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All that glitters is not gold: a stereological study of human donor oocytes

Published online by Cambridge University Press:  20 March 2023

Tânia Santos ,
Ana S. Pires-Luís ,
Ângela Alves ,
Elsa Oliveira ,
Carla Leal ,
Mónica Fernandes ,
Emídio Vale-Fernandes Open the ORCID record for Emídio Vale-Fernandes [Opens in a new window] ,
Márcia Barreiro ,
Ana-Margarida Calado  and
Rosália Sá
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Tânia Santos
Affiliation:
Laboratory of Cell Biology, Department of Microscopy, ICBAS-School of Medicine and Biomedical Sciences, University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal Department of Veterinarian Science, School of Veterinary and Agricultural Sciences (ECAV), CECAV – Interdisciplinary Research Center in Animal Health, Associated Laboratory for Animal and Veterinary Science (AL4AnimalS), University of Trás-os-Montes e Alto Douro (UTAD), Quinta de Prados, 5000–801 Vila Real, Portugal
Ana S. Pires-Luís
Affiliation:
Department of Pathology, Centro Hospitalar de Vila Nova de Gaia/Espinho, Unidade 1, Rua Conceição Fernandes 1079, 4434–502, Vila Nova de Gaia, Portugal Laboratory of Histology and Embryology, Department of Microscopy, ICBAS-School of Medicine and Biomedical Sciences, University of Porto
Ângela Alves
Affiliation:
Laboratory of Cell Biology, Department of Microscopy, ICBAS-School of Medicine and Biomedical Sciences, University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal UMIB-Unit for Multidisciplinary Research in Biomedicine/ITR-Laboratory for Integrative and Translational Research in Population Health, University of Porto, Porto, Portugal
Elsa Oliveira
Affiliation:
Laboratory of Cell Biology, Department of Microscopy, ICBAS-School of Medicine and Biomedical Sciences, University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal UMIB-Unit for Multidisciplinary Research in Biomedicine/ITR-Laboratory for Integrative and Translational Research in Population Health, University of Porto, Porto, Portugal
Carla Leal
Affiliation:
UMIB-Unit for Multidisciplinary Research in Biomedicine/ITR-Laboratory for Integrative and Translational Research in Population Health, University of Porto, Porto, Portugal Centro de Procriação Medicamente Assistida (CPMA), Centro Materno-Infantil do Norte (CMIN) Albino Aroso, Centro Hospitalar do Porto (CHUPorto), Largo da Maternidade de Júlio Dinis 45, 4050–651 Porto, Portugal
Mónica Fernandes
Affiliation:
UMIB-Unit for Multidisciplinary Research in Biomedicine/ITR-Laboratory for Integrative and Translational Research in Population Health, University of Porto, Porto, Portugal Centro de Procriação Medicamente Assistida (CPMA), Centro Materno-Infantil do Norte (CMIN) Albino Aroso, Centro Hospitalar do Porto (CHUPorto), Largo da Maternidade de Júlio Dinis 45, 4050–651 Porto, Portugal
Emídio Vale-Fernandes
Affiliation:
UMIB-Unit for Multidisciplinary Research in Biomedicine/ITR-Laboratory for Integrative and Translational Research in Population Health, University of Porto, Porto, Portugal Centro de Procriação Medicamente Assistida (CPMA), Centro Materno-Infantil do Norte (CMIN) Albino Aroso, Centro Hospitalar do Porto (CHUPorto), Largo da Maternidade de Júlio Dinis 45, 4050–651 Porto, Portugal
Márcia Barreiro
Affiliation:
UMIB-Unit for Multidisciplinary Research in Biomedicine/ITR-Laboratory for Integrative and Translational Research in Population Health, University of Porto, Porto, Portugal Centro de Procriação Medicamente Assistida (CPMA), Centro Materno-Infantil do Norte (CMIN) Albino Aroso, Centro Hospitalar do Porto (CHUPorto), Largo da Maternidade de Júlio Dinis 45, 4050–651 Porto, Portugal
