Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Cloning in companion animal, non-domestic and endangered species: can the technology become a practical reality?

Gabriela F. Mastromonaco A and W. Allan King A B
+ Author Affiliations
- Author Affiliations

A Department of Biomedical Sciences, Ontario Veterinary College, University of Guelph, Guelph, Ontario N1G 2W1, Canada.

B Corresponding author. Email: waking@uoguelph.ca

Reproduction, Fertility and Development 19(6) 748-761 https://doi.org/10.1071/RD07034
Submitted: 26 February 2007  Accepted: 27 April 2007   Published: 2 August 2007

Abstract

Somatic cell nuclear transfer (SCNT) can provide a unique alternative for the preservation of valuable individuals, breeds and species. However, with the exception of a handful of domestic animal species, successful production of healthy cloned offspring has been challenging. Progress in species that have little commercial or research interest, including many companion animal, non-domestic and endangered species (CANDES), has lagged behind. In this review, we discuss the current and future status of SCNT in CANDES and the problems that must be overcome to improve pre- and post-implantation embryo survival in order for this technology to be considered a viable tool for assisted reproduction in these species.


Acknowledgements

The authors would like to thank the funding agencies, Natural Sciences and Engineering Council of Canada, Canada Research Chair Program, and Ontario Graduate Scholarships, for their support of the research in the laboratory of W. A. King.


References

Adams, A. M. , Pratt, S. L. , Gibbons, J. R. , Arat, S. , Respess, D. S. , and Stice, S. L. (2004). Production of a cloned calf using kidney cells obtained from a 48-hour cooled carcass. Reprod. Fertil. Dev. 16, 133.[Abstract]
Crossref | GoogleScholarGoogle Scholar | Ball M. (2005). Copied cat gives pause at veterinarian’s convention. Las Vegas Sun, 22 February 2005.

Barrientos, A. , Kenyon, L. , and Moraes, C. T. (1998). Human xenomitochondrial cybrids. Cellular models of mitochondrial complex I deficiency. J. Biol. Chem. 273, 14210–14217.
Crossref | GoogleScholarGoogle Scholar | PubMed | Popescu P. C. (1990). Chromosomes of the cow and bull. In ‘Domestic Animal Cytogenetics’. (Ed. R. A. McFeely.) pp. 41–71. (Academic Press: San Diego, CA.)

Raff, M. C. (1992). Social controls on cell survival and cell death. Nature 356, 397–400.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Rangel-Figueiredo, T. , and Iannuzzi, L. (1991). A cattle breed close to 58 diploid number due to high frequency of rob(1;29). Hereditas 115, 73–78.
PubMed |

Rideout, W. M. , Eggan, K. , and Jaenisch, R. (2001). Nuclear cloning and epigenetic reprogramming of the genome. Science 293, 1093–1098.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Rubin, H. (1997). Cell aging in vivo and in vitro. Mech. Ageing Dev. 98, 1–35.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Saikhun, J. , Pavasuthipaisit, K. , Jaruansuwan, M. , and Kitiyanant, Y. (2002). Xenonuclear transplantation of buffalo (Bubalus bubalis) fetal and adult somatic cell nuclei into bovine (Bos indicus) oocyte cytoplasm and their subsequent development. Theriogenology 57, 1829–1837.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sankaran, S. , and Parvin, J. D. (2006). Centrosome function in normal and tumor cells. J. Cell. Biochem. 99, 1240–1250.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sansinena, M. J. , Taylor, S. A. , Taylor, P. J. , Denniston, R. S. , and Godke, R. A. (2003). Production of nuclear transfer llama (Llama glama) embryos from in vitro matured llama oocytes. Cloning Stem Cells 5, 191–198.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sansinena, M. , Hylan, D. , Hebert, K. , Denniston, R. S. , and Godke, R. A. (2005). Banteng (Bos javanicus) embryos and pregnancies produced by interspecies nuclear transfer. Theriogenology 63, 1081–1091.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Shiga, K. , Fujita, T. , Hirose, K. , Sasae, Y. , and Nagai, Y. (1999). Production of calves by transfer of nuclei from cultured somatic cells obtained from Japanese black bulls. Theriogenology 52, 527–535.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Shin, T. , Kraemer, D. , Pryor, J. , Liu, L. , Rugila, J. , Howe, L. , Buck, S. , Murphy, K. , Lyons, L. , and Westhusin, M. (2002a). A cat cloned by nuclear transplantation. Nature 415, 859.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Shin, M. R. , Park, S. W. , Shim, H. , and Kim, N. H. (2002b). Nuclear and microtubule reorganization in nuclear-transferred bovine embryos. Mol. Reprod. Dev. 62, 74–82.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Skrzyszowska, M. , Katska, L. , Rynska, B. , Kania, G. , Smorag, Z. , and Pienkowski, M. (2002). In vitro developmental competence of domestic cat embryos after somatic cloning: a preliminary report. Theriogenology 58, 1615–1621.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Slimane Bureau, W. , Bordignon, V., , Leveillee, C., , Smith, L. C. , and King, W. A. (2003). Assessment of chromosomal abnormalities in bovine nuclear transfer embryos and in their donor cells. Cloning Stem Cells 5, 123–132.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Smith, L. C. , and Wilmut, I. (1989). Influence of nuclear and cytoplasmic activity on the development in vivo of sheep embryos after nuclear transplantation. Biol. Reprod. 40, 1027–1035.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Smith, L. C. , Bordignon, V. , Babkine, M. , Fecteau, G. , and Keefer, C. (2000a). Benefits and problems with cloning animals. Can. Vet. J. 41, 919–924.
PubMed |

