Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-28T11:39:22.420Z Has data issue: false hasContentIssue false

Stereological study of organelle distribution in human oocytes at metaphase I

Published online by Cambridge University Press:  14 April 2020

Sofia Coelho
Affiliation:
Laboratory of Cell Biology, Department of Microscopy, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto (UP), Rua Jorge Viterbo Ferreira, 228, 4050-313Porto, Portugal Department of Life Sciences, Faculty of Sciences and Technology, New Lisbon University (UNL), Campus da Caparica, 2829-516Lisbon, Portugal
Ana Sílvia Pires-Luís
Affiliation:
Laboratory of Histology and Embryology, Department of Microscopy, Institute of Biomedical Sciences Abel Salazar, University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050-313Porto, Portugal Department of Pathology, Hospital Centre of Vila Nova de Gaia/Espinho, Unit 1, Rua Conceição Fernandes, 1079, 4434-502Vila Nova de Gaia, Portugal
Elsa Oliveira
Affiliation:
Laboratory of Cell Biology, Department of Microscopy, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto (UP), Rua Jorge Viterbo Ferreira, 228, 4050-313Porto, Portugal Multidisciplinary Unit for Biomedical Research (UMIB), University of Porto, Portugal
Ângela Alves
Affiliation:
Laboratory of Cell Biology, Department of Microscopy, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto (UP), Rua Jorge Viterbo Ferreira, 228, 4050-313Porto, Portugal Multidisciplinary Unit for Biomedical Research (UMIB), University of Porto, Portugal
Carla Leal
Affiliation:
Centre of Assisted Medical Procriation (CPMA), Maternal Child Centre of the North (CMIN), Hospital and University Center of Porto (CHUP), Largo da Maternidade de Júlio Dinis, 4050-651Porto, Portugal
Mariana Cunha
Affiliation:
Center for Reproductive Genetics A. Barros (CGR), Av. do Bessa, 240, 1° Dto. Frente, 4100–012Porto, Portugal
Márcia Barreiro
Affiliation:
Centre of Assisted Medical Procriation (CPMA), Maternal Child Centre of the North (CMIN), Hospital and University Center of Porto (CHUP), Largo da Maternidade de Júlio Dinis, 4050-651Porto, Portugal
Alberto Barros
Affiliation:
Center for Reproductive Genetics A. Barros (CGR), Av. do Bessa, 240, 1° Dto. Frente, 4100–012Porto, Portugal Department of Genetics, Faculty of Medicine, University of Porto (FMUP), Alameda Prof. Hernâni Monteiro, 4200–319Porto, Portugal Institute of Health Research and Innovation (IPATIMUP/i3S), University of Porto, Rua Alfredo Allen, 208, 4200–135Porto, Portugal
Rosália Sá
Affiliation:
Laboratory of Cell Biology, Department of Microscopy, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto (UP), Rua Jorge Viterbo Ferreira, 228, 4050-313Porto, Portugal Multidisciplinary Unit for Biomedical Research (UMIB), University of Porto, Portugal
Mário Sousa*
Affiliation:
Laboratory of Cell Biology, Department of Microscopy, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto (UP), Rua Jorge Viterbo Ferreira, 228, 4050-313Porto, Portugal Multidisciplinary Unit for Biomedical Research (UMIB), University of Porto, Portugal
*
Author for correspondence: Mário Sousa. Laboratory of Cell Biology, Department of Microscopy, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto (UP), Rua Jorge Viterbo Ferreira, 228, 4050-313Porto, Portugal. Tel: +351 919974476. E-mail: [email protected]

Summary

We have previously presented a stereological analysis of organelle distribution in human prophase I oocytes. In the present study, using a similar stereological approach, we quantified the distribution of organelles in human metaphase I (MI) oocytes also retrieved after ovarian stimulation. Five MI oocytes were processed for transmission electron microscopy and a classical manual stereological technique based on point-counting with an adequate stereological grid was used. Kruskal–Wallis and Mann–Whitney U-tests with Bonferroni correction were used to compare the means of relative volumes (Vv) occupied by organelles. In all oocyte regions, the most abundant organelles were mitochondria and smooth endoplasmic reticulum (SER) elements. No significant differences were observed in Vv of mitochondria, dictyosomes, lysosomes, or SER small and medium vesicles, tubular aggregates and tubules. Significant differences were observed in other organelle distributions: cortical vesicles presented a higher Vv (P = 0.004) in the cortex than in the subcortex (0.96% vs 0.1%) or inner cytoplasm (0.96% vs 0.1%), vesicles with dense granular contents had a higher Vv (P = 0.005) in the cortex than in the subcortex (0.1% vs 0%), and SER large vesicles exhibited a higher Vv (P = 0.011) in the inner cytoplasm than in the subcortex (0.2% vs 0%). Future stereological analysis of metaphase II oocytes and a combined quantitative data of mature and immature oocytes, will enable a better understanding of oocyte organelle distribution during in vivo maturation. Combined with molecular approaches, this may help improve stimulation protocols and in vitro maturation methods.