Ana-Margarida Calado
Affiliation:
Department of Veterinarian Science, School of Veterinary and Agricultural Sciences (ECAV), CECAV – Interdisciplinary Research Center in Animal Health, Associated Laboratory for Animal and Veterinary Science (AL4AnimalS), University of Trás-os-Montes e Alto Douro (UTAD), Quinta de Prados, 5000–801 Vila Real, Portugal
Rosália Sá
Affiliation:
Laboratory of Cell Biology, Department of Microscopy, ICBAS-School of Medicine and Biomedical Sciences, University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal UMIB-Unit for Multidisciplinary Research in Biomedicine/ITR-Laboratory for Integrative and Translational Research in Population Health, University of Porto, Porto, Portugal
Mário Sousa*
Affiliation:
Laboratory of Cell Biology, Department of Microscopy, ICBAS-School of Medicine and Biomedical Sciences, University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal UMIB-Unit for Multidisciplinary Research in Biomedicine/ITR-Laboratory for Integrative and Translational Research in Population Health, University of Porto, Porto, Portugal
*
Author for correspondence: Mário Sousa. Laboratory of Cell Biology (Director), Department of Microscopy, ICBAS-School of Medicine and Biomedical Sciences, University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal. Tel: +91 9974476. E-mail: msousa@icbas.up.pt
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Summary

Here we report a quantitative analysis of human metaphase II (MII) oocytes from a 22-year-old oocyte donor, retrieved after ovarian-controlled hyperstimulation. Five surplus donor oocytes were processed for transmission electron microscopy (TEM), and a stereological analysis was used to quantify the distribution of organelles, using the point-counting technique with an adequate stereological grid. Comparisons between means of the relative volumes (Vv) occupied by organelles in the three oocyte regions, cortex (C), subcortex (SC) and inner cytoplasm (IC), followed the Kruskal–Wallis test and Mann–Whitney U-test with Bonferroni correction. Life cell imaging and TEM analysis confirmed donor oocyte nuclear maturity. Results showed that the most abundant organelles were smooth endoplasmic reticulum (SER) elements (26.8%) and mitochondria (5.49%). Significant differences between oocyte regions were found for lysosomes (P = 0.003), cortical vesicles (P = 0.002) and large SER vesicles (P = 0.009). These results were quantitatively compared with previous results using prophase I (GV) and metaphase I (MI) immature oocytes. In donor MII oocytes there was a normal presence of cortical vesicles, SER tubules, SER small, medium and large vesicles, lysosomes and mitochondria. However, donor MII oocytes displayed signs of cytoplasmic immaturity, namely the presence of dictyosomes, present in GV oocytes and rare in MI oocytes, of SER very large vesicles, characteristic of GV oocytes, and the rarity of SER tubular aggregates. Results therefore indicate that the criterion of nuclear maturity used for donor oocyte selection does not always correspond to cytoplasmic maturity, which can partially explain implantation failures with the use of donor oocytes.

Keywords

Human donor oocytesHuman oocytesOocyte organelle distributionStereologyUltrastructure

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Type
Research Article
Information
