Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-23T21:08:45.677Z Has data issue: false hasContentIssue false

Mitochondria during sea urchin oogenesis

Published online by Cambridge University Press:  09 March 2017

Maria Agnello*
Affiliation:
Dipartimento di Scienze e Tecnologie Biologiche, Chimiche e Farmaceutiche, Università degli Studi di Palermo, Viale delle Scienze, Ed. 16, Palermo 90128, Italy.
Maria Carmela Roccheri
Affiliation:
Dipartimento di Scienze e Tecnologie Biologiche, Chimiche e Farmaceutiche, Università degli Studi di Palermo, Viale delle Scienze, Ed. 16, 90128 Palermo, Italy.
Giovanni Morici
Affiliation:
Dipartimento di Scienze e Tecnologie Biologiche, Chimiche e Farmaceutiche, Università degli Studi di Palermo, Viale delle Scienze, Ed. 16, 90128 Palermo, Italy.
Anna Maria Rinaldi
Affiliation:
Dipartimento di Scienze e Tecnologie Biologiche, Chimiche e Farmaceutiche, Università degli Studi di Palermo, Viale delle Scienze, Ed. 16, 90128 Palermo, Italy.
*
All correspondence to: Maria Agnello. Dipartimento di Scienze e Tecnologie Biologiche, Chimiche e Farmaceutiche, Università degli Studi di Palermo, Viale delle Scienze, Ed. 16, Palermo 90128, Italy. Tel: +39 091 238 97 419. Fax: +39 091 65 77 210. E-mail: [email protected]

Summary

Sea urchin represents an ideal model for studies on fertilization and early development, but the achievement of egg competence and mitochondrial behaviour during oogenesis remain to be enlightened. Oocytes of echinoid, such as sea urchin, unlike other echinoderms and other systems, complete meiotic maturation before fertilization. Mitochondria, the powerhouse of eukaryotic cells, contain a multi-copy of the maternally inherited genome, and are involved directly at several levels in the reproductive processes, as their functional status influences the quality of oocytes and contributes to fertilization and embryogenesis. In the present paper, we report our latest data on mitochondrial distribution, content and activity during Paracentrotus lividus oogenesis. The analyses were carried out using confocal microscopy, in vivo incubating oocytes at different maturation stages with specific probes for mitochondria and mtDNA, and by immunodetection of Hsp56, a well known mitochondrial marker. Results show a parallel rise of mitochondrial mass and activity, and, especially in the larger oocytes, close to germinal vesicle (GV) breakdown, a considerable increase in organelle activity around the GV, undoubtedly for an energetic aim. In the mature eggs, mitochondrial activity decreases, in agreement with their basal metabolism. Further and significant information was achieved by studying the mitochondrial chaperonin Hsp56 and mtDNA. Results show a high increase of both Hsp56 and mtDNA. Taken together these results demonstrate that during oogenesis a parallel rise of different mitochondrial parameters, such as mass, activity, Hsp56 and mtDNA occurs, highlighting important tools in the establishment of developmental competence.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agnello, M., Chiarelli, R., Martino, C., Bosco, L. & Roccheri, A.M. (2016). Autophagy is required for sea urchin oogenesis and early development. Zygote 24, 918–26.Google Scholar
Agnello, M., Morici, G. & Rinaldi, A.M. (2008). A method for measuring mitochondrial mass and activity. Cytotechnology 56,145–9.CrossRefGoogle ScholarPubMed
Babayev, E. & Seli, E. (2015). Oocyte mitochondrial function and reproduction. Curr. Opin. Obstet. Gynecol. 27, 175–81.Google Scholar
Barritt, J., Brenner, C., Cohen, J. & Matt, D. (1999). Mitochondrial rearrangements in human oocytes and embryos. Mol. Hum. Reprod. 5, 927–33.CrossRefGoogle ScholarPubMed
Barritt, J.A., Kokot, M., Cohen, J., Steuerwald, N. & Brenner, C.A. (2002). Quantification of human ooplasmic mitochondria. Reprod. Biomed. 4, 243–7.CrossRefGoogle ScholarPubMed
Berg, L. & Wessel, G.M. (1997). Cortical granules of the sea urchin translocate early in oocyte maturation. Development 124, 1845–50.CrossRefGoogle ScholarPubMed
Billett, F.S. & Adam, E. (1976). The structure of the mitochondrial cloud of Xenopus laevis oocytes. J. Embryol. Exp. Morphol. 36, 697710.Google Scholar
Bresch, H. (1978). Mitochondrial profile densities and areas in different developmental stages of the sea urchin Sphaerechinus granularis . Exp. Cell Res. 111, 205–9.Google Scholar
Bukovsky, A., Caudle, M.R., Svetