[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content
Log in

Blastocyst hatching in humans

  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

The human oocyte is surrounded by the zona pellucida—an elastic, transparent extracellular matrix consisting of specific glycoproteins. The zona pellucida is preserved after fertilization and surrounds the developing human embryo for a few days. The embryo needs to get out of the zona pellucida before implantation to establish cell contacts between the trophectoderm and endometrial epithelium. The release of the embryo from the zona pellucida is carried out at the stage of the blastocyst and called zona hatching. During zona hatching the blastocyst breaks the zona pellucida and performs active movements to escape through a gap formed in the zona. While microscopic description of zone hatching is well known, biochemical and cytological basis of zone hatching remains poorly understood. The break of the zona pellucida occurs under the influence of two forces: mechanical pressure of the growing blastocyst on the zone and chemical dissolution of the zone material with secreted lytic enzymes. There is only one paper (Sathananthan et al., 2003), which describes the specialized cells in the trophectoderm that locally dissolve the zona pellucida, promoting the emergence of the hole for blastocyst release. Taking into account the singleness of the paper and the absence of further development of this subject by the authors in the following decade, the existence of specialized cells for zone hatching should be assumed with great care. Lytic enzymes, secreted by cells of the trophectoderm for dissolving the zona pellucida, are different. Depending on the species of the mammal, different classes of proteases participate in the zone hatching process: serine proteases, cysteine proteases, metal-loproteinases. Proteases, secreted by human trophectoderm, are not described. The mechanisms of the active movement during blastocyst hatching are investigated to a lesser degree. Only the involvement of the cytoskeleton of trophectoderm cells in the mechanism of blastocyst compression was shown, and the participation of desmosomes in the coordinated change in the form of trophectoderm cells during compression is suggested. This review summarizes literature data on the possible mechanisms of zone hatching in the development of human embryos, obtained in experiments in vitro, as well as in animal models.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adjaye, J., Whole-genome approaches for large-scale gene identification and expression analysis in mammalian preimplantation embryos, Reprod. Fertil. Dev., 2005, vol. 17, nos. 1–2, pp. 37–45.

    Article  CAS  PubMed  Google Scholar 

  • Balakier, H., Sojecki, A., Motamedi, G., et al., Is the zona pellucida thickness of human embryos influenced by women’s age and hormonal levels?, Fertil. Steril., 2012, vol. 98, no. 1, pp. 77–83.

    Article  CAS  PubMed  Google Scholar 

  • Barber, M.R., Lee, S.M., Steffens, W.L., et al., Immunolocalization of zona pellucida antigens in the ovarian follicle of dogs, cats, horses and elephants, Theriogenology, 2001, vol. 55, no. 8, pp. 1705–1717.

    Article  CAS  PubMed  Google Scholar 

  • Barisone, G.A., Krapf, D., Correa-Fiz, F., et al., Glycoproteins of the vitelline envelope of amphibian oocyte: biological and molecular characterization of ZPC component (gp41) in Bufo arenarum, Mol. Reprod. Dev., 2007, vol. 74, no. 5, pp. 629–640.

    Article  CAS  PubMed  Google Scholar 

  • Bianchi, E. and Wright, G.J., Izumo meets Juno: preventing polyspermy in fertilization, Cell Cycle, 2014, vol. 13, no. 13, pp. 2019–2020.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blackmore, D.G., Baillie, L.R., Holt, J.E., et al., Biosynthesis of the canine zona pellucida requires the integrated participation of both oocytes and granulosa cells, Biol. Reprod., 2004, vol. 71, no. 2, pp. 661–668.

    Article  CAS  PubMed  Google Scholar 

  • Bleil, J.D. and Wassarman, P.M., Structure and function of the zona pellucida: identification and characterization of the proteins of the mouse oocyte’s zona pellucida, Dev. Biol., 1980, vol. 76, no. 1, pp. 185–202.

    Article  CAS  PubMed  Google Scholar 

  • Boccaccio, A., Frassanito, M.C., Lamberti, L., et al., Nanoscale characterization of the biomechanical hardening of bovine zona pellucida, J. R. Soc. Interface, 2012, vol. 9, no. 76, pp. 2871–2882.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bogner, K., Hinsch, K.D., Nayudu, P., et al., Localization and synthesis of zona pellucida proteins in the marmoset monkey (Callithrix jacchus) ovary, Mol. Hum. Reprod., 2004, vol. 10, no. 7, pp. 481–488.

    Article  CAS  PubMed  Google Scholar 

  • Boja, E.S., Hoodbhoy, T., Garfield, M., et al., Structural conservation of mouse and rat zona pellucida glycoproteins. probing the native rat zona pellucida proteome by mass spectrometry, Biochemistry, 2005, vol. 44, no. 50, pp. 16445–16460.

    Article  CAS  PubMed  Google Scholar 

  • Bronson, R.A. and McLaren, A., Transfer to the mouse oviduct of eggs with and without the zona pellucida, J. Reprod. Fertil., 1970, vol. 22, no. 1, pp. 129–137.

    Article  CAS  PubMed  Google Scholar 

  • Burkart, A.D., Xiong, B., Baibakov, B., et al., Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy, J. Cell Biol., 2012, vol. 197, no. 1, pp. 37–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caballero-Campo, P., Chirinos, M., Fan, X.J., et al., Biological effects of recombinant human zona pellucida proteins on sperm function, Biol. Reprod., 2006, vol. 74, no. 4, pp. 760–768.

    Article  CAS  PubMed  Google Scholar 

  • Celik-Ozenci, C., Akkoyunlu, G., Kayisli, U.A., et al., Localization of vascular endothelial growth factor in the zona pellucida of developing ovarian follicles in the rat: a possible role in destiny of follicles, Histochem. Cell. Biol., 2003, vol. 120, no. 5, pp. 383–390.

    Article  CAS  PubMed  Google Scholar 

  • Clark, G.F., The mammalian zona pellucida: a matrix that mediates both gamete binding and immune recognition?, Syst. Biol. Reprod. Med., 2010, vol. 56, no. 5, pp. 349–364.

    Article  CAS  PubMed  Google Scholar 

  • Clark, G.F., The role of carbohydrate recognition during human sperm-egg binding, Hum. Reprod., 2013, vol. 28, no. 3, pp. 566–577.

    Article  CAS  PubMed  Google Scholar 

  • Clarysse, L., Guéguinou, M., Potier-Cartereau, M., et al., cAMP-PKA inhibition of SK3 channel reduced both Ca2+ entry and cancer cell migration by regulation of SK3-Orai1 complex, Pflugers. Arch., 2014, vol. 466, no. 10, pp. 1921–1932.

    Article  CAS  PubMed  Google Scholar 

  • Darie, C.C., Biniossek, M.L., Jovine, L., et al., Structural characterization of fish egg vitelline envelope proteins by mass spectrometry, Biochemistry, 2004, vol. 43, pp. 7459–7478.

    Article  CAS  PubMed  Google Scholar 

  • Dietl, J., Ultrastructural aspects of the developing mammalian zona pellucida, in The Mammalian Egg Coat: Structure and Function, Berlin: Springer-Verlag, 1989, pp. 49–60.

    Chapter  Google Scholar 

  • Drobnis, E., Andrew, J., and Katz, D., Biophysical properties of the zona pellucida measured by capillary suction: is zona hardening a mechanical phenomenon, J. Exp. Zool., 1988, vol. 245, no. 2, pp. 206–219.

    Article  CAS  PubMed  Google Scholar 

  • Eberspaecher, U., Becker, A., Bringmann, P., et al., Immunohistochemical localization of zona pellucida proteins ZPA, ZPB and ZPC in human, cynomolgus monkey and mouse ovaries, Cell. Tissue Res., 2001, vol. 303, no. 2, pp. 277–287.

    Article  CAS  PubMed  Google Scholar 

  • Familiari, G., Heyn, R., Relucenti, M., et al., Structural changes of the zona pellucida during fertilization and embryo development, Front. Biosci., 2008, vol. 1, no. 13, pp. 6730–6751.

    Article  Google Scholar 

  • Fierro-Gonzalez, J.C., White, M.D., Silva, J.C., et al., Cadherin-dependent filopodia control preimplantation embryo compaction, Nat. Cell. Biol., 2013, vol. 15, no. 12, pp. 1424–1433.

    Article  CAS  PubMed  Google Scholar 

  • Girault, A., Haelters, J.P., Potier-Cartereau, M., et al., New alkyl–lipid blockers of SK3 channels reduce cancer cell migration and occurrence of metastasis, Curr. Cancer. Drug. Targets, 2011, vol. 11, no. 9, pp. 1111–1125.

    Article  CAS  PubMed  Google Scholar 

  • Gogolevskii, P.A., Assisted hatching: indications, application, and results, Probl. Reprod., 1998, vol. 4, no. 1, pp. 10–13.

    Google Scholar 

  • Gonzales, D.S., Jones, J.M., Pinyopummintr, T., et al., Trophectoderm projections: a potential means for locomotion, attachment and implantation of bovine, equine and human blastocysts, Hum. Reprod., 1996, vol. 11, no. 12, pp. 2739–2745.

    Article  CAS  PubMed  Google Scholar 

  • Gook, D.A., Edgar, D.H., Borg, J., et al., Detection of zona pellucida proteins during human folliculogenesis, Hum. Reprod., 2008, vol. 23, no. 2, pp. 394–402.

    Article  CAS  PubMed  Google Scholar 

  • Goudet, G., Mugnier, S., Callebaut, I., et al., Phylogenetic analysis and identification of pseudogenes reveal a progressive loss of zona pellucida genes during evolution of vertebrates, Biol. Reprod., 2008, vol. 78, no. 5, pp. 796–806.

    Article  CAS  PubMed  Google Scholar 

  • Gupta, S.K. and Bhandari, B., Acrosome reaction: relevance of zona pellucida glycoproteins, Asian. J. Androl., 2011, vol. 13, no. 1, pp. 97–105.

    Article  CAS  PubMed  Google Scholar 

  • Gupta, S.K., Role of zona pellucida glycoproteins during fertilization in human, J. Reprod. Immunol., 2015, vol. 108, pp. 90–97.

    Article  CAS  PubMed  Google Scholar 

  • Han, L., Monné, M., Okumura, H., et al., Insights into egg coat assembly and egg-sperm interaction from the X-ray structure of full-length ZP3, Cell, 2010, vol. 143, no. 3, pp. 404–415.

    Article  CAS  PubMed  Google Scholar 

  • Harris, J.D., Hibler, D.W., Fontenot, G.K., et al., Cloning and characterization of zona pellucida genes and cdnas from a variety of mammalian species: the ZPA, ZPB and ZPC gene families, DNA Seq., 1994, vol. 4, no. 6, pp. 361–393.

    CAS  PubMed  Google Scholar 

  • Hedrick, J.L. and Wardrip, N.J., Isolation of the zona pellucida and purification of its glycoprotein families from pig oocytes, Anal. Biochem., 1986, vol. 157, pp. 63–70.

    Article  CAS  PubMed  Google Scholar 

  • Hoodbhoy, T., Joshi, S., Boja, E.S., et al., Human sperm do not bind to rat zonae pellucidae despite the presence of four homologous glycoproteins, J. Biol. Chem., 2005, vol. 280, no. 1, pp. 12721–12731.

    Article  CAS  PubMed  Google Scholar 

  • Huang, Z. and Wells, D., The human oocyte and cumulus cells relationship: new insights from the cumulus cell transcriptome, Mol. Hum. Reprod., 2010, vol. 16, no. 10, pp. 715–725.

    Article  CAS  PubMed  Google Scholar 

  • Izquierdo-Rico, M.J., Jiménez-Movilla, M., Llop, E., et al., Hamster zona pellucida is formed by four glycoproteins: ZP1, ZP2, ZP3, and ZP4, J. Proteome Res., 2009, vol. 8, no. 2, pp. 926–941.

    Article  CAS  PubMed  Google Scholar 

  • Jewgenow, K. and Rudolph, M., Timing and location of zona pellucida synthesis during oogenesis in domestic cats-an ultrastructural immunohistological investigation, J. Reprod. Fertil., vol. 57, no. Suppl. 2001, pp. 23–29.

    CAS  Google Scholar 

  • Jovine, L., Qi, H., Williams, Z., et al., Features that affect secretion and assembly of zona pellucida glycoproteins during mammalian oogenesis, Soc. Reprod. Fertil. Suppl., vol. 63, 2007, pp. 187–201.

    CAS  Google Scholar 

  • Kane, M.T., Morgan, P.M., and Coonan, C., Peptide growth factors and preimplantation development, Hum. Reprod. Update, 1997, vol. 3, no. 2, pp. 137–157.

    Article  CAS  PubMed  Google Scholar 

  • Kapur, R.P. and Johnson, L.V., Selective sequestration of an oviductal fluid glycoprotein in the perivitelline space of mouse oocytes and embryos, J. Exp. Zool., 1986, vol. 238, no. 2, pp. 249–260.