Zygote , Volume 31 , Issue 3 , June 2023 , pp. 253 - 265
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© The Author(s), 2023. Published by Cambridge University Press

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References

Arroyo, A., Kim, B. and Yeh, J. (2020). Luteinizing hormone action in human oocyte maturation and quality: Signaling pathways, regulation, and clinical impact. Reproductive Sciences, 27(6), 1223–1252. doi: 10.1007/s43032-019-00137-x CrossRefGoogle ScholarPubMed
Azevedo, A. R., Pinho, M. J., Silva, J., Sá, R., Thorsteinsdóttir, S., Barros, A. and Sousa, M. (2014). Molecular cytogenetics of human single pronucleated zygotes. Reproductive Sciences, 21(12), 1472–1482. doi: 10.1177/1933719114530185 CrossRefGoogle ScholarPubMed
Baca, M. and Zamboni, L. (1967). The fine structure of human follicular oocytes. Journal of Ultrastructure Research, 19(3), 354–381. doi: 10.1016/s0022-5320(67)80225-9 CrossRefGoogle ScholarPubMed
Braga, D. P. A. F., Setti, A. S., Figueira, R. C. S. F., Machado, R. B., Iaconelli, A. and Borges, E. (2013). Influence of oocyte dysmorphisms on blastocyst formation and quality. Fertility and Sterility, 100(3), 748–754. doi: 10.1016/j.fertnstert.2013.05.021 CrossRefGoogle ScholarPubMed
Braga, D. P. A. F., Zanetti, B. F., Setti, A. S., Iaconelli, A. and Borges, E. (2020). Immature oocyte incidence: Contributing factors and effects on mature sibling oocytes in intracytoplasmic sperm injection cycles. JBRA Assisted Reproduction, 24(1), 70–76. doi: 10.5935/1518-0557.20190056 Google ScholarPubMed
Canosa, S., Adriaenssens, T., Coucke, W., Dalmasso, P., Revelli, A., Benedetto, C. and Smitz, J. (2017). Zona pellucida gene mRNA expression in human oocytes is related to oocyte maturity, zona inner layer retardance and fertilization competence. Molecular Human Reproduction, 23(5), 292–303. doi: 10.1093/molehr/gax008 CrossRefGoogle ScholarPubMed
Cillo, F., Brevini, T. A. L., Antonini, S., Paffoni, A., Ragni, G. and Gandolfi, F. (2007). Association between human oocyte developmental competence and expression levels of some cumulus genes. Reproduction, 134(5), 645–650. doi: 10.1530/REP-07-0182 CrossRefGoogle ScholarPubMed
Coelho, S., Pires-Luís, A. S., Oliveira, E., Alves, Â., Leal, C., Cunha, M., Barreiro, M., Barros, A., Sá, R. and Sousa, M. (2020). Stereological study of organelle distribution in human oocytes at metaphase I. Zygote, 28(4), 308–317. doi: 10.1017/S0967199420000131 CrossRefGoogle ScholarPubMed
Conselho nacional de procriação medicamente assistida. (2018). Requisitos e parâmetros de funcionamento dos centros de PMA. Available from https://www.cnpma.org.pt/profissionais/Documents/Profissionais_Requisitos_CentrosPMA_2018_.pdf Google Scholar
Conti, M. and Franciosi, F. (2018). Acquisition of oocyte competence to develop as an embryo: Integrated nuclear and cytoplasmic events. Human Reproduction Update, 24(3), 245–266. doi: 10.1093/humupd/dmx040 CrossRefGoogle ScholarPubMed
Cornet-Bartolomé, D., Barragán, M., Zambelli, F., Ferrer-Vaquer, A., Tiscornia, G., Balcells, S., Rodriguez, A., Grinberg, D. and Vassena, R. (2021). Human oocyte meiotic maturation is associated with a specific profile of alternatively spliced transcript isoforms. Molecular Reproduction and Development, 88(9), 605–617. doi: 10.1002/mrd.23526 CrossRefGoogle ScholarPubMed
Coticchio, G., Dal Canto, M., Mignini Renzini, M. M., Guglielmo, M. C., Brambillasca, F., Turchi, D., Novara, P. V. and Fadini, R. (2015). Oocyte maturation: Gamete-somatic cells interactions, meiotic resumption, cytoskeletal dynamics and cytoplasmic reorganization. Human Reproduction Update, 21(4), 427–454. doi: 10.1093/humupd/dmv011 CrossRefGoogle ScholarPubMed
