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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Developmental competence of 8–16-cell stage bison embryos produced by interspecies somatic cell nuclear transfer

L. Antonio González-Grajales A , Laura A. Favetta A , W. Allan King A and Gabriela F. Mastromonaco A B C
+ Author Affiliations
- Author Affiliations

A Department of Biomedical Sciences, University of Guelph, 50 Stone Road E, Guelph, ON N1G 2W1, Canada.

B Reproductive Physiology, Toronto Zoo, Toronto, ON M1B 5K7, Canada.

C Corresponding author. Email: gmastromonaco@torontozoo.ca

Reproduction, Fertility and Development 28(9) 1360-1368 https://doi.org/10.1071/RD14376
Submitted: 4 October 2014  Accepted: 15 January 2015   Published: 13 March 2015

Abstract

Altered communication between nuclear and cytoplasmic components has been linked to impaired development in interspecies somatic cell nuclear transfer (iSCNT) embryos as a result of genetic divergence between the two species. This study investigated the developmental potential and mitochondrial function of cattle (Bos taurus), plains bison (Bison bison bison) and wood bison (Bison bison athabascae) embryos produced by iSCNT using domestic cattle oocytes as cytoplasts. Embryos in all groups were analysed for development, accumulation of ATP, apoptosis and gene expression of nuclear- and mitochondrial-encoded genes at the 8–16-cell stage. The results of this study showed no significant differences in the proportion of developed embryos at the 2-, 4- and 8–16-cell stages between groups. However, significantly higher ATP levels were observed in cattle SCNT embryos compared with bison iSCNT embryos. Significantly more condensed and terminal deoxynucleotidyl transferase-mediated dUTP nick-end labelling (TUNEL)-positive nuclei were found in plains bison iSCNT embryos. No significant differences in the expression levels of nuclear respiratory factor 2 (NRF2) or mitochondrial subunit 2 of cytochrome c oxidase (mt-COX2) were found in any of the groups. However, mitochondrial transcription factor A (TFAM) expression significantly differed between groups. The results of this study provide insights into the potential causes that might lead to embryonic arrest in bison iSCNT embryos, including mitochondrial dysfunction, increased apoptosis and abnormal gene expression.

Additional keywords: ATP, apoptosis, heteroplasmy, mitochondrial incompatibility.


References

Amarnath, D., Choi, I., Moawad, A. R., Wakayama, T., and Campbell, K. H. S. (2011). Nuclear–cytoplasmic incompatibility and inefficient development of pig–mouse cytoplasmic hybrid embryos. Reproduction 142, 295–307.
Nuclear–cytoplasmic incompatibility and inefficient development of pig–mouse cytoplasmic hybrid embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtV2gs73O&md5=ae37862a718276525f4a75eef66b19d6CAS | 21555359PubMed |

Anderson, S., Bankier, A. T., Barrell, B. G., de Bruijn, M. H. L., Coulson, A. R., Drouin, J., Eperon, I. C., Nierlich, D. P., Roe, B. A., Sanger, F., Schreier, P. H., Smith, A. J. H., Staden, R., and Young, I. G. (1981). Sequence and organisation of the human mitochondrial genome. Nature 290, 457–465.
Sequence and organisation of the human mitochondrial genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlt1OlsL8%3D&md5=a0c53ea7c5483727988abd8a57b8d80eCAS | 7219534PubMed |

Asin-Cayuela, J., and Gustafsson, C. M. (2007). Mitochondrial transcription and its regulation in mammalian cells. Trends Biochem. Sci. 32, 111–117.
Mitochondrial transcription and its regulation in mammalian cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXisleisLg%3D&md5=1f14ff041ea1f5c4780154adebff4725CAS | 17291767PubMed |

Bowles, E. J., Lee, J.-H., Alberio, R., Lloyd, R. E. I., Stekel, D., Campbell, K. H. S., and St. John, J. C. (2007). Contrasting effects of in vitro fertilisation and nuclear transfer on the expression of mtDNA replication factors. Genetics 176, 1511–1526.
Contrasting effects of in vitro fertilisation and nuclear transfer on the expression of mtDNA replication factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeiurzO&md5=edddd3cd7118bf3d2bc40e6890e0906bCAS | 17507682PubMed |

