Asymmetrical allocation of mitochondrial DNA to blastomeres during the first two cleavages in mouse embryos
Yuichi Kameyama A C , Hidehisa Ohnishi A , Gaku Shimoi A , Ryoichi Hashizume A , Masao Ito A and Lawrence C. Smith BA Faculty of Bioindustry, Tokyo University of Agriculture, Abashiri, Hokkaido 099-2493, Japan.
B Centre de Recherche en Reproduction Animale, Faculté de Médecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Québec J2S7C6, Canada.
C Corresponding author. Email: y-kameya@bioindustry.nodai.ac.jp
Reproduction, Fertility and Development 22(8) 1247-1253 https://doi.org/10.1071/RD10076
Submitted: 13 April 2010 Accepted: 21 June 2010 Published: 1 October 2010
Abstract
A recent report showed higher oxygen consumption, adenosine triphosphate (ATP) production and mitochondrial localisation in trophectoderm cells than in the inner cell mass of mouse blastocysts. We hypothesised that this phenomenon was due to the asymmetrical distribution of mitochondria in the blastomeres during the earlier stages. Oocytes, 2-cell embryos and 4-cell embryos were analysed to determine the volume, ATP content and mitochondrial DNA (mtDNA) copy number in the whole egg and individual blastomeres. Significant differences were detected in the volumes of cytoplasm and ATP contents between blastomeres from the 2-cell and 4-cell embryos. Moreover, whilst remaining stable in whole embryos, mtDNA copy number differed between blastomeres, indicating that mitochondria in oocytes are unevenly delivered into the daughter blastomeres during the first two cleavages. Although their volume and ATP content were not correlated, there was a significant correlation between volume and mtDNA copy number in 2- and 4-cell blastomeres. These results indicate that the number of mitochondria delivered to blastomeres during early cleavage is not precisely equal, suggesting that the allocation of mitochondria into daughter blastomeres is affected by uneven cytoplasmic distribution during cytokinesis in the oocyte and mother blastomeres.
Additional keywords: ATP, early cleavage, mtDNA copy number.
Baltz, J. M. , and Tartia, A. P. (2010). Cell volume regulation in oocytes and early embryos: connecting physiology to successful culture media. Hum. Reprod. Update 16, 166–176.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Bavister, B. D. , and Squirrell, J. M. (2000). Mitochondrial distribution and function in oocytes and early embryos. Hum. Reprod. 15(Suppl. 2), 189–198.
| PubMed |
Brenner, C. A. , Kubisch, H. M. , and Pierce, K. E. (2004). Role of the mitochondrial genome in assisted reproductive technologies and embryonic stem cell-based therapeutic cloning. Reprod. Fertil. Dev. 16, 743–751.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Cao, L. , Shitara, H. , Horii, T. , Nagao, Y. , Imai, H. , Abe, K. , Hara, T. , Hayashi, J. , and Yonekawa, H. (2007). The mitochondrial bottleneck occurs without reduction of mtDNA content in female mouse germ cells. Nat. Genet. 39, 386–390.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Cummins, J. M. (2004). The role of mitochondria in the establishment of oocyte functional competence. Eur. J. Obstet. Gynecol. Reprod. Biol. 115(Suppl. 1), S23–S29.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Dumollard, R. , Duchen, M. , and Carroll, J. (2007). The role of mitochondrial function in the oocyte and embryo. Curr. Top. Dev. Biol. 77, 21–49.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
El Shourbagy, S. H. , Spikings, E. C. , Freitas, M. , and St John, J. C. (2006). Mitochondria directly influence fertilisation outcome in the pig. Reproduction 131, 233–245.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Fleming, T. P. , Papenbrock, T. , Fesenko, I. , Hausen, P. , and Sheth, B. (2000). Assembly of tight junctions during early vertebrate development. Semin. Cell Dev. Biol. 11, 291–299.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Ginsberg, L. , and Hillman, N. (1973). ATP metabolism in cleavage-staged mouse embryos. J. Embryol. Exp. Morphol. 30, 267–282.
| PubMed | CAS |
Houghton, F. D. (2006). Energy metabolism of the inner cell mass and trophectoderm of the mouse blastocyst. Differentiation 74, 11–18.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Houghton, F. D. , Thompson, J. G. , Kennedy, C. J. , and Leese, H. J. (1996). Oxygen consumption and energy metabolism of the early mouse embryo. Mol. Reprod. Dev. 44, 476–485.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Johnson, M. H. , and Ziomek, C. A. (1981). The foundation of two distinct cell lineages within the mouse morula. Cell 24, 71–80.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Kameyama, Y. , Filion, F. , Yoo, J. G. , and Smith, L. C. (2007). Characterization of mitochondrial replication and transcription control during rat early development in vivo and in vitro. Reproduction 133, 423–432.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Lawitts, J. A. , and Biggers, J. D. (1993). Culture of preimplantation embryos. Methods Enzymol. 225, 153–164.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Lin, D. P. , Huang, C. C. , Wu, H. M. , Cheng, T. C. , Chen, C. I. , and Lee, M. S. (2004). Comparison of mitochondrial DNA contents in human embryos with good or poor morphology at the 8-cell stage. Fertil. Steril. 81, 73–79.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Mahowald, A. P. , and Hennen, S. (1971). Ultrastructure of the “germ plasm” in eggs and embryos of Rana pipiens. Dev. Biol. 24, 37–53.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
McConnell, J. M. , and Petrie, L. (2004). Mitochondrial DNA turnover occurs during preimplantation development and can be modulated by environmental factors. Reprod. Biomed. Online 9, 418–424.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
McLaren, A. (2003). Primordial germ cells in the mouse. Dev. Biol. 262, 1–15.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Michaels, G. S. , Hauswirth, W. W. , and Laipis, P. J. (1982). Mitochondrial DNA copy number in bovine oocytes and somatic cells. Dev. Biol. 94, 246–251.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Motta, P. M. , Nottola, S. A. , Makabe, S. , and Heyn, R. (2000). Mitochondrial morphology in human fetal and adult female germ cells. Hum. Reprod. 15(Suppl. 2), 129–147.
