Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-26T10:13:09.415Z Has data issue: false hasContentIssue false

Supplementation of insulin–transferrin–selenium to embryo culture medium improves the in vitro development of pig embryos

Published online by Cambridge University Press:  18 March 2013

Ziban Chandra Das
Affiliation:
Department of Animal Biotechnology, Animal Resources Research Center/Bio-Organ Research Center, Konkuk University, Seoul 143 701, South Korea. Department of Gynecology, Obstetrics and Reproductive Health, BSMR Agricultural University, Gazipur 1706, Bangladesh.
Mukesh Kumar Gupta*
Affiliation:
Department of Animal Biotechnology, Animal Resources Research Center, Bio-Organ Research Center, Konkuk University, Seoul 143 701, South Korea. Department of Animal Biotechnology, Animal Resources Research Center/Bio-Organ Research Center, Konkuk University, Seoul 143 701, South Korea.
Sang Jun Uhm
Affiliation:
Department of Animal Biotechnology, Animal Resources Research Center/Bio-Organ Research Center, Konkuk University, Seoul 143 701, South Korea. Department of Animal Science and Biotechnology, Sangji Youngseo College, Wonju 220–713, South Korea.
Hoon Taek Lee*
Affiliation:
Department of Animal Biotechnology, Animal Resources Research Center, Bio-Organ Research Center, Konkuk University, Seoul 143 701, South Korea.
*
All correspondence to: Hoon Taek Lee or Mukesh Kumar Gupta. Department of Animal Biotechnology, Animal Resources Research Center, Bio-Organ Research Center, Konkuk University, Seoul 143 701, South Korea. Tel: +82 2 4503675. Fax: +82 2 4578488. E-mail: htl3675@konkuk.ac.kr or Department of Biotechnology and Medical Engineering, National Institute of Technology, Rourkela, Odisha 769 008, India. Tel: +91 661 2462294. E-mail: guptam@nitrkl.ac.in
All correspondence to: Hoon Taek Lee or Mukesh Kumar Gupta. Department of Animal Biotechnology, Animal Resources Research Center, Bio-Organ Research Center, Konkuk University, Seoul 143 701, South Korea. Tel: +82 2 4503675. Fax: +82 2 4578488. E-mail: htl3675@konkuk.ac.kr or Department of Biotechnology and Medical Engineering, National Institute of Technology, Rourkela, Odisha 769 008, India. Tel: +91 661 2462294. E-mail: guptam@nitrkl.ac.in

Summary

Insulin, transferrin and selenium (ITS) supplementation to oocyte maturation medium improves the post-fertilization embryonic development in pigs. ITS is also commonly used as a supplement for the in vitro culture (IVC) of embryos and stem cells in several mammalian species. However, its use during IVC of pig embryos has not been explored. This study investigated the effect of ITS supplementation to IVC medium on the in vitro development ability of pig embryos produced by parthenogenetic activation (PA), in vitro fertilization (IVF) or somatic cell nuclear transfer (SCNT). We observed that ITS had no significant effect on the rate of first cleavage (P > 0.05). However, the rate of blastocyst formation in ITS-treated PA (45.3 ± 1.9 versus 27.1 ± 2.3%), IVF (31.6 ± 0.6 versus 23.5 ± 0.6%) and SCNT (17.6 ± 2.3 versus 10.7 ± 1.4%) embryos was significantly higher (P < 0.05) than those of non-treated controls. Culture of PA embryos in the presence of ITS also enhanced the expansion and hatching ability (29.1 ± 3.0 versus 18.2 ± 3.8%; P < 0.05) of blastocysts and increased the total number of cells per blastocyst (53 ± 2.5 versus 40.9 ± 2.6; P < 0.05). Furthermore, the beneficial effect of ITS on PA embryos was associated with significantly reduced level of intracellular reactive oxygen species (ROS) (20.0 ± 2.6 versus 46.9 ± 3.0). However, in contrast to PA embryos, ITS had no significant effect on the blastocyst quality of IVF and SCNT embryos (P > 0.05). Taken together, these data suggest that supplementation of ITS to the IVC medium exerts a beneficial but differential effect on pig embryos that varies with the method of embryo production in vitro.