Abstract
Mitochondrial biogenesis and function is under dual genetic control and requires extensive interaction between biparentally inherited nuclear genes and maternally inherited mitochondrial genes. Standard SCNT procedures deprive an oocytes’ mitochondrial DNA (mtDNA) of the corresponding maternal nuclear DNA and require it to interact with an entirely foreign nucleus that is again interacting with foreign somatic mitochondria. As a result, most SCNT embryos, -fetuses, and -offspring carry somatic cell mtDNA in addition to recipient oocyte mtDNA, a condition termed heteroplasmy. It is thus evident that somatic cell mtDNA can escape the selective mechanism that targets and eliminates intraspecific sperm mitochondria in the fertilized oocyte to maintain homoplasmy. However, the factors responsible for the large intra- and interindividual differences in heteroplasmy level remain elusive. Furthermore, heteroplasmy is probably confounded with mtDNA recombination. Considering the essential roles of mitochondria in cellular metabolism, cell signalling, and programmed cell death, future experiments will need to assess the true extent and impact of unorthodox mtDNA transmission on various aspects of SCNT success.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Hiendleder S, Zakhartchenko V, Wolf E. Mitochondria and the success of somatic cell nuclear transfer cloning: From nuclear-mitochondrial interactions to mitochondrial complementation and mitochondrial DNA recombination. Reprod Fertil Dev 2005; 17:69–83.
Mirkes PE. 2001 Warkany lecture: To die or not to die, the role of apoptosis in normal and abnormal mammalian development. Teratology 2002; 65:228–239.
Bhuyan PK, Young LL, Lindahl KF et al. Identification of the rat maternally transmitted minor histocompatibility antigen. J Immunol 1997; 158:3753–3760.
Sulijoadikusumo I, Horikoshi N, Usheva A. Another function for the mitochondrial ribosomal RNA: Protein folding. Biochemistry 2001; 40:11559–11564.
Van Blerkom J, Davis P, Alexander S. Differential mitochondrial distribution in human pronuclear embryos leads to disproportionate inheritance between blastomeres: Relationship to microtubular organization, ATP content and competence. Hum Reprod 2000; 15:2621–2633.
Boiani M, Gambles V, Schöler H. ATP levels in cloned mouse embryos. Cytogenet Genome Res 105:270–278.
Westermann B. Merging mitochondria matters: Cellular role and molecular machinery of mitochondrial fusion. EMBO Rep 2002; 3:527–531.
Chen H, Chan DC. Emerging functions of mammalian mitochondrial fusion and fission. Hum Mol Genet 2005; 14:R283–289.
Chen XJ, Butow RA. The organization and inheritance of the mitochondrial genome. Nat Rev Genet 2005; 6:815–825.
Anderson S, Bankier AT, Barrell BG et al. Sequence and organization of the human mitochondrial genome. Nature 1981; 290:457–465.
GOBASE. The Organelle Genome Database. 2005, (http://www.bch.umontreal.ca/ogmp/projects/other/mt_list.html).
Hiendleder S, Wolf E. The mitochondrial genome in embryo technologies. Reprod Domest Anim 2003; 38:290–304.
Hiendleder S, Kaupe B, Wassmuth R et al. Molecular analysis of wild and domestic sheep questions current nomenclature and provides evidence for domestication from two different subspecies. Proc Biol Sci 2002; 269:893–904.
Lott MT, Brandon M, Brown MD et al. MITOMAP: A human mitochondrial genome database. 2003, (http://www.mitomap.org).
Cotter D, Guda P, Fahy E et al. MitoProteome: Mitochondrial protein sequence database and annotation system. Nucleic Acids Res 2004; 32 (Database issue):D463–467.
Iborra FJ, Kimura H, Cook PR. The functional organization of mitochondrial genomes in human cells. BMC Biol 2004; 2:9.
Hutchison IIIrd CA, Newbold JE, Potter SS et al. Maternal inheritance of mammalian mitochondrial DNA. Nature 1974; 251:536–538.
Gyllensten U, Wharton D, Wilson AC. Maternal inheritance of mitochondrial DNA during back-crossing of two species of mice. J Hered 1985; 76:321–324.
