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Development of interspecies cloned embryos reconstructed with rabbit (Oryctolagus cuniculus) oocytes and cynomolgus monkey (Macaca fascicularis) fibroblast cell nuclei

Published online by Cambridge University Press:  05 April 2012

Takayuki Yamochi
Affiliation:
Division of Biological Science, Graduate School of Biology-Oriented Science and Technology, Kinki University, Wakayama, 649-6493, Japan.
Yuta Kida
Affiliation:
Division of Biological Science, Graduate School of Biology-Oriented Science and Technology, Kinki University, Wakayama, 649-6493, Japan.
Noriyoshi Oh
Affiliation:
Division of Biological Science, Graduate School of Biology-Oriented Science and Technology, Kinki University, Wakayama, 649-6493, Japan.
Sei Ohta
Affiliation:
Eve Bioscience Co. Ltd, Wakayama, 648–0003, Japan.
Tomoko Amano
Affiliation:
Division of Biological Science, Graduate School of Biology-Oriented Science and Technology, Kinki University, Wakayama, 649-6493, Japan.
Masayuki Anzai
Affiliation:
Institute of Advanced Technology, Kinki University, Wakayama, 642-0017, Japan.
Hiromi Kato
Affiliation:
Institute of Advanced Technology, Kinki University, Wakayama, 642-0017, Japan.
Satoshi Kishigami
Affiliation:
Division of Biological Science, Graduate School of Biology-Oriented Science and Technology, Kinki University, Wakayama, 649-6493, Japan.
Tasuku Mitani
Affiliation:
Institute of Advanced Technology, Kinki University, Wakayama, 642-0017, Japan.
Kazuya Matsumoto
Affiliation:
Division of Biological Science, Graduate School of Biology-Oriented Science and Technology, Kinki University, Wakayama, 649-6493, Japan. Institute of Advanced Technology, Kinki University, Wakayama, 642-0017, Japan.
Kazuhiro Saeki
Affiliation:
Division of Biological Science, Graduate School of Biology-Oriented Science and Technology, Kinki University, Wakayama, 649-6493, Japan. Institute of Advanced Technology, Kinki University, Wakayama, 642-0017, Japan.
Makoto Takenoshita
Affiliation:
Eve Bioscience Co. Ltd, Wakayama, 648–0003, Japan.
Akira Iritani
Affiliation:
Division of Biological Science, Graduate School of Biology-Oriented Science and Technology, Kinki University, Wakayama, 649-6493, 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, Wakayama, 649-6493, Japan. Institute of Advanced Technology, Kinki University, Wakayama, 642-0017, 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]

Summary

Interspecies somatic cell nuclear transfer (ISCNT) has been proposed as a technique to produce cloned offspring of endangered species as well as to investigate nucleus–cytoplasm interactions in mammalian embryo. However, it is still not known which embryo culture medium is optimal for ISCNT embryos for the nuclear donor or the oocyte recipient. We assessed the effects of the culture medium on the developmental competence of the ISCNT embryos by introducing cynomolgus monkey (Macaca fascicularis) fibroblast nuclei into enucleated rabbit (Oryctolagus cuniculus) oocytes (monkey–rabbit embryo). The monkey–rabbit ISCNT embryos that were cultured in mCMRL-1066 developed to the blastocyst stage, although all monkey–rabbit ISCNT embryos cultured in M199 were arrested by the 4-cell stage. When monkey–rabbit ISCNT and rabbit–rabbit somatic cell nuclear transfer (SCNT) embryos were cultured in mCMRL-1066, the blastocyst cell numbers of the monkey–rabbit ISCNT embryos corresponded to the cell numbers of the control rabbit–rabbit SCNT embryos, which were produced from a rabbit fibroblast nucleus and an enucleated rabbit oocyte. In addition, the presence of mitochondria, which were introduced with