Type
Research Article
Copyright
© Cambridge University Press 2020

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.)

Footnotes

*

Both authors contributed equally to this work.

References

Álvarez, C, García-Garrido, C, Taronger, R and González de Merlo, G (2013) In vitro maturation, fertilization, embryo development and clinical outcome of human metaphase-I oocytes retrieved from stimulated intracytoplasmic sperm injection cycles. Indian J Med Res 137, 331–8.Google ScholarPubMed
Beall, S, Brenner, C and Segars, J (2010) Oocyte maturation failure: a syndrome of bad eggs. Fertil Steril 94, 2507–13.CrossRefGoogle ScholarPubMed
Bracewell-Milnes, T, Saso, S, Abdalla, H, Nikolau, D, Norman-Taylor, J, Johnson, M, Holmes, E and Thum, M-Y (2017) Metabolomics as a tool to identify biomarkers to predict and improve outcomes in reproductive medicine: a systematic review. Hum Reprod Update 23, 723–36.CrossRefGoogle ScholarPubMed
Capalbo, A, Hoffmann, ER, Cimadomo, D, Ubaldi, FM and Rienzi, L (2017) Human female meiosis revised: new insights into the mechanisms of chromosome segregation and aneuploidies from advanced genomics and time-lapse imaging. Hum Reprod Update 23, 706–22.CrossRefGoogle ScholarPubMed
Cha, K-Y and Chian, R-C (1998) Maturation in vitro of immature human oocytes for clinical use. Hum Reprod Update 4, 103–20.CrossRefGoogle ScholarPubMed
Chen, B, Li, B, Li, D, Yan, Z, Mao, X, Xu, Y, Mu, J, Li, Q, Jin, L, He, L, Kuang, Y, Sang, Q and Wang, L (2017a) Novel mutations and structural deletions in TUBB8: expanding mutational and phenotypic spectrum of patients with arrest in oocyte maturation, fertilization or early embryonic development. Hum Reprod 32, 457–64.CrossRefGoogle ScholarPubMed
Chen, B, Zhang, Z, Sun, X, Kuang, Y, Mao, X, Wang, X, Yan, Z, Li, B, Xu, Y, Yu, M, Fu, J, Mu, J, Zhou, Z, Li, Q, Jin, L, He, L, Sang, Q and Wang, L (2017b) Biallelic mutations in PATL2 cause female infertility characterized by oocyte maturation arrest. Am J Hum Genet 101, 609–15.CrossRefGoogle ScholarPubMed
Chian, R-C, Uzelac, PS and Nargund, G (2013) In vitro maturation of human immature oocytes for fertility preservation. Fertil Steril 99, 1173–81.CrossRefGoogle ScholarPubMed
Conti, M and Franciosi, F (2018) Acquisition of oocyte competence to develop as an embryo: integrated nuclear and cytoplasmic events. Hum Reprod Update 24, 245–66.CrossRefGoogle ScholarPubMed
Coticchio, G, Dal Canto, M, Renzini, MM, Guglielmo, MC, Brambillasca, F, Turchi, D, Novara, PV and Fadini, R (2015) Oocyte maturation: gamete–somatic cell interactions, meiotic resumption, cytoskeletal dynamics and cytoplasmic reorganization. Hum Reprod Update 21, 427–54.CrossRefGoogle ScholarPubMed
Cui, X-S and Kim, N-H (2017) Maternally derived transcripts: identification and characterization during oocyte maturation and early cleavage. Reprod Fertil Dev 19, 2534.CrossRefGoogle Scholar
El Shafie, M, Windt, M-L, Kitshoff, M, McGregor, P, Sousa, M, Wranz, PAB and Kruger, TF (2000) Ultrastructure of human oocytes: a transmission electron microscopy view. In An Atlas of the Ultrastructure of Human Oocytes (eds El Shafie, M, Sousa, M, Windt, M-L and Kruger, TF), pp. 83173. The Parthenon Publishing Group.Google Scholar