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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

Aleshire, S.L., Osteen, K.G., Maxson, W.S., Entman, S.S., Bradley, C.A. & Parl, F.F. (1989). Localization of transferrin and its receptor in ovarian follicular cells: morphologic studies in relation to follicular development. Fertil. Steril. 51, 444–9.CrossRefGoogle ScholarPubMed
Augustin, R., Pocar, P., Wrenzycki, C., Niemann, H. & Fischer, B. (2003). Mitogenic and anti-apoptotic activity of insulin on bovine embryos produced in vitro . Reproduction 126, 91–9.CrossRefGoogle ScholarPubMed
Chung, Y.G., Mann, M.R., Bartolomei, M.S. & Latham, K.E. (2002). Nuclear-cytoplasmic “tug of war” during cloning: effects of somatic cell nuclei on culture medium preferences of preimplantation cloned mouse embryos. Biol. Reprod. 66, 1178–84.Google Scholar
Cordova, B., Morato, R., Izquierdo, D., Paramio, T. & Mogas, T. (2010). Effect of the addition of insulin–transferrin–selenium and/or L-ascorbic acid to the in vitro maturation of prepubertal bovine oocytes on cytoplasmic maturation and embryo development. Theriogenology 74, 1341–8.Google Scholar
Dang-Nguyen, T.Q., Somfai, T., Haraguchi, S., Kikuchi, K., Tajima, A., Kanai, Y. & Nagai, T. (2011). In vitro production of porcine embryos: current status, future perspectives and alternative applications. Anim. Sci. J. 82, 374–82.Google Scholar
Das, Z.C., Gupta, M.K., Uhm, S.J. & Lee, H.T. (2010a). Increasing histone acetylation of cloned embryos, but not donor cells, by sodium butyrate improves their in vitro development in pigs. Cell Reprogram. 12, 95104.CrossRefGoogle Scholar
Das, Z.C., Gupta, M.K., Uhm, S.J. & Lee, H.T. (2010b). Lyophilized somatic cells direct embryonic development after whole cell intracytoplasmic injection into pig oocytes. Cryobiology 61, 220–4.Google Scholar
Gupta, M.K., Uhm, S.J., Han, D.W. & Lee, H.T. (2007a). Embryo quality and production efficiency of porcine parthenotes is improved by phytohemagglutinin. Mol. Reprod. Dev. 74, 435–44.CrossRefGoogle ScholarPubMed
Gupta, M.K., Uhm, S.J. & Lee, H.T. (2007b). Cryopreservation of immature and in vitro matured porcine oocytes by solid surface vitrification. Theriogenology 67, 238–48.Google Scholar
Gupta, M.K., Uhm, S.J. & Lee, H.T. (2007c). Differential but beneficial effect of phytohemagglutinin on efficiency of in vitro porcine embryo production by somatic cell nuclear transfer or in vitro fertilization. Mol. Reprod. Dev. 74, 1557–67.CrossRefGoogle ScholarPubMed
Gupta, M.K., Uhm, S.J. & Lee, H.T. (2008a). Sexual maturity and reproductive phase of oocyte donor influence the developmental ability and apoptosis of cloned and parthenogenetic porcine embryos. Anim. Reprod. Sci. 108, 107–21.Google Scholar
Gupta, M.K., Uhm, S.J., Lee, S.H., Lee, H.T. (2008b). Role of nonessential amino acids on porcine embryos produced by parthenogenesis or somatic cell nuclear transfer. Mol. Reprod. Dev. 75, 588–97.Google Scholar
