Jacques, C., Vasseur, C., Malthiery, Y., and Reynier, P. (2005). Low oocyte mitochondrial DNA content in ovarian insufficiency. Hum. Reprod. 20, 593–597.
Low oocyte mitochondrial DNA content in ovarian insufficiency.Crossref | GoogleScholarGoogle Scholar |

Meldrum, D. R., Casper, R. F., Diez-Juan, A., Simon, C., Domar, A. D., and Frydman, R. (2016). Aging and the environment affect gamete and embryo potential: can we intervene? Fertil. Steril. 105, 548–559.
Aging and the environment affect gamete and embryo potential: can we intervene?Crossref | GoogleScholarGoogle Scholar |

Moore, G. P., and Lintern-Moore, S. (1974). A correlation between growth and RNA synthesis in the mouse oocyte. J. Reprod. Fertil. 39, 163–166.
A correlation between growth and RNA synthesis in the mouse oocyte.Crossref | GoogleScholarGoogle Scholar |

Navot, D., Bergh, P. A., Williams, M. A., Garrisi, G. J., Guzman, I., Sandler, B., and Grunfeld, L. (1991). Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility. Lancet 337, 1375–1377.
Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility.Crossref | GoogleScholarGoogle Scholar |

O’Brien, J. K., Dwarte, D., Ryan, J. P., Maxwell, W. M. C., and Evans, G. (1996). Developmental capacity, energy metabolism and ultrastructure of mature oocytes from prepubertal and adult sheep. Reprod. Fertil. Dev. 8, 1029–1037.
Developmental capacity, energy metabolism and ultrastructure of mature oocytes from prepubertal and adult sheep.Crossref | GoogleScholarGoogle Scholar |

Paczkowski, M., and Krisher, R. (2010). Aberrant protein expression is associated with decreased developmental potential in porcine cumulus–oocyte complexes. Mol. Reprod. Dev. 77, 51–58.
Aberrant protein expression is associated with decreased developmental potential in porcine cumulus–oocyte complexes.Crossref | GoogleScholarGoogle Scholar |

Paczkowski, M., Yuan, Y., Fleming-Waddell, J., Bidwell, C. A., Spurlock, D., and Krisher, R. L. (2011). Alterations in the transcriptome of porcine oocytes derived from prepubertal and cyclic females is associated with developmental potential. J. Anim. Sci. 89, 3561–3571.
Alterations in the transcriptome of porcine oocytes derived from prepubertal and cyclic females is associated with developmental potential.Crossref | GoogleScholarGoogle Scholar |

Paczkowski, M., Schoolcraft, W. B., and Krisher, R. L. (2015). Dysregulation of methylation and expression of imprinted genes in oocytes and reproductive tissues in mice of advanced maternal age. J. Assist. Reprod. Genet. 32, 713–723.
Dysregulation of methylation and expression of imprinted genes in oocytes and reproductive tissues in mice of advanced maternal age.Crossref | GoogleScholarGoogle Scholar |

Palma, G. A., Tortonese, D. J., and Sinowatz, F. (2001). Developmental capacity in vitro of prepubertal oocytes. Anat. Histol. Embryol. 30, 295–300.
Developmental capacity in vitro of prepubertal oocytes.Crossref | GoogleScholarGoogle Scholar |

Park, S. S., Park, M. J., Joo, B. S., Joo, J. K., Son, J. B., and Lee, K. S. (2012). Improvement of ovarian response and oocyte quality of aged female by administration of bone morphogenetic protein-6 in a mouse model. Reprod. Biol. Endocrinol. 10, 117.

Patel, O. V., Bettegowda, A., Ireland, J. J., Coussens, P. M., Lonergan, P., and Smith, G. W. (2007). Functional genomics studies of oocyte competence: evidence that reduced transcript abundance for follistatin is associated with poor developmental competence of bovine oocytes. Reproduction 133, 95–106.
Functional genomics studies of oocyte competence: evidence that reduced transcript abundance for follistatin is associated with poor developmental competence of bovine oocytes.Crossref | GoogleScholarGoogle Scholar |

Patrizio, P., and Sakkas, D. (2009). From oocyte to baby: a clinical evaluation of the biological efficiency of in vitro fertilization. Fertil. Steril. 91, 1061–1066.
From oocyte to baby: a clinical evaluation of the biological efficiency of in vitro fertilization.Crossref | GoogleScholarGoogle Scholar |

Pawlak, P., Cieslak, A., Warzych, E., Zejden, Z., Szumacher-Strabel, M., Molinska-Glura, M., and Lechniak, D. (2012). No single way to explain cytoplasmic maturation of oocytes from prepubertal and cyclic gilts. Theriogenology 78, 2020–2030.
No single way to explain cytoplasmic maturation of oocytes from prepubertal and cyclic gilts.Crossref | GoogleScholarGoogle Scholar |

Pawlak, P., Warzych, E., Hryciuk, M., and Lechniak, D. (2015). Transcript abundance, glutathione and apoptosis levels differ between porcine oocytes collected from prepubertal and cyclic gilts. Theriogenology 84, 86–93.
Transcript abundance, glutathione and apoptosis levels differ between porcine oocytes collected from prepubertal and cyclic gilts.Crossref | GoogleScholarGoogle Scholar |

Pawlak, P., Chabowska, A., Malyszka, N., and Lechniak, D. (2016). Mitochondria and mitochondrial DNA in porcine oocytes and cumulus cells – a search for developmental competence marker. Mitochondrion 27, 48–55.
Mitochondria and mitochondrial DNA in porcine oocytes and cumulus cells – a search for developmental competence marker.Crossref | GoogleScholarGoogle Scholar |

Paynton, B. V., Rempel, R., and Bachvarova, R. (1988). Changes in state of adenylation and time course of degradation of maternal mRNAs during oocyte maturation and early embryonic development in the mouse. Dev. Biol. 129, 304–314.
Changes in state of adenylation and time course of degradation of maternal mRNAs during oocyte maturation and early embryonic development in the mouse.Crossref | GoogleScholarGoogle Scholar |

Pellestor, F., Andreo, B., Arnal, F., Humeau, C., and Demaille, J. (2003). Maternal aging and chromosomal abnormalities: new data drawn from in vitro unfertilized human oocytes. Hum. Genet. 112, 195–203.

Reader, K. L., Cox, N. R., Stanton, J. A., and Juengel, J. L. (2015). Mitochondria and vesicles differ between adult and prepubertal sheep oocytes during IVM. Reprod. Fertil. Dev. 27, 513–522.
Mitochondria and vesicles differ between adult and prepubertal sheep oocytes during IVM.Crossref | GoogleScholarGoogle Scholar |

Revel, F., Mermillod, P., Peynot, N., Renard, J. P., and Heyman, Y. (1995). Low developmental capacity of in vitro matured and fertilized oocytes from calves compared with that of cows. J. Reprod. Fertil. 103, 115–120.
Low developmental capacity of in vitro matured and fertilized oocytes from calves compared with that of cows.Crossref | GoogleScholarGoogle Scholar |

Reyes, J. M., Silva, E., Chitwood, J. L., Schoolcraft, W. B., Krisher, R. L., and Ross, P. J. (2017). Differing molecular response of young and advanced maternal age human oocytes to IVM. Hum. Reprod. 32, 2199–2208.
Differing molecular response of young and advanced maternal age human oocytes to IVM.Crossref | GoogleScholarGoogle Scholar |

Romaguera, R., Morato, R., Jimenez-Macedo, A. R., Catala, M., Roura, M., Paramio, M. T., Palomo, M. J., Mogas, T., and Izquierdo, D. (2010). Oocyte secreted factors improve embryo developmental competence of COCs from small follicles in prepubertal goats. Theriogenology 74, 1050–1059.
Oocyte secreted factors improve embryo developmental competence of COCs from small follicles in prepubertal goats.Crossref | GoogleScholarGoogle Scholar |

Salamone, D. F., Damiani, P., Fissore, R. A., Robl, J. M., and Duby, R. T. (2001). Biochemical and developmental evidence that ooplasmic maturation of prepubertal bovine oocytes is compromised. Biol. Reprod. 64, 1761–1768.
Biochemical and developmental evidence that ooplasmic maturation of prepubertal bovine oocytes is compromised.Crossref | GoogleScholarGoogle Scholar |

Sasaki, R., Nakayama, T., and Kato, T. (1999). Microelectrophoretic analysis of changes in protein expression patterns in mouse oocytes and preimplantation embryos. Biol. Reprod. 60, 1410–1418.
Microelectrophoretic analysis of changes in protein expression patterns in mouse oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar |

Schmidt, L., Sobotka, T., Bentzen, J. G., and Nyboe Andersen, A. (2012). Demographic and medical consequences of the postponement of parenthood. Hum. Reprod. Update 18, 29–43.
Demographic and medical consequences of the postponement of parenthood.Crossref | GoogleScholarGoogle Scholar |

Selesniemi, K., Lee, H. J., Muhlhauser, A., and Tilly, J. L. (2011). Prevention of maternal aging-associated oocyte aneuploidy and meiotic spindle defects in mice by dietary and genetic strategies. Proc. Natl Acad. Sci. USA 108, 12319–12324.
Prevention of maternal aging-associated oocyte aneuploidy and meiotic spindle defects in mice by dietary and genetic strategies.Crossref | GoogleScholarGoogle Scholar |

Sherrer, E. S., Rathbun, T. J., and Davis, D. L. (2004). Fertilization and blastocyst development in oocytes obtained from prepubertal and adult pigs. J. Anim. Sci. 82, 102–108.
Fertilization and blastocyst development in oocytes obtained from prepubertal and adult pigs.Crossref | GoogleScholarGoogle Scholar |

Simsek-Duran, F., Li, F., Ford, W., Swanson, R. J., Jones, H. W., and Castora, F. J. (2013). Age-associated metabolic and morphologic changes in mitochondria of individual mouse and hamster oocytes. PLoS One 8, e64955.
Age-associated metabolic and morphologic changes in mitochondria of individual mouse and hamster oocytes.Crossref | GoogleScholarGoogle Scholar |

Spricigo, J. F., Morato, R., Arcarons, N., Yeste, M., Dode, M. A., Lopez-Bejar, M., and Mogas, T. (2017). Assessment of the effect of adding l-carnitine and/or resveratrol to maturation medium before vitrification on in vitro-matured calf oocytes. Theriogenology 89, 47–57.
Assessment of the effect of adding l-carnitine and/or resveratrol to maturation medium before vitrification on in vitro-matured calf oocytes.Crossref | GoogleScholarGoogle Scholar |

Stebbins-Boaz, B., Hake, L. E., and Richter, J. D. (1996). CPEB controls the cytoplasmic polyadenylation of cyclin, Cdk2 and c-mos mRNAs and is necessary for oocyte maturation in Xenopus. EMBO J. 15, 2582–2592.

Steeves, T. E., and Gardner, D. K. (1999). Metabolism of glucose, pyruvate, and glutamine during the maturation of oocytes derived from pre-pubertal and adult cows. Mol. Reprod. Dev. 54, 92–101.
Metabolism of glucose, pyruvate, and glutamine during the maturation of oocytes derived from pre-pubertal and adult cows.Crossref | GoogleScholarGoogle Scholar |

Su, Y. Q., Sugiura, K., Woo, Y., Wigglesworth, K., Kamdar, S., Affourtit, J., and Eppig, J. J. (2007). Selective degradation of transcripts during meiotic maturation of mouse oocytes. Dev. Biol. 302, 104–117.
Selective degradation of transcripts during meiotic maturation of mouse oocytes.Crossref | GoogleScholarGoogle Scholar |

