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Bovine ICSI: limiting factors, strategies to improve its efficiency and alternative approaches

Published online by Cambridge University Press:  09 September 2022

Fernanda Fuentes ,
Erwin Muñoz ,
María José Contreras ,
María Elena Arias  and
Ricardo Felmer Open the ORCID record for Ricardo Felmer [Opens in a new window]
Fernanda Fuentes
Affiliation:
Laboratory of Reproduction, Centre of Reproductive Biotechnology (CEBIOR-BIOREN), Faculty of Medicine, Universidad de la Frontera, Temuco, Chile PhD Program in Applied Cellular and Molecular Biology. Universidad de la Frontera, Temuco, Chile
Erwin Muñoz
Affiliation:
Laboratory of Reproduction, Centre of Reproductive Biotechnology (CEBIOR-BIOREN), Faculty of Medicine, Universidad de la Frontera, Temuco, Chile PhD Program in Applied Cellular and Molecular Biology. Universidad de la Frontera, Temuco, Chile
María José Contreras
Affiliation:
Laboratory of Reproduction, Centre of Reproductive Biotechnology (CEBIOR-BIOREN), Faculty of Medicine, Universidad de la Frontera, Temuco, Chile PhD Program in Applied Cellular and Molecular Biology. Universidad de la Frontera, Temuco, Chile
María Elena Arias
Affiliation:
Laboratory of Reproduction, Centre of Reproductive Biotechnology (CEBIOR-BIOREN), Faculty of Medicine, Universidad de la Frontera, Temuco, Chile Department of Agricultural Production, Faculty of Agriculture and Forestry Sciences, Universidad de la Frontera, Temuco, Chile
Ricardo Felmer*
Affiliation:
Laboratory of Reproduction, Centre of Reproductive Biotechnology (CEBIOR-BIOREN), Faculty of Medicine, Universidad de la Frontera, Temuco, Chile Department of Agricultural Sciences and Natural Resources, Faculty of Agriculture and Forestry Sciences, Universidad de la Frontera, Temuco, Chile
*
Author for correspondence: Ricardo Felmer. Laboratory of Reproduction, Centre of Reproductive Biotechnology (CEBIOR-BIOREN), Department of Agricultural Sciences and Natural Resources, Faculty of Agriculture and Forestry, Universidad de La Frontera, Montevideo 0870, P.O. Box 54-D, Temuco, Chile. Tel: +56 45 2325591. E-mail: ricardo.felmer@ufrontera.cl
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Summary

Intracytoplasmic sperm injection (ICSI) is an assisted reproductive technique mainly used to overcome severe infertility problems associated with the male factor, but in cattle its efficiency is far from optimal. Artificial activation treatments combining ionomycin (Io) with 6-dimethylaminopurine after piezo-ICSI or anisomycin after conventional ICSI have recently increased the blastocyst rate obtained. Compounds to capacitate bovine spermatozoa, such as heparin and methyl-β-cyclodextrin and compounds to destabilize sperm membranes such as NaOH, lysolecithin and Triton X-100, have been assessed, although they have failed to substantially improve post-ICSI embryonic development. Disulfide bond reducing agents, such as dithiothreitol (DTT), dithiobutylamine and reduced glutathione, have been assessed to decondense the hypercondensed head of bovine spermatozoa, the two latter being more efficient than DTT and less harmful. Although piezo-directed ICSI without external activation has generated high fertilization rates and modest rates of early embryo development, other studies have required exogenous activation to improve the results. This manuscript thoroughly reviews the different strategies used in bovine ICSI to improve its efficiency and proposes some alternative approaches, such as the use of extracellular vesicles (EVs) as ‘biological methods of oocyte activation’ or the incorporation of EVs in the in vitro maturation and/or culture medium as antioxidant defence agents to improve the competence of the ooplasm, as well as a preincubation of the spermatozoa in estrous oviductal fluid to induce physiological capacitation and acrosome reaction before ICSI, and the use of hyaluronate in the sperm immobilization medium.

Keywords

BovineChromatin decondensationIntracytoplasmic sperm injection (ICSI)Oocyte activationPiezoSperm capacitation
Type
Review Article
Information
Zygote , Volume 30 , Issue 6 , December 2022 , pp. 749 - 767
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Aarabi, M., Balakier, H., Bashar, S., Moskovtsev, S. I., Sutovsky, P., Librach, C. L. and Oko, R. (2014). Sperm-derived WW domain-binding protein, PAWP, elicits calcium oscillations and oocyte activation in humans and mice. FASEB Journal, 28(10), 4434–4440. doi: 10.1096/fj.14-256495 CrossRefGoogle ScholarPubMed
Abdalla, H., Shimoda, M., Hirabayashi, M. and Hochi, S. (2009). A combined treatment of ionomycin with Et improves blastocyst development of bovine oocytes harvested from stored ovaries and microinjected with spermatozoa. Theriogenology, 72(4), 453–460. doi: 10.1016/j.theriogenology.2009.03.011 CrossRefGoogle Scholar
Águila, L., Zambrano, F., Arias, M. E. and Felmer, R. (2017). Sperm capacitation pretreatment positively impacts bovine intracytoplasmic sperm injection. Molecular Reproduction and Development, 84(7), 649–659. doi: 10.1002/mrd.22834 CrossRefGoogle ScholarPubMed
Alberio, R., Kubelka, M., Zakhartchenko, V., Hajdúch, M., Wolf, E. and Motlik, J. (2000). Activation of bovine oocytes by specific inhibition of cyclin-dependent kinases. Molecular Reproduction and Development, 55(4), 422–432. doi: 10.1002/(SICI)1098-2795(200004)55:4<422::AID-MRD10>3.0.CO;2-C 3.0.CO;2-C>CrossRefGoogle ScholarPubMed
Alberio, R., Zakhartchenko, V., Motlik, J. and Wolf, E. (2001). Mammalian oocyte activation: Lessons from the sperm and implications for nuclear transfer. International Journal of Developmental Biology, 45(7), 797–809.Google ScholarPubMed
Almiñana, C., Tsikis, G., Labas, V., Uzbekov, R., da Silveira, J. C., Bauersachs, S. and Mermillod, P. (2018). Deciphering the oviductal extracellular vesicles content across the estrous cycle: Implications for the gametes-oviduct interactions and the environment of the potential embryo. BMC Genomics, 19(1), 622. doi: 10.1186/s12864-018-4982-5 CrossRefGoogle ScholarPubMed
Alvarez, J. G. and Storey, B. T. (1983). Taurine, hypotaurine, epinephrine and albumin inhibit lipid peroxidation in rabbit spermatozoa and protect against loss of motility. Biology of Reproduction, 29(3), 548–555. doi: 10.1095/biolreprod29.3.548 CrossRefGoogle ScholarPubMed
Andrews, J. C., Nolan, J. P., Hammerstedt, R. H. and Bavister, B. D. (1994). Role of zinc during hamster sperm capacitation. Biology of Reproduction, 51(6), 1238–1247. doi: 10.1095/biolreprod51.6.1238 CrossRefGoogle ScholarPubMed
Arias, M. E., Sánchez, R., Risopatrón, J., Pérez, L. and Felmer, R. (2014). Effect of sperm pretreatment with sodium hydroxide and dithiothreitol on the efficiency of bovine intracytoplasmic sperm injection. Reproduction, Fertility, and Development, 26(6), 847–854. doi: 10.1071/RD13009 CrossRefGoogle ScholarPubMed
Arias, M. E., Risopatrón, J., Sánchez, R. and Felmer, R. (2015). Intracytoplasmic sperm injection affects embryo developmental potential and gene expression in cattle. Reproductive Biology, 15(1), 34–41. doi: 10.1016/j.repbio.2014.11.001 CrossRefGoogle ScholarPubMed
Arias, M. E., Sánchez, R. and Felmer, R. (2016). Effect of anisomycin, a protein synthesis inhibitor, on the in vitro developmental potential, ploidy and embryo quality of bovine ICSI embryos. Zygote, 24(5), 724–732. doi: 10.1017/S0967199416000034 CrossRefGoogle ScholarPubMed
Arias, M. E., Andara, K., Briones, E. and Felmer, R. (2017). Bovine sperm separation by swim-up and density gradients (Percoll and BoviPure): Effect on sperm quality, function and gene expression. Reproductive Biology, 17(2), 126–132. doi: 10.1016/j.repbio.2017.03.002 CrossRefGoogle ScholarPubMed
Ashibe, S., Miyamoto, R., Kato, Y. and Nagao, Y. (2019). Detrimental effects of oxidative stress in bovine oocytes during intracytoplasmic sperm injection (ICSI). Theriogenology, 133, 71–78. doi: 10.1016/j.theriogenology.2019.04.012 CrossRefGoogle Scholar
Awda, B. J., Miller, S. P., Montanholi, Y. R., Voort, G. V., Caldwell, T., Buhr, M. M. and Swanson, K. C. (2013). The relationship between feed efficiency traits and fertility in young beef bulls. Canadian Journal of Animal Science, 93(2), 185–192. doi: 10.4141/cjas2012-092 CrossRefGoogle Scholar
Balhorn, R. (1982). A model for the structure of chromatin in mammalian sperm. Journal of Cell Biology, 93(2), 298–305. doi: 10.1083/jcb.93.2.298 CrossRefGoogle Scholar
Balhorn, R. (1989). Mammalian protamines: Structure and molecular interactions. In: Adolph, K. W. (ed.), Molecular biology of chromosome function (1st edn), 1 (pp. 366–395). Springer.CrossRefGoogle Scholar
Bangham, A. D. and Horne, R. W. (1964). Negative staining of phospholipids and their structural modification by surface-active agents as observed in the electron microscope. Journal of Molecular Biology, 8, 660–668-IN10. doi: 10.1016/s0022-2836(64)80115-7 CrossRefGoogle ScholarPubMed
Baqir, S., Orabah, A. B., Al-Zeheimi, N., Al-Shakaili, Y., Al-Rasbi, K., Gartley, C. J. and Mastromonaco, G. (2018). Computer assisted sperm analysis (CASA) in the critically endangered captive Arabian leopard (Panthera pardus nimr): A multivariate clustering analysis. Rasbi, K. Journal of Veterinary Science and Technology, 9, 2.Google Scholar
Barrachina, F., Soler-Ventura, A., Oliva, R. and Jodar, M. (2018). Sperm nucleoproteins (histones and protamines). In Zini, A. and Agarwal, A. (eds), A clinician’s guide to sperm DNA and chromatin damage (1st edn), 1 (pp. 31–51). Springer.CrossRefGoogle Scholar
Bathala, P., Fereshteh, Z., Li, K., Al-Dossary, A. A., Galileo, D. S. and Martin-DeLeon, P. A. (2018). Oviductal extracellular vesicles (oviductosomes, OVS) are conserved in humans: Murine OVS play a pivotal role in sperm capacitation and fertility. Molecular Human Reproduction, 24(3), 143–157. doi: 10.1093/molehr/gay003 Google ScholarPubMed
Bernecic, N. C., Gadella, B. M., de Graaf, S. P. and Leahy, T. (2020). Synergism between albumin, bicarbonate and cAMP upregulation for cholesterol efflux from ram sperm. Reproduction, 160(2), 269–280. doi: 10.1530/REP-19-0430 CrossRefGoogle ScholarPubMed
Bevacqua, R. J., Pereyra-Bonnet, F., Fernandez-Martin, R. and Salamone, D. F. (2010). High rates of bovine blastocyst development after ICSI-mediated gene transfer assisted by chemical activation. Theriogenology, 74(6), 922–931. doi: 10.1016/j.theriogenology.2010.04.017 CrossRefGoogle ScholarPubMed
Bromfield, E. G., Aitken, R. J., Gibb, Z., Lambourne, S. R. and Nixon, B. (2014). Capacitation in the presence of methyl-b-cyclodextrin results in enhanced zona pellucida-binding ability of stallion spermatozoa. Reproduction, 147(2), 153–166. doi: 10.1530/REP-13-0393 CrossRefGoogle Scholar
Cai, Z. G., An, J. H., Liu, Y. L., Yie, S. M., Zhang, Y., Li, F. P., Chen, J. S., Wang, X., Morrell, J. M. and Hou, R. (2018). Single layer centrifugation improves the quality of frozen–thawed sperm of giant panda (Ailuropoda melanoleuca). Animal Reproduction Science, 195, 58–64. doi: 10.1016/j.anireprosci.2018.05.006 CrossRefGoogle Scholar
Canel, N. G., Bevacqua, R. J., Hiriart, M. I., Rabelo, N. C., de Almeida Camargo, L. S., Romanato, M., de Calvo, L. P. and Salamone, D. F. (2017). Sperm pretreatment with heparin and l-glutathione, sex-sorting, and double cryopreservation to improve intracytoplasmic sperm injection in bovine. Theriogenology, 93, 62–70. doi: 10.1016/j.theriogenology.2016.12.018 CrossRefGoogle ScholarPubMed
Canel, N. G., Suvá, M., Bevacqua, R. J., Arias, M. E., Felmer, R. and Salamone, D. F. (2018). Improved embryo development using high cysteamine concentration during IVM and sperm co-culture with COCs previous to ICSI in bovine. Theriogenology, 117, 26–33. doi: 10.1016/j.theriogenology.2018.05.017 CrossRefGoogle ScholarPubMed
Cassuto, N. G., Hazout, A., Bouret, D., Balet, R., Larue, L., Benifla, J. L. and Viot, G. (2014). Low birth defects by deselecting abnormal spermatozoa before ICSI. Reproductive Biomedicine Online, 28(1), 47–53. doi: 10.1016/j.rbmo.2013.08.013 CrossRefGoogle ScholarPubMed
Cesari, A., Kaiser, G. G., Mucci, N., Mutto, A., Vincenti, A., Fornés, M. W. and Alberio, R. H. (2006). Integrated morphophysiological assessment of two methods for sperm selection in bovine embryo production in vitro . Theriogenology, 66(5), 1185–1193. doi: 10.1016/j.theriogenology.2006.03.029 CrossRefGoogle ScholarPubMed
Chen, S. H. and Seidel, G. E. Jr. (1997). Effects of oocyte activation and treatment of spermatozoa on embryonic development following intracytoplasmic sperm injection in cattle. Theriogenology, 48(8), 1265–1273. doi: 10.1016/S0093-691X(97)00369-5 CrossRefGoogle Scholar
Chowdhury, M. M. R., Choi, B. H., Khan, I., Lee, K. L., Mesalam, A., Song, S. H., Xu, L., Joo, M. D., Afrin, F. and Kong, I. K. (2017). Supplementation of lycopene in maturation medium improves bovine embryo quality in vitro . Theriogenology, 103, 173–184. doi: 10.1016/j.theriogenology.2017.08.003 CrossRefGoogle Scholar
Corzett, M., Mazrimas, J. and Balhorn, R. (2002). Protamine 1: Protamine 2 stoichiometry in the sperm of eutherian mammals. Molecular Reproduction and Development, 61(4), 519–527. doi: 10.1002/mrd.10105 CrossRefGoogle ScholarPubMed
da Silveira, J. C., Andrade, G. M., Del Collado, M., Sampaio, R. V., Sangalli, J. R., Silva, L. A., Pinaffi, F. V. L., Jardim, I. B., Cesar, M. C., Nogueira, M. F. G., Cesar, A. S. M., Coutinho, L. L., Pereira, R. W., Perecin, F. and Meirelles, F. V. (2017). Supplementation with small-extracellular vesicles from ovarian follicular fluid during in vitro production modulates bovine embryo development. PLOS ONE, 12(6), e0179451. doi: 10.1371/journal.pone.0179451 CrossRefGoogle ScholarPubMed
Ded, L., Hwang, J. Y., Miki, K., Shi, H. F. and Chung, J. J. (2020). 3D in situ imaging of the female reproductive tract reveals molecular signatures of fertilizing spermatozoa in mice. eLife, 9, e62043. doi: 10.7554/eLife.62043 CrossRefGoogle ScholarPubMed