    Article  CAS  PubMed  Google Scholar 

  • Kawamura, K., Chen, Y., Shu, Y., et al., Promotion of human early embryonic development and blastocyst outgrowth in vitro using autocrine/paracrine growth factors, PLoS One, 2012, vol. 7, no. 11, p. e49328.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keefe, D., Tran, P., Pellegrini, C., et al., Polarized light microscopy and digital image processing identify a multilaminar structure of the hamster zona pellucida, Hum. Reprod., 1997, vol. 12, no. 6, pp. 1250–1252.

    Article  CAS  PubMed  Google Scholar 

  • Kiefer, S.M. and Saling, P., Proteolytic processing of human zona pellucida proteins, Biol. Reprod., 2002, vol. 66, no. 2, pp. 407–414.

    Article  CAS  PubMed  Google Scholar 

  • Kim, J. and Kim, J., Viscoelastic characterization of mouse zona pellucida, IEEE Trans. Biomed. Eng., 2013, vol. 60, no. 2, pp. 569–575.

    Article  PubMed  Google Scholar 

  • Kimura, T.E., Merritt, A.J., Lock, F.R., et al., Desmosomal adhesiveness is developmentally regulated in the mouse embryo and modulated during trophectoderm migration, Dev. Biol., 2012, vol. 369, no. 2, pp. 286–297.

    Article  CAS  PubMed  Google Scholar 

  • Kirkegaard, K., Hindkjaer, J.J., and Ingerslev, H.J., Human embryonic development after blastomere removal: a time-lapse analysis, Hum. Reprod, 2012, vol. 27, no. 1, pp. 97–105.

    Article  PubMed  Google Scholar 

  • Kirkegaard, K., Hindkjaer, J.J., and Ingerslev, H.J., Hatching of in vitro fertilized human embryos is influenced by fertilization method, Fertil. Steril., 2013, vol. 100, no. 5, pp. 1277–1282.

    Article  PubMed  Google Scholar 

  • Ko, C.S., Ding, D.C., Chu, T.W., et al., Changes to the meiotic spindle and zona pellucida of mature mouse oocytes following different cryopreservation methods, Anim. Reprod. Sci., 2008, vol. 105, nos. 3–4, pp. 272–282.

    Article  CAS  PubMed  Google Scholar 

  • Koblinski, J.E., Ahram, M., and Sloane, B.F., Unraveling the role of proteases in cancer, Clin. Chim. Acta, 2000, vol. 291, no. 2, pp. 113–135.

    Article  CAS  PubMed  Google Scholar 

  • Kolle, S., Sinowatz, F., Boie, G., et al., Differential expression of ZPC in the bovine ovary, oocyte, and embryo, Mol. Reprod. Dev., 1998, vol. 49, no. 2, pp. 435–443.

    Article  CAS  PubMed  Google Scholar 

  • Kolle, S., Dubois, C.S., Caillaud, M., et al., Equine zona protein synthesis and ZP structure during folliculogenesis, oocyte maturation, and embryogenesis, Mol. Reprod. Dev., 2007, vol. 74, no. 7, pp. 851–859.

    Article  PubMed  CAS  Google Scholar 

  • Lee, V.H., Expression of rabbit zona pellucida-1 messenger ribonucleic acid during early follicular development, Biol. Reprod., 2000, vol. 63, no. 2, pp. 401–408.

    Article  CAS  PubMed  Google Scholar 

  • Lefièvre, L., Conner, S.J., Salpekar, A., et al., Four zona pellucida glycoproteins are expressed in the human, Hum. Reprod., 2004, vol. 19, no. 7, pp. 1580–1586.

    Article  PubMed  Google Scholar 

  • Liu, C., Litscher, E.S., Mortillo, S., et al., Targeted disruption of the mZP3 gene results in production of eggs lacking a zona pellucida and infertility in female mice, Proc. Natl. Acad. Sci. U. S. A., 1996, vol. 93, no. 11, pp. 5431–5436.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, M., The biology and dynamics of mammalian cortical granules, Reprod. Biol. Endocrinol., 2011, vol. 9, p. 149.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopata, A. and Hey, D.L., The potential of early human to form blastocysts, hatch from their zona and secrete HCG in culture, Hum. Reprod., 1989, vol. 4 (suppl.), pp. 87–94.

