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  • Print publication year: 2020
  • Online publication date: December 2019

Chapter 4 - Gamete Interaction

Summary

Mature human gametes ready for fertilization differ in their state of nuclear maturation: the spermatozoon has completed meiosis and the oocyte is arrested at metaphase II. However, both gametes must also undergo a process of cytoplasmic maturation before they are capable of fertilization. This involves a complex series of biochemical, physiological and structural events that occur in a carefully orchestrated temporal and spatial pattern in parallel with, but independent from, nuclear maturation. Cytoplasmic and nuclear maturation are often asynchronous (Dale, 2018a): therefore, a cohort of human metaphase II oocytes collected after controlled ovarian hyperstimulation in an IVF program may appear to be similar with regards to the nuclear apparatus, but they are in fact at various stages of cytoplasmic maturation. This may partly explain the different developmental capabilities of embryos generated from a single cohort of oocytes.

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Auerbach, L (1874) Organologische Studien. Breslau.
Boveri, T (1902) Über mehrpolige Mitosen als Mittel zur Analyse des Zellkerns. Verhandlungen der physicalisch-medizinischen Gesselschaft zu Würzburg N.F. 35: 6790.
Coy, P, Aviles, M (2010) What controls polyspermy in mammals: the oviduct or the oocyte? Biological Reviews 85: 593605.
Dale, B (1983a) Fertilization in Animals. Edward Arnold, London.
Dale, B (2018b) Fertilization: The Beginning of Life. Cambridge University Press, Cambridge, UK.
Dale, B (2018) Polyspermy. In: Skinner, M (ed.) Encyclopedia of Reproduction, 2nd edn. Elsevier, New York, pp. 309313.
Edwards, RG (1982) Conception in the Human Female. Academic Press, New York.
Fleming, TA, Johnson, MH (1988) From egg to epithelium. Annual Review of Cell Biology 4: 459485.
Forman, H, Fissore, R (2015) Fertilization in mammals. In: Plant TM, Zelezni, AJ (eds.) Knobil and Neill’s Physiology of Reproduction, 4th edn. Elsevier, New York, pp. 149196.
Gwatkin, R (1974) Fertilization Mechanisms in Man and Mammals. Plenum Press, New York.
Lauria, A, Gandolfi, E, Enne, G, Gianaroli, L (eds.) (1998) Gametes: Development and Function. Serono Symposia, Rome.
Nuccitelli, R, Cherr, G, Clark, A (1989) Mechanisms of Egg Activation. Plenum Press, New York.
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): 299335.
Tosti, E, Boni, R (2004) Electrical events during gamete maturation and fertilization in animals and humans. Human Reproduction Update 10(1): 53-65.
Tosti, E, Ménézo, Y (2016) Gamete activation: basic knowledge and clinical applications. Human Reproduction Update 22(4): 420439.
Wilson, EB (1900) The Cell in Development and Inheritance. Macmillan, London.
Yanagimachi, R (1981) Mechanisms of fertilization in mammals. In: Mastroianni, L, Biggers, JD (eds.) Fertilization and Embryonic Development in Vitro. Plenum Press, New York, pp. 81182.
Yanagimachi, R (1994) Mammalian fertilization. In: Knobil, E, Neill, J (eds.) The Physiology of Reproduction. Raven Press, New York, pp. 189317.
Breitbart, H, Spungin, B (1997) The biochemistry of the acrosome reaction. Molecular Human Reproduction 3(3): 195202.
Cappell, SD, Mark, KG, Garbett, D, Pack, LR, Rape, M, Meyer, T (2018) Emi1 switches from being a substrate to an inhibitor of APC/CCdh1 to start the cell cycle. Nature 558: 313317.
Cohen-Dayag, A, Tur-Kaspa, I, Dor, J, Mashiach, S, Eisenbach, M (1995) Sperm capacitation in humans is transient and correlates with chemotactic responsiveness to follicular factors. Proceedings of the National Academy of Sciences 92: 1103911043.
Collas, P (1998) Cytoplasmic control of nuclear assembly. Reproduction, Fertility, and Development 10: 581592.
Collas, P, Poccia, D (1998) Remodeling the sperm nucleus into a male pronucleus at fertilization. Theriogenology 49(1): 6781.
Conner, SJ, Lefièvre, L, Hughes, DC, Barratt, CL (2005) Cracking the egg: increased complexity in the zona pellucida. Human Reproduction 20: 11481152.
Dale, B (2016) Achieving monospermy or preventing polyspermy? Research and Reports in Biology 7: 4757.
Dale, B, DeFelice, LJ (1990) Soluble sperm factors, electrical events and egg activation. In: Dale, B (ed.) Mechanism of Fertilization: Plants to Humans. NATO ASI cell biology ser H 45. Springer, Berlin, pp. 475487.
Dale, B, DeFelice, LJ (2011) Polyspermy prevention: facts and artifacts. Journal of Assisted Reproduction and Genetics 28: 199207.
Dale, B, Di Matteo, L, Marino, M, Russo, G, Wilding, M (1999) Soluble sperm activating factor. In: Ganon, C (ed.) The Male Gamete: from Basic Knowledge to Clinical Applications. Cache River Press, Vienna, IL, pp. 291302.
Dale, B, Marino, M, Wilding, M (1998) Soluble sperm factor, factors or receptors. Molecular Human Reproduction 5: 14.
Dale, B, Monroy, A (1981) How is polyspermy prevented? Gamete Research 4: 151169.
Dale, B, Tosti, E, Iaccarino, M (1995) Is the plasma membrane of the human oocyte reorganized following fertilisation and early cleavage? Zygote 3(1): 3136.
Dale, B, Wilding, M, Coppola, G, Tosti, E (2010) How do spermatozoa activate oocytes. Reproductive BioMedicine Online 21: 13.
Davidson, EH (1990) How embryos work: a comparative view of diverse modes of cell fate specification. Development 108: 365389.
Eisenbach, M, Ralt, D (1992) Precontact mammalian sperm-egg communication and role in fertilization. American Journal of Physiology 262: 10951101.
Foltz, KR, Lennarz, WJ (1993) The molecular basis of sea urchin gamete interactions at the egg plasma membrane. Developmental Biology 158: 4661.
Gianaroli, L, Magli, C, Ferraretti, A, et al. (1996) Reducing the time of sperm-oocyte interaction in human IVF improves the implantation rate. Human Reproduction 11: 166171.
Gianaroli, L, Tosti, E, Magli, C, Ferrarreti, A, Dale, B (1994) The fertilization current in the human oocyte. Molecular Reproduction and Development 38: 209214.
Gupta, SK (2015) Role of zona pellucida glycoproteins during fertilization in humans. Journal of Reproductive Immunology 108: 9097.
Gur, Y, Breitbart, H (2006) Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes. Genes and Development 20(4): 411416.
Hertwig, O (1876) Beiträge zur Kenntniss der Bildung, Befruchtung und Theilung des thierischen Eies. Morphologische Jahrbuch 1: 347434.
Hewitson, L, Simerley, C, Schatten, G (1999) ICSI: Unravelling the mysteries. Nature Medicine 5(4): 431433.
Holubcova, Z, Howard, G, Schuh, M (2013) Vesicles modulate an actin network for asymmetric spindle positioning. Nature Cell Biology 15: 937947.
Holy, J, Schatten, G (1991) Spindle pole centrosomes of sea urchin embryos are partially composed of material recruited from maternal stores. Developmental Biology 147: 343353.
Jaffe, L (1980) Calcium explosions as triggers of development. Annals of the New York Academy of Sciences 339: 86101.
Kinz, G, Beil, D, Deininger, H, Wildt, L, Leyendecker, G (1996) The dynamics of rapid sperm transport through the female genital tract: evidence from vaginal sonography of uterine peristalsis and hysterosalpingoscintigraphy. Human Reproduction 11(3): 627632.
Lanzafame, F, Chapman, M, Guglielmino, A, Gearon, CM, Forman, RG (1994) Pharmacological stimulation of sperm motility. Human Reproduction 9(2): 192194.
Lefèvre, B (2008) The nucleolus of the maternal gamete is essential for life. Bioassays 30: 613616.
Lefièvre, L, Conner, SJ, Salpekar, A, et al. (2004) Four zona pellucida glycoproteins are expressed in the human. Human Reproduction 19: 15801586.
Lennarz, WJ (1994) Fertilization in sea urchins: how many different molecules are involved in gamete interaction and fusion? Zygote 2(1): 14.
Maro, B, Gueth-Hallonet, C, Aghion, J, Antony, C (1991) Cell polarity and microtubule organization during mouse early embryogenesis. Development Supplement 10: 1725.
Miller, MR, Mansell, SA, Meyers, SA, Lishko, PV (2015) Flagellar ion channels of sperm: similarities and differences between species. Cell Calcium 58: 105113.
Myles, DG (1992) Molecular mechanism of sperm-egg membrane binding and fusion in mammals. Developmental Biology 158: 3545.
Nasr-Esfahani, MH, Razavi, S, Mardani, M, Shirazi, R, Javanmardi, S (2007) Effects of failed oocyte activation and sperm protamine deficiency on fertilization post-ICSI. Reproductive BioMedicine Online 14(4): 422429.
Ogushi, S, Palmieri, C, Fulka, H, et al. (2008) The maternal nucleolus is essential for early embryonic development in mammals. Science 319: 613616.
Patrat, C, Auer, J, Fauque, P, et al. (2006) Zona pellucida from fertilised human oocytes induces a voltage-dependent calcium influx and the acrosome reaction in spermatozoa, but cannot be penetrated by sperm. BMC Developmental Biology 6: 59.
Ralt, D, Goldenberg, M, Fetterolf, P, et al. (1991) Sperm attraction to a follicular factor(s) correlates with human egg fertilizability. Proceedings of the National Academy of Sciences of the USA 88: 28402844.
Reichmann, J, Nijmeijer, B, Hossein, MJ (2018) Dual spindle formation in zygotes keeps parental genomes apart in early mammalian embryos. Science 361(6398): 189193.
Sakkas, D, Ramalingam, M, Garrido, N, Barratt, CLR (2015) Sperm selection in natural conception: what can we learn from Mother Nature to improve assisted reproduction outcomes? Human Reproduction Update 21(6): 711726.
Santella, L, Alikani, M, Talansky, B, Cohen, J, Dale, B (1992) Is the human oocyte plasma membrane polarized? Human Reproduction 7: 9991003.
Santella, L, Dale, B (2015). Assisted yes, but where do we draw the line? Reproductive BioMedicine Online 31: 476478.
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): 67856789.
Schulz, MC, Leblond, CP (1990) Nucleolar structure and synthetic activity during meiotic prophase and spermiogenesis in the rat. American Journal of Anatomy 189: 110.
Scott, L, Alvero, R, Leondires, M, et al. (2000) The morphology of human pronuclear embryos is positively related to blastocyst development and implantation. Human Reproduction 15: 23942403.
Shapiro, S (1987) The existential decision of a sperm. Cell 49: 293294.
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: 4753.
Spehr, M, Schwane, K, Riffell, JA, et al. (2004) Particulate adenylate cyclase plays a key role in human sperm olfactory receptor-mediated chemotaxis. Journal of Biological Chemistry 279: 4019440203.
Suarez, SS, Pacey, AA (2006) Sperm transport in the female reproductive tract. Human Reproduction Update 12(1): 2327.
Sutovsky, P, Navara, CS, Schatten, G (1996) Fate of the sperm mitochondria, and the incorporation, conversion, and disassembly of the sperm tail structures during bovine fertilization. Biology of Reproduction 55: 11951205.
Tanphaichitr, N, Kongmanas, K, Kruevaisayawan, H, et al. (2015) Remodeling of the plasma membrane in preparation for sperm-egg recognition: roles of acrosomal proteins. Asian Journal of Andrology 17: 574582.
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: 13181323.
Tesarik, J, Kopecny, V (1989a) Developmental control of the human male pronucleus by ooplasmic factors. Human Reproduction 4: 962968.
Tesarik, J, Kopecny, V (1989b) Nucleic acid synthesis and development of human male pronucleus. Journal of Reproduction and Fertility 86: 549558.
Tesarik, J, Kopecny, V (1989c) Development of human male pronucleus: ultrastructure and timing. Gamete Research 24: 135149.
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: 1520.
Tesarik, J, Kopecny, V, Plachot, M, Mandelbaum, J, Da Lage, C, Fléchon, J-E (1986) Nucleologenesis in the human embryo developing in vitro: ultrastructural and autoradiographic analysis. Developmental Biology 115: 193203.
Tesarik, I, Sousa, M, Testart, J (1994) Human oocyte activation after intracytoplasmic sperm injection. Human Reproduction 9: 511514.
Tosti, E (1994) Sperm activation in species with external fertilization. Zygote 2(4): 359361.
van der Heijdn, GW, Ramos, L, Baart, EB, et al. (2008) Sperm derived histones contribute to zygotic chromatin in humans. BMC Developmental Biology 8: 34.
Ward, CR, Kopf, GS (1993) Molecular events mediating sperm activation. Developmental Biology 158: 934.
Wassarman, PM (1990) Profile of a mammalian sperm receptor. Development 108: 117.
Wassarman, P (2014) Sperm protein finds its mate. Nature 508: 466467.
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. 341360.
Wassarman, PM, Liu, C, Litscher, ES (1996) Constructing the mammalian egg zona pellucida: some new pieces of an old puzzle. Journal of Cell Science 109: 20012004.
Weindling, PJ (1991) Darwinism and Social Darwinism in Imperial Germany: The Contribution of the Cell Biologist Oscar Hertwig (1849–1922). G. Fischer Verlag, Stuttgart, p. 71.
Zumoffen, CM, Massa, E, Caille, AM, Munuce, MJ, Ghersevich, SA (2015) Effects of lactoferrin, a protein present in the female reproductive tract, on parameters of human sperm capacitation and gamete interaction. Andrology 3: 10681075.
Auerbach, L (1874) Organologische Studien. Breslau.
Boveri, T (1902) Über mehrpolige Mitosen als Mittel zur Analyse des Zellkerns. Verhandlungen der physicalisch-medizinischen Gesselschaft zu Würzburg N.F. 35: 6790.
Coy, P, Aviles, M (2010) What controls polyspermy in mammals: the oviduct or the oocyte? Biological Reviews 85: 593605.
Dale, B (1983a) Fertilization in Animals. Edward Arnold, London.
Dale, B (2018b) Fertilization: The Beginning of Life. Cambridge University Press, Cambridge, UK.
Dale, B (2018) Polyspermy. In: Skinner, M (ed.) Encyclopedia of Reproduction, 2nd edn. Elsevier, New York, pp. 309313.
Edwards, RG (1982) Conception in the Human Female. Academic Press, New York.
Fleming, TA, Johnson, MH (1988) From egg to epithelium. Annual Review of Cell Biology 4: 459485.
Forman, H, Fissore, R (2015) Fertilization in mammals. In: Plant TM, Zelezni, AJ (eds.) Knobil and Neill’s Physiology of Reproduction, 4th edn. Elsevier, New York, pp. 149196.
Gwatkin, R (1974) Fertilization Mechanisms in Man and Mammals. Plenum Press, New York.
Lauria, A, Gandolfi, E, Enne, G, Gianaroli, L (eds.) (1998) Gametes: Development and Function. Serono Symposia, Rome.
Nuccitelli, R, Cherr, G, Clark, A (1989) Mechanisms of Egg Activation. Plenum Press, New York.
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): 299335.
Tosti, E, Boni, R (2004) Electrical events during gamete maturation and fertilization in animals and humans. Human Reproduction Update 10(1): 53-65.
Tosti, E, Ménézo, Y (2016) Gamete activation: basic knowledge and clinical applications. Human Reproduction Update 22(4): 420439.
Wilson, EB (1900) The Cell in Development and Inheritance. Macmillan, London.
Yanagimachi, R (1981) Mechanisms of fertilization in mammals. In: Mastroianni, L, Biggers, JD (eds.) Fertilization and Embryonic Development in Vitro. Plenum Press, New York, pp. 81182.
Yanagimachi, R (1994) Mammalian fertilization. In: Knobil, E, Neill, J (eds.) The Physiology of Reproduction. Raven Press, New York, pp. 189317.
Breitbart, H, Spungin, B (1997) The biochemistry of the acrosome reaction. Molecular Human Reproduction 3(3): 195202.
Cappell, SD, Mark, KG, Garbett, D, Pack, LR, Rape, M, Meyer, T (2018) Emi1 switches from being a substrate to an inhibitor of APC/CCdh1 to start the cell cycle. Nature 558: 313317.
Cohen-Dayag, A, Tur-Kaspa, I, Dor, J, Mashiach, S, Eisenbach, M (1995) Sperm capacitation in humans is transient and correlates with chemotactic responsiveness to follicular factors. Proceedings of the National Academy of Sciences 92: 1103911043.
Collas, P (1998) Cytoplasmic control of nuclear assembly. Reproduction, Fertility, and Development 10: 581592.
Collas, P, Poccia, D (1998) Remodeling the sperm nucleus into a male pronucleus at fertilization. Theriogenology 49(1): 6781.
Conner, SJ, Lefièvre, L, Hughes, DC, Barratt, CL (2005) Cracking the egg: increased complexity in the zona pellucida. Human Reproduction 20: 11481152.
Dale, B (2016) Achieving monospermy or preventing polyspermy? Research and Reports in Biology 7: 4757.
Dale, B, DeFelice, LJ (1990) Soluble sperm factors, electrical events and egg activation. In: Dale, B (ed.) Mechanism of Fertilization: Plants to Humans. NATO ASI cell biology ser H 45. Springer, Berlin, pp. 475487.
Dale, B, DeFelice, LJ (2011) Polyspermy prevention: facts and artifacts. Journal of Assisted Reproduction and Genetics 28: 199207.
Dale, B, Di Matteo, L, Marino, M, Russo, G, Wilding, M (1999) Soluble sperm activating factor. In: Ganon, C (ed.) The Male Gamete: from Basic Knowledge to Clinical Applications. Cache River Press, Vienna, IL, pp. 291302.
Dale, B, Marino, M, Wilding, M (1998) Soluble sperm factor, factors or receptors. Molecular Human Reproduction 5: 14.
Dale, B, Monroy, A (1981) How is polyspermy prevented? Gamete Research 4: 151169.
Dale, B, Tosti, E, Iaccarino, M (1995) Is the plasma membrane of the human oocyte reorganized following fertilisation and early cleavage? Zygote 3(1): 3136.
Dale, B, Wilding, M, Coppola, G, Tosti, E (2010) How do spermatozoa activate oocytes. Reproductive BioMedicine Online 21: 13.
Davidson, EH (1990) How embryos work: a comparative view of diverse modes of cell fate specification. Development 108: 365389.
Eisenbach, M, Ralt, D (1992) Precontact mammalian sperm-egg communication and role in fertilization. American Journal of Physiology 262: 10951101.
Foltz, KR, Lennarz, WJ (1993) The molecular basis of sea urchin gamete interactions at the egg plasma membrane. Developmental Biology 158: 4661.
Gianaroli, L, Magli, C, Ferraretti, A, et al. (1996) Reducing the time of sperm-oocyte interaction in human IVF improves the implantation rate. Human Reproduction 11: 166171.