Devito, L. G., Fernandes, C. B., Blanco, I. D. P., Tsuribe, P. M. and Landim-Alvarenga, F. C. (2010). Use of a Piezo drill for intracytoplasmic sperm injection into cattle oocytes activated with ionomycin associated with roscovitine. Reproduction in Domestic Animals, 45(4), 654–658. doi: 10.1111/j.1439-0531.2008.01323.x Google ScholarPubMed
Ding, D., Wang, Q., Li, X., Chen, B., Zou, W., Ji, D. and Zhang, Z. (2020). Effects of different polyvinylpyrrolidone concentrations on intracytoplasmic sperm injection. Zygote, 28, 148–153 CrossRefGoogle Scholar
Dozortsev, D., Rybouchkin, A., De Sutter, P. and Dhont, M. (1995). Sperm plasma membrane damage prior to intracytoplasmic sperm injection: A necessary condition for sperm nucleus decondensation. Human Reproduction, 10(11), 2960–2964. doi: 10.1093/oxfordjournals.humrep.a135829 CrossRefGoogle ScholarPubMed
Dreger, H., Westphal, K., Weller, A., Baumann, G., Stangl, V., Meiners, S. and Stangl, K. (2009). Nrf2-dependent upregulation of antioxidative enzymes: A novel pathway for proteasome inhibitor-mediated cardioprotection. Cardiovascular Research, 83(2), 354–361. doi: 10.1093/cvr/cvp107 CrossRefGoogle ScholarPubMed
Ducibella, T., Huneau, D., Angelichio, E., Xu, Z., Schultz, R. M., Kopf, G. S., Fissore, R., Madoux, S. and Ozil, J. P. (2002). Egg-to-embryo transition is driven by differential responses to Ca2+ oscillation number. Developmental Biology, 250(2), 280–291. doi: 10.1006/dbio.2002.0788 CrossRefGoogle Scholar
Feitosa, W. B., Lopes, E., Visintin, J. A. and Assumpção, M. E. O. D. (2020). Endoplasmic reticulum distribution during bovine oocyte activation is regulated by protein kinase C via actin filaments. Journal of Cellular Physiology, 235(7–8), 5823–5834. doi: 10.1002/jcp.29516 CrossRefGoogle ScholarPubMed
Felmer, R. and Arias, M. E. (2015). Activation treatment of recipient oocytes affects the subsequent development and ploidy of bovine parthenogenetic and somatic cell nuclear transfer (SCNT) embryos. Molecular Reproduction and Development, 82(6), 441–449. doi: 10.1002/mrd.22492 CrossRefGoogle ScholarPubMed
Fernandes, C. B., Devito, L. G., Martins, L. R., Blanco, I. D., de Lima Neto, J. F., Tsuribe, P. M., Gonçalves, C. G. and da Cruz Landim-Alvarenga, F. (2014). Artificial activation of bovine and equine oocytes with cycloheximide, roscovitine, strontium, or 6-dimethylaminopurine in low or high calcium concentrations. Zygote, 22(3), 387–394. doi: 10.1017/S0967199412000627 CrossRefGoogle ScholarPubMed
Fissore, R. A. and Robl, J. M. (1992). Intracellular Ca2+ response of rabbit oocytes to electrical stimulation. Molecular Reproduction and Development, 32(1), 9–16. doi: 10.1002/mrd.1080320103 CrossRefGoogle ScholarPubMed
Franklin, A. D., Waddell, W. T. and Goodrowe, K. L. (2018). Red wolf (Canis rufus) sperm quality and quantity is affected by semen collection method, extender components, and post-thaw holding temperature. Theriogenology, 116, 41–48. doi: 10.1016/j.theriogenology.2018.05.007 CrossRefGoogle ScholarPubMed
Fujinami, N., Hosoi, Y., Kato, H., Matsumoto, K., Saeki, K. and Iritani, A. (2004). Activation with Et improves embryo development of ICSI-derived oocytes by regulation of kinetics of MPF activity. Journal of Reproduction and Development, 50(2), 171–178. doi: 10.1262/jrd.50.171 CrossRefGoogle Scholar
Furuhashi, K., Saeki, Y., Enatsu, N., Iwasaki, T., Ito, K., Mizusawa, Y., Matsumoto, Y., Kokeguchi, S. and Shiotani, M. (2019). Piezo-assisted ICSI improves fertilization and blastocyst development rates compared with conventional ICSI in women aged more than 35 years. Reproductive Medicine and Biology, 18(4), 357–361. doi: 10.1002/rmb2.12290 CrossRefGoogle ScholarPubMed
Galli, C., Vassiliev, I., Lagutina, I., Galli, A. and Lazzari, G. (2003). Bovine embryo development following ICSI: Effect of activation, sperm capacitation and pre-treatment with dithiothreitol. Theriogenology, 60(8), 1467–1480. doi: 10.1016/s0093-691x(03)00133-x CrossRefGoogle ScholarPubMed
Hashimoto, S., Minami, N., Takakura, R., Yamada, M., Imai, H. and Kashima, N. (2000). Low oxygen tension during in vitro maturation is beneficial for supporting the subsequent development of bovine cumulus–oocyte complexes. Molecular Reproduction and Development, 57(4), 353–360. doi: 10.1002/1098-2795(200012)57:4<353::AID-MRD7>3.0.CO;2-R 3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Hassan, B. M. S., Fang, X., Roy, P. K., Shin, S. T. and Cho, J. K. (2017). Effect of alpha lipoic acid as an antioxidant supplement during in vitro maturation medium on bovine embryonic development. Journal of Animal Reproduction and Biotechnology, 32(3), 123–130. doi: 10.12750/JET.2017.32.3.123 CrossRefGoogle Scholar
He, W., Chen, J. and Gao, S. (2019). Mammalian haploid stem cells: Establishment, engineering and applications. Cellular and Molecular Life Sciences, 76(12), 2349–2367. doi: 10.1007/s00018-019-03069-6 Google ScholarPubMed
Hirose, M., Honda, A., Fulka, H., Tamura-Nakano, M., Matoba, S., Tomishima, T., Mochida, K., Hasegawa, A., Nagashima, K., Inoue, K., Ohtsuka, M., Baba, T., Yanagimachi, R. and Ogura, A. (2020). Acrosin is essential for sperm penetration through the zona pellucida in hamsters. Proceedings of the National Academy of Sciences of the United States of America, 117(5), 2513–2518. doi: 10.1073/pnas.1917595117 CrossRefGoogle ScholarPubMed
Horiuch, T., Emuta, C., Yamauchi, Y., Oikawa, T., Numabe, T. and Yanagimachi, R. (2002). Birth of normal calves after intracytoplasmic sperm injection of bovine oocytes: A methodological approach. Theriogenology, 57(3), 1013–1024. doi: 10.1016/s0093-691x(01)00701-4 CrossRefGoogle ScholarPubMed
Horiuchi, T. and Numabe, T. (1999). Intracytoplasmic sperm injection (ICSI) in cattle and other domestic animals: Problems and improvements in practical use. Journal of Mammalian Ova Research, 16(1), 1–9. doi: 10.1274/jmor.16.1 CrossRefGoogle Scholar
Hoth, M. and Penner, R. (1992). Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature, 355(6358), 353–356. doi: 10.1038/355353a0 CrossRefGoogle ScholarPubMed
Howlett, S. K. and Bolton, V. N. (1985). Sequence and regulation of morphological and molecular events during the first cell cycle of mouse embryogenesis. Journal of Embryology and Experimental Morphology, 87, 175–206. doi: 10.1242/dev.87.1.175 Google ScholarPubMed
Hu, L. L., Shen, X. H., Zheng, Z., Wang, Z. D., Liu, Z. H., Jin, L. H. and Lei, L. (2012). Cytochalasin B treatment of mouse oocytes during intracytoplasmic sperm injection (ICSI) increases embryo survival without impairment of development. Zygote, 20(4), 361–369. doi: 10.1017/S0967199411000438 CrossRefGoogle ScholarPubMed
Hwang, S., Lee, E., Yoon, J., Yoon, B. K., Lee, J. H. and Choi, D. (2000). Effects of electric stimulation on bovine oocyte activation and embryo development in intracytoplasmic sperm injection procedure. Journal of Assisted Reproduction and Genetics, 17(6), 310–314. doi: 10.1023/a:1009496726343 CrossRefGoogle ScholarPubMed
