Clinical and Experimental Reproductive Medicine

The Korean Society for Reproductive Medicine (대한생식의학회)
권호 표지
DOI QR코드

DOI QR Code

Function of the pentose phosphate pathway and its key enzyme, transketolase, in the regulation of the meiotic cell cycle in oocytes

  • Kim, Yunna (Department of Biomedical Science, College of Life Science, CHA University) ;
  • Kim, Eun-Young (Department of Biomedical Science, College of Life Science, CHA University) ;
  • Seo, You-Mi (Department of Biomedical Science, College of Life Science, CHA University) ;
  • Yoon, Tae Ki (CHA Research Institute, Fertility Center, CHA General Hospital) ;
  • Lee, Woo-Sik (CHA Research Institute, Fertility Center, CHA General Hospital) ;
  • Lee, Kyung-Ah (Department of Biomedical Science, College of Life Science, CHA University)
  • Received : 2012.06.04
  • Accepted : 2012.06.16
  • Published : 2012.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: Previously, we identified that transketolase (Tkt), an important enzyme in the pentose phosphate pathway, is highly expressed at 2 hours of spontaneous maturation in oocytes. Therefore, this study was performed to determine the function of Tkt in meiotic cell cycle regulation, especially at the point of germinal vesicle breakdown (GVBD). Methods: We evaluated the loss-of-function of Tkt by microinjecting Tkt double-stranded RNAs (dsRNAs) into germinal vesicle-stage oocytes, and the oocytes were cultured in vitro to evaluate phenotypic changes during oocyte maturation. In addition to maturation rates, meiotic spindle and chromosome rearrangements, and changes in expression of other enzymes in the pentose phosphate pathway were determined after Tkt RNA interference (RNAi). Results: Despite the complete and specific knockdown of Tkt expression, GVBD occurred and meiosis was arrested at the metaphase I (MI) stage. The arrested oocytes exhibited spindle loss, chromosomal aggregation, and declined maturation promoting factor and mitogen-activated protein kinase activities. The modified expression of two enzymes in the pentose phosphate pathway, Prps1 and Rbks, after Tkt RNAi and decreased maturation rates were amended when ribose-5-phosphate was supplemented in the culture medium, suggesting that the Tkt and pentose phosphate pathway are important for the maturation process. Conclusion: We concluded that Tkt and its associated pentose phosphate pathway play an important role in the MI-MII transition of the oocytes' meiotic cell cycle, but not in the process of GVBD.

Keywords

Acknowledgement

Supported by : Ministry for Health, Welfare & Family Affair, NRF

References

  1. Pincus G, Enzmann EV. The comparative behavior of mammalian dggs in vivo and in vitro: I. the activation of ovarian eggs. J Exp Med 1935;62:665-75.
  2. Schmitt A, Nebreda AR. Signalling pathways in oocyte meiotic maturation. J Cell Sci 2002;115:2457-9.
  3. Comizzoli P, Urner F, Sakkas D, Renard JP. Up-regulation of glucose metabolism during male pronucleus formation determines the early onset of the s phase in bovine zygotes. Biol Reprod 2003;68:1934-40.
  4. Downs SM, Humpherson PG, Leese HJ. Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway. Biol Reprod 1998;58:1084-94.
  5. Urner F, Sakkas D. Involvement of the pentose phosphate pathway and redox regulation in fertilization in the mouse. Mol Reprod Dev 2005;70:494-503.
  6. Salamon C, Chervenak M, Piatigorsky J, Sax CM. The mouse transketolase (TKT) gene: cloning, characterization, and functional promoter analysis. Genomics 1998;48:209-20.
  7. Colton SA, Humpherson PG, Leese HJ, Downs SM. Physiological changes in oocyte-cumulus cell complexes from diabetic mice that potentially influence meiotic regulation. Biol Reprod 2003;69:761-70.
  8. Cho WK, Stern S, Biggers JD. Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J Exp Zool 1974;187:383-6.
  9. Downs SM. Involvement of purine nucleotide synthetic pathways in gonadotropin-induced meiotic maturation in mouse cumulus cell-enclosed oocytes. Mol Reprod Dev 1997;46:155-67.
  10. Kim KH, Kim EY, Lee KA. SEBOX is essential for early embryogenesis at the two-cell stage in the mouse. Biol Reprod 2008;79:1192-201.
  11. Cascante M, Centelles JJ, Veech RL, Lee WN, Boros LG. Role of thiamin (vitamin B-1) and transketolase in tumor cell proliferation. Nutr Cancer 2000;36:150-4.
  12. Hammes HP, Du X, Edelstein D, Taguchi T, Matsumura T, Ju Q, et al. Benfotiamine blocks three major pathways of hyperglycemic damage and prevents experimental diabetic retinopathy. Nat Med 2003;9:294-9.
  13. Paoletti F, Mocali A, Tombaccini D. Cysteine proteinases are responsible for characteristic transketolase alterations in Alzheimer fibroblasts. J Cell Physiol 1997;172:63-8.
  14. Sax CM, Salamon C, Kays WT, Guo J, Yu FX, Cuthbertson RA, et al. Transketolase is a major protein in the mouse cornea. J Biol Chem 1996;271:33568-74.
  15. Xu ZP, Wawrousek EF, Piatigorsky J. Transketolase haploinsufficiency reduces adipose tissue and female fertility in mice. Mol Cell Biol 2002;22:6142-7.
  16. Herrick JR, Brad AM, Krisher RL. Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro. Reproduction 2006;131:289-98.
  17. Maro B, Johnson MH, Pickering SJ, Flach G. Changes in actin distribution during fertilization of the mouse egg. J Embryol Exp Morphol 1984;81:211-37.
  18. Verlhac MH, Kubiak JZ, Clarke HJ, Maro B. Microtubule and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development 1994;120:1017-25.
  19. Han SJ, Chen R, Paronetto MP, Conti M. Wee1B is an oocyte-specific kinase involved in the control of meiotic arrest in the mouse. Curr Biol 2005;15:1670-6.
  20. Lincoln AJ, Wickramasinghe D, Stein P, Schultz RM, Palko ME, De Miguel MP, et al. Cdc25b phosphatase is required for resumption of meiosis during oocyte maturation. Nat Genet 2002;30:446-9.
  21. Schultz RM, Montgomery RR, Belanoff JR. Regulation of mouse oocyte meiotic maturation: implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis. Dev Biol 1983;97:264-73.
  22. Kanatsu-Shinohara M, Schultz RM, Kopf GS. Acquisition of meiotic competence in mouse oocytes: absolute amounts of p34(cdc2), cyclin B1, cdc25C, and wee1 in meiotically incompetent and competent oocytes. Biol Reprod 2000;63:1610-6.
  23. Mitra J, Schultz RM. Regulation of the acquisition of meiotic competence in the mouse: changes in the subcellular localization of cdc2, cyclin B1, cdc25C and wee1, and in the concentration ofthese proteins and their transcripts. J Cell Sci 1996;109:2407-15.
  24. Verlhac MH, de Pennart H, Maro B, Cobb MH, Clarke HJ. MAP kinase becomes stably activated at metaphase and is associated with microtubule-organizing centers during meiotic maturation of mouse oocytes. Dev Biol 1993;158:330-40.
  25. Brunet S, Maro B. Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction 2005;130:801-11.
  26. Abrieu A, Dorée M, Fisher D. The interplay between cyclin-B-Cdc2 kinase (MPF) and MAP kinase during maturation of oocytes. J Cell Sci 2001;114:257-67.
  27. Yoon SJ, Koo DB, Park JS, Choi KH, Han YM, Lee KA. Role of cytosolic malate dehydrogenase in oocyte maturation and embryo development. Fertil Steril 2006;86:1129-36.
  28. Kim EY, Kim KH, Kim YS, Lee HS, Kim Y, Lee KA. Comparative functional analysis of the malate dehydrogenase (Mor2) during in vitro maturation of the mouse and porcine oocytes. Dev Reprod 2007;11:263-72.

Cited by

  1. RNA Polymerase II Inhibitor, ${\alpha}$-Amanitin, Affects Gene Expression for Gap Junctions and Metabolic Capabilities of Cumulus Cells, but Not Oocyte, during In Vitro Mouse Oocyte Maturation vol.17, pp.1, 2013, https://doi.org/10.12717/dr.2013.17.1.063
  2. Pentose Phosphate Pathway in Disease and Therapy vol.995, pp.None, 2012, https://doi.org/10.4028/www.scientific.net/amr.995.1
  3. Nutrient pathways regulating the nuclear maturation of mammalian oocytes vol.27, pp.4, 2012, https://doi.org/10.1071/rd14343
  4. Proteomics reveals reduced expression of transketolase in pyrimidine 5′‐nucleotidase deficient patients vol.10, pp.8, 2012, https://doi.org/10.1002/prca.201500130
  5. The Role of Glucose Metabolism on Porcine Oocyte Cytoplasmic Maturation and Its Possible Mechanisms vol.11, pp.12, 2012, https://doi.org/10.1371/journal.pone.0168329
  6. Genome-wide association study provides strong evidence of genes affecting the reproductive performance of Nellore beef cows vol.12, pp.5, 2012, https://doi.org/10.1371/journal.pone.0178551
  7. D -Ribose as a Contributor to Glycated Haemoglobin vol.25, pp.None, 2012, https://doi.org/10.1016/j.ebiom.2017.10.001
  8. GWAS on prolonged gestation (post-term birth): analysis of successive Finnish birth cohorts vol.55, pp.1, 2018, https://doi.org/10.1136/jmedgenet-2017-104880
  9. B Vitamins Can Reduce Body Weight Gain by Increasing Metabolism-related Enzyme Activities in Rats Fed on a High-Fat Diet vol.38, pp.1, 2018, https://doi.org/10.1007/s11596-018-1862-9
  10. Knockdown of PRKAR2B Results in the Failure of Oocyte Maturation vol.45, pp.5, 2012, https://doi.org/10.1159/000487978
  11. D-ribose is elevated in T1DM patients and can be involved in the onset of encephalopathy vol.11, pp.14, 2012, https://doi.org/10.18632/aging.102089
  12. Cells grown in three-dimensional spheroids mirror in vivo metabolic response of epithelial cells vol.3, pp.1, 2012, https://doi.org/10.1038/s42003-020-0973-6
  13. Molecular and Biochemical Pathways of Catalpol in Alleviating Diabetes Mellitus and Its Complications vol.11, pp.2, 2021, https://doi.org/10.3390/biom11020323
  14. In Vitro and In Vivo Antidiabetic Potential of Monoterpenoids: An Update vol.27, pp.1, 2022, https://doi.org/10.3390/molecules27010182