Gianaroli, L, Tosti, E, Magli, C, Ferrarreti, A, Dale, B (1994) The fertilization current in the human oocyte. Molecular Reproduction and Development 38: 209214.
Gupta, SK (2015) Role of zona pellucida glycoproteins during fertilization in humans. Journal of Reproductive Immunology 108: 9097.
Gur, Y, Breitbart, H (2006) Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes. Genes and Development 20(4): 411416.
Hertwig, O (1876) Beiträge zur Kenntniss der Bildung, Befruchtung und Theilung des thierischen Eies. Morphologische Jahrbuch 1: 347434.
Hewitson, L, Simerley, C, Schatten, G (1999) ICSI: Unravelling the mysteries. Nature Medicine 5(4): 431433.
Holubcova, Z, Howard, G, Schuh, M (2013) Vesicles modulate an actin network for asymmetric spindle positioning. Nature Cell Biology 15: 937947.
Holy, J, Schatten, G (1991) Spindle pole centrosomes of sea urchin embryos are partially composed of material recruited from maternal stores. Developmental Biology 147: 343353.
Jaffe, L (1980) Calcium explosions as triggers of development. Annals of the New York Academy of Sciences 339: 86101.
Kinz, G, Beil, D, Deininger, H, Wildt, L, Leyendecker, G (1996) The dynamics of rapid sperm transport through the female genital tract: evidence from vaginal sonography of uterine peristalsis and hysterosalpingoscintigraphy. Human Reproduction 11(3): 627632.
Lanzafame, F, Chapman, M, Guglielmino, A, Gearon, CM, Forman, RG (1994) Pharmacological stimulation of sperm motility. Human Reproduction 9(2): 192194.
Lefèvre, B (2008) The nucleolus of the maternal gamete is essential for life. Bioassays 30: 613616.
Lefièvre, L, Conner, SJ, Salpekar, A, et al. (2004) Four zona pellucida glycoproteins are expressed in the human. Human Reproduction 19: 15801586.
Lennarz, WJ (1994) Fertilization in sea urchins: how many different molecules are involved in gamete interaction and fusion? Zygote 2(1): 14.
Maro, B, Gueth-Hallonet, C, Aghion, J, Antony, C (1991) Cell polarity and microtubule organization during mouse early embryogenesis. Development Supplement 10: 1725.
Miller, MR, Mansell, SA, Meyers, SA, Lishko, PV (2015) Flagellar ion channels of sperm: similarities and differences between species. Cell Calcium 58: 105113.
Myles, DG (1992) Molecular mechanism of sperm-egg membrane binding and fusion in mammals. Developmental Biology 158: 3545.
Nasr-Esfahani, MH, Razavi, S, Mardani, M, Shirazi, R, Javanmardi, S (2007) Effects of failed oocyte activation and sperm protamine deficiency on fertilization post-ICSI. Reproductive BioMedicine Online 14(4): 422429.
Ogushi, S, Palmieri, C, Fulka, H, et al. (2008) The maternal nucleolus is essential for early embryonic development in mammals. Science 319: 613616.
Patrat, C, Auer, J, Fauque, P, et al. (2006) Zona pellucida from fertilised human oocytes induces a voltage-dependent calcium influx and the acrosome reaction in spermatozoa, but cannot be penetrated by sperm. BMC Developmental Biology 6: 59.
Ralt, D, Goldenberg, M, Fetterolf, P, et al. (1991) Sperm attraction to a follicular factor(s) correlates with human egg fertilizability. Proceedings of the National Academy of Sciences of the USA 88: 28402844.
Reichmann, J, Nijmeijer, B, Hossein, MJ (2018) Dual spindle formation in zygotes keeps parental genomes apart in early mammalian embryos. Science 361(6398): 189193.
