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

Acute fasting decreases the expression of GLUT1 and glucose utilisation involved in mouse oocyte maturation and cumulus cell expansion

Yingying Han A , Jun Yan B , Jinlian Zhou C , Zhen Teng A , Fenghua Bian A , Meng Guo A , Guankun Mao A , Junxia Li A , Jianwei Wang A , Meijia Zhang A and Guoliang Xia A D
+ Author Affiliations
- Author Affiliations

A State Key Laboratory of Agrobiotechnology, College of Biological Sciences, China Agricultural University, Beijing 100093, People’s Republic of China.

B Beijing Royal School, Beijing 102209, People’s Republic of China.

C Department of Pathology, 306 Hospital of PLA, Beijing, 100101, People’s Republic of China.

D Corresponding author. Email: glxiachina@sohu.com

Reproduction, Fertility and Development 24(5) 733-742 https://doi.org/10.1071/RD10301
Published online: 15 December 2011

Abstract

Acute fasting impairs meiotic resumption and glucose consumption in mouse cumulus cell and oocyte complexes (COCs). This study examines the effects of acute fasting on the regulation of glucose transporter 1 (GLUT1) expression and glucose consumption in oocyte maturation. Our results indicate that the restriction of glucose utilisation by 2-deoxyglucose (2-DG) mimicked the inhibitory effects of acute fasting on oocyte meiotic resumption and cumulus cell expansion, effects that were rescued by high glucose concentrations in the culture medium. GLUT1 protein levels were higher in cumulus cells compared with oocytes, and GLUT1 expression in COCs increased with FSH treatment in vitro. However, under acute fasting conditions, GLUT1 expression in COCs decreased and the response to FSH disappeared. Exposure to high glucose conditions (27.5 mM and 55 mM), significantly increased both glucose consumption and GLUT1 levels in COCs. Inhibition of GLUT1 function using an anti-GLUT1 antibody significantly inhibited FSH-induced oocyte meiotic resumption. Taken together, these results suggest that acute fasting decreases GLUT1 expression and glucose utilisation, inhibiting the processes of oocyte maturation and cumulus cell expansion.

Additional keywords: food deprivation, glucose transport, nutrition, oocyte development.


References

Augustin, R. (2010). The protein family of glucose transport facilitators: it’s not only about glucose after all. IUBMB Life 62, 315–333.
| 1:CAS:528:DC%2BC3cXkvFegtLY%3D&md5=a891b8c6c89943fd7c1266773cba01a7CAS | 20209635PubMed |

Augustin, R., Pocar, P., Navarrete-Santos, A., Wrenzycki, C., Gandolfi, F., Niemann, H., and Fischer, B. (2001). Glucose transporter expression is developmentally regulated in in vitro-derived bovine preimplantation embryos. Mol. Reprod. Dev. 60, 370–376.
Glucose transporter expression is developmentally regulated in in vitro-derived bovine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnsV2hsbc%3D&md5=83d12f5815c1e33aab67536cf8b5f6ebCAS | 11599048PubMed |

Blondin, P., and Sirard, M. A. (1995). Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes. Mol. Reprod. Dev. 41, 54–62.
Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlsVagsrs%3D&md5=3ea1c789debb597816356512c30cf1ccCAS | 7619506PubMed |

Colton, S. A., Pieper, G. M., and Downs, S. M. (2002). Altered meiotic regulation in oocytes from diabetic mice. Biol. Reprod. 67, 220–231.
Altered meiotic regulation in oocytes from diabetic mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvV2itb8%3D&md5=13ddaa6c6a6a7cd9f3310fe8beb2df4dCAS | 12080021PubMed |

Costello, P. M., Rowlerson, A., Astaman, N. A., Anthony, F. E., Sayer, A. A., Cooper, C., Hanson, M. A., and Green, L. R. (2008). Peri-implantation and late gestation maternal undernutrition differentially affect fetal sheep skeletal muscle development. J. Physiol. 586, 2371–2379.
Peri-implantation and late gestation maternal undernutrition differentially affect fetal sheep skeletal muscle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtlartbs%3D&md5=be94659d756f038d469b8d0325189f3cCAS | 18339691PubMed |

Dan-Goor, M., Sasson, S., Davarashvili, A., and Almagor, M. (1997). Expression of glucose transporter and glucose uptake in human oocytes and preimplantation embryos. Hum. Reprod. 12, 2508–2510.
Expression of glucose transporter and glucose uptake in human oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjt1Sltw%3D%3D&md5=d280d9d5760230ed275cae1c51385e16CAS | 9436695PubMed |

Downs, S. M., and Mastropolo, A. M. (1994). The participation of energy substrates in the control of meiotic maturation in murine oocytes. Dev. Biol. 162, 154–168.
The participation of energy substrates in the control of meiotic maturation in murine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhvVyitLs%3D&md5=0c38b1affd242df951265cb578055173CAS | 8125183PubMed |

Downs, S. M., and Utecht, A. M. (1999). Metabolism of radiolabelled glucose by mouse oocytes and oocyte–cumulus cell complexes. Biol. Reprod. 60, 1446–1452.
Metabolism of radiolabelled glucose by mouse oocytes and oocyte–cumulus cell complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsVeisLs%3D&md5=59bd8d98ac84fad3dcf0c26d8a1840cdCAS | 10330104PubMed |

Downs, S. M., Humpherson, P. G., Martin, K. L., and Leese, H. J. (1996). Glucose utilization during gonadotrophin-induced meiotic maturation in cumulus cell-enclosed mouse oocytes. Mol. Reprod. Dev. 44, 121–131.
Glucose utilization during gonadotrophin-induced meiotic maturation in cumulus cell-enclosed mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XivV2mt7g%3D&md5=a9760e61746d5fcc5bd761f503a661a6CAS | 8722700PubMed |

Downs, S. M., Humpherson, P. G., and Leese, H. J. (1998). Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway. Biol. Reprod. 58, 1084–1094.
Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXit1KhtL0%3D&md5=5701b0da82971440fe7697555eb0dd1cCAS | 9546744PubMed |

Frolova, A., Flessner, L., Chi, M., Kim, S. T., Foyouzi-Yousefi, N., Moley, K. H., and Moley, H. (2009). Facilitative glucose transporter type 1 is differentially regulated by progesterone and oestrogen in murine and human endometrial stromal cells. Endocrinology 150, 1512–1520.
Facilitative glucose transporter type 1 is differentially regulated by progesterone and oestrogen in murine and human endometrial stromal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisV2guro%3D&md5=0e6cfb3cb27de46b1e96ede9f6a437adCAS | 18948400PubMed |

Gilchrist, R. B., Ritter, L. J., and Armstrong, D. T. (2004). Oocyte–somatic cell interactions during follicle development in mammals. Anim. Reprod. Sci. 82–83, 431–446.
Oocyte–somatic cell interactions during follicle development in mammals.Crossref | GoogleScholarGoogle Scholar | 15271471PubMed |

Gnudi, L., Viberti, G., Raij, L., Rodriguez, V., Burt, D., Cortes, P., Hartley, B., Thomas, S., Maestrini, S., and Gruden, G. (2003). GLUT-1 overexpression: link between haemodynamic and metabolic factors in glomerular injury? Hypertension 42, 19–24.
GLUT-1 overexpression: link between haemodynamic and metabolic factors in glomerular injury?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvVKmtr8%3D&md5=9be37451abd34b3e5afbfb2b5b6f6c99CAS | 12771048PubMed |

Hediger, M. A., and Rhoads, D. B. (1994). Molecular physiology of sodium–glucose cotransporters. Physiol. Rev. 74, 993–1026.
| 1:CAS:528:DyaK2MXitFGnsLs%3D&md5=c7c0c92ed990547965904c2d5893015cCAS | 7938229PubMed |

Heilig, C. W., Concepcion, L. A., Riser, B. L., Freytag, S. O., Zhu, M., and Cortes, P. (1995). Overexpression of glucose transporters in rat mesangial cells cultured in a normal glucose milieu mimics the diabetic phenotype. J. Clin. Invest. 96, 1802–1814.
Overexpression of glucose transporters in rat mesangial cells cultured in a normal glucose milieu mimics the diabetic phenotype.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXosFyhsb8%3D&md5=e9f73fcd75d78ab389d805d099fb2aaaCAS | 7560072PubMed |

Heilig, C. W., Saunders, T., Brosius, F. C., Moley, K., Heilig, K., Baggs, R., Guo, L., and Conner, D. (2003). Glucose transporter-1-deficient mice exhibit impaired development and deformities that are similar to diabetic embryopathy. Proc. Natl. Acad. Sci. USA 100, 15613–15618.
Glucose transporter-1-deficient mice exhibit impaired development and deformities that are similar to diabetic embryopathy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVChtw%3D%3D&md5=209fe10ff57bb7533e3f2a07aa852fe7CAS | 14673082PubMed |

Herrick, J. R., Brad, A. M., and Krisher, R. L. (2006). Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro. Reproduction 131, 289–298.
Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFalsLs%3D&md5=a92cc5f6ca024c9141c68af8dc0ed90bCAS | 16452722PubMed |

Jensen, P. J., Gitlin, J. D., and Carayannopoulos, M. O. (2006). GLUT1 deficiency links nutrient availability and apoptosis during embryonic development. J. Biol. Chem. 281, 13382–13387.
GLUT1 deficiency links nutrient availability and apoptosis during embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xkt1ymsbc%3D&md5=24fd7c6be676253f9aa76c3a25d86622CAS | 16543226PubMed |

Joost, H. G., and Thorens, B. (2001). The extended GLUT-family of sugar/polyol transport facilitators: nomenclature, sequence characteristics and potential function of its novel members. Mol. Membr. Biol. 18, 247–256.
The extended GLUT-family of sugar/polyol transport facilitators: nomenclature, sequence characteristics and potential function of its novel members.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvVWrsA%3D%3D&md5=0fc41c7c19fcbdb51a3f038a14e22819CAS | 11780753PubMed |

Khurana, N. K., and Niemann, H. (2000). Effects of oocyte quality, oxygen tension, embryo density, cumulus cells and energy substrates on cleavage and morula/blastocyst formation of bovine embryos. Theriogenology 54, 741–756.
Effects of oocyte quality, oxygen tension, embryo density, cumulus cells and energy substrates on cleavage and morula/blastocyst formation of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FovVGrtA%3D%3D&md5=aacc56c70077cb6746a89a6cb693e405CAS | 11101035PubMed |

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=cfb7f4f832bbb3ffebf2cab546217396CAS | 9151802PubMed |

Krisher, R. L., and Bavister, B. D. (1998). Responses of oocytes and embryos to the culture environment. Theriogenology 49, 103–114.
Responses of oocytes and embryos to the culture environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsFCrtQ%3D%3D&md5=01de0069dc9ee321d9a3f3b714fb1a68CAS | 10732124PubMed |

Martin, K. L., and Leese, H. J. (1999). Role of developmental factors in the switch from pyruvate to glucose as the major exogenous energy substrate in the preimplantation mouse embryo. Reprod. Fertil. Dev. 11, 425–433.
Role of developmental factors in the switch from pyruvate to glucose as the major exogenous energy substrate in the preimplantation mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXns1Smuro%3D&md5=b1f8cea2fe5e7bdb42fcf905669c4bc4CAS | 11101279PubMed |

McClure, T. J. (1967). Infertility in mice caused by fasting at about the time of mating. 3. Pathogenesis. J. Reprod. Fertil. 13, 393–403.
Infertility in mice caused by fasting at about the time of mating. 3. Pathogenesis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF2s7nsV2qsg%3D%3D&md5=da360e4a1b0153ea71c38ecb94edbf79CAS | 6027843PubMed |

Mueckler, M. (1994). Facilitative glucose transporters. Eur. J. Biochem. 219, 713–725.
Facilitative glucose transporters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhsFKrs7Y%3D&md5=abc2634f911531ec2249150f5e771fcaCAS | 8112322PubMed |

Osgerby, J. C., Wathes, D. C., Howard, D., and Gadd, T. S. (2002). The effect of maternal undernutrition on ovine fetal growth. J. Endocrinol. 173, 131–141.
The effect of maternal undernutrition on ovine fetal growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1ejtr4%3D&md5=d3cd117978353073b138e751008e7047CAS | 11927392PubMed |

Preis, K. A., Seidel, G., and Gardner, D. K. (2005). Metabolic markers of developmental competence for in vitro-matured mouse oocytes. Reproduction 130, 475–483.
Metabolic markers of developmental competence for in vitro-matured mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFent7rI&md5=a352a78439b50e5f586bfaa5a707c2f2CAS | 16183865PubMed |

Prunier, A., and Quesnel, H. (2000). Influence of the nutritional status on ovarian development in female pigs. Anim. Reprod. Sci. 60–61, 185–197.
Influence of the nutritional status on ovarian development in female pigs.Crossref | GoogleScholarGoogle Scholar | 10844194PubMed |

Richards, J. S., Sharma, S. C., Falender, A. E., and Lo, Y. H. (2002). Expression of FKHR, FKHRL1 and AFX genes in the rodent ovary: evidence for regulation by IGF-I, oestrogen and the gonadotrophins. Mol. Endocrinol. 16, 580–599.
Expression of FKHR, FKHRL1 and AFX genes in the rodent ovary: evidence for regulation by IGF-I, oestrogen and the gonadotrophins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitFSisLk%3D&md5=9729e1a81b4c01734bc177bb68ed7534CAS | 11875118PubMed |

Roberts, A. J., Paisley, S. I., Geary, T. W., Grings, E. E., Waterman, R. C., and MacNeil, M. D. (2007). Effects of restricted feeding of beef heifers during the postweaning period on growth, efficiency and ultrasound carcass characteristics. J. Anim. Sci. 85, 2740–2745.
Effects of restricted feeding of beef heifers during the postweaning period on growth, efficiency and ultrasound carcass characteristics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFSjtrbM&md5=d703a51d87c9a20b843c4713f638da46CAS | 17565051PubMed |

Roberts, R., Stark, J., Iatropoulou, A., Becker, D. L., Franks, S., and Hardy, K. (2004). Energy substrate metabolism of mouse cumulus–oocyte complexes: response to follicle-stimulating hormone is mediated by the phosphatidylinositol 3-kinase pathway and is associated with oocyte maturation. Biol. Reprod. 71, 199–209.
Energy substrate metabolism of mouse cumulus–oocyte complexes: response to follicle-stimulating hormone is mediated by the phosphatidylinositol 3-kinase pathway and is associated with oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFKkurs%3D&md5=3b4e8cb1dbfc237f131322b86b800bd6CAS | 15028625PubMed |

Salustri, A., Yanagishita, M., and Hascall, V. C. (1989). Synthesis and accumulation of hyaluronic acid and proteoglycans in the mouse cumulus cell–oocyte complex during follicle-stimulating hormone-induced mucification. J. Biol. Chem. 264, 13840–13847.
| 1:CAS:528:DyaL1MXlt1OgsLg%3D&md5=be321d0a44f8a5b107be9638e0f469d1CAS | 2503506PubMed |

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.
Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvFCntbY%3D&md5=f2aed67204cba3a40ecce6668f6d1bdaCAS | 12814344PubMed |

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.
Cumulus expansion and glucose utilisation by bovine cumulus–oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXot1KitLk%3D&md5=c0ee73cf3631e359cdd6ed74a40a9c10CAS | 15333782PubMed |

Wang, D., Pascual, J. M., Yang, H., Engelstad, K., Mao, X., Cheng, J., Yoo, J., Noebels, J. L., and De Vivo, D. C. (2006). A mouse model for Glut-1 haploinsufficiency. Hum. Mol. Genet. 15, 1169–1179.
A mouse model for Glut-1 haploinsufficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Shsrc%3D&md5=d3f6f02c10a5990b82f98849ba607a55CAS | 16497725PubMed |

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=9aca974f05414a5e2168a3ab176f260bCAS | 11732990PubMed |

Wood, I. S., and Trayhurn, P. (2003). Glucose transporters (GLUT and SGLT): expanded families of sugar transport proteins. Br. J. Nutr. 89, 3–9.
Glucose transporters (GLUT and SGLT): expanded families of sugar transport proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsFWmu74%3D&md5=44074bfdffa2bf54508a4b321f35fae7CAS | 12568659PubMed |

Wu, G., Bazer, F. W., Cudd, T. A., Meininger, C. J., and Spencer, T. E. (2004). Maternal nutrition and fetal development. J. Nutr. 134, 2169–2172.
| 1:CAS:528:DC%2BD2cXns1ejtLg%3D&md5=7c9d08ec93db564544bf4aa50a3c9b35CAS | 15333699PubMed |

Yan, J., Zhou, B., Yang, J., Tai, P., Chen, X., Zhang, H., Zhang, M., and Xia, G. (2008). Glucose can reverse the effects of acute fasting on mouse ovulation and oocyte maturation. Reprod. Fertil. Dev. 20, 703–712.
Glucose can reverse the effects of acute fasting on mouse ovulation and oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlCnu74%3D&md5=dddb89ef47d8b3381a163b301cff1b03CAS | 18671918PubMed |

Zhao, F. Q., Zheng, Y. C., Wall, E. H., and McFadden, T. B. (2005). Cloning and expression of bovine sodium/glucose cotransporters. J. Dairy Sci. 88, 182–194.
Cloning and expression of bovine sodium/glucose cotransporters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXms12g&md5=6f6c04d79bd2c43972b73f7e5fc49f89CAS | 15591382PubMed |

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.
Energy substrate requirement for in vitro maturation of oocytes from unstimulated adult rhesus monkeys.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtVShsro%3D&md5=894360e93282016ff36f17e26e862f38CAS | 11170277PubMed |

Zheng, P., Vassena, R., and Latham, K. E. (2007). Effects of in vitro oocyte maturation and embryo culture on the expression of glucose transporters, glucose metabolism and insulin signalling genes in rhesus monkey oocytes and preimplantation embryos. Mol. Hum. Reprod. 13, 361–371.
Effects of in vitro oocyte maturation and embryo culture on the expression of glucose transporters, glucose metabolism and insulin signalling genes in rhesus monkey oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnvFCqu7s%3D&md5=51beb9fdb707f1b75c194be2fea08f4aCAS | 17416905PubMed |

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.
Reduced GLUT1 expression in Igf1–/– null oocytes and follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmvVSjt7k%3D&md5=3dc1f67c7adac8787e083498a91fffd2CAS | 10942631PubMed |