Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-20T15:18:31.153Z Has data issue: false hasContentIssue false
  • English
  • Français

Production of somatic cell nuclear transfer embryos using in vitro-grown and in vitro-matured oocytes in rabbits

Published online by Cambridge University Press:  26 March 2014

Hironobu Sugimoto ,
Yuta Kida ,
Noriyoshi Oh ,
Kensaku Kitada ,
Kazuya Matsumoto ,
Kazuhiro Saeki ,
Takeshi Taniguchi  and
Yoshihiko Hosoi
Hironobu Sugimoto
Affiliation:
Taniguchi Hospital, 1–5-20 Onishi, Izumisano, Osaka 598-0043, Japan. Division of Biological Science, Graduate School of Biology-oriented Science and Technology, Kinki University, 930 Nishimitani, Kinokawa, Wakayama 649-6493, Japan.
Yuta Kida
Affiliation:
Division of Biological Science, Graduate School of Biology-oriented Science and Technology, Kinki University, 930 Nishimitani, Kinokawa, Wakayama 649-6493, Japan.
Noriyoshi Oh
Affiliation:
Division of Biological Science, Graduate School of Biology-oriented Science and Technology, Kinki University, 930 Nishimitani, Kinokawa, Wakayama 649-6493, Japan.
Kensaku Kitada
Affiliation:
Kitayama Labes Co. Ltd., Ina Research Laboratory, Ina, Nagano 396-0021, Japan.
Kazuya Matsumoto
Affiliation:
Division of Biological Science, Graduate School of Biology-oriented Science and Technology, Kinki University, 930 Nishimitani, Kinokawa, Wakayama 649-6493, Japan.
Kazuhiro Saeki
Affiliation:
Division of Biological Science, Graduate School of Biology-oriented Science and Technology, Kinki University, 930 Nishimitani, Kinokawa, Wakayama 649-6493, Japan.
Takeshi Taniguchi
Affiliation:
Taniguchi Hospital, 1–5-20 Onishi, Izumisano, Osaka 598-0043, Japan.
Yoshihiko Hosoi*
Affiliation:
Department of Genetic Development, Kinki University, Wakayama 649-6493, Japan. Division of Biological Science, Graduate School of Biology-oriented Science and Technology, Kinki University, 930 Nishimitani, Kinokawa, Wakayama 649-6493, Japan.
*
All correspondence to: Y. Hosoi. Department of Genetic Development, Kinki University, Wakayama 649-6493, Japan. Tel: +81 736 77 3888. Fax: +81 736 77 4754. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

We examined growing oocytes collected from follicles remaining in superovulated rabbit ovaries, that were grown (in vitro growth, IVG) and matured (in vitro maturation, IVM) in vitro. We produced somatic cell nuclear transfer (SCNT) embryos using the mature oocytes and examined whether these embryos have the ability to develop to the blastocyst stage. In addition, we examined the effects of trichostatin A (TSA), a histone deacetylase inhibitor (HDACi), on the developmental competence of SCNT embryos derived from IVG–IVM oocytes. After growth for 7 days and maturation for 14–16 h in vitro, the growing oocytes reached the metaphase II stage (51.4%). After SCNT, these reconstructed embryos reached the blastocyst stage (20%). Furthermore, the rate of development to the blastocyst stage and the number of cells in the blastocysts in SCNT embryos derived from IVG–IVM oocytes were significantly higher for TSA-treated embryos compared with TSA-untreated embryos (40.6 versus 21.4% and 353.1 ± 59.1 versus 202.5 ± 54.6, P < 0.05). These results indicate that rabbit SCNT embryos using IVG–IVM oocytes have the developmental competence to reach the blastocyst stage.

