Key Glycometabolism During Oocyte Maturation and Early Embryonic Development

Overview

Journal Reproduction

Date 2025 Jan 23

PMID 39846956

Authors

Yichuan Zhang

Tianjie Li

Yibo Wang

Yang Yu

Affiliations

Soon will be listed here.

Abstract

In Brief: Glucose metabolism is central to the successful progression from oocyte maturation to blastocyst formation, influencing not only energy production but also key developmental decisions and epigenetic regulation. This review uncovers the intricate interplay between glucose, fatty acids, amino acids and nucleotides, highlighting their crucial roles in early embryonic development and exploring how noninvasive metabolic monitoring can revolutionize embryo selection and personalized assisted reproductive technologies, offering new hope for fertility treatments.

Abstract: In recent decades, it has become increasingly clear that mammalian gametes and early embryos are highly sensitive to metabolic substrates. With advances in single-cell sequencing, metabolomics and bioinformatics, we now recognize that metabolic pathways not only meet cellular energy demands but also play a critical role in cell proliferation, differentiation and fate determination. Investigating metabolic processes during oocyte maturation and early embryonic development is thus essential to advancing reproductive medicine and embryology. This review highlights the intricate metabolic pathways, particularly glucose metabolism, that drive the transition from an oocyte to an embryo. These processes involve a complex interaction of signaling pathways, nutrient availability and environmental factors, with glucose metabolism not only providing essential energy but also offering a variety of metabolic substrates and intermediates that regulate developmental events, influence cell signaling and impact epigenetic modifications. This article emphasizes that future research will focus on regulating maternal metabolic environments and noninvasive metabolic monitoring of embryonic systems, particularly glucose metabolism, with promising opportunities to improve embryo selection and personalized assisted reproductive technologies, ultimately enhancing fertility treatment outcomes.

References

Rayon T, Menchero S, Nieto A, Xenopoulos P, Crespo M, Cockburn K . Notch and hippo converge on Cdx2 to specify the trophectoderm lineage in the mouse blastocyst. Dev Cell. 2014; 30(4):410-22. PMC: 4146744. DOI: 10.1016/j.devcel.2014.06.019. View

Zhang L, Zhao J, Lam S, Chen L, Gao Y, Wang W . Low-input lipidomics reveals lipid metabolism remodelling during early mammalian embryo development. Nat Cell Biol. 2024; 26(2):278-293. DOI: 10.1038/s41556-023-01341-3. View

Sharpley M, Chi F, Hoeve J, Banerjee U . Metabolic plasticity drives development during mammalian embryogenesis. Dev Cell. 2021; 56(16):2329-2347.e6. PMC: 8584261. DOI: 10.1016/j.devcel.2021.07.020. View

Augustin R, Pocar P, Navarrete-Santos A, Wrenzycki C, Gandolfi F, Niemann H . Glucose transporter expression is developmentally regulated in in vitro derived bovine preimplantation embryos. Mol Reprod Dev. 2001; 60(3):370-6. DOI: 10.1002/mrd.1099. View

Tan T, Brown H, Thompson J, Mustafa S, Dunning K . Optical imaging detects metabolic signatures associated with oocyte quality†. Biol Reprod. 2022; 107(4):1014-1025. PMC: 9562116. DOI: 10.1093/biolre/ioac145. View

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

Cao Z, Carey T, Ganguly A, Wilson C, Paul S, Knott J . Transcription factor AP-2γ induces early Cdx2 expression and represses HIPPO signaling to specify the trophectoderm lineage. Development. 2015; 142(9):1606-15. PMC: 4419278. DOI: 10.1242/dev.120238. View

de Souza D, Salles L, Rosa e Silva A . Aspects of energetic substrate metabolism of in vitro and in vivo bovine embryos. Braz J Med Biol Res. 2015; 48(3):191-7. PMC: 4381938. DOI: 10.1590/1414-431X20143744. View

Zhang S, Zeng X, Ren M, Mao X, Qiao S . Novel metabolic and physiological functions of branched chain amino acids: a review. J Anim Sci Biotechnol. 2017; 8:10. PMC: 5260006. DOI: 10.1186/s40104-016-0139-z. View

10.

Martinez-Vizcaino V, Sanabria-Martinez G, Fernandez-Rodriguez R, Cavero-Redondo I, Pascual-Morena C, Alvarez-Bueno C . Exercise during pregnancy for preventing gestational diabetes mellitus and hypertensive disorders: An umbrella review of randomised controlled trials and an updated meta-analysis. BJOG. 2022; 130(3):264-275. PMC: 10092296. DOI: 10.1111/1471-0528.17304. View

11.

Wang M, Xue J, Li C, Qi L, Nie L, Xue Z . Glucose promoting the early embryonic development by increasing the lipid synthesis at 2-cell stage. Front Cell Dev Biol. 2023; 11:1208501. PMC: 10392834. DOI: 10.3389/fcell.2023.1208501. View

12.

Yang Z, Feng G, Gao X, Yan X, Li Y, Wang Y . Maternal adiposity and perinatal and offspring outcomes: an umbrella review. Nat Hum Behav. 2024; 8(12):2406-2422. DOI: 10.1038/s41562-024-01994-6. View

13.

Sun H, Zhang Z, Li T, Li T, Chen W, Pan T . Live-cell imaging reveals redox metabolic reprogramming during zygotic genome activation. J Cell Physiol. 2023; 238(9):2039-2049. DOI: 10.1002/jcp.31054. View

14.

Seli E, Sakkas D, Scott R, Kwok S, Rosendahl S, Burns D . Noninvasive metabolomic profiling of embryo culture media using Raman and near-infrared spectroscopy correlates with reproductive potential of embryos in women undergoing in vitro fertilization. Fertil Steril. 2007; 88(5):1350-7. DOI: 10.1016/j.fertnstert.2007.07.1390. View

15.

Sfakianoudis K, Maziotis E, Karantzali E, Kokkini G, Grigoriadis S, Pantou A . Molecular Drivers of Developmental Arrest in the Human Preimplantation Embryo: A Systematic Review and Critical Analysis Leading to Mapping Future Research. Int J Mol Sci. 2021; 22(15). PMC: 8347543. DOI: 10.3390/ijms22158353. View

16.

Minge C, Bennett B, Norman R, Robker R . Peroxisome proliferator-activated receptor-gamma agonist rosiglitazone reverses the adverse effects of diet-induced obesity on oocyte quality. Endocrinology. 2008; 149(5):2646-56. DOI: 10.1210/en.2007-1570. View

17.

Harris S, Gopichandran N, Picton H, Leese H, Orsi N . Nutrient concentrations in murine follicular fluid and the female reproductive tract. Theriogenology. 2005; 64(4):992-1006. DOI: 10.1016/j.theriogenology.2005.01.004. View

18.

Zhang H, Yan K, Sui L, Li P, Du Y, Hu J . Low-level pyruvate inhibits early embryonic development and maternal mRNA clearance in mice. Theriogenology. 2021; 166:104-111. DOI: 10.1016/j.theriogenology.2021.02.022. View

19.

Lane M, Gardner D . Lactate regulates pyruvate uptake and metabolism in the preimplantation mouse embryo. Biol Reprod. 1999; 62(1):16-22. DOI: 10.1095/biolreprod62.1.16. View

20.

Gardner D, Wale P . Analysis of metabolism to select viable human embryos for transfer. Fertil Steril. 2013; 99(4):1062-72. DOI: 10.1016/j.fertnstert.2012.12.004. View