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Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Effect of monosaccharide sugars on LH-induced differentiation and sugar transport facilitator (SLC2A) expression in sheep theca cells in vitro

B. K. Campbell A D , N. R. Kendall A C , V. Onions A , L. Guo A and R. J. Scaramuzzi B
+ Author Affiliations
- Author Affiliations

A Division of Human Development, School of Clinical Sciences, University of Nottingham, Queen’s Medical Centre, Nottingham NG7 2UH, UK.

B Department of Veterinary Basic Sciences, The Royal Veterinary College, Hawkshead Lane, Herts AL9 7TA, UK.

C Present address: School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD, UK.

D Corresponding author. Email: bruce.campbell@nottingham.ac.uk

Reproduction, Fertility and Development 26(3) 453-461 https://doi.org/10.1071/RD12064
Submitted: 29 February 2012  Accepted: 26 February 2013   Published: 28 May 2013

Abstract

The aim of the present study was to investigate the effects of glucose, galactose and fructose on the LH-induced differentiation and mRNA expression of sugar transport facilitators (SLC2A) by sheep thecal cells derived from small antral follicles cultured under serum-free conditions for 6 days. The dose and type of monosaccharide had a significant effect on LH-induced androstenedione production by theca cells and there was a significant interaction (P < 0.001). Glucose and galactose were used with equal efficiency so that cell numbers and androstenedione production at the end of the culture were comparable. Pharmacological doses of glucose (16.7 mM) inhibited steroidogenesis (P < 0.05). Cell numbers and androstenedione production by cells cultured with fructose were lower than for cells cultured with either glucose or galactose (P < 0.001). None of the monosaccharides resulted in the production of lactate. Expression of SLC2A1, SLC2A4 and SLC2A8, but not SLC2A5, mRNA was detected in fresh and cultured theca cells. Large doses (16.7 mM) of glucose and fructose, but not galactose, suppressed (P < 0.05) SLC2A expression. The results show that glucose and galactose, but not fructose, are readily metabolised via oxidative pathways to support LH-induced differentiation of sheep theca cells. Further work is required to determine the mechanisms resulting in these differences in relation to the established effects of nutrition on reproductive function.

Additional keywords: fructose, galactose, glucose.


References

Benomar, Y., Naour, N., Aubourg, A., Bailleux, V., Gertler, A., Djiane, J., Guerre-Millo, M., and Taouis, M. (2006). Insulin and leptin induce Glut4 plasma membrane translocation and glucose uptake in a human neuronal cell line by a phosphatidylinositol 3-kinase- dependent mechanism. Endocrinology 147, 2550–2556.
Insulin and leptin induce Glut4 plasma membrane translocation and glucose uptake in a human neuronal cell line by a phosphatidylinositol 3-kinase- dependent mechanism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvFOqs7s%3D&md5=82d4475eda2fae3bd6fe1224370b9057CAS | 16497805PubMed |

Burant, C. F., Takeda, J., Brotlaroche, E., Bell, G. I., and Davidson, N. O. (1992). Fructose transporter in human spermatozoa and small intestine is GLUT5. J. Biol. Chem. 267, 14 523–14 526.
| 1:CAS:528:DyaK38Xlt1ylsbs%3D&md5=5b62b93cc8962ab153f531be39c708daCAS |

Campbell, B., Scaramuzzi, R., and Webb, R. (1996). Induction and maintenance of oestradiol and immuno-reactive inhibin production with FSH by ovine granulosa cells cultured in serum free media. J. Reprod. Fertil. 106, 7–16.
Induction and maintenance of oestradiol and immuno-reactive inhibin production with FSH by ovine granulosa cells cultured in serum free media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmtVCnsw%3D%3D&md5=93c1f9d333f2764e907be91d0fea594bCAS | 8667349PubMed |

Campbell, B. K., Baird, D. T., and Webb, R. (1998). Effects of dose of LH on androgen production and luteinization of ovine theca cells cultured in a serum-free system. J. Reprod. Fertil. 112, 69–77.
Effects of dose of LH on androgen production and luteinization of ovine theca cells cultured in a serum-free system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitVKqtrc%3D&md5=68a9fbb3a41aaf42a57406cf385ce9a4CAS | 9538331PubMed |

Campbell, B. K., Kendall, N. R., Onions, V., and Scaramuzzi, R. J. (2010a). The effect of systemic and ovarian infusion of glucose, galactose and fructose on ovarian function in sheep. Reproduction 140, 721–732.
The effect of systemic and ovarian infusion of glucose, galactose and fructose on ovarian function in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFCnsbfF&md5=05329a661943c9adc2ff5304864374bdCAS | 20716612PubMed |

Campbell, B. K., Onions, V., Kendall, N. R., Guo, L., and Scaramuzzi, R. J. (2010b). The effect of monosaccharide sugars and pyruvate on the differentiation and metabolism of sheep granulosa cells in vitro. Reproduction 140, 541–550.
The effect of monosaccharide sugars and pyruvate on the differentiation and metabolism of sheep granulosa cells in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlCqurrI&md5=692d4f31ca13f924bae8d72a59f6ecd5CAS | 20634389PubMed |

Curi, R., Lagranha, C. J., Doi, S. Q., Sellitti, D. F., Procopio, J., Pithon-Curi, T. C., Corless, M., and Newsholme, P. (2005). Molecular mechanisms of glutamine action. J. Cell. Physiol. 204, 392–401.
Molecular mechanisms of glutamine action.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvFCrs7w%3D&md5=55692d4e06f7c90bb6d72bce69efd938CAS | 15795900PubMed |

Curry, D. L. (1989). Effects of mannose and fructose on the synthesis and secretion of insulin. Pancreas 4, 2–9.
Effects of mannose and fructose on the synthesis and secretion of insulin.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M3ktVKgtA%3D%3D&md5=5e198f3cdf3175650cc32611839ba405CAS | 2654926PubMed |

Daniels, L. B., Perkins, J. L., Krieder, D., Tugwell, D., and Carpente, D. (1974). Blood glucose and fructose in newborn ruminant. J. Dairy Sci. 57, 1196–1200.
Blood glucose and fructose in newborn ruminant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXitF2n&md5=ef1d85a227322426bd6481709efaff6fCAS | 4427002PubMed |

Elliott, S. S., Keim, N. L., Stern, J. S., Teff, K., and Havel, P. J. (2002). Fructose, weight gain, and the insulin resistance syndrome. Am. J. Clin. Nutr. 76, 911–922.
| 1:CAS:528:DC%2BD38XosF2ru7k%3D&md5=3fd6da4b399412516635f6d2a2b6cbe1CAS | 12399260PubMed |

Forges, T., Monnier-Barbarino, P., Leheup, B., and Jouvet, P. (2006). Pathophysiology of impaired ovarian function in galactosaemia. Hum. Reprod. Update 12, 573–584.
Pathophysiology of impaired ovarian function in galactosaemia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xotl2ls7w%3D&md5=e123120b4b3ba53500d2534bd062557dCAS | 16835432PubMed |

Havel, P. J. (1997). Glucose but not fructose infusion increases circulating leptin in proportion to adipose stores in rhesus monkeys. Exp. Clin. Endocrinol. Diabetes 105, 37–38.
Glucose but not fructose infusion increases circulating leptin in proportion to adipose stores in rhesus monkeys.Crossref | GoogleScholarGoogle Scholar |

Klip, A., Tsakiridis, T., Marette, A., and Ortiz, P. A. (1994). Regulation of expression of glucose transporters by glucose: a review of studies in vivo and in cell cultures. FASEB J. 8, 43–53.
| 1:CAS:528:DyaK2cXhvVOkt7o%3D&md5=85f23c91b91210fb307971a9bfb5d7b8CAS | 8299889PubMed |

Kol, S., Ben-Shlomo, I., Ruutiainen, K., Ando, M., Davies-Hill, T. M., Rohan, R. M., Simpson, I. A., and Adashi, E. Y. (1997). The midcycle increase in ovarian glucose uptake is associated with enhanced expression of glucose transporter 3. Possible role for interleukin-1, a putative intermediary in the ovulatory process. J. Clin. Invest. 99, 2274–2283.
The midcycle increase in ovarian glucose uptake is associated with enhanced expression of glucose transporter 3. Possible role for interleukin-1, a putative intermediary in the ovulatory process.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtFCit7w%3D&md5=d076154c7a05519e06148434994b4880CAS | 9151802PubMed |

Liu, G. T., Hale, G. E., and Hughes, C. L. (2000). Galactose metabolism and ovarian toxicity. Reprod. Toxicol. 14, 377–384.
Galactose metabolism and ovarian toxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntVWgsbg%3D&md5=e780d237dcf3943c2c362071567c8823CAS |

Luick, J. R., Kleiber, M., Lucas, J. M., and Rogers, T. A. (1957). Fructose metabolism in dairy cows. Am. J. Physiol. 191, 90–94.
| 1:CAS:528:DyaG1cXhs1yhtw%3D%3D&md5=8d55383778c53dc94c74bb74903f81d6CAS | 13478691PubMed |

Magoffin, D. (2005). Ovarian theca cell. Int. J. Biochem. Cell Biol. 37, 1344–1349.
Ovarian theca cell.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjt1Wjsrc%3D&md5=2940c9b58cb2e89a0de8de0e9c8bf63bCAS | 15833266PubMed |

Marshall, S., Garvey, W. T., and Traxinger, R. R. (1991). New insights into the metabolic regulation of insulin action and insulin resistance: role of glucose and amino acids. FASEB J. 5, 3031–3036.
| 1:CAS:528:DyaK38XltFKlsw%3D%3D&md5=52beeaa5a4de6517fe3e79e04954244fCAS | 1743436PubMed |

McNeilly, A. S., Picton, H. M., Campbell, B. K., and Baird, D. T. (1991). Gonadotrophic control of follicle growth in the ewe. J. Reprod. Fertil. Suppl. 43, 177–186.
| 1:CAS:528:DyaK38XisVymu74%3D&md5=66f23ea3106a64788a8d50a76dc1c8fcCAS | 1843339PubMed |

Merezhinskaya, N., and Fishbein, W. N. (2009). Monocarboxylate transporters: past, present, and future. Histol. Histopathol. 24, 243–264.
| 19085840PubMed |

Murray, J. F., Giles, R. M., Carter, N. D., and Robinson, S. P. (2009). The antrums of ovine ovarian preovulatory follicles are severely hypoxic. In: ‘Proceedings of the Society For Reproduction and Fertility Annual Conference, 12–14 July 2009’. p. 38. [Abstract]

Nandi, S., Kumar, V. G., Manjunatha, B. M., Ramesh, H. S., and Gupta, P. S. P. (2008). Follicular fluid concentrations of glucose, lactate and pyruvate in buffalo and sheep, and their effects on cultured oocytes, granulosa and cumulus cells. Theriogenology 69, 186–196.
Follicular fluid concentrations of glucose, lactate and pyruvate in buffalo and sheep, and their effects on cultured oocytes, granulosa and cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVyrsg%3D%3D&md5=90a21313dd435fa88878d852724245b1CAS | 17950822PubMed |

Nishimoto, H., Matsutani, R., Yamamoto, S., Takahashi, T., Hayashi, K. G., Miyamoto, A., Hamano, S., and Tetsuka, M. (2006). Gene expression of glucose transporter (GLUT) 1, 3 and 4 in bovine follicle and corpus luteum. J. Endocrinol. 188, 111–119.
Gene expression of glucose transporter (GLUT) 1, 3 and 4 in bovine follicle and corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVCisL8%3D&md5=589437159fb8655cd86720a04299dcc7CAS | 16394180PubMed |

Obici, S., and Rossetti, L. (2003). Minireview: Nutrient sensing and the regulation of insulin action and energy balance. Endocrinology 144, 5172–5178.
Minireview: Nutrient sensing and the regulation of insulin action and energy balance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsV2gt7c%3D&md5=7b1fe717a4476d65051ee716218b0824CAS | 12970158PubMed |

Pisani, L. F., Antonini, S., Pocar, P., Ferrari, S., Brevini, T. A., Rhind, S. M., and Gandolfi, F. (2008). Effects of pre-mating nutrition on mRNA levels of developmentally relevant genes in sheep oocytes and granulosa cells. Reproduction 136, 303–312.
Effects of pre-mating nutrition on mRNA levels of developmentally relevant genes in sheep oocytes and granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1GmtLzE&md5=239a695736db98f1bf7874db42741d58CAS | 18515315PubMed |

Rabiee, A. R., Lean, I. J., Gooden, J. M., Miller, B. G., and Scaramuzzi, R. J. (1997). An evaluation of transovarian uptake of metabolites using arterio-venous difference methods in dairy cattle. Anim. Reprod. Sci. 48, 9–25.
An evaluation of transovarian uptake of metabolites using arterio-venous difference methods in dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmvFSqsb4%3D&md5=bc3270e40ed19334fdbb8c47eb5dc6afCAS | 9412729PubMed |

