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Effect of dibutyryl cyclic adenosine monophosphate on reactive oxygen species and glutathione of porcine oocytes, apoptosis of cumulus cells, and embryonic development

Published online by Cambridge University Press:  22 November 2012

Sang-Hyoun Park
Affiliation:
Department of Theriogenology and Reproductive Biotechnologies, College of Veterinary Medicine, Chonbuk National University, Jeonju 561–756, Republic of Korea.
Il-Jeoung Yu*
Affiliation:
Department of Theriogenology and Reproductive Biotechnologies, College of Veterinary Medicine, Chonbuk National University, Jeonju 561–756, Republic of Korea.
*
All correspondence to: Il-Jeoung Yu, Department of Theriogenology and Reproductive Biotechnologies, College of Veterinary Medicine, Chonbuk National University, Jeonju 561–756, Republic of Korea. Tel: +82 63 2703785. Fax: +82 63 2703780. e-mail: iyu@jbnu.ac.kr or iyu571@gmail.com

Summary

The present study was conducted to investigate the effect of dibutyryl cyclic adenosine monophosphate (dbcAMP) supplemented into porcine maturation medium on reactive oxygen species (ROS) and glutathione (GSH) levels of oocytes, and apoptosis of cumulus cells (CC). In addition, the effect of dbcAMP on embryonic development following in vitro fertilization (IVF) or parthenogenetic activation (PA) was determined. Cumulus–oocyte complexes (COCs) were cultured in 0 mM (control), 0.5 mM, 1 mM, 5 mM, or 10 mM dbcAMP-supplemented medium for 22 h, then for another 22 h without dbcAMP. GSH and ROS levels of oocytes were assessed at 44 h of culture by dichlorohydrofluorescein diacetate or 4-chloromethyl-6,8-difluoro-7-hydroxycoumarin staining, respectively. Additionally, COCs were cultured in 0.5 mM or 1 mM dbcAMP and then fertilized in vitro or activated parthenogenetically. Embryonic development and blastocyst cell numbers and apoptosis levels on day 8 of culture were investigated. CC apoptosis at 44 h of culture and blastocyst apoptosis were assessed by terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL) assay. GSH levels in the 0.5 mM dbcAMP and control groups were increased (P < 0.05), while levels of oocyte ROS and CC apoptosis in the control, 0.5 mM, and 1 mM dbcAMP groups were significantly lower than the levels in other groups. Cleavage and blastocyst rates, cell numbers, and apoptosis levels were not significantly different in embryos derived by either IVF or PA among the groups, with the exception of significantly increased apoptotic levels in IVF blastocysts produced from oocytes treated with 1 mM dbcAMP. In conclusion, dbcAMP treatment during in vitro maturation (IVM) did not improve embryonic development under our study's parameters compared with control conditions, although 0.5 mM dbcAMP showed significantly higher GSH levels and lower blastocyst apoptotic levels compared with 1 mM dbcAMP.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012 

