DOI QR코드

DOI QR Code

Effect of Glycosaminoglycans on In vitro Fertilizing Ability and In vitro Developmental Potential of Bovine Embryos

  • Kim, Eun Young (Mirae Biotech/Jeju National University Stem Cell Research Center) ;
  • Noh, Eun Hyung (College of Applied Life Sciences, Jeju National University) ;
  • Noh, Eun Ji (College of Applied Life Sciences, Jeju National University) ;
  • Park, Min Jee (College of Applied Life Sciences, Jeju National University) ;
  • Park, Hyo Young (Mirae Biotech/Jeju National University Stem Cell Research Center) ;
  • Lee, Dong Sun (College of Applied Life Sciences, Jeju National University) ;
  • Riu, Key Zung (College of Applied Life Sciences, Jeju National University) ;
  • Park, Se Pill (College of Applied Life Sciences, Jeju National University)
  • Received : 2012.07.30
  • Accepted : 2012.10.12
  • Published : 2013.02.01

Abstract

The glycosaminoglycans (GAGs) present in the female reproductive tract promote sperm capacitation. When bovine sperm were exposed to 10 ${\mu}g/ml$ of one of four GAGs (Chondroitin sulfate, CS; Dermatan sulfate, DS; Hyaluronic acid, HA; Heparin, HP) for 5 h, the total motility (TM), straight-line velocity (VSL), and curvilinear velocity (VCL) were higher in the HP- or HA-treated sperm, relative to control and CS- or DS-treated sperm. HP and HA treatments increased the levels of capacitated and acrosome-reacted sperm over time, compared to other treatment groups (p<0.05). In addition, sperm exposed to HP or HA for 1 h before IVF exhibited significantly improved fertilizing ability, as assessed by 2 pronucleus (PN) formation and cleavage rates at d 2. Exposure to these GAGs also enhanced in vitro embryo development rates and embryo quality, and increased the ICM and total blastocyst cell numbers at d 8 after IVF (p<0.05). A real-time PCR analysis showed that the expression levels of pluripotency (Oct 4), cell growth (Glut 5), and anti-apoptosis (Bax inhibitor) genes were significantly higher in embryos derived from HA- or HP-treated sperm than in control or other treatment groups, while pro-apoptotic gene expression (caspase-3) was significantly lower in all GAG treatment groups (p<0.05). These results demonstrated that exposure of bovine sperm to HP or HA positively correlates with in vitro fertilizing ability, in vitro embryo developmental potential, and embryonic gene expression.

Keywords

References

  1. Anderson, S. H. and G. J. Killian. 1994. Effect of macromolecules from oviductal conditioned medium on bovine sperm motion and capacitation. Biol. Reprod. 51:795-799. https://doi.org/10.1095/biolreprod51.4.795
  2. Balaban, B ., B. Urman , A. Isiklar , C. Alatas , S. Aksoy , R. Mercan , A. Mumcu and A. Nuhoglu. 2001. The effect of pronuclear morphology on embryo quality parameters and blastocyst transfer outcome. Hum. Reprod. 16:2357-2361.
  3. Bergqvist, A. S., J. Ballester, A. Johannisson, N. Lundeheim and H. Rodriguez-Martinez. 2007. Heparin and dermatan sulphate induced capacitation of frozen-thawed bull spermatozoa measured by merocyanine-540. Zygote 15:225-232. https://doi.org/10.1017/S0967199407004182
  4. Berqqvist, A. S., J. Ballester, A. Johannisson, M. Hemandez, N. Lundeheim and H. Rodriuez-Martinez. 2006. In vitro capacitation of bull spermatozoa by oviductal fluid and its components. Zygote 14:259-273. https://doi.org/10.1017/S0967199406003777
  5. Borg, N. and M. Holland. 2008. The effect of glycosaminoglycans on rat gametes in vitro and the associated signal pathway. Reproduction 135:311-319. https://doi.org/10.1530/REP-07-0267
  6. Choi, B. S., T. K. Kim and C. Hyun. 2011. Chromatin assays for DNA fragmentation evaluation in canine sperm. J. Anim. Vet. Adv. 10:1501-1503. https://doi.org/10.3923/javaa.2011.1501.1503
  7. Dasgupta, S., C. L. Mills and L. R. Fraser. 1993. $Ca^{2+}$ related changes in the capacitation state of human spermatozoa assessed by a chlortetracycline fluorescence assay. J. Reprod. Fertil. 99:135-143. https://doi.org/10.1530/jrf.0.0990135
  8. Dora, G. D., E. M. Patricia and O. C. Marcelo. 2006. Effect of heparin on in vitro capacitation of boar sperm. Biol. Res. 39:631-639.
  9. Fraser, L. R., L. R. Abeydera and K. Niwa. 1995. $Ca^{2+}$ regulating mechanisms that modulate bull sperm capacitation and acrosomal exocytosis as determined by chlortetracycline analysis. Mol. Reprod. Dev. 40:233-241. https://doi.org/10.1002/mrd.1080400213
  10. Fukui, Y., T. Sonoyama, H. Mochizuki and H. Ono. 1990. Effects of heparin dosage and sperm capacitation time on in vitro fertilization and cleavage of bovine oocytes matured in vitro. Theriogenology 34:579-591. https://doi.org/10.1016/0093-691X(90)90013-J
  11. Goncalves, F. S., L. S. Barretto, R. P. Arruda, S. H. Perri and G. Z. Mingoti. 2010. Effect of antioxidants during bovine in vitro fertilization procedures on spermatozoa and embryo development. Reprod. Domest. Anim. 45:129-135. https://doi.org/10.1111/j.1439-0531.2008.01272.x
  12. Hamamah, S., C. Wittemer, C. Barthelemy, C. Richet, F. Zerimech, D. Royere and P. Degand. 1996. Identification of hyaluronic acid and chondroitin sulfates in human follicular fluid and their effects on human sperm motility and the outcome of in vitro fertilization. Reprod. Nutr. Dev. 36:43-52. https://doi.org/10.1051/rnd:19960104
  13. Handrow, R. R., R. W. Lenz and R. L. Ax. 1982. Structural comparisons among glycosaminoglycans to promote an acrosome reaction in bovine spermatozoa. Biochem. Biophys. Res. Commun. 107:1326-1332. https://doi.org/10.1016/S0006-291X(82)80143-5
  14. Hileman, R. E., J. R. Fromm, J. M. Wiler and R. J. Linhardt. 1998. Glycosaminoglycan-protein interactions: definition of consensus site in glycosaminoglycan binding proteins. Bioessays 20:156-167. https://doi.org/10.1002/(SICI)1521-1878(199802)20:2<156::AID-BIES8>3.0.CO;2-R
  15. Kano, K., T. Miyano and S. Kato. 1998. Effects of glycosaminoglycans on the development of in vitro-matured and fertilized porcine oocytes to the blastocyst stage in vitro. Biol. Reprod. 58:1226-1232. https://doi.org/10.1095/biolreprod58.5.1226
  16. Kato, Y. and Y. Nagao. 2009. Effect of PVP on sperm capacitation status and embryonic development in cattle. Theriogenology 72:624-635. https://doi.org/10.1016/j.theriogenology.2009.04.018
  17. Kuroda, K., M. Fukushima and H. Harayama. 2007. Premature capacitation of frozen-thawed spermatozoa from subfertile Japanese black cattle. J. Reprod. Dev. 53:1079-1086. https://doi.org/10.1262/jrd.19031
  18. Kurosaka, S., S. Eckardt and K. J. Mclaughlin. 2004. Pluripotent lineage definition in bovine embryo by Oct4 transcript localization. Biol. Reprod. 71:1578-1582. https://doi.org/10.1095/biolreprod.104.029322
  19. Lane, M. E., I. Therien, R. Moreau and P. Manjunath. 1999. Heparin and high-density lipoprotein mediate bovine sperm capacitation by different mechanisms. Biol. Reprod. 60:169-175. https://doi.org/10.1095/biolreprod60.1.169
  20. Lenz, R. W., J. L. Martin, M. E. Bellin and R. L. Ax. 1988. Predicting fertility of dairy bulls by inducing acrosome reactions in sperm with chondroitin sulfates. J. Dairy Sci. 71:1073-1077. https://doi.org/10.3168/jds.S0022-0302(88)79654-X
  21. Livak, K. J. and T. D. Schmittgen. 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
  22. Lu, K. H. and G. E. Jr. Seidel. 2004. Effects of heparin and sperm concentration on cleavage and blastocyst development rates of bovine oocytes inseminated with flow cytometrically- sorted sperm. Theriogenology 62:819-830. https://doi.org/10.1016/j.theriogenology.2003.12.029
  23. Mahmoud, A. I. and J. J. Parrish. 1996. Oviductal fluid and heparin induce similar surface changes in bovine sperm during capacitation: a flow cytometric study using lectins. Mol. Reprod. Dev. 43:554-560. https://doi.org/10.1002/(SICI)1098-2795(199604)43:4<554::AID-MRD19>3.0.CO;2-Z
  24. Miller, D. J., M. A. Winer and R. L. Ax. 1990. Heparin-binding proteins from seminal plasma bind to bovine spermatozoa and modulate capacitation by heparin. Biol. Reprod. 42:899-915. https://doi.org/10.1095/biolreprod42.6.899
  25. Parrish, J. J., J. L. Susko-Parrish and N. L. First. 1985. Effect of heparin and chondroitin sulfate on the acrosome reaction and fertility of bovine sperm in vitro. Theriogenology 24:537-549. https://doi.org/10.1016/0093-691X(85)90060-3
  26. Parrish, J. J., J. Susko-Parrish, M. A. Winer and N. L. First. 1988. Capacitation of bovine sperm by heparin. Biol. Reprod. 38:1171-1180. https://doi.org/10.1095/biolreprod38.5.1171
  27. Parrish, J. J., J Susko-Parrish, R, R. Handrow, R. L. Ax and N. L. First. 1989. Effect of sulfated glycoconjugates on capacitation and the acrosome reaction of bovine and hamster spermatozoa. Gamete. Res. 24:403-413. https://doi.org/10.1002/mrd.1120240407
  28. Parrish, J. J., J. Susko-Parrish, C. Uguz and N. L. First. 1994. Differences in the role of cyclic adenosine 3, 5-monophosphate during capacitation of bovine sperm by heparin or oviduct fluid. Biol. Reprod. 51:1099-1108. https://doi.org/10.1095/biolreprod51.6.1099
  29. Purdy, P. H. and J. K. Graham. 2004. Effect of adding cholesterol to bull sperm membranes on sperm capacitation, the acrosome reaction, and fertility. Biol. Reprod. 71:522-527. https://doi.org/10.1095/biolreprod.103.025577
  30. Rehman, N., A. R. Collins, T. K. Suh and R. W. Jr. Wright. 1994. Effect of sperm exposure time on in vitro fertilization and embryo development of bovine oocytes matured in vitro. Theriogenology 41:1447-1452. https://doi.org/10.1016/0093-691X(94)90195-O
  31. Rizos, D., A. A. Gutierrez, G. S. Perez, J. De La Fuente, M. P. Boland and P. Lonergan. 2003. Bovine embryo culture in the presence or absence of serum: Implications for blastocyst development, cryotolerance, and messenger RNA expression. Biol. Reprod. 68:236-243.
  32. Rodriguez-Almeida, F. A., M. Cuadras, A. Anchondo, S. Romo-Garcia and B. E. Sanchez. 2005. Heparin level effect on sperm capacitation of fresh and frozen-thawed bovine semen. In: Proceedings of the 2005 American Society of Animal Science Western Section, New Mexico State University, Las Cruces. p. 56.
  33. Slotte, H., E. Akerlof and A. Pousette. 1993. Separation of human spermatozoa with hyaluronic acid induces, and Percoll inhibits, the acrosome reaction. Int. J. Androl. 16:349-354. https://doi.org/10.1111/j.1365-2605.1993.tb01361.x
  34. Sostaric, E., H. A. Chris, B. Colenbrander and B. M. Gadella. 2005. Dynamics of carbohydrate affinities at the cell surface of capacitating bovine sperm cells. Biol. Reprod. 72:346-357. https://doi.org/10.1095/biolreprod.104.029330
  35. Therien, I., S. Soubeyrand and P. Manjunath. 1997. Major proteins of bovine seminal plasma modulate sperm capacitation by high-density lipoprotein. Biol. Reprod. 57:1080-1088. https://doi.org/10.1095/biolreprod57.5.1080
  36. Therien, I. and P. Manjunath. 2003. Effect of progesterone on bovine sperm capacitation and acrosome reaction. Biol. Reprod. 69:1408-1415. https://doi.org/10.1095/biolreprod.103.017855
  37. Thouas, G. A., N. A. Korfiatis, A. J. French, G. M. Jones and A. O. Trounson. 2001. Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod. Biomed. Online 3:25-29. https://doi.org/10.1016/S1472-6483(10)61960-8
  38. Tienthai, P., A, Johannisson and M. H. Rodriguez. 2004. Sperm capacitation in the porcine oviduct. Anim. Reprod. Sci. 80:131-146. https://doi.org/10.1016/S0378-4320(03)00134-9
  39. Towhidi, A., Y. H. Meharabani, J. M. Daliri, A. Ranjbar and M. Zhandi. 2009. Effect of plasmin and heparin on in vitro ovine sperm-oocyte interaction. Afr. J. Biotechnol. 8:3677-3681.
  40. Ward, C. R. and B. T. Storey. 1984. Determination of the time course of capacitation in mouse spermatozoa using a chlortetracycline assay. Dev. Biol. 104:287-296. https://doi.org/10.1016/0012-1606(84)90084-8
  41. Way, A. L. and G. J. Killian. 2006. Sperm binding, in vitro fertilization and in vitro embryonic development of bovine oocytes fertilized with spermatozoa incubated with norepinephrine. Anim. Reprod. Sci. 96:1-9. https://doi.org/10.1016/j.anireprosci.2005.10.006
  42. Yanagimachi, R. 1994. Mammalian fertilization. In: The Physiology of Reproduction (Ed. E. Knobil and J. D. Neill). Eds New York: Raven Press. 189-131.

Cited by

  1. Post-Death Cloning of Endangered Jeju Black Cattle (Korean Native Cattle): Fertility and Serum Chemistry in a Cloned Bull and Cow and Their Offspring vol.59, pp.6, 2013, https://doi.org/10.1262/jrd.2013-047
  2. Bovine sperm cell motility after incubation in follicular fluid vol.53, pp.7, 2018, https://doi.org/10.1590/s0100-204x2018000700011
  3. Changes in fertilization medium viscosity using hyaluronic acid impact bull sperm motility and acrosome status vol.55, pp.8, 2013, https://doi.org/10.1111/rda.13739