    Google Scholar 

  • Louros, N.N., Iconomidou, V.A., Giannelou, P., et al., Structural analysis of peptide-analogues of human zona pellucida ZP1 protein with amyloidogenic properties: insights into mammalian zona pellucida formation, PLoS One, 2013, vol. 8, no. 9, p. e73258.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu, Y.C., Ding, G.L., Yang, J., et al., Small-conductance calcium-activated K(+) channels 3 (SK3) regulate blastocyst hatching by control of intracellular calcium concentration, Hum. Reprod., 2012, vol. 27, no. 5, pp. 1421–1430.

    Article  CAS  PubMed  Google Scholar 

  • Magerkurth, C., Töpfer-Petersen, E., Schwartz, P., et al., Scanning electron microscopy analysis of the human zona pellucida: influence of maturity and fertilization on morphology and sperm binding pattern, Hum. Reprod., 1999, vol. 14, no. 4, pp. 1057–1066.

    Article  CAS  PubMed  Google Scholar 

  • Menezes, J., Gunasheela, S., and Sathananthan, H., Video observations on human blastocyst hatching, Reprod. Biomed. Online, 2003, vol. 7, no. 2, pp. 217–218.

    Article  PubMed  Google Scholar 

  • Meslin, C., Mugnier, S., Callebaut, I., et al., Evolution of genes involved in gamete interaction: evidence for positive selection, duplications and losses in vertebrates, PLoS One, 2012, vol. 7, no. 9, pp. 44–48.

    Article  CAS  Google Scholar 

  • Michelmann, H.W., Rath, D., Töpfer-Petersen, E., et al., Structural and functional events on the porcine zona pellucida during maturation, fertilization and embryonic development: a scanning electron microscopy analysis, Reprod. Domest. Anim., 2007, vol. 42, no. 6, pp. 594–602.

    Article  CAS  PubMed  Google Scholar 

  • Mio, Y. and Maeda, K., Time-lapse cinematography of dynamic changes occurring during in vitro development of human embryos, Am. J. Obstet. Gynecol., 2008, vol. 199, no. 6, pp. 1–5.

    Article  Google Scholar 

  • Mio, Y., Iwata, K., Yumoto, K., et al., Possible mechanism of polyspermy block in human oocytes observed by time-lapse cinematography, J. Assist. Reprod. Genet., 2012, vol. 29, no. 9, pp. 951–956.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mishra, A. and Seshagiri, P.B., Heparin binding-epidermal growth factor improves blastocyst hatching and trophoblast outgrowth in the golden hamster, Reprod. Biomed. Online, 2000, vol. 1, no. 3, pp. 87–95.

    Article  CAS  PubMed  Google Scholar 

  • Monné, M. and Jovine, L., A structural view of egg coat architecture and function in fertilization, Biol. Reprod., 2011, vol. 85, no. 4, pp. 661–669.

    Article  PubMed  CAS  Google Scholar 

  • Murayama, Y., Mizuno, J., Kamakura, H., et al., Mouse zona pellucida dynamically changes its elasticity during oocyte maturation, fertilization and early embryo development, Human Cell, 2006, vol. 19, no. 4, pp. 119–125.

    Article  PubMed  Google Scholar 

  • Novo, S., Barrios, L., Ibáñez, E., et al., The zona pellucida porosity: three-dimensional reconstruction of four types of mouse oocyte zona pellucida using a dual beam microscope, Microsc. Microanal., 2012, vol. 18, no. 6, pp. 1442–1449.

    Article  CAS  PubMed  Google Scholar 

  • Odor, D.L. and Blandau, R.J., Ultrastructural studies on fetal and early postnatal mouse ovaries. i. histogenesis and organogenesis, Am. J. Anat., 1969, vol. 124, no. 2, pp. 163–186.

    Article  CAS  PubMed  Google Scholar 

  • O’Sullivan, C.M., Liu, S.Y., Karpinka, J.B., et al., Embryonic hatching enzyme strypsin/ISP1 is expressed with ISP2 in endometrial glands during implantation, Mol. Reprod. Dev., 2002, vol. 62, no. 3, pp. 328–334.