Byrne, A. T., Southgate, J., Brison, D. R., and Leese, H. J. (1999). Analysis of apoptosis in the preimplantation bovine embryo using TUNEL. J. Reprod. Fertil. 117, 97–105.
Analysis of apoptosis in the preimplantation bovine embryo using TUNEL.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtlalt7k%3D&md5=d0a6da42404621daf5537192b619a90bCAS | 10645250PubMed |

Capaldi, R. A. (1990). Structure and function of cytochrome c oxidase. Annu. Rev. Biochem. 59, 569–596.
Structure and function of cytochrome c oxidase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXls1Oks7s%3D&md5=428c7c8c28f3787f05045d91dd0b5322CAS | 2165384PubMed |

Chiaratti, M. R., Bressan, F. F., Ferreira, C. R., Caetano, A. R., Smith, L. C., Vercesi, A. E., and Meirelles, F. V. (2010). Embryo mitochondrial DNA depletion is reversed during early embryogenesis in cattle. Biol. Reprod. 82, 76–85.
Embryo mitochondrial DNA depletion is reversed during early embryogenesis in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1WgsrrI&md5=0e083bffe0493f8afe636aa4b2119102CAS | 19696017PubMed |

Chung, Y., Bishop, C. E., Treff, N. R., Walker, S. J., Sandler, V. M., Becker, S., Klimanskaya, I., Wun, W. S., Dunn, R., Hall, R. M., Su, J., Lu, S. J., Maserati, M., Choi, Y. H., Scott, R., Atala, A., Dittman, R., and Lanza, R. (2009). Reprogramming of human somatic cells using human and animal oocytes. Cloning Stem Cells 11, 213–223.
Reprogramming of human somatic cells using human and animal oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnt1Cis78%3D&md5=f90163c04deb8b6a3797cfe811e424fdCAS | 19186982PubMed |

Dominko, T., Mitalipova, M., Haley, B., Beyhan, Z., Memili, E., McKusick, B., and 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, 1496–1502.
Bovine oocyte cytoplasm supports development of embryos produced by nuclear transfer of somatic cell nuclei from various mammalian species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsVeitbk%3D&md5=2567c6c38ee0b6e821c9ed1ceb7eec2cCAS | 10330111PubMed |

Dumollard, R., Carroll, J., Duchen, M. R., Campbell, K., and Swann, K. (2009). Mitochondrial function and redox state in mammalian embryos. Semin. Cell Dev. Biol. 20, 346–353.
Mitochondrial function and redox state in mammalian embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltVCmsLo%3D&md5=8e1436f46bb793d40b3bb0450eec5a94CAS | 19530278PubMed |

Esteves, T. C., Psathaki, O. E., Pfeiffer, M. J., Balbach, S. T., Zeuschner, D., Shitara, H., Yonekawa, H., Siatkowski, M., Fuellen, G., and Boiani, M. (2012). Mitochondrial physiology and gene expression analyses reveal metabolic and translational dysregulation in oocyte-induced somatic nuclear reprogramming. PLoS ONE 7, e36850.
Mitochondrial physiology and gene expression analyses reveal metabolic and translational dysregulation in oocyte-induced somatic nuclear reprogramming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1Kgsbg%3D&md5=37b72339fd146787194b6de0afd51c42CAS | 22693623PubMed |

Favetta, L. A., Robert, C., St.John, E. J., Betts, D. H., and King, W. A. (2004). p66shc, but not p53, is involved in early arrest of in vitro-produced bovine embryos. Mol. Hum. Reprod. 10, 383–392.
p66shc, but not p53, is involved in early arrest of in vitro-produced bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvVSisr8%3D&md5=c7e5f784212387a4e1de4f58adc34742CAS | 15064348PubMed |

Gómez, M. C., Pope, C. E., Giraldo, A., Lyons, L. A., Harris, R. F., King, A. L., Cole, A., Godke, R. A., and Dresser, B. L. (2004). Birth of African wildcat cloned kittens born from domestic cats. Cloning Stem Cells 6, 247–258.
Birth of African wildcat cloned kittens born from domestic cats.Crossref | GoogleScholarGoogle Scholar | 15671671PubMed |

Gómez, M. C., Pope, C. E., Kutner, R. H., Ricks, D. M., Lyons, L. A., Ruhe, M., Dumas, C., Lyons, J., Lopez, M., Dresser, B. L., and 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, 469–484.
Nuclear transfer of sand cat cells into enucleated domestic cat oocytes is affected by cryopreservation of donor cells.Crossref | GoogleScholarGoogle Scholar | 18795868PubMed |

