Mechanisms contributing to the reduced developmental competence of glucosamine-exposed mouse oocytes
Cheryl J. Schelbach A , Karen L. Kind B , Michelle Lane A and Jeremy G. Thompson A C
+ Author Affiliations
- Author Affiliations
A The Research Centre for Reproductive Health, Discipline of Obstetrics and Gynaecology, School of Paediatrics and Reproductive Health, The University of Adelaide, Adelaide, SA 5005, Australia.
B Animal Science, School of Agriculture, Food and Wine, The University of Adelaide, Adelaide, SA 5005, Australia.
C Corresponding author. Email: jeremy.thompson@adelaide.edu.au
Reproduction, Fertility and Development 22(5) 771-779 https://doi.org/10.1071/RD09193
Submitted: 17 August 2009 Accepted: 4 November 2009 Published: 7 April 2010
Abstract
Glucosamine (GlcN) is a widely used hyperglycaemia mimetic because of its ability to upregulate the ‘energy-sensing’ hexosamine biosynthesis pathway in a dose-dependent manner. A previous study demonstrated that addition of GlcN (2.5–5 mM) during IVM of cattle and pig cumulus–oocyte complexes (COC) inhibited development following fertilisation and early cleavage. In the present study, we demonstrate that the addition of 2.5 mM GlcN during IVM of mouse COCs similarly inhibits embryo development, with the degree of inhibition dependent upon the availability of glucose in the maturation medium. Furthermore, we determined that the effect of GlcN is likely mediated by the cumulus cell vestment, because we failed to observe inhibitory effects of GlcN following maturation of denuded (and therefore already developmentally compromised) oocytes. As with cattle oocytes, inhibition of O-linked glycosylation of unknown proteins within mouse cumulus cells significantly reversed the effects of GlcN. Finally, we also provide preliminary evidence that GlcN may inhibit the pentose phosphate metabolic pathway within the oocyte, an effect possibly mediated by cumulus cells in intact COCs. Collectively, our results demonstrate that GlcN inhibits the developmental competence of IVM mouse oocytes and suggest that this occurs via cumulus cell-mediated mechanisms. Therefore, the in vitro addition of GlcN is a useful experimental tool to determine the mechanisms of hyperglycaemic responses within COCs.
Additional keywords: glycosylation, hyperglycemia, oocyte maturation, pentose phosphate.
Acknowledgements
This work was supported by the National Institutes of Health, USA, as part of the NICHD National Cooperative Program on Female Health and Egg Quality under cooperative agreement U01 HD044664. The authors thank R. M. Schultz for his helpful comments.
References
Aghayan, M. , Rao, L. V. , Smith, R. M. , Jarett, L. , Charron, M. J. , Thorens, B. , and Heyner, S. (1992). Developmental expression and cellular localization of glucose transporter molecules during mouse preimplantation development. Development 115, 305–312.
| PubMed | CAS |
Leoni, G. G. , Bebbere, D. , Succu, S. , Berlinguer, F. , Mossa, F. , Galioto, M. , Boglioli, L. , Ledda, S. , and Naitana, S. (2007). Relations between relative mRNA abundance and developmental competence of ovine oocytes. Mol. Reprod. Dev. 74, 249–257.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Lequarre, A. S. , Grisart, B. , Moreau, B. , Schuurbiers, N. , Massip, A. , and Dessy, F. (1997). Glucose metabolism during bovine preimplantation development: analysis of gene expression in single oocytes and embryos. Mol. Reprod. Dev. 48, 216–226.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Leroy, J. L. , Vanholder, T. , Opsomer, G. , Van Soom, A. , and de Kruif, A. (2006). The in vitro development of bovine oocytes after maturation in glucose and beta-hydroxybutyrate concentrations associated with negative energy balance in dairy cows. Reprod. Domest. Anim. 41, 119–123.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Lonergan, P. , Gutierrez-Adan, A. , Rizos, D. , Pintado, B. , de la Fuente, J. , and Boland, M. P. (2003). Relative messenger RNA abundance in bovine oocytes collected in vitro or in vivo before and 20 hr after the preovulatory luteinizing hormone surge. Mol. Reprod. Dev. 66, 297–305.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Luciano, A. M. , Lodde, V. , Beretta, M. S. , Colleoni, S. , Lauria, A. , and Modina, S. (2005). Developmental capability of denuded bovine oocyte in a co-culture system with intact cumulus–oocyte complexes: role of cumulus cells, cyclic adenosine 3′,5′-monophosphate, and glutathione. Mol. Reprod. Dev. 71, 389–397.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Marshall, S. , Garvey, W. T. , and Traxinger, R. R. (1991a). New insights into the metabolic regulation of insulin action and insulin resistance: role of glucose and amino acids. FASEB J. 5, 3031–3036.
| PubMed | CAS |
Marshall, S. , Bacote, V. , and Traxinger, R. R. (1991b). Discovery of a metabolic pathway mediating glucose-induced desensitization of the glucose transport system. Role of hexosamine biosynthesis in the induction of insulin resistance. J. Biol. Chem. 266, 4706–4712.
