CSIRO Publishing blank image blank image blank image blank imageBooksblank image blank image blank image blank imageJournalsblank image blank image blank image blank imageAbout Usblank image blank image blank image blank imageShopping Cartblank image blank image blank image You are here: Journals > Reproduction, Fertility and Development   
Reproduction, Fertility and Development
Journal Banner
  Vertebrate Reproductive Science & Technology
 
blank image Search
 
blank image blank image
blank image
 
  Advanced Search
   

Journal Home
About the Journal
Editorial Board
Contacts
Content
All Issues
Special Issues
Research Fronts
Sample Issue
For Authors
General Information
Instructions to Authors
Submit Article
Open Access
For Referees
Referee Guidelines
Review an Article
Annual Referee Index
For Subscribers
Subscription Prices
Customer Service
Print Publication Dates

blue arrow e-Alerts
blank image
Subscribe to our email Early Alert or RSS feeds for the latest journal papers.

red arrow Connect with us
blank image
facebook twitter youtube

red arrow Connect with SRB
blank image
facebook TwitterIcon

Affiliated Societies

RFD is the official journal of the International Embryo Transfer Society and the Society for Reproductive Biology.


 

Article << Previous     |     Next >>        Online Early    

Mitochondria and vesicles differ between adult and prepubertal sheep oocytes during IVM

Karen L. Reader A D , Neil R. Cox B , Jo-Ann L. Stanton C and Jennifer L. Juengel A

A Animal Productivity, AgResearch, Invermay Agricultural Centre, Private Bag 50034, Mosgiel 9053, New Zealand.
B Bioinformatics and Statistics, AgResearch, Invermay Agricultural Centre, Private Bag 50034, Mosgiel 9053, New Zealand.
C Department of Anatomy, University of Otago, PO Box 56, Dunedin 9054, New Zealand.
D Corresponding author. Email: karen.reader@agresearch.co.nz

Reproduction, Fertility and Development - http://dx.doi.org/10.1071/RD13359
Submitted: 23 October 2013  Accepted: 20 December 2013   Published online: 24 January 2014


 
PDF (474 KB) $25
 Export Citation
 Print
  
Abstract

Oocytes from prepubertal animals have a reduced ability to undergo normal embryo development and produce viable offspring. The correct quantity, activity and cytoplasmic distribution of oocyte organelles are essential for oocyte maturation, fertilisation and subsequent embryo development. The aim of this study was to quantify the ultrastructural differences between oocytes from prepubertal lamb and adult ewes using electron microscopy and stereology. We also determined whether quantitative polymerase chain reaction (qPCR) methods give comparable estimates of mitochondrial number to stereology. Mean storage vesicle volume was greater in adult compared with lamb oocytes before IVM and decreased during maturation in both adult and lamb oocytes. Mitochondrial volume and number increased in adult oocytes during maturation; however, no increase was observed in lamb oocytes. Mitochondrial DNA copy number measured by qPCR showed no differences between adult and lamb oocytes. A different distribution of mitochondria was observed in lamb oocytes before maturation, while the percentage of hooded mitochondria increased during maturation in adult oocytes and decreased in the lamb. In conclusion, the present study has identified differences in the vesicles and mitochondria between adult and lamb oocytes from ewes that may contribute to reduced developmental competence in prepubertal oocytes.

Additional keywords: embryo, electron microscopy, in vitro maturation, lipid, mtDNA copy number, oocyte quality.


References

Angermüller, S., and Fahimi, H. D. (1982). Imidazole-buffered osmium tetroxide: an excellent stain for visualization of lipids in transmission electron microscopy. Histochem. J. 14, 823–835.
CrossRef | PubMed |

Armstrong, D. T. (2001). Effects of maternal age on oocyte developmental competence. Theriogenology 55, 1303–1322.
CrossRef | CAS | PubMed |

Auclair, S., Uzbekov, R., Elis, S., Sanchez, L., Kireev, I., Lardic, L., Dalbies-Tran, R., and Uzbekova, S. (2013). Absence of cumulus cells during in vitro maturation affects lipid metabolism in bovine oocytes. Am. J. Physiol. Endocrinol. Metab. 304, E599–E613.
CrossRef | CAS | PubMed |

Barakat, I. A. H., El-Ashmaoui, H. M., Barkawi, A., Kandeal, S. A., and El-Nahass, E. (2012). Ultra-structural study of Egyptian buffalo oocytes before and after in vitro maturation. Afr. J. Biotechnol. 11, 7592–7602.
CrossRef | CAS |

Berlinguer, F., Leoni, G., Succu, S., Satta, V., Manca, M., Piu, P., Gallus, M., Gonzales Bulnes, A., and Naitana, S. (2011). Effect of season on the in vitro embryo production from prepubertal ovine oocytes. Reprod. Domest. Anim. 46, 90.

