Journal of Embryo Transfer (한국수정란이식학회지)

The Korean Society of Embryo Transfer (한국수정란이식학회)
권호 표지
DOI QR코드

DOI QR Code

Ganglioside GD1a Activates the Phosphorylation of EGFR in Porcine Oocytes Maturation in vitro

  • Park, Hyo-Jin (Department of Biotechnology, College of Engineering, Daegu University) ;
  • Kim, Jin-Woo (Department of Biotechnology, College of Engineering, Daegu University) ;
  • Park, Jae-Young (Department of Biotechnology, College of Engineering, Daegu University) ;
  • Yang, Seul-Gi (Department of Biotechnology, College of Engineering, Daegu University) ;
  • Jung, Jae-Min (Department of Biotechnology, College of Engineering, Daegu University) ;
  • Kim, Min-Ji (Department of Biotechnology, College of Engineering, Daegu University) ;
  • Koo, Deog-Bon (Department of Biotechnology, College of Engineering, Daegu University)
  • Received : 2016.11.21
  • Accepted : 2017.03.15
  • Published : 2017.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Ganglioside GD1a is specifically formed by the addition of sialic acid to ganglioside GM1a by ST3 ${\beta}$-galactoside ${\alpha}$-2,3-sialyltransferase 2 (ST3GAL2). Above all, GD1a are known to be related with the functional regulation of several growth factor receptors, including activation and dimerization of epidermal growth factor receptor (EGFR) in tumor cells. The activity of EGF and EGFR is known to be a very important factor for meiotic and cytoplasmic maturation during in vitro maturation (IVM) of mammalian oocytes. However, the role of gangliosides GD1a for EGFR-related signaling pathways in porcine oocyte is not yet clearly understood. Here, we investigated that the effect of ST3GAL2 as synthesizing enzyme GD1a for EGFR activation and phosphorylation during meiotic maturation. To investigate the expression of ST3GAL2 according to the EGF treatment (0, 10 and 50 ng/ml), we observed the patterns of ST3GAL2 genes expression by immunofluorescence staining in denuded oocyte (DO) and cumulus cell-oocyte-complex (COC) during IVM process (22 and 44 h), respectively. Expression levels of ST3GAL2 significantly decreased (p<0.01) in an EGF concentration (10 and 50 ng/ml) dependent manner. And fluorescence expression of ST3GAL2 increased (p<0.01) in the matured COCs for 44 h. Under high EGF concentration (50 ng/ml), ST3GAL2 protein levels was decreased (p<0.01), and their shown opposite expression pattern of phosphorylation-EGFR in COCs of 44 h. Phosphorylation of EGFR significantly increased (p<0.01) in matured COCs treated with GD1a for 44 h. In addition, ST3GAL2 protein levels significantly decreased (p<0.01) in GD1a ($10{\mu}M$) treated COCs without reference to EGF pre-treatment. These results suggest that treatment of exogenous ganglioside GD1a may play an important role such as EGF in EGFR-related activation and phosphorylation in porcine oocyte maturation of in vitro.

Keywords

References

  1. Ben-Yosef D, Galiani D, Dekel N and Shalgi R. 1992. Rat oocytes induced to mature by epidermal growth factor are successfully fertilized. Mol. Cell Endocrinol. 88:135-141. https://doi.org/10.1016/0303-7207(92)90018-2
  2. Bornslaeger EA and Schultz RM. 1985. Regulation of mouse oocyte maturation: effect of elevating cumulus cell cAMP on oocyte cAMP levels. Biol. Reprod. 33:698-704. https://doi.org/10.1095/biolreprod33.3.698
  3. Choo YK, Chiba K, Tai T, Ogiso M and Hoshi M. 1995. Differential distribution of gangliosides in adult rat ovary during the oestrous cycle. Glycobiology 5:299-309. https://doi.org/10.1093/glycob/5.3.299
  4. Choo YK. 1999. Distribution of ganglioside GM3 in the rat ovary after gonadotropin stimulation. Mol. Cells. 31;9(4): 365-375.
  5. Conti M, Hsieh M, Park JY and Su YQ. 2005. Role of the epidermal growth factor network in ovarian follicles. Mol. Endocrinol. 20:715-723.
  6. De La Fuente R, O'Brien MJ and Eppig JJ. 1999. Epidermal growth factor enhances preimplantation developmental competence of maturing mouse oocytes. Hum. Reprod. 14:3060-3068. https://doi.org/10.1093/humrep/14.12.3060
  7. Kwak DH, Seo BB, Chang KT and Choo YK. 2011. Roles of gangliosides in mouse embryogenesis and embryonic stem cell differentiation. Exp. Mol. Med. 31; 43(7): 379-388. https://doi.org/10.3858/emm.2011.43.7.048
  8. Edry I, Sela-Abramovich S and Dekel N. 2006. Meiotic arrest of oocytes depends on cell-to-cell communication in the ovarian follicle. Mol. Cell Endocrinol. 27;252(1-2):102-106. https://doi.org/10.1016/j.mce.2006.03.009
  9. Goud PT, Goud AP, Qian C, Laverge H, Van der Elst J, De Sutter P and Dhont M. 1998. In-vitro maturation of human germinal vesicle stage oocytes: role of cumulus cells and epidermal growth factor in the culture medium. Hum. Reprod. 13:1638-1644. https://doi.org/10.1093/humrep/13.6.1638
  10. Hsieh M, Lee D, Panigone S, Horner K, Chen R, Theologis A, Lee DC, Threadgill DW and Conti M. 2007. Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation. Mol. Cell Biol. 27:1914-1924. https://doi.org/10.1128/MCB.01919-06
  11. Hwang SU, Jeon Y, Yoon JD, Cai L, Kim E, Yoo H, Kim KJ, Park KM, Jin M, Kim H and Hyun SH. 2015.Effect of ganglioside GT1b on the in vitro maturation of porcine oocytes and embryonic development. J. Reprod. Dev. 61: 549-557. https://doi.org/10.1262/jrd.2015-049
  12. Illera MJ, Lorenzo PL, Illera JC and Petters RM. 1998. Developmental competence of immature pig oocytes under the influence of EGF, IGF-I, follicular fluid and gonadotropins during IVM-IVF processes. Int. J. Dev. Biol. 42:1169-1172.
  13. Jamnongjit M, Gill A and Hammes SR. 2005. Epidermal growth factor receptor signaling is required for normal ovarian steroidogenesis and oocyte maturation. Proc. Natl. Acad. Sci. U.S.A. 8;102(45):16257-16262. https://doi.org/10.1073/pnas.0508521102
  14. Julien S, Bobowski M, Steenackers A, Le Bourhis X and Delannoy P. 2013. How Do Gangliosides Regulate RTKs Signaling?. Cells 2:751-767. https://doi.org/10.3390/cells2040751
  15. Kim SM, Kwak DH, Kim SM, Jung JU, Lee DH, Lee S, Jung KY, Do SI and Choo YK. 2006. Differential expression of gangliosides in the ovary and uterus of streptozotocin-induced and db/db diabetic mice. Arch. Pharm. Res. 29:666-676. https://doi.org/10.1007/BF02968251
  16. Kim JW, Park HJ, Chae SK, Ahn JH, Do GY, Choo YK, Park JJ, Jung BD, Kim SU, Chang KT and Koo DB. 2016. Ganglioside GD1a promotes oocyte maturation, furthers preimplantation development, and increases blastocyst quality in pigs. J. Reprod. Dev. 62:249-255. https://doi.org/10.1262/jrd.2015-083
  17. Kwak DH, Seo BB, Chang KT and Choo YK. 2011. Roles of gangliosides in mouse embryogenesis and embryonic stem cell differentiation. Exp. Mol. Med. 31; 43(7): 379-388. https://doi.org/10.3858/emm.2011.43.7.048
  18. Lee E, Min SH, Song BS, Yeon JY, Kim JW, Bae JH, Park SY, Lee YH, Kim SU, Lee DS, Chang KT and Koo DB. 2015. Exogenous $\gamma$-tocotrienol promotes preimplantation development and improves the quality of porcine embryos. Reprod. Fertil. Dev. 27:481-490. https://doi.org/10.1071/RD13167
  19. Li R, Liu Y and Ladisch S. 2001. Enhancement of epidermal growth factor signaling and activation of SRC kinase by gangliosides. J. Biol. Chem. 276: 42782-42792. https://doi.org/10.1074/jbc.M101481200
  20. Liu Y, Li R and Ladisch S. 2004. Exogenous ganglioside GD1a enhances epidermal growth factor receptor binding and dimerization. J. Biol. Chem. 27;279(35):36481-36489. https://doi.org/10.1074/jbc.M402880200
  21. Lloyd KO and Furukawa K. 1998. Biosynthesis and functions of gangliosides: recent advances. Glycoconj. J. 15: 627-636. https://doi.org/10.1023/A:1006924128550
  22. Lonergan P, Carolan C, Van Langendonckt A, Donnay I, Khatir H and Mermillod P. 1996. Role of epidermal growth factor in bovine oocyte maturation and preimplantation embryo development in vitro. Biol. Reprod. 54:1420-1429. https://doi.org/10.1095/biolreprod54.6.1420
  23. Sandhoff K and Harzer K. 2013. Gangliosides and gangliosidoses: principles of molecular and metabolic pathogenesis. J. Neurosci. 33: 10195-10208. https://doi.org/10.1523/JNEUROSCI.0822-13.2013
  24. Sela-Abramovich S, Chorev E, Galiani D and Dekel N. 2005. Mitogen-activated protein kinase mediates luteinizing hormone-induced breakdown of communication and oocyte maturation in rat ovarian follicles. Endocrinology 146: 1236-1244. https://doi.org/10.1210/en.2004-1006
  25. Sturgill ER, Aoki K, Lopez PH, Colacurcio D, Vajn K, Lorenzini I, Majic S, Yang WH, Heffer M, Tiemeyer M, Marth JD and Schnaar RL. 2012. Biosynthesis of the major brain gangliosides GD1a and GT1b. Glycobiology 22:1289-1301. https://doi.org/10.1093/glycob/cws103
  26. Yang HJ, Jung KY, Kwak DH, Lee SH, Ryu JS, Kim JS, Chang KT, Lee JW and Choo YK. 2011. Inhibition of ganglioside GD1a synthesis suppresses the differentiation of human mesenchymal stem cells into osteoblasts. Dev. Growth Differ. 53:323-332. https://doi.org/10.1111/j.1440-169X.2010.01240.x
  27. Zhang L, Wang Y, Wang L, Cao T, Hyuga S, Sato T, Wu Y, Yamagata S and Yamagata T. 2011. Ganglioside GD1a negatively regulates hepatocyte growth factor expression through caveolin-1 at the transcriptional level in murine osteosarcoma cells. Biochim. Biophys. Acta. 1810:759-768. https://doi.org/10.1016/j.bbagen.2011.04.006