Document Type : Original Article

Authors

1 Department of Theriogenology, Faculty of Veterinary Sciences, University of Veterinary and Animal Sciences, Lahore, Pakistan

2 Institute of Molecular Biology and Biotechnology, University of Lahore, Lahore, Pakistan

3 Department of Theriogenology, University of Veterinary and Animal Sciences, Lahore, Pakistan

4 Department of Physics, Faculty of Natural Sciences, University of Engineering and Technology, Lahore, Pakistan

Abstract

Currently, artificial oocyte activation has attracted wide attention in assisted reproduction due to extensive range of applications, particularly in somatic cell nuclear transfer and deriving pluripotent stem cell lines and it is the unique model to determine the role of paternal genome. Numbers of artificial activating agents have been used extensively to induce the oocytes activation; however, embryos developmental competency of artificially activated oocytes is still very low. In the present study, we determined the functional impact of strontium chloride supplementation with gold nanoparticles (AuNPs) in artificial oocytes activation and subsequent embryonic development. Oocytes were activated artificially in the culture medium containing 250 nM AuNPs with constant concentration of strontium chloride 10.00 mM. We found that adding 250 nM AuNPs with constant concentration of strontium chloride (10.00 mM for 3 hr) in culture medium improves the proportion of embryos reaching to the morula and blastocyst stages from 61.00% and 42.00% (controls) to 75.00% and 58.00% (250 nM AuNPs), respectively. In addition, foster mothers receiving AuNPs-treated embryos showed more implantation percentage and pregnancy rate relative to females received control embryos. Finally, embryos treated with 250 nM AuNPs concentration showed no toxic effect in term of blastocyst development. Collectively, our findings suggest the potential role of AuNPs in early embryonic development for mouse oocytes activated artificially and provide new insights in the field of animal biotechnology and assisted reproduction in humans.

Keywords

  1. Ju JY, Park CY, Gupta MK, et al. Establishment of stem cell lines from nuclear transferred and partheno-genetically activated mouse oocytes for therapeutic cloning. Fertil Steril 2008; 89(5 Suppl): 1314-1323.
  2. Campbell KH. Nuclear equivalence, nuclear transfer, and the cell cycle. Cloning 1999; 1(1): 3-15.
  3. Kishikawa H, Wakayama T, Yanagimachi R. Comparison of oocyte-activating agents for mouse cloning. Cloning 1999; 1(3): 153-159.
  4. Miyazaki S, Shirakawa H, Nakada K, et al. Essential role of the inositol 1, 4, 5-trisphosphate receptor/Ca2+ release channel in Ca 2+ waves and Ca 2+ oscillations at fertilization of mammalian eggs. Dev Biol 1993; 158(1): 62-78.
  5. Ducibella T, Huneau D, Angelichio E, et al. Egg-to-embryo transition is driven by differential responses to Ca (2+) oscillation number. Dev Biol 2002; 250(2): 280-291.
  6. Zhang D, Pan L, Yang L-H, et al. 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. Hum Reprod 2005; 20(11): 3053-3061.
  7. Bos-Mikich A, Swann K, Whittingham DG. Calcium oscillations and protein synthesis inhibition synergistically activate mouse oocytes. Mol Reprod Dev 1995; 41(1): 84-90.
  8. Che L, Lalonde A, Bordignon V. Chemical activation of parthenogenetic and nuclear ‎transfer porcine oocytes using ionomycin and strontium chloride. Theriogenology 2007; 67(7): 1297-1304.
  9. Varga E, Pataki R, Lorincz Z, et al. Parthenogenetic development of in vitro matured porcine oocytes treated with chemical agents. Anim Reprod Sci 2008; 105(3-4): 226-233.
  10. Boisselier E, Astruc D. Gold nanoparticles in nanomedicine: preparations, imaging, diagnostics, therapies and toxicity. Chem Soc Rev 2009; 38(6): 1759-1782.
  11. Duncan B, Kim C, Rotello VM. Gold nanoparticle platforms as drug and biomacromolecule delivery systems. J Control Release 2010; 148(1): 122-127.
  12. Hashmi ASK, Hutchings GJ. Gold catalysis. Angew Chem Int Ed 2006; 45(47): 7896-7936.
  13. Mills G, Gordon MS, Metiu H. Oxygen adsorption on Au clusters and a rough Au(111) surface: The role of surface flatness, electron confinement, excess electrons, and band gap. J Chem Phys 2003; 118(9): 4198-4205.
  14. Bond GC, Thompson DT. Gold-catalysed oxidation of carbon monoxide. Gold Bull 2000; 33(2): 41-50.
  15. Comotti M, Della Pina C, Matarrese R, et al. The catalytic activity of “naked” gold particles. Angew Chem Int Ed 2004; 43(43): 5812-5815.
  16. De Jong WH, Hagens WI, Krystek P, et al. Particle size-dependent organ distribution of gold nanoparticles after intravenous administration. Biomaterials 2008; 29(12): 1912-1919.
  17. Browning LM, Lee KJ, Huang T, et al. Random walk of single gold nanoparticles in zebrafish embryos leading to stochastic toxic effects on embryonic developments. Nanoscale 2009; 1(1): 138-152.
  18. Jamal MA, Ahmed AM, Tahir M, et al. Safety and efficacy of ketamine xylazine along with atropine anesthesia in BALB/c mice. Braz J Pharm Sci 2019; 55:e17231. doi:10.1590/s2175-97902019000317231.
  19. Kroemer G, El-Deiry WS, Golstein P, et al. Classification of cell death: recommendations of the nomenclature committee on cell death. Cell Death Differ 2005; 12(Suppl 2): 1463-1467.
  20. Tomashov-Matar R, Tchetchik D, Eldar A, et al. Strontium-induced rat egg activation. Reproduction 2005; 130(4): 467-474.
  21. Ozil JP, Huneau D. Activation of rabbit oocytes: the impact of the Ca2+ signal regime on development. Development 2001; 128(6): 917-928.
  22. Méo SC, Leal CLV, Garcia JM. Activation and early parthenogenesis of bovine oocytes treated with ethanol and strontium. Anim Reprod Sci 2004; 81(1-2): 35-46.
  23. Hao YH, Lai LX, Liu ZH, et al. Developmental competence of porcine parthenogenetic embryos relative to embryonic chromosomal abnormalities. Mol Reprod Dev 2006; 73(1): 77-82.
  24. Versieren K, Heindryckx B, Lierman S, et al. Developmental competence of parthenogenetic mouse and human embryos after chemical or electrical activation. Reprod Biomed Online 2010; 21(6): 769-775.
  25. Heytens E, Soleimani R, Lierman S, et al. Effect of ionomycin on oocyte activation and embryo development in mouse. Reprod Biomed Online 2008; 17(6): 764-771.
  26. Loren J, Lacham-Kaplan O. The employment of strontium to activate mouse oocytes: effects on spermatid-injection outcome. Reproduction 2006; 131(2): 259-267.
  27. Han BS, Gao JL. Effects of chemical combinations on the parthenogenetic activation of mouse oocytes. Exp Ther Med 2013; 5(5): 1281-1288.
  28. Ozil JP, Banrezes B, Tóth S, et al. Ca 2+ oscillatory pattern in fertilized mouse eggs affects gene expression and development to term. Dev Biol 2006; 300(2): 534-544.
  29. Farooq MU, Novosad V, Rozhkova EA, et al. Gold nanoparticles-enabled efficient dual delivery of anticancer therapeutics to HeLa cells. Sci Rep 2018; 8(1): 2907. doi: 10.1038/s41598-018-21331-y.
  30. Kong FY, Zhang JW, Li RF, et al. Unique roles of gold nanoparticles in drug delivery, targeting and imaging applications. Molecules 2017; 22(9): 1445. doi: 10.3390/molecules22091445.
  31. Jin Z, Li R, Zhou C, et al. Efficient gene knockdown in mouse oocytes through peptide nanoparticle-mediated SiRNA transfection. PloS One 2016; 11(3): e0150462. doi:10.1371/journal.pone.0150462.
  32. Li R, Jin Z, Gao L, et al. Effective protein inhibition in intact mouse oocytes through peptide nanoparticle-mediated antibody transfection. Peer J 2016; 4:e1849. doi: 10.7717/peerj.1849.
  33. Heddle JG. Gold nanoparticle-biological molecule inter-actions and catalysis. Catalysts 2013; 3(3): 683-708.
  34. Asharani PV, Lianwu Y, Gong Z, et al. Comparison of the toxicity of silver, gold and platinum nanoparticles in developing zebrafish embryos. Nanotoxicology 2011; 5(1): 43-54.
  35. Pineda L, Sawosz E, Hotowy A, et al. Effect of nanoparticles of silver and gold on metabolic rate and development of broiler and layer embryos. Comp Biochem Phyiol A Mol Integr Physiol 2012; 161(3): 315-319.
  36. Yanagimachi R. Intracytoplasmic injection of spermatozoa and spermatogenic cells: its biology and applications in humans and animals. Reprod Biomed online 2005; 10(2): 247-288.
  37. Nasr-Esfahani MH, Deemeh MR, Tavalaee M. Artificial oocyte activation and intracytoplasmic sperm injection. Fertil Steril 2010; 94(2): 520-526.