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Embryological, clinical and ultrastructural study of human oocytes presenting indented zona pellucida

Published online by Cambridge University Press:  02 September 2013

M. Sousa ,
J. Teixeira da Silva ,
J. Silva ,
M. Cunha ,
P. Viana ,
E. Oliveira ,
R. Sá ,
C. Soares ,
C. Oliveira  and
A. Barros
M. Sousa*
Affiliation:
Department of Microscopy, Laboratory of Cell Biology, Building 1, Floor 2, Room 10.2.3, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal.
J. Teixeira da Silva
Affiliation:
Centre for Reproductive Genetics Alberto Barros, Av. do Bessa, 240, 1° Dto. Frente, 4100–009 Porto, Portugal.
J. Silva
Affiliation:
Centre for Reproductive Genetics Alberto Barros, Av. do Bessa, 240, 1° Dto. Frente, 4100–009 Porto, Portugal.
M. Cunha
Affiliation:
Centre for Reproductive Genetics Alberto Barros, Av. do Bessa, 240, 1° Dto. Frente, 4100–009 Porto, Portugal.
P. Viana
Affiliation:
Centre for Reproductive Genetics Alberto Barros, Av. do Bessa, 240, 1° Dto. Frente, 4100–009 Porto, Portugal.
E. Oliveira
Affiliation:
Department of Microscopy, Laboratory of Cell Biology, UMIB, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal.
R. Sá
Affiliation:
Department of Microscopy, Laboratory of Cell Biology, UMIB, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal.
C. Soares
Affiliation:
Department of Microscopy, Laboratory of Cell Biology, UMIB, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal.
C. Oliveira
Affiliation:
Centre for Reproductive Genetics Alberto Barros, Av. do Bessa, 240, 1° Dto. Frente, 4100–009 Porto, Portugal.
A. Barros
Affiliation:
Centre for Reproductive Genetics Alberto Barros, Av. do Bessa, 240, 1° Dto. Frente, 4100–009 Porto, Portugal. Department of Genetics, Faculty of Medicine, University of Porto, Alameda Prof. Hernâni Monteiro, 4200–319 Porto, Portugal.
*
All correspondence to: Mário Sousa. Department of Microscopy, Laboratory of Cell Biology, Building 1, Floor 2, Room 10.2.3, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal. Tel: +351 220 428 000 (General), +351 220 428 246 (Office). Fax: +351 222 062 232. e-mail: msousa@icbas.up.pt
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Summary

Human oocyte dysmorphisms attain a large proportion of retrieved oocytes from assisted reproductive technology (ART) treatment cycles. Extracytoplasmic defects involve abnormal morphology of the zona pellucida (ZP), perivitelline space and first polar body. The aim of the present study was to describe a novel dysmorphism affecting the ZP, indented ZP. We also evaluated the clinical, embryological and ultrastructural features of these cases. We evaluated all ART treatment cycles during 7 consecutive years and found 13 treatment cycles (six patients) with all oocytes presenting an indented ZP. In addition, these oocytes presented total or partial absence of the perivitelline space, absence of resistance to ZP and oolemma penetration during microinjection, and low ooplasm viscosity during aspiration. This novel described dysmorphism was recurrent and attained all oocytes in three cases that had more than one treatment cycle. When compared with controls, data showed significant low oocyte maturity (42% versus 81.6%) and high cycle cancellation (30.8% versus 8.5%) rates, normal degeneration (3.4% versus 6.3%) and fertilization rates (69% versus 69.5%), and low pregnancy (15.4% versus 33.3%) and live-birth delivery (7.7% versus 27.7%) rates per cycle. Ultrastructure analysis revealed a zona pellucida structure with large empty electrolucent regions, an outer ZP layer with an indented surface with protuberances and a thick inner ZP that obliterated the perivitelline space. There was evidence of exocytosis of ZP material by the oocyte. In conclusion, oocytes with this novel described dysmorphism (indented ZP) are associated with low maturity, pregnancy and live-birth delivery rates.

Keywords

Clinical and embryological outcomesIndented zona pellucidaOocyte dysmorphismsUltrastructure
Type
Research Article
Information
Zygote , Volume 23 , Issue 1 , February 2015 , pp. 145 - 157
Copyright
Copyright © Cambridge University Press 2013 

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References

Alikani, M., Palermo, G., Adler, A., Bertoli, M., Blake, M. & Cohen, J. (1995). Intracytoplasmic sperm injection in dysmorphic human oocytes. Zygote 3, 283–8.Google Scholar
Balaban, B., Urman, B., Sertac, A., Alatas, C., Aksoy, S. & Mercan, R. (1998). Oocyte morphology does not affect fertilization rate, embryo quality and implantation rate alter intracytoplasmic sperm injection. Hum. Reprod. 13, 3431–3.CrossRefGoogle ScholarPubMed
Balakier, H., Sojecki, A., Motamedi, G., Bashar, S., Mandel, R. & Librach, C. (2012). Is the zona pellucida thickness of human embryos influenced by women's age and hormonal levels? Fertil. Steril. 98, 77–83.Google Scholar
Beall, S., Brenner, C. & Segars, J. (2010). Oocyte maturation failure: a syndrome of bad eggs. Fertil. Steril. 94, 2507–213.Google Scholar
Bloor, D.J., Metcalf, A.D., Rutherford, A., Brison, D.R. & Kimber, S.J. (2002). Expression of cell adhesion molecules during human preimplantation embryo development. Mol. Hum. Reprod. 8, 237–45.Google Scholar
Braga, A.F.D.P., Figueira, R.C.S., Queiroz, P., Madaschi, C., Iaconelli, A. & Borges, E. (2010). Zona pellucida birefringence in in vivo and in vitro matured oocytes. Fertil. Steril. 94, 2050–3.Google Scholar
Brunet, S. & Maro, B. (2005). Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction 130, 801–11.Google Scholar
Caballero-Campo, P., Chirinos, M., Fan, X.J., Gonzalez-Gonzalez, M.E., Galicia-Chavarria, M., Larrea, F. & Gerton, G.L. (2006). Biological effects of recombinant human zona pellucida proteins on sperm function. Biol. Reprod. 74, 760–8.Google Scholar
Chiu, P.C.N., Wong, B.S.T., Chung, M.-K., Lam, K.K.W., Pang, R.T.K., Lee, K.-F., Sumitro, S.B., Gupta, S.K. & Yeung, W.S.B. (2008). Effects of native human zona pellucida glycoproteins 3 and 4 on acrosome reaction and zona pellucida binding of human spermatozoa. Biol. Reprod. 79, 869–77.Google Scholar
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.Google Scholar
Dale, B., Tosti, E. & Iaccarino, M. (1995). Is the plasma membrane of the human oocyte reorganized following fertilization and early cleavage? Zygote 1, 31–6.Google Scholar
Dale, B., Wilding, M., Coppola, G.F. & Tosti, E. (2010). How do spermatozoa activate oocytes? Reprod. BioMed. Online 21, 1–3.Google Scholar
De Sutter, P., Dozortsev, D., Qian, C. & Dhont, M. (1996). Oocyte morphology does not correlate with fertilization rate and embryo quality after intracytoplasmic sperm injection. Hum. Reprod. 11, 595–7.CrossRefGoogle Scholar
Ebner, T., Yaman, C., Moser, M., Sommergruber, M., Feichtinger, O. & Tews, G. (2000). Prognostic value of first polar body morphology on fertilization rate and embryo quality in intracytoplasmic sperm injection. Hum. Reprod. 15, 427–30.CrossRefGoogle ScholarPubMed
Ebner, T., Shebl, O., Moser, M., Sommergruber, M. & Tews, G. (2008). Developmental fate of ovoid oocytes. Hum. Reprod. 23, 62–6.Google Scholar
Ebner, T., Balaban, B., Moser, M., Shebl, O., Urman, B., Ata, B. & Tews, G. (2010). Automatic user-independent zona pellucida imaging at the oocyte stage allows for the prediction of preimplantation development. Fertil. Steril. 94, 913–20.Google Scholar
El Shafie, M., Sousa, M., Windt, M.-L. & Kruger, T.F. (2000). An Atlas of the Ultrastructure of Human Oocytes. A Guide for Assisted Reproduction. Parthenon Publishing Group, New York, USA.Google Scholar
Esfandiari, N., Ryan, E.A.J., Gotlieb, L. & Casper, R.F. (2005). Successful pregnancy following transfer of embryos from oocytes with abnormal zona pellucida and cytoplasm morphology. Reprod. BioMed. Online 11, 620–3.Google Scholar
