First Stages of Development

Kay Elder; Brian Dale

doi:10.1017/9781108611633.006

Chapter 5 - First Stages of Development

Published online by Cambridge University Press: 24 December 2019

Kay Elder and

Brian Dale

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Kay Elder: Affiliation:
Bourn Hall Clinic, Cambridge
Brian Dale: Affiliation:
Centre for Assisted Reproduction, Naples

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Summary

After completing fertilization with fusion of the pronuclei during syngamy, the zygote now has a diploid complement of chromosomes, undergoes its first mitotic division and then continues to divide by mitosis into a number of smaller cells known as blastomeres. In humans, the first few cleavage divisions take place in the oviduct, before the embryo reaches its site of implantation in the uterus (Figure 5.1).

Type: Chapter
Information: In-Vitro Fertilization , pp. 97 - 119

DOI: https://doi.org/10.1017/9781108611633.006 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2020

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References

Primary Sources

Balinsky, BI (1965) An Introduction to Embryology. Saunders, London.Google Scholar

Cummins, JM, Jequier, AM, Kan, R (1994) Molecular biology of human male infertility: links with ageing, mitochondrial genetics, and oxidative stress? Molecular Reproduction and Development 37: 345–362.Google Scholar

Dekel, N (1996) Protein phosphorylation/dephosphorylation in the meiotic cell cycle of mammalian oocytes. Reviews of Reproduction 1: 82–88.Google Scholar

Eddy, EM (1998) Regulation of gene expression during spermatogenesis. Seminars in Cell and Developmental Biology 19: 451–457.Google Scholar

Eppig, JJ (2001) Oocyte control of ovarian follicular development and function in mammals. Reproduction 122: 829–838.Google Scholar

Gilchrist, RB, Lane, M, Thompson, JG (2008) Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Human Reproduction Update 14(2): 159–177.CrossRef Google Scholar PubMed

Jurisicova, A, Acton, BM (2004) Deadly decisions: the roles of genes regulating programmed cell death in human preimplantation embryo development. Reproduction 128(3): 281–291.Google Scholar

Kane, MT, Morgan, PM, Coonan, C (1997) Peptide growth factors and preimplantation development. Human Reproduction Update 3: 137–157.Google Scholar

Kola, I, Trounson, A (1989) Dispermic Human Fertilization: Violation of Expected Cell Behaviour. Academic Press, San Diego.Google Scholar

Masui, Y (2001) From oocyte maturation to the in vitro cell cycle: the history of discoveries of Maturation Promoting Factor (MPF) and Cytostatic Factor (CSF). Differentiation 69: 1–17.CrossRef Google Scholar

Ménézo, Y, Dale, B, Cohen, M (2010) DNA damage and repair in human oocytes and embryos: a review. Zygote 18(4): 357–365.Google Scholar

Reik, W, Dean, W, Walter, J (2001) Epigenetic reprogramming in mammalian development (Review). Science 293: 1089–1093.Google Scholar

Sathananthan, AH, Ng, SC, Bongo, A, Trounson, A, Ratnam, S (1993) Visual Atlas of Early Human Development of Assisted Reproduction Technology. Singapore University Press, Singapore.Google Scholar

Schultz, RM (2002) The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Human Reproduction Update 8(4): 323–331.Google Scholar

Tosti, E (2006) Calcium ion currents mediating oocyte maturation events (Review). Reproductive Biology and Endocrinology 4: 26–35.CrossRef Google Scholar

Van den Bergh, M, Ebner, T, Elder, K (2012) Atlas of Oocytes, Zygotes and Embryos in Reproductive Medicine. Cambridge University Press, Cambridge, UK.Google Scholar

Secondary Sources

Adams, JM, Cory, S (1998) The Bcl-2 protein family: arbiters of cell survival. Science 281: 1322–1326.CrossRef Google Scholar PubMed

Adenot, PG, Mercier, Y, Renard, JP, Thompson, EM (1997) Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. Development 124(22): 4615–4625.Google Scholar

Alikani, M (2007) The origins and consequences of fragmentation in mammalian oocytes and embryos. In: Elder, K, Cohen, J (eds.) Human Preimplantation Embryo Selection. Taylor-Francis, London, pp. 51–78.Google Scholar

Alikani, M, Cohen, J, Tomkin, G, et al. (1999) Human embryo fragmentation in vitro and its implications for pregnancy and implantation. Fertility and Sterility 71: 836–842.Google Scholar

Antczak, M, Van Blerkom, J (1997) Oocyte influences on early development: the regulatory proteins leptin and STAT3 are polarized in mouse and human oocytes and differentially distributed within the cells of the preimplantation stage embryo. Molecular Human Reproduction 3: 1067–1086.Google Scholar