Familiari, G, Makabe, S and Motta, PM (1989) The ovary and ovulation: a three dimensional ultrastructural study. In Ultrastructure of Human Gametogenesis and Early Embryogenesis (eds Blerkom, JV and Motta, PM), pp. 85124. Kluwer Academic Publishers, Boston, MA, USA.CrossRefGoogle Scholar
Feng, R, Sang, Q, Kuang, Y, Sun, X, Yan, Z, Zhang, S, Shi, J, Tian, G, Luchniak, A, Fukuda, Y, Li, B, Yu, M, Chen, J, Xu, Y, Guo, L, Qu, R, Wang, X, Sun, Z, Liu, M, Shi, H, Wang, H, Feng Yi, Shao R, Chai, R, Li, Q, Xing, Q, Zhang, R, Nogales, E, Jin, L, He, L, Gupta, ML Jr, Cowan, NJ and Wang, L (2016) Mutations in TUBB8 cause human oocyte meiotic arrest. N Engl J Med. 374, 223–32.CrossRefGoogle ScholarPubMed
Ferrer-Buitrago, M, Dhaenens, L, Lu, Y, Bonte, D, Vanden Meerschaut, F, De Sutter, P, Leybaert, L and Heindryckx, B (2018) Human oocyte calcium analysis predicts the response to assisted oocyte activation in patients experiencing fertilization failure after ICSI. Hum Reprod 33, 416–25.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. Reprod Biomed Online 14, 175–83.CrossRefGoogle ScholarPubMed
Greaney, J, Wei, Z and Homer, H (2018) Regulation of chromosome segregation in oocytes and the cellular basis for female meiotic errors. Hum Reprod Update 24, 135–61.CrossRefGoogle ScholarPubMed
Hoshino, Y (2018) Updating the markers for oocyte quality evaluation: intracellular temperature as a new index. Reprod Med Biol 17, 434–41.CrossRefGoogle ScholarPubMed
Huirne, JA, Homburg, R and Lambalk, CB (2007) Are GnRH antagonists comparable to agonists for use in IVF? Hum Reprod 22, 2805–13.CrossRefGoogle ScholarPubMed
Keef, D, Kumar, M and Kalmbach, K (2015) Oocyte competency is the key to embryo potential. Fertil Steril 103, 317–22.CrossRefGoogle Scholar
Labrecque, R and Sirard, M-A (2014) The study of mammalian oocyte competence by transcriptome analysis: progress and challenges. Mol Hum Reprod 20, 103–16.CrossRefGoogle Scholar
Levran, D, Farhi, J, Nahum, H, Glezerman, M and Weissman, A (2002) Maturation arrest of human oocytes as a cause of infertility. Hum Reprod 17, 1604–9.CrossRefGoogle ScholarPubMed
Li, Y, Liu, H, Yu, Q, Liu, H, Huang, T, Zhao, S, Ma, J and Zhao, H (2019) Growth hormone promotes in vitro maturation of human oocytes. Front Endocrinol 10, 485.CrossRefGoogle ScholarPubMed
Liu, C, Li, M, Li, T, Zhao, H, Huang, J, Wang, Y, Gao, Q, Yu, Y and Shi, Q (2016) ECATI is essential for human oocyte maturation and pre-implantation development of the resulting embryos. Sci Rep 6, 38192.CrossRefGoogle Scholar
MacLennan, M, Crichton, JH, Playfoot, CJ and Adams, IR (2015) Oocyte development, meiosis and aneuploidy. Semin Cell Dev Biol 45, 6876.CrossRefGoogle ScholarPubMed
Madgwick, S and Jones, KT (2007) How eggs arrest at metaphase II: MPF stabilization plus APC/C inhibition equals cytostatic factor. Cell Division 2, 4.CrossRefGoogle Scholar
Marangos, P, Stevense, M, Niaka, K, Lagoudaki, M, Nabti, I, Jessberger, R and Carroll, J (2015) DNA damage-induced metaphase I arrest is mediated by the spindle assembly checkpoint and maternal age. Nat Commun 6, 8706.CrossRefGoogle ScholarPubMed
Mehlmann, LM (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
Morimoto, Y (2009) Ultrastructure of the human oocytes during in vitro maturation. J Mamm Ova Res 26, 10–7.CrossRefGoogle Scholar
Motta, PM, Nottola, SA, Micara, G and Familiari, G (1988) Ultrastructure of human unfertilized oocytes and polyspermic embryos in an IVF-ET program. Ann NY Acad Sci 541, 367–83.CrossRefGoogle Scholar
