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Distribution pattern and activity of mitochondria during oocyte growth and maturation in the ascidian Styela plicata*

Published online by Cambridge University Press:  18 January 2013

Amina Bezzaouia ,
Alessandra Gallo ,
Francesco Silvestre ,
Saïda Tekaya  and
Elisabetta Tosti
Amina Bezzaouia
Affiliation:
Université de Tunis El-Manar, Faculté des Sciences de Tunis, UR11ES12 Biologie de la Reproduction et du Développement Animal, 2092, Tunis, Tunisie
Alessandra Gallo
Affiliation:
Animal Physiology and Evolution Laboratory, Stazione Zoologica Anton Dohrn, Napoli, Italy.
Francesco Silvestre
Affiliation:
Animal Physiology and Evolution Laboratory, Stazione Zoologica Anton Dohrn, Napoli, Italy.
Saïda Tekaya
Affiliation:
Université de Tunis El-Manar, Faculté des Sciences de Tunis, UR11ES12 Biologie de la Reproduction et du Développement Animal, 2092, Tunis, Tunisie
Elisabetta Tosti*
Affiliation:
Animal Physiology and Evolution Laboratory, Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy.
*
All correspondence to: Elisabetta Tosti. Animal Physiology and Evolution Laboratory, Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy. Tel: +39 0815833288. Fax: +39 0817641355. e-mail: tosti@szn.it
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Summary

The process of oocyte maturation is underlined by a redistribution of cellular organelles, among which mitochondria play a functional role for the acquisition of fertilization and developmental competence. In this paper, we applied electron and confocal microscopy by using DIOC6 and JC-1 stain to evaluate mitochondria distribution pattern and activity during different stages of oocyte growth in the ascidian Styela plicata. Three categories of oocytes at the germinal vesicle stage underlying the vitellogenic process were characterized on the basis of size, pigmentation and accessory cells. Mitochondria were spread throughout the cytoplasm at the smallest oocyte stage and gradually migrated to the periphery of the subcortical cytoplasm at the intermediate stage. At the fully grown oocyte stage, mitochondria were aggregated in the subcortical cytoplasm. This pattern of polarized mitochondria distribution correlates significantly with an increase in mitochondria potential and activity. In this paper we discuss the relationship of mitochondria to the acquisition of oocyte developmental competence.

Keywords

Mitochondria distributionMitochondria membrane potentialOocyte growthOocyte maturationStyela plicata
Type
Research Article
Information
Zygote , Volume 22 , Issue 4 , November 2014 , pp. 462 - 469
Copyright
Copyright © Cambridge University Press 2013 

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Footnotes

*

This work is dedicated to the dear memory of Prof. Charles Lambert.