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References

Abeydeera, L.R. & Day, B.N. (1997). Fertilization and subsequent development in vitro of pig oocytes inseminated in a modified Tris-buffered medium with frozen–thawed ejaculated spermatozoa. Biol. Reprod. 57, 729–34.CrossRefGoogle Scholar
Albertini, D.F., Combelles, C.M., Benecchi, E. & Carabatsos, M.J. (2001). Cellular basis for paracrine regulation of ovarian follicle development. Reproduction 121, 647–53.CrossRefGoogle ScholarPubMed
Ayoub, M.A. & Hunter, A.G. (1993). Inhibitory effect of bovine follicular fluid on in vitro maturation of bovine oocytes. J. Dairy Sci. 76, 95100.CrossRefGoogle ScholarPubMed
Bagg, M.A., Nottle, M.B., Grupen, C.G. & Armstrong, D.T. (2006). Effect of dibutyryl cAMP on the cAMP content, meiotic progression, and developmental potential of in vitro matured pre-pubertal and adult pig oocytes. Mol. Reprod. Dev. 73, 1326–32.CrossRefGoogle ScholarPubMed
Byskov, A.G., Andersen, C.Y. & Leonardsen, L. (2002). Role of meiosis activating sterols, MAS, in induced oocyte maturation. Mol. Cell. Endocrinol. 187, 189–96.CrossRefGoogle ScholarPubMed
Cayo-Colca, I.S., Yamagami, Y., Phan, T-C. & Miyano, T. (2011). A combination of FSH and dibutryl cyclic AMP promotes growth and acquisition of meiotic competence of oocytes from early porcine antral follicles. Theriogenology 75, 1602–12.CrossRefGoogle Scholar
Chian, R.C., Niwa, K. & Sirad, M.A. (1994). Effect of cumulus cells on the male pronuclear formation and subsequent early development of bovine oocytes in vitro. Theriogenology 41, 1499–508.CrossRefGoogle ScholarPubMed
Circu, M.L. & Aw, T.Y. (2008). Glutathione and apoptosis. Free. Radic. Res. 42, 689706.CrossRefGoogle ScholarPubMed
Deleuze, S. & Goudet, G. (2010). Cysteamine supplementation of in vitro maturation media: a review. Reprod. Dom. Anim. 45, 476–82.CrossRefGoogle ScholarPubMed
Dostal, J. & Pavlok, A. (1996). Isolation and characterization of maturation inhibiting compound in bovine follicular fluid. Reprod. Nutri. Dev. 36, 681–90.Google ScholarPubMed
Funahashi, H., Cantley, T.C. & Day, B.N. (1997). Synchronization of meiosis in porcine oocytes by exposure to dibutyryl cyclic adenosine monophosphate improves developmental competence following in vitro fertilization. Biol. Reprod. 57, 4953.CrossRefGoogle ScholarPubMed
Gasparrini, B., Sayound, H., Negali, G., Matos, D.G., Donnay, I. & Zicarelli, L. (2003). Glutathione synthesis during in vitro maturation of buffalo (Bubalus bubalis) oocytes: effects of cysteamine on embryo development. Theriogenology 60, 943–52.CrossRefGoogle ScholarPubMed
Gil, M.A., Cuello, I., Parrilla, J.M., Vazquez, J.M., Roca, J. & Martinez, E.A. (2010). Advances in swine in vitro embryo production technologies. Reprod. Dom. Anim. 45 (Suppl. 2), 40–8.CrossRefGoogle ScholarPubMed
Hashimoto, S., Minami, N., Yamada, M. & Imai, H. (2000). Excessive concentration of glucose during in vitro maturation impairs the developmental competence of bovine oocytes after in vitro fertilization: relevance to intracellular reactive oxygen species and glutathione contents. Mol. Reprod. Dev. 56, 520–6.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Kim, J.S., Cho, Y.S., Song, B.S., Wee, G., Park, J.S., Cho, Y.K., Yu, K., Lee, K.K., Han, Y.M. & Koo, D.B. (2008). Exogenous dibutyryl cAMP affects meiotic maturation via protein kinase A activation; it stimulates further embryonic development including blastocyst quality in pigs. Theriogenology 69, 290301.CrossRefGoogle ScholarPubMed
Lee, K.S., Joo, B.S., Na, Y.J., Yoon, M.S., Choi, O.H. & Kim, W.W. (2001). Cumulus cells apoptosis as an indicator to predict the quality of oocytes and the outcome of IVF-ET. J. Assist. Reprod. Genet. 18, 490–8.CrossRefGoogle ScholarPubMed
Luberda, Z. (2005). The role of glutathione in mammalian gametes. Reprod. Biol. 5, 517.Google ScholarPubMed
Marques, M.G., de Barros, F.R.O., Goissis, M.D., Cavalcanti, P.V., Viana, C.H.C., Assumpção, M.E.O.D. & Visintin, J.A. (2012). Effect of low oxygen tension atmosphere and maturation media supplementation on nuclear maturation, cortical granules migration and sperm penetration in swine in vitro fertilization. Reprod. Dom. Anim. 47, 491–7.CrossRefGoogle ScholarPubMed
de Matos, D.G., Furnus, C.C. & Moses, D.F. (1997). Gluthathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells. Biol. Reprod. 57, 1420–5.CrossRefGoogle Scholar