Boni, R., Cocchia, N., Silvestre, F., Tortora, G., Lorizio, R., and Tosti, E. (2008). Juvenile and adult immature and in vitro matured ovine oocytes evaluated in relation to membrane electrical properties, calcium stores, IP3 sensitivity and apoptosis occurrence in cumulus cells. Mol. Reprod. Dev. 75, 1752–1760.
CrossRef | CAS | PubMed |

Brevini, T. A. L., Cillo, F., Antonini, S., and Gandolfi, F. (2007). Cytoplasmic remodelling and the acquisition of developmental competence in pig oocytes. Anim. Reprod. Sci. 98, 23–38.
CrossRef | 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 | CAS | PubMed |

Cognié, Y., Poulin, N., Locatelli, Y., and Mermillod, P. (2004). State-of-the-art production, conservation and transfer of in-vitro-produced embryos in small ruminants. Reprod. Fertil. Dev. 16, 437–445.
CrossRef | PubMed |

Cotterill, M., Harris, S. E., Collado Fernandez, E., Lu, J., Huntriss, J. D., Campbell, B. K., and 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, 444–450.
CrossRef | CAS | PubMed |

Cran, D. G. (1985). Qualitative and quantitative structural changes during pig oocyte maturation. J. Reprod. Fertil. 74, 237–245.
CrossRef | CAS | PubMed |

Cran, D. G., Moor, R. M., and Hay, M. F. (1980). Fine structure of the sheep oocyte during antral follicle development. J. Reprod. Fertil. 59, 125–132.
CrossRef | CAS | PubMed |

Cruz-Orive, L. M., and Hunziker, E. B. (1986). Stereology for anisotropic cells: application to growth cartilage. J. Microsc. 143, 47–80.
CrossRef | CAS | PubMed |

Damiani, P., Fissore, R. A., Cibelli, J. B., Long, C. R., Balise, J. J., Robl, J. M., and Duby, R. T. (1996). Evaluation of developmental competence, nuclear and ooplasmic maturation of calf oocytes. Mol. Reprod. Dev. 45, 521–534.
CrossRef | CAS | PubMed |

de Paz, P., Sánchez, A. J., De la Fuente, J., Chamorro, C. A., Alvarez, M., Anel, E., and Anel, L. (2001). Ultrastructural and cytochemical comparison between calf and cow oocytes. Theriogenology 55, 1107–1116.
CrossRef | CAS | PubMed |

Docampo, R., and Moreno, S. N. J. (2011). Acidocalcisomes. Cell Calcium 50, 113–119.
CrossRef | CAS | PubMed |

Docampo, R., de Souza, W., Miranda, K., Rohloff, P., and Moreno, S. N. H. (2005). Acidocalcisomes – conserved from bacteria to man. Nat. Rev. Microbiol. 3, 251–261.
CrossRef | CAS | PubMed |

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 | CAS | PubMed |

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 | CAS | PubMed |

Fair, T., Hulshof, S. C., Hyttel, P., Greve, T., and Boland, M. (1997). Oocyte ultrastructure in bovine primordial to early tertiary follicles. Anat. Embryol. (Berl.) 195, 327–336.
CrossRef | CAS | PubMed |

Falconnier, C., and Kress, A. (1992). Ultrastructural aspects of oocyte growth in the marsupial Monodelphis domestica (grey short-tailed opossum). J. Anat. 181, 481–498.
| PubMed |

Ferreira, E. M., Vireque, A. A., Adona, P. R., Meirelles, F. V., Ferriani, R. A., and Navarro, P. A. A. S. (2009). Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71, 836–848.
CrossRef | CAS | PubMed |