Takeuchi, T., Neri, Q. V., Katagiri, Y., Rosenwaks, Z., and Palermo, G. D. (2005). Effect of treating induced mitochondrial damage on embryonic development and epigenesis. Biol. Reprod. 72, 584–592.
Effect of treating induced mitochondrial damage on embryonic development and epigenesis.Crossref | GoogleScholarGoogle Scholar |

Tarin, J. J., Perez-Albala, S., and Cano, A. (2002). Oral antioxidants counteract the negative effects of female aging on oocyte quantity and quality in the mouse. Mol. Reprod. Dev. 61, 385–397.
Oral antioxidants counteract the negative effects of female aging on oocyte quantity and quality in the mouse.Crossref | GoogleScholarGoogle Scholar |

Thouas, G. A., Trounson, A. O., and Jones, G. M. (2006). Developmental effects of sublethal mitochondrial injury in mouse oocytes. Biol. Reprod. 74, 969–977.
Developmental effects of sublethal mitochondrial injury in mouse oocytes.Crossref | GoogleScholarGoogle Scholar |

Tilly, J. L., and Sinclair, D. A. (2013). Germline energetics, aging, and female infertility. Cell Metab. 17, 838–850.
Germline energetics, aging, and female infertility.Crossref | GoogleScholarGoogle Scholar |

Titus, S., Li, F., Stobezki, R., Akula, K., Unsal, E., Jeong, K., Dickler, M., Robson, M., Moy, F., Goswami, S., and Oktay, K. (2013). Impairment of BRCA1-related DNA double-strand break repair leads to ovarian aging in mice and humans. Sci. Transl. Med. 5, 172ra21.
Impairment of BRCA1-related DNA double-strand break repair leads to ovarian aging in mice and humans.Crossref | GoogleScholarGoogle Scholar |

Torres-Rovira, L., Gonzalez-Bulnes, A., Succu, S., Spezzigu, A., Manca, M. E., Leoni, G. G., Sanna, M., Pirino, S., Gallus, M., Naitana, S., and Berlinguer, F. (2014). Predictive value of antral follicle count and anti-Mullerian hormone for follicle and oocyte developmental competence during the early prepubertal period in a sheep model. Reprod. Fertil. Dev. 26, 1094–1106.
Predictive value of antral follicle count and anti-Mullerian hormone for follicle and oocyte developmental competence during the early prepubertal period in a sheep model.Crossref | GoogleScholarGoogle Scholar |

Van Blerkom, J. (1991). Microtubule mediation of cytoplasmic and nuclear maturation during the early stages of resumed meiosis in cultured mouse oocytes. Proc. Natl Acad. Sci. USA 88, 5031–5035.
Microtubule mediation of cytoplasmic and nuclear maturation during the early stages of resumed meiosis in cultured mouse oocytes.Crossref | GoogleScholarGoogle Scholar |

Van Blerkom, J. (2011). Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion 11, 797–813.
Mitochondrial function in the human oocyte and embryo and their role in developmental competence.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 |

Volarcik, K., Sheean, L., Goldfarb, J., Woods, L., Abdul-Karim, F. W., and Hunt, P. (1998). The meiotic competence of in-vitro matured human oocytes is influenced by donor age: evidence that folliculogenesis is compromised in the reproductively aged ovary. Hum. Reprod. 13, 154–160.
The meiotic competence of in-vitro matured human oocytes is influenced by donor age: evidence that folliculogenesis is compromised in the reproductively aged ovary.Crossref | GoogleScholarGoogle Scholar |

Wakai, T., Harada, Y., Miyado, K., and Kono, T. (2014). Mitochondrial dynamics controlled by mitofusins define organelle positioning and movement during mouse oocyte maturation. Mol. Hum. Reprod. 20, 1090–1100.
Mitochondrial dynamics controlled by mitofusins define organelle positioning and movement during mouse oocyte maturation.Crossref | GoogleScholarGoogle Scholar |