Keywords

FollicleIn vitro growthNuclear transferRabbitTrichostatin A
Type
Research Article
Information
Zygote , Volume 23 , Issue 4 , August 2015 , pp. 494 - 500
Copyright
Copyright © Cambridge University Press 2014 

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

Betthauser, J., Forsberg, E., Augenstein, M., Childs, L., Eilertsen, K., Enos, J., Forsythe, T., Golueke, P., Jurgella, G., Koppang, R., Lesmeister, T., Mallon, K., Mell, G., Misica, P., Pace, M., Pfister-Genskow, M., Strelchenko, N., Voelker, G., Watt, S., Thompson, S. & Bishop, M. (2000). Production of cloned pigs from in vitro systems. Nat. Biotechnol. 18, 1055–9.CrossRefGoogle ScholarPubMed
Chesné, P., Adenot, P.G., Viglietta, C., Baratte, M., Boulanger, L. & Renard, J.P. (2002). Cloned rabbits produced by nuclear transfer from adult somatic cells. Nat. Biotechnol. 20, 366–9.CrossRefGoogle ScholarPubMed
Cibelli, J.B., Stice, S.L., Golueke, P.J., Kane, J.J., Jerry, J., Blackwell, C., Ponce de Leon, F.A. & Robl, J.M. (1998). Transgenic bovine chimeric offspring produced from somatic cell-derived stem-like cells. Nat. Biotechnol. 16, 642–6.CrossRefGoogle ScholarPubMed
Cortvrindt, R., Smitz, J. & Van Steirteghem, A.C. (1996). In-vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepuberal mice in a simplified culture system. Hum. Reprod. 11, 2656–66.CrossRefGoogle Scholar
Dean, W., Santos, F., Stojkovic, M., Zakhartchenko, V., Walter, J., Wolf, E. & Reik, W. (2001). Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc. Natl. Acad. Sci. USA 98, 13734–8.CrossRefGoogle ScholarPubMed
Donnez, J., Martinez-Madrid, B., Jadoul, P., Van Langendonckt, A., Demylle, D. & Dolmans, M.M. (2006). Ovarian tissue cryopreservation and transplantation: a review. Hum. Reprod. Update 12, 519–35.CrossRefGoogle ScholarPubMed
Eppig, J.J. & O'Brien, M.J. (1996). Development in vitro of mouse oocytes from primordial follicles. Biol. Reprod. 54, 197–207.CrossRefGoogle ScholarPubMed
Eppig, J.J. & Schroeder, A.C. (1989). Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biol. Reprod. 41, 268–76.CrossRefGoogle ScholarPubMed
Garibaldi, B.A. & Goad, M.E. (1988). Lipid keratopathy in the watanabe (WHHL) rabbit. Vet. Pathol. 25, 173–4.CrossRefGoogle ScholarPubMed
Gutierrez, C.G., Ralph, J.H., Telfer, E.E., Wilmut, I. & Webb, R. (2000). Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Biol. Reprod. 62, 1322–8.CrossRefGoogle ScholarPubMed
Hashimoto, S., Kimura, K., Kuramochi, T., Aoyagi, K., Hirako, M., Kawaguchi, M., Iwata, H., Hirao, M., Kitada, K., Hirasawa, K. & Ueda, M. (2007a). Responsiveness of rabbits to superovulation treatment by a single injection of follicle-stimulating hormone with aluminum hydroxide gel. Mol. Reprod. Dev. 74, 1208–12.CrossRefGoogle ScholarPubMed
Hashimoto, S., Ohsumi, K., Tsuji, Y., Harauma, N., Miyata, Y., Fukuda, A., Hosoi, Y., Iritani, A. & Morimoto, Y. (2007b). Growing porcine oocyte–granulosa cell complexes acquired meiotic competence during in vitro culture. J. Reprod. Dev. 53, 379–84.CrossRefGoogle ScholarPubMed
Hirao, Y., Nagai, T., Kubo, M., Miyano, T., Miyake, M. & Kato, S. (1994). In-vitro growth and maturation of pig oocytes. J. Reprod. Fertil. 100, 333–9.CrossRefGoogle ScholarPubMed