Gou, K., Guan, H., Bai, J., Cui, X., Wu, Z., Yan, F., and An, X. (2009). Field evaluation of juvenile in vitro embryo transfer (JIVET) in sheep. Anim. Reprod. Sci. 112, 316–324.
CrossRef | PubMed |

Hyttel, P., Callesen, H., and Greve, T. (1986a). Ultrastructural features of preovulatory oocyte maturation in superovulated cattle. J. Reprod. Fertil. 76, 645–656.
CrossRef | CAS | PubMed |

Hyttel, P., Xu, K. P., Smith, S., and Greve, T. (1986b). Ultrastructure of in-vitro oocyte maturation in cattle. J. Reprod. Fertil. 78, 615–625.
CrossRef | CAS | PubMed |

Iwata, H., Goto, H., Tanaka, H., Sakaguchi, Y., Kimura, K., Kuwayama, T., and Monji, Y. (2011). Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes. Reprod. Fertil. Dev. 23, 424–432.
CrossRef | CAS | PubMed |

Kochhar, H. P. S., Wu, B., Morris, L. H. A., Buckrell, B. C., Pollard, J. W., Basrur, P. K., and King, W. A. (2002). Maturation status, protein synthesis and developmental competence of oocytes derived from lambs and ewes. Reprod. Domest. Anim. 37, 19–25.
CrossRef | CAS |

Kruip, T. A. M., Cran, D. G., van Beneden, T. H., and Dieleman, S. J. (1983). Structural changes in bovine oocytes during final maturation in vivo. Gamete Res. 8, 29–47.
CrossRef | CAS |

Ledda, S., Bogliolo, L., Calvia, P., Leoni, G., and Naitana, S. (1997). Meiotic progression and developmental competence of oocytes collected from juvenile and adult ewes. J. Reprod. Fertil. 109, 73–78.
CrossRef | CAS | PubMed |

Leoni, G. G., Bebbere, D., Succu, S., Berlinguer, F., Mossa, F., Galioto, M., Bogliolo, L., Ledda, S., and Naitana, S. (2007). Relations between relative mRNA abundance and developmental competence of ovine oocytes. Mol. Reprod. Dev. 74, 249–257.
CrossRef | CAS | PubMed |

Máximo, D. M., Martins da Silva, I. G., Mondadori, R. G., Neves, J. P., and Lucci, C. M. (2012). Ultrastructural characteristics of sheep oocytes during in vitro maturation (IVM). Small Rumin. Res. 105, 210–215.
CrossRef |

Mayhew, T. M. (1991). The new stereological methods for interpreting functional morphology from slices of cells and organs. Exp. Physiol. 76, 639–665.
| CAS | PubMed |

McEvoy, T. G., Coull, G. D., Broadbent, P. J., Hutchinson, J. S. M., and Speake, B. K. (2000). Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J. Reprod. Fertil. 118, 163–170.
| CAS | PubMed |

O’Brien, J. K., Dwarte, D., Ryan, J. P., Maxwell, W. M., and Evans, G. (1996). Developmental capacity, energy metabolism and ultrastructure of mature oocytes from prepubertal and adult sheep. Reprod. Fertil. Dev. 8, 1029–1037.
CrossRef | CAS | PubMed |

O’Brien, J. K., Catt, S. L., Ireland, K. A., Maxwell, W. M. C., and Evans, G. (1997). In vitro and in vivo developmental capacity of oocytes from prepubertal and adult sheep. Theriogenology 47, 1433–1443.
CrossRef | CAS | PubMed |

O’Brien, J. K., Dwarte, D., Ryan, J. P., Maxwell, W. M. C., and Evans, G. (2000). Comparison of in vitro maturation, in vitro fertilization, metabolism and ultrastructure of oocytes from prepubertal and adult pigs. Reprod. Domest. Anim. 35, 101–107.