Ao, A, Erickson, RP, Winston, RML, Handyside, AH (1994) Transcription of paternal Y-linked genes in the human zygote as early as the pronucleate stage. Zygote 2: 281–287.Google Scholar

Bachvarova, R (1992) A maternal tail of poly(A): the long and short of it. Cell 69: 895–897.CrossRef Google Scholar

Baines, KJ, Renaud, SJ (2017) Transcription factors that regulate trophoblast development and function. Progress in Molecular Biology Translational Science 145: 39–88.Google Scholar

Barritt, J, Brenner, CA, Cohen, J, Matt, DW (1999) Mitochondrial DNA rearrangements in oocytes and embryos. Molecular Human Reproduction 5(10): 927–933.Google Scholar

Bateson, P, Barker, D, Clutton-Brock, T, et al. (2004) Developmental plasticity and human health. Nature 430(6998): 419–421.Google Scholar

Benkhalifa, M, Montjean, D, Cohen-Bacrie, P, Ménézo, Y (2010) Imprinting: RNA expression for homocysteine recycling in the human oocyte. Fertility and Sterility 93(5): 1585–1590.Google Scholar

Blakeley, P, Fogarty, NME, del Valle, I, et al. (2015) Defining the three cell lineages of the human blastocyst by single-cell RNA-seq. Development 142: 3151–3165.Google Scholar

Bonnerot, C, Vernet, M, Grimber, G, Brioand, P, Nicolas, JF (1993) Transcriptional selectivity in early mouse embryos: a qualitative study. Bioessays 15(8): 531–538.Google Scholar

Bouniol-Baly, C, Nguyen, E, Besombes, D, Debey, P (1997) Dynamic organization of DNA replication in one-cell mouse embryos: relationship to transcriptional activation. Experimental Cell Research 236: 201–211.CrossRef Google Scholar PubMed

Braude, P, Bolton, V, Moore, S (1988) Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature 332: 459–461.Google Scholar

Brenner, C, Wolny, YM, Adler, RR, Cohen, J (1999) Alternative splicing of the telomerase catalytic submit in human oocytes and embryos. Molecular Human Reproduction 5(9): 845–850.Google Scholar

Brenner, CA, Wolny, YM, Barritt, JA, et al. (1998) Mitochondrial DNA deletion in human oocytes and embryos. Molecular Human Reproduction 4(9): 887–892.Google Scholar

Brison, DR, Schulz, RM (1997) Apoptosis during mouse blastocyst formation: evidence for a role for survival factors including transforming growth factor alpha. Biology of Reproduction 56: 1088–1096.Google Scholar

Brison, DR, Schulz, RM (1998) Increased incidence of apoptosis in TGF-alpha deficient mouse blastocysts. Biology of Reproduction 59: 136–144.Google Scholar

Calarco, PG (1995) Polarization of mitochondria in the unfertilized mouse oocyte. Developmental Genetics 16: 36–43.Google Scholar

Chen, C, Sathanantan, AH (1986) Early penetration of human sperm through the vestments of human eggs in vitro. Archives of Andrology 16: 183–197.Google Scholar

Cho, WK, Stern, S, Biggers, JD (1974) Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. Journal of Experimental Zoology 187: 383–386.CrossRef Google Scholar PubMed

Clayton, L, McConnell, JM, Johnson, MH (1995) Control of the surface expression of uvomorulin after activation of mouse oocytes. Zygote 3(2): 177–189.Google Scholar

Conaghan, J, Handyside, AH, Winston, RM, Leese, HJ (1993) Effects of pyruvate and glucose on the development of human preimplantation embryos in vitro. Journal of Reproduction and Fertility 99(1): 87–95.Google Scholar

Coticchio, G, Fleming, S (1998) Inhibition of phosphoinositide metabolism or chelation of intracellular calcium blocks FSH-induced but not spontaneous meiotic resumption in mouse oocytes. Developmental Biology 203: 201–209.Google Scholar

Dale, B, Gualtieri, R, Talevi, R, et al. (1991) Intercellular communication in the early human embryo. Molecular Reproduction and Development 29: 22–28.Google Scholar

Dale, B, Marino, M, Wilding, M (1998) Sperm-induced calcium oscillations: soluble factor, factors or receptors? Molecular Human Reproduction 5: 1–4.Google Scholar

Dale, B, Tosti, E, Iaccarino, M (1995) Is the plasma membrane of the human oocyte re-organized following fertilization and early cleavage? Zygote 3: 31–37.Google Scholar

Delhanty, JDA, Harper, JC, Ao, A, Handyside, AH, Winston, RML (1997) Multicolour FISH detects frequent chromosomal mosaicism and chaotic division in normal preimplantation embryos from fertile patients. Human Genetics 99: 755–760.Google Scholar

De Sousa, PA, Caveney, A, Westhusin, ME, Watson, AJ (1998) Temporal patterns of embryonic gene expression and their dependence on oogenetic factors. Theriogenology 49: 115–128.Google Scholar

Dobson, AT, Raja, R, Abeyta, MJ, et al (2004) The unique transcriptome through day 3 of human preimplantation development. Human Molecular Genetics 13(14): 1461–1470.Google Scholar

Dominko, T, First, N (1997) Timing of meiotic progression in bovine oocytes and its effect on early embryo development. Molecular Reproduction and Development 47: 456–467.3.0.CO;2-U>CrossRef Google Scholar PubMed

Dulcibella, T (1996) The cortical reaction and development of activation competence in mammalian oocytes. Human Reproduction Update 2(1): 29–42.Google Scholar

Edwards, RG, Beard, H (1997) Oocyte polarity and cell determination in early mammalian embryos. Molecular Human Reproduction 3: 868–905.Google Scholar

Edwards, RG, Hansis, C (2005) Initial differentiation of blastomeres in 4-cell human embryos and its significance for early embryogenesis and implantation. Reproductive BioMedicine Online 11(2): 206–218.Google Scholar

Eichenlaub-Ritter, U (2002) Manipulation of the oocyte: possible damage to the spindle apparatus. Reproductive BioMedicine Online 5: 117–124.Google Scholar

Eppig, JJ, Chesnel, F, Hirao, Y, et al. (1997) Oocyte control of granulosa cell development: how and why. Human Reproduction 12(11 Suppl.): 127–132.Google Scholar

Flach, G, Johnsom, MH, Braude, PR, Taylor, RAS, Bolton, VN (1982) The transition from maternal to embryonic control in the 2-cell mouse embryo. The EMBO Journal 1(6): 681–686.CrossRef Google Scholar PubMed

Fogarty, NME, McCarthy, A, Snijders, KE, et al. (2017) Genome editing reveals a role for OCT4 in human embryogenesis. Nature 550: 67–73.Google Scholar

Fulka, J Jr., First, NL, Moor, RM (1998) Nuclear and cytoplasmic determinants involved in the regulation of mammalian oocyte maturation. Molecular Human Reproduction 4: 41–49.Google Scholar

Fulka, H, Mrazek, M, Tepla, O, Fulka, J (2004) DNA methylation pattern in human zygotes and developing embryos. Reproduction 128: 703–708.Google Scholar

Gabdoulline, R, Kaisers, W, Gaspar, A, et al. (2015) Differences in the early development of human and mouse embryonic stem cells. PLoS One 10(10): e0140803.CrossRef Google Scholar

Galan, A, Montaner, DD, Poo, M, et al. (2010) Functional genomics of 5- to 8-cell stage human embryos by blastomere single-cell cDNA analysis. PLoS One 5: e13615.Google Scholar

Gardner, DK (1998) Changes in requirements and utilization of nutrients during mammalian preimplantation embryo development and their significance in embryo culture. Theriogenology 49: 83–102.Google Scholar

Gardner, DK, Lane, M (1993) Amino acids and ammonium regulate mouse embryo development in culture. Biology of Reproduction 48(2): 377–385.Google Scholar

Gardner, RL (2001) Specification of embryonic axes begins before cleavage in normal mouse development. Development 128(6): 839–847.Google Scholar

Gardner, RL (2007) The axis of polarity of the mouse blastocyst is specified before blastulation and independently of the zona pellucida. Human Reproduction 22: 798–806.Google Scholar

Glabowski, W, Kurzawa, R, Wisniewska, B, et al. (2005) Growth factors effects on preimplantation development of mouse embryos exposed to tumour necrosis factor alpha. Reproductive Biology 5(1): 83–99.Google Scholar

Glinsky, G, Durruthy, J, Wossidlo, M et al. (2018) Single cell expression analysis of primate-specific retroviruses-derived HPAT lincRNAs in viable human blastocysts identifies embryonic cells co-expressing genetic markers of multiple lineages. Heliyon 4(2018): e00667.Google Scholar

Gopichandran, N, Leese, HJ (2003) Metabolic characterisation of the bovine blastocyst, inner cell mass, trophectoderm and blastocoel fluid. Reproduction 126: 299–308.Google Scholar

Grammont, G, Irvine, KD (2002) Organiser activity of the polar cells during Drosophila oogenesis. Development 129: 5131–5140.Google Scholar

Gregory, L (1998) Ovarian markers of implantation potential in assisted reproduction. Human Reproduction 13(Suppl. 4): 117–132.Google Scholar

Grobstein, C (1988) Biological characteristics of the preembryo. Annals of the New York Academy of Sciences 541: 346–348.Google Scholar

Gualtieri, R, Santella, L, Dale, B (1992) Tight junctions and cavitation in the human pre-embryo. Molecular Reproduction and Development 32: 81–87.Google Scholar

Guyader-Joly, C, Khatchadourian, C, Ménézo, Y (1996) Comparative glucose and fructose incorporation and conversion by in vitro produced bovine embryos. Zygote 4: 85–91.Google Scholar

Hales, BF, Barton, TS, Robaire, B (2005) Impact of paternal exposure to chemotherapy on offspring in the rat. Journal of the National Cancer Institute Monograph 34: 28–31.Google Scholar

Hales, BF, Robaire, B (2001) Paternal exposure to drugs and environmental chemicals: effects on progeny outcome. Journal of Andrology 22(6): 927–936.Google Scholar

Hamatani, T, Carter, MG, Sharov, AA, Ko, MS (2004) Dynamics of global gene expression changes during mouse preimplantation development. Developmental Cell 6(1): 117–131.Google Scholar

Hamberger, L, Nilsson, L, Sjögren, A (1998) Microscopic imaging techniques: practical aspects. Human Reproduction 13: Abstract book 1: 15, L.Google Scholar

Hansis, C, Grifo, JA, Tang, Y, Krey, LC (2002) Assessment of beta-HCG, beta-LH mRNA and ploidy in individual human blastomeres. Reproductive BioMedicine Online 5(2): 156–161.CrossRef Google Scholar PubMed

Hardy, K (1999) Apoptosis in the human embryo. Reviews of Reproduction 4: 125–134.CrossRef Google Scholar PubMed

Harper, JC, Delhanty, JDA (2008) Preimplantation genetic diagnosis. In: Rodeck, CH, Whittle, MJ (eds.) Fetal Medicine: Basic Science and Clinical Practice, 2nd edn. Churchill Livingstone, Edinburgh, pp. 323–330.Google Scholar

Heidmann, O, Vernochet, C, Dupressoir, A, Heidmann, T (2009) Identification of an endogenous retroviral envelope gene with fusogenic activity and placenta-specific expression in the rabbit: a new ‘syncytin’ in a third order of mammals. Retrovirology 6: 107.Google Scholar

Heikinheimo, O, Gibbons, W (1998) The molecular mechanisms of oocyte maturation and early embryonic development are unveiling new insights into reproductive medicine. Molecular Human Reproduction 4(8): 745–756.Google Scholar

Henery, CC, Miranda, M, Wiekowski, M, Wilmut, I, DePamphilis, ML (1995) Repression of gene expression at the beginning of mouse development. Developmental Biology 169(2): 448–460.Google Scholar

Henkel, R, Miller, C, Miska, H, Gips, H, Schill, WB (1993) Early embryology: determination of the acrosome reaction in human spermatozoa is predictive of fertilization in vitro. Human Reproduction 8(12): 2128–2132.Google Scholar

Hertig, AT, Rock, J, Adams, EC (1956) A description of 34 human ova within the first 17 days of development. American Journal of Anatomy 98(3): 435–493.Google Scholar

Hertig, A, Rock, J, Adams, E, Mulligan, W (1954) On the preimplantation stages of the human ovum: a description of four normal and four abnormal specimens ranging from the second to the fifth day of development. Contributions to Embryology of the Carnegie Institution of Washington 35: 119–220.Google Scholar

Hewitson, LC, Simerly, CR, Dominko, T, Schatten, G (2000) Cellular and molecular events after in vitro fertilization and intracytoplasmic sperm injection. Theriogenology 53: 95–104.Google Scholar

Hewitson, LC, Simerly, C, Schatten, G (1997) Inheritance defects of the sperm centrosome in humans and its possible role in male infertility. International Journal of Andrology 20(Suppl. 3): 35–43.Google Scholar

Hewitson, LC, Simerly, CR, Tengowski, MW, et al. (1996) Microtubule and chromatin configuration during Rhesus intracytoplasmic sperm injection: successes and failures. Biology of Reproduction 55: 271–280.Google Scholar

Houghton, FD (2005) Role of gap junctions during early embryo development. Reproduction 129: 129–131.Google Scholar

Houghton, FD (2006) Energy metabolism of the inner cell mass and trophectoderm of the mouse blastocyst. Differentiation 74: 11–18.CrossRef Google Scholar PubMed

Huang, TTF, Chinn, K, Kosasa, T, et al. (2016) Morphokinetics of human blastocyst expansion in vitro. Reproductive BioMedicine Online 33: 659–667.Google Scholar

Huarte, J, Stutz, A, O’Connell, ML, et al. (1992) Transient translational silencing by reversible mRNA deadenylation. Cell 69: 1021–1030.Google Scholar