Coticchio, G., Ophir, L., Yung, Y., Baum, M., Dal Canto, M., Mignini-Renzini, M., Brambillasca, F., Fadini, R. and Hourvitz, A. (2017). Differential regulation of cumulus cell transcription during oocyte maturation in vivo and in vitro . International Journal of Developmental Biology, 61(6–7), 433–437. doi: 10.1387/ijdb.160364gc CrossRefGoogle ScholarPubMed
Dale, B., Wilding, M., Coppola, G. and Tosti, E. (2010). How do spermatozoa activate oocytes? Reproductive Biomedicine Online, 21(1), 1–3. doi: 10.1016/j.rbmo.2010.02.015 CrossRefGoogle ScholarPubMed
De Vos, M., Grynberg, M., Ho, T. M., Yuan, Y., Albertini, D. F. and Gilchrist, R. B. (2021). Perspectives on the development and future of oocyte IVM in clinical practice. Journal of Assisted Reproduction and Genetics, 38(6), 1265–1280. doi: 10.1007/s10815-021-02263-5 CrossRefGoogle ScholarPubMed
Dumesic, D. A., Meldrum, D. R., Katz-Jaffe, M. G., Krisher, R. L. and Schoolcraft, W. B. (2015). Oocyte environment: Follicular fluid and cumulus cells are critical for oocyte health. Fertility and Sterility, 103(2), 303–316. doi: 10.1016/j.fertnstert.2014.11.015 CrossRefGoogle ScholarPubMed
Ebner, T., Moser, M., Sommergruber, M. and Tews, G. (2003). Selection based on morphological assessment of oocytes and embryos at different stages of preimplantation development: A review. Human Reproduction Update, 9(3), 251–262. doi: 10.1093/humupd/dmg021 CrossRefGoogle ScholarPubMed
Ebner, T., Moser, M. and Tews, G. (2006). Is oocyte morphology prognostic of embryo developmental potential after ICSI? Reproductive Biomedicine Online, 12(4), 507–512. doi: 10.1016/s1472-6483(10)62006-8 CrossRefGoogle ScholarPubMed
El-Shafie, M., Windt, M.-L., Kitshoff, M., McGregor, P., Sousa, M., Wranz, P. A. B. and Kruger, T. F. (2000). Ultrastructure of human oocytes: a transmission electron microscopy view. In: El-Shafie, M., Sousa, M. and Kruger, T. F. (eds). An Atlas of the Ultrastructure of Human Oocytes: A Guide for Assisted Reproduction. The Parthenon Publishing Group, NY, USA. pp. 82–173.Google Scholar
Eppig, J. J. (1996). Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reproduction, Fertility, and Development, 8(4), 485–489. doi: 10.1071/RD9960485 CrossRefGoogle ScholarPubMed
European IVF-Monitoring Consortium (EIM) for the European Society of Human Reproduction and Embryology (ESHRE), Wyns, C., De Geyter, C., Calhaz-Jorge, C., Kupka, M. S., Motrenko, T., Smeenk, J., Bergh, C., Tandler-Schneider, A., Rugescu, I. A., Vidakovic, S. and Goossens, V. (2021). ART in Europe, 2017: Results generated from European registries by ESHRE. Human Reproduction Open, 2021(3), hoab026. doi: 10.1093/hropen/hoab026 CrossRefGoogle Scholar
Familiari, G., Heyn, R., Relucenti, M., Nottola, S. A. and Sathananthan, A. H. (2006). Ultrastructural dynamics of human reproduction, from ovulation to fertilization and early embryo development. International Review of Cytology, 249, 53–141. doi: 10.1016/S0074-7696(06)49002-1 CrossRefGoogle ScholarPubMed
Gasca, S., Pellestor, F., Assou, S., Loup, V., Anahory, T., Dechaud, H., De Vos, J. and Hamamah, S. (2007). Identifying new human oocyte marker genes: A microarray approach. Reproductive Biomedicine Online, 14(2), 175–183. doi: 10.1016/s1472-6483(10)60785-7 CrossRefGoogle Scholar
