Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-27T09:14:43.270Z Has data issue: false hasContentIssue false
  • English
  • Français

Developmental competence of porcine oocytes after in vitro maturation and in vitro culture under different oxygen concentrations

Published online by Cambridge University Press:  27 July 2011

Jung-Taek Kang ,
Mohammad Atikuzzaman ,
Dae-Kee Kwon ,
Sol-Ji Park ,
Su-Jin Kim ,
Joon-Ho Moon ,
Ok-Jae Koo ,
Goo Jang  and
Byeong-Chun Lee
Jung-Taek Kang
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul 151–742, Korea.
Mohammad Atikuzzaman
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul 151–742, Korea.
Dae-Kee Kwon
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul 151–742, Korea.
Sol-Ji Park
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul 151–742, Korea.
Su-Jin Kim
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul 151–742, Korea.
Joon-Ho Moon
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul 151–742, Korea.
Ok-Jae Koo
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul 151–742, Korea.
Goo Jang
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul 151–742, Korea.
Byeong-Chun Lee*
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine, Seoul National University, 599 Gwanangno, Gwanak-gu, Seoul, 151–742, Korea.
*
All correspondence to: Byeong-Chun Lee. Department of Theriogenology and Biotechnology, College of Veterinary Medicine, Seoul National University, 599 Gwanangno, Gwanak-gu, Seoul, 151–742, Korea. Tel: +822 880 1269. Fax: +822 873 1269. e-mail: bclee@snu.ac.kr
Get access Rights & Permissions [Opens in a new window]

Summary

In this study, we investigated the effect of two oxygen concentrations (5 and 20%) during in vitro maturation (IVM) and during in vitro culture (IVC) on porcine embryo development and analysed differences in gene expression between cumulus–oocyte complexes matured under 5 or 20% oxygen and the resulting blastocysts cultured under 5% or 20% oxygen following parthenogenetic activation. There was no significant difference in oocyte maturation rate. However, the numbers of resulting blastocysts were significantly increased in the 5% IVC group compared with the 20% IVC group. Moreover, the M20C5 treatment group (23.01%) supported greater blastocyst development compared with the M5C5 (14.32%), M5C20 (10.30%), and M20C20 (17.88%) groups. However, total cell numbers were not significantly different among groups. According to mRNA abundance data of multiple genes, each treatment altered the expression of genes in different patterns. GLUT1, G6PD and LDHA were up-regulated in cumulus cells that had been matured in low oxygen, suggesting a higher glucose uptake and an increase in anaerobic glycolysis, whereas cyclin B1 (CCNB) and MnSOD (Mn-superoxide dismutase) were upregulated in cumulus cells that had been matured in high oxygen, which suggests a higher activity of mitosis-promoting factor and antioxidant response. In spite of these differential effects on cumulus cells, oocytes could mature normally regardless of different oxygen concentrations. Therefore, it can be concluded that high oxygen concentration during in vitro maturation and low oxygen during in vitro culture may alter the expression of multiple genes related to oocyte competence and significantly improves embryo development (p < 0.05) but not blastocyst quality.

Keywords

Embryo developmentOxygen tensionPorcine embryo
Type
Research Article
Information
Zygote , Volume 20 , Issue 1 , February 2012 , pp. 1 - 8
Copyright
Copyright © Cambridge University Press 2011