| PubMed |
Nagai, S. , Mabuchi, T. , Hirata, S. , Shoda, T. , Kasai, T. , Yokota, S. , Shitara, H. , Yonekawa, H. , and Hoshi, K. (2004). Oocyte mitochondria: strategies to improve embryogenesis. Hum. Cell 17, 195–201.
| PubMed |
Nagai, S. , Mabuchi, T. , Hirata, S. , Shoda, T. , Kasai, T. , Yokota, S. , Shitara, H. , Yonekawa, H. , and Hoshi, K. (2006). Correlation of abnormal mitochondrial distribution in mouse oocytes with reduced developmental competence. Tohoku J. Exp. Med. 210, 137–144.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Nishi, Y. , Takeshita, T. , Sato, K. , and Araki, T. (2003). Change of the mitochondrial distribution in mouse ooplasm during in vitro maturation. J. Nippon Med. Sch. 70, 408–415.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Piko, L. , and Matsumoto, L. (1976). Number of mitochondria and some properties of mitochondrial DNA in the mouse egg. Dev. Biol. 49, 1–10.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Piko, L. , and Taylor, K. D. (1987). Amounts of mitochondrial DNA and abundance of some mitochondrial gene transcripts in early mouse embryos. Dev. Biol. 123, 364–374.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Reynier, P. , May-Panloup, P. , Chretien, M. F. , Morgan, C. J. , Jean, M. , Savagner, F. , Barriere, P. , and Malthiery, Y. (2001). Mitochondrial DNA content affects the fertilizability of human oocytes. Mol. Hum. Reprod. 7, 425–429.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Rossant, J. , and Tam, P. P. (2009). Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136, 701–713.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Santos, T. A. , El Shourbagy, S. , and St John, J. C. (2006). Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil. Steril. 85, 584–591.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Smith, L. C. , Thundathil, J. , and Filion, F. (2005). Role of the mitochondrial genome in preimplantation development and assisted reproductive technologies. Reprod. Fertil. Dev. 17, 15–22.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Spielmann, H. , Jacob-Mueller, U. , Schulz, P. , and Schimmel, A. (1984). Changes of the adenine ribonucleotide content during preimplantation development of mouse embryos in vivo and in vitro. J. Reprod. Fertil. 71, 467–473.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Steuerwald, N. , Barritt, J. A. , Adler, R. , Malter, H. , Schimmel, T. , Cohen, J. , and Brenner, C. A. (2000). Quantification of mtDNA in single oocytes, polar bodies and subcellular components by real-time rapid-cycle fluorescence-monitored PCR. Zygote 8, 209–215.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Suzuki, H. , Satoh, M. , and Kabashima, K. (2006). Distribution of mitochondria and the cytoskeleton in hamster embryos developed in vivo and in vitro. J. Mamm. Ova Res. 23, 128–134.
| Crossref | GoogleScholarGoogle Scholar |
Thundathil, J. , Filion, F. , and Smith, L. C. (2005). Molecular control of mitochondrial function in preimplantation mouse embryos. Mol. Reprod. Dev. 71, 405–413.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Trimarchi, J. R. , Liu, L. , Porterfield, D. M. , Smith, P. J. , and Keefe, D. L. (2000). Oxidative phosphorylation-dependent and -independent oxygen consumption by individual preimplantation mouse embryos. Biol. Reprod. 62, 1866–1874.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Van Blerkom, J. (2008). Mitochondria as regulatory forces in oocytes, preimplantation embryos and stem cells. Reprod. Biomed. Online 16, 553–569.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Van Blerkom, J. (2009). Mitochondria in early mammalian development. Semin. Cell Dev. Biol. 20, 354–364.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Van Blerkom, J. , Sinclair, J. , and Davis, P. (1998). Mitochondrial transfer between oocytes: potential applications of mitochondrial donation and the issue of heteroplasmy. Hum. Reprod. 13, 2857–2868.
| PubMed | CAS |
Van Blerkom, J. , Davis, P. , and Alexander, S. (2000). Differential mitochondrial distribution in human pronuclear embryos leads to disproportionate inheritance between blastomeres: relationship to microtubular organization, ATP content and competence. Hum. Reprod. 15, 2621–2633.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Wai, T. , Ao, A. , Zhang, X. , Dufort, D. , and Shoubridge, E. A. (2010). The role of mitochondrial DNA copy number in mammalian fertility. Biol. Reprod. 83, 52–62.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |