Xenooplasmic Transfer between Buffalo and Bovine Enables Development of Homoplasmic Offspring

Chiaratti, Marcos Roberto; Ferreira, Christina R.; Meirelles, Flávio Vieira; Méo, Simone Cristina; Perecin, Felipe; Smith, Lawrence C.; Ferraz, Márcio Leão; Filho, Manoel Francisco de Sá; Gimenes, Lindsay Unno; Baruselli, Pietro Sampaio; Gasparrini, B.; Garcia, Joaquim Mansano

doi:10.1089/cell.2009.0076

Cited by 10 publications

(10 citation statements)

References 31 publications

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“…Embryo transfer of SVCH morulae/blastocysts at 96 h post-hCG failed to develop into offspring. Although our results were different from a recent study (Chiaratti et al 2010) that reported generation of homoplasmic bovine offspring from buffalo-cattle cytoplasm hybrids, the species involved in the later study belong to the same family and a hybrid was reportedly born from hybridization of buffalo and cattle in China and USSR (Mason 1976). Then, we investigated whether mitochondrial heteroplasmy contributed to developmental failure in cytoplasm hybrids.…”

Section: Discussioncontrasting

confidence: 99%

“…The percentage of pig mtDNA present in LVCH embryos was !5% of total mitochondrial numbers. In view of the presence of more than 95% mouse mtDNA of the total mtDNA in pig-mouse cytoplasm hybrid embryos and the birth of homoplasmic cattle from buffalo-bovine cytoplasm hybrids (Chiaratti et al 2010), we speculate that mitochondrial heteroplasmy may not be a major cause of developmental failure in cytoplasmic hybrid embryos. The fact that cytoplasmic hybrid embryos developed to four-cell and later stages indicate that these embryos have successfully undergone first and second wave of EGA at late one-and two-cell stages respectively.…”

Section: Discussionmentioning

confidence: 90%

“…Xenooplasmic transfer (XOT) in somatic cell models is a valuable tool to address nuclear and mtDNA interactions between different species (Kenyon & Moraes 1997, Trounce & Pinkert 2007. Unlike iSCNT embryos that usually arrest around the stage of EGA, XOT embryos develop beyond EGA (Sansinena et al 2011) and even into live offspring (Chiaratti et al 2010). Thus the XOT approach would provide a better model to address nuclear and cytoplasmic cross talk between different species.…”

Section: Introductionmentioning

confidence: 99%

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Nuclear–cytoplasmic incompatibility and inefficient development of pig–mouse cytoplasmic hybrid embryos

Amarnath

Choi²,

Moawad³

et al. 2011

Reproduction

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Inter-species somatic cell nuclear transfer (iSCNT) embryos usually fail to develop to the blastocyst stage and beyond due to incomplete reprogramming of donor cell. We evaluated whether using a karyoplast that would require less extensive reprogramming such as an embryonic blastomere or the meiotic spindle from metaphase II oocytes would provide additional insight into the development of iSCNT embryos. Our results showed that karyoplasts of embryonic or oocyte origin are no different from somatic cells; all iSCNT embryos, irrespective of karyoplast origin, were arrested during early development. We hypothesized that nuclear-cytoplasmic incompatibility could be another reason for failure of embryonic development from iSCNT. We used pig-mouse cytoplasmic hybrids as a model to address nuclear-cytoplasmic incompatibility in iSCNT embryos. Fertilized murine zygotes were reconstructed by fusing with porcine cytoplasts of varying cytoplasmic volumes (1/10 (small) and 1/5 (large) total volume of mouse zygote). The presence of pig cytoplasm significantly reduced the development of mouse zygotes to the blastocyst stage compared with control embryos at 120 h post-human chorionic gondotropin (41 vs 6 vs 94%, P!0.05; 1/10, 1/5, control respectively). While mitochondrial DNA copy numbers remained relatively unchanged, expression of several important genes namely Tfam, Polg, Polg2, Mfn2, Slc2a3 (Glut3), Slc2a1 (Glut1), Bcl2, Hspb1, Pou5f1 (Oct4), Nanog, Cdx2, Gata3, Tcfap2c, mt-Cox1 and mt-Cox2 was significantly reduced in cytoplasmic hybrids compared with control embryos. These results demonstrate that the presence of even a small amount of porcine cytoplasm is detrimental to murine embryo development and suggest that a range of factors are likely to contribute to the failure of inter-species nuclear transfer embryos.

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Section: Discussioncontrasting

confidence: 99%

Section: Discussionmentioning

confidence: 90%

Section: Introductionmentioning

confidence: 99%

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Nuclear–cytoplasmic incompatibility and inefficient development of pig–mouse cytoplasmic hybrid embryos

Amarnath

Choi²,

Moawad³

et al. 2011

Reproduction

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“…Interestingly, we did not observe any adverse effect of xenogenic mitochondrial transfer on in vitro development and embryo quality of pig oocytes. Our results are consistent with those of Chiaratti et al (2010), who observed that xeno-ooplasmic transfer of buffalo ooplasm into bovine zygotes did not affect the blastocyst development. Takeda mtDNA from mice fibroblasts did not affect the in vitro development of cattle oocytes.…”

Section: Discussionsupporting

confidence: 93%

Transgenic Chicken, Mice, Cattle, and Pig Embryos by Somatic Cell Nuclear Transfer into Pig Oocytes

Gupta

Das

Heo

et al. 2013

Cellular Reprogramming

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This study explored the possibility of producing transgenic cloned embryos by interspecies somatic cell nuclear transfer (iSCNT) of cattle, mice, and chicken donor cells into enucleated pig oocytes. Enhanced green florescent protein (EGFP)-expressing donor cells were used for the nuclear transfer. Results showed that the occurrence of first cleavage did not differ significantly when pig, cattle, mice, or chicken cells were used as donor nuclei (p>0.05). However, the rate of blastocyst formation was significantly higher in pig (14.9±2.1%; p<0.05) SCNT embryos than in cattle (6.3±2.5%), mice (4.2±1.4%), or chicken (5.1±2.4%) iSCNT embryos. The iSCNT embryos also contained a significantly less number of cells per blastocyst than those of SCNT pig embryos (p<0.05). All (100%) iSCNT embryos expressed the EGFP gene, as evidenced by the green florescence under ultraviolet (UV) illumination. Microinjection of purified mitochondria from cattle somatic cells into pig oocytes did not have any adverse effect on their postfertilization in vitro development and embryo quality (p>0.05). Moreover, NCSU23 medium, which was designed for in vitro culture of pig embryos, was able to support the in vitro development of cattle, mice, and chicken iSCNT embryos up to the blastocyst stage. Taken together, these data suggest that enucleated pig oocytes may be used as a universal cytoplast for production of transgenic cattle, mice, and chicken embryos by iSCNT. Furthermore, xenogenic transfer of mitochondria to the recipient cytoplast may not be the cause for poor embryonic development of cattle-pig iSCNT embryos.

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“…Transfer of buffalo ooplasm into bovine zygotes by fusion methodology introduced 8.3 % buffalo mtDNA and maintained a comparable ratio through to the blastocyst stage. However, no vestiges of buffalo mtDNA were found in subsequent offspring [66]. This would support an inability of buffalo mtDNA to establish a functional interaction with the bovine nucleus.…”

Section: Fate Of Interspecies or Intergeneric Mtdna In Ooplasmmentioning

confidence: 86%

Mitochondrial DNA transmission and confounding mitochondrial influences in cloned cattle and pigs

Takeda

2013

Reprod Medicine & Biology

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Although somatic cell nuclear transfer (SCNT) is a powerful tool for production of cloned animals, SCNT embryos generally have low developmental competency and many abnormalities. The interaction between the donor nucleus and the enucleated ooplasm plays an important role in early embryonic development, but the underlying mechanisms that negatively impact developmental competency remain unclear. Mitochondria have a broad range of critical functions in cellular energy supply, cell signaling, and programmed cell death; thus, affect embryonic and fetal development. This review focuses on mitochondrial considerations influencing SCNT techniques in farm animals. Donor somatic cell mitochondrial DNA (mtDNA) can be transmitted through what has been considered a ''bottleneck'' in mitochondrial genetics via the SCNT maternal lineage. This indicates that donor somatic cell mitochondria have a role in the reconstructed cytoplasm. However, foreign somatic cell mitochondria may affect the early development of SCNT embryos. Nuclear-mitochondrial interactions in interspecies/intergeneric SCNT (iSCNT) result in severe problems. A major biological selective pressure exists against survival of exogenous mtDNA in iSCNT. Yet, mtDNA differences in SCNT animals did not reflect transfer of proteomic components following proteomic analysis. Further study of nuclear-cytoplasmic interactions is needed to illuminate key developmental characteristics of SCNT animals associated with mitochondrial biology.

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Xenooplasmic Transfer between Buffalo and Bovine Enables Development of Homoplasmic Offspring

Cited by 10 publications

References 31 publications

Nuclear–cytoplasmic incompatibility and inefficient development of pig–mouse cytoplasmic hybrid embryos

Nuclear–cytoplasmic incompatibility and inefficient development of pig–mouse cytoplasmic hybrid embryos

Transgenic Chicken, Mice, Cattle, and Pig Embryos by Somatic Cell Nuclear Transfer into Pig Oocytes

Mitochondrial DNA transmission and confounding mitochondrial influences in cloned cattle and pigs

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