Bowles, Emma J., Tecirlioglu, R. Tayfur, French, Andrew J., Holland, Michael K. and St. John, Justin C.. (2008) Mitochondrial DNA transmission and transcription after somatic cell fusion to one or more cytoplasts. Stem Cells, Vol.26 (No.3). pp. 775-782. ISSN 1066-5099

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Abstract

Following fertilization, mitochondrial DNA is inherited from the oocyte and transmitted homoplasmically. However, following nuclear transfer, mitochondrial DNA can be transmitted from both the donor cell and recipient oocyte, resulting in a state of heteroplasmy. To determine whether the genetic diversity between donor cell and recipient cytoplast mitochondrial DNA influences development, we generated bovine embryos by fusing a donor cell to one or more enucleated cytoplasts. Analysis of mitochondrial DNA from embryos, fetal tissues, and blood samples from offspring revealed that early preimplantation embryos from two or three cytoplasts had significantly more mitochondrial DNA variants than fetal tissues. Phylogenic analysis of embryos generated using single cytoplasts divided the mitochondrial DNA sequence variants into three separate groups with various amounts of genetic divergence from the donor cell line. In heteroplasmic tissue and blood samples, the predominant mitochondrial DNA population was significantly more divergent from the donor cell than the less frequent allele. Furthermore, analysis of the mitochondrially encoded cytochrome B gene showed that two heteroplasmic alleles encoded for different amino acids, and the ratios of mitochondrial DNA/mRNA for each allele differed significantly between tissues. The degree of evolutionary distance between the donor cell and the cytoplast and the variability in heteroplasmy between tissues may have an impact on more divergent intergeneric nuclear transfer and the use of this approach for the generation of embryonic stem cells.

Item Type:	Journal Article
Subjects:	Q Science > QH Natural history > QH426 Genetics Q Science > QP Physiology
Divisions:	Faculty of Medicine > Warwick Medical School > Clinical Sciences Research Institute (CSRI) Faculty of Medicine > Warwick Medical School
Library of Congress Subject Headings (LCSH):	Mitochondrial DNA, Cloning, Genetic transformation, Genetic transcription, Mitochondrial pathology, DNA replication, Somatic hybrids
Journal or Publication Title:	Stem Cells
Publisher:	AlphaMed Press, Inc.
ISSN:	1066-5099
Date:	2008
Volume:	Vol.26
Number:	No.3
Number of Pages:	8
Page Range:	pp. 775-782
Identification Number:	10.1634/stemcells.2007-0747
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Restricted or Subscription Access
References:	1 Anderson S, Bankier AT, Barrell BG et al. Sequence and organization of the human mitochondrial genome. Nature 1981;290:457– 465. 2 Wallace DC. Mitochondrial diseases in man and mouse. Science 1999; 283:1482–1488. 3 Birky CW Jr. Uniparental inheritance of mitochondrial and chloroplast genes: Mechanisms and evolution. Proc Natl Acad Sci USA 1995;92:11331–11338. 4 Sutovsky P, Moreno RD, Ramalho-Santos J et al. Ubiquitin tag for sperm mitochondria. Nature 1999;402:371–372. 5 Gyllensten U, Wharton D, Josefsson A et al. Paternal inheritance of mitochondrial DNA in mice. Nature 1991;352:255–257. 6 Jansen RP, de Boer K. The bottleneck: Mitochondrial imperatives in oogenesis and ovarian follicular fate. Mol Cell Endocrinol 1998;145:81–88. 7 Hauswirth WW, Laipis PJ. Mitochondrial DNA polymorphism in a maternal lineage of Holstein cows. Proc Natl Acad Sci U S A 1982;79:4686–4690. 