Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-24T06:27:42.507Z Has data issue: false hasContentIssue false
  • English
  • Français

A stereological study on organelle distribution in human oocytes at prophase I

Published online by Cambridge University Press:  14 July 2015

Ana Sílvia Pires-Luís ,
Eduardo Rocha ,
Carla Bartosch ,
Elsa Oliveira ,
Joaquina Silva ,
Alberto Barros ,
Rosália Sá  and
Mário Sousa
Ana Sílvia Pires-Luís
Affiliation:
Department of Microscopy, Laboratory of Cell Biology, Multidisciplinary Unit for Biomedical Research – UMIB, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto (UP), Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal. Department of Pathology and Cancer Biology and Epigenetics Group, Research Centre-LAB3, Portuguese Oncology Institute-Porto (IPO-P), Rua Dr. António Bernardino de Almeida, 4200–072, PortoPortugal. Department of Microscopy, Laboratory of Histology and Embryology, ICBAS-UP, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal.
Eduardo Rocha
Affiliation:
Department of Microscopy, Laboratory of Histology and Embryology, ICBAS-UP, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal.
Carla Bartosch
Affiliation:
Department of Pathology and Cancer Biology and Epigenetics Group, Research Centre-LAB3, Portuguese Oncology Institute-Porto (IPO-P), Rua Dr. António Bernardino de Almeida, 4200–072, PortoPortugal. Department of Pathology, Hospital Centre of St. John (CHSJ), Alameda Professor Hernâni Monteiro, 4200–319 Porto, Portugal.
Elsa Oliveira
Affiliation:
Department of Microscopy, Laboratory of Cell Biology, Multidisciplinary Unit for Biomedical Research – UMIB, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto (UP), Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal.
Joaquina Silva
Affiliation:
Centre for Reproductive Genetics Alberto Barros (CGR), Av. do Bessa, 240, 1º Dto. Frente, 4100–012 Porto, Portugal.
Alberto Barros
Affiliation:
Centre for Reproductive Genetics Alberto Barros (CGR), Av. do Bessa, 240, 1º Dto. Frente, 4100–012 Porto, Portugal. Department of Genetics, Faculty of Medicine, Institute of Health Research and Innovation, University of Porto, Alameda Prof. Hernâni Monteiro, 4200–319 Porto, Portugal.
Rosália Sá
Affiliation:
Department of Microscopy, Laboratory of Cell Biology, Multidisciplinary Unit for Biomedical Research – UMIB, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto (UP), Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal.
Mário Sousa*
Affiliation:
Department of Microscopy, Laboratory of Cell Biology, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto (UP), Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal.
*
All correspondence to: Mário Sousa. Department of Microscopy, Laboratory of Cell Biology, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto (UP), Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal. Tel: +351 220 428 000 (General); +351 220 428 246 (Office). Fax: +351 220 428 090. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The ultrastructural analysis of human oocytes at different maturation stages has only been descriptive. The aim of this study was to use a stereological approach to quantify the distribution of organelles in oocytes at prophase I (GV). Seven immature GV oocytes were processed for transmission electron microscopy and a classical manual stereological technique based on point-counting with an adequate stereological grid was used. The Kruskal–Wallis test and Mann–Whitney U-test with Bonferroni correction were used to compare the means of the relative volumes occupied by organelles in oocyte regions: cortex (C), subcortex (SC) and inner cytoplasm (IC). Here we first describe in GV oocytes very large vesicles of the smooth endoplasmic reticulum (SER), vesicles containing zona pellucida-like materials and coated vesicles. The most abundant organelles were the very large vesicles of the SER (6.9%), mitochondria (6.3%) and other SER vesicles (6.1%). Significant differences in organelle distribution were observed between ooplasm regions: cortical vesicles (C: 1.3% versus SC: 0.1%, IC: 0.1%, P = 0.001) and medium-sized vesicles containing zona pellucida-like materials (C: 0.2% versus SC: 0.02%, IC: 0%, P = 0.004) were mostly observed at the oocyte cortex, whereas mitochondria (C: 3.6% versus SC: 6.0%, IC: 7.2%, P = 0.005) were preferentially located in the subcortex and inner cytoplasm, and SER very large vesicles (IC: 10.1% versus C: 0.9%, SC: 1.67%, P = 0.001) in the oocyte inner cytoplasm. Further quantitative studies are needed in immature metaphase-I and mature metaphase-II oocytes, as well as analysis of correlations between ultrastructural and molecular data, to better understand human oocyte in vitro maturation.