de Matos, D.G., Gasparrini, B., Pasqualini, S.R. & Thompson, J.G. (2002). Effect of gluthathione synthesis stimulation during in vitro maturation of ovine oocytes on embryo development and intracellular peroxide content. Theriogenology 57, 1443–51.CrossRefGoogle Scholar
Meister, A. (1983). Selective modification of glutathione metabolism. Science 220, 472–7.CrossRefGoogle ScholarPubMed
Monget, P., Mazerbourg, S., Delpuech, T., Maurel, M.C., Maniere, S., Zapf, J., Lalmanach, G., Oxvig, C. & Overgarrd, M.T. (2003). Pregnancy-associated plasma protein-A is involved in insulin-like growth factor binding protein-2 (IGFBP-2) proteolytic degradation in bovine and porcine preovulatory follicles: identification of cleavage site and characterization of IGFBP-2 degradation. Biol. Reprod. 68, 7786.CrossRefGoogle ScholarPubMed
Nabenishi, H., Ohta, H., Nishimoto, T., Morita, T., Ashizawa, K. & Tsuzuki, Y. (2011). The effects of cysteine addition during in vitro maturation on the developmental competence, ROS, GSH and apoptosis level of bovine oocytes exposed to heat stress. Zygote 20, 249–59.CrossRefGoogle ScholarPubMed
Nagai, T. (2001). The improvement of in vitro maturation systems for bovine and porcine oocytes. Theriogenology 55, 1291–301.CrossRefGoogle ScholarPubMed
Nascimento, A.B., Albornoz, M.S., Che, L., Visintin, J.A. & Bordignon, V. (2010). Synergistic effect of porcine follicular fluid and dibutyryl cyclic adenosine monophosphate on development of parthenogenetically activated oocytes from pre-pubertal gilts. Reprod. Dom. Anim. 45, 851–9Google ScholarPubMed
Sawai, K., Funahashi, H. & Niwa, K. (1997). Stage-specific requirement of cysteine during in vitro maturation of porcine oocytes for glutathione synthesis associated with male pronuclear formation. Biol. Reprod. 57, 16.CrossRefGoogle ScholarPubMed
Sugimura, S., Yamanaka, K-I., Kawahara, M., Wakai, T., Yokoo, M. & Sato, E. (2010). Early metaphase II oocytes treated with dibutyryl cyclic adenosine monophosphate provide suitable recipient cytoplasm for the production of miniature pig somatic cell nuclear transfer embryos. Anim. Sci. J. 81, 4857.CrossRefGoogle ScholarPubMed
Suzuki, H., Jeong, B.S. & Yang, X. (2000). Dynamic changes of cumulus–oocyte cell communication during in vitro maturation of porcine oocytes. Biol. Reprod. 63, 723–9.CrossRefGoogle ScholarPubMed
Tanghe, S., Van Soom, A., Nauwynck, H., Coryn, M. & de Kruif, A. (2002). Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol. Reprod. Dev. 61, 414–24.CrossRefGoogle ScholarPubMed
Tatemoto, H., Sakurai, N. & Muto, N. (2000). Protection of porcine oocytes against apoptotic cell death by oxidative stress during in vitro maturation: role of cumulus cells. Biol. Reprod. 63, 805–10.CrossRefGoogle ScholarPubMed
Tatemoto, H., Muto, N., Sunagawa, I., Shinjo, A. & Nakada, T. (2004). Protection of porcine oocytes against cell damage caused by oxidative stress during in vitro maturation: role of superoxide dismutase activity in porcine follicular fluid. Biol. Reprod. 71, 1150–7.CrossRefGoogle ScholarPubMed
Thompson, J.G., Lane, M. & Gilchrist, R.B. (2007). Metabolism of the bovine cumulus–oocyte complex and influence on subsequent developmental competence. Soc. Reprod. Fertil. Suppl. 64, 179–90.Google ScholarPubMed
Van Soom, A., Vandaele, L., Goossens, K., de Kruif, A. & Peelman, L. (2007). Gamete origin in relation to early embryo development. Theriogenology 68 (suppl. 1), S1317.CrossRefGoogle ScholarPubMed
Yoshida, M., Bamba, K. & Kojima, Y. (1989). Effects of gonadotropins and estradiol-17β on the timing of nuclear maturation and cumulus mass expansions in pig oocytes cultured in vitro. Jpn. J. Anim. Reprod. 35, 8691.CrossRefGoogle Scholar
Yoshida, M., Ishigaki, K., Nagai, T., Chikyu, M. & Pursel, V.G. (1993). Glutathione concentration during maturation and after fertilization in pig oocytes: relevance to the ability of oocytes to form male pronucleus. Biol. Reprod. 49, 8994.CrossRefGoogle Scholar
Yu, I.J. (2011). Effect of 0.5 mM dibutyryl cAMP on meiotic maturation during different time and embryonic development following in vitro fertilization or parthenogenetic activation in porcine oocytes. J. Emb. Trans. 26, 251–6.Google Scholar
Yuan, Y., Hao, Z.D., Liu, J., Wu, Y., Yang, L., Liu, G.S., Tian, J.H., Zhu, S.E., Zeng, S.M. (2008). Heat shock at the germinal vesicle breakdown stage induces apoptosis in surrounding cumulus cells and reduces maturation rates of porcine oocytes in vitro. Theriogenology 70, 168–78.CrossRefGoogle ScholarPubMed