Hirao, Y., Itoh, T., Shimizu, M., Iga, K., Aoyagi, K., Kobayashi, M., Kacchi, M., Hoshi, H. & Takenouchi, N. (2004). In vitro growth and development of bovine oocyte-granulosa cell complexes on the flat substratum: effects of high polyvinylpyrrolidone concentration in culture medium. Biol. Reprod. 70, 83–91.CrossRefGoogle ScholarPubMed
Hirao, Y., Naruse, K., Kaneda, M., Somfai, T., Iga, K., Shimizu, M., Akagi, S., Cao, F., Kono, T., Nagai, T. & Takenouchi, N. (2013). Production of fertile offspring from oocytes grown in vitro by nuclear transfer in cattle. Biol. Reprod. 89, 1–11.CrossRefGoogle ScholarPubMed
Holker, M., Petersen, B., Hassel, P., Kues, W.A., Lemme, E., Lucas-Hahn, A. & Niemann, H. (2005). Duration of in vitro maturation of recipient oocytes affects blastocyst development of cloned porcine embryos. Cloning Stem Cells. 7, 35–44.CrossRefGoogle ScholarPubMed
Hosoi, Y., Niwa, K., Hatanaka, S. & Iritani, A. (1981). Fertilization in vitro of rabbit eggs by epididymal spermatozoa capacitated in a chemically defined medium. Biol. Reprod. 24, 637–42.CrossRefGoogle Scholar
Johnson, L.D., Albertini, D.F., McGinnis, L.K. & Biggers, J.D. (1995). Chromatin organization, meiotic status and meiotic competence acquisition in mouse oocytes from cultured ovarian follicles. J. Reprod. Fertil. 104, 277–84.CrossRefGoogle ScholarPubMed
Kanaya, H., Hashimoto, S., Teramura, T., Morimoto, Y., Matsumoto, K., Saeki, K., Iritani, A. & Hosoi, Y. (2007). Mitochondrial dysfunction of in vitro grown rabbit oocytes results in preimplantation embryo arrest after activation. J. Reprod. Dev. 53, 631–7.CrossRefGoogle ScholarPubMed
Kato, Y., Tani, T., Sotomaru, Y., Kurokawa, K., Kato, J., Doguchi, H., Yasue, H. & Tsunoda, Y. (1998). Eight calves cloned from somatic cells of a single adult. Science. 282, 2095–8.CrossRefGoogle ScholarPubMed
Keefer, C.L. (2008). Lessons learned from nuclear transfer (cloning). Theriogenology 69, 48–54.CrossRefGoogle ScholarPubMed
Kishigami, S., Mizutani, E., Ohta, H., Hikichi, T., Thuan, N.V., Wakayama, S., Bui, H.T. & Wakayama, T. (2006). Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem. Biophys. Res. Commun. 340, 183–9.CrossRefGoogle ScholarPubMed
Martins, F.S., Celestino, J.J., Saraiva, M.V., Matos, M.H., Bruno, J.B., Rocha-Junior, C.M., Lima-Verde, I.B., Lucci, C.M., Bao, S.N. & Figueiredo, J.R. (2008). Growth and differentiation factor-9 stimulates activation of goat primordial follicles in vitro and their progression to secondary follicles. Reprod. Fertil. Dev. 20, 916–24.CrossRefGoogle ScholarPubMed
Meng, Q., Polgar, Z., Liu, J. & Dinnyes, A. (2009). Live birth of somatic cell-cloned rabbits following trichostatin A treatment and cotransfer of parthenogenetic embryos. Cloning Stem Cells 11, 203–8.CrossRefGoogle ScholarPubMed
Miyoshi, K., Rzucidlo, S.J., Gibbons, J.R., Arat, S. & Stice, S.L. (2001). Development of porcine embryos reconstituted with somatic cells and enucleated metaphase I and II oocytes matured in a protein free medium. BMC Dev. Biol. 1, 12.CrossRefGoogle Scholar