May-Panloup P, Chretien MF, Savagner F et al. Increased sperm mitochondrial DNA content in male infertility. Hum Reprod 2003; 18:550–556.
May-Panloup P, Chretien MF, Jacques C et al. Low oocyte mitochondrial DNA content in ovarian insufficiency. Hum Reprod 2005; 20:593–597.
Tamassia M, Nuttinck F, May-Panloup P et al. 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 2004; 71:697–704.
Barritt JA, Kokot M, Cohen J et al. Quantification of human ooplasmic mitochondria. Reprod Biomed Online 2002; 4:243–247.
Gyllensten U, Wharton D, Josefsson A et al. Paternal inheritance of mitochondrial DNA in mice. Nature 1991; 352:255–7.
Kaneda H, Hajashi JI, Takahama S et al. Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc Natl Acad Sci USA 1995; 92:4542–4546.
Sutovsky P, Moreno RD, Ramalho-Santos J et al. Ubiquitin tag for sperm mitochondria. Nature 1999; 402:371–372.
Sutovsky P, Van Leyen K, McCauley T et al. Degradation of paternal mitochondria after fertilization: Implications for heteroplasmy, assisted reproductive technologies and mtDNA inheritance. Reprod Biomed Online 2004; 8:24–33.
Schwartz M, Vissing J. Paternal inheritance of mitochondrial DNA. New Engl J Med 2002; 347:576–580.
Kraytsberg Y, Schwartz M, Brown TA et al. Recombination of human mitochondrial DNA. Science 2004; 304:981.
Zsurka G, Kraytsberg Y, Kudina T et al. Recombination of mitochondrial DNA in skeletal muscle of individuals with multiple mitochondrial DNA heteroplasmy. Nat Genet 2005; 37:873–877.
Evans MJ, Gurer C, Loike JD et al. Mitochondrial DNA genotypes in nuclear transfer-derived cloned sheep. Nat Genet 1999; 23:90–93.
Loi P, Ptak G, Barboni B et al. Genetic rescue of an endangered mammal by cross-species nuclear transfer using post-mortem somatic cells. Nat Biotechnol 2001; 19:962–964.
Steinborn R, Schinogl P, Zakhartchenko V et al. Mitochondrial DNA heteroplasmy in cloned cattle produced by fetal and adult cell cloning. Nat Genet 2000; 25:255–257.
Do JT, Lee JW, Lee BY et al. Fate of donor mitochondrial DNA in cloned bovine embryos produced by microinjection of cumulus cells. Biol Reprod 2002; 67:555–560.
Steinborn R, Schinogl P, Wells DN et al. Coexistence of Bos taurus and B. indicus mitochondrial DNAs in nuclear transfer-derived somatic cattle clones. Genetics 2002; 162:823–829.
Hiendleder S, Zakhartchenko V, Wenigerkind H et al. Heteroplasmy in bovine fetuses produced by intra-and inter-subspecific somatic cell nuclear transfer: Neutral segregation of nuclear donor mitochondrial DNA in various tissues and evidence for recipient cow mitochondria in fetal blood. Biol Reprod 2003; 68:159–166.
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.
Han ZM, Chen DY, Li JS et al. Mitochondrial DNA heteroplasmy in calves cloned by using adult somatic cell. Mol Reprod Dev 2004; 67:207–214.
Theoret CL, Dore M, Mulon PY et al. Short-and long-term skin graft survival in cattle clones with different mitochondrial haplotypes. Theriogenology 2006; 65:1465–1479.
Jiang Y, Liu SZ, Zhang YL. The fate of mitochondria in Ibex-hirus reconstructed early embryos. Acta Biochim Biophys Sin 2004; 36:371–374.
St John JC, 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.
Takeda K, Tasai M, Iwamoto M et al. Transmission of mitochondrial DNA in pigs and progeny derived from nuclear transfer of Meishan pig fibroblast cells. Mol Reprod Dev 2006; 73:306–312.
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.
Polejaeva IA, Chen SH, Vaught TD et al. Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 2000; 407:86–90.
Battersby BJ, Loredo-Osti JC, Shoubridge EA. Nuclear genetic control of mitochondrial DNA segregation. Nat Genet 2003; 33:183–186.