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

Agung, B., Piao, Y., Fuchimoto, D., Senbon, S., Onishi, A., Otoi, T. & Nagai, T. (2010). Effects of oxygen tension and follicle cells on maturation and fertilization of porcine oocytes during in vitro culture in follicular fluid. Theriogenology 73, 893–9.CrossRefGoogle ScholarPubMed
Bauer, B.K., Isom, S.C., Spate, L.D., Whitworth, K.M., Spollen, W.G., Blake, S.M., Springer, G.K., Murphy, C.N. & Prather, R.S. (2010). Transcriptional profiling by deep sequencing identifies differences in mRNA transcript abundance in in vivo-derived versus in vitro-cultured porcine blastocyst stage embryos. Biol. Reprod. 83, 791–8.CrossRefGoogle ScholarPubMed
Bavister, B. D. (1995). Culture of preimplantation embryos: facts and artifacts. Hum. Reprod. Update 1, 91–148.CrossRefGoogle Scholar
Dai, Y., Vaught, T.D., Boone, J., Chen, S.H., Phelps, C.J., Ball, S., Monahan, J.A., Jobst, P.M., McCreath, K.J., Lamborn, A.E., Cowell-Lucero, J.L., Wells, K.D., Colman, A., Polejaeva, I.A. & Ayares, D.L. (2002). Targeted disruption of the alpha1,3-galactosyltransferase gene in cloned pigs. Nat. Biotechnol. 20, 251–5.CrossRefGoogle ScholarPubMed
de Castro e Paula, L.A. & Hansen, P.J. (2007). Interactions between oxygen tension and glucose concentration that modulate actions of heat shock on bovine oocytes during in vitro maturation. Theriogenology 68, 763–70.CrossRefGoogle ScholarPubMed
Fischer, B. & Bavister, B.D. (1993). Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J. Reprod. Fertil. 99, 673–9.CrossRefGoogle ScholarPubMed
Gil, M.A., Cuello, C., Parrilla, I., Vazquez, J.M., Roca, J. & Martinez, E.A. (2010). Advances in swine in vitro embryo production technologies. Reprod. Domest. Anim. 45 Suppl 2, 40–8.CrossRefGoogle ScholarPubMed
Hashimoto, S., Minami, N., Takakura, R., Yamada, M., Imai, H. & Kashima, N. (2000). Low oxygen tension during in vitro maturation is beneficial for supporting the subsequent development of bovine cumulus–oocyte complexes. Mol. Reprod. Dev. 57, 353–60.3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Hsieh, C.H., Tang, P.C., Chang, W.H., Weng, Y.C., Sha, S.W., Tseng, J.K., Chang, L.H. & Ju, J.C. (2006). The kinase inhibitor indirubin-3′-oxime prevents germinal vesicle breakdown and reduces parthenogenetic development of pig oocytes. Theriogenology 65, 744–56.CrossRefGoogle ScholarPubMed
Iwamoto, M., Onishi, A., Fuchimoto, D., Somfai, T., Takeda, K., Tagami, T., Hanada, H., Noguchi, J., Kaneko, H., Nagai, T. & Kikuchi, K. (2005). Low oxygen tension during in vitro maturation of porcine follicular oocytes improves parthenogenetic activation and subsequent development to the blastocyst stage. Theriogenology 63, 1277–89.CrossRefGoogle Scholar
Jiang, L., Lai, L., Samuel, M., Prather, R.S., Yang, X. & Tian, X.C. (2008). Expression of X-linked genes in deceased neonates and surviving cloned female piglets. Mol. Reprod. Dev. 75, 265–73.CrossRefGoogle ScholarPubMed
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, 1033–41.CrossRefGoogle ScholarPubMed
Knudsen, J.F., Litkowski, L.J., Wilson, T.L., Guthrie, H.D. & Batta, S.K. (1978). Concentrations of hydrogen ions, oxygen, carbon dioxide and bicarbonate in porcine follicular fluid. J. Endocrinol. 79, 249–50.CrossRefGoogle ScholarPubMed
Koo, O.J., Park, H.J., Kwon, D.K., Kang, J.T., Jang, G. & Lee, B.C. (2009). Effect of recipient breed on delivery rate of cloned miniature pig. Zygote 17, 203–7.CrossRefGoogle ScholarPubMed
Kuroda, T., Naito, K., Sugiura, K., Yamashita, M., Takakura, I. & Tojo, H. (2004). Analysis of the roles of cyclin B1 and cyclin B2 in porcine oocyte maturation by inhibiting synthesis with antisense RNA injection. Biol. Reprod. 70, 154–9.CrossRefGoogle ScholarPubMed