    Article  PubMed  CAS  Google Scholar 

  • Ozawa, M., Sakatani, M., Yao, J., et al., Global gene expression of the inner cell mass and trophectoderm of the bovine blastocyst, BMC Dev. Biol., 2012, vol. 12, p. 33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan, X., Wang, X., Wang, X., et al., Nitric oxide regulates blastocyst hatching in mice, Int. J. Clin. Exp. Med., 2015, vol. 8, no. 5, pp. 6994–7001.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pökkylä, R.M., Lakkakorpi, J.T., Nuojua-Huttunen, S.H., et al., Sequence variations in human ZP genes as potential modifiers of zona pellucida architecture, Fertil. Steril., 2011, vol. 95, no. 8, pp. 2669–2672.

    Article  PubMed  CAS  Google Scholar 

  • Potier, M., Joulin, V., Roger, S., et al., Identification of SK3 channel as a new mediator of breast cancer cell migration, Mol. Cancer. Ther., 2006, vol. 5, no. 11, pp. 2946–2953.

    Article  CAS  PubMed  Google Scholar 

  • Quesada, V., Sanchez, L.M., Alvarez, J., et al., Identification and characterization of human and mouse ovastacin: a novel metalloproteinase similar to hatching enzymes from arthropods, birds, amphibians, and fish, J. Biol. Chem., 2004, vol. 279, no. 25, pp. 26627–26634.

    Article  CAS  PubMed  Google Scholar 

  • Rankin, T., Familari, M., Lee, E., et al., Mice homozygous for an insertional mutation in the Zp3 gene lack a zona pellucida and are infertile, Development, 1996, vol. 122, no. 9, pp. 2903–2910.

    CAS  PubMed  Google Scholar 

  • Rankin, T., Soyal, S., and Dean, J., The mouse zona pellucida: folliculogenesis, fertility, and preimplantation development, Mol. Cell. Endocrinol., 2000, vol. 163, nos. 1–2, pp. 21–25.

    Article  CAS  PubMed  Google Scholar 

  • Rankin, T.L., O’Brien, M., Lee, E., et al., Defective zonae pellucidae in Zp2-null mice disrupt folliculogenesis, fertility and development, Development, 2001, vol. 128, no. 7, pp. 1119–1126.

    CAS  PubMed  Google Scholar 

  • Richter, K.S., The importance of growth factors for preimplantation embryo development and in-vitro culture, Curr. Opin. Obstet. Gynecol., 2008, vol. 20, no. 3, pp. 292–304.

    Article  PubMed  Google Scholar 

  • Sargent, I.L., Martin, K.L., and Barlow, D.H., The use of recombinant growth factors to promote human embryo development in serum-free medium, Hum. Reprod., 1998, vol. 4, suppl. 13, pp. 239–248.

    Article  Google Scholar 

  • Sathananthan, H., Menezes, J., and Gunasheela, S., Mechanics of human blastocyst hatching in vitro, Reprod. Biomed. Online, 2003, vol. 7, no. 2, pp. 228–234.

    Article  PubMed  Google Scholar 

  • Sellens, M.H. and Jenkinson, E.J., Permeability of the mouse zona pellucida to immunoglobulins, J. Reprod. Fertil., 1975, vol. 42, no. 1, pp. 153–157.

    Article  CAS  PubMed  Google Scholar 

  • Serdarogullari, M., Findikli, N., Goktas, C., et al., Comparison of gender-specific human embryo development characteristics by time-lapse technology, Reprod. Biomed. Online, 2014, vol. 29, no. 2, pp. 193–199.

    Article  PubMed  Google Scholar 

  • Serizawa, M., Kinoshita, M., Rodler, D., et al., Oocytic expression of zona pellucida protein ZP4 in Japanese quail (Coturnix japonica), Anim. Sci. J., 2011, vol. 82, no. 2, pp. 227–235.

    Article  CAS  PubMed  Google Scholar 

  • Seshagiri, P.B., Mishra, A., Ramesh, G., et al., Regulation of peri-attachment embryo development in the golden hamster: role of growth factors, J. Reprod. Immunol., 2002, vol. 53, nos. 1–2, pp. 203–213.

    Article  CAS  PubMed  Google Scholar 

  • Seshagiri, P.B., Sen Roy, S., Sireesha, G., et al., Cellular and molecular regulation of mammalian blastocyst hatching, J. Reprod. Immunol., 2009, vol. 83, nos. 1–2, pp. 79–84.