Ivanov, PL, Wadhams, MJ, Roby, RK, et al. (1996) Mitochondrial DNA sequence heteroplasmy in the Grand Duke of Russia Georgij Romanov establishes the authenticity of the remains of Tsar Nicholas II. Nature Genetics 12: 417–420.Google Scholar

Janny, L, Ménézo, YJR (1994) Evidence for a strong paternal effect on human preimplantation embryo development and blastocyst formation. Molecular Reproduction and Development 38: 36–42.Google Scholar

Jansen, S, Esmaeilpour, T, Pantaleon, M, Kaye, PL (2006) Glucose affects monocarboxylate cotransporter (MCT) 1 expression during mouse preimplantation development. Reproduction and Fertility 131: 469–479.Google Scholar

Jennings, MO, Owen, RC, Keefe, DD, Kim, ED (2017) Management and counseling of the male with advanced paternal age. Fertility and Sterility 107(2): 324–328.Google Scholar

Johnson, MH (2002) Time and development. Reproductive BioMedicine Online 4(Suppl. 1): 39–45.Google Scholar

Johnson, MH, Day, ML (2000) Egg timers: how is developmental time measured in the early vertebrate embryo? Bioessays 22: 57–63.Google Scholar

Johnson, MH, Lim, A, Fenando, D, Day, ML (2002) Circadian clockwork genes are expressed in the reproductive tract and conceptus of the early pregnant mouse. Reproductive BioMedicine Online 4(12): 140–145.Google Scholar

Kaneda, H, Hayashi, J, Takahama, S, et al. (1995) Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proceedings of the National Academy of Sciences of the USA 92: 4542–4546.Google Scholar

Katari, S, Turan, N, Bibikova, M, et al. (2009) DNA methylation and gene expression differences in children conceived in vitro or in vivo. Human Molecular Genetics 18(20): 3769–3778.Google Scholar

Kawamura, K, Fukuda, J, Shimizu, Y, Kodama, H, Tanaka, T (2005) Survivin contributes to the anti-apoptotic activities of transforming growth factor alpha in mouse blastocysts through phosphatidylinositol 3′-kinase pathway. Biology and Reproduction 73: 1094–1101.Google Scholar

Kidder, GM, McLachlin, JR (1985) Timing of transcription and protein synthesis underlying morphogenesis in preimplantation mouse embryos. Developmental Biology 112: 265–275.Google Scholar

Krakauer, DC, Mira, A (1999) Mitochondria and germ cell death. Nature 400: 125–126.Google Scholar

Lane, M, Gardner, DK (1997) Nonessential amino acids and glutamine decrease the time of the first three cleavage divisions and increase compaction of mouse zygotes in vitro. Journal of Assisted Reproduction and Genetics 14(7): 398–403.Google Scholar

Lane, M, Gardner, DK (2000) Lactate regulates pyruvate uptake and metabolism in the preimplantation mouse embryo. Biology and Reproduction 62: 16–22.Google Scholar

Lee, L, Miyano, T, Moor, RM (2000) Localisation of phosphorylated MAP kinase during the transition from meiosis I to meiosis II in pig oocytes. Zygote 8: 119–125.Google Scholar

Lefièvre, L, Conner, SJ, Salpekar, A, et al. (2004) Four zona pellucida glycoproteins are expressed in the human. Human Reproduction 19(7): 1580–1586.Google Scholar

Levy, R, Elder, K, Ménézo, Y (2004) Cytoplasmic transfer in oocytes: biochemical aspects. Human Reproduction Update 10(3): 241–250.CrossRef Google Scholar PubMed

Lightman, A, Kol, S, Wayner, V, et al. (1997) The presence of a sponsoring embryo in a batch of poor quality thawed embryos significantly increases pregnancy and implantation rate. Fertility and Sterility 67(4): 711–716.Google Scholar

Lin, YC, Chang, SY, Lan, KC, et al. (2003) Human oocyte maturity in vivo determines the outcome of blastocyst development in vitro. Journal of Assisted Reproduction and Genetics 20(12): 506–512.Google Scholar

Lo, H (1996) The role of gap junction membrane channels in development. Journal of Bioenergetics and Biomembranes 8(4): 399–409.Google Scholar

Majumder, S, DePamphilis, ML (1994) Requirements for DNA transcription and replication at the beginning of mouse development. Journal of Cell Biochemistry 55(1): 59–68.CrossRef Google Scholar PubMed

Marangos, P, FitzHarris, G, Carroll, J (2003) Ca²⁺ oscillations at fertilization in mammals are regulated by the formation of pronuclei. Development 130: 1461–1472.Google Scholar

Maro, B, Gueth-Hallonet, C, Aghion, J, Antony, C (1991) Cell polarity and microtubule organization during mouse early embryogenesis. Development, Supplement 1: 17–25.Google Scholar

Mattioli, M, Barboni, B (2000) Signal transduction mechanism for LH in the cumulus oocyte complex. Molecular and Cellular Endocrinology 161: 19–23.Google Scholar

Memili, E, Dominko, T, First, N (1998) Onset of transcription in bovine oocytes and embryos. Molecular Reproduction and Development 51: 36–41.Google Scholar

Memili, E, First, NL (1999) Control of gene expression at the onset of bovine embryonic development. Biology of Reproduction 61: 1198–1207.CrossRef Google Scholar PubMed

Ménézo, Y, Janny, L (1997) Influence of paternal factors in early embryogenesis. In: Barratt, C, De Jonge, C, Mortimer, D, Parinaud, J (eds.) Genetics of Human Male Infertility. EDK, Paris, pp. 246–257.Google Scholar

Ménézo, Y, Lichtblau, I, Elder, K (2013). New insights into human embryo metabolism in vitro and in vivo. Journal of Assisted Reproduction and Genetics 30(3): 293–303.Google Scholar

Mio, Y (2006) Morphological analysis of human embryonic development using time-lapse cinematography. Journal of Mammalian Ova Research 23(1): 27–35.Google Scholar

Munné, S, Alikani, M, Tomkin, G, Grifo, J, Cohen, J (1995) Embryo morphology, developmental rates, and maternal age are correlated with chromosome abnormalities. Fertility and Sterility 64: 382–391.Google Scholar

Nargund, G, Bourne, T, Doyle, P, et al. (1996) Associations between ultrasound indices of follicular blood flow, oocyte recovery and preimplantation embryo quality. Human Reproduction 11(1): 109–113.Google Scholar

Niakan, KK, Eggan, K (2013) Analysis of human embryos from zygote to blastocyst reveals distinct gene expression patterns relative to the mouse. Developmental Biology 375: 54–64.Google Scholar

Niemann, H, Wrenzycki, C (1999) Alterations of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture condition: implications for subsequent development. Theriogenology 53: 21–34.Google Scholar

Nikas, G, Ao, A, Winston, RM, Handyside, AH (1996) Compaction and surface polarity in the human embryo in vitro. Biology of Reproduction 55: 32–37.Google Scholar

Nikas, G, Paraschos, T, Psychoyos, A, Handyside, AH (1994) The zona reaction in human oocytes as seen with scanning electron microscopy. Human Reproduction 9(11): 2135–2138.Google Scholar

Nothias, JY, Majumder, S, Kaneko, KJ, DePamphilis, ML (1995) Regulation of gene expression at the beginning of mammalian development. Journal of Biological Chemistry 270: 22077–22080.Google Scholar

Nothias, JY, Miranda, M, De Pamphilis, ML (1996) Uncoupling of transcription and translation during zygotic gene activation in the mouse. EMBO Journal 14: 5715–5725.Google Scholar

O’Neill, C (1998) Role of autocrine mediators in the regulation of embryo viability: lessons from animal models. Journal of Assisted Reproduction and Genetics 15(8): 460–465.Google Scholar

Orsi, NM, Leese, HJ (2004) Ammonium exposure and pyruvate affect the amino acid metabolism of bovine blastocysts in vitro. Reproduction 127: 131–140.Google Scholar

Payne, D, Flaherty, SP, Barry, MF, Matthews, CD (1997) Preliminary observations on polar body extrusion and pronuclear formation in human oocytes using time-lapse video cinematography. Human Reproduction 12(3): 532–541.Google Scholar

Payne, D, Flaherty, SP, Newble, CD, Swann, NJ, Wang, XJ, Matthews, CD (1994) The influence of sperm morphology and the acrosome reaction on fertilization. Human Reproduction 9: 1281–1288.Google Scholar

Pfeffer, PL (2018) Building principles for constructing a mammalian blastocyst embryo. Biology 7: pii: E41. DOI: 10.3390/biology7030041Google Scholar

Picton, HM, Briggs, D, Gosden, RG (1998) The molecular basis of oocyte growth and development. Molecular and Cellular Endocrinology 145: 27–37.Google Scholar

Piotrowska, K, Wianny, F, Pedersen, RA, Zernicka-Goetz, M (2001) Blastomeres arising from the first cleavage division have distinguishable fates in normal mouse development. Development 128: 3739–3748.Google Scholar

Piotrowska-Nitsche, K, Perea-Gomez, A, Haraguchi, S, et al. (2005) Four-cell stage mouse blastomeres have different developmental properties. Development 132: 479–490.Google Scholar

Piotrowska-Nitsche, K, Zernicka-Goetz, M (2005) Spatial arrangement of individual 4-cell stage blastomeres and the order in which they are generated correlate with blastocyst pattern in the mouse embryo. Mechanisms of Development 122: 487–500.Google Scholar