Furlong, L.I., Harris, J.D. & Vazquez-Levin, M.H. (2005). Binding of recombinant human proacrosin/acrosin to zona pellucida (ZP) glycoproteins. I. Studies with recombinant human ZPA, ZPB, and ZPC. Fertil. Steril. 83, 1780–190.Google Scholar
Gardner, D.K., Phil, D., Lane, M., Stevens, J., Schlenker, T. & Schoolcraft, W.B. (2000). Blastocyst score affects implantation and pregnancy outcome: towards a single blastocyst transfer. Fertil. Steril. 73, 1155–8.Google Scholar
Gasca, S., Pellestor, F., Assou, S., Loup, V., Anahory, T., Dechaud, H., De Vos, J. & Hamamah, S. (2007). Identifying new human oocyte marker genes: a microarray approach. Reprod. BioMed. Online 14, 175–83.Google Scholar
Green, D.P.L. (1997). Three-dimensional structure of the zona pellucida. Rev. Reprod. 2, 147–56.Google Scholar
Hasan, A.K.M.M., Matsumoto, T., Kihira, J., Yoshida, J. & Sato, K.-I. (2012). Phospho-signalling at oocyte maturation and fertilization: set up for embryogenesis and beyond. Part II. Kinase regulators and substrates. In Embryogenesis, (ed. Sato, K-I.). InTech, Croatia/China. pp. 499–554.Google Scholar
Kashir, J., Konstantinidis, M., Jones, C., Lemmon, B., Lee, H.C., Hamer, R., Heindryckx, B., Deane, C.M., De Sutter, P., Fissore, R.A., Parrington, J., Wells, D. & Coward, K. (2012). A maternally inherited autosomal point mutation in human phospholipase C zeta (PLCζ) leads to male infertility. Hum. Reprod. 27, 222–31.CrossRefGoogle ScholarPubMed
Kwon, S. & Lim, H.J. (2011). Small GTPases and formins in mammalian oocyte maturation: cytoskeletal organizers. Clin. Exp. Reprod. Med. 38, 1–5.Google Scholar
Lefièvre, L., Conner, S.J., Salpekar, A., Olufowobi, O., Ashton, P., Pavlovic, B., Lenton, W., Afnan, M., Brewis, I.A., Monk, M., Hughes, D.C. & Barratt, C.L.R. (2004). Four zona pellucida glycoproteins are expressed in the human. Hum. Reprod. 19, 1580–6.CrossRefGoogle ScholarPubMed
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
Madaschi, C., Aoki, T., Braga, D.P.A.F., Figueira, R.C.S., Francisco, L.S., Iaconelli, A. Jr. & Borges, E. (2009). Zona pellucida birefringence score and meiotic spindle visualization in relation to embryo development and ICSI outcomes. Reprod. BioMed. Online 18, 681–6.Google Scholar
Mansour, G., Abdelrazik, H., Sharma, R.K., Radwan, E., Falcone, T. & Agarwal, A. (2009). L-carnitine supplementation reduces oocyte cytoskeleton damage and embryo apoptosis induced by incubation in peritoneal fluid from patients with endometriosis. Fertil. Steril. 91, 2079–86.CrossRefGoogle ScholarPubMed
Meriano, J.S., Alexis, J., Visram-Zaver, S., Cruz, M. & Casper, R.F. (2001). Tracking of oocyte dysmorphisms for ICSI patients may prove relevant to the outcome in subsequent patient cycles. Hum. Reprod. 16, 2118–213.CrossRefGoogle Scholar
Montag, M., Schimming, T., Koster, M., Zhou, C., Dorn, C., Rosing, B., van der Ven, H. & van der Ven, K. (2008). Oocyte zona birefringence intensity is associated with embryonic implantation potential in ICSI cycles. Reprod. BioMed. Online 16, 239–44.CrossRefGoogle ScholarPubMed
Montag, M., Koster, M., van der Ven, K. & van der Ven, H. (2011). Gamete competence assessment by polarizing optics in assisted reproduction. Hum. Reprod. Update 17, 654–66.CrossRefGoogle ScholarPubMed
Mrazek, M. & Fulka, J. (2003). Failure of oocyte maturation: possible mechanisms for oocyte maturation arrest. Hum. Reprod. 18, 2249–52.Google Scholar
Palmstierna, M., Murkes, D., Csemiczky, G., Andersson, O. & Wramsby, H. (1998). Zona pellucida thickness variation and occurrence of visible mononucleated blastomeres in the embryos are associated with a high pregnancy rate in IVF treatment. J. Ass. Reprod. Genet. 15, 70–5.Google Scholar
Pelletier, C., Keef, D.L. & Trimarchi, J.R. (2004). Noninvasive polarized light microscopy quantitatively distinguishes the multilamellar structure of the zona pellucida of living human eggs and embryos. Fertil. Steril. 81(Suppl. 1), 850–6.Google Scholar
Pinto, F., Oliveira, C., Cardoso, M.F., Teixeira da Silva, J.M., Silva, J., Sousa, M. & Barros, A. (2009). Impact of GnRH stimulation protocols on intracytoplasmic sperm injection outcomes. Reprod. Biol. Endocrinol. 7, 1–10.Google Scholar