8 Campbell KHS, Alberio R. Reprogramming the genome: Role of the cell cycle. Reprod Suppl 2003;61:477– 494. 9 Tecirlioglu RT, Guo J, Trounson AO. Inter-species somatic cell nuclear transfer (iSCNT) and preliminary data for horse-cow/mouse iSCNT. Stem Cell Rev 2006;2:277–287. 10 Bowles E, Campbell K, St. John J. Nuclear transfer: Preservation of a nuclear genome at the expense of its associated mtDNA genome(s). Cur Top Dev Biol 2007;77:251–290. 11 St. John JC, Lloyd RE, Bowles EJ et al. The consequences of nuclear transfer for mammalian foetal development and offspring survival. A mitochondrial DNA perspective. Reprod 2004;127:631– 641. 12 Takeda K, Akagi S, Kaneyama K et al. Proliferation of donor mitochondrial DNA in nuclear transfer calves (Bos taurus) derived from cumulus cells. Mol Reprod Dev 2003;64:429–437. 13 Lloyd RE, Lee J-H, Alberio R. Aberrant nucleo-cytoplasmic cross-talk results in donor cell mtDNA persistence in cloned embryos. Genetics 2006;172:2515–2527. 14 Bowles EJ, Lee J-H, Alberio R et al. Contrasting effects of in vitro fertilization and nuclear transfer on the expression of mtDNA replication factors. Genetics 2007;176:1511–1526. 15 Steinborn R, Schinogl P, Wells DN. Coexistence of Bos taurus and B. indicus mitochondrial DNAs in nuclear transfer-derived somatic cattle clones. Genetics 2002;162:823– 829. 16 St. John J, Moffatt O, D’Souza N. Aberrant heteroplasmic transmission of mtDNA in cloned pigs arising from double nuclear transfer. Mol Reprod Dev 2005;72:450–460. 17 Chang KH, Lim JM, Kang SK et al. Blastocyst formation, karyotype, and mitochondrial DNA of interspecies embryos derived from nuclear transfer of human cord fibroblasts into enucleated bovine oocytes. Fertil Steril 2003;80:1380 –1387. 18 Yang CX, Han ZM, Wen DC et al. In vitro development and mitochondrial fate of macaca-rabbit cloned embryos. Mol Reprod Dev 2003;65:396–401. 19 Yang CX, Kou ZH, Wang K et al. Quantitative analysis of mitochondrial DNAs in Macaque embryos reprogrammed by rabbit oocytes. Reproduction 2004;127:201–205. 20 Liu SZ, Zhou ZM, Chen T. Blastocysts produced by nuclear transfer between chicken blastodermal cells and rabbit oocytes. Mol Reprod Dev 2004;69:296 –302. 21 Vajta G, Lewis IM, Hyttel P et al. Somatic cell cloning without micromanipulators. Cloning 2001;3:89 –95. 22 Tecirlioglu RT, Cooney MA, Lewis IM et al. Comparison of two approaches to nuclear transfer in the bovine: Hand-made cloning with modifications and the conventional nuclear transfer technique. Reprod Fertil Dev 2005;17:573–585. 23 Williamson MM, Tecirlioglu RT, French AJ et al. Anatomical abnormalities in calves produced by nuclear transfer. Reprod Fertil Dev 2005;17:187. 24 Sullivan KM, Hopgood R, Lang B et al. Automated amplification and sequencing of human mitochondrial DNA. Electrophoresis 1991;12:17–21. 25 St. John JC, Schatten G. Paternal mitochondrial DNA transmission during nonhuman primate nuclear transfer. Genetics 2004;167:897–905. 26 Anderson S, de Bruijn MH, Coulson AR et al. Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J Mol Biol 1982;156:683–717. 27 Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 1994;22:4673– 4680. 28 Felsenstein J. PHYLIP (Phylogeny Inference Package) version 3.6. Available at http://evolution.genetics.washington.edu/phylip/doc/main.html. Accessed May 2006. 29 Meirelles FV, Bordignon V, Watanabe Y. Complete replacement of the mitochondrial genotype in a Bos indicus calf reconstructed by nuclear transfer to a Bos taurus oocyte. Genetics 2001;158:351–356. 30 Polejaeva IA, Chen SH, Vaught TD et al. Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 2000;407:86 –90. 31 Sato A, Kono T, Nakada K et al. Gene therapy for progeny of mito-mice carrying pathogenic mtDNA by nuclear transplantation. Proc Natl Acad Sci U S A 2005;102:16765–16770. 32 Laipis PJ. Construction of heteroplasmic mice containing two mitochondrial DNA genotypes by micromanipulation of single-cell embryos. Methods Enzymol 1996;264:345–357. 33 Brenner CA, Barritt JA, Willadsen S et al. Mitochondrial DNA heteroplasmy after human ooplasmic transplantation. Fertil Steril 2000;74:573–578. 34 May-Panloup P, Vignon X, Chretien MF. Increase of mitochondrial DNA content and transcripts in early bovine embryogenesis associated with upregulation of mtTFA and NRF1 transcription factors. Reprod Biol Endocrinol 2005;3:65. 35 Spikings EC, Alderson J, St. John JC. Regulated mtDNA replication during oocyte maturation is essential for successful porcine embryonic development. Biol Reprod 2007;76:327–335. 36 Shoubridge EA, Wai T. Mitochondrial DNA and the mammalian oocyte. Curr Top Dev Biol 2007;77:87–111. 37 Herna´ndez-Cero´n J, Chase CC, Hansen PJ. Differences in heat tolerance between preimplantation embryos from Brahman, Romosinuano, and Angus breeds. J Dairy Sci 2004;87:53–58. 38 Lanza RP, Cibelli JB, Diaz F et al. Cloning of an endangered species (Bos gaurus) using interspecies nuclear transfer. Cloning 2000;2:79 –90. 39 Loftus RT, MacHugh DE, Ngere LO. Mitochondrial genetic variation in European, African and Indian cattle populations. Anim Genet 1994;25:265–271. 40 Sansinena MJ, Hylan D, Hebert K et al. Banteng (Bos javanicus) embryos and pregnancies produced by interspecies nuclear transfer. Theriogenology 2005;63:1081–1091. 41 Loi P, Ptak G, Barboni B. Genetic rescue of an endangered mammal by cross-species nuclear transfer using post-mortem somatic cells. Nat Biotechnol 2001;19:962–964. 42 Hiendleder S, Lewalski H, Wassmuth R et al. The complete mitochondrial DNA sequence of the domestic sheep (Ovis aries) and comparison with the other major ovine haplotype. J Mol Evol 1998;47:441– 448. 43 Chen Y, He ZX, Liu A et al. 2003 Embryonic stem cells generated by nuclear transfer of human somatic nuclei into rabbit oocytes. Cell Res 2003;13:251–263. 44 Leahy A, Xiong J, Kuhnert F et al. Use of developmental markers genes to define temporal and spatial patterns of differentiation during embryoid body formation. J Exp Zool 1999;284:67– 81. 45 St. John J, Lovell-Badge R. Human-animal cytoplasmic hybrid embryos, mitochondria, and an energetic debate. Nat Cell Biol 2007;9:988 –992. 46 Takeda K, Tasai M, Iwamoto M et al. Transmission of mitochondrial DNA in pigs and progeny derived from nuclear transfer of Meisham pig fibroblast cells. Mol Reprod Dev 2006;73:306 –312. 47 Inoue K, Ogonuki N, Yamamoto Y et al. Tissue-specific distribution of donor mitochondrial DNA in cloned mice produced by somatic cell nuclear transfer. Genesis 2004;39:79–83. 48 Kenyon L, Moraes CT. Expanding the functional human mitochondrial DNA database by the establishment of primate xenomitochondrial cybrids. Proc Natl Acad Sci U S A 1997;94:9131–9135. 49 Barrientos A, Kenyon L, Moraes CT. Human xenomitochondrial cybrids. Cellular models of mitochondrial complex I deficiency. J Biol Chem 1998;273:14210 –14217. 50 Dey R, Barrientos A, Moraes CT. Functional constraints of nuclearmitochondrial DNA interactions in xenomitochondrial rodent cell lines. J Biol Chem 2000;275:31520 –31527.
URI:	http://wrap.warwick.ac.uk/id/eprint/30314

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