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Chapter 11 - Cellular and Molecular Events after ICSI in Clinically Relevant Animal Models

Published online by Cambridge University Press:  02 December 2021

Gianpiero D. Palermo
Affiliation:
Cornell Institute of Reproductive Medicine, New York
Zsolt Peter Nagy
Affiliation:
Reproductive Biology Associates, Atlanta, GA
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Summary

Interactions between the sperm-borne oocyte activating factor(s) (SOAF) and the molecules within the oocyte cytoplasm, trigger the molecular pathways associated with oocyte activation. Of note, release of calcium from the endoplasmic reticulum (ER) creates calcium oscillations in mammals and one large calcium release in non-mammalian species. As the newly activated ovum begins to transform, the components of the fertilizing spermatozoon function cooperatively with the contents of the ooplasm as development progresses. The spermatozoon has been shown to contribute the main microtubule framework to the embryo through the integration of its centriole and has also been implicated in facilitating processes. Through oocyte-driven mechanisms, unnecessary sperm components must also be degraded. Many of these processes are centered around the reducing power of oocyte-produced glutathione (GSH) and facilitated by both the sperm-borne and oocyte-borne enzymatic activity. In this chapter we explore underlying molecular and biochemical processes that drive developmental progression of newly fertilized oocytes, and how ICSI procedures could change the molecular pathways found in natural fertilization.

Type
Chapter
Information
Manual of Intracytoplasmic Sperm Injection in Human Assisted Reproduction
With Other Advanced Micromanipulation Techniques to Edit the Genetic and Cytoplasmic Content of the Oocyte
, pp. 103 - 113
Publisher: Cambridge University Press
Print publication year: 2021