Rizos, D., Gutierrez-Adan, A., Moreira, P., O’Meara, C., Fair, T., Evans, A. C., Boland, M. P., and Lonergan, P. (2004). Species-related differences in blastocyst quality are associated with differences in relative mRNA transcription. Mol. Reprod. Dev. 69, 381–386.
Species-related differences in blastocyst quality are associated with differences in relative mRNA transcription.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpvFOluro%3D&md5=795db912d20689cb6b6209c4281016c5CAS | 15457517PubMed |

Scaramuzzi, R. J., Campbell, B. K., Downing, J. A., Kendall, N. R., Khalid, M., Munoz-Gutierrez, M., and Somchit, A. (2006). A review of the effects of supplementary nutrition in the ewe on the concentrations of reproductive and metabolic hormones and the mechanisms that regulate folliculogenesis and ovulation rate. Reprod. Nutr. Dev. 46, 339–354.
A review of the effects of supplementary nutrition in the ewe on the concentrations of reproductive and metabolic hormones and the mechanisms that regulate folliculogenesis and ovulation rate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOnsrzF&md5=8a64193bb2d5e00d9ed8ece12429b785CAS | 16824444PubMed |

Scaramuzzi, R. J., Campbell, B. K., Souza, C. J. H., and Baird, D. T. (2010). Glucose uptake and lactate production by the autotransplanted ovary of the ewe during the luteal and follicular phases of the oestrous cycle. Theriogenology 73, 1061–1067.
Glucose uptake and lactate production by the autotransplanted ovary of the ewe during the luteal and follicular phases of the oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlClu7o%3D&md5=055d9af0d4640674aee37f883f9cc853CAS | 20189236PubMed |

Somchit, A., Campbell, B. K., Khalid, M., Kendall, N. R., and Scaramuzzi, R. J. (2007). The effect of short-term nutritional supplementation of ewes with lupin grain (Lupinus luteus), during the luteal phase of the estrous cycle on the number of ovarian follicles and the concentrations of hormones and glucose in plasma and follicular fluid. Theriogenology 68, 1037–1046.
The effect of short-term nutritional supplementation of ewes with lupin grain (Lupinus luteus), during the luteal phase of the estrous cycle on the number of ovarian follicles and the concentrations of hormones and glucose in plasma and follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVOgsLfN&md5=1494755a561d518a03c62d4e7363f70dCAS | 17826826PubMed |

Teff, K. L., Elliott, S. S., Tschöp, M., Kieffer, T. J., Rader, D., Heiman, M., Townsend, R. R., Keim, N. L., D’Alessio, D., and Havel, P. J. (2004). Dietary fructose reduces circulating insulin and leptin, attenuates postprandial suppression of ghrelin, and increases triglycerides in women. J. Clin. Endocrinol. Metab. 89, 2963–2972.
Dietary fructose reduces circulating insulin and leptin, attenuates postprandial suppression of ghrelin, and increases triglycerides in women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtlKjs7Y%3D&md5=42b83a83642cd0b74fd2b0a47370765fCAS | 15181085PubMed |

Williams, S. A., Blache, D., Martin, G. B., Foot, R., Blackberry, M. A., and Scaramuzzi, R. J. (2001). Effect of nutritional supplementation on quantities of glucose transporters 1 and 4 in sheep granulosa and theca cells. Reproduction 122, 947–956.
Effect of nutritional supplementation on quantities of glucose transporters 1 and 4 in sheep granulosa and theca cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvVWitw%3D%3D&md5=674645c94723f3d9413d829cd643aa6aCAS | 11732990PubMed |

Zhao, F. Q., and Keating, A. F. (2007). Functional properties and genomics of glucose transporters. Curr. Genomics 8, 113–128.
Functional properties and genomics of glucose transporters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Kntb7O&md5=f4be11bbcc4dec5078faf31afd1f1639CAS | 18660845PubMed |

Zubay, G. (1998). Glycolysis, gluconeogenesis and the pentose phosphate pathway. In ‘Biochemistry’. (Ed. G. Zubay.) pp. 293–323. (Wm. C. Brown Publishers: London.)