Sakkas, D, Ramalingam, M, Garrido, N, Barratt, CLR (2015) Sperm selection in natural conception: what can we learn from Mother Nature to improve assisted reproduction outcomes? Human Reproduction Update 21(6): 711726.
Santella, L, Alikani, M, Talansky, B, Cohen, J, Dale, B (1992) Is the human oocyte plasma membrane polarized? Human Reproduction 7: 9991003.
Santella, L, Dale, B (2015). Assisted yes, but where do we draw the line? Reproductive BioMedicine Online 31: 476478.
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): 67856789.
Schulz, MC, Leblond, CP (1990) Nucleolar structure and synthetic activity during meiotic prophase and spermiogenesis in the rat. American Journal of Anatomy 189: 110.
Scott, L, Alvero, R, Leondires, M, et al. (2000) The morphology of human pronuclear embryos is positively related to blastocyst development and implantation. Human Reproduction 15: 23942403.
Shapiro, S (1987) The existential decision of a sperm. Cell 49: 293294.
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: 4753.
Spehr, M, Schwane, K, Riffell, JA, et al. (2004) Particulate adenylate cyclase plays a key role in human sperm olfactory receptor-mediated chemotaxis. Journal of Biological Chemistry 279: 4019440203.
Suarez, SS, Pacey, AA (2006) Sperm transport in the female reproductive tract. Human Reproduction Update 12(1): 2327.
Sutovsky, P, Navara, CS, Schatten, G (1996) Fate of the sperm mitochondria, and the incorporation, conversion, and disassembly of the sperm tail structures during bovine fertilization. Biology of Reproduction 55: 11951205.
Tanphaichitr, N, Kongmanas, K, Kruevaisayawan, H, et al. (2015) Remodeling of the plasma membrane in preparation for sperm-egg recognition: roles of acrosomal proteins. Asian Journal of Andrology 17: 574582.
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: 13181323.
Tesarik, J, Kopecny, V (1989a) Developmental control of the human male pronucleus by ooplasmic factors. Human Reproduction 4: 962968.
Tesarik, J, Kopecny, V (1989b) Nucleic acid synthesis and development of human male pronucleus. Journal of Reproduction and Fertility 86: 549558.
Tesarik, J, Kopecny, V (1989c) Development of human male pronucleus: ultrastructure and timing. Gamete Research 24: 135149.
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: 1520.
Tesarik, J, Kopecny, V, Plachot, M, Mandelbaum, J, Da Lage, C, Fléchon, J-E (1986) Nucleologenesis in the human embryo developing in vitro: ultrastructural and autoradiographic analysis. Developmental Biology 115: 193203.
Tesarik, I, Sousa, M, Testart, J (1994) Human oocyte activation after intracytoplasmic sperm injection. Human Reproduction 9: 511514.
Tosti, E (1994) Sperm activation in species with external fertilization. Zygote 2(4): 359361.
van der Heijdn, GW, Ramos, L, Baart, EB, et al. (2008) Sperm derived histones contribute to zygotic chromatin in humans. BMC Developmental Biology 8: 34.
Ward, CR, Kopf, GS (1993) Molecular events mediating sperm activation. Developmental Biology 158: 934.
Wassarman, PM (1990) Profile of a mammalian sperm receptor. Development 108: 117.
Wassarman, P (2014) Sperm protein finds its mate. Nature 508: 466467.
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. 341360.
Wassarman, PM, Liu, C, Litscher, ES (1996) Constructing the mammalian egg zona pellucida: some new pieces of an old puzzle. Journal of Cell Science 109: 20012004.
Weindling, PJ (1991) Darwinism and Social Darwinism in Imperial Germany: The Contribution of the Cell Biologist Oscar Hertwig (1849–1922). G. Fischer Verlag, Stuttgart, p. 71.
Zumoffen, CM, Massa, E, Caille, AM, Munuce, MJ, Ghersevich, SA (2015) Effects of lactoferrin, a protein present in the female reproductive tract, on parameters of human sperm capacitation and gamete interaction. Andrology 3: 10681075.