Society for Reproductive Biology Founders’ Lecture 2005. Control of metabolic cooperativity between oocytes and their companion granulosa cells by mouse oocytes
Koji Sugiura A and John J. Eppig A BA The Jackson Laboratory, Bar Harbor, Maine 04609, USA.
B Corresponding author. Email: jje@jax.org
Reproduction, Fertility and Development 17(7) 667-674 https://doi.org/10.1071/RD05071
Submitted: 28 June 2005 Accepted: 19 July 2005 Published: 7 September 2005
Abstract
Oocytes orchestrate the rate of follicular development and expression of genes in the surrounding granulosa cells. Oocytes are deficient in their ability to carry out some metabolic processes, such as glycolysis and amino acid uptake, and depend on the cooperation of granulosa cells to carry out these processes. In this dependency, the oocyte was previously considered a passive recipient of the nutritional support from granulosa cells. However, recent studies indicate an active role for the oocyte in controlling metabolic activity in granulosa cells. The ability of oocytes to control granulosa cell metabolism is achieved, at least in part, by regulating granulosa cell expression of genes encoding proteins involved in the metabolic processes. This review summarises current knowledge of intercellular communication between oocytes and granulosa cells from the perspective of oocyte control of gene expression in granulosa cells and metabolic cooperativity between the two cell types. The oocyte probably controls metabolism in granulosa cells to provide metabolites for its own development. In addition, we hypothesise that oocytes use their ability to regulate metabolic pathways in granulosa cells to orchestrate the rate of follicular development.
Acknowledgments
This research was supported by grants from the National Institute of Child Health and Human Development (HD23839 and HD44416). The authors thank Drs Ann Dorward, Mary Ann Handel and You Qiang Su for their helpful comments in the preparation of this manuscript.
Aaltonen, J. , Laitinen, M. P. , Vuojolainen, K. , Jaatinen, N. , and Horelli-Kuitunen, N. (1999). Human growth differentiation factor 9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J. Clin. Endocr. Metab. 84, 2744–2750.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ralph, J. H. , Telfer, E. E. , and Wilmut, I. (1995). Bovine cumulus cell expansion does not depend on the presence of an oocyte secreted factor. Mol. Reprod. Dev. 42, 248–253.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Roy, S. K. , and Terada, D. M. (1999). Activities of glucose metabolic enzymes in human preantral follicles: In vitro modulation by follicle-stimulating hormone, luteinizing hormone, epidermal growth factor, insulin-like growth factor I, and transforming growth factor beta 1. Biol. Reprod. 60, 763–768.
| PubMed |
Rubinstein, L. , Moguilevsky, J. A. , and Schiaffini, O. (1966). Glycolytic and oxidative metabolism of isolated prepuberal rat ovaries of androgenized rats. Life Sci. 5, 411–414.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schmid, P. , Cox, D. , van der Putten, H. , McMaster, G. K. , and Bilbe, G. (1994). Expression of TGF-βs and TGF-β type II receptor mRNAs in mouse folliculogenesis: stored maternal TGF-β2 message in oocytes. Biochem. Biophys. Res. Commun. 201, 649–656.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schultz, R. M. (1985). Roles of cell-to-cell communication in development. Biol. Reprod. 32, 27–42.
| PubMed |
Seamark, R. F. , Amato, F. , Hendrickson, S. , and Moor, R. M. (1976). Oxygen uptake, glucose utilization, lactate release and adenine nucleotide content of sheep ovarian follicles in culture: effect of human chorionic gonadotrophin. Aust. J. Biol. Sci. 29, 557–563.
| PubMed |
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 |
Surwilo, B. O. , and Doeg, K. A. (1973). Oxygen and glucose uptake, and lactate production in polycystic rat ovary. Endocrinology 93, 652–659.
| PubMed |
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 |
Tsafriri, A. , Lieberman, M. E. , Ahren, K. , and Lindner, H. R. (1976). Dissociation between LH-induced aerobic glycolysis and oocyte maturation in cultured Graafian follicles of the rat. Acta Endocrinol. (Copenh.) 81, 362–366.
| PubMed |
Valve, E. , Penttila, T. L. , Paranko, J. , and Harkonen, P. (1997). FGF-8 is expressed during specific phases of rodent oocyte and spermatogonium development. Biochem. Biophys. Res. Commun. 232, 173–177.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yan, C. , Wang, P. , DeMayo, J. , DeMayo, F. J. , and Elvin, J. A. (2001). Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol. Endocrinol. 15, 854–866.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zuelke, K. A. , and Brackett, B. G. (1992). Effects of luteinizing hormone on glucose metabolism in cumulus-enclosed bovine oocytes matured in vitro. Endocrinology 131, 2690–2696.
| Crossref | GoogleScholarGoogle Scholar | PubMed |