Nayudu, P.L. & Osborn, S.M. (1992). Factors influencing the rate of preantral and antral growth of mouse ovarian follicles in vitro. J. Reprod. Fertil. 95, 349–62.CrossRefGoogle ScholarPubMed
Ogonuki, N., Inoue, K., Miki, H., Mochida, K., Hatori, M., Okada, H., Takeiri, S., Shimozawa, N., Nagashima, H., Sankai, T. & Ogura, A. (2005). Differential development of rabbit embryos following microinsemination with sperm and spermatids. Mol. Reprod. Dev. 72, 411–7.CrossRefGoogle ScholarPubMed
Ohgane, J., Wakayama, T., Senda, S., Yamazaki, Y., Inoue, K., Ogura, A., Marh, J., Tanaka, S., Yanagimachi, R. & Shiota, K. (2004). The Sall3 locus is an epigenetic hotspot of aberrant DNA methylation associated with placentomegaly of cloned mice. Genes Cell. 9, 253–60.CrossRefGoogle ScholarPubMed
Polejaeva, I.A., Chen, S.H., Vaught, T.D., Page, R.L., Mullins, J., Ball, S., Dai, Y., Boone, J., Walker, S., Ayares, D.L., Colman, A. & Campbell, K.H. (2000). Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407, 86–90.CrossRefGoogle ScholarPubMed
Shi, L.H., Miao, Y.L., Ouyang, Y.C., Huang, J.C., Lei, Z.L., Yang, J.W., Han, Z.M., Song, X.F., Sun, Q.Y. & Chen, D.Y. (2008). Trichostatin A (TSA) improves the development of rabbit-rabbit intraspecies cloned embryos, but not rabbit-human interspecies cloned embryos. Dev. Dyn. 237, 640–8.CrossRefGoogle Scholar
Silva, C.M., Matos, M.H., Rodrigues, G.Q., Faustino, L.R., Pinto, L.C., Chaves, R.N., Araujo, V.R., Campello, C.C. & Figueiredo, J.R. (2010). In vitro survival and development of goat preantral follicles in two different oxygen tensions. Anim. Reprod. Sci. 117, 83–9.CrossRefGoogle ScholarPubMed
Sugimoto, H., Miyamoto, Y., Tsuji, Y., Morimoto, K., Taniguchi, T., Morimoto, Y. & Hosoi, Y. (2009). Examination of effective culture methods for rabbit preantral follicles. J. Mamm. Ova. Res. 26, 221–6.CrossRefGoogle Scholar
Sugimoto, H., Kida, Y., Miyamoto, Y., Kitada, K., Matsumoto, K., Saeki, K., Taniguchi, T. & Hosoi, Y. (2012). Growth and development of rabbit oocytes in vitro: effect of fetal bovine serum concentration on culture medium. Theriogenology 78, 1040–7.CrossRefGoogle ScholarPubMed
Takahashi, R., Kuramochi, T., Aoyagi, K., Hashimoto, S., Miyoshi, I., Kasai, N., Hakamata, Y., Kobayashi, E. & Ueda, M. (2007). Establishment and characterization of CAG/EGFP transgenic rabbit line. Transgenic. Res. 16, 115–20.CrossRefGoogle ScholarPubMed
Wakayama, T., Perry, A.C.F., Zuccotti, M., Johnson, K.R. & Yanagimachi, R. (1998). Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature. 394, 369–74.CrossRefGoogle ScholarPubMed
Wells, D.N., Misica, P.M., Day, A.M. & Tervit, H.R. (1997). Production of cloned lambs from an established embryonic cell line: a comparison between in vivo- and in vitro-matured cytoplasts. Biol. Reprod. 57, 385–93.CrossRefGoogle ScholarPubMed
Wilmut, I., Schnieke, A.E., McWhir, J., Kind, A.J. & Campbell, K.H.S. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810–3.CrossRefGoogle ScholarPubMed
Yamamoto, K., Otoi, T., Koyama, N., Horikita, N., Tachikawa, S. & Miyano, T. (1999). Development to live young from bovine small oocytes after growth, maturation and fertilization in vitro. Theriogenology 52, 81–9.CrossRefGoogle ScholarPubMed