monkey fibroblasts into rabbit recipient cytoplasm, was confirmed up to the blastocyst stage by polymerase chain reaction (PCR). This study demonstrated that: (1) rabbit oocytes can reprogramme cynomolgus monkey somatic cell nuclei, and support preimplantation development; (2) monkey–rabbit ISCNT embryos developed well in monkey culture medium at early embryonic developmental stages; (3) the cell number of monkey–rabbit ISCNT embryos is similar to that of rabbit–rabbit SCNT embryos; and (4) the mitochondrial fate of monkey–rabbit ISCNT embryos is heteroplasmic from the time just after injection to the blastocyst stage that has roots in both rabbit oocytes and monkey fibroblasts.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012 

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References

Baguisi, A., Behboodi, E., Melican, D.T., Pollock, J.S., Destrempes, M.M., Cammuso, C., Williams, J.L., Nims, S.D., Porter, C.A., Midura, P., Palacios, M.J. & Ayres, SL. (1999). Production of goats by somatic cell nuclear transfer. Nat. Biotechnol. 17, 456–61.CrossRefGoogle ScholarPubMed
Chen, D.Y., Wen, D.C., Zhang, Y.P., Sun, Q.Y., Han, Z.M., Liu, Z.H., Shi, P., Li, J.S., Xiangyu, J.G., Lian, L., Kou, Z.H., Wu, Y.Q., Chen, Y.C., Wang, P.Y. & Zhang, H.M. (2002). Interspecies implantation and mitochondria fate of panda–rabbit cloned embryos. Biol. Reprod. 67, 637–42.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
Dominko, T., Mitalipova, M., Haley, B., Beyhan, Z., Memili, E., McKusick, B. & First, N.L. (1999). Bovine oocyte cytoplasm supports development of embryos produced by nuclear transfer of somatic cell nuclei from various mammalian species. Biol. Reprod. 60, 1496–502.CrossRefGoogle ScholarPubMed
Evans, M.J., Gurer, C., Loike, J.D., Wilmut, I., Schnieke, A.E. & Schon, E.A. (1999). Mitochondrial DNA genotypes in nuclear transfer-derived cloned sheep. Nat. Genet. 23, 90–3.CrossRefGoogle ScholarPubMed
Folch, J., Cocero, M.J., Chesné, P., Alabart, J.L., Domínguez, V., Cognié, Y., Roche, A., Fernández-Árias, A., Martí, J.I., Sánchez, P., Echegoyen, E., Beckers, J.F., Bonastre, A.S. & Vignon, X. (2009). First birth of an animal from an extinct subspecies (Capra pyrenaica pyrenaica) by cloning. Theriogenology 71, 1026–34.CrossRefGoogle ScholarPubMed
Galli, C., Lagutina, I., Crotti, G., Colleoni, S., Turini, P., Ponderato, N., Duchi, R. & Lazzari, G. (2003). A cloned horse born to its dam twin. Nature 424–35.CrossRefGoogle Scholar
Gómez, M.C., Pope, C.E., Giraldo, A., Lyons, L.A., Harris, R.F., King, A.L., Cole, A., Robert, A., Godke, R.A. & Dresser, B.L. (2004). Birth of African wildcat cloned kittens born from domestic cats. Cloning Stem Cells 6, 247–58.CrossRefGoogle ScholarPubMed
Gómez, M.C., Pope, C.E., Kutner, R.H., Ricks, D.M., Lyons, L.A., Ruhe, M., Dumas, C., Lyons, J., López, M., Dresser, B.L. & Reiser, J. (2008). Nuclear transfer of sand cat cells into enucleated domestic cat oocytes is affected by cryopreservation of donor cells. Cloning Stem Cells 10, 469–83.CrossRefGoogle ScholarPubMed
Gómez, M.C., Pope, C.E., Ricks, D.M., Lyons, J., Dumas, C. & Dresser, B.L. (2009). Cloning endangered felids using heterospecific donor oocytes and interspecies embryo transfer. Reprod. Fertil. Dev. 21, 7682.CrossRefGoogle ScholarPubMed
Hua, S., Zhang, Y., Song, K., Song, J., Zhang, Z., Zhang, L., Zhang, C., Cao, J. & Ma, L. (2008) Development of bovine–ovine interspecies cloned embryos and mitochondria segregation in blastomeres during preimplantation. Anim. Reprod. Sci. 105, 245–57.CrossRefGoogle ScholarPubMed