Smith, L. C. , Bordignon, V. , Garcia, J. M. , and Meirelles, F. V. (2000b). Mitochondrial genotype segregation and effects during mammalian development: applications to biotechnology. Theriogenology 53, 35–46.
Crossref | GoogleScholarGoogle Scholar |

Steinborn, R. , Zakhartchenko, Z. , Jelyazkov, J. , Klein, D. , Wolf, E. , Muller, M. , and Brem, G. (1998). Composition of parental mitochondrial DNA in cloned bovine embryos. FEBS Lett. 426, 352–356.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Steinborn, R. , Schinogl, P. , Wells, D. N. , Bergthaler, A. , Muller, M. , and Brem, G. (2002). Coexistence of Bos taurus and Bos indicus mitochondrial DNAs in nuclear transfer-derived somatic cattle clones. Genetics 162, 823–829.
PubMed |

Takeda, K. , Akagi, S. , Takahashi, S. , Onishi, A. , Hanada, H. , and Pinkert, C. A. (2002). Mitochondrial activity in response to serum starvation in bovine (Bos taurus) cell culture. Cloning Stem Cells 4, 223–229.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Tamassia, M. , Heyman, Y. , Lavergne, Y. , Richard, C. , Gelin, V. , Renard, J. P. , and Chastant-Maillard, S. (2003). Evidence of oocyte donor cow effect over oocyte production and embryo development in vitro. Reproduction 126, 629–637.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Tamassia, M. , Nuttinck, F. , May-Panloup, P. , Reynier, P. , Heyman, Y. , Charpigny, G. , Stojkovic, M. , Hiendleder, S. , Renard, J. P. , and Chastant-Maillard, S. (2004). In vitro embryo production efficiency in cattle and its association with oocyte adenosine triphosphate content, quantity of mitochondrial DNA, and mitochondrial DNA haplogroup. Biol. Reprod. 71, 697–704.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Thongphakdee, A. , Numchaisrika, P. , Omsongkram, S. , Chatdarong, K. , Kamolnorranath, S. , Dumnui, S. , and Techakumphu, M. (2006). In vitro development of marbled cat embryos derived from interspecies somatic cell nuclear transfer. Reprod. Dom. Anim. 41, 219–226.
Crossref | GoogleScholarGoogle Scholar |

Tsunoda, Y. , and Kato, Y. (2002). Recent progress and problems in animal cloning. Differentiation 69, 158–161.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ty, L. V. , Hanh, N. V. , Uoc, N. T. , Duc, N. G. , Thanh, N. T. , Bui, L. C. , Huu, Q. X. , and Nguyen, B. X. (2003). Preliminary results of cell cryobanking and embryo production of black bear (Ursus thibetanus) by interspecies somatic cell nuclear transfer. Theriogenology 59, 290.[Abstract]


Uoc, N. T. , Ty, L. V. , Tuoc, D. , Due, N. H. , Hanh, N. V. , Thanh, N. T. , Bui, L. C. , Laloy, E. , and Renard, J. P. (2002). Effect of tissue sampling conditions on the in vitro multiplication and reprogramming potential of somatic cells obtained from different specimens of the saola (Pseudoryx nghetinhensis) species. Theriogenology 57, 437.[Abstract]


Vassart, M. , Greth, A. , Durand, V. , and Cribiu, E. P. (1993). Chromosomal polymorphism in sand gazelles (Gazella subgutturosa marica). J. Hered. 84, 478–481.
PubMed |

Viuff, D. , Greve, T. , Avery, B. , Hyttel, P. , Brockhoff, P. B. , and Thomsen, P. B. (2000). Chromosome aberrations in in vitro-produced bovine embryos at Days 2–5 post-insemination. Biol. Reprod. 63, 1143–1148.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wakayama, T. , Perry, A. C. F. , Zuccotti, M. , Johnson, K. R. , and Yanagimachi, R. (1998). Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394, 369–374.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wakayama, T. , Rodriguez, I. , Perry, A. C. , Yanagimachi, R. , and Mombaerts, P. (1999). Mice cloned from embryonic stem cells. Proc. Natl. Acad. Sci. USA 96, 14984–14989.
Crossref | GoogleScholarGoogle Scholar |