Lim, H., Paria, B. C., Das, S.K., Dinchuk, J.E., Langenbach, R., Trzaskos, J.M. & Dey, S.K. (1997). Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 91, 197–208.CrossRefGoogle ScholarPubMed
McKenzie, L.J., Pangas, S.A., Carson, S.A., Kovanci, E., Cisneros, P., Buster, J.E., Amato, P. & Matzuk, M. M. (2004). Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF. Hum. Reprod. 19, 2869–74.CrossRefGoogle ScholarPubMed
Park, J.I., Hong, J.Y., Yong, H.Y., Hwang, W.S., Lim, J.M. & Lee, E.S. (2005). High oxygen tension during in vitro oocyte maturation improves in vitro development of porcine oocytes after fertilization. Anim. Reprod. Sci. 87, 133–41.CrossRefGoogle ScholarPubMed
Petters, R.M., Johnson, B.H., Reed, M.L. & Archibong, A.E. (1990). Glucose, glutamine and inorganic phosphate in early development of the pig embryo in vitro. J. Reprod. Fertil. 89, 269–75.CrossRefGoogle ScholarPubMed
Pinyopummintr, T. & Bavister, B.D. (1995). Optimum gas atmosphere for in vitro maturation and in vitro fertilization of bovine oocytes. Theriogenology 44, 471–7.CrossRefGoogle ScholarPubMed
Preis, K.A., SeidelG.E., Jr. G.E., Jr. & Gardner, D.K. (2007). Reduced oxygen concentration improves the developmental competence of mouse oocytes following in vitro maturation. Mol. Reprod. Dev. 74, 893–903.CrossRefGoogle ScholarPubMed
Ross, J.W., Ashworth, M.D., White, F.J., Johnson, G.A., Ayoubi, P.J., DeSilva, U., Whitworth, K.M., Prather, R.S. & Geisert, R.D. (2007). Premature estrogen exposure alters endometrial gene expression to disrupt pregnancy in the pig. Endocrinology 148, 4761–73.CrossRefGoogle ScholarPubMed
Sugiura, K., Naito, K., Endo, T. & Tojo, H. (2006). Study of germinal vesicle requirement for the normal kinetics of maturation/M-phase-promoting factor activity during porcine oocyte maturation. Biol. Reprod. 74, 593–600.CrossRefGoogle ScholarPubMed
Takahashi, Y. & Kanagawa, H. (1998). Effect of oxygen concentration in the gas atmosphere during in vitro insemination of bovine oocytes on the subsequent embryonic development in vitro. J. Vet. Med. Sci. 60, 365–7.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 caused by oxidative stress during In vitro maturation: role of cumulus cells. Biol. Reprod. 63, 805–10.CrossRefGoogle ScholarPubMed
Tucker, A., Belcher, C., Moloo, B., Bell, J., Mazzulli, T., Humar, A., Hughes, A., McArdle, P. & Talbot, A. (2002). The production of transgenic pigs for potential use in clinical xenotransplantation: baseline clinical pathology and organ size studies. Xenotransplantation 9, 203–8.CrossRefGoogle ScholarPubMed
Wang, Z.G., Wang, W., Yu, S.D. & Xu, Z.R. (2008). Effects of different activation protocols on preimplantation development, apoptosis and ploidy of bovine parthenogenetic embryos. Anim. Reprod. Sci. 105, 292–301.CrossRefGoogle ScholarPubMed
Wongsrikeao, P., Kaneshige, Y., Ooki, R., Taniguchi, M., Agung, B., Nii, M. & Otoi, T. (2005). Effect of the removal of cumulus cells on the nuclear maturation, fertilization and development of porcine oocytes. Reprod. Domest. Anim. 40, 166–70.CrossRefGoogle ScholarPubMed
WrightR.W., Jr. R.W., Jr. (1977). Successful culture in vitro of swine embryos to the blastocyst stage. J. Anim. Sci. 44, 854–8.CrossRefGoogle Scholar
Yamashita, Y., Kawashima, I., Gunji, Y., Hishinuma, M. & Shimada, M. (2010). Progesterone is essential for maintenance of Tace/Adam17 mRNA expression, but not EGF-like factor, in cumulus cells, which enhances the EGF receptor signaling pathway during in vitro maturation of porcine COCs. J. Reprod. Dev. 56, 315–23.CrossRefGoogle Scholar
Yoshioka, K., Suzuki, C., Tanaka, A., Anas, I. M. & Iwamura, S. (2002). Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol. Reprod. 66, 112–9.CrossRefGoogle Scholar