Iwata, H., Akamatsu, S., Minami, N. & Yamada, M. (1998). Effects of antioxidants on the development of bovine IVM/IVF embryos in various concentrations of glucose. Theriogenology 50, 365–75.CrossRefGoogle ScholarPubMed
Jiang, M.X., Yang, C.X., Zhang, L.S., Zheng, Y.L., Liu, S.Z., Sun, Q.Y. & Chen, D.Y. (2004). The effects of chemical enucleation combined with whole cell intracytoplasmic injection on panda–rabbit interspecies nuclear transfer. Zygote 12, 315–20.CrossRefGoogle ScholarPubMed
Jiang, Y., Chen, T., Nan, C.L., Ouyang, Y.C., Sun, Q.Y. & Chen, D.Y. (2005) In vitro culture and mtDNA fate of ibex–rabbit nuclear transfer embryos. Zygote 13, 233–40.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 single adult. Science 282, 2095–8.CrossRefGoogle ScholarPubMed
Kim, M.K., Jang, G., Oh, H.J., Yuda, F., Kim, H.J., Hwang, W.S., Hossein, M.S., Kim, J.J., Shin, N.S., Kang, S.K. & Lee, B.C. (2007). Endangered wolves cloned from adult somatic cells. Cloning Stem Cells 9, 130137.CrossRefGoogle ScholarPubMed
Lanza, R.P., Cibelli, I.B., Diaz, F., Moraes, C.T., Farin, C.E., Hammer, C.J., West, M.D. & Damiani, P. (2000). Cloning of an endangered species (Bos gaurus) using interspecies nuclear transfer. Cloning 2, 7990.CrossRefGoogle ScholarPubMed
Lee, B.C., Kim, M.K., Jang, G., Oh, H.J., Yuda, F., Kim, H.J., Shamim, M.H., Kim, J.J., Kang, S.K., Schatten, G. & Hwang, W.S. (2005). Dogs cloned from adult somatic cells. Nature 436, 604.CrossRefGoogle ScholarPubMed
Li, Z., Sun, X., Chen, J., Liu, X., Wisely, S.M., Zhou, Q., Renard, J.P., Leno, G.H. & Engelhardt, J.F. (2006). Cloned ferrets produced by somatic cell nuclear transfer. Dev. Biol. 293, 439–48.CrossRefGoogle ScholarPubMed
Liu, S.Z., Zhou, Z.M., Chen, T., Zhang, Y.L., Wen, D.C., Kou, Z.H., Li, Z.D., Sun, Q.Y. & Chen, D.Y. (2004). Blastocysts produced by nuclear transfer between chicken blastodermal cells and rabbit oocytes. Mol. Reprod. Dev. 69, 296302.CrossRefGoogle ScholarPubMed
Loi, P., Ptak, G., Fulka, J. Jr., Cappai, P. & Clinton, M. (2001). Genetic rescue of an endangered mammal by cross-species nuclear transfer using post-mortem somatic cells. Nat. Biotech. 19, 962–4.CrossRefGoogle ScholarPubMed
Ma, L.B., Yang, L., Hua, S., Cao, J.W., Li, J.X. & Zhang, Y. (2008). Development in vitro and mitochondrial fate of interspecies cloned embryos. Reprod. Dom. Anim. 43, 279.CrossRefGoogle ScholarPubMed
Narita, J., Tsuchiya, H., Takada, T. & Torii, R. (2007). Cloned blastocysts produced by nuclear transfer from somatic cells in cynomolgus monkeys (Macaca fascicularis). Primate 48, 232–40.CrossRefGoogle Scholar
Oh, H.J., Kim, M.K., Jang, G., Kim, H.J., Hong, S.G., Park, J.E., Park, K., Park, C., Sohn, S.H., Kim, D.Y., Shin, N.S. & Lee, B.C. (2008). Cloning endangered gray wolves (Canis lupus) from somatic cells collected postmortem. Theriogenology 70, 638–47.CrossRefGoogle ScholarPubMed
Polejaeva, I.A., Chen, S.H., Vaught, T.D., Page, R.L., Mullins, J., Suyapa, B., 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, 8690.CrossRefGoogle ScholarPubMed
Schramm, R.D. & Bavister, B.D. (1996). Development of in-vitro-fertilized primate embryos into blastocysts in a chemically defined, protein-free culture medium. Hum. Reprod. 11, 1690–7.CrossRefGoogle Scholar
Shi, D., Lu, F., Wei, Y., Cui, K., Yang, S., Wei, J. & Liu, Q. (2007). Buffalos (Bubalus bubalis) cloned by nuclear transfer of somatic cells. Biol. Reprod. 77, 285–91.CrossRefGoogle ScholarPubMed
Shin, T., Kraemer, D., Pryor, J., Liu, L., Rugila, J., Howe, L., Buck, S., Murphy, K., Lyons, L. & Westhusin, M. (2002). A cat cloned by nuclear transplantation. Nature 415, 859.CrossRefGoogle ScholarPubMed
