Reproductive and Developmental Biology

  • 제37권2호
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  • Pages.65-73
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  • 2013
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  • 1738-2432(pISSN)
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  • 2288-0151(eISSN)
한국동물번식학회 (The Korean Society of Animal Reproduction)
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Hyperglycemia Influences Apoptosis and Autophagy in Porcine Parthenotes Developing In Vitro

  • Xu, Yong-Nan (Department of Animal Sciences, Chungbuk National University) ;
  • Li, Ying-Hua (Department of Animal Sciences, Chungbuk National University) ;
  • Lee, Sung Hyun (Department of Animal Sciences, Chungbuk National University) ;
  • Kwon, Jung-Woo (Department of Animal Sciences, Chungbuk National University) ;
  • Lee, Seul Ki (Department of Animal Sciences, Chungbuk National University) ;
  • Heo, Young-Tae (Department of Animal Sciences, Chungbuk National University) ;
  • Cui, Xiang-Shun (Department of Animal Sciences, Chungbuk National University) ;
  • Kim, Nam-Hyung (Department of Animal Sciences, Chungbuk National University)
  • 투고 : 2013.05.28
  • 심사 : 2013.06.06
  • 발행 : 2013.06.30
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초록

The objective of this study was to examine the effects of high concentrations of glucose on porcine parthenotes developing in vitro. Addition of 55 mM glucose to the culture medium of embryos at the four-cell-stage significantly inhibited blastocyst formation, resulting in fewer cells in blastocyst-stage embryos and increased levels of apoptosis and autophagy compared to control. Quantitative reverse transcriptase (RT) PCR analysis revealed that the expression of pro-apoptotic genes (Caspase 3, Bax and Bak) and autophagy genes (Atg6 and Atg8/Lc3) were increased significantly by the addition of 55 mM glucose to the culture medium compared to control. MitoTracker Green fluorescence revealed a decrease in the overall mitochondrial mass compared to control. However, the addition of 55 mM glucose had no effect on mRNA expression of the nuclear DNA-encoded mitochondrial-related genes, cytochrome oxidase (Cox) 5a, Cox5b and Cox6b1. These results suggest that hyperglycemia reduced the mitochondrial content of porcine embryos developing in vitro and that this may hinder embryonic development to the blastocyst stage and embryo quality by increasing apoptosis and autophagy in these embryos.

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참고문헌

  1. Adastra KL, Chi MM, Riley JK, Moley KH (2011): A differential autophagic response to hyperglycemia in the developing murine embryo. Reproduction 141:607- https://doi.org/10.1530/REP-10-0265
  2. Baehrecke EH (2005): Autophagy: dual roles in life and death? Nat Rev Mol Cell Biol 6:505-510. https://doi.org/10.1038/nrm1666
  3. Biggers JD, Stern S (1973): Metabolism of the preimplantation mammalian embryo. Adv Reprod Physiol 6:1-59.
  4. Chen Y, Gibson SB (2008): Is mitochondrial generation of reactive oxygen species a trigger for autophagy? Autophagy 4:246-248. https://doi.org/10.4161/auto.5432
  5. Cory S, Adams JM (1998): Matters of life and death: programmed cell death at Cold Spring Harbor. Biochim Biophys Acta 1377:R25-44.
  6. Cui XS, Li XY, Jeong YJ, Jun JH, Kim NH (2006): Gene expression of cox5a, 5b, or 6b1 and their roles in preimplantation mouse embryos. Biol Reprod 74: 601-610. https://doi.org/10.1095/biolreprod.105.045633
  7. De Hertogh R, Vanderheyden I, Pampfer S, Robin D, Dufrasne E, Delcourt J (1991): Stimulatory and inhibitory effects of glucose and insulin on rat blastocyst development in vitro. Diabetes 40:641-647. https://doi.org/10.2337/diab.40.5.641
  8. Diamond MP, Moley KH, Pellicer A, Vaughn WK, DeCherney AH (1989): Effects of streptozotocin- and alloxan- induced diabetes mellitus on mouse follicular and early embryo development. J Reprod Fertil 86:1-10. https://doi.org/10.1530/jrf.0.0860001
  9. Flood MR, Wiebold JL (1988): Glucose metabolism by preimplantation pig embryos. Journal of Reproduction and Fertility 84:7-12. https://doi.org/10.1530/jrf.0.0840007
  10. Fraser RB, Waite SL, Wood KA, Martin KL (2007): Impact of hyperglycemia on early embryo development and embryopathy: In vitro experiments using a mouse model. Human Reproduction 22:3059-3068. https://doi.org/10.1093/humrep/dem318
  11. Funahashi H, Kim NH, Stumpf TT, Cantley TC, Day BN (1996): Presence of organic osmolytes in maturation medium enhances cytoplasmic maturation of porcine oocytes. Biol Reprod 54:1412-1419. https://doi.org/10.1095/biolreprod54.6.1412
  12. Gandhi AP, Lane M, Gardner DK, Krisher RL (2001): Substrate utilization in porcine embryos cultured in NCSU23 and G1.2/G2.2 sequential culture media. Mol Reprod Dev 58:269-275. https://doi.org/10.1002/1098-2795(200103)58:3<269::AID-MRD4>3.0.CO;2-L
  13. Gardner DK, Lane M, Batt P (1993): Uptake and metabolism of pyruvate and glucose by individual sheep preattachment embryos developed in vivo. Mol Reprod Dev 36:313-319. https://doi.org/10.1002/mrd.1080360305
  14. Gardner DK, Leese HJ (1990): Concentrations of nutrients in mouse oviduct fluid and their effects on embryo development and metabolism in vitro. J Reprod Fertil 88:361-368. https://doi.org/10.1530/jrf.0.0880361
  15. Gardner DK, Leese HJ (1988): The role of glucose and pyruvate transport in regulating nutrient utilization by preimplantation mouse embryos. Development 104:423-429.
  16. Gozuacik D, Kimchi A (2004): Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23: 2891-2906. https://doi.org/10.1038/sj.onc.1207521
  17. Im GS, Lai L, Liu Z, Hao Y, Wax D, Bonk A, Prather RS (2004): In vitro development of preimplantation porcine nuclear transfer embryos cultured in different media and gas atmospheres. Theriogenology 61:1125-1135. https://doi.org/10.1016/j.theriogenology.2003.06.006
  18. Khurana NK, Niemann H (2000): Energy metabolism in preimplantation bovine embryos derived in vitro or in vivo. Biol Reprod 62:847-856. https://doi.org/10.1095/biolreprod62.4.847
  19. Kihara A, Noda T, Ishihara N, Ohsumi Y (2001): Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J Cell Biol 152:519- https://doi.org/10.1083/jcb.152.3.519
  20. Kikuchi K, Onishi A, Kashiwazaki N, Iwamoto M, Noguchi J, Kaneko H, Akita T, Nagai T (2002): Successful piglet production after transfer of blastocysts produced by a modified in vitro system. Biol Reprod 66:1033-1041. https://doi.org/10.1095/biolreprod66.4.1033
  21. Kim HS, Lee GS, Hyun SH, Lee SH, Nam DH, Jeong YW, Kim S, Kang SK, Lee BC, Hwang WS (2004): Improved in vitro development of porcine embryos with different energy substrates and serum. Theriogenology 61:1381-1393. https://doi.org/10.1016/j.theriogenology.2003.08.012
  22. Kirisako T, Ichimura Y, Okada H, Kabeya Y, Mizushima N, Yoshimori T, Ohsumi M, Takao T, Noda T, Ohsumi Y (2000): The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J Cell Biol 151:263-276. https://doi.org/10.1083/jcb.151.2.263
  23. Lee SJ, Cho KS, Koh JY (2009): Oxidative injury triggers autophagy in astrocytes: the role of endogenous zinc. Glia 57:1351-1361. https://doi.org/10.1002/glia.20854
  24. Leunda-Casi A, Genicot G, Donnay I, Pampfer S, De Hertogh R (2002): Increased cell death in mouse blastocysts exposed to high D-glucose in vitro: implications of an oxidative stress and alterations in glucose metabolism. Diabetologia 45:571-579. https://doi.org/10.1007/s00125-001-0752-y
  25. Livak KJ, Schmittgen TD (2001): Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) Method. Methods 25: 402-408. https://doi.org/10.1006/meth.2001.1262
  26. Martin KL, Leese HJ (1995): Role of glucose in mouse preimplantation embryo development. Mol Reprod Dev 40:436-443. https://doi.org/10.1002/mrd.1080400407
  27. Moley KH, Chi MM, Knudson CM, Korsmeyer SJ, Mueckler MM (1998): Hyperglycemia induces apoptosis in pre-implantation embryos through cell death effector pathways. Nat Med 4:1421-1424. https://doi.org/10.1038/4013
  28. Moley KH, Chi MM, Manchester JK, McDougal DB, Lowry OH (1996): Alterations of intraembryonic metabolites in preimplantation mouse embryos exposed to elevated concentrations of glucose: a metabolic explanation for the developmental retardation seen in preimplantation embryos from diabetic animals. Biol Reprod 54:1209-1216. https://doi.org/10.1095/biolreprod54.6.1209
  29. Moley KH (2001): Hyperglycemia and apoptosis: mechanisms for congenital malformations and pregnancy loss in diabetic women. Trends Endocrinol Metab 12: 78-82. https://doi.org/10.1016/S1043-2760(00)00341-6
  30. Noda T, Kim J, Huang WP, Baba M, Tokunaga C, Ohsumi Y, Klionsky DJ (2000): Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the Cvt and autophagy pathways. J Cell Biol 148:465-480. https://doi.org/10.1083/jcb.148.3.465
  31. Nutt LK, Gogvadze V, Uthaisang W, Mirnikjoo B, Mc- Conkey DJ, Orrenius S (2005): Indirect effects of Bax and Bak initiate the mitochondrial alterations that lead to cytochrome C release during arsenic trioxide-induced apoptosis. Cancer Biol Ther 4:459-467. https://doi.org/10.4161/cbt.4.4.1652
  32. Pampfer S, de Hertogh R, Vanderheyden I, Michiels B, Vercheval M (1990): Decreased inner cell mass proportion in blastocysts from diabetic rats. Diabetes 39: 471-476. https://doi.org/10.2337/diab.39.4.471
  33. Pampfer S, Vanderheyden I, McCracken JE, Vesela J, De Hertogh R (1997): Increased cell death in rat blastocysts exposed to maternal diabetes in utero and to high glucose or tumor necrosis factor-alpha in vitro. Development 124:4827-4836.
  34. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B (2005): Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122:927-939. https://doi.org/10.1016/j.cell.2005.07.002
  35. Petiot A, Ogier-Denis E, Blommaart EF, Meijer AJ, Codogno P (2000): Distinct classes of phosphatidylinositol 3'-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J Biol Chem 275:992-998. https://doi.org/10.1074/jbc.275.2.992
  36. Rieger D, Loskutoff NM, Betteridge KJ (1992): Developmentally related changes in the metabolism of glucose and glutamine by cattle embryos produced and co-cultured in vitro. J Reprod Fertil 95:585-595. https://doi.org/10.1530/jrf.0.0950585
  37. Suzuki K, Ohsumi Y (2007): Molecular machinery of autophagosome formation in yeast, Saccharomyces cerevisiae. FEBS Lett 581:2156-2161. https://doi.org/10.1016/j.febslet.2007.01.096
  38. Xie Z, Klionsky DJ (2007): Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9: 1102-1109. https://doi.org/10.1038/ncb1007-1102
  39. Yang MY, Rajamahendran R (2002): Expression of Bcl- 2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro. Anim Reprod Sci 70:159-169. https://doi.org/10.1016/S0378-4320(01)00186-5
  40. Yu L, Alva A, Su H, Dutt P, Freundt E, Welsh S, Baehrecke EH, Lenardo MJ (2004): Regulation of an ATG7- beclin 1 program of autophagic cell death by caspase-8. Science 304:1500-1502. https://doi.org/10.1126/science.1096645
  41. Yu T, Robotham JL, Yoon Y (2006): Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc Natl Acad Sci USA 103:2653-2658. https://doi.org/10.1073/pnas.0511154103
  42. Zhang H, Kong X, Kang J, Su J, Li Y, Zhong J, Sun L (2009): Oxidative stress induces parallel autophagy and mitochondria dysfunction in human glioma U251 cells. Toxicol Sci 110:376-388. https://doi.org/10.1093/toxsci/kfp101
  43. Zusman I, Ornoy A, Yaffe P, Shafrie E (1985): Effects of glucose and serum from streptozotocin-diabetic and nondiabetic rats on the in vitro development of preimplantation mouse embryos. Isr J Med Sci 21:359-