Loftus RT, MacHugh DE, Bradley DG et al. Evidence for two independent domestications of cattle. Proc Natl Acad Sci USA 1994; 91:2757–2761.
Luikart G, Gielly L, Excoffier L et al. Multiple maternal origins and weak phylogeographic structure in domestic goats. Proc Natl Acad Sci USA 2001; 98:5927–5932.
Giuffra E, Kijas J, Amarger V et al. The origin of the domestic pig: independent domestication and subsequent introgression. Genetics 2000; 154:1785–1791.
Lanza RP, Cibelli JB, Diaz F et al. Cloning of an endangered species (Bos gaurus) using interspecies nuclear transfer. Cloning 2000; 2:79–90.
Chen DY, Wen DC, Zhang YP et al. Interspecies implantation and mitochondria fate of panda-rabbit cloned embryos. Biol Reprod 2002; 67:637–642.
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.
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.
Chen Y, He ZX, Liu A et al. Embryonic stem cells generated by nuclear transfer of human somatic nuclei into rabbit oocytes. Cell Res 2003; 13:251–263.
Jiang Y, Chen T, Wang K et al. Different fates of donor mitochondrial DNA in bovine-rabbit and cloned bovine-rabbit reconstructed embryos during preimplantation development. Front Biosci 2006; 11:1425–1432.
Jiang Y, Chen T, Nan CL et al. In vitro culture and mtDNA fate of ibex-rabbit nuclear transfer embryos. Zygote 2005; 13:233–240.
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.
Li Y, Dai Y, Du W et al. Cloned endangered species takin (Budorcas taxicolor) by inter-species nuclear transfer and comparison of the blastocyst development with yak (Bos grunniens) and bovine. Mol Reprod Dev 2006; 73:189–195.
Sansinena M, Lynn J, Denniston R et al. Ooplasmic transfer after interspecies nuclear transfer: Presence of foreign mitochondria, pattern of migration and effect on embryo development. Reprod Fert Dev 2005; 17:182.
Richly E, Leister D. NUMTs in sequenced eukaryotic genomes. Mol Biol Evol 2004; 21:1081–108.
Parfait B, Rustin P, Munnich A et al. Coamplification of nuclear pseudogenes and assessment of heteroplasmy of mitochondrial DNA mutations. Biochem Biophys Res Commun 1998; 247:57–59.
Sorenson MD, Fleischer RC. Multiple independent transpositions of mitochondrial DNA control region sequences to the nucleus. Proc Natl Acad Sci USA 1996; 93:15239–15243.
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.
Tully LA, Parsons TJ, Steighner RJ et al. A sensitive denaturing gradient-Gel electrophoresis assay reveals a high frequency of heteroplasmy in hypervariable region 1 of the human mtDNA control region. Am J Hum Genet 2000; 67:432–443.
Hiendleder S, Bebbere D, Zakhartchenko V et al. Maternal-fetal transplacental leakage of mitochondrial DNA in bovine nuclear transfer pregnancies: Potential implications for offspring and recipients. Cloning Stem Cells 2004; 6:150–156.
Jansen RP. Germline passage of mitochondria: Quantitative considerations and possible embryo-logical sequelae. Hum Reprod 2000; 15(Suppl 2):112–128.
Takeda K, Tasai M, Iwamoto M et al. Microinjection of cytoplasm or mitochondria derived from somatic cells affects parthenogenetic development of murine oocytes. Biol Reprod 2005; 72:1397–1404.
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.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2007 Landes Bioscience and Springer Science+Business Media
About this chapter
Cite this chapter
Hiendleder, S. (2007). Mitochondrial DNA Inheritance after SCNT. In: Sutovsky, P. (eds) Somatic Cell Nuclear Transfer. Advances in Experimental Medicine and Biology, vol 591. Springer, New York, NY. https://doi.org/10.1007/978-0-387-37754-4_8
Download citation
DOI: https://doi.org/10.1007/978-0-387-37754-4_8
Publisher Name: Springer, New York, NY
Print ISBN: 978-0-387-37753-7
Online ISBN: 978-0-387-37754-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)