Petr, J., Rozinek, J., Hruban, V., Jílek, F., Sedmíková, M., Vaňourková, Z., and Němeček, Z. (2001). Ultrastructural localization of calcium deposits during in vitro culture of pig oocytes. Mol. Reprod. Dev. 58, 196–204.
CrossRef | CAS | PubMed |

Pikó, L., and Matsumoto, L. (1976). Number of mitochondria and some properties of mitochondrial DNA in the mouse egg. Dev. Biol. 49, 1–10.
CrossRef | PubMed |

Pikó, 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 | PubMed |

Ptak, G., Loi, P., Dattena, M., Tischner, M., and Cappai, P. (1999). Offspring from one-month-old lambs: studies on the developmental capability of prepubertal oocytes. Biol. Reprod. 61, 1568–1574.
CrossRef | CAS | PubMed |

Quirke, J. F., and Hanrahan, J. P. (1977). Comparison of the survival in the uteri of adult ewes of cleaved ova from adult ewes and ewe lambs. J. Reprod. Fertil. 51, 487–489.
CrossRef | CAS | PubMed |

Ramos, I. B., Miranda, K., Pace, D. A., Verbist, K. C., Lin, F. Y., Zhang, Y., Oldfield, E., Machado, E. A., De Souza, W., and Docampo, R. (2010). Calcium- and polyphosphate-containing acidic granules of sea urchin eggs are similar to acidocalcisomes, but are not the targets for NAADP. Biochem. J. 429, 485–495.
CrossRef | CAS | PubMed |

Reader, K. L., Haydon, L. J., Littlejohn, R. P., Juengel, J. L., and McNatty, K. P. (2012). Booroola BMPR1B mutation alters early follicular development and oocyte ultrastructure in sheep. Reprod. Fertil. Dev. 24, 353–361.
CrossRef | CAS | PubMed |

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 | CAS | PubMed |

Salamone, D. F., Damiani, P., Fissore, R. A., Robl, J. M., and Duby, R. T. (2001). Biochemical and developmental evidence that ooplasmic maturation of prepubertal bovine oocytes is compromised. Biol. Reprod. 64, 1761–1768.
CrossRef | CAS | PubMed |

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 | CAS | PubMed |

Senger, P. L., and Saacke, R. G. (1970). Unusual mitochondria of the bovine oocyte. J. Cell Biol. 46, 405–408.
CrossRef | CAS | PubMed |

Shoubridge, E. A., and Wai, T. (2007). Mitochondrial DNA and the mammalian oocyte. Curr. Top. Dev. Biol. 77, 87–111.
CrossRef | CAS | PubMed |

Stephens, R. J., and Bils, R. F. (1965). An atypical mitochondrial form in normal rat liver. J. Cell Biol. 24, 500–504.
CrossRef | CAS | PubMed |

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 | CAS | PubMed |

Stojkovic, M., Machado, S. A., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Gonçalves, P. B., and Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 64, 904–909.
CrossRef | CAS | PubMed |

Tandler, B., Krahenbuhl, S., and Brass, E. P. (1991). Unusual mitochondria in the hepatocytes of rats treated with a vitamin B12 analogue. Anat. Rec. 231, 1–6.
CrossRef | CAS | PubMed |

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 | CAS | PubMed |

Van Blerkom, J. (2008). Mitochondria as regulatory forces in oocytes, preimplantation embryos and stem cells. Reprod. Biomed. Online 16, 553–569.
CrossRef | PubMed |

Van Blerkom, J. (2009). Mitochondria in early mammalian development. Semin. Cell Dev. Biol. 20, 354–364.
CrossRef | CAS | PubMed |

Vasilev, F., Chun, J. T., Gragnaniello, G., Garante, E., and Santella, L. (2012). Effects of ionomycin on egg activation and early development in starfish. PLoS ONE 7, e39231.
CrossRef | CAS | PubMed |

Velilla, E., Rodriguez-Gonzalez, E., Vidal, F., Izquierdo, D., and Paramio, M. T. (2006). Mitochondrial organization in prepubertal goat oocytes during in vitro maturation and fertilization. Mol. Reprod. Dev. 73, 617–626.
CrossRef | CAS | PubMed |

Zeng, H. T., Yeung, W. S., Cheung, M. P., Ho, P. C., Lee, C. K., Zhuang, G. L., Liang, X. Y., and O, W. S. (2009). In vitro-matured rat oocytes have low mitochondrial deoxyribonucleic acid and adenosine triphosphate contents and have abnormal mitochondrial redistribution. Fertil. Steril. 91, 900–907.
CrossRef | CAS | PubMed |


   
Subscriber Login
Username:
Password:  

 
    
Legal & Privacy | Contact Us | Help

CSIRO

© CSIRO 1996-2014