Posillico, J, and The Metabolomics Study Group for Assisted Reproductive Technologies (2007) Selection of viable embryos and gametes by rapid, noninvasive metabolomic profiling of oxidative stress biomarkers. In: Elder, K, Cohen, J (eds.) Human Preimplantation Embryo Evaluation and Selection. Taylor-Francis, London, pp. 245–262.Google Scholar

Puissant, F, Van Rysselberge, M, Barlow, P, et al. (1987) Embryo scoring as a prognostic tool in IVF treatment. Human Reproduction 2: 705–708.Google Scholar

Robaire, B, Hales, BF (2003) Mechanisms of action of cyclophosphamide as a male-mediated developmental toxicant. Advances in Experimental Medicine and Biology 518: 169–180.Google Scholar

Roode, M, Blair, K, Snell, P, Elder, K, et al. (2012) Human hypoblast formation is not dependent on FGF signaling. Developmental Biology 361: 358–363.Google Scholar

Rosebloom, T (2018) Developmental plasticity and its relevance to assisted human reproduction. Human Reproduction 33(4): 546–552.Google Scholar

Rossant, J (2004) Lineage development and polar asymmetries in the peri-implantation mouse blastocyst. Seminars in Cell and Developmental Biology 15(5): 573–581.Google Scholar

Sakkas, D, Urner, F, Bizzaro, D, et al. (1998) Sperm nuclear DNA damage and altered chromatin structure: effect on fertilization and embryo development. Human Reproduction 13(Suppl. 4): 11–19.Google Scholar

Santella, L, Alikani, M, Talansky, BE, Cohen, J, Dale, B (1992) Is the human oocyte plasma membrane polarized? Human Reproduction 7: 999–1003.Google Scholar

Sapienza, C, Peterson, AC, Rossant, J, Balling, R (1987) Degree of methylation of transgenes is dependent on gamete of origin. Nature 328(6127): 251–254.Google Scholar

Sathanathan, AH, Chen, C (1986) Sperm-oocyte membrane fusion in the human during monospermic fertilization. Gamete Research 15: 177–186.Google Scholar

Sathananthan, AH, Ng, SC, Trounson, AO, Ratnam, SS, Bongso, TA (1990) Human sperm-oocyte fusion. In: Dale, B (ed.) Mechanism of Fertilization: Plants to Humans. NATO ASI Series, Vol. h45. Springer-Verlag, Berlin, pp. 329–350.Google Scholar

Schatten, G (1994) The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Developmental Biology 165(2): 299–335.Google Scholar

Schatten, G (1999) Fertilization. In: Fauser, BCJM (ed.) Molecular Biology in Reproductive Medicine. Parthenon Publishing, London, pp. 297–311.Google Scholar

Schatten, G, Simerly, C, Schatten, H (1991) Maternal inheritance of centrosomes in mammals; studies on parthenogenesis and polyspermy in mice. Proceedings of the National Academy of Sciences of the USA 88(15): 6785–6789.Google Scholar

Schultz, RM (1995) Role of chromatin structure in zygotic gene activation in the mammalian embryo. Seminars in Cell Biology 6(4): 201–208.Google Scholar

Schultz, RM (1999) Preimplantation embryo development. In: Fauser, BCJM (ed.) Molecular Biology in Reproductive Medicine. Parthenon Publishing, London, pp. 313–331.Google Scholar

Shabazi, MN, Jedrusik, A, Vuoristo, S et al. (2016). Self-organisation of the human embryo in the absence of maternal tissues. Nature Cell Biology 18(6): 700–708.Google Scholar

Simerly, C, Navara, CS (2007) The sperm centriole: its effect on the developing embryo. In: Elder, K, Cohen, J (eds.) Human Preimplantation Embryo Evaluation and Selection. Taylor&Francis, London, pp. 337–354.Google Scholar

Simerly, C, Wu, G, Zoran, S, et al. (1995) The paternal inheritance of the centrosome, the cell’s microtubule-organising center, in humans and the implications of infertility. Nature Medicine 1: 47–53.Google Scholar

Spanos, S, Becker, DL, Winston, RM, Hardy, K (2000) Anti-apoptotic action of insulin-like growth factor-1 during human preimplantation embryo development. Biology and Reproduction 63: 1413–1420.Google Scholar

Stein, P, Worrad, DM, Belyaev, ND, Turner, BM, Schultz, RM (1997) Stage-dependent redistributions of acetylated histones in nuclei of the early preimplantation mouse embryo. Molecular Reproduction and Development 47(4): 421–429.Google Scholar

Steuerwald, N (2007) Gene expression analysis in the human oocyte and embryo. In: Elder, K, Cohen, J (eds.) Human Preimplantation Embryo Evaluation and Selection. Taylor&Francis, London, pp. 263–272.Google Scholar