Wells, D. N. , Misica, P. M. , Tervit, H. R. , and Vivanco, W. H. (1998). Adult somatic cell nuclear transfer is used to preserve the last surviving cow of the Enderby Island cattle breed. Reprod. Fertil. Dev. 10, 369–378.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wells, D. N. , Misica, P. M. , and Tervit, H. R. (1999). Production of cloned calves following nuclear transfer with cultured adult mural granulosa cells. Biol. Reprod. 60, 996–1005.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wells, D. N. , Laible, G. , Tucker, F. C. , Miller, A. L. , and Oliver, J. E. , et al. (2003). Coordination between donor cell type and cell cycle stage improves nuclear cloning efficiency in cattle. Theriogenology 59, 45–59.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wen, D. , Yang, C. , Cheng, Y. , Li, J. , and Liu, Z. , et al. (2003). Comparison of developmental capacity for intra- and interspecies cloned cat (Felis catus) embryos. Mol. Reprod. Dev. 66, 38–45.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wen, D. C. , Bi, C. M. , Xu, Y. , Yang, C. X. , Zhu, Z. Y. , Sun, Q. Y. , and 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. Zoolog. A Comp. Exp. Biol. 303A, 689–697.
Crossref | GoogleScholarGoogle Scholar |

Westhusin, M. E. , Burghardt, R. C. , Ruglia, J. N. , Willingham, L. A. , Liu, L. , Shin, T. , Howe, L. M. , and Kraemer, D. C. (2001). Potential for cloning dogs. J. Reprod. Fertil. Suppl. 57, 287–293.
PubMed |

White, K. L. , Bunch, T. D. , Mitalipov, S. , and Reed, W. A. (1999). Establishment of pregnancy after the transfer of nuclear transfer embryos produced from the fusion of Argali (Ovis ammon) nuclei into domestic sheep (Ovis aries) enucleated oocytes. Cloning 1, 47–54.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Williams, J. B. , Shin, T. , Liu, L. , Flores-Foxworth, G. , Romano, J. , Blue-McClendon, A. , Kraemer, D. , and Westhusin, M. E. (2006). Cloning of exotic/endangered species: desert bighorn sheep. Methods Mol. Biol. 348, 169–182.
PubMed |

Wilmut, I. , Schnieke, A. E. , McWhir, J. , King, A. J. , and Campbell, K. H. S. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810–813.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wilmut, I. , Beaujean, N. , de Sousa, P. A. , Dinnyes, A. , King, T. J. , Paterson, L. A. , Wells, D. N. , and Young, L. E. (2002). Somatic cell nuclear transfer. Nature 419, 583–586.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wolf, D. P. , Meng, L. , Ouhibi, N. , and Zelinski-Wooten, M. (1999). Nuclear transfer in the Rhesus monkey: practical and basic implications. Biol. Reprod. 60, 199–204.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Woods, G. L. , White, K. L. , Vanderwall, D. K. , Li, G. , Aston, K. I. , Bunch, T. D. , Meerdo, L. N. , and Pate, B. J. (2003). A mule cloned from fetal cells by nuclear transfer. Science 301, 1063.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wrenzycki, C. , Wells, D. , Herrmann, D. , Miller, A. , Oliver, J. , Tervit, R. , and Niemann, H. (2001). Nuclear transfer protocol affects messenger RNA expression patterns in cloned bovine blastocysts. Biol. Reprod. 65, 309–317.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yang, C. , Han, Z. , Wen, D. , Sun, Q. , Zhang, K. , Zhang, L. , Wu, Y. , Kou, Z. , and Chen, D. (2003). In vitro development and mitochondrial fate of macaca-rabbit cloned embryos. Mol. Reprod. Dev. 65, 396–401.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yang, C. X. , Kou, Z. H. , Wang, K. , Jiang, Y. , Mao, W. W. , Sun, Q. Y. , Sheng, H. Z. , and Chen, D. Y. (2004). Quantitative analysis of mitochondrial DNAs in macaque embryos reprogrammed by rabbit oocytes. Reproduction 127, 201–205.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yin, X. , Lee, Y. , Lee, H. , Kim, N. , Kim, L. , Shin, H. , and Kong, I. (2006a). In vitro production and initiation of pregnancies in inter-genus nuclear transfer embryos derived from leopard cat (Prionailurus bengalensis) nuclei fused with domestic cat (Felis silvestris catus) enucleated oocytes. Theriogenology 66, 275–282.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yin, X. H. , Lee, Y. H. , Jin, J. Y. , Kim, N. H. , and Kong, I. K. (2006b). Nuclear and microtubule remodeling and in vitro development of nuclear transferred cat oocytes with skin fibroblasts of the domestic cat (Felis silvestris catus) and leopard cat (Prionailurus bengalensis). Anim. Reprod. Sci. 95, 307–315.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yin, X. J. , Lee, H. S. , Lee, Y. H. , Seo, Y. I. , and Jeon, S. J. , et al. (2005). Cats cloned from fetal and adult somatic cells by nuclear transfer. Reproduction 129, 245–249.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Zhao, Z. , Li, R. , Cao, H. , Zhang, Q. , and Jiang, M. , et al. (2006). Interspecies nuclear transfer of Tibetan antelope using caprine oocyte as recipient. Mol. Reprod. Dev. ,
Crossref | GoogleScholarGoogle Scholar |