Hinduja, I. N., Kumar, A. and Anand Kumar, T. C. (1990). Ultrastructure of the cortex in the human egg. Human Reproduction, 5(1), 66–70. doi: 10.1093/oxfordjournals.humrep.a137043 CrossRefGoogle ScholarPubMed
Huirne, J. A., Homburg, R. and Lambalk, C. B. (2007). Are GnRH antagonists comparable to agonists for use in IVF? Human Reproduction, 22(11), 2805–2813. doi: 10.1093/humrep/dem270 CrossRefGoogle ScholarPubMed
Karavani, G., Wasserzug-Pash, P., Mordechai-Daniel, T., Bauman, D., Klutstein, M. and Imbar, T. (2021). Age-dependent in vitro maturation efficacy of human oocytes – Is there an optimal age? Frontiers in Cell and Developmental Biology, 9, 667682. doi: 10.3389/fcell.2021.667682 CrossRefGoogle ScholarPubMed
Mao, L., Lou, H., Lou, Y., Wang, N. and Jin, F. (2014). Behaviour of cytoplasmic organelles and cytoskeleton during oocyte maturation. Reproductive Biomedicine Online, 28(3), 284–299. doi: 10.1016/j.rbmo.2013.10.016 CrossRefGoogle ScholarPubMed
May-Panloup, P., Boucret, L., Chao de la Barca, J. M., Desquiret-Dumas, V., Ferré-L’Hotellier, V., Morinière, C., Descamps, P., Procaccio, V. and Reynier, P. (2016). Ovarian ageing: The role of mitochondria in oocytes and follicles. Human Reproduction Update, 22(6), 725–743. doi: 10.1093/humupd/dmw028 CrossRefGoogle ScholarPubMed
Morimoto, Y. (2009). Ultrastructure of the human oocytes during in vitro maturation. Journal of Mammalian Ova Research, 26(1), 10–17. https://doi.otg/40.1274/jmor.26.10. doi: 10.1274/jmor.26.10 CrossRefGoogle Scholar
Motta, P. M., Nottola, S. A., Makabe, S., Heyn, R. and Jansen, R. (2000). Mitochondrial morphology in human fetal and adult female germ cells. Human Reproduction, 15 (Suppl. 2), 129–147. doi: 10.1093/humrep/15.suppl_2.129 CrossRefGoogle ScholarPubMed
Motta, P. M., Nottola, S. A., Micara, G. and Familiari, G. (1988). Ultrastructure of human unfertilized oocytes and polyspermic embryos in an IVF-ET program. Annals of the New York Academy of Sciences, 541, 367–383. doi: 10.1111/j.1749-6632.1988.tb22274.x CrossRefGoogle Scholar
Nottola, S. A., Macchiarelli, G. and Familiari, G. (2014). Fine structural markers of human oocyte quality in assisted reproduction. Austin Journal of Reproductive Medicine and Infertility, 1(1), 5. Available at https://austinpublishinggroup.com/reproductive-medicine/fulltext/ajrm-v1-id1002.pdf Google Scholar
Ouandaogo, Z. G., Frydman, N., Hesters, L., Assou, S., Haouzi, D., Dechaud, H., Frydman, R. and Hamamah, S. (2012). Differences in transcriptomic profiles of human cumulus cells isolated from oocytes at GV, MI and MII stages after in vivo and in vitro oocyte maturation. Human Reproduction, 27(8), 2438–2447. doi: 10.1093/humrep/des172 CrossRefGoogle ScholarPubMed
Ozturk, S. (2020). Selection of competent oocytes by morphological criteria for assisted reproductive technologies. Molecular Reproduction and Development, 87(10), 1021–1036. doi: 10.1002/mrd.23420 CrossRefGoogle ScholarPubMed
Pinto, F., Oliveira, C., Cardoso, M. F., Teixeira-da-Silva, J., Silva, J., Sousa, M. and Barros, A. (2009). Impact of GnRH ovarian stimulation protocols on intracytoplasmic sperm injection outcomes. Reproductive Biology and Endocrinology: RB&E, 7, 5. doi: 10.1186/1477-7827-7-5 CrossRefGoogle ScholarPubMed
Pires-Luís, A. S., Rocha, E., Bartosch, C., Oliveira, E., Silva, J., Barros, A., Sá, R. and Sousa, M. (2016). A stereological study on organelle distribution in human oocytes at prophase I. Zygote, 24(3), 346–354. doi: 10.1017/S0967199415000258 CrossRefGoogle Scholar
Reader, K. L., Stanton, J. L. and Juengel, J. L. (2017). The role of oocyte organelles in determining developmental competence. Biology, 6(3), 35. doi: 10.3390/biology6030035 CrossRefGoogle ScholarPubMed