Sun, QY (2003) Cellular and molecular mechanisms leading to cortical reaction and polyspermy block in mammalian eggs. Microscopy Research and Technique 61(4): 342–348.Google Scholar

Surani, MA, Barton, SC, Norris, ML (1986) Nuclear transplantation in the mouse: heritable differences between parental genomes after activation of the embryonic genome. Cell 45(1): 127–136.Google Scholar

Temeles, GL, Ram, PT, Rothstein, JL, Schulz, RM (1994) Expression patterns of novel genes during mouse preimplantation embryogenesis. Molecular Reproduction and Development 37: 121–129.Google Scholar

Tesarik, J, Greco, E (1999) The probability of abnormal preimplantation development can be predicted by a single static observation on pronuclear stage morphology. Human Reproduction 14: 1318–1323.Google Scholar

Tesarik, J, Kopecny, V (1989a) Developmental control of the human male pronucleus by ooplasmic factors. Human Reproduction 4: 962–968.Google Scholar

Tesarik, J, Kopecny, V (1989b) Nucleic acid synthesis and development of human male pronucleus. Journal of Reproduction and Fertility 86: 549–558.Google Scholar

Tesarik, J, Kopecny, V (1989c) Development of human male pronucleus: ultrastructure and timing. Gamete Research 24: 135–149.Google Scholar

Tesarik, J, Kopecny, V, Plachot, M, Mandelbaum, J (1988) Early morphological signs of embryonic genome expression in human preimplantation development as revealed by quantitative electron microscopy. Developmental Biology 128: 15–20.Google Scholar

Torres-Padilla, ME, Zernicka-Goetz, M (2006) Role of TIF1α as a modulator of embryonic transcription in the mouse zygote. Journal of Cell Biology 174(3): 329–338.Google Scholar

Valdimarsson, G, Kidder, GM (1995) Temporal control of gap junction assembly in preimplantation mouse embryos. Journal of Cell Science 108 (Pt 4): 1715–1722.Google Scholar

Vassena, R, Boué, S, González-Roca, E, et al. (2011) Waves of early transcriptional activation and pluripotency program initiation during human preimplantation development. Development 138(17): 3699–3709.Google Scholar

Van Blerkom, J, Davis, P, Alexander, S (2004) Occurrence of maternal and paternal spindles in unfertilized human oocytes: possible relationship to nucleation defects after silent fertilization. Reproductive BioMedicine Online 8(4): 454–459.Google Scholar

Wang, QT, Piotrowska, K, Ciemerych, MA, et al. (2004) A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Developmental Cell 6(1): 133–144.Google Scholar

Warner, CM, Cao, W, Exley, GE et al. (1998) Genetic regulation of egg and embryo survival. Human Reproduction 13(Suppl. 3): 178–190.Google Scholar

Wassarman, P (1987) The biology and chemistry of fertilization. Science 235: 553–560.Google Scholar

Wassarman, P (1990) Profile of a mammalian sperm receptor. Development 108: 1–17.Google Scholar

Wassarman, PM, Florman, HM, Greve, IM (1985) Receptor-mediated sperm–egg interactions in mammals. In: Metz, CB, Monroy, A (eds.) Fertilization, Vol. 2. Academic Press, New York, pp. 341–360.Google Scholar

Wiekowski, M, Miranda, M, DePamphilis, ML (1991) Regulation of gene expression in preimplantation mouse embryos: effects of the zygotic clock and the first mitosis on promoter and enhancer activities. Developmental Biology 147(2): 403–414.Google Scholar

Wolffe, AP (1998) Packaging principle: how DNA methylation and histone acetylation control the transcriptional activity of chromatin. Journal of Experimental Zoology 282: 239–244.Google Scholar

Wong, C, Loewke, K, Bossert, N, et al. (2010) Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nature Biotechnology 28: 1115–1121.Google Scholar

Woodward, BJ, Lenton, EA, MacNeil, S (1993) Requirement of preimplantation human embryos for extracellular calmodulin for development. Human Reproduction 8(2): 272–276.Google Scholar

Worrad, DM, Turner, BM, Schultz, RM (1995) Temporally restricted spatial localization of acetylated isoforms of histone H4 and RNA polymerase II in the 2-cell mouse embryo. Development 121(9): 2949–2959.Google Scholar

Xu, Y, Zhang, JJ, Grifo, JA, Krey, LC (2005) DNA methylation patterns in human tripronucleate zygotes. Molecular Human Reproduction 11(3): 167–171.Google Scholar

Zeng, F, Schultz, R (2005) RNA transcript profiling during zygotic gene activation in the preimplantation mouse embryo. Developmental Biology 283: 40–57.Google Scholar