Gupta, M.K., Jang, J.M., Jung, J.W., Uhm, S.J., Kim, K.P. & Lee, H.T. (2009). Proteomic analysis of parthenogenetic and in vitro fertilized porcine embryos. Proteomics 9, 2846–60.CrossRefGoogle ScholarPubMed
Gupta, M.K., Uhm, S.J. & Lee, H.T. (2010). Effect of vitrification and beta-mercaptoethanol on reactive oxygen species activity and in vitro development of oocytes vitrified before or after in vitro fertilization. Fertil. Steril. 93, 2602–7.Google Scholar
Han, D.W., Song, S.J., Uhum, S.J., Do, J.T., Kim, N.H., Chung, K.S. & Lee, H.T. (2003). Expression of IGF2 and IGF receptor mRNA in bovine nuclear transferred embryos. Zygote 11, 245–52.Google Scholar
Han, D.W., Im, Y.B., Do, J.T., Gupta, M.K., Uhm, S.J., Kim, J.H., Scholer, H.R. & Lee, H.T. (2008). Methylation status of putative differentially methylated regions of porcine IGF2 and H19. Mol. Reprod. Dev. 75, 777–84.Google Scholar
Harvey, M.B. & Kaye, P.L. (1988). Insulin stimulates protein synthesis in compacted mouse embryos. Endocrinology 122, 1182–4.Google Scholar
Heindryckx, B., Rybouchkin, A., Van Der Elst, J. & Dhont, M. (2001). Effect of culture media on in vitro development of cloned mouse embryos. Cloning 3, 4150.Google Scholar
Hofmann, W.K., Takeuchi, S., Frantzen, M.A., Hoelzer, D. & Koeffler, H.P. (2002). Loss of genomic imprinting of insulin-like growth factor 2 is strongly associated with cellular proliferation in normal hematopoietic cells. Exp. Hematol. 30, 318–23.Google Scholar
Hu, J., Ma, X., Bao, J.C., Li, W., Cheng, D., Gao, Z., Lei, A., Yang, C. & Wang, H. (2011). Insulin–transferrin–selenium (ITS) improves maturation of porcine oocytes in vitro . Zygote 19, 191–7.CrossRefGoogle ScholarPubMed
Jeong, Y.W., Hossein, M.S., Bhandari, D.P., Kim, Y.W., Kim, J.H., Park, S.W., Lee, E., Park, S.M., Jeong, Y.I., Lee, J.Y., Kim, S. & Hwang, W.S. (2008). Effects of insulin–transferrin–selenium in defined and porcine follicular fluid supplemented IVM media on porcine IVF and SCNT embryo production. Anim. Reprod. Sci. 106, 1324.Google Scholar
Kahn, C.R. (1985). The molecular mechanism of insulin action. Annu. Rev. Med. 36, 429–51.Google Scholar
Karja, N.W., Wongsrikeao, P., Murakami, M., Agung, B., Fahrudin, M., Nagai, T. & Otoi, T. (2004). Effects of oxygen tension on the development and quality of porcine in vitro fertilized embryos. Theriogenology 62, 1585–95.CrossRefGoogle ScholarPubMed
Kim, H.S., Lee, G.S., Kim, J.H., Kang, S.K., Lee, B.C. & Hwang, W.S. (2006). Expression of leptin ligand and receptor and effect of exogenous leptin supplement on in vitro development of porcine embryos. Theriogenology 65, 831–44.CrossRefGoogle ScholarPubMed
Kitagawa, Y., Suzuki, K., Yoneda, A. & Watanabe, T. (2004). Effects of oxygen concentration and antioxidants on the in vitro developmental ability, production of reactive oxygen species (ROS), and DNA fragmentation in porcine embryos. Theriogenology 62, 1186–97.Google Scholar
Koo, D.B., Kim, N.H., Lee, H.T. & Chung, K.S. (1997). Effects of fetal calf serum, amino acids, vitamins and insulin on blastocoel formation and hatching of in vivo and IVM/IVF-derived porcine embryos developing in vitro . Theriogenology 48, 791802.Google Scholar
Kurzawa, R., Glabowski, W., Baczkowski, T. & Brelik, P. (2002). Evaluation of mouse preimplantation embryos exposed to oxidative stress cultured with insulin-like growth factor I and II, epidermal growth factor, insulin, transferrin and selenium. Reprod. Biol. 2, 143–62.Google ScholarPubMed
