Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-27T08:48:14.908Z Has data issue: false hasContentIssue false
  • English
  • Français

Heparin effect on in vitro nuclear maturation of bovine oocytes

Published online by Cambridge University Press:  01 February 2008

Juan Carlos Flores-Alonso ,
Leticia Lezama-Monfil ,
María Luisa Sánchez-Vázquez ,
Rosalina Reyes  and
Néstor M. Delgado
Juan Carlos Flores-Alonso
Affiliation:
Biology of Reproduction Laboratory, East Biomedical Research Center, General Zone Hospital #5, Mexican Institute of Social Security, Puebla, Mexico
Leticia Lezama-Monfil
Affiliation:
Biology of Reproduction Laboratory, East Biomedical Research Center, General Zone Hospital #5, Mexican Institute of Social Security, Puebla, Mexico
María Luisa Sánchez-Vázquez
Affiliation:
Biology of Reproduction Laboratory, East Biomedical Research Center, General Zone Hospital #5, Mexican Institute of Social Security, Puebla, Mexico
Rosalina Reyes
Affiliation:
Biology of Reproduction Laboratory, East Biomedical Research Center, General Zone Hospital #5, Mexican Institute of Social Security, Puebla, Mexico
Néstor M. Delgado*
Affiliation:
Biology of Reproduction Laboratory, East Biomedical Research Center, General Zone Hospital #5, Mexican Institute of Social Security, Puebla, Mexico
*
†All correspondence to: Juan Carlos Flores-Alonso, Biology of Reproduction Laboratory, East Biomedical Research Center, Benito Juárez 1915 Colonia Guadalupe Victoria. C. P. 74280. Atlixco, Puebla, Mexico. Tel: +244 44 401 22 or +244 447 20 46; Fax: +222 2 36 35 27; e-mail: jcarfa@prodigy.net.mx
Get access Rights & Permissions [Opens in a new window]

Summary

Oocytes undergo numerous biochemical and morphological changes during their development from preantral to preovulatory phases. In vitro studies have suggested several compounds that might induce oocyte maturation. Heparin is a natural component of ooplasm, follicular fluid and uterine fluid and previous studies indicated that it might act as a chromatin maturation factor in bovine oocytes. We tested this hypothesis in vitro by timing germinal vesicle breakdown (GVBD) and first polar body (PB) formation without any other natural or introduced factors that might influence the rate of oocyte maturation. We also determined if these oocytes could be fertilized.

Bovine oocytes were incubated in a salt medium and TCM 199 supplemented with different concentrations of heparin for 24 h at 37.5 °C in a humidified atmosphere of 5% CO2. With 1.0 and 6.5 mg/ml heparin, the time of GVBD was reduced from 4.7 ± 1.1 h to about 1.5 h and the time of first PB formation was reduced from 22.0 ± 1.1 h to 9.0–11.0 h in salt medium. In TCM 199, only 6.5 mg/ml heparin significantly reduced the time of PB formation. In both incubation media, 1.0 and 6.5 mg/ml heparin induced GVBD, extrusion of the first PB and formation of the metaphase II nucleus. Moreover, heparin did not interfere with the fertilization of oocytes matured in TCM 199. Based on the results, we propose that heparin plays an important role in the rearrangement of the oocyte chromatin and acts as an oocyte maturation factor.

Keywords

Chromatin reorganizationGerminal vesicle breakdownHeparinOocyte maturationPolar body formation
Type
Research Article
Information
Zygote , Volume 16 , Issue 1 , February 2008 , pp. 1 - 8
Copyright
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aárabi, S.Y., Roussel, J.D. & Candler, J.E. (1997). Chromo-somal analysis of mammalian oocyte matured in vitro with various culture systems. Theriogenology 48, 1173–83.CrossRefGoogle Scholar
Ax, R.L. & Bellin, M.E. (1988). Glycosaminoglycans and follicular development. J. Anim. Sci. Suppl. 66, 32–49.Google Scholar
Bhuiyan, M.M., Cho, J.K., Jang, G., Park, E.S., Kang, S.K., Lee, B.C. & Hwang, W.S. (2004). Effect of protein supplementation in potassium simplex optimization medium on preimplantation development of bovine non-transgenic and transgenic cloned embryos. Theriogenology 62, 1403–16.CrossRefGoogle ScholarPubMed
Bu, S., Xie, H., Tao, Y., Wang, J. & Xia, G. (2004). Nitric oxide influences the maturation of cumulus cell-enclosed mouse oocyte cultured in spontaneous maturation medium and hypoxanthine-supplemented medium through different signaling pathways. Mol. Cell. Endocrinol. 223, 85–93.CrossRefGoogle ScholarPubMed
Carolan, C., Lonergan, P., Monget, P., Monniaux, D. & Mermillod, P. (1996). Effect of follicle size and quality on the ability of follicular fluid to support cytoplasmic maturation of bovine oocyte. Mol. Reprod. Dev. 43, 477–83.3.0.CO;2-X>CrossRefGoogle Scholar
Carranco, A., Reyes, R., Magdaleno, V.M., Huacuja, L., Hernández, O., Rosado, A., Merchant, H. & Delgado, N.M. (1983). Heparin induced nuclei decondensation of mammalian epididymal spermatozoa. Arch. Androl. 10, 213–8.CrossRefGoogle ScholarPubMed
Chamberland, A., Fournier, V., Tardif, S., Sirard, M.A., Sullivan, R. & Bailey, J.L. (2001). The effect of heparin on motility parameters and protein phosphorylation during bovine sperm capacitation. Theriogenology 55, 823–35.CrossRefGoogle ScholarPubMed
Choi, Y.H., Takagi, M., Kamishita, H., Wijayagunawardane, M.P., Acosta, T.J., Miyazawa, K. & Sato, K. (1998). Developmental capacity of bovine oocytes matured in two kinds of follicular fluid and fertilized in vitro. Anim. Reprod. Sci. 50, 27–33.CrossRefGoogle ScholarPubMed
Cook, R.T. & Aikawa, M. (1973). The effect of heparin on endogenous DNA polymerase activity of rat liver nuclei and chromatin fractions. Exp. Cell Res. 78, 257–70.CrossRefGoogle ScholarPubMed
Downs, S.M. (1989). Specificity of epidermal growth factor action on maturation of the murine oocyte and cumulus oophorus in vitro. Biol. Reprod. 41, 371–9.CrossRefGoogle ScholarPubMed
Eckert, J. & Niemann, H. (1995). In vitro maturation, fertilization and culture to blastocysts of bovine oocytes in protein-free media. Theriogenology 43, 1211–25.CrossRefGoogle ScholarPubMed
Fenton, S.E., Dentine, M.R. & Ax, R.L. (1993). Modulation of bovine oocyte–cumulus cell complex maturation and fertilization in vitro by glycosaminoglycans. J. Dairy Sci. 76, 701–12.CrossRefGoogle ScholarPubMed
Foley, M.E., Griffin, B.D., Zuzel, M., Aparicio, S.R., Bradbury, K., Bird, C.C., Clayton, J.K., Jenkins, D.M., Scott, J.S., Rajah, S.M. & McNichol, G.P. (1978). Heparin-like activity in uterine fluid. Br. Med. J. 2, 322–4.CrossRefGoogle ScholarPubMed
Gebauer, H., Lindner, H.R. & Amsterdam, A. (1978). Synthesis of heparin-like glycosaminoglycans in rat ovarian slices. Biol. Reprod. 18, 350–8.CrossRefGoogle ScholarPubMed
Homa, S.T. (1995). Calcium and meiotic maturation of the mammalian oocyte. Mol. Reprod. Dev. 40, 122–34.CrossRefGoogle ScholarPubMed
Homa, S.T., Webster, S.D. & Russell, R.K. (1991). Phospholipid turnover and ultrastructural correlates during spontaneous germinal vesicle breakdown of the bovine oocyte: effects of a cyclic AMP phosphodiesterase inhibitor. Dev. Biol. 146, 461–72.CrossRefGoogle ScholarPubMed
Hyttel, P., Greve, T. & Callesen, H. (1989). Ultrastructural aspects of oocyte maturation and fertilization in cattle. J. Reprod. Fertil. Suppl. 38, 35–47.Google ScholarPubMed
Ikeda, S., Azuma, T., Hashimoto, S. & Yamada, M. (1999). In vitro maturation of bovine oocyte with fractions of bovine follicular fluid separated by heparin affinity chromatography. J. Reprod. Develop. 45, 397–404.CrossRefGoogle Scholar