Sutovsky, P., Moreno, R.D., Santos, J.R., Dominko, T., Simerly, C. & Schatten, G. (2000). Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of itochondrial inheritance in mammalian embryos. Biol. Reprod. 63, 582–90.CrossRefGoogle Scholar
Tao, Y., Liu, J., Zhang, Y., Zhang, M., Fang, J., Han, W., Zhang, Z., Liu, Y., Ding, J. & Zhang, X. (2009). Fibroblast cell line establishment, cryopreservation and interspecies embryos reconstruction in red panda (Ailurus fulgens). Zygote 17, 117–24.CrossRefGoogle ScholarPubMed
Thongphakdee, A., Numchaisrika, P., Omsongkram, S., Chatdarong, K., Kamolnorranath, S., Dumnui, S. & Techakumphu, M. (2006). In vitro development of marbled cat embryos derived from interspecies somatic cell nuclear transfer. Domest. Anim. 41, 219–26.CrossRefGoogle ScholarPubMed
Wakayama, T., Perry, A.C., 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
Wani, N.A., Wernery, U., Hassan, F.A.H., Wernery, R. & Skidmore, J.A. (2010). Production of the first cloned camel by somatic cell nuclear transfer. Biol. Reprod. 82, 373–79.CrossRefGoogle ScholarPubMed
Wen, D.C., Yang, C.X., Cheng, Y., Li, J.S., Liu, Z.H., Sun, Q.Y., Zhang, J.X., Lei, L., Wu, Y.Q., Kou, Z.H. & Chen, D.Y. (2003). Comparison of developmental capacity for intra- and interspecies cloned cat (Felis catus) embryos. Mol. Reprod. Dev. 66, 3845.CrossRefGoogle ScholarPubMed
Wen, D.C., Bi, C.M., Xu, Y., Yang, C.X., Zhu, Z.Y., Sun, Q.Y. & Chen, D.Y. (2005). Hybrid embryos produced by transferring panda or cat somatic nuclei into rabbit MII oocytes can develop to blastocyst in vitro. J. Exp. Zool. 303, 689–97.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
Woods, G.L., White, K.L., Vanderwall, D.K., Li, G.P., Aston, K.I., Bunch, T.D. & Meerdo, L.N., Pate, B.J. (2003). A mule cloned from fetal cells by nuclear transfer. Science 301, 1063.CrossRefGoogle ScholarPubMed
Yang, C.X., Han, Z.M., Wen, D.C., Sun, Q.Y., Zhang, K.Y., Zhang, L.S., Wu, Y.Q., Kou, Z.H & Chen, D.Y. (2003). In vitro development and mitochondrial fate of macaca–rabbit cloned embryos. Mol. Reprod. Dev. 65, 396401.CrossRefGoogle ScholarPubMed
Yang, C.X., Kou, Z.H., Wang, K., Jiang, Y., Mao, W.W., Sun, Q.Y., Sheng, H.Z. & Chen, D.Y. (2004). Quantitative analysis of mitochondrial DNAs in macaque embryos reprogrammed by rabbit oocytes. Reproduction 127, 201–5.CrossRefGoogle ScholarPubMed
Yang, C.Y., Li, R.C., Pang, C.Y., Yang, B.Z., Qin, G.S., Chen, M.T., Zhang, X.F., Huang, F.X., Zheng, H.Y., Huang, Y.J. & Liang, X.W. (2010). Study on the inter-subspecies nuclear transfer of river buffalo somatic cell nuclei into swamp buffalo oocyte cytoplasm. Anim. Reprod. Sci. 121, 7883.CrossRefGoogle Scholar
Zhao, Z.J., Ouyang, Y.C., Nan, C.L., Lei, Z.L., Song, X.F., Sun, Q.Y. & Chen, D.Y. (2006). Rabbit oocyte cytoplasm supports development of nuclear transfer embryos derived from the somatic cells of the camel and Tibetan antelope. J. Reprod. Dev. 52, 449–59.CrossRefGoogle ScholarPubMed
Zhao, J.Z., LI, R.C., Cao, H.H., Jiang, M.X., Ouyang, Y.C., Nan, C.L., Lei, Z.L., Song, X.F., Sun, Q.Y. & Chen, D.Y (2007). Interspecies nuclear transfer of tibetan antelope using caprine oocyte as recipient. Mol. Reprod. Dev. 74, 412–9.CrossRefGoogle ScholarPubMed
Zheng, Y.L., Jiang, M.X., Zhang, Y.L., Sun, Q.Y. & Chen, D.Y. (2004). Effect of oocyte age, cumulus cells and injection methods on in vitro development of intracytoplasmic sperm injection rabbit embryos. Zygote 12, 7580.CrossRefGoogle ScholarPubMed
Zhou, Q., Renard, J.P., Le, F.G., Brochard, V., Beaujean, N., Cherifi, Y., Fraichard, A. & Cozzi, J. (2003). Generation of fertile cloned rats by regulating oocyte activation. Science 302, 1179.CrossRefGoogle ScholarPubMed