Preimplantation Developmental Competence of Bovine and Porcine Oocytes Activated by Zinc Chelation

Overview

Journal Animals (Basel)

Date 2022 Dec 23

PMID 36552480

Authors

Juan P Cabeza

Juan Camera

Olinda Briski

Minerva Yauri Felipe

Daniel F Salamone

Andres Gambini

Affiliations

Soon will be listed here.

Abstract

After sperm-oocyte fusion, intracytoplasmic rises of calcium (Ca) induce the release of zinc (Zn) out of the oocyte (Zn sparks). Both phenomena are known to play an essential role in the oocyte activation process. Our work aimed to explore different protocols for activating bovine and porcine oocytes using the novel zinc chelator 1,10-phenanthroline (PHEN) and to compare developmental rates and quality to bovine IVF and parthenogenetic ionomycin-induced embryos in both species. Different incubation conditions for the zinc chelator were tested, including its combination with ionomycin. Embryo quality was assessed by immunofluorescence of SOX2, SOX17, OCT4, and CDX2 and total cell number at the blastocyst stage. Even though blastocyst development was achieved using a zinc chelator in bovine, bypassing calcium oscillations, developmental rates, and blastocyst quality were compromised compared to embryos generated with sperm-induced or ionomycin calcium rise. On the contrary, zinc chelation is sufficient to trigger oocyte activation in porcine. Additionally, we determined the optimal exposure to PHEN for this species. Zinc chelation and artificial induction of calcium rise combined did not improve developmental competence. Our results contribute to understanding the role of zinc during oocyte activation and preimplantation embryo development across different mammalian species.

Citing Articles

Selection and Conservation of Gametes and Embryos for Improving Assisted Reproductive Technologies.

Gambini A, Ortiz I, Hidalgo M, Dorado J Animals (Basel). 2023; 13(17).

PMID: 37685025 PMC: 10486582. DOI: 10.3390/ani13172761.

References

Telford W, Fraker P . Preferential induction of apoptosis in mouse CD4+CD8+ alpha beta TCRloCD3 epsilon lo thymocytes by zinc. J Cell Physiol. 1995; 164(2):259-70. DOI: 10.1002/jcp.1041640206. View

Ciapa B, Arnoult C . Could modifications of signalling pathways activated after ICSI induce a potential risk of epigenetic defects?. Int J Dev Biol. 2011; 55(2):143-52. DOI: 10.1387/ijdb.103122bc. View

Kong B, Duncan F, Que E, Xu Y, Vogt S, OHalloran T . The inorganic anatomy of the mammalian preimplantation embryo and the requirement of zinc during the first mitotic divisions. Dev Dyn. 2015; 244(8):935-47. PMC: 4617753. DOI: 10.1002/dvdy.24285. View

Jeon Y, Yoon J, Cai L, Hwang S, Kim E, Lee E . Effect of zinc on in vitro development of porcine embryos. Theriogenology. 2015; 84(4):531-7. DOI: 10.1016/j.theriogenology.2015.04.006. View

Duncan F, Que E, Zhang N, Feinberg E, OHalloran T, Woodruff T . The zinc spark is an inorganic signature of human egg activation. Sci Rep. 2016; 6:24737. PMC: 4845039. DOI: 10.1038/srep24737. View

Briski O, Salamone D . Past, present and future of ICSI in livestock species. Anim Reprod Sci. 2022; 246:106925. DOI: 10.1016/j.anireprosci.2022.106925. View

Garner T, Hester J, Carothers A, Diaz F . Role of zinc in female reproduction. Biol Reprod. 2021; 104(5):976-994. PMC: 8599883. DOI: 10.1093/biolre/ioab023. View

Ozil J, Banrezes B, Toth S, Pan H, Schultz R . Ca2+ oscillatory pattern in fertilized mouse eggs affects gene expression and development to term. Dev Biol. 2006; 300(2):534-44. DOI: 10.1016/j.ydbio.2006.08.041. View

Brackett B, Oliphant G . Capacitation of rabbit spermatozoa in vitro. Biol Reprod. 1975; 12(2):260-74. DOI: 10.1095/biolreprod12.2.260. View

10.

Suva M, Canel N, Salamone D . Effect of single and combined treatments with MPF or MAPK inhibitors on parthenogenetic haploid activation of bovine oocytes. Reprod Biol. 2019; 19(4):386-393. DOI: 10.1016/j.repbio.2019.09.001. View

11.

Kim A, Bernhardt M, Kong B, Ahn R, Vogt S, Woodruff T . Zinc sparks are triggered by fertilization and facilitate cell cycle resumption in mammalian eggs. ACS Chem Biol. 2011; 6(7):716-23. PMC: 3171139. DOI: 10.1021/cb200084y. View

12.

Lee K, Davis A, Zhang L, Ryu J, Spate L, Park K . Pig oocyte activation using a Zn²⁺ chelator, TPEN. Theriogenology. 2015; 84(6):1024-32. PMC: 4553067. DOI: 10.1016/j.theriogenology.2015.05.036. View

13.

Nasr-Esfahani M, Deemeh M, Tavalaee M . Artificial oocyte activation and intracytoplasmic sperm injection. Fertil Steril. 2009; 94(2):520-6. DOI: 10.1016/j.fertnstert.2009.03.061. View

14.

Kambe T, Yamaguchi-Iwai Y, Sasaki R, Nagao M . Overview of mammalian zinc transporters. Cell Mol Life Sci. 2004; 61(1):49-68. PMC: 11138893. DOI: 10.1007/s00018-003-3148-y. View

15.

Tao Y . Oocyte activation during round spermatid injection: state of the art. Reprod Biomed Online. 2022; 45(2):211-218. DOI: 10.1016/j.rbmo.2022.03.024. View

16.

Tokuhiro K, Dean J . Glycan-Independent Gamete Recognition Triggers Egg Zinc Sparks and ZP2 Cleavage to Prevent Polyspermy. Dev Cell. 2018; 46(5):627-640.e5. PMC: 6549238. DOI: 10.1016/j.devcel.2018.07.020. View

17.

Stein P, Savy V, Williams A, Williams C . Modulators of calcium signalling at fertilization. Open Biol. 2020; 10(7):200118. PMC: 7574550. DOI: 10.1098/rsob.200118. View

18.

Kim A, Vogt S, OHalloran T, Woodruff T . Zinc availability regulates exit from meiosis in maturing mammalian oocytes. Nat Chem Biol. 2010; 6(9):674-81. PMC: 2924620. DOI: 10.1038/nchembio.419. View

19.

Lopez-Saucedo J, Paramio-Nieto M, Fierro R, Pina-Aguilar R . Intracytoplasmic sperm injection (ICSI) in small ruminants. Anim Reprod Sci. 2012; 133(3-4):129-38. DOI: 10.1016/j.anireprosci.2012.07.003. View

20.

Savy V, Stein P, Shi M, Williams C . PMCA1 depletion in mouse eggs amplifies calcium signaling and impacts offspring growth†. Biol Reprod. 2022; 107(6):1439-1451. PMC: 10144700. DOI: 10.1093/biolre/ioac180. View