Plachot, M., Selva, J., Wolf, J.P., Bastit, P. & de Mouzon, J. (2002). Consequences of oocyte dysmorphy on the fertilization rate and embryo development after intracytoplasmic sperm injection. A prospective multicentric study. Gynecol. Obstet. Fertil. 30, 772–9.Google Scholar
Rama Raju, G.A., Prakash, G.J., Krishna, K.M. & Madan, K. (2007). Meiotic spindle and zona pellucida characteristics as predictors of embryonic development: a preliminary study using PolScope imaging. Reprod. BioMed. Online 14, 166–74.Google Scholar
Rankin, T., Familari, M., Lee, E., Ginsberg, A., Dwyer, N., Blanchette-Mackie, J., Drago, J., Westphal, H. & Dean, J. (1996). Mice homozygous for an insertional mutation in the Zp3 gene lack a zona pellucida and are infertile. Development 122, 2903–10.Google Scholar
Rankin, T.L., Talbot, P., Lee, E. & Dean, J. (1999). Abnormal zonae pellucida in mice lacking ZP1 result in early embryonic loss. Development 126, 3847–55.CrossRefGoogle ScholarPubMed
Rankin, T., O'Brien, M., Lee, E., Wigglesworth, K., Eppig, J. & Dean, J. (2001). Defective zonae pellucida in Zp2-null mice disrupt folliculogenesis, fertility and development. Development 128, 1119–26.Google Scholar
Reid, A.T., Redgrove, K., Aitken, R.J. & Nixon, B. (2011). Cellular mechanisms regulating sperm-zona pellucida interaction. Asian. J. Androl. 13, 88–96.Google Scholar
Rienzi, L., Ubaldi, F.M., Iacobelli, M., Minasi, M.G., Romano, S., Ferrero, S., Sapienza, F. & Baroni, E. (2008). Significance of metaphase II human oocyte morphology on ICSI outcome. Fertil. Steril. 90, 1682–700.Google Scholar
Rienzi, L., Vajta, G. & Ubaldi, F. (2011). Predictive value of oocyte morphology in human IVF: a systematic review of the literature. Hum. Reprod. Update 17, 34–45.Google Scholar
Sá, R., Cunha, M., Silva, J., Luís, A., Oliveira, C, Teixeira 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.Google Scholar
Shen, Y., Stalf, T., Mehnert, C., Eichenlaub-Ritter, U. & Tinneberg, H.-K. (2005). High magnitude of light retardation by the zona pellucida is associated with conception cycles. Hum. Reprod. 20, 1596–606.CrossRefGoogle ScholarPubMed
Sousa, M. & Tesarik, J. (1994). Ultrastructural analysis of fertilization failure after intracytoplasmic sperm injection. Hum. Reprod. 9, 2374–80.CrossRefGoogle ScholarPubMed
Sousa, M., Cremades, N., Silva, J., Oliveira, C., Teixeira da Silva, J., Viana, P. & Barros, A. (2002). Predictive value of testicular histology in secretory azoospermic subgroups and clinical outcome after microinjection of fresh and frozen–thawed sperm and spermatids. Hum. Reprod. 17, 1800–10.Google Scholar
Sousa, M., Barros, A., Silva, J. & Tesarik, J. (1997a). Developmental changes in calcium content of ultrastructurally distinct subcellular compartments of preimplantation human embryos. Mol. Hum. Reprod. 3, 83–90.Google Scholar
Sousa, M., Barros, A., Mendoza, C. & Tesarik, J. (1997b). Role of Ca2+ oscillations during human preimplantation embryo development. Ass. Reprod. Rev. 7, 139–50.Google Scholar
Stanger, J.D., Stevenson, K., Lakmaker, A. & Woolcott, R. (2001). Pregnancy following fertilization of zona-free, corona cell intact human ova: case report. Hum. Reprod. 16, 164–7.CrossRefGoogle Scholar
Ten, J., Mendiola, J., Vioque, J., de Juan, J. & Bernabeu, R. (2007). Donor oocyte dysmorphisms and their influence on fertilization and embryo quality. Reprod. Biomed. Online 14, 40–8.Google Scholar
Tesarik, J. & Sousa, M. (1995). Key elements of a highly efficient intracytoplasmic sperm injection technique: Ca2+ fluxes and oocyte cytoplasmic dislocation. Fertil. Steril. 64, 770–6.CrossRefGoogle ScholarPubMed
Vandervorst, M., Liebaers, I., Sermon, K., Staessen, C., De Vos, A., Van de Velde, H., Assche, E.V., Joris, H., Van Steirteghem, A. & Devroey, P. (1998). Successful preimplantation genetic diagnosis is related to the number of available cumulus–oocyte complexes. Hum. Reprod. 13, 3169–76.Google Scholar