One Carbon Metabolism Supplementation in Maturation Medium but Not Embryo Culture Medium Improves the Yield of Blastocysts from Bovine Oocytes

Overview

Journal Sci Rep

Date 2025 Jan 21

PMID 39837964

Authors

Arefeh Golestanfar

Amir Niasari Naslaji

Farnoosh Jafarpour

Nima Sadeghi Borujen

Shiva Rouhollahi Varnosfaderani

Yves Menezo

Maurizio Dattilo

Mohammad Hossein Nasr-Esfahani

Affiliations

Soon will be listed here.

Abstract

Optimizing oocyte maturation and embryo culture media could enhance in vitro embryo production. The purpose of the present study was to investigate the role of supplementing one carbon metabolism (OCM) substrates and its cofactors (Cystine, Zinc, Betaine, B2, B3, B6, B12 and 5-methyltetrahydrofolate) in maturation and/or embryo culture media on the rate of blastocyst formation and pregnancy outcomes following the transfer of the resulting blastocysts in bovines. In the first experiment, 2537 bovine oocytes were recovered from slaughterhouse ovaries and then matured either in conventional maturation medium (IVM) or IVM supplemented with OCM substrates (Sup-IVM). After in vitro fertilization, the putative zygotes from each treatment (IVM or Sup-IVM) were cultured in the media either without (IVM/IVC or Sup-IVM/IVC) or with (IVM/Sup-IVC or Sup-IVM/Sup-IVC) OCM supplementation. The blastocyst rate, assessed on day 8, was significantly increased in Sup-IVM/IVC group (34.90 ± 2.52) as compared to IVM/IVC (17.06 ± 1.69; P = 0.0001) and Sup-IVM/Sup-IVC (20.29 ± 2.75; P = 0.004) and non-significantly as compared to IVM/Sup-IVC (24.86 ± 5.37). In the second experiment, non-matured bovine oocytes were collected by transvaginal ovum pick up after FSH stimulation, randomly allocated into IVM/IVC (n = 275) and Sup-IVM/IVC (n = 260) and the blastocysts achieved at day 7 were transferred in recipient cattle. The blastocyst rate was significantly higher in Sup-IVM/IVC group (38.85%) as compared to the IVM/IVC group (23.64%; P < 0.0001). After single embryo transfer, the supplemented blastocysts were at least as competent as non-supplemented ones with a non-significantly higher (20% vs. 14%) pregnancy rate and the advantage of several good quality blastocysts available for future use. In conclusion, optimizing the maturation medium with OCM substrates and its cofactors could enhance the formation of viable blastocysts with the potential to increase the cumulative birth rate in cattle.

References

Li L, Zhu S, Shu W, Guo Y, Guan Y, Zeng J . Characterization of Metabolic Patterns in Mouse Oocytes during Meiotic Maturation. Mol Cell. 2020; 80(3):525-540.e9. PMC: 8034554. DOI: 10.1016/j.molcel.2020.09.022. View

Teng Y, Mehedint M, Garrow T, Zeisel S . Deletion of betaine-homocysteine S-methyltransferase in mice perturbs choline and 1-carbon metabolism, resulting in fatty liver and hepatocellular carcinomas. J Biol Chem. 2011; 286(42):36258-67. PMC: 3196139. DOI: 10.1074/jbc.M111.265348. View

Nicodemo D, Pauciullo A, Cosenza G, Peretti V, Perucatti A, Di Meo G . Frequency of aneuploidy in in vitro-matured MII oocytes and corresponding first polar bodies in two dairy cattle (Bos taurus) breeds as determined by dual-color fluorescent in situ hybridization. Theriogenology. 2009; 73(4):523-9. DOI: 10.1016/j.theriogenology.2009.10.007. View

Eckersley-Maslin M, Alda-Catalinas C, Reik W . Dynamics of the epigenetic landscape during the maternal-to-zygotic transition. Nat Rev Mol Cell Biol. 2018; 19(7):436-450. DOI: 10.1038/s41580-018-0008-z. View

Gregory J, DeRatt B, Rios-Avila L, Ralat M, Stacpoole P . Vitamin B6 nutritional status and cellular availability of pyridoxal 5'-phosphate govern the function of the transsulfuration pathway's canonical reactions and hydrogen sulfide production via side reactions. Biochimie. 2016; 126:21-6. PMC: 4899128. DOI: 10.1016/j.biochi.2015.12.020. View

Hosseini S, Moulavi F, Nasr-Esfahani M . A Novel Method of Somatic Cell Nuclear Transfer with Minimum Equipment. Methods Mol Biol. 2015; 1330:169-88. DOI: 10.1007/978-1-4939-2848-4_15. View

Son W, Lee S, Lim J . Fertilization, cleavage and blastocyst development according to the maturation timing of oocytes in in vitro maturation cycles. Hum Reprod. 2005; 20(11):3204-7. DOI: 10.1093/humrep/dei195. View

Wang L, Xiong X, Zhang H, Li Y, Li Q, Wang Y . Defined media optimization for in vitro culture of bovine somatic cell nuclear transfer (SCNT) embryos. Theriogenology. 2012; 78(9):2110-9. DOI: 10.1016/j.theriogenology.2012.03.011. View

Lindner G, Wright Jr R . Bovine embryo morphology and evaluation. Theriogenology. 1983; 20(4):407-16. DOI: 10.1016/0093-691x(83)90201-7. View

10.

Pfeffer P . Building Principles for Constructing a Mammalian Blastocyst Embryo. Biology (Basel). 2018; 7(3). PMC: 6164496. DOI: 10.3390/biology7030041. View

11.

Kucuk T, Horozal P, Karakulak A, Timucin E, Dattilo M . Follicular homocysteine as a marker of oocyte quality in PCOS and the role of micronutrients. J Assist Reprod Genet. 2023; 40(8):1933-1941. PMC: 10371946. DOI: 10.1007/s10815-023-02847-3. View

12.

Zhang D, Jing H, Dou C, Zhang L, Wu X, Wu Q . Supplement of Betaine into Embryo Culture Medium Can Rescue Injury Effect of Ethanol on Mouse Embryo Development. Sci Rep. 2018; 8(1):1761. PMC: 5789050. DOI: 10.1038/s41598-018-20175-w. View

13.

Clare C, Pestinger V, Kwong W, Tutt D, Xu J, Byrne H . Interspecific Variation in One-Carbon Metabolism within the Ovarian Follicle, Oocyte, and Preimplantation Embryo: Consequences for Epigenetic Programming of DNA Methylation. Int J Mol Sci. 2021; 22(4). PMC: 7918761. DOI: 10.3390/ijms22041838. View

14.

Rushworth G, Megson I . Existing and potential therapeutic uses for N-acetylcysteine: the need for conversion to intracellular glutathione for antioxidant benefits. Pharmacol Ther. 2013; 141(2):150-9. DOI: 10.1016/j.pharmthera.2013.09.006. View

15.

Messerschmidt D, Knowles B, Solter D . DNA methylation dynamics during epigenetic reprogramming in the germline and preimplantation embryos. Genes Dev. 2014; 28(8):812-28. PMC: 4003274. DOI: 10.1101/gad.234294.113. View

16.

Zamudio N, Barau J, Teissandier A, Walter M, Borsos M, Servant N . DNA methylation restrains transposons from adopting a chromatin signature permissive for meiotic recombination. Genes Dev. 2015; 29(12):1256-70. PMC: 4495397. DOI: 10.1101/gad.257840.114. View

17.

Ereno-Orbea J, Majtan T, Oyenarte I, Kraus J, Martinez-Cruz L . Structural insight into the molecular mechanism of allosteric activation of human cystathionine β-synthase by S-adenosylmethionine. Proc Natl Acad Sci U S A. 2014; 111(37):E3845-52. PMC: 4169959. DOI: 10.1073/pnas.1414545111. View

18.

Hosseini S, Dufort I, Nieminen J, Moulavi F, Ghanaei H, Hajian M . Epigenetic modification with trichostatin A does not correct specific errors of somatic cell nuclear transfer at the transcriptomic level; highlighting the non-random nature of oocyte-mediated reprogramming errors. BMC Genomics. 2016; 17:16. PMC: 4698792. DOI: 10.1186/s12864-015-2264-z. View

19.

Xiao W, Loscalzo J . Metabolic Responses to Reductive Stress. Antioxid Redox Signal. 2019; 32(18):1330-1347. PMC: 7247050. DOI: 10.1089/ars.2019.7803. View

20.

Yusuf A, Abubakar M, Malami I, Ibrahim K, Abubakar B, Bello M . Zinc Metalloproteins in Epigenetics and Their Crosstalk. Life (Basel). 2021; 11(3). PMC: 7996840. DOI: 10.3390/life11030186. View