References

Acton, B., Jurisicova, A., Jurisica, I. & Casper, R. (2004). Alterations in mitochondrial membrane potential during preimplantation stages of mouse and human embryo development. Mol. Hum. Reprod. 10, 23–32.CrossRefGoogle ScholarPubMed
Bavister, B.D. & Squirrell, J.M. (2000). Mitochondrial distribution and function in oocytes and early embryos. Hum. Reprod. 15 Suppl. 2, 189–98.Google Scholar
Cummins, J.M. (2004). The role of mitochondria in the establishment of oocyte functional competence. Eur. J. Obstet. Gynecol. Reprod. Biol. 115 Suppl. 1, S23–9.Google Scholar
Dale, B. (1983). Fertilization in Animals. London: Edward Arnold.Google Scholar
Dale, B. (1989). Fertilization in ascidians. In: Non Mammalian Animal Models for Biomedical Research (eds. Woodhead, A.) pp. 87–103. Boca Raton: CRC Press.Google Scholar
Dale, B. & Elder, K. (1997). In Vitro Fertilization. Cambridge: Cambridge University Press.Google Scholar
Dumollard, R., Hammar, K., Porterfield, M., Smith, P.J., Cibert, C., Rouvière, C. & Sardet, C. (2003). Mitochondrial respiration and Ca2+ waves are linked during fertilization and meiosis completion. Development 130, 683–92.Google Scholar
Dumollard, R., Marangos, P., Fitzharris, G., Swann, K., Duchen, M. & Carroll, J. (2004). Sperm-triggered [Ca2+] oscillations and Ca2+ homeostasis in the mouse egg have an absolute requirement for mitochondrial ATP production. Development 131, 3057–67.Google Scholar
Dumollard, R., Duchen, M. & Sardet, C. (2006). Calcium signals and mitochondria at fertilisation. Semin. Cell. Dev. Biol. 17, 314–23.Google Scholar
Dumollard, R., Duchen, M. & Carroll, J. (2007). The role of mitochondrial function in the oocyte and embryo. Curr. Top. Dev. Biol. 77, 21–49.Google Scholar
Duran, H.E., Simsek-Duran, F., Oehninger, S.C., Jones, H.W. Jr. & Castora, F.J. (2011). The association of reproductive senescence with mitochondrial quantity, function, and DNA integrity in human oocytes at different stages of maturation. Fertil. Steril. 96, 384–8.Google Scholar
Eppig, J.J. (1996). Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod. Fertil. Dev. 8, 485–89.Google Scholar
Ferreira, E.M., Vireque, A.A., Adona, P.R., Meirelles, F.V., Ferriani, R.A. & Navarro, P.A.A.S. (2009). Cytoplasmic maturation of bovine oocytes: Structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71, 836–48.Google Scholar
Jeffery, W.R. & Capco, D.G. (1978). Differential accumulation and localization of maternal poly(A)-containing RNA during early development of the ascidian, Styela. Dev. Biol. 67, 152–66.Google Scholar
Motta, P.M., Nottola, S.A., Makabe, S. & Heyn, R. (2000). Mitochondrial morphology in human fetal and adult female germ cells. Hum. Reprod. 15 Suppl. 2, 129–47.Google Scholar
Nagai, S., Mabuchi, T., Hirata, S., Shoda, T., Kasai, T., Yokota, S., Shitara, H., Yonekawa, H. & Hoshi, K. (2006). Correlation of abnormal mitochondrial distribution in mouse oocytes with reduced developmental competence. Tohoku J. Exp. Med. 210, 137–44.Google Scholar
Nagano, M., Katagiri, S. & Takahashi, Y. (2006). ATP content and maturational/developmental ability of bovine oocytes with various cytoplasmic morphologies. Zygote 14, 299–04.Google Scholar
Nishi, Y., Takeshita, T., Sato, K. & Araki, T. (2003). Change of the mitochondrial distribution in mouse ooplasm during in vitro maturation. J. Nihon Med. Sch. 70, 408–15.Google Scholar
Prodon, F., Chenevert, J. & Sardet, C. (2006). Establishment of animal–vegetal polarity during maturation in ascidian oocytes. Dev. Biol. 290, 297–11.Google Scholar
Quinn, P., Warnes, G., Kerin, J. & Kirby, C. (1984). Culture factors in relation to the success of human in vitro fertilization and embryo transfer. Fertil. Steril. 41, 202–9.Google Scholar
Satoh, N. (1994). Developmental Biology of Ascidian. Cambridge: Cambridge University Press.Google Scholar
Stojkovic, M., Machado, S.A., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Goncalves, P.B. & 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 fertilisation and culture. Biol. Reprod. 64, 904–9.Google Scholar
Sun, Q.Y., Wu, G.M., Lai, L., Park, K.W., Cabot, R., Cheong, H.T., Day, B.N., Prather, R.S. & Schatten, H. (2001). Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction 122, 155–63.Google Scholar
Torner, H., Brüssow, K.P., Alm, H., Ratky, J., Pöhland, R., Tuchscherer, A. & Kanitz, W. (2004). Mitochondrial aggregation patterns and activity in porcine oocytes and apoptosis in surrounding cumulus cells depend on the stage of pre-ovulatory maturation. Theriogenology 61, 1675–89.Google Scholar
Tosti, E. & Boni, R. (2011). Oocyte Maturation and Fertilization: A Long History for a Short Event. Karachi: Bentham Science Publishers.Google Scholar
Tourmente, S., Lecher, P., Degroote, F. & Renaud, M. (1990). Mitochondrial development during Drosophila oogenesis: distribution, density and in situ RNA hybridizations. Biol. Cell. 68, 119–27.Google Scholar
Van Blerkom, J. (2004). Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction 128, 269–80.Google Scholar
Van Blerkom, J. (2008). Mitochondria as regulatory forces in oocytes, preimplantation embryos and stem cells. Reprod. Biomed. Online 16, 553–69.Google Scholar
Van Blerkom, J. (2011). Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion 11, 797–13.CrossRefGoogle ScholarPubMed
Van Blerkom, J. & Davis, P. (2007). Mitochondrial signaling and fertilization. Mol. Hum. Reprod. 13, 759–70.Google Scholar
Van Blerkom, J., Davis, P., Mathwig, V. & Alexander, S. (2002). Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos. Hum. Reprod. 17, 393–06.Google Scholar
Wassarman, P.M. & Josefowicz, W.J. (1978). Oocyte development in the mouse: an ultrastructural comparison of oocytes isolated at various stages of growth and meiotic competence. J. Morphol. 156, 209–35.Google Scholar
Wilding, M., Carotenuto, R., Infante, V., Dale, B., Marino, M., Di Matteo, L. & Campanella, C. (2001a). Confocal microscopy analysis of the activity of mitochondria contained within the ‘mitochondrial cloud’ during oogenesis in Xenopus laevis. Zygote 9, 347–52.Google Scholar
Wilding, M., Dale, B., Marino, M., Di Matteo, L., Alviggi, C., Pisaturo, M.L., Lombardi, L. & De Placido, G. (2001b). Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum. Reprod. 16, 909–17.Google Scholar
Wilding, M., De Placido, G., De Matteo, L., Marino, M., Alviggi, C. & Dale, B. (2003). Chaotic mosaicism in human preimplantation embryos is correlated with a low mitochondrial membrane potential. Fertil. Steril. 79, 340–6.Google Scholar
Wilk, K., Bilinski, S., Dougherty, M.T. & Kloc, M. (2005). Delivery of germinal granules and localized RNAs via the messenger transport organizer pathway to the vegetal cortex of Xenopus oocytes occurs through directional expansion of the mitochondrial cloud. Int. J. Dev. Biol. 49, 17–21.Google Scholar
Yanagimachi, R. (1994). Mammalian Fertilization. In The Physiology of Reproduction (eds. Knobil, E. & Neill, J.D.) vol. 1, pp. 189–317. New York: Raven press.Google Scholar
Zhang, Y.Z., Ouyang, Y.C., Hou, Y., Schatten, H., Chen, D.Y. & Sun, Q.Y. (2008). Mitochondrial behavior during oogenesis in zebrafish: a confocal microscopy analysis. Dev. Growth. Differ. 50, 189–201.Google Scholar