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References

Johnson, M. H. Robert Edwards: the path to IVF. Reprod. Biomed. Online 23, 245262 (2011).CrossRefGoogle Scholar
Palermo, G., Joris, H., Devroey, P. & Van Steirteghem, A. C. Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet 340, 1718 (1992).CrossRefGoogle ScholarPubMed
Parrington, J., Swann, K., Shevchenko, V. I., Sesay, A. K. & Lai, F. A. Calcium oscillations in mammalian eggs triggered by a soluble sperm protein. Nature 379, 364 (1996).CrossRefGoogle ScholarPubMed
Stice, S. L. & Robl, J. M. Activation of mammalian oocytes by a factor obtained from rabbit sperm. Mol. Reprod. Dev. 25, 272280 (1990).CrossRefGoogle ScholarPubMed
Swann, K. A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development 110, 12951302 (1990).CrossRefGoogle ScholarPubMed
Kimura, Y. et al. Analysis of mouse oocyte activation suggests the involvement of sperm perinuclear material. Biol. Reprod. 58, 14071415 (1998).CrossRefGoogle ScholarPubMed
Oko, R., Donald, A., Xu, W. & van der Spoel, A. C. Fusion failure of dense-cored proacrosomal vesicles in an inducible mouse model of male infertility. Cell Tissue Res. 346, 119 (2011).CrossRefGoogle Scholar
Wu, A. T. H. et al. The postacrosomal assembly of sperm head protein, PAWP, is independent of acrosome formation and dependent on microtubular manchette transport. Dev. Biol. 312, 471483 (2007).CrossRefGoogle ScholarPubMed
Suganuma, R. et al. Alkylated imino sugars, reversible male infertility-inducing agents, do not affect the genetic integrity of male mouse germ cells during short-term treatment despite induction of sperm deformities. Biol. Reprod. 72, 805813 (2005).CrossRefGoogle Scholar
Sutovsky, P., Manandhar, G., Wu, A. & Oko, R. Interactions of sperm perinuclear theca with the oocyte: Implications for oocyte activation, anti‐polyspermy defense, and assisted reproduction. Microsc. Res. Tech. 61, 362378 (2003).CrossRefGoogle ScholarPubMed
Aarabi, M. et al. The testicular and epididymal expression profile of PLCζ in mouse and human does not support its role as a sperm-borne oocyte activating factor. PLoS One 7, e33496 (2012).CrossRefGoogle Scholar
Amdani, S. N., Yeste, M., Jones, C. & Coward, K. Sperm factors and oocyte activation: current controversies and considerations. Biol. Reprod. 93, 5051 (2015).CrossRefGoogle ScholarPubMed
Aarabi, M. et al. Sperm-derived WW domain-binding protein, PAWP, elicits calcium oscillations and oocyte activation in humans and mice. FASEB J. 28, 44344440 (2014).CrossRefGoogle ScholarPubMed
Saunders, C. M. et al. PLCζ: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 129, 35333544 (2002).CrossRefGoogle Scholar
Satouh, Y., Nozawa, K. & Ikawa, M. Sperm postacrosomal WW domain-binding protein is not required for mouse egg activation. Biol. Reprod. 93, 9194 (2015).CrossRefGoogle Scholar
Hachem, A. et al. PLCζ is the physiological trigger of the Ca2+ oscillations that induce embryogenesis in mammals but offspring can be conceived in its absence. Development 144, 29142924 (2017).Google Scholar
Duncan, F. E. et al. The zinc spark is an inorganic signature of human egg activation. Sci. Rep. 6, 18 (2016).CrossRefGoogle ScholarPubMed
Austin, C. R. Cortical granules in hamster eggs. Exp. Cell Res. 10, 533540 (1956).CrossRefGoogle ScholarPubMed
Liu, M. The biology and dynamics of mammalian cortical granules. Reprod. Biol. Endocrinol. 9, 149 (2011).CrossRefGoogle ScholarPubMed
Burkart, A. D., Xiong, B., Baibakov, B., Jiménez-Movilla, M. & Dean, J. Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy. J. Cell Biol. 197, 3744 (2012).CrossRefGoogle ScholarPubMed
Wortzman-Show, G. B., Kurokawa, M., Fissore, R. A. & Evans, J. P. Calcium and sperm components in the establishment of the membrane block to polyspermy: studies of ICSI and activation with sperm factor. Mol. Hum. Reprod. 13, 557565 (2007).CrossRefGoogle ScholarPubMed
Bianchi, E., Doe, B., Goulding, D. & Wright, G. J. Juno is the egg Izumo receptor and is essential for mammalian fertilization. Nature 508, 483487 (2014).CrossRefGoogle ScholarPubMed