Hyttel, P., Greve, T. and Callesen, H. (1988). Ultrastructure of in-vivo fertilization in superovulated cattle. Journal of Reproduction and Fertility, 82(1), 1–13. doi: 10.1530/jrf.0.0820001 CrossRefGoogle ScholarPubMed
Jakop, U., Fuchs, B., Süß, R., Wibbelt, G., Braun, B., Müller, K. and Schiller, J. (2009). The solubilisation of boar sperm membranes by different detergents - a microscopic, MALDI-TOF MS, 31P NMR and PAGE study on membrane lysis, extraction efficiency, lipid and protein composition. Lipids in Health and Disease, 8, 1–16. doi: 10.1186/1476-511X-8-49 CrossRefGoogle Scholar
Joiakim, A., Mathieu, P. A., Elliott, A. A. and Reiners, J. J. (2004). Superinduction of CYP1A1 in MCF10A cultures by cycloheximide, anisomycin, and puromycin: A process independent of effects on protein translation and unrelated to suppression of aryl hydrocarbon receptor proteolysis by the proteasome. Molecular Pharmacology, 66(4), 936–947. doi: 10.1124/mol.66.4.CrossRefGoogle ScholarPubMed
Katayama, M., Sutovsky, P., Yang, B. S., Cantley, T., Rieke, A., Farwell, R., Oko, R. and Day, B. N. (2005). 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(6), 907–916. doi: 10.1530/rep.1.0680 CrossRefGoogle ScholarPubMed
Katayose, H., Yanagida, K., Shinoki, T., Kawahara, T., Horiuchi, T. and Sato, A. (1999). Efficient injection of bull spermatozoa into oocytes using a Piezo-driven pipette. Theriogenology, 52(7), 1215–1224. doi: 10.1016/S0093-691X(99)00213-7 CrossRefGoogle ScholarPubMed
Kaya, A. and Memili, E. (2016). Sperm macromolecules associated with bull fertility. Animal Reproduction Science, 169, 88–94. doi: 10.1016/j.anireprosci.2016.02.015 CrossRefGoogle ScholarPubMed
Kato, Y. and Nagao, Y. (2009). Effect of PVP on sperm capacitation status and embryonic development in cattle. Theriogenology, 72(5), 624–635. doi: 10.1016/j.theriogenology.2009.04.018 CrossRefGoogle ScholarPubMed
Kato, Y. and Nagao, Y. (2012). Effect of polyvinylpyrrolidone on sperm function and early embryonic development following intracytoplasmic sperm injection in human assisted reproduction. Reproductive Medicine and Biology, 11(4), 165–176. doi: 10.1007/s12522-012-0126-9 CrossRefGoogle ScholarPubMed
Kato, Y. and Nagao, Y. (2015). Changes in sperm motility and capacitation induce chromosomal aberration of the bovine embryo following intracytoplasmic sperm injection. PLOS ONE, 10(6), e0129285. doi: 10.1371/journal.pone.0129285 CrossRefGoogle ScholarPubMed
Kerns, K., Sharif, M., Zigo, M., Xu, W., Hamilton, L. E., Sutovsky, M., Ellersieck, M., Drobnis, E. Z., Bovin, N., Oko, R., Miller, D. and Sutovsky, P. (2020). Sperm cohort-specific zinc signature acquisition and capacitation-induced zinc flux regulate sperm-oviduct and sperm–zona pellucida interactions. International Journal of Molecular Sciences, 21(6), 2121. doi: 10.3390/ijms21062121 CrossRefGoogle ScholarPubMed
Kerns, K., Zigo, M., Drobnis, E. Z., Sutovsky, M. and Sutovsky, P. (2018). Zinc ion flux during mammalian sperm capacitation. Nature Communications, 9(1), 2061. doi: 10.1038/s41467-018-04523-y CrossRefGoogle ScholarPubMed
Keskintepe, L., Pacholczyk, G., Machnicka, A., Norris, K., Curuk, M. A., Khan, I. and Brackett, B. G. (2002). Bovine blastocyst development from oocytes injected with freeze-dried spermatozoa. Biology of Reproduction, 67(2), 409–415. doi: 10.1095/biolreprod67.2.409 CrossRefGoogle ScholarPubMed
Kimura, Y. and Yanagimachi, R. (1995). Intracytoplasmic sperm injection in the mouse. Biology of Reproduction, 52(4), 709–720. doi: 10.1095/biolreprod52.4.709 CrossRefGoogle ScholarPubMed
Kline, D. and Kline, J. T. (1992). Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Developmental Biology, 149(1), 80–89. doi: 10.1016/0012-1606(92)90265-i CrossRefGoogle ScholarPubMed
Knitlova, D., Hulinska, P., Jeseta, M., Hanzalova, K., Kempisty, B. and Machatkova, M. (2017). Supplementation of l-carnitine during in vitro maturation improves embryo development from less competent bovine oocytes. Theriogenology, 102, 16–22. doi: 10.1016/j.theriogenology.2017.06.025 CrossRefGoogle ScholarPubMed
Kosower, N. S., Katayose, H. and Yanagimachi, R. (1992). Thiol-disulfide status and acridine orange fluorescence of mammalian sperm nuclei. Journal of Andrology, 13(4), 342–348.Google ScholarPubMed
Kubiak, J. Z., Ciemerych, M. A., Hupalowska, A., Sikora-Polaczek, M. and Polanski, Z. (2008). On the transition from the meiotic to mitotic cell cycle during early mouse development. International Journal of Developmental Biology, 52(2–3), 201–217. doi: 10.1387/ijdb.072337jk CrossRefGoogle ScholarPubMed
Kumar, A., Pandita, S., Ganguly, S., Soren, S. and Pagrut, N. (2018). Beneficial effects of seminal prostasomes on sperm functional parameters. Journal of Entomology and Zoology Studies, 6, 2464–2471.Google Scholar
Kumaresan, A., Johannisson, A., Humblot, P. and Bergqvist, A. S. (2019). Effect of bovine oviductal fluid on motility, tyrosine phosphorylation, and acrosome reaction in cryopreserved bull spermatozoa. Theriogenology, 124, 48–56. doi: 10.1016/j.theriogenology.2018.09.028 CrossRefGoogle ScholarPubMed
Lee, J. W., Chang, H. C., Wu, H. Y., Liu, S. S., Wang, C. H., Chu, C. Y. and Shen, P. C. (2015). Effects of sperm pretreatment and embryo activation methods on the development of bovine embryos produced by intracytoplasmic sperm injection. Reproductive Biology, 15(3), 154–162. doi: 10.1016/j.repbio.2015.07.001 CrossRefGoogle ScholarPubMed
Lee, K. B. and Niwa, K. (2006). Fertilization and development in vitro of bovine oocytes following intracytoplasmic injection of heat-dried sperm heads. Biology of Reproduction, 74(1), 146–152. doi: 10.1095/biolreprod.105.044743 CrossRefGoogle ScholarPubMed
Li, C., Mizutani, E., Ono, T. and Wakayama, T. (2009). Production of normal mice from spermatozoa denatured with high alkali treatment before ICSI. Reproduction, 137(5), 779–792. doi: 10.1530/REP-08-0476 CrossRefGoogle ScholarPubMed
Li, C., Mizutani, E., Ono, T. and Wakayama, T. (2010). An efficient method for generating transgenic mice using NaOH-treated spermatozoa. Biology of Reproduction, 82(2), 331–340. doi: 10.1095/biolreprod.109.078501 CrossRefGoogle ScholarPubMed
Liang, Y. Y., Ye, D. N., Laowtammathron, C., Phermthai, T., Nagai, T., Somfai, T. and Parnpai, R. (2011). Effects of chemical activation treatment on development of swamp buffalo (Bubalus bubalis) oocytes matured in vitro and fertilized by intracytoplasmic sperm injection. Reproduction in Domestic Animals, 46(1), e67–e73. doi: 10.1111/j.1439-0531.2010.01636.x CrossRefGoogle ScholarPubMed
Liu, D. Y. and Baker, H. W. (1993). Inhibition of acrosin activity with a trypsin inhibitor blocks human sperm penetration of the zona pellucida. Biology of Reproduction, 48(2), 340–348. doi: 10.1095/biolreprod48.2.340 CrossRefGoogle ScholarPubMed