Gómez, M. C., Pope, C. E., Biancardi, M. N., Dumas, C., Galiguis, J., Morris, A. C., Wang, G., and Dresser, B. L. (2011). Trichostatin A modified histone covalent pattern and enhanced expression of pluripotent genes in interspecies black-footed cat cloned embryos but did not improve in vitro and in vivo viability. Cell. Reprogram. 13, 315–329.
Trichostatin A modified histone covalent pattern and enhanced expression of pluripotent genes in interspecies black-footed cat cloned embryos but did not improve in vitro and in vivo viability.Crossref | GoogleScholarGoogle Scholar | 21718106PubMed |

Hardy, K. (1997). Cell death in the mammalian blastocyst. Mol. Hum. Reprod. 3, 919–925.
Cell death in the mammalian blastocyst.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c%2FlsFKntg%3D%3D&md5=52a00846aec492d9f459fffb358c680cCAS | 9395266PubMed |

Harvey, A. J., Kind, K. L., and Thompson, J. G. (2002). REDOX regulation of early embryo development. Reproduction 123, 479–486.
REDOX regulation of early embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivFGhtLk%3D&md5=c2d308268e1c58238eede61818421703CAS | 11914110PubMed |

Hedrick, P. W. (2010). Cattle ancestry in bison: explanations for higher mtDNA than autosomal ancestry. Mol. Ecol. 19, 3328–3335.
Cattle ancestry in bison: explanations for higher mtDNA than autosomal ancestry.Crossref | GoogleScholarGoogle Scholar | 20637048PubMed |

Hwang, I., Jeong, Y. W., Kim, J. J., Lee, H. J., Kang, M., Park, K. B., Park, J. H., Kim, Y. W., Kim, W. T., Shin, T., Hyun, S. H., Jeung, E.-B., and Hwang, W. S. (2013). Successful cloning of coyotes through interspecies somatic cell nuclear transfer using domestic dog oocytes. Reprod. Fertil. Dev. 25, 1142–1148.
Successful cloning of coyotes through interspecies somatic cell nuclear transfer using domestic dog oocytes.Crossref | GoogleScholarGoogle Scholar | 23217630PubMed |

Jiang, Y., Kelly, R., Peters, A., Fulka, H., Dickinson, A., Mitchell, D. A., and St. John, J. C. (2011). Interspecies somatic cell nuclear transfer is dependent on compatible mitochondrial DNA and reprogramming factors. PLoS ONE 6, e14805.
Interspecies somatic cell nuclear transfer is dependent on compatible mitochondrial DNA and reprogramming factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXls1SmsLw%3D&md5=9dfb536b2645768f29b9e17b2f497594CAS | 21556135PubMed |

Kamjoo, M., Brison, D. R., and Kimber, S. J. (2002). Apoptosis in the preimplantation mouse embryo: effect of strain difference and in vitro culture. Mol. Reprod. Dev. 61, 67–77.
Apoptosis in the preimplantation mouse embryo: effect of strain difference and in vitro culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptVejur8%3D&md5=4eb12f1821321d4c5b21d3ba33b86644CAS | 11774377PubMed |

Kenyon, L., and Moraes, C. T. (1997). Expanding the functional human mitochondrial DNA database by the establishment of primate xenomitochondrial cybrids. Proc. Natl. Acad. Sci. USA 94, 9131–9135.
Expanding the functional human mitochondrial DNA database by the establishment of primate xenomitochondrial cybrids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXls1Klsr4%3D&md5=8e3678923d23697900dfe99667f8a4c2CAS | 9256447PubMed |

Kim, M. K., Jang, G., Oh, H. J., Yuda, F., Kim, H., Hwang, W. S., Hossein, M. S., Kim, J. J., Shin, N. S., Kang, S. K., and Lee, B. C. (2007). Endangered wolves cloned from adult somatic cells. Cloning Stem Cells 9, 130–137.
Endangered wolves cloned from adult somatic cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsVWrtLs%3D&md5=abd3ef53e3c3320099ad97f7ca1f9231CAS | 17386020PubMed |

Lagutina, I., Zakhartchenko, V., Fulka, H., Colleoni, S., Wolf, E., Fulka, J., Lazzari, G., and Galli, C. (2011). Formation of nucleoli in interspecies nuclear transfer embryos derived from bovine, porcine and rabbit oocytes and nuclear donor cells of various species. Reproduction 141, 453–465.
Formation of nucleoli in interspecies nuclear transfer embryos derived from bovine, porcine and rabbit oocytes and nuclear donor cells of various species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlKiur4%3D&md5=e87113c556797e730b81226ed9609208CAS | 21239525PubMed |

Leibfried, L., and First, N. L. (1979). Characterisation of bovine follicular oocytes and their ability to mature in vitro. J. Anim. Sci. 48, 76–86.
| 1:STN:280:DyaL3c%2Fgs1arsA%3D%3D&md5=ac131ed4cb4cd21d9eb2bd32c2e5f4ceCAS | 573253PubMed |

Lloyd, R. E., Lee, J.-H., Alberio, R., Bowles, E. J., Ramalho-Santos, J., Campbell, K. H. S., and St. John, J. C. (2006). Aberrant nucleo–cytoplasmic cross-talk results in donor cell mtDNA persistence in cloned embryos. Genetics 172, 2515–2527.
Aberrant nucleo–cytoplasmic cross-talk results in donor cell mtDNA persistence in cloned embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkvFOgtL4%3D&md5=bc1826eb83bbac578e78647cddbf4854CAS | 16452133PubMed |

Maloyan, A., Sanbe, A., Osinska, H., Westfall, M., Robinson, D., Imahashi, K.-i., Murphy, E., and Robbins, J. (2005). Mitochondrial dysfunction and apoptosis underlie the pathogenic process in α-B-crystallin desmin-related cardiomyopathy. Circulation 112, 3451–3461.
Mitochondrial dysfunction and apoptosis underlie the pathogenic process in α-B-crystallin desmin-related cardiomyopathy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Cqt7%2FF&md5=38aa2e851e07348458b85c3eb6ddadfeCAS | 16316967PubMed |

Mastromonaco, G. F., Semple, E., Robert, C., Rho, G. J., Betts, D. H., and King, W. A. (2004). Different culture media requirements of IVF and nuclear transfer bovine embryos. Reprod. Domest. Anim. 39, 462–467.
Different culture media requirements of IVF and nuclear transfer bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2cnisVCiuw%3D%3D&md5=ebb1cb6272cf79fffe5f846b13fe49acCAS | 15598239PubMed |

Mastromonaco, G. F., Favetta, L. A., Smith, L. C., Filion, F., and King, W. A. (2007). The influence of nuclear content on developmental competence of gaur × cattle hybrid in vitro-fertilised and somatic cell nuclear transfer embryos. Biol. Reprod. 76, 514–523.
The influence of nuclear content on developmental competence of gaur × cattle hybrid in vitro-fertilised and somatic cell nuclear transfer embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitlWhu7g%3D&md5=fac7396549c396e2e1b76148f12d7fc0CAS | 17151347PubMed |

Mastromonaco, G. F., González-Grajales, L. A., Filice, M., and Comizzoli, P. (2014). Somatic cells, stem cells and induced pluripotent stem cells: how do they now contribute to conservation? Adv. Exp. Med. Biol. 753, 385–427.
Somatic cells, stem cells and induced pluripotent stem cells: how do they now contribute to conservation?Crossref | GoogleScholarGoogle Scholar | 25091918PubMed |

Mateusen, B., Van Soom, A., Maes, D. G. D., Donnay, I., Duchateau, L., and Lequarre, A. S. (2005). Porcine embryo development and fragmentation and their relation to apoptotic markers: a cinematographic and confocal laser-scanning microscopic study. Reproduction 129, 443–452.
Porcine embryo development and fragmentation and their relation to apoptotic markers: a cinematographic and confocal laser-scanning microscopic study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjs1ertLc%3D&md5=cd3ec87a9745e1d96be3c1220d7d2f13CAS | 15798019PubMed |

Matwee, C., Betts, D. H., and King, W. A. (2000). Apoptosis in the early bovine embryo. Zygote 8, 57–68.
Apoptosis in the early bovine embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjvVemtLw%3D&md5=fc46fe95c8951dec8955d0d3439a136eCAS | 10840875PubMed |

May-Panloup, P., Vignon, X., Chretien, M.-F., Heyman, Y., Tamassia, M., Malthiery, Y., and Reynier, P. (2005). Increase of mitochondrial DNA content and transcripts in early bovine embryogenesis associated with upregulation of mtTFA and NRF1 transcription factors. Reprod. Biol. Endocrinol. 3, 65.
Increase of mitochondrial DNA content and transcripts in early bovine embryogenesis associated with upregulation of mtTFA and NRF1 transcription factors.Crossref | GoogleScholarGoogle Scholar | 16285882PubMed |

McCulloch, V., Seidel-Rogol, B. L., and Shadel, G. S. (2002). A human mitochondrial transcription factor is related to RNA adenine methyltransferases and binds S-adenosylmethionine. Mol. Cell. Biol. 22, 1116–1125.
A human mitochondrial transcription factor is related to RNA adenine methyltransferases and binds S-adenosylmethionine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVWruw%3D%3D&md5=1a3f0010712b3c66245f5dc6ba68563eCAS | 11809803PubMed |

Monfort, S. L. (2014). “Mayday Mayday Mayday”, the millennium ark is sinking! Adv. Exp. Med. Biol. 753, 15–31.
“Mayday Mayday Mayday”, the millennium ark is sinking!Crossref | GoogleScholarGoogle Scholar | 25091904PubMed |

Narbonne, P., Simpson, D. E., and Gurdon, J. B. (2011). Deficient induction response in a Xenopus nucleocytoplasmic hybrid. PLoS Biol. 9, e1001197.
Deficient induction response in a Xenopus nucleocytoplasmic hybrid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsF2isbbM&md5=74f73702000fbe374d35d18d8d4b697eCAS | 22131902PubMed |

Nelson, D. L., and Cox, M. M. (2004). Oxidative phosphorylation and photophosphorylation. In ‘Lehninger’s Principles of Biochemistry, 4th Edition’. pp. 690–750. (W.H. Freeman and Company: New York.)

Perry, G. (2013). ‘2012 Statistics of Embryo Collection and Transfer in Domestic Farm Animals’. Available at http://www.iets.org/pdf/comm_data/December2013.pdf [Verified 1 September 2014].

Pukazhenthi, B., Comizzoli, P., Travis, A. J., and Wildt, D. E. (2006). Applications of emerging technologies to the study and conservation of threatened and endangered species. Reprod. Fertil. Dev. 18, 77–90.
Applications of emerging technologies to the study and conservation of threatened and endangered species.Crossref | GoogleScholarGoogle Scholar | 16478605PubMed |

Rozell, M. D., Williams, J. E., and Butler, J. E. (1992). Changes in concentration of adenosine triphosphate and adenosine diphosphate in individual preimplantation sheep embryos. Biol. Reprod. 47, 866–870.
Changes in concentration of adenosine triphosphate and adenosine diphosphate in individual preimplantation sheep embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmsV2jtrY%3D&md5=6b3265907e8914757a3f7d2752e169cfCAS | 1477212PubMed |

Rozen, S., and Skaletsky, H. J. (2000). Primer3 on the WWW for general users and for biologist programmers. In ‘Bioinformatics Methods and Protocols: Methods in Molecular Biology’. (Eds S. Krawetz and S. Misener.) pp. 365–385. (Humana Press Inc.: Totowa, NJ, USA.)

Seaby, R. P., Alexander, B., King, W. A., and Mastromonaco, G. F. (2013). In vitro development of bison embryos using interspecies somatic cell nuclear transfer. Reprod. Domest. Anim. 48, 881–887.
In vitro development of bison embryos using interspecies somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3snlsV2htQ%3D%3D&md5=d97c6fe1a35c6a773731e597a5eed790CAS | 23692072PubMed |

Sturmey, R. G., and Leese, H. J. (2003). Energy metabolism in pig oocytes and early embryos. Reproduction 126, 197–204.
Energy metabolism in pig oocytes and early embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntFyjtr4%3D&md5=64ce8e53c53d9e7b3d87d6e095fa23a0CAS | 12887276PubMed |

Sutovsky, P., Van Leyen, K., McCauley, T., Day, B. N., and Sutovsky, M. (2004). Degradation of paternal mitochondria after fertilisation: implications for heteroplasmy, assisted reproductive technologies and mtDNA inheritance. Reprod. Biomed. Online 8, 24–33.
Degradation of paternal mitochondria after fertilisation: implications for heteroplasmy, assisted reproductive technologies and mtDNA inheritance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXht1Ojsb8%3D&md5=e54af878efe5f480aead835ec2e0d9ccCAS | 14759284PubMed |

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.
In vitro embryo production efficiency in cattle and its association with oocyte adenosine triphosphate content, quantity of mitochondrial DNA and mitochondrial DNA haplogroup.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFWgu7c%3D&md5=0f13eb08767c700de26afa4dc47652c0CAS | 15084486PubMed |

Thouas, G. A., Trounson, A. O., Wolvetang, E. J., and Jones, G. M. (2004). Mitochondrial dysfunction in mouse oocytes results in preimplantation embryo arrest in vitro. Biol. Reprod. 71, 1936–1942.
Mitochondrial dysfunction in mouse oocytes results in preimplantation embryo arrest in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWgsr3O&md5=c2086e980332d91c61fd5280b43fb573CAS | 15286028PubMed |

Van Blerkom, J., and Davis, P. (2007). Mitochondrial signalling and fertilisation. Mol. Hum. Reprod. 13, 759–770.
Mitochondrial signalling and fertilisation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaqtr3O&md5=2993c9ab01451734ae20c4b24a1b7b08CAS | 17893093PubMed |

Van Blerkom, J., David, P., Mathwig, V., and Alexander, S. (2000). Differential mitochondrial inheritance between blastomeres in cleavage-stage human embryos: determination at the pronuclear stage and relationship to microtubular organisation, ATP content and developmental competence. Hum. Reprod. 15, 2621–2633.
Differential mitochondrial inheritance between blastomeres in cleavage-stage human embryos: determination at the pronuclear stage and relationship to microtubular organisation, ATP content and developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktFOisQ%3D%3D&md5=1811e150c2bfa5863959594fb73306d7CAS | 11098036PubMed |

Wakefield, S. L., Lane, M., and Mitchell, M. (2011). Impaired mitochondrial function in the preimplantation embryo perturbs fetal and placental development in the mouse. Biol. Reprod. 84, 572–580.
Impaired mitochondrial function in the preimplantation embryo perturbs fetal and placental development in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXis1OmtL4%3D&md5=fb753a4c8cdf01e8f2e05832760e38b4CAS | 21076083PubMed |

Wang, K., Beyhan, Z., Rodríguez, R. M., Ross, P. J., Iager, A. E., Kaiser, G. G., Chen, Y., and Cibelli, J. B. (2009). Bovine ooplasm partially remodels primate somatic nuclei following somatic cell nuclear transfer. Cloning Stem Cells 11, 187–202.
Bovine ooplasm partially remodels primate somatic nuclei following somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt1Cmtro%3D&md5=7c0023108fd8f536e471d69148859874CAS | 19196039PubMed |

Wang, Q., Frolova, A. I., Purcell, S., Adastra, K., Schoeller, E., Chi, M. M., Schedl, T., and Moley, K. H. (2010). Mitochondrial dysfunction and apoptosis in cumulus cells of Type I diabetic mice. PLoS ONE 5, e15901.
Mitochondrial dysfunction and apoptosis in cumulus cells of Type I diabetic mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlslyqtw%3D%3D&md5=bf25ee94c4bf7f703173fffaaa1aa080CAS | 21209947PubMed |

Wang, K., Otu, H. H., Chen, Y., Lee, Y., Latham, K., and Cibelli, J. B. (2011). Reprogrammed transcriptome in rhesus–bovine interspecies somatic cell nuclear transfer embryos. PLoS ONE 6, e22197.
Reprogrammed transcriptome in rhesus–bovine interspecies somatic cell nuclear transfer embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVKgtLjL&md5=fff1b4bcc9d96c495cea03831a9e5ae4CAS | 21799794PubMed |

Wildt, D. E., Monfort, S. L., Donoghue, A. M., Johnston, L. A., and Howard, J. (1992). Embryogenesis in conservation biology, or, how to make an endangered species embryo. Theriogenology 37, 161–184.
Embryogenesis in conservation biology, or, how to make an endangered species embryo.Crossref | GoogleScholarGoogle Scholar |

Wildt, D. E., Ellis, E., Janssen, D., and Buff, J. (2003). Toward more effective reproductive science in conservation. In ‘Reproductive Sciences and Integrated Conservation’. (Eds W. V. Holt, A. Pickard, J. C. Rodger and D. E. Wildt.) pp. 2–20. (Cambridge University Press: Cambridge.)