Warzych, E., Pawlak, P., Pszczola, M., Cieslak, A., and Lechniak, D. (2017). Prepubertal heifers versus cows – the differences in the follicular environment. Theriogenology 87, 36–47.
Prepubertal heifers versus cows – the differences in the follicular environment.Crossref | GoogleScholarGoogle Scholar |

Wilding, M., Dale, B., Marino, M., di Matteo, L., Alviggi, C., Pisaturo, M. L., Lombardi, L., and De Placido, G. (2001). Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum. Reprod. 16, 909–917.
Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar |

Wu, L. L., Russell, D. L., Wong, S. L., Chen, M., Tsai, T. S., St John, J. C., Norman, R. J., Febbraio, M. A., Carroll, J., and Robker, R. L. (2015). Mitochondrial dysfunction in oocytes of obese mothers: transmission to offspring and reversal by pharmacological endoplasmic reticulum stress inhibitors. Development 142, 681–691.
Mitochondrial dysfunction in oocytes of obese mothers: transmission to offspring and reversal by pharmacological endoplasmic reticulum stress inhibitors.Crossref | GoogleScholarGoogle Scholar |

Yamamoto, T., Iwata, H., Goto, H., Shiratuki, S., Tanaka, H., Monji, Y., and Kuwayama, T. (2010). Effect of maternal age on the developmental competence and progression of nuclear maturation in bovine oocytes. Mol. Reprod. Dev. 77, 595–604.
Effect of maternal age on the developmental competence and progression of nuclear maturation in bovine oocytes.Crossref | GoogleScholarGoogle Scholar |

Yamochi, T., Hashimoto, S., Amo, A., Goto, H., Yamanaka, M., Inoue, M., Nakaoka, Y., and Morimoto, Y. (2016). Mitochondrial dynamics and their intracellular traffic in porcine oocytes. Zygote 24, 517–528.
Mitochondrial dynamics and their intracellular traffic in porcine oocytes.Crossref | GoogleScholarGoogle Scholar |

Yu, Y., Dumollard, R., Rossbach, A., Lai, F. A., and Swann, K. (2010). Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J. Cell. Physiol. 224, 672–680.
Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation.Crossref | GoogleScholarGoogle Scholar |

Yuan, Y., Ida, J. M., Paczkowski, M., and Krisher, R. L. (2011). Identification of developmental competence-related genes in mature porcine oocytes. Mol. Reprod. Dev. 78, 565–575.
Identification of developmental competence-related genes in mature porcine oocytes.Crossref | GoogleScholarGoogle Scholar |

Yuan, Y., Wheeler, M. B., and Krisher, R. L. (2012). Disrupted redox homeostasis and aberrant redox gene expression in porcine oocytes contribute to decreased developmental competence. Biol. Reprod. 87, 78.
Disrupted redox homeostasis and aberrant redox gene expression in porcine oocytes contribute to decreased developmental competence.Crossref | GoogleScholarGoogle Scholar |

Zeng, H.-t., Ren, Z., Yeung, W. S. B., Shu, Y.-m., Xu, Y.-w., Zhuang, G.-l., and Liang, X.-Y. (2007). Low mitochondrial DNA and ATP contents contribute to the absence of birefringent spindle imaged with PolScope in in vitro matured human oocytes. Hum. Reprod. 22, 1681–1686.
Low mitochondrial DNA and ATP contents contribute to the absence of birefringent spindle imaged with PolScope in in vitro matured human oocytes.Crossref | GoogleScholarGoogle Scholar |

Zhang, X., Wu, X. Q., Lu, S., Guo, Y. L., and Ma, X. (2006). Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles. Cell Res. 16, 841–850.
Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles.Crossref | GoogleScholarGoogle Scholar |