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Porcine oocyte mtDNA copy number is high or low depending on the donor

Published online by Cambridge University Press:  18 December 2015

Hanne Skovsgaard Pedersen*
Affiliation:
Department of Animal Science, Aarhus University, DK-8830 Tjele, Denmark.
Peter Løvendahl
Affiliation:
Department of Molecular Biology and Genetics, Aarhus University, DK-8830 Tjele, Denmark.
Knud Larsen
Affiliation:
Department of Molecular Biology and Genetics, Aarhus University, DK-8830 Tjele, Denmark.
Lone Bruhn Madsen
Affiliation:
Department of Molecular Biology and Genetics, Aarhus University, DK-8830 Tjele, Denmark.
Henrik Callesen
Affiliation:
Department of Animal Science, Aarhus University, DK-8830 Tjele, Denmark.
*
All correspondence to: Hanne Skovsgaard Pedersen. Department of Animal Science, Aarhus University, DK-8830 Tjele, Denmark. Tel: +45 8715 7984. Fax: +45 8715 4249. E-mail: [email protected]

Summary

Oocyte capacity is relevant in understanding decreasing female fertility and in the use of assisted reproductive technologies in human and farm animals. Mitochondria are important to the development of a functionally good oocyte and the oocyte mtDNA copy number has been introduced as a useful parameter for prediction of oocyte competence. The aim of this study was to investigate: (i) if the oocyte donor has an influence on its oocyte's mtDNA copy number; and (ii) the relation between oocyte size and mtDNA copy number using pre- and postpubertal pig oocytes. Cumulus–oocyte complexes were collected from individual donor pigs. The oocytes were allocated into different size-groups, snap-frozen and single-oocyte mtDNA copy number was estimated by quantitative real-time PCR using the genes ND1 and COX1. Results showed that mean mtDNA copy number in oocytes from any individual donor could be categorized as either ‘high’ (≥100,000) or ‘low’ (<100,000) with no difference in threshold between pre- and postpubertal oocytes. No linear correlation was detected between oocyte size and mtDNA copy number within pre- and postpubertal oocytes. This study demonstrates the importance of the oocyte donor in relation to oocyte mtDNA copy number, irrespectively of the donor's puberty status and the oocyte's growth stage. Observations from this study facilitate both further investigations of the importance of mtDNA copy number and the unravelling of relations between different mitochondrial parameters and oocyte competence.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

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References

Al-Mashhadi, R.H., Sørensennm, C.B., Kragh, P.M., Christoffersen, C., Mortensen, M.B., Tolbod, L.P., Thim, T., Du, Y., Li, J., Liu, Y., Moldt, B., Schmidt, M., Vajta, G., Larsen, T., Purup, S., Bolund, L., Nielsen, L.B., Callesen, H., Falk, E., Mikkelsen, J.G. & Bentzon, J.F. (2013). Familial hypercholesterolemia and atherosclerosis in cloned minipigs created by DNA transposition of a human PCSK9 gain-of-function mutant. Sci. Transl. Med. 5, 166ra1 doi: 10.1126/scitranslmed.3004853 CrossRefGoogle ScholarPubMed
Alviggi, C., Humaidan, P., Howles, C.M., Tredway, D. & Hillier, S.G. (2009). Biological versus chronological ovarian age: implications for assisted reproductive technology. Reprod. Biol. Endocrinol. 7, 101–14.CrossRefGoogle ScholarPubMed
Bagg, M.A., Nottle, M.B., Armstrong, D.T. & Grupen, C.G. (2007). Relationship between follicle size and oocyte developmental competence in prepubertal and adult pigs. Reprod. Fertil. Dev. 19, 797803.CrossRefGoogle ScholarPubMed
Barritt, J., Willadsen, S., Brenner, C. & Cohen, J. (2001). Cytoplasmic transfer in assisted reproduction. Hum. Reprod. Update 7, 428–35.CrossRefGoogle ScholarPubMed
Bernt, M., Brabrand, A., Schierwater, B. & Stadler, P.F. (2013). Genomic aspects of mitochondrial genome evolution. Mol. Phylogenet. Evol. 69, 328–38.CrossRefGoogle ScholarPubMed
Bjerre, D., Madsen, L.B., Bendixen, C. & Larsen, K. (2006). Porcine Parkin: molecular cloning of PARK2 cDNA, expression analysis., and identification of a splicing variant. Biochem. Biophys. Res. Commun. 347, 803–13.CrossRefGoogle ScholarPubMed
Cotterill, M., Harris, S.E., Fernandez, E.C., Lu, J., Huntriss, J.D., Campbell, B.K. & Picton, H.M. (2013). The activity and copy number of mitochondrial DNA in ovine oocytes throughout oogenesis in vivo and during oocyte maturation in vitro . Mol. Hum. Reprod. 19, 444–50.CrossRefGoogle ScholarPubMed
Eisele, J., Schaefer, I.M., Randel Nyengaard, J., Post, H., Liebetanz, D., Brüel, A. & Mühlfeld, C. (2008). Effect of voluntary exercise on number and volume of cardiomyocytes and their mitochondria in the mouse left ventricle. Basic Res. Cardiol. 103, 1221.CrossRefGoogle ScholarPubMed
El Shourbagy, S.H., Spikings, E.C., Freitas, M. & St John, J.C. (2006). Mitochondria directly influence fertilisation outcome in the pig. J. Reprod. Fertil. 131, 233–45.CrossRefGoogle ScholarPubMed
Endo, M., Kimura, K., Kuwayama, T., Monji, Y. & Iwata, H. (2012). Effect of oestradiol during culture of bovine oocyte–granulosa cell complexes on the mitochondrial DNA copies of oocytes and telomere length of granulosa cells. Zygote 12, 19.Google Scholar
Hansen, P.J. (2011). Challenges to fertility in dairy cattle: from ovulation to the fetal stage of pregnancy. Rev. Bras. Reprod. Anim. 35, 229–38.Google Scholar
Human Fertilisation and Embryology Authority (2012). Fertility treatment in 2012, trends and figures. http://www.hfea.gov.uk/docs/FertilityTreatment2012TrendsFigures.PDF Google Scholar
Ikeda, K. & Takahashi, Y. (2003). Comparison of maturational and developmental parameters of oocytes recovered from prepubertal and adult pigs. Reprod. Fertil. Dev. 15, 215–21.CrossRefGoogle ScholarPubMed
Iwata, H., Goto, H., Tanaka, H., Sakaguchi, Y., Kimura, K., Kuwayama, T. & Monji, Y. (2011). Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes. Reprod. Fertil. Dev. 23, 424–32.CrossRefGoogle ScholarPubMed
Li, J., Pedersen, H.S., Li, R., Adamsen, J., Liu, Y., Schmidt, M., Purup, S. & Callesen, H. (2013). Developmental potential of pig embryos reconstructed by use of sow versus pre-pubertal gilt oocytes after somatic cell nuclear transfer. Zygote 18, 110.Google Scholar
Løvendahl, P. & Chagunda, M.G.G. (2011). Covariance among milking frequency., milk yield., and milk composition from automatically milked cows. J. Dairy Sci. 94, 5381–92.CrossRefGoogle ScholarPubMed