Richani, D. and Gilchrist, R. B. (2018). The epidermal growth factor network: Role in oocyte growth, maturation and developmental competence. Human Reproduction Update, 24(1), 1–14. doi: 10.1093/humupd/dmx029 CrossRefGoogle ScholarPubMed
Rienzi, L., Vajta, G. and Ubaldi, F. (2011). Predictive value of oocyte morphology in human IVF: A systematic review of the literature. Human Reproduction Update, 17(1), 34–45. doi: 10.1093/humupd/dmq029 CrossRefGoogle ScholarPubMed
Sá, R., Cunha, M., Silva, J., Luís, A., Oliveira, C., Teixeira da Silva, J., Barros, A. and Sousa, M. (2011). Ultrastructure of tubular smooth endoplasmic reticulum aggregates in human metaphase II oocytes and clinical implications. Fertility and Sterility, 96(1), 143–149.e7. doi: 10.1016/j.fertnstert.2011.04.088 CrossRefGoogle ScholarPubMed
Sánchez, F. and Smitz, J. (2012). Molecular control of oogenesis. Biochimica et Biophysica Acta, 1822(12), 1896–1912. doi: 10.1016/j.bbadis.2012.05.013 CrossRefGoogle ScholarPubMed
Sathananthan, A. H. (1985). Maturation of the human oocyte in vitro: Nuclear events during meiosis (an ultrastructural study). Gamete Research, 12(3), 237–254. doi: 10.1002/mrd.1120120303 CrossRefGoogle Scholar
Sathananthan, A. H. (1994). Ultrastructural changes during meiotic maturation in mammalian oocytes: Unique aspects of the human oocyte. Microscopy Research and Technique, 27(2), 145–164. doi: 10.1002/jemt.1070270208 CrossRefGoogle ScholarPubMed
Sathananthan, A. H. (1997). Ultrastructure of the human egg. Human Cell, 10(1), 21–38.Google ScholarPubMed
Sathananthan, A. H. (2003). Morphology and pathology of the human oocyte. In: Trounson, A. O. and Gosden, R. G. (eds). Biology and Pathology of the Oocyte (1st edn), pp. 185–208. Cambridge University Press.CrossRefGoogle Scholar
Sathananthan, A. H. (2013). Ultrastructure of human gametes, fertilization and embryos in assisted reproduction: A personal survey. Micron, 44, 1–20. doi: 10.1016/j.micron.2012.05.002 CrossRefGoogle ScholarPubMed
Sathananthan, A. H. and Trounson, A. O. (1982). Ultrastructural observations on cortical granules in human follicular oocytes cultured in vitro . Molecular Reproduction and Development, 5, 191–198. doi: 10.1002/mrd.112005o2o9 Google Scholar
Sathananthan, A. H. and Trounson, A. O. (2000). Mitochondrial morphology during preimplantational human embryogenesis. Human Reproduction, 15 (Suppl. 2), 148–159. doi: 10.1093/humrep/15.suppl_2.148 CrossRefGoogle ScholarPubMed
Sathananthan, A. H., Selvaraj, K., Girijashankar, M. L., Ganesh, V., Selvaraj, P. and Trounson, A. O. (2006). From oogonia to mature oocytes: Inactivation of the maternal centrosome in humans. Microscopy Research and Technique, 69(6), 396–407. doi: 10.1002/jemt.20299 CrossRefGoogle ScholarPubMed
Sciorio, R., Antonini, E. and Engl, B. (2021) Live birth and clinical outcome of vitrification-warming donor oocyte programme: An experience of a single IVF unit. Zygote, 29(5), 410–416. doi: 10.1017/S0967199421000204 CrossRefGoogle ScholarPubMed
Setti, A. S., Braga, D. P. A. F., Iaconelli, A. and Borges, E. (2021). Fresh oocyte cycles yield improved embryo quality compared with frozen oocyte cycles in an egg-sharing donation programme. Zygote, 29(3), 234–238. doi: 10.1017/S0967199420000842 CrossRefGoogle Scholar
Shen, X., Liu, X., Zhu, P., Zhang, Y., Wang, J., Wang, Y., Wang, W., Liu, J., Li, N. and Liu, F. (2017). Proteomic analysis of human follicular fluid associated with successful in vitro fertilization. Reproductive Biology and Endocrinology: RB&E, 15(1), 58. doi: 10.1186/s12958-017-0277-y CrossRefGoogle ScholarPubMed