Jang, G., Lee, B.C., Kang, S.K. & Hwang, W.S. (2003). Effect of glycosaminoglycans on the preimplantation development of embryos derived from in vitro fertilization and somatic cell nuclear transfer. Reprod. Fertil. Dev. 15, 179–85.CrossRefGoogle ScholarPubMed
Kawakami, E., Arai, T., Oishi, I., Hori, T. & Tsutsui, T. (2000). Induction of dog sperm capacitation by glycosamino-glycans and glycosaminoglycan amounts of oviductal and uterine fluids in bitches. J. Vet. Med. Sci. 62, 65–8.CrossRefGoogle Scholar
Keyhani, E. & Storey, B.T. (1973). Energy conservation capacity and morphological integrity of mitochondria in hypotonically treated rabbit epididymal spermatozoa. Biochem. Biophys. Acta 305, 557–69.Google ScholarPubMed
Khatir, H., Carolan, C., Lonergan, P. & Mermillod, P. (1997). Characterization of calf follicular fluid and its ability to support cytoplasmic maturation of cow and calf oocyte. J. Reprod. Fertil. 111, 267–75.CrossRefGoogle Scholar
Kim, H.S., Lee, G.S., Hyun, S.H., Nam, D.H., Lee, S.H., Jeong, Y.W., Kim, S., Kim, J.H., Kang, S.K., Lee, B.C. & Hwang, W.S. (2005). Embryotropic effect of glycosaminoglycans and receptors in development of porcine pre-implantation embryos. Theriogenology 63, 1167–80.CrossRefGoogle ScholarPubMed
Li, G.P., Seidel, G.E. Jr & Squires, E.L. (2004). Improved cleavage of bovine ICSI ova cultured in heparin-containing medium. Theriogenology 61, 1077–84.CrossRefGoogle ScholarPubMed
Lonergan, P., Gutiérrez-Adán, A., Rizos, D., Pintado, B., De la Fuente, J. & Boland, M.P. (2003). Relative messenger RNA abundance in bovine oocyte collected in vitro or in vivo before and 20 hr after preovulatory luteinizing hormone surge. Mol. Reprod. Dev. 66, 297–305.CrossRefGoogle ScholarPubMed
McGaughey, R.W. (1975). A comparison of the fluids from small and large ovarian follicles of the pig. Biol. Reprod. 13, 147–53.CrossRefGoogle ScholarPubMed
McGinnis, L.K., Zhu, L., Lawitts, J.A., Bhowmick, S., Toner, M. & Biggers, J.D. (2005). Mouse sperm desiccated and stored in trehalose medium without freezing. Biol. Reprod. 73, 627–633.CrossRefGoogle ScholarPubMed
Nedambale, T.L., Dinnyes, A., Groen, W., Dobrinsky, J.R., Tian, X.C. & Yang, X. (2004), Comparison on in vitro fertilized bovine embryos cultured in KSOM or SOF and cryopreserved by slow freezing or vitrification. Theriogenology 62, 437–49.CrossRefGoogle ScholarPubMed
Reyes, R., Ramírez, G. & Delgado, N.M. (2004). Fluorescent berberine binding as a marker of internal glycosaminoglycans sulfate in bovine oocytes and sperm cells. Arch. Androl. 50, 327–32.CrossRefGoogle ScholarPubMed
Russo, G.L., Kyozuka, K., Antonazzo, L., Tosti, E. & Dale, B. (1996). Maturation promoting factor in ascidians oocytes is regulated by different intracellular signals at meiosis I and II. Development 122, 1995–2003.CrossRefGoogle ScholarPubMed
Saiga, H. & Kinoshita, S. (1976). Changes of chromatin structure induce by acid mucopolysaccharides. Exp. Cell Res. 102,143–52.CrossRefGoogle ScholarPubMed
Sánchez-Vázquez, M.L., Reyes, R., Ramírez, G., Merchant-Larios, H., Rosado, A. & Delgado, N.M. (1998). DNA unpacking in guinea pig sperm chromatin by heparin and reduced glutathione. Arch. Androl. 40, 15–28.CrossRefGoogle ScholarPubMed
Sato, E., Ishibashi, T. & Koide, S.S. (1987). Prevention of spontaneous degeneration of mouse oocytes in culture by ovarian glycosaminoglycans. Biol. Reprod. 37, 371–6.CrossRefGoogle ScholarPubMed
Sirard, M.A., Florman, H.M., Leibfried-Rutledge, M.L., Barnes, F.L., Sims, M.L. & First, N.L. (1989). Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes. Biol. Reprod. 40, 1257–63.CrossRefGoogle ScholarPubMed
Sutton-McDowall, M.L., Gilchrist, R.B. & Thompson, J.G. (2005). Effect of hexoses and gonadotrophin supplementation on bovine oocyte nuclear maturation during in vitro maturation in a synthetic follicle fluid medium. Reprod. Fertil. Dev. 17, 407–15.CrossRefGoogle Scholar
Tanghe, S., Van Soom, A., Duchateau, L., Nauwynck, H. & De Kruif, A. (2004). Carbohydrates and glycoproteins involved in bovine fertilization in vitro. Mol. Reprod. Dev. 68, 492–9.CrossRefGoogle ScholarPubMed
Valencia, A., Wens, M.A., Merchant, H., Reyes, R. & Delgado, N.M. (1984). Capacitation of human spermatozoa by heparin. Arch. Androl. Suppl. 12, 109–13.Google ScholarPubMed
Yoshimura, Y. & Wallach, E.E. (1987). Studies of the mechanism(s) of mammalian ovulation. Fertil. Steril. 47, 22–34.CrossRefGoogle ScholarPubMed