Lee, S.H., Kim, D.Y., Nam, D.H., Hyun, S.H., Lee, G.S., Kim, H.S., Lee, C.K., Kang, S.K., Lee, B.C. & Hwang, W.S. (2004). Role of messenger RNA expression of platelet activating factor and its receptor in porcine in vitro-fertilized and cloned embryo development. Biol. Reprod. 71, 919–25.CrossRefGoogle ScholarPubMed
Lewis, A.M., Kaye, P.L., Lising, R. & Cameron, R.D. (1992). Stimulation of protein synthesis and expansion of pig blastocysts by insulin in vitro . Reprod. Fertil. Dev. 4, 119–23.Google Scholar
Lim, J.M. & Hansel, W. (2000). Exogeneous substances affecting development of in vitro-derived bovine embryos before and after embryonic genome activation. Theriogenology 53, 1081–91.CrossRefGoogle ScholarPubMed
Lopata, A. & Oliva, K. (1993). Chorionic gonadotrophin secretion by human blastocysts. Hum. Reprod. 8, 932–8.Google Scholar
Nasr-Esfahani, M.H. & Johnson, M.H. (1992). How does transferrin overcome the in vitro block to development of the mouse preimplantation embryo? J. Reprod. Fertil. 96, 41–8.CrossRefGoogle ScholarPubMed
Raghu, H.M., Nandi, S. & Reddy, S.M. (2002). Effect of insulin, transferrin and selenium and epidermal growth factor on development of buffalo oocytes to the blastocyst stage in vitro in serum-free, semidefined media. Vet. Rec. 151, 260–5.Google Scholar
Rappolee, D.A., Sturm, K.S., Behrendtsen, O., Schultz, G.A., Pedersen, R.A. & Werb, Z. (1992). Insulin-like growth factor II acts through an endogenous growth pathway regulated by imprinting in early mouse embryos. Genes Dev. 6, 939–52.CrossRefGoogle ScholarPubMed
Sneddon, A.A., Wu, H.C., Farquharson, A., Grant, I., Arthur, J.R., Rotondo, D., Choe, S.N. & Wahle, K.W. (2003). Regulation of selenoprotein GPx4 expression and activity in human endothelial cells by fatty acids, cytokines and antioxidants. Atherosclerosis 171, 5765.Google Scholar
Sugimura, S., Yokoo, M., Yamanaka, K., Kawahara, M., Moriyasu, S., Wakai, T., Nagai, T., Abe, H. & Sato, E. (2011). Anomalous oxygen consumption in porcine somatic cell nuclear transfer embryos. Cell Reprogram. 12, 463–74.Google Scholar
Uhm, S.J., Gupta, M.K., Yang, J.H., Lee, S.H. & Lee, H.T. (2007). Selenium improves the developmental ability and reduces the apoptosis in porcine parthenotes. Mol. Reprod. Dev. 74, 1386–94.Google Scholar
Uhm, S.J., Gupta, M.K., Yang, J.H., Chung, H.J., Min, T.S. & Lee, H.T. (2010). Epidermal growth factor can be used in lieu of follicle-stimulating hormone for nuclear maturation of porcine oocytes in vitro . Theriogenology 73, 1024–36.Google Scholar
Uhm, S.J., Gupta, M.K., Das, Z.C., Kim, N.H. & Lee, H.T. (2011a). 3-Hydroxyflavone improves the in vitro development of cloned porcine embryos by inhibiting ROS production. Cell Reprogram. 13, 441–9.Google Scholar
Uhm, S.J., Gupta, M.K., Das, Z.C., Lim, K.T., Yang, J.H. & Lee, H.T. (2011b). Effect of 3-hydroxyflavone on pig embryos produced by parthenogenesis or somatic cell nuclear transfer. Reprod. Toxicol. 31, 231–8.CrossRefGoogle ScholarPubMed
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
Zhang, X. & Armstrong, D.T. (1990). Presence of amino acids and insulin in a chemically defined medium improves development of 8-cell rat embryos in vitro and subsequent implantation in vivo . Biol. Reprod. 42, 662–8.Google Scholar
Zhu, Y., Goodridge, A.G. & Stapleton, S.R. (1994). Zinc, vanadate and selenate inhibit the tri-iodothyronine-induced expression of fatty acid synthase and malic enzyme in chick-embryo hepatocytes in culture. Biochem. J. 303 (Pt 1), 213–6.Google Scholar