Shu, Y., Gebhardt, J., Watt, J., Lyon, J., Dasig, D. and Behr, B. (2007). Fertilization, embryo development, and clinical outcome of immature oocytes from stimulated intracytoplasmic sperm injection cycles. Fertility and Sterility, 87(5), 1022–1027. doi: 10.1016/J.FERTNSTERT.2006.08.110 CrossRefGoogle ScholarPubMed
Sirait, B., Wiweko, B., Jusuf, A. A., Iftitah, D. and Muharam, R. (2021). Oocyte competence biomarkers associated with oocyte maturation: A review. Frontiers in Cell and Developmental Biology, 9(9), 710292. doi: 10.3389/fcell.2021.710292 CrossRefGoogle ScholarPubMed
Sousa, M. and Tesarik, J. (1994). Ultrastructural analysis of fertilization failure after intracytoplasmic sperm injection. Human Reproduction, 9(12), 2374–2380. doi: 10.1093/oxfordjournals.humrep.a138455 CrossRefGoogle ScholarPubMed
Sousa, M., Barros, A. and Tesarik, J. (1996). Developmental changes in calcium dynamics, protein kinase C distribution and endoplasmic reticulum organization in human preimplantation embryos. Molecular Human Reproduction, 2(12), 967–977. doi: 10.1093/molehr/2.12.967 CrossRefGoogle ScholarPubMed
Sousa, M., Barros, A., Silva, J. and Tesarik, J. (1997). Developmental changes in calcium content of ultrastructurally distinct subcellular compartments of preimplantation human embryos. Molecular Human Reproduction, 3(2), 83–90. doi: 10.1093/molehr/3.2.83 CrossRefGoogle ScholarPubMed
Sousa, M., Teixeira da Silva, J., Silva, J., Cunha, M., Viana, P., Oliveira, E., Sá, R., Soares, C., Oliveira, C. and Barros, A. (2015). Embryological, clinical and ultrastructural study of human oocytes presenting indented zona pellucida. Zygote, 23(1), 145–157. doi: 10.1017/S0967199413000403 CrossRefGoogle ScholarPubMed
Sousa, M., Cunha, M., Silva, J., Oliveira, E., Pinho, M. J., Almeida, C., Sá, R., da Silva, J. T., Oliveira, C. and Barros, A. (2016a). Ultrastructural and cytogenetic analyses of mature human oocyte dysmorphisms with respect to clinical outcomes. Journal of Assisted Reproduction and Genetics, 33(8), 1041–1057. doi: 10.1007/s10815-016-0739-8 CrossRefGoogle ScholarPubMed
Sousa, M., Oliveira, E., Barros, N., Barros, A. and Sá, R. (2016b). New ultrastructural observations of human oocyte smooth endoplasmic reticulum tubular aggregates and cortical reaction: Update on the molecular mechanisms involved. Revista Internacional de Andrología, 14(4), 113–122. doi: 10.1016/j.androl.2016.04.005 CrossRefGoogle Scholar
Stigliani, S., Moretti, S., Casciano, I., Canepa, P., Remorgida, V., Anserini, P. and Scaruffi, P. (2018). Presence of aggregates of smooth endoplasmic reticulum in MII oocytes affects oocyte competence: Molecular-based evidence. Molecular Human Reproduction, 24(6), 310–317. doi: 10.1093/molehr/gay018 CrossRefGoogle ScholarPubMed
Sundström, P., Nilsson, B. O., Liedholm, P. and Larsson, E. (1985). Ultrastructure of maturing human oocytes. Annals of the New York Academy of Sciences, 442, 324–331. doi: 10.1111/j.1749-6632.1985.tb37536.x CrossRefGoogle ScholarPubMed
Taylor, A. (2019). Gamete donation. In: Stuart, J. A. (ed.), Subfertility, Reproductive Endocrinology and Assisted Reproduction, pp. 241–250. Cambridge University Press. doi: 10.1017/9781316488294.032 CrossRefGoogle Scholar
Ten, J., Mendiola, J., Vioque, J., de Juan, J. and Bernabeu, R. (2007). Donor oocyte dysmorphisms and their influence on fertilization and embryo quality. Reproductive Biomedicine Online, 14(1), 40–48. doi: 10.1016/s1472-6483(10)60762-6 CrossRefGoogle ScholarPubMed
