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Glucosamine Supplementation During In Vitro Maturation Inhibits Subsequent Embryo Development: Possible Role of the Hexosamine Pathway as a Regulator of Developmental Competence¹

Research Centre for Reproductive Health,³ Department of Obstetrics and Gynaecology, The University of Adelaide, The Queen Elizabeth Hospital, Woodville, South Australia 5011, Australia Area of Biochemistry,⁴ School of Veterinary Sciences, University of Buenos Aires, C1427CWO Buenos Aires, Argentina Department of Physiology and Pharmacology,⁵ School of Biomedical Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia

ABSTRACT

Glucose concentration during cumulus-oocyte complex (COC) maturation influences several functions, including progression of oocyte meiosis, oocyte developmental competence, and cumulus mucification. Glucosamine (GlcN) is an alternative hexose substrate, specifically metabolized through the hexosamine biosynthesis pathway, which provides the intermediates for extracellular matrix formation during cumulus cell mucification. The aim of this study was to determine the influence of GlcN on meiotic progression and oocyte developmental competence following in vitro maturation (IVM). The presence of GlcN during bovine IVM did not affect the completion of nuclear maturation and early cleavage, but severely perturbed blastocyst development. This effect was subsequently shown to be dose-dependent and was also observed for porcine oocytes matured in vitro. Hexosamine biosynthesis upregulation using GlcN supplementation is well known to increase O-linked glycosylation of many intracellular signaling molecules, the best-characterized being the phosphoinositol-3-kinase (PI3K) signaling pathway. We observed extensive O-linked glycosylation in bovine cumulus cells, but not oocytes, following IVM in either the presence or the absence of GlcN. Inhibition of O-linked glycosylation significantly reversed the effect of GlcN-induced reduction in developmental competence, but inhibition of PI3K signaling had no effect. Our data are the first to link hexosamine biosynthesis, involved in cumulus cell mucification, to oocyte developmental competence during in vitro maturation.

cumulus, cumulus cells, embryo, early development, glucose, glucosamine, hexosamine, oocyte, oocyte development

¹ Supported by an Australia Research Council (SPIRT, C00107702 to M.S.-M.) and Cook Australia Pty Ltd (to M.S.-M.) and partially supported as part of the NICHD National Cooperative Program on Female Health and Egg Quality under cooperative agreement U01 HD044644 (to J.G.T.).

² Correspondence: Jeremy G. Thompson, Department of Obstetrics and Gynaecology, The University of Adelaide, The Queen Elizabeth Hospital, Woodville Rd., Woodville, SA 5011, Australia. FAX: 61 8 8222 7521; jeremy.thompson{at}adelaide.edu.au

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