Keywords

Cell polarityHuman germinal vesicle oocytesOrganelle distributionStereologyUltrastructure
Type
Research Article
Information
Zygote , Volume 24 , Issue 3 , June 2016 , pp. 346 - 354
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Assou, S., Anahory, T., Pantesco, V., Le Carrour, T., Pellestor, F., Klein, B., Reyftmann, L., Dechaud, H., De Vos, J. & Hamamah, S. (2006). The human cumulus–oocyte complex gene-expression profile. Hum. Reprod. 21, 1705–19.CrossRefGoogle ScholarPubMed
Cha, K.-Y. & Chian, R.-C. (1998). Maturation of immature human oocytes for clinical use. Hum. Reprod. Update 4, 103–20.CrossRefGoogle ScholarPubMed
Cui, X.-S. & Kim, N.-H. (2007). Maternally derived transcripts: identification and characterization during oocyte maturation and early cleavage. Reprod. Fertil. Dev. 19, 25–34.CrossRefGoogle ScholarPubMed
Di Luigi, A., Weitzman, V.N., Pace, M.C., Siano, L.J., Maier, D. & Mehlmann, L.M. (2008). Meiotic arrest in human oocytes is maintained by a Gs signaling pathway. Biol. Reprod. 78, 667–72.CrossRefGoogle ScholarPubMed
El Shafie, M, Sousa, M., Windt, M.-L. & Kruger, T.F. (2000). In An Atlas of the Ultrastructure of Human Oocytes . A Guide For Assisted Reproduction. New York: The Parthenon Publishing Group.Google Scholar
Han, S.J., Vaccari, S., Nedachi, T., Andersen, C.B., Kovacina, K.S., Roth, R.A. & Conti, M. (2006). Protein kinase B/Akt phosphorylation of PDE3A and its role in mammalian oocyte maturation. EMBO J. 25, 5716–25.CrossRefGoogle ScholarPubMed
Hertig, A.T. & Adams, E.C. (1967). Studies on the human oocyte and its follicle: I. Ultrastructural and histochemical observations on the primordial follicle stage. J. Cell Biol. 34, 647–75.CrossRefGoogle ScholarPubMed
Huirne, J.A., Homburg, R. & Lambalk, C.B. (2007). Are GnRH antagonists comparable to agonists for use in IVF? Hum. Reprod. 22, 2805–13.CrossRefGoogle ScholarPubMed
Khalili, M.A., Maione, M., Palmerini, M.G., Bianchi, S., Macchiarelli, G. & Nottola, S.A. (2012). Ultrastructure of human mature oocytes after vitrification. Eur. J. Histochem. 56, 236–42.CrossRefGoogle ScholarPubMed
Khalili, M.A., Nottola, S.A., Shahedi, A. & Macchiarelli, G. (2013). Contribution of human oocyte architecture to success of in vitro maturation technology. Iran J. Reprod. Med. 11, 1–10.Google ScholarPubMed
Li, Q., McKenzie, L.J. & Matzuk, M.M. (2008). Revisiting oocyte-somatic cell interactions: in search of novel intrafollicular predictors and regulators of oocyte developmental competence. Mol. Hum. Reprod. 14, 673–8.CrossRefGoogle ScholarPubMed
Li, R. & Albertini, D.F. (2013). The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat. Rev. Mol. Cell Biol. 13, 141–52.CrossRefGoogle Scholar
Liang, L.-f., Soyal, S.M. & Dean, J. (1997). FIGα, a germ cell specific transcription factor involved in the coordinate expression of the zona pellucida genes. Development 124, 4939–47.CrossRefGoogle ScholarPubMed
Mao, L., Lou, H., Lou, Y, Wang, N. & Jin, F. (2014). Behavior of cytoplasmic organelles and cytoskeleton during oocyte maturation. Reprod. BioMed. Online. 28, 284–99.CrossRefGoogle ScholarPubMed
McGinnis, L.K., Carroll, D.J. & Kinsey, W.H. (2011). Protein tyrosine kinase signaling during oocyte maturation and fertilization. Mol. Reprod. Develop. 78 (10–11), 831–45.CrossRefGoogle ScholarPubMed
Mehlmann, L.M. (2005). Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130, 791–9.CrossRefGoogle ScholarPubMed
Nogueira, D., Albano, C., Adriaenssens, T., Cortvrindt, R., Bourgain, C., Devroey, P. & Smitz, J. (2003). Human oocytes reversibly arrested in prophase I by phosphodiesterase type 3 inhibitor in vitro . Biol. Reprod. 69, 1042–52.CrossRefGoogle ScholarPubMed
Palmerini, M.G., Antinori, M., Maione, M., Cerusico, F., Versaci, C., Nottola, S.A., Macchiarelli, G., Khalili, M.A. & Antinori, S. (2014). Ultrastructure of immature and mature human oocytes after cryotop vitrification. J. Reprod. Dev. 60, 411–20.CrossRefGoogle ScholarPubMed
Picton, H.M., Harris, S.E., Muruvi, W. & Chambers, E.L. (2008). The in vitro growth and maturation of follicles. Reproduction 136, 703–15.CrossRefGoogle ScholarPubMed
Pinto, F., Oliveira, C., Cardoso, M.F., Teixeira da Silva, J., Silva, J., Sousa, M. & Barros, A. (2009). Impact of GnRH ovarian stimulation protocols on intracytoplasmic sperm injection outcomes. Reprod. Biol. Endocrinol. 7, 5.CrossRefGoogle ScholarPubMed
Sá, R., Cunha, M., Silva, J., Luis, A., Oliveira, C., Tixeira da Silva, J, Barros, A & Sousa, M. (2011). Ultrastructure of tubular smooth endoplasmic reticulum aggregates in human metaphase-II oocytes and clinical implications. Fertil. Steril. 96, 143–9.CrossRefGoogle ScholarPubMed
Sathananthan, A.H. & Trouson, A.O. (2000). Mitochondrial morphology during preimplantational human embryogenesis. Hum. Reprod. 15 (Suppl. 2), 148–59.CrossRefGoogle ScholarPubMed
Sathananthan, A.H., Selvaraj, K., Girijashankar, M.L., Ganesh, V., Selvaraj, P. & Trouson, A.O. (2006). From oogonia to mature oocytes: inactivation of the maternal centrosome in humans. Microsc. Res. Tech. 69, 396–407.CrossRefGoogle ScholarPubMed
Shahedi, A., Khalili, M.A., Soleimani, M. & Morshedizad, S. (2013a). Ultrastructure of in vitro matured human oocytes. Iran Red Cresc. Med. J. 15, e7379.Google ScholarPubMed
Shahedi, A., Hosseini, A., Khalili, M.A., Norouzian, M., Salehi, M., Piriaei, A. & Nottola, S.A. (2013b). The effect of vitrification on ultrastructure of human in vitro matured germinal vesicle oocytes. Eur. J. Obstet. Gynecol. Reprod. Biol. 167, 69–75.CrossRefGoogle Scholar
Sousa, M. & Tesarik, J. (1994). Ultrastructural analysis of fertilization failure after intracytoplasmic sperm injection. Hum. Reprod. 9, 2374–80.CrossRefGoogle ScholarPubMed
Sousa, M., Barros, A., Silva, J. & Tesarik, J. (1997). Developmental changes in calcium content of ultrastructurally distinct subcellular compartments of preimplantation human embryos. Mol. Hum. Reprod. 3, 83–90.CrossRefGoogle ScholarPubMed
Sousa, M., Teixeira da Silva, J., Silva, J., Cunha, M., Viana, P., Oliveira, E., Sá, R., Soares, C., Oliveira, C. & Barros, A. (2015). Embryological, clinical and ultrastructural study of human oocytes presenting indented zona pellucida. Zygote 23, 145–57.CrossRefGoogle ScholarPubMed
Tan, S.L. & Child, T.J. (2002). In-vitro maturation of oocytes from unstimulated polycystic ovaries. Reprod. BioMed. Online 4 (Suppl. 1), 18–23.CrossRefGoogle ScholarPubMed
Tesarik, J & Kopecny, V. (1986). Late preovulatory synthesis of proteoglycans by the human oocyte and cumulus cells and their secretion into the oocyte-cumulus-complex extracellular matrices. Histochemistry 85, 523–8.CrossRefGoogle ScholarPubMed
Tosti, E. (2006). Calcium ion currents mediating oocyte maturation events. Reprod. Biol. Endocrinol. 4, 26.CrossRefGoogle ScholarPubMed
Virant-Klun, I., Knez, K., Tonazevic, T & Skutella, T. (2013). Gene expression profiling of human oocytes developed and matured in vivo or in vitro . BioMed. Res. Internat. 2013, 879489.CrossRefGoogle ScholarPubMed
Weibel, E.R., Kistler, G.S. & Scherle, W.F. (1966). Practical stereological methods for morphometric cytology. J. Cell Biol. 30, 23–38.CrossRefGoogle ScholarPubMed
Zamboni, L., Thompson, R.S. & Smith, D.M. (1972). Fine morphology of human oocyte maturation in vitro . Biol. Reprod. 7, 425–57.CrossRefGoogle ScholarPubMed