Dysregulation of glycosaminoglycans during oocyte maturation in vitro: implications for developmental potential

A complex extracellular matrix (ECM) assembles around the mammalian oocyte during maturation and ovulation, comprising hyaluronan as well as proteoglycans. These proteoglycans are hypothesised to carry heparan and chondroitin sulfate side chains. This matrix is essential for ovulation, mediates signalling, and regulates solute diffusion to control the oocyte environment. In vivo, ECM formation is initiated by epidermal growth factor-like peptides released within the follicle, acting together with oocyte-derived growth factors. Although proteoglycans are known components, the specific glycosaminoglycan (GAG) composition remains poorly understood. Here, we characterised GAG abundance in murine cumulus-oocyte-complexes and assessed differences between in vivo and in vitro maturation. The latter is an assisted reproductive technology that requires less drugs than IVF, but oocytes have reduced developmental potential. We found that sulfated GAG abundance increased significantly in vivo but not during in vitro oocyte maturation. We also employed high performance liquid-chromatography to measure the abundance of specific GAGs-hyaluronan, chondroitin sulfate, and heparan sulfate-in this matrix at different stages of maturation. These were enriched within the ECM during in vivo maturation but reduced or undetectable in vitro. Reduced GAG abundance following in vitro maturation was associated with poorer oocyte developmental potential. GAG deficiency following in vitro maturation likely arises from the failure of in vitro conditions to replicate the signalling milieu that occurs in vivo. Altered GAG abundance during in vitro maturation may impair functions of the ECM, including growth factor binding and activity or the regulated diffusion of solutes, potentially contributing to decreased oocyte developmental potential.