Trebichalská, Z., Kyjovská, D., Kloudová, S., Otevřel, P., Hampl, A. and Holubcová, Z. (2021). Cytoplasmic maturation in human oocytes: An ultrastructural study. Biology of Reproduction, 104(1), 106–116. doi: 10.1093/BIOLRE/IOAA174 CrossRefGoogle ScholarPubMed
Tripathi, A., Kumar, K. V. and Chaube, S. K. (2010). Meiotic cell cycle arrest in mammalian oocytes. Journal of Cellular Physiology, 223(3), 592–600. doi: 10.1002/jcp.22108 Google ScholarPubMed
Venturas, M., Yang, X., Kumar, K., Wells, D., Racowsky, C. and Needleman, D. J. (2021). Metabolic imaging of human cumulus cells reveals associations among metabolic profiles of cumulus cells, patient clinical factors, and oocyte maturity. Fertility and Sterility, 116(6), 1651–1662. doi: 10.1016/j.fertnstert.2021.07.1204 CrossRefGoogle ScholarPubMed
Virant-Klun, I., Leicht, S., Hughes, C. and Krijgsveld, J. (2016). Identification of maturation-specific proteins by single-cell proteomics of human oocytes. Molecular and Cellular Proteomics, 15(8), 2616–2627. doi: 10.1074/mcp.M115.056887 CrossRefGoogle ScholarPubMed
Walker, M. H. and Tobler, K. J. (2022) Female Infertility. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2022 Jan-. [Updated 2022 May 26] Available from: https://www.ncbi.nlm.nih.gov/books/NBK556033/ Google Scholar
Watson, A. J. (2007). Oocyte cytoplasmic maturation: A key mediator of oocyte and embryo developmental competence. Journal of Animal Science, 85(13) (Suppl.), E1–E3. doi: 10.2527/jas.2006-432 CrossRefGoogle ScholarPubMed
Weibel, E. R., Kistler, G. S. and Scherle, W. F. (1966). Practical stereological methods for morphometric cytology. Journal of Cell Biology, 30(1), 23–38. doi: 10.1083/jcb.30.1.23 CrossRefGoogle ScholarPubMed
Wells, D. and Patrizio, P. (2008). Gene expression profiling of human oocytes at different maturational stages and after in vitro maturation. American Journal of Obstetrics and Gynecology, 198(4), 455.e1–9; discussion 455.e9. doi: 10.1016/j.ajog.2007.12.030 CrossRefGoogle ScholarPubMed
Williams, R. S., Ellis, D. D., Wilkinson, E. A., Kramer, J. M., Datta, S. and Guzick, D. S. (2022). Factors affecting live birth rates in donor oocytes from commercial egg banks vs. program egg donors: An analysis of 40,485 cycles from the Society for Assisted Reproductive Technology registry in 2016–2018. Fertility and Sterility, 117(2), 339–348. doi: 10.1016/j.fertnstert.2021.10.006 CrossRefGoogle Scholar
Windt, M. L., Coetzee, K., Kruger, T. F., Marino, H., Kitshoff, M. S. and Sousa, M. (2001). Ultrastructural evaluation of recurrent and in-vitro maturation resistant metaphase I arrested oocytes. Human Reproduction, 16(11), 2394–2398. doi: 10.1093/humrep/16.11.2394 CrossRefGoogle ScholarPubMed
World Health Organization. (2020). Infertility. Available from https://www.who.int/news-room/fact-sheets/detail/infertility Google Scholar
Yeh, J. S., Steward, R. G., Dude, A. M., Shah, A. A., Goldfarb, J. M. and Muasher, S. J. (2014). Pregnancy outcomes decline in recipients over age 44: an analysis of 27,959 fresh donor oocyte in vitro fertilization cycles from the Society for Assisted Reproductive Technology. Fertility and Sterility, 101(5), 1331–1336.e1. doi: 10.1016/J.FERTNSTERT.2014.01.056 CrossRefGoogle Scholar
Zamboni, L., Thompson, R. S. and Smith, D. M. (1972). Fine morphology of human oocyte maturation in vitro . Biology of Reproduction, 7(3), 425–457. doi: 10.1093/BIOLREPROD/7.3.425 CrossRefGoogle ScholarPubMed