Marchal, R., Vigneron, C., Perreau, C., Bali-Papp, A. & Mermillod, P. (2002). Effect of follicular size on meiotic and developmental competence of porcine oocytes. Theriogenology 57, 1523–32.CrossRefGoogle ScholarPubMed
May-Panloup, P., Chretien, M.F., Jacques, C., Vasseur, C., Malthiery, Y. & Reynier, P. (2005). Low oocyte mitochondrial DNA content in ovarian insufficiency. Hum. Reprod. 20, 593–7.CrossRefGoogle ScholarPubMed
Pedersen, H.S., Callesen, H., Løvendahl, P., Chen, F., Nyengaard, J.R., Nikolaisen, N.K., Holm, P. & Hyttel, P. (2014). Ultrastructure and mitochondrial numbers in pre- and postpubertal pig oocytes. Reprod. Fert. Dev. doi.org/10.1071/RD14220 [Epub ahead of print]CrossRefGoogle Scholar
Pedersen, H.S., Løvendahl, P., Larsen, K., Madsen, L.B. & Callesen, H. (2015a). mtDNA copy number in oocytes of different sizes from individual pre- and postpubertal pigs. Reprod. Fert. Dev. 27, 181182.CrossRefGoogle Scholar
Pedersen, H.S., Liu, Y., Li, R., Purup, S., Løvendahl, P., Holm, P., Hyttel, P. & Callesen, H. (2015b). Selection of pre- versus postpubertal pig oocytes for parthenogenetic activation and somatic cell nuclear transfer. Reprod. Fert. Dev. 27, 544–50.CrossRefGoogle ScholarPubMed
Piko, L. & Matsumoto, L. (1976). Number of mitochondria and some properties of mitochondrial DNA in the mouse egg. Dev. Biol. 49, 110.CrossRefGoogle ScholarPubMed
Ponsart, C., Le Bourhis, D., Knijn, H., Fritz, S., Guyader-Joly, C., Otter, T., Lacaze, S., Charreauz, F., Schibler, L., Dupassieux, D. & Mullaart, E. (2014). Reproductive technologies and genomic selection in dairy cattle. Reprod. Fert. Dev. 26, 1221.CrossRefGoogle Scholar
Reader, K.L., Cox, N.R., Stanton, J.L. & Juengel, J.L. (2014). Mitochondria and vesicles differ between adult and prepubertal sheep oocytes during IVM. Reprod. Fertil. Dev. doi.org/10.1071/RD13359 [Epub ahead of print]Google Scholar
Reynier, P., May-Panloup, P., Chrétien, M.F., Morgan, C.J., Jean, M., Savagner, F., Barrière, P. & Malthièry, Y. (2001). Mitochondrial DNA content affects the fertilizability of human oocytes. Mol. Hum. Reprod. 7, 425–9.CrossRefGoogle ScholarPubMed
Santos, T.A., El Shourbagy, S. & St John, J.C. (2006). Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil. Steril. 85, 584–91.CrossRefGoogle ScholarPubMed
Sato, D., Itami, N., Tasaki, H., Takeo, S., Kuwayama, T. & Iwata, H. (2014). Relationship between mitochondrial DNA copy number and SIRT1 expression in porcine oocytes. PLoS One 9, e94488.CrossRefGoogle ScholarPubMed
Schilling, M.F., Watkins, A.E. & Watkins, W. (2002). Is human height bimodal? The American Statistician 56, 223–9.CrossRefGoogle Scholar
Shoubridge, E.A. & Wai, T. (2007). Mitochondrial DNA and the mammalian oocyte. Curr. Top. Dev. Biol. 77, 87111.CrossRefGoogle ScholarPubMed
Society for Assisted Reproductive Technologies (2013). Clinic Summary Reports. https://www.sartcorsonline.com/rptCSR_PublicMultYear.aspx?ClinicPKID=0 Google Scholar
Wai, T., Ao, A., Zhang, X., Cyr, D., Dufort, D. & Shoubridge, E.A. (2010). The role of mitochondrial DNA copy number in mammalian fertility. Biol. Reprod. 83, 5262.CrossRefGoogle ScholarPubMed
Wang, J. & Sauer, M.V. (2006). In vitro fertilization (IVF): a review of three decades of clinical innovation and technological advancement. Ther. Clin. Risk Manag. 2, 355–64.CrossRefGoogle Scholar
Yoshioka, K., Suzuki, C., Tanaka, A., Anas, I.M.K. & Iwamura, S. (2002). Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol. Reprod. 66, 112–9.CrossRefGoogle Scholar
Zeng, H.T., Ren, Z., Yeung, W.S., Shu, Y.M., Xu, Y.W., Zhuang, G.L. & Liang, X.Y. (2007). Low mitochondrial DNA and ATP contents contribute to the absence of birefringent spindle imaged with PolScope in in vitro matured human oocytes. Hum. Reprod. 22, 1681–6.CrossRefGoogle Scholar
Zick, M., Rabl, R. & Reichert, A.S. (2009). Cristae formation – linking ultrastructure and function of mitochondria. Biochim. Biophys. Acta 1793, 519.CrossRefGoogle ScholarPubMed