Lukesh, J. C., Palte, M. J. and Raines, R. T. (2012). A potent, versatile disulfide-reducing agent from aspartic acid. Journal of the American Chemical Society, 134(9), 4057–4059. doi: 10.1021/ja211931f CrossRefGoogle ScholarPubMed
Luo, M., Shang, L., Brooks, M. D., Jiagge, E., Zhu, Y., Buschhaus, J. M., Conley, S., Fath, M. A., Davis, A., Gheordunescu, E., Wang, Y., Harouaka, R., Lozier, A., Triner, D., McDermott, S., Merajver, S. D., Luker, G. D., Spitz, D. R. and Wicha, M. S. (2018). Targeting breast cancer stem cell state equilibrium through modulation of redox signaling. Cell Metabolism, 28(1), 69–86.e6. doi: 10.1016/j.cmet.2018.06.006 CrossRefGoogle ScholarPubMed
Madgwick, S., Levasseur, M. and Jones, K. T. (2005). Calmodulin-dependent protein kinase II, and not protein kinase C, is sufficient for triggering cell-cycle resumption in mammalian eggs. Journal of Cell Science, 118(17), 3849–3859. doi: 10.1242/jcs.02506 CrossRefGoogle Scholar
Malcuit, C., Maserati, M., Takahashi, Y., Page, R. and Fissore, R. A. (2006). Intracytoplasmic sperm injection in the bovine induces abnormal [Ca2+]I responses and oocyte activation. Reproduction, Fertility, and Development, 18(1–2), 39–51. doi: 10.1071/rd05131 CrossRefGoogle ScholarPubMed
Matamoros-Volante, A., Moreno-Irusta, A., Torres-Rodriguez, P., Giojalas, L., Gervasi, M. G., Visconti, P. E. and Treviño, C. L. (2018). Semi-automatized segmentation method using image-based flow cytometry to study sperm physiology: The case of capacitation-induced tyrosine phosphorylation. Molecular Human Reproduction, 24(2), 64–73. doi: 10.1093/molehr/gax062 CrossRefGoogle ScholarPubMed
Mehmood, A., Anwar, M. and Naqvi, S. M. (2009). Motility, acrosome integrity, membrane integrity and oocyte cleavage rate of sperm separated by swim-up or Percoll gradient method from frozen–thawed buffalo semen. Animal Reproduction Science, 111(2–4), 141–148. doi: 10.1016/j.anireprosci.2008.02.011 CrossRefGoogle ScholarPubMed
Meizel, S. (1985). Molecules that initiate or help stimulate the acrosome reaction by their interaction with the mammalian sperm surface. American Journal of Anatomy, 174(3), 285–302. doi: 10.1002/aja.1001740309 CrossRefGoogle ScholarPubMed
Mermillod, P., Tomanek, M., Marchal, R. and Meijer, L. (2000). High developmental competence of cattle oocytes maintained at the germinal vesicle stage for 24 hours in culture by specific inhibition of MPF kinase activity. Molecular Reproduction and Development, 55(1), 89–95. doi: 10.1002/(SICI)1098-2795(200001)55:1<89::AID-MRD12>3.0.CO;2-M 3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Minamihashi, A., Watson, A. J., Watson, P. H., Church, R. B. and Schultz, G. A. (1993). Bovine parthenogenetic blastocysts following in vitro maturation and oocyte activation with Et. Theriogenology, 40(1), 63–76. doi: 10.1016/0093-691x(93)90341-2 CrossRefGoogle Scholar
Moreira, P. N., De la Fuente, J., Palasz, A. T. and Gutiérrez-Adán, A. (2005). 320 Use of synthetic hyaluronan or polyvinylpyrrolidone for intracytoplasmic sperm injection into mouse oocytes. Reproduction, Fertility and Development, 17(2), 310–311. doi: 10.1071/RDv17n2Ab320 CrossRefGoogle Scholar
Morozumi, K. and Yanagimachi, R. (2005). Incorporation of the acrosome into the oocyte during intracytoplasmic sperm injection could be potentially hazardous to embryo development. Proceedings of the National Academy of Sciences of the United States of America, 102(40), 14209–14214. doi: 10.1073/pnas.0507005102.CrossRefGoogle ScholarPubMed
Morozumi, K., Shikano, T., Miyazaki, S. and Yanagimachi, R. (2006). Simultaneous removal of sperm plasma membrane and acrosome before intracytoplasmic sperm injection improves oocyte activation/embryonic development. Proceedings of the National Academy of Sciences of the United States of America, 103(47), 17661–17666. doi: 10.1073/pnas.0608183103 CrossRefGoogle ScholarPubMed
Morrell, J. M. and Rodriguez-Martinez, H. (2009). Biomimetic techniques for improving sperm quality in animal breeding: A review. Open Andrology Journal, 1, 1–9.Google Scholar
Mrsny, R. J. and Meizel, S. (1985). Inhibition of hamster sperm Na+, K+-ATPase activity by taurine and hypotaurine. Life Sciences, 36(3), 271–275. doi: 10.1016/0024-3205(85)90069-4 CrossRefGoogle ScholarPubMed
Nabi, A., Entezari, F., Miresmaeili, S. M., Vahidi, S., Lorian, K., Anbari, F. and Motamedzadeh, L. (2021). Evaluation of sperm parameters and DNA integrity following different incubation times in PVP medium. Urology Journal, 1, 6936–6936 Google Scholar
Nair, R., Aboobacker, S., Mutalik, S., Kalthur, G. and Adiga, S. K. (2017). Sperm-derived factors enhance the in vitro developmental potential of haploid parthenotes. Zygote, 25(6), 697–710. doi: 10.1017/S0967199417000569 CrossRefGoogle ScholarPubMed
Nakai, M., Ito, J., Suzuki, S. I., Fuchimoto, D. I., Sembon, S., Suzuki, M., Noguchi, J., Kaneko, H., Onishi, A., Kashiwazaki, N. and Kikuchi, K. (2016). Lack of calcium oscillation causes failure of oocyte activation after intracytoplasmic sperm injection in pigs. Journal of Reproduction and Development, 62(6), 615–621. doi: 10.1262/jrd.2016-113 CrossRefGoogle ScholarPubMed
Navarrete, F. A., Águila, L., Martin-Hidalgo, D., Tourzani, D. A., Luque, G. M., Ardestani, G., Garcia-Vazquez, F. A., Levin, L. R., Buck, J., Darszon, A., Buffone, M. G., Mager, J., Fissore, R. A., Salicioni, A. M., Gervasi, M. G. and Visconti, P. E. (2019). Transient sperm starvation improves the outcome of assisted reproductive technologies. Frontiers in Cell and Developmental Biology, 7, 262. doi: 10.3389/fcell.2019.00262 CrossRefGoogle ScholarPubMed
Ng, S. C., Martelli, P., Liow, S. L., Herbert, S. and Oh, S. H. (2002). Intracytoplasmic injection of frozen–thawed epididymal spermatozoa in a nonhuman primate model, the cynomolgus monkey (Macaca fascicularis). Theriogenology, 58(7), 1385–1397. doi: 10.1016/s0093-691x(02)01035-x CrossRefGoogle Scholar
Ni, K., Spiess, A. N., Schuppe, H. C. and Steger, K. (2016). The impact of sperm protamine deficiency and sperm DNA damage on human male fertility: A systematic review and meta-analysis. Andrology, 4(5), 789–799. doi: 10.1111/andr.12216 CrossRefGoogle ScholarPubMed
Nomikos, M., Sanders, J. R., Kashir, J., Sanusi, R., Buntwal, L., Love, D., Ashley, P., Sanders, D., Knaggs, P., Bunkheila, A., Swann, K. and Lai, F. A. (2015). Functional disparity between human PAWP and PLCζ in the generation of Ca2+ oscillations for oocyte activation. Molecular Human Reproduction, 21(9), 702–710. doi: 10.1093/molehr/gav034 CrossRefGoogle ScholarPubMed
Ock, S. A., Bhak, J. S., Balasubramanian, S., Lee, H. J., Choe, S. Y. and Rho, G. J. (2003). Different activation treatments for successful development of bovine oocytes following intracytoplasmic sperm injection. Zygote, 11(1), 69–76. doi: 10.1017/s0967199403001096 CrossRefGoogle ScholarPubMed
Oh, J. S., Susor, A. and Conti, M. (2011). Protein tyrosine kinase Wee1B is essential for metaphase II exit in mouse oocytes. Science, 332(6028), 462–465. doi: 10.1126/science.1199211 CrossRefGoogle ScholarPubMed
Oikawa, T., Takada, N., Kikuchi, T., Numabe, T., Takenaka, M. and Horiuchi, T. (2005). Evaluation of activation treatments for blastocyst production and birth of viable calves following bovine intracytoplasmic sperm injection. Animal Reproduction Science, 86(3–4), 187–194. doi: 10.1016/j.anireprosci.2004.07.003 CrossRefGoogle ScholarPubMed
Oikawa, T., Itahashi, T., Yajima, R. and Numabe, T. (2018). Glutathione treatment of Japanese Black bull sperm prior to intracytoplasmic sperm injection promotes embryo development. Journal of Reproduction and Development, 64(4), 303–309. doi: 10.1262/jrd.2018-023 CrossRefGoogle ScholarPubMed
Olivares, C. C. S., Souza-Fabjan, J. M. Gd, Fonseca, J. Fd, Balaro, M. F. A., Freitas, V. JdF., Oliveira, R. Vd and Brandão, F. Z. (2017). Comparison of different sperm selection techniques in ram frozen–thawed sperm. Acta Scientiae Veterinariae, 45(1), 1–10. doi: 10.22456/1679-9216.79384 CrossRefGoogle Scholar
Palermo, G., Joris, H., Devroey, P. and Van Steirteghem, A. C. (1992). Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet, 340(8810), 17–18. doi: 10.1016/0140-6736(92)92425-f CrossRefGoogle ScholarPubMed
Pang, Y., Zhao, S., Sun, Y., Jiang, X., Hao, H., Du, W. and Zhu, H. (2018). Protective effects of melatonin on the in vitro developmental competence of bovine oocytes. Animal Science Journal, 89(4), 648–660. doi: 10.1111/asj.12970 CrossRefGoogle ScholarPubMed
Parmar, M. S., Pant, C., Karuppanas, K., Mili, B., Upadhyay, D. and Kant, V. (2013). Intracytoplasmic sperm injection (ICSI) and its applications in veterinary sciences: An overview. Science International, 1(8), 266–270. doi: 10.17311/sciintl.2013.266.270 Google Scholar
Parrish, J. J. (2014). Bovine in vitro fertilization: In vitro oocyte maturation and sperm capacitation with heparin. Theriogenology, 81(1), 67–73. doi: 10.1016/j.theriogenology.2013.08.005 CrossRefGoogle ScholarPubMed
Parsons, W. J., Ramkumar, V. and Stiles, G. L. (1988). Isobutylmethylxanthine stimulates adenylate cyclase by blocking the inhibitory regulatory protein, Gi. Molecular Pharmacology, 34(1), 37–41.Google ScholarPubMed
Pereyra-Bonnet, F., Fernández-Martín, R., Olivera, R., Jarazo, J., Vichera, G., Gibbons, A. and Salamone, D. (2008). A unique method to produce transgenic embryos in ovine, porcine, feline, bovine and equine species. Reproduction, Fertility, and Development, 20(7), 741–749. doi: 10.1071/rd07172 CrossRefGoogle ScholarPubMed
Perreault, S. D., Wolff, R. A. and Zirkin, B. R. (1984). The role of disulfide bond reduction during mammalian sperm nuclear decondensation in vivo . Developmental Biology, 101(1), 160–167. doi: 10.1016/0012-1606(84)90126-x CrossRefGoogle ScholarPubMed
Perreault, S. D., Barbee, R. R. and Slott, V. L. (1988a). Importance of glutathione in the acquisition and maintenance of sperm nuclear decondensing activity in maturing hamster oocytes. Developmental Biology, 125(1), 181–186. doi: 10.1016/0012-1606(88)90070-x CrossRefGoogle ScholarPubMed
Perreault, S. D., Barbee, R. R., Elstein, K. H., Zucker, R. M. and Keefer, C. L. (1988b). Interspecies differences in the stability of mammalian sperm nuclei assessed in vivo by sperm microinjection and in vitro by flow cytometry. Biology of Reproduction, 39(1), 157–167. doi: 10.1095/biolreprod39.1.157 CrossRefGoogle ScholarPubMed
Perry, A. C., Wakayama, T., Kishikawa, H., Kasai, T., Okabe, M., Toyoda, Y. and Yanagimachi, R. (1999). Mammalian transgenesis by intracytoplasmic sperm injection. Science, 284(5417), 1180–1183. doi: 10.1126/science.284.5417.1180 CrossRefGoogle ScholarPubMed
Prochowska, S., Niżański, W., Partyka, A., Kochan, J., Młodawska, W., Nowak, A., Skotnicki, J., Grega, T. and Pałys, M. (2019). Influence of the type of semen and morphology of individual sperm cells on the results of ICSI in domestic cats. Theriogenology, 131, 140–145. doi: 10.1016/j.theriogenology.2018.10.031 CrossRefGoogle ScholarPubMed
Ressaissi, Y., Anzalone, D. A., Palazzese, L., Czernik, M. and Loi, P. (2021). The impaired development of sheep ICSI derived embryos is not related to centriole dysfunction. Theriogenology, 159, 7–12. doi: 10.1016/j.theriogenology.2020.10.008 CrossRefGoogle Scholar
Rho, G. J., Wu, B., Kawarsky, S., Leibo, S. P. and Betteridge, K. J. (1998a). Activation regimens to prepare bovine oocytes for intracytoplasmic sperm injection. Molecular Reproduction and Development, 50(4), 485–492. doi: 10.1002/(SICI)1098-2795(199808)50:4<485::AID-MRD12>3.0.CO;2-1 3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Rho, G. J., Kawarsky, S., Johnson, W. H., Kochhar, K. and Betteridge, K. J. (1998b). Sperm and oocyte treatments to improve the formation of male and female pronuclei and subsequent development following intracytoplasmic sperm injection into bovine oocytes. Biology of Reproduction, 59(4), 918–924. doi: 10.1095/biolreprod59.4.918 CrossRefGoogle ScholarPubMed
Sá, N. A. R., Vieira, L. A., Ferreira, A. C. A., Cadenas, J., Bruno, J. B., Maside, C., Sousa, F. G. C., Cibin, F. W. S., Alves, B. G., Rodrigues, A. P. R., Leal-Cardoso, J. H., Gastal, E. L. and Figueiredo, J. R. (2020). Anethole supplementation during oocyte maturation improves in vitro production of bovine embryos. Reproductive Sciences, 27(8), 1602–1608. doi: 10.1007/s43032-020-00190-x CrossRefGoogle ScholarPubMed
Saeed-Zidane, M., Linden, L., Salilew-Wondim, D., Held, E., Neuhoff, C., Tholen, E., Hoelker, M., Schellander, K. and Tesfaye, D. (2017). Cellular and exosome mediated molecular defense mechanism in bovine granulosa cells exposed to oxidative stress. PLOS ONE, 12(11), e0187569. doi: 10.1371/journal.pone.0187569 CrossRefGoogle ScholarPubMed
Salamone, D. F., Canel, N. G. and Rodríguez, M. B. (2017). Intracytoplasmic sperm injection in domestic and wild mammals. Reproduction, 154(6), F111–F124. doi: 10.1530/REP-17-0357 CrossRefGoogle ScholarPubMed
Salgado, R. M., Brom-de-Luna, J. G., Resende, H. L., Canesin, H. S. and Hinrichs, K. (2018). Lower blastocyst quality after conventional vs. piezo ICSI in the horse reflects delayed sperm component remodeling and oocyte activation. Journal of Assisted Reproduction and Genetics, 35(5), 825–840. doi: 10.1007/s10815-018-1174-9 CrossRefGoogle ScholarPubMed
Sánchez-Villalba, E., Arias, M. E., Loren, P., Fuentes, F., Pereyra-Bonnet, F., Salamone, D. and Felmer, R. (2018). Improved expression of green fluorescent protein in cattle embryos produced by ICSI-mediated gene transfer with spermatozoa treated with streptolysin-O. Animal Reproduction Science, 196, 130–137. doi: 10.1016/j.anireprosci.2018.07.005 CrossRefGoogle ScholarPubMed
Sanders, J. R. and Swann, K. (2016). Molecular triggers of egg activation at fertilization in mammals. Reproduction, 152(2), R41–R50. doi: 10.1530/REP-16-0123 CrossRefGoogle ScholarPubMed
Sanders, J. R., Ashley, B., Moon, A., Woolley, T. E. and Swann, K. (2018). PLCζ induced Ca2+ oscillations in mouse eggs involve a positive feedback cycle of Ca2+ induced InsP3 formation from cytoplasmic PIP2 . Frontiers in Cell and Developmental Biology, 6, 36. doi: 10.3389/fcell.2018.00036 CrossRefGoogle ScholarPubMed
Seita, Y., Ito, J. and Kashiwazaki, N. (2009). Removal of acrosomal membrane from sperm head improves development of rat zygotes derived from intracytoplasmic sperm injection. Journal of Reproduction and Development, 55(5), 475–479. doi: 10.1262/jrd.20216 CrossRefGoogle ScholarPubMed
Sekhavati, M. H., Shadanloo, F., Hosseini, M. S., Tahmoorespur, M., Nasiri, M. R., Hajian, M. and Nasr-Esfahani, M. H. (2012). Improved bovine ICSI outcomes by sperm selected after combined heparin-glutathione treatment. Cell Reprogram, 14(4), 295–304. doi: 10.1089/cell.2012.0014 CrossRefGoogle ScholarPubMed
Shahverdi, A., Movahedin, M., Rezazadeh Valojerdi, M. and Kazemi Ashtiani, S. (2007). Comparison of embryo development between intracytoplasmic and piezo-assisted sperm injection after treating mouse sperms by Ca2+ ionophore. Iranian Biomedical Journal, 11(4), 245–250.Google ScholarPubMed
Shiina, Y., Kaneda, M., Matsuyama, K., Tanaka, K., Hiroi, M. and Doi, K. (1993). Role of the extracellular Ca2+ on the intracellular Ca2+ changes in fertilized and activated mouse oocytes. Journal of Reproduction and Fertility, 97(1), 143–150. doi: 10.1530/jrf.0.0970143 CrossRefGoogle ScholarPubMed
Singh, A. and Agarwal, A. (2011). The role of sperm chromatin integrity and DNA damage on male infertility. Open Reproductive Science Journal, 3(1), 65–71. doi: 10.2174/1874255601103010065 Google Scholar
Somfai, T., Bodó, S., Nagy, S., Papp, A. B., Iváncsics, J., Baranyai, B., Gócza, E. and Kovács, A. (2002). Effect of swim up and Percoll treatment on viability and acrosome integrity of frozen–thawed bull spermatozoa. Reproduction in Domestic Animals, 37(5), 285–290. doi: 10.1046/j.1439-0531.2002.00350.x CrossRefGoogle ScholarPubMed
Sovernigo, T. C., Adona, P. R., Monzani, P. S., Guemra, S., Barros, F., Lopes, F. G., Leal, C. F. D. A., Lopes, F. G. and Leal, C. L. V. (2017). Effects of supplementation of medium with different antioxidants during in vitro maturation of bovine oocytes on subsequent embryo production. Reproduction in Domestic Animals, 52(4), 561–569. doi: 10.1111/rda.12946 CrossRefGoogle ScholarPubMed
Speyer, B., O’Neill, H., Saab, W., Seshadri, S., Cawood, S., Heath, C., Gaunt, M. and Serhal, P. (2019). In assisted reproduction by IVF or ICSI, the rate at which embryos develop to the blastocyst stage is influenced by the fertilization method used: A split IVF/ICSI study. Journal of Assisted Reproduction and Genetics, 36(4), 647–654. doi: 10.1007/s10815-018-1358-3 CrossRefGoogle ScholarPubMed
Susko-Parrish, J. L., Leibfried-Rutledge, M. L., Northey, D. L., Schutzkus, V. and First, N. L. (1994). Inhibition of protein kinases after an induced calcium transient causes transition of bovine oocytes to embryonic cycles without meiotic completion. Developmental Biology, 166(2), 729–739. doi: 10.1006/dbio.1994.1351 CrossRefGoogle ScholarPubMed
Sutovsky, P. and Schatten, G. (2000). Paternal contributions to the mammalian zygote: fertilization after sperm–egg fusion. International Review of Cytology, 195, 1–65. doi: 10.1016/s0074-7696(08)62703-5 Google Scholar
Sutovsky, P., Manandhar, G., Wu, A. and Oko, R. (2003). Interactions of sperm perinuclear theca with the oocyte: Implications for oocyte activation, anti-polyspermy defense, and assisted reproduction. Microscopy Research and Technique, 61(4), 362–378. doi: 10.1002/jemt.10350 CrossRefGoogle ScholarPubMed
Suttirojpattana, T., Somfai, T., Matoba, S., Nagai, T., Parnpai, R. and Geshi, M. (2016). Pretreatment of bovine sperm with dithiobutylamine (DTBA) significantly improves embryo development after ICSI. Journal of Reproduction and Development, 62(6), 577–585. doi: 10.1262/jrd.2016-084 CrossRefGoogle ScholarPubMed
Suttner, R., Zakhartchenko, V., Stojkovic, P., Müller, S., Alberio, R., Medjugorac, I., Brem, G., Wolf, E. and Stojkovic, M. (2000). Intracytoplasmic sperm injection in bovine: Effects of oocyte activation, sperm pretreatment and injection technique. Theriogenology, 54(6), 935–948. doi: 10.1016/S0093-691X(00)00403-9 CrossRefGoogle ScholarPubMed
Suvá, M., Canel, N. G. and Salamone, D. F. (2019). Effect of single and combined treatments with MPF or MAPK inhibitors on parthenogenetic haploid activation of bovine oocytes. Reproductive Biology, 19(4), 386–393. doi: 10.1016/j.repbio.2019.09.001 CrossRefGoogle ScholarPubMed
Takahashi, T., Hanazawa, K., Inoue, T., Sato, K., Sedohara, A., Okahara, J., Suemizu, H., Yagihashi, C., Yamamoto, M., Eto, T., Konno, Y., Okano, H., Suematsu, M. and Sasaki, E. (2014). Birth of healthy offspring following ICSI in in vitro-matured common marmoset (Callithrix jacchus) oocytes. PLoS ONE, 9(4), e95560. doi: 10.1371/journal.pone.0095560 CrossRefGoogle ScholarPubMed
Takei, G. L. and Hayashi, K. (2020). Na+/K+-ATPase α4 regulates sperm hyperactivation while Na+/K+-ATPase α1 regulates basal motility in hamster spermatozoa. Theriogenology, 157, 48–60. doi: 10.1016/j.theriogenology.2020.06.028 CrossRefGoogle ScholarPubMed
Tapia, B. C. (2020). Situación de la industria láctea: Producción, precios y comercio exterior. [Santiago de Chile: Oficina de Estudios y Políticas agrarias – Odepa]. Ministerio de Agricultura, pp. 1–25.Google Scholar
Tavalaee, M., Parivar, K., Shahverdi, A. H., Ghaedi, K. and Nasr-Esfahani, M. H. (2017). Status of sperm-born oocyte activating factors (PAWP, PLCζ) and sperm chromatin in uncapacitated, capacitated and acrosome-reacted conditions. Human Fertility, 20(2), 96–103. doi: 10.1080/14647273.2016.1264011 CrossRefGoogle ScholarPubMed
Torres-Flores, U. and Hernández-Hernández, A. (2020). The interplay between replacement and retention of histones in the sperm genome. Frontiers in Genetics, 11, 780. doi: 10.3389/fgene.2020.00780 CrossRefGoogle ScholarPubMed
Tsaadon, L., Kaplan-Kraicer, R. and Shalgi, R. (2008). Myristoylated alanine-rich C kinase substrate, but not Ca2+/calmodulin-dependent protein kinase II, is the mediator in cortical granules exocytosis. Reproduction, 135(5), 613–624. doi: 10.1530/REP-07-0554 CrossRefGoogle Scholar
Tscharke, M., Kind, K., Kelly, J., Kleemann, D. and Len, J. (2020). The phosphodiesterase inhibitor, isobutyl-1-methylxanthine prevents the sudden drop in cyclic adenosine monophosphate concentration and modulates glucose metabolism of equine cumulus–oocyte complexes matured in vitro . Journal of Equine Veterinary Science, 91, 103112. doi: 10.1016/j.jevs.2020.103112 CrossRefGoogle ScholarPubMed
Tsujimoto, Y., Fujiki, K., Alam, M. E., Tsukamoto, M., Azuma, R., Kanegi, R., Anzai, M., Inaba, T., Sugiura, K. and Hatoya, S. (2019). Development of feline embryos produced by piezo-actuated intracytoplasmic sperm injection of elongated spermatids. Journal of Reproduction and Development, 65(3), 245–250. doi: 10.1262/jrd.2018-119 CrossRefGoogle ScholarPubMed
Uehara, T. and Yanagimachi, R. (1976). Microsurgical injection of spermatozoa into hamster eggs with subsequent transformation of sperm nuclei into male pronuclei. Biology of Reproduction, 15(4), 467–470. doi: 10.1095/biolreprod15.4.467 CrossRefGoogle ScholarPubMed
Unnikrishnan, V., Kastelic, J. and Thundathil, J. (2021). Intracytoplasmic sperm injection in cattle. Genes, 12(2), 198. doi: 10.3390/genes12020198 CrossRefGoogle ScholarPubMed
Valencia, C., Pérez, F. A., Matus, C., Felmer, R. and Arias, M. E. (2021). Activation of bovine oocytes by protein synthesis inhibitors: New findings on the role of MPF/MAPKs. Biology of Reproduction, 104(5), 1126–1138. doi: 10.1093/biolre/ioab019 CrossRefGoogle Scholar
Visconti, P. E., Bailey, J. L., Moore, G. D., Pan, D., Olds-Clarke, P. and Kopf, G. S. (1995a). Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development, 121(4), 1129–1137. doi: 10.1242/dev.121.4.1129 CrossRefGoogle ScholarPubMed
Visconti, P. E., Moore, G. D., Bailey, J. L., Leclerc, P., Connors, S. A., Pan, D., Olds-Clarke, P. and Kopf, G. S. (1995b). Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development, 121(4), 1139–1150. doi: 10.1242/dev.121.4.1139 CrossRefGoogle ScholarPubMed
Visconti, P. E., Galantino-Homer, H., Ning, X., Moore, G. D., Valenzuela, J. P., Jorgez, C. J., Alvarez, J. G. and Kopf, G. S. (1999). Cholesterol efflux-mediated signal transduction in mammalian sperm β-cyclodextrins initiate transmembrane signaling leading to an increase in protein tyrosine phosphorylation and capacitation. Journal of Biological Chemistry, 274(5), 3235–3242. doi: 10.1074/jbc.274.5.3235 CrossRefGoogle Scholar
Wang, B., Baldassarre, H., Pierson, J., Cote, F., Rao, K. M. and Karatzas, C. N. (2003). The in vitro and in vivo development of goat embryos produced by intracytoplasmic sperm injection using tail-cut spermatozoa. Zygote, 11(3), 219–227. doi: 10.1017/s0967199403002260 CrossRefGoogle ScholarPubMed
Wei, H. and Fukui, Y. (1999). Effects of bull, sperm type and sperm pretreatment on male pronuclear formation after intracytoplasmic sperm injection in cattle. Reproduction, Fertility, and Development, 11(1), 59–65. doi: 10.1071/rd98106 CrossRefGoogle ScholarPubMed
Wei, H. and Fukui, Y. (2002). Births of calves derived from embryos produced by intracytoplasmic sperm injection without exogenous oocyte activation. Zygote, 10(2), 149–153. doi: 10.1017/s0967199402002204 CrossRefGoogle ScholarPubMed
Wu, H., Wang, J., Cheng, H., Gao, Y., Liu, W., Zhang, Z., Jiang, H., Li, W., Zhu, F., Lv, M., Liu, C., Tan, Q., Zhang, X., Wang, C., Ni, X., Chen, Y., Song, B., Zhou, P., Wei, Z., et al. (2020). Patients with severe astenoteratospermia carrying SPAG6 or RSPH3 mutations have a positive pregnancy outcome following intracytoplasmic sperm injection. Journal of Assisted Reproduction and Genetics, 37(4), 829–840. doi: 10.1007/s10815-020-01721-w CrossRefGoogle ScholarPubMed
Yamaguchi, K., Hada, M., Fukuda, Y., Inoue, E., Makino, Y., Katou, Y., Shirahige, K. and Okada, Y. (2018). Re-evaluating the localization of sperm-retained histones revealed the modification-dependent accumulation in specific genome regions. Cell Reports, 23(13), 3920–3932. doi: 10.1016/j.celrep.2018.05.094 CrossRefGoogle ScholarPubMed
Yanagida, K., Katayose, H., Yazawa, H., Kimura, Y., Konnai, K. and Sato, A. (1999). The usefulness of a piezo-micromanipulator in intracytoplasmic sperm injection in humans. Human Reproduction, 14(2), 448–453. doi: 10.1093/humrep/14.2.448 CrossRefGoogle ScholarPubMed
Yanagimachi, R. (2005). Intracytoplasmic injection of spermatozoa and spermatogenic cells: Its biology and applications in humans and animals. Reproductive Biomedicine Online, 10(2), 247–288. doi: 10.1016/S1472-6483(10)60947-9 CrossRefGoogle Scholar
Yang, X., Presicce, G. A., Moraghan, L., Jiang, S. E. and Foote, R. H. (1994). Synergistic effect of ethanol and cycloheximide on activation of freshly matured bovine oocytes. Theriogenology, 41(2), 395–403. doi: 10.1016/0093-691x(94)90075-t CrossRefGoogle ScholarPubMed
Yeste, M., Jones, C., Amdani, S. N. and Coward, K. (2019). Oocyte activation deficiency and advances to overcome. In Nagy, Z., Varghese, A. and Agarwal, A. (eds), In vitro fertilization (2nd edn), 1 (pp. 429–445). Springer, Cham. doi: 10.1007/978-3-319-43011-9_34 CrossRefGoogle Scholar
Yoshimoto, H., Takeo, T., Irie, T. and Nakagata, N. (2017). Fertility of cold-stored mouse sperm is recovered by promoting acrosome reaction and hyperactivation after cholesterol efflux by methyl-beta-cyclodextrin. Biology of Reproduction, 96(2), 446–455. doi: 10.1095/biolreprod.116.142901 CrossRefGoogle ScholarPubMed
Zambrano, F., Águila, L., Arias, M. E., Sánchez, R. and Felmer, R. (2016). Improved preimplantation development of bovine ICSI embryos generated with spermatozoa pretreated with membrane-destabilizing agents lysolecithin and Triton X-100. Theriogenology, 86(6), 1489–1497. doi: 10.1016/j.theriogenology.2016.05.007 CrossRefGoogle ScholarPubMed
Zambrano, F., Águila, L., Arias, M. E., Sánchez, R. and Felmer, R. (2017). Effect of sperm pretreatment with glutathione and membrane destabilizing agents lysolecithin and Triton X-100, on the efficiency of bovine intracytoplasmic sperm injection. Reproduction in Domestic Animals, 52(2), 305–311. doi: 10.1111/rda.12906 CrossRefGoogle ScholarPubMed
Zander-Fox, D., Lam, K., Pacella-Ince, L., Tully, C., Hamilton, H., Hiraoka, K., McPherson, N. O. and Tremellen, K. (2021). PIEZO-ICSI increases fertilization rates compared with standard ICSI: a prospective cohort study. Reproductive Biomedicine Online, 43(3), 404–412. doi: 10.1016/j.rbmo.2021.05.020 CrossRefGoogle ScholarPubMed
Zhang, D., Pan, L., Yang, L. H., He, X. K., Huang, X. Y. and Sun, F. Z. (2005). Strontium promotes calcium oscillations in mouse meiotic oocytes and early embryos through InsP3 receptors, and requires activation of phospholipase and the synergistic action of InsP3 . Human Reproduction, 20(11), 3053–3061. doi: 10.1093/humrep/dei215 CrossRefGoogle ScholarPubMed
Zhao, X. M., Wang, N., Hao, H. S., Li, C. Y., Zhao, Y. H., Yan, C. L., Wang, H. Y., Du, W. H., Wang, D., Liu, Y., Pang, Y. W. and Zhu, H. B. (2018). Melatonin improves the fertilization capacity and developmental ability of bovine oocytes by regulating cytoplasmic maturation events. Journal of Pineal Research, 64(1), e12445. doi: 10.1111/jpi.12445 CrossRefGoogle ScholarPubMed
Zhou, W. J., Huang, C., Jiang, S. H., Ji, X. R., Gong, F., Fan, L. Q. and Zhu, W. B. (2021). Influence of sperm morphology on pregnancy outcome and offspring in in vitro fertilization and intracytoplasmic sperm injection: A matched case-control study. Asian Journal of Andrology, 23(4), 421–428. doi: 10.4103/aja.aja_91_20 CrossRefGoogle ScholarPubMed
Zhu, J., Cui, W. and Dai, Y. F. (2018). Production of inbred offspring by intracytoplasmic sperm injection of oocytes from juvenile female mice. Reproduction, Fertility, and Development, 30(3), 451–458. doi: 10.1071/RD16399 CrossRefGoogle ScholarPubMed