    Article  CAS  PubMed  Google Scholar 

  • Sharma, N., Kumar, R., Renaux, B., et al., Implantation serine proteinase 1 exhibits mixed substrate specificity that silences signaling via proteinase-activated receptors, PLoS One, 2011, vol. 6, no. 11, p. e27888.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen, Y., Stalf, T., Mehnert, C., et al., High magnitude of light retardation by the zona pellucida is associated with conception cycles, Hum. Reprod., 2005, vol. 20, no. 6, pp. 1596–1606.

    Article  CAS  PubMed  Google Scholar 

  • Sinowatz, F., Kolle, S., and Topfer-Petersen, E., Biosynthesis and expression of zona pellucida glycoproteins in mammals, Cells. Tissues. Organs, 2001, vol. 168, nos. 1–2, pp. 24–35.

    CAS  PubMed  Google Scholar 

  • Sireesha, G.V., Mason, R.W., Hassanein, M., et al., Role of cathepsins in blastocyst hatching in the golden hamster, Mol. Hum. Reprod., 2008, vol. 14, no. 6, pp. 337–346.

    Article  CAS  PubMed  Google Scholar 

  • Van Soom, A., Wrathall, A.E., Herrler, A., et al., Is the zona pellucida an efficient barrier to viral infection?, Reprod. Fertil. Dev., 2010, vol. 22, no. 1, pp. 21–31.

    Article  PubMed  Google Scholar 

  • Sterchi, E.E., Stöcker, W., and Bond, J.S., Meprins, membrane-bound and secreted astacin metalloproteinases, Mol. Aspects. Med., 2008, vol. 29, no. 5, pp. 309–328.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stetson, I., Avilés, M., Moros, C., et al., Four glycoproteins are expressed in the cat zona pellucida, Theriogenology, 2015, vol. 83, no. 7, pp. 1162–11673.

    Article  CAS  PubMed  Google Scholar 

  • Sun, Q.Y., Cellular and molecular mechanisms leading to cortical reaction and polyspermy block in mammalian eggs, Microsc. Res. Tech., 2003, vol. 61, no. 4, pp. 342–348.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki, H., Togashi, M., Adachi, J., et al., Developmental ability of zona-free mouse embryos is influenced by cell association at the 4-cell stage, Biol. Reprod., 1995, vol. 53, no. 1, pp. 78–83.

    Article  CAS  PubMed  Google Scholar 

  • Swiatecka, J., Bielawski, T., Anchim, T., et al., Oocyte zona pellucida and meiotic spindle birefringence as a biomarker of pregnancy rate outcome in IVF-ICSI treatment, Ginekol. Pol., 2014, vol. 85, no. 4, pp. 264–271.

    Article  PubMed  Google Scholar 

  • Thouas, G.A., Dominguez, F., Green, M.P., et al., Soluble ligands and their receptors in human embryo development and implantation, Endocr. Rev., 2015, vol. 36, no. 1, pp. 92–130.

    Article  CAS  PubMed  Google Scholar 

  • Thurin, A., Rogberg, L., Lundin, K., et al., Assisted hatching: is it worthwhile?, Human Reprod., 1998, vol. 13, p. 45.

    Article  Google Scholar 

  • Vajta, G., Rienzi, L., and Bavister, B.D., Zona-free embryo culture: is it a viable option to improve pregnancy rates?, Reprod. Biomed. Online, 2010, vol. 21, no. 1, pp. 17–25.

    Article  PubMed  Google Scholar 

  • Veeck, L. and Zaninovic, N., Blastocyst hatching, in An Atlas of Human Blastocysts, London: Parthenon Publishing, 2003, pp. 159–171.

    Google Scholar 

  • Wassarman, P.M., Zona pellucida glycoproteins, J. Biol. Chem., 2008, vol. 283, no. 36, pp. 24285–24289.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wassarman, P.M. and Litscher, E.S., Influence of the zona pellucida of the mouse egg on folliculogenesis and fertility, Int. J. Dev. Biol., 2012, vol. 56, nos. 10–12, pp. 833–839.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. A. Shafei.

Additional information

Original Russian Text © R.A. Shafei, A.G. Syrkasheva, A.Yu. Romanov, N.P. Makarova, N.V. Dolgushina, M.L. Semenova, 2017, published in Ontogenez, 2017, Vol. 48, No. 1, pp. 8–20.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shafei, R.A., Syrkasheva, A.G., Romanov, A.Y. et al. Blastocyst hatching in humans. Russ J Dev Biol 48, 5–15 (2017). https://doi.org/10.1134/S1062360417010106

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062360417010106

Keywords

Navigation