Mrazek, M and Fulka, J Jr (2003) Failure of oocyte maturation: possible mechanism for oocyte maturation arrest. Hum Reprod 18, 2249–52.CrossRefGoogle Scholar
Nogueira, D, Romero, S, Vanhoutte, L, de Matos, DG and Smitz, J (2009) Oocyte in vitro maturation. In Textbook of Assisted Reproductive Technologies 3rd edn (eds Gardner, DK, Weissman, A, Howles, CM and Shoham, Z) pp. 111153. London UK: Informa Healthcare.Google Scholar
Nottola, SA, Macchiarelli, G and Familiari, G (2014) Fine structural markers of human oocyte quality in assisted reproduction. Austin J Reprod Med Infertil 1, 5.Google Scholar
Pinto, F, Oliveira, C, Cardoso, MF, Teixeira da Silva, J, Silva, J, Sousa, M and Barros, A (2009) Impact of GnRH ovarian stimulation protocols on intracytoplasmic sperm injection outcomes. Reprod Biol Endocrinol 7, 5.CrossRefGoogle ScholarPubMed
Pires-Luís, AS, Rocha, E, Bartosch, C, Oliveira, E, Silva, J, Barros, A, , R and Sousa, M (2016) A stereological study on organelle distribution in human oocytes at prophase I. Zygote 24, 346–54.CrossRefGoogle Scholar
Reader, KL, Stanton, J-AL and Juengel, J (2017) The role of oocyte organelles in determining developmental competence. Biology 6, 35.CrossRefGoogle ScholarPubMed
Richani, D and Gilchrist, RB (2018) The epidermal growth factor network: role in oocyte growth, maturation and developmental competence. Hum Reprod Update 24, 114.CrossRefGoogle ScholarPubMed
, 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. Fertil Steril 96, 143–9.CrossRefGoogle ScholarPubMed
Sathananthan, AH (1985) Maturation of the human oocyte in vitro: nuclear events during meiosis (an ultrastructural study). Gamete Res 12, 237–54.CrossRefGoogle Scholar
Sathananthan, AH (1994) Ultrastructural changes during meiotic maturation in mammalian oocytes: unique aspects of the human oocyte. Microsc Res Tech 27, 145–64.CrossRefGoogle ScholarPubMed
Sathananthan, AH (2000) Ultrastructure of human gametes, fertilization, and embryo development. In Handbook of In Vitro Fertilization 2nd edn (eds Trouson, AO and Gardner, DK), pp. 431–64. Boca Raton, FL, USA: CRC Press LLC.Google Scholar
Sathananthan, AH (2003) Morphology and pathology of the human oocyte. In Biology and Pathology of the Oocyte 1st edn (eds Trouson, AO and Gosden, RG), pp. 185208. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Sathananthan, AH, Trouson, AO and Wood, C (1986) Oocyte maturation. In Atlas of Fine Structure of Human Sperm Penetration, Eggs and Embryos Cultured In Vitro (eds AH Sathananthan, AO Trouson and C Wood), pp. 1–47. New York, USA: Praeger Publishers.Google Scholar
Smitz, JEJ, Thompson, JG and Gilchrist, RB (2011) The promise of in vitro maturation in assisted reproduction and fertility preservation. Semin Reprod Med 29, 2437.CrossRefGoogle ScholarPubMed
Sousa, M and Tesarik, J (1994) Ultrastructural analysis of fertilization failure after intracytoplasmic sperm injection. Hum Reprod 9, 2374–80.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. Mol Hum Reprod 2, 967–77.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. Mol Hum Reprod 3, 8390.CrossRefGoogle ScholarPubMed
Sousa, M, Oliveira, E, Barros, N, Barros, A and , R (2016) New ultrastructural observations of human oocyte smooth endoplasmic reticulum tubular aggregates and cortical reaction: update on the molecular mechanisms involved. Rev Int Androl 14, 113–22.Google Scholar
