Carbohydrate Uptake in Water Buffalo Cumulus-Oocyte Complexes (COCs) Supplemented with Retinoic Acid During In Vitro Maturation
Lilibeth A. Cajuday1*, Annabelle A. Herrera2, and Danilda H. Duran3
1Biology Department, College of Science, Bicol University,
Legazpi City 4500 Albay, Philippines
2Institute of Biology, College of Science, University of the Philippines,
Diliman, Quezon City 1101 Philippines
3Reproductive Biotechnology Laboratory, Philippine Carabao Center,
Muñoz, Nueva Ecija 3119 Philippines
Carbohydrate uptake by water buffalo oocytes after in vitro maturation was evaluated in the present study. The concentrations of glucose and pyruvate were analysed in the spent culture media. Glucose uptake (mM) was increased significantly in the COCs that were supplemented with all-trans RA at doses of 1 (5.00), 3 (4.98), and 5 (5.20) μM compared to control (4.14) and vehicle (4.25). Pyruvate concentration (μM) in the spent culture media was very minimal
indicating sufficient uptake by the COCs. However, pyruvate uptake was not significantly different between the control and vehicle compared with RA-treated groups. The data suggest that pyruvate uptake by the COCs does not require all-trans RA. Likewise this research suggests a potential role of all- trans RA in glucose uptake which coincides with its effect in enhancing the developmental competence of water buffalo oocytes.
During mammalian oogenesis, the oocyte grows by more than twice of its original volume, produces large quantities of a myriad macromolecules, as it undergoes a complex series of morphological and developmental changes. In vivo the process begins with the formation of primordial germ cells (PGCs) and proceeds through a series of cellular transformations, from PGC to oogonia to oocytes then to eggs in the adult (Wassarman 1999). In both natural and artificial conditions, oocyte development encompasses a variety of cellular changes categorized as either nuclear or cytoplasmic maturation necessary for normal fertilization and successful embryonic development (Eppig 1996). . . . . . . . . .
BIGGERS J, WHITTINGHAM D, DONAHUE R. 1967. The pattern of energy metabolism in the mouse oocyte and zygote. Proc Nat Acad Sci 58:567.
BLUMENTRATH J, NEYE H, VERSPOHL EJ. 2001. Effects of retinoids and thiazolidinediones on proliferation, insulin release, insulin mRNA, GLUT 2 transporter protein and mRNA of INS-1 cells. Cell Biochem Funct 19: 159-169.
BOLAND NI, HUMPHERSON PG, LEESE HJ, GOSDEN RG. 1993. Pattern of lactate production and steroidogenesis during growth and maturation of mouse ovarian follicles in vitro. Biol of Reprod 48: 798-806.
BOLAND NI, HUMPHERSON PG, LEESE HJ, GOSDEN RG. 1994. The effect of glucose metabolism on murine follicle development and steroidogenesis in vitro. Hum Reprod 9: 617-623.
BONDAR RJL, MEAD DC. 1974. Evaluation of glucose6-phosphate dehydrogenase from Leuconostoc mesenteroides in the hexokinass method for determining glucose in serum. Clin Chem 20: 586.
BRINSTER RL. 1971. Oxidation of pyruvate and glucose by oocytes of the mouse and rhesus monkey. J Reprod Fertil 24: 187-191.
DOWNS SM, MASTROPOLO AM. 1994. The participation of energy substrates in the control of meiotic maturation in murine oocytes. Dev Biol 162: 154-168.
EPPIG JJ. 1996. Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod Fert Dev 8: 485-489.
FAGBOHUN CF, DOWNS SM. 1992. Requirement for glucose in ligand stimulated meiotic maturation of cumulus cell-enclosed mouse oocytes. J Reprod Fert 96: 681-697.
GARDNER DK, LEESE HJ. 1990. Concentrations of nutrients in mouse oviduct fluid and their effects on embryo development and metabolism in vitro. J Reprod Fert 88: 361-368.
GARDNER DK, POOL TB, LANE M. 2000. Embryo nutrition and energy metabolism and its realtionship to embryo growth, development and viability. Sem. Reprod Med 18: 205-218.
GESHI M, TAKENOUCHI N, YAMAUCHI N, NAGAI T. 2000. Effects of sodium pyruvate in nonserum maturation medium on maturation, fertilization, and subsequent development of bovine oocytes with or without cumulus cells. Biol Reprod 63: 1730-34.
GUTNISKY C, DALVIT GC, PINTOS LN, THOMPSON JG, BECONI MT, CELTICA PD. 2007. Influence of hyaluronic acid synthesis and cumulus mucification on bovine oocyte in vitro maturation, fertilisation and embryo development. Reprod Fert Dev 19: 488-497.
HARDY K, HOOPER MA, HANDYSIDE AH, RUTHERFORD AJ, WINSTON RM, LEESE HJ. 1989. Non-invasive measurement of glucose and pyruvate uptake by individual human oocytes and preimplantation embryos. Hum Reprod 4: 188-91. Abst.
HARDY K, ROBINSON FM, PARASCHOS T, WICKS R, FRANKS S, WINSTON RM. 1995. Normal development and metabolic activity of preimplantation embryos in vitro from patients with polycystic ovaries. Hum Reprod 10: 2125-35.
HARRIS SE, ADRIAENS I, LEESE HJ, GOSDEN RG, PICTON HM. 2007. Carbohydrate metabolism by murine ovarian follicles and oocytes grown in vitro. Reproduction 134: 415-424.
HERRICK JR, BRAD AM, KRISHER RL. 2006. Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro. Reproduction 131: 289-298.
HUFANA-DURAN D, PEDRO PB, VENTURINA HV, HUFANA RD, SALAZAR AL, DURAN PG, RUZ LC. 2004. Post-warming hatching and birth of live calves following transfer of in vitro derived water buffalo (Bubalus bubalis) embryos. Theriogenology 61: 1429-39.
IWATA N, INAZU N, SATOH T. 1990 The purification and properties of aldose reductase from rat ovary. Arch Biochem and Biophysics 282: 70-77.
JOHNSON MT, FREEMAN EA, GARDNER DK, HUNT PA. 2007. Oxidative metabolism of pyruvate is required for meiotic maturation of murine oocytes in vivo. Biol Reprod 77: 2-8.
KANEKO T, IUCHI Y, TAKAHASHI M, FUJII J. 2003. Colocalization of polyolmetabolizing enzymes and immunological detection of fructated proteins in the female reproductive system of the rat. Histochem and Cell Biol 119: 309-315.
KOSUGI T, YUZAWA Y, SATO W, ARATA-KAWAI HA, SUZUKI N, KATO N, MATSUO S, KADOMATSU K. 2007. Midkine is involved in tubulointerstitial inflammation associated with diabetic nephropathy. Laboratory Invest 87: 903-913.
KRISHER RL, BAVISTER BD. 1998. Responses of oocytes and embryos to the culture environment. Theriogenology 49: 103-114.
LANE M, GARDNER DK. 1996. Selection of viable mouse blastocysts prior to transfer using a metabolic criterion. Hum Reprod 11: 1975-78.
LEE YM, LEE JO, JUNG JH, KIM JH, PARK SH, PARK JM, KIM EK, SUH PG, KIM HS. 2008. Retinoic Acid Leads to Cytoskeletal Rearrangement through AMPK-Rac1 and Stimulates Glucose Uptake through AMPK-p38 MAPK in Skeletal Muscle Cells. J of Biol Chem 283: 33969-74.
LEESE HJ, BARTON AM. 1985. Production of pyruvate by isolated mouse cumulus cells. J Exp Zool 234: 231-236.
LEESE HJ, HOOPER MA, EDWARD RG, ASHWOODSMITH MJ. 1986. Uptake of pyruvate by early human embryos determined by a non-invasive technique. Hum Reprod 1: 181-2.
NANSI S, KUMAR GV, MANJUNATHA BM, RAMESH HS, GUPTA PSP. 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.
NISHIMOTO H, MATSUTANI R, YAMAMOTO S, TAKAHASHI T, HAYASHI KG, MIYAMOTO A, HAMANO S, TETSUKA M. 2006. Gene expression of glucose transporter (GLUT) 1, 3 and 4 in bovine follicle and corpus luteum. J Endocrinol 188: 111-119.
PISANI LF, ANTONINI S, POCAR P, FERRARI S, BREVINI TA, RHIND SM, 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.
PREIS KA, SEIDEL GJ, GARDNER DK. 2005. Metabolic markers of developmental competence for in vitro matured mouse oocytes. Reproduction 130: 475-483.
ROSE-HELLEKANT TA, LIBERSKY-WILLIAMSON EA, BAVISTER BD. 1998. Energy substrates and amino acids provided during in vitro maturation of bovine oocytes alter acquisition of developmental competence. Zygote 6:285-294.
ROBERTS R, STARK J, IATROPOULOU A, BECKER DL, FRANKS S, 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 of Reprod 71: 199-209.
STEEVES TE, GARDNER DK. 1999. Metabolism of glucose, pyruvate, and glutamine during the maturation of oocytes derived from prepubertal and adult cows. Mol Reprod and Dev 54: 92-101.
SUTTON ML, CETICA PD, BECONI MT, KIND KL, GILCHRIST RB, THOMPSON JG. 2003. Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes. Reproduction 126: 27-34.
SUTTON-MCDOWALL ML, GILCHRIST RB, THOMPSON JG. 2010. The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 139: 685-695.
WASSARMAN PM. 1999. Zona pellucida glycoprotein mZP3: a versatile player during mammalian fertilization. J Reprod and Fert 116: 211-216.
WELLS L, WHALEN SA, HART GW. 2003. O-GlcNAc: a regulatory post-translational modification. Biochem and Biophy Res Comm 302: 435-441.
ZEILMAKER GH, VERHAMME CM. 1974. Observations on rat oocyte maturation in vitro: morphology and energy requirements. Biol Reprod 11: 145-152.
ZHAO FQ, KEATING AF. 2007. Functional Properties and Genomics of Glucose Transporters. Cur Genomics 8: 113-128.
ZHENG P, BAVISTER BD, JI W. 2001. Energy substrate requirement for in vitro maturation of oocytes from unstimulated adult rhesus monkeys. Mol Reprod Dev 58: 348-355.
ZHENG P, VASSENA R, LATHAM KE. 2007. Effects of in vitro oocyte maturation and embryo culture on the expression of glucose transporters, glucose metabolism and insulin signaling genes in rhesus monkey oocytes and preimplantation embryos. Mol Hum Reprod 13: 361-371.