Que, E. L. et al. Zinc sparks induce physiochemical changes in the egg zona pellucida that prevent polyspermy. Integr. Biol. 9, 135144 (2017).CrossRefGoogle ScholarPubMed
Yamamoto, T. M., Iwabuchi, M., Ohsumi, K. & Kishimoto, T. APC/C–Cdc20-mediated degradation of cyclin B participates in CSF arrest in unfertilized Xenopus eggs. Dev. Biol. 279, 345355 (2005).CrossRefGoogle ScholarPubMed
Dupont, G. Link between fertilization-induced Ca2+ oscillations and relief from metaphase II arrest in mammalian eggs: a model based on calmodulin-dependent kinase II activation. Biophys. Chem. 72, 153167 (1998).CrossRefGoogle Scholar
Gautier, J. et al. Cyclin is a component of maturation-promoting factor from Xenopus. Cell 60, 487494 (1990).CrossRefGoogle ScholarPubMed
Zhang, N., Duncan, F. E., Que, E. L., O’Halloran, T. V. & Woodruff, T. K. The fertilization-induced zinc spark is a novel biomarker of mouse embryo quality and early development. Sci. Rep. 6, 19 (2016).Google ScholarPubMed
Luberda, Z. The role of glutathione in mammalian gametes. Reprod Biol 5, 517 (2005).Google ScholarPubMed
Sutovsky, P. & Schatten, G. Depletion of glutathione during bovine oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization. Biol. Reprod. 56, 15031512 (1997).CrossRefGoogle ScholarPubMed
Hamilton, L. E. et al. Sperm-borne glutathione-s-transferase omega 2 accelerates the nuclear decondensation of spermatozoa during fertilization in mice. Biol. Reprod. 101, 368376 (2019).CrossRefGoogle Scholar
Fishman, E. L. et al. A novel atypical sperm centriole is functional during human fertilization. Nat. Commun. 9, (2018).Google ScholarPubMed
Navara, C. S., Simerly, C., Zoran, S. & Schatten, G. The sperm centrosome during fertilization in mammals: implications for fertility and reproduction. Reprod. Fertil. Dev. 7, 747754 (1995).CrossRefGoogle ScholarPubMed
Palermo, G. D., Colombero, L. T. & Rosenwaks, Z. The human sperm centrosome is responsible for normal syngamy and early embryonic development. Rev. Reprod. 2, 1927 (1997).CrossRefGoogle ScholarPubMed
Hewitson, L. C. et al. Microtubule and chromatin configurations during rhesus intracytoplasmic sperm injection: successes and failures. Biol. Reprod. 55, 271280 (1996).CrossRefGoogle ScholarPubMed
Sutovsky, P. et al. Fertilization and early embryology: Intracytoplasmic sperm injection for Rhesus monkey fertilization results in unusual chromatin, cytoskeletal, and membrane events, but eventually leads to pronuclear development and sperm aster assembly. Hum. Reprod. 11, 17031712 (1996).CrossRefGoogle Scholar
Nakamura, S. et al. Human sperm aster formation and pronuclear decondensation in bovine eggs following intracytoplasmic sperm injection using a piezo-driven pipette: a novel assay for human sperm centrosomal function. Biol. Reprod. 65, 13591363 (2001).CrossRefGoogle ScholarPubMed
Terada, Y. et al. Human sperm aster formation after intracytoplasmic sperm injection with rabbit and bovine eggs. Fertil. Steril. 77, 12831284 (2002).CrossRefGoogle ScholarPubMed
Simerly, C. et al. Biparental inheritance of γ-tubulin during human fertilization: molecular reconstitution of functional zygotic centrosomes in inseminated human oocytes and in cell-free extracts nucleated by human sperm. Mol. Biol. Cell 10, 29552969 (1999).CrossRefGoogle ScholarPubMed
Katayama, M. et al. Improved fertilization and embryo development resulting in birth of live piglets after intracytoplasmic sperm injection and in vitro culture in a cysteine-supplemented medium. Theriogenology 67, 835847 (2007).CrossRefGoogle Scholar
Ward, W. S. Function of sperm chromatin structural elements in fertilization and development. MHR Basic Sci. Reprod. Med. 16, 3036 (2009).CrossRefGoogle ScholarPubMed
Björndahl, L. & Kvist, U. Human sperm chromatin stabilization: a proposed model including zinc bridges. Mol. Hum. Reprod. 16, 2329 (2009).CrossRefGoogle ScholarPubMed
Hammoud, S. S. et al. Distinctive chromatin in human sperm packages genes for embryo development. Nature 460, 473 (2009).CrossRefGoogle ScholarPubMed
van der Heijden, G. W. et al. Sperm-derived histones contribute to zygotic chromatin in humans. BMC Dev. Biol. 8, 34 (2008).CrossRefGoogle ScholarPubMed
Tovich, P. R. & Oko, R. J. Somatic histones are components of the perinuclear theca in bovine spermatozoa. J. Biol. Chem. 278, 3243132438 (2003).CrossRefGoogle ScholarPubMed
Ramalho-Santos, J. et al. ICSI choreography: fate of sperm structures after monospermic rhesus ICSI and first cell cycle implications. Hum. Reprod. 15, 26102620 (2000).CrossRefGoogle ScholarPubMed
Sutovsky, P. & Song, W. H. Post-fertilisation sperm mitophagy: The tale of Mitochondrial Eve and Steve. Reprod. Fertil. Dev. 30, 5663 (2018).CrossRefGoogle Scholar
Gresson, R. A. R. Presence of the sperm middle-piece in the fertilized egg of the mouse (Mus musculus). Nature 145, 425 (1940).CrossRefGoogle Scholar
St. John, J. C., Jokhi, R. P. & Barratt, C. L. R. The impact of mitochondrial genetics on male infertility. Int. J. Androl. 28, 6573 (2005).CrossRefGoogle ScholarPubMed
Kramer, P. & Bressan, P. Mitochondria inspire a lifestyle. In Sutovsky, P. (ed.) Cellular and Molecular Basis of Mitochondrial Inheritance. Springer International Publishing, 105126 (2019).CrossRefGoogle Scholar
Song, W. H., Yi, Y. J., Sutovsky, M., Meyers, S. & Sutovsky, P. Autophagy and ubiquitin-proteasome system contribute to sperm mitophagy after mammalian fertilization. Proc. Natl. Acad. Sci. U. S. A. 113, E5261E5270 (2016).CrossRefGoogle ScholarPubMed
Zuidema, D. & Sutovsky, P. The domestic pig as a model for the study of mitochondrial inheritance. Cell Tissue Res. 380, 263271 (2020).CrossRefGoogle Scholar
Luo, S. et al. Biparental inheritance of mitochondrial DNA in humans. Proc. Natl. Acad. Sci. 115, 13039–13044 (2018).CrossRefGoogle ScholarPubMed
Peng, L. et al. Persistence and transcription of paternal mtDNA dependent on the delivery strategy rather than mitochondria source in fish embryos. Cell. Physiol. Biochem. 47, 18981908 (2018).CrossRefGoogle ScholarPubMed
Kuretake, S., Kimura, Y., Hoshi, K. & Yanagimachi, R. Fertilization and development of mouse oocytes injected with isolated sperm heads. Biol. Reprod. 55, 789795 (1996).CrossRefGoogle ScholarPubMed
Huang, T., Kimura, Y. & Yanagimachi, R. The use of piezo micromanipulation for intracytoplasmic sperm injection of human oocytes. J. Assist. Reprod. Genet. 13, 320328 (1996).CrossRefGoogle ScholarPubMed
Katayama, M. et al. Increased disruption of sperm plasma membrane at sperm immobilization promotes dissociation of perinuclear theca from sperm chromatin after intracytoplasmic sperm injection in pigs. Reproduction 130, 907916 (2005).CrossRefGoogle ScholarPubMed
Katayose, H. et al. Efficient injection of bull spermatozoa into oocytes using a piezo-driven pipette. Theriogenology 52, 12151224 (1999).CrossRefGoogle ScholarPubMed
Kerns, K., Zigo, M., Drobnis, E. Z., Sutovsky, M. & Sutovsky, P. Zinc ion flux during mammalian sperm capacitation. Nat. Commun. 9, 2061 (2018).CrossRefGoogle ScholarPubMed
De Lamirande, E., San Gabriel, M. C. & Zini, A. Human sperm chromatin undergoes physiological remodeling during in vitro capacitation and acrosome reaction. J. Androl. 33, 10251035 (2012).CrossRefGoogle ScholarPubMed
Sutovsky, P., Oko, R., Hewitson, L. & Schatten, G. The removal of the sperm perinuclear theca and its association with the bovine oocyte surface during fertilization. Dev. Biol. 188, 7584 (1997).CrossRefGoogle ScholarPubMed
Luetjens, C. M., Payne, C. & Schatten, G. Non-random chromosome positioning in human sperm and sex chromosome anomalies following intracytoplasmic sperm injection. Lancet 353, 1240 (1999).CrossRefGoogle ScholarPubMed
Wu, A. T. H. et al. PAWP, a sperm-specific WW domain-binding protein, promotes meiotic resumption and pronuclear development during fertilization. J. Biol. Chem. 282, 1216412175 (2007).CrossRefGoogle ScholarPubMed

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