Strassburger, D, Friedler, S, Raziel, A, Kasterstein, E, Schachter, M and Ron-El, R (2004) The outcome of ICSI of immature MI oocytes and rescued in vitro matured MII oocytes. Hum Reprod 19, 1587–90.CrossRefGoogle ScholarPubMed
Strassburger, D, Goldstein, A, Friedler, S, Raziel, A, Kasterstein, E, Mashevich, M, Schachter, M, Ron-El, R and Reish, O (2010) The cytogenic constitution of embryos derived from immature (metaphase I) oocytes obtained after ovarian hyperstimulation. Fertil Steril 94, 971–8.CrossRefGoogle Scholar
Sundström, P and Nilsson, BO (1988) Meiotic and cytoplasmic maturation of oocytes collected in stimulated cycles is asynchronous. Hum Reprod 3, 613–9.CrossRefGoogle ScholarPubMed
Sundström, P, Nilsson, BO, Liedholm, P and Larsson, E (1985a) Ultrastructural characteristics of human oocytes fixed at follicular puncture or after culture. J In Vitro Fert Embryo Transf 2, 195206.CrossRefGoogle ScholarPubMed
Sundström, P, Nilsson, BO, Liedholm, P and Larsson, E (1985b) Ultrastructure of maturing human oocytes. Ann NY Acad Sci 442, 324–31.CrossRefGoogle ScholarPubMed
Tripathi, A, Kumar, P and Chaube, SK (2010) Meiotic cell cycle arrest in mammalian oocytes. J Cell Physiol 223, 592600.Google ScholarPubMed
Vanhoutte, L, De Sutter, P, Van der Elst, J and Dhont, M (2005) Clinical benefit of metaphase I oocytes. Reprod Biol Endocrinol 3, 71.CrossRefGoogle ScholarPubMed
Virant-Klun, I, Knez, K, Tomazevic, T and Skutella, T (2013) Gene expression profiling of human oocytes developed and matured in vivo or in vitro. Biomed Res Int 2013, Article ID 879489.Google Scholar
Virant-Klun, I, Leicht, S, Hughes, C and Krijgsveld, J (2016) Identification of maturation-specific proteins by single-cell proteomics of human oocytes. Mol Cell Proteomics 15, 2616–27.CrossRefGoogle ScholarPubMed
Watson, AJ (2007) Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence. J Anim Sci 85, E13.CrossRefGoogle ScholarPubMed
Weibel, ER, Kistler, GS and Scherle, WF (1966) Practical stereological methods for morphometric cytology. J Cell Biol 30, 2338.CrossRefGoogle ScholarPubMed
Windt, M-L, Coetzee, K, Kruger, TF, Marino, H, Kitshoff, MS and Sousa, M (2001) Ultrastructural evaluation of recurrent and in-vitro maturation resistant metaphase I arrested oocytes. Hum Reprod 16, 2394–8.CrossRefGoogle ScholarPubMed
Yu, B, Dong, X, Gravina, S, Kartal, Ö, Schimmel, T, Cohen, J, Tortoriello, D, Zody, R, Hawkins, RD and Vijg, J (2017) Genome-wide, single-cell DNA methylomics reveals increased non-CpG methylation during human oocyte maturation. Stem Cell Rep 9, 397407.CrossRefGoogle ScholarPubMed
Zamboni, L, Thompson, RS and Smith, DM (1972) Fine morphology of human oocyte maturation in vitro. Biol Reprod 7, 425–57.CrossRefGoogle ScholarPubMed
Zhao, H, Li, T, Zhao, Yue, Tan, T, Liu, C, Liu, Y, Chang, L, Huang, N, Li, C, Fan, Y, Yu, Y, Li, R and Qiao, J (2019) Single-cell transcriptomics of human oocytes: environment-driven metabolic competition and compensatory mechanisms during oocyte maturation. Antioxid Redox Signal 30, 542–59.CrossRefGoogle ScholarPubMed
Supplementary material: File

Coelho et al. Supplementary Materials

Coelho et al. Supplementary Materials

Download Coelho et al. Supplementary Materials(File)
File 826 KB