| PubMed | CAS |
Marshall, S. , Nadeau, O. , and Yamasaki, K. (2004). Dynamic actions of glucose and glucosamine on hexosamine biosynthesis in isolated adipocytes: differential effects on glucosamine 6-phosphate, UDP-N-acetylglucosamine, and ATP levels. J. Biol. Chem. 279, 35 313–35 319.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Marshall, S. , Nadeau, O. , and Yamasaki, K. (2005a). Glucosamine-induced activation of glycogen biosynthesis in isolated adipocytes. Evidence for a rapid allosteric control mechanism within the hexosamine biosynthesis pathway. J. Biol. Chem. 280, 11 018–11 024.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Marshall, S. , Yamasaki, K. , and Okuyama, R. (2005b). Glucosamine induces rapid desensitization of glucose transport in isolated adipocytes by increasing GlcN-6-P levels. Biochem. Biophys. Res. Commun. 329, 1155–1161.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
McClain, D. A. (2002). Hexosamines as mediators of nutrient sensing and regulation in diabetes. J. Diabetes Complicat. 16, 72–80.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Morita, Y. , Tsutsumi, O. , Hosoya, I. , Taketani, Y. , Oka, Y. , and Kato, T. (1992). Expression and possible function of glucose transporter protein GLUT1 during preimplantation mouse development from oocytes to blastocysts. Biochem. Biophys. Res. Commun. 188, 8–15.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Nelson, B. A. , Robinson, K. A. , and Buse, M. G. (2000). High glucose and glucosamine induce insulin resistance via different mechanisms in 3T3-L1 adipocytes. Diabetes 49, 981–991.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Park, J. , Kwon, H. , Kang, Y. , and Kim, Y. (2007). Proteomic analysis of O-GlcNAc modifications derived from streptozotocin and glucosamine induced beta-cell apoptosis. J. Biochem. Mol. Biol. 40, 1058–1068.
| PubMed | CAS |
Patti, M. E. , Virkamaki, A. , Landaker, E. J. , Kahn, C. R. , and Yki-Jarvinen, H. (1999). Activation of the hexosamine pathway by glucosamine in vivo induces insulin resistance of early postreceptor insulin signaling events in skeletal muscle. Diabetes 48, 1562–1571.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Ratchford, A. M. , Chang, A. S. , Chi, M. M. , Sheridan, R. , and Moley, K. H. (2007). Maternal diabetes adversely affects AMP-activated protein kinase activity and cellular metabolism in murine oocytes. Am. J. Physiol. Endocrinol. Metab. 293, E1198–E1206.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Sayeski, P. P. , and Kudlow, J. E. (1996). Glucose metabolism to glucosamine is necessary for glucose stimulation of transforming growth factor-alpha gene transcription. J. Biol. Chem. 271, 15 237–15 243.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Su, Y. Q. , Sugiura, K. , Wigglesworth, K. , O’Brien, M. J. , Affoutit, J. P. , Pangas, S. A. , Matzuk, M. M. , and Eppig, J. J. (2008). Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development 135, 111–121.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Suchanek, E. V. , Simunic, V. , Juretic, D. , and Grizelj, V. (1994). Follicular fluid contents of hyaluronic acid, follicle-stimulating hormone and steroids relative to the success of in vitro fertilization of human oocytes. Fertil. Steril. 62, 347–352.
| PubMed | CAS |
Sugiura, K. , Pendola, F. L. , and Eppig, J. J. (2005). Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism. Dev. Biol. 279, 20–30.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Sugiura, K. , Su, Y. Q. , Diaz, F. J. , Pangas, S. A. , Sharma, S. , Wigglesworth, K. , O’Brien, M. J. , Matzuk, M. M. , Shimasaki, S. , and Eppig, J. J. (2007). Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 134, 2593–2603.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Sutton, M. L. , Cetica, P. D. , Beconi, M. T. , Kind, K. L. , Gilchrist, R. B. , and Thompson, J. G. (2003). Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes. Reproduction 126, 27–34.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Sutton-McDowall, M. L. , Gilchrist, R. B. , and Thompson, J. G. (2004). Cumulus expansion and glucose utilisation by bovine cumulus–oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone. Reproduction 128, 313–319.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Sutton-McDowall, M. L. , Mitchell, M. , Cetica, P. , Dalvit, G. , Pantaleon, M. , Lane, M. , Gilchrist, R. B. , and Thompson, J. G. (2006). Glucosamine supplementation during in vitro maturation inhibits subsequent embryo development: possible role of the hexosamine pathway as a regulator of developmental competence. Biol. Reprod. 74, 881–888.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Talbot, P. (1984). Hyaluronidase dissolves a component in the hamster zona pellucida. J. Exp. Zool. 229, 309–316.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Torres, C. R. , and Hart, G. W. (1984). Topography and polypeptide distribution of terminal N-acetylglucosamine residues on the surfaces of intact lymphocytes. Evidence for O-linked GlcNAc. J. Biol. Chem. 259, 3308–3317.
| PubMed | CAS |
Vanderhyden, B. C. , Caron, P. J. , Buccione, R. , and Eppig, J. J. (1990). Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev. Biol. 140, 307–317.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Virkamäki, A. , and Yki-Jarvinen, H. (1999). Allosteric regulation of glycogen synthase and hexokinase by glucosamine-6-phosphate during glucosamine-induced insulin resistance in skeletal muscle and heart. Diabetes 48, 1101–1107.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vosseller, K. , Wells, L. , Lane, M. D. , and Hart, G. W. (2002). Elevated nucleocytoplasmic glycosylation by O-GlcNAc results in insulin resistance associated with defects in Akt activation in 3T3-L1 adipocytes. Proc. Natl Acad. Sci. USA 99, 5313–5318.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Zheng, P. , Bavister, B. D. , and Ji, W. (2001). Energy substrate requirement for in vitro maturation of oocytes from unstimulated adult rhesus monkeys. Mol. Reprod. Dev. 58, 348–355.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Zhou, J. , Bievre, M. , and Bondy, C. A. (2000). Reduced GLUT1 expression in Igf1–/– null oocytes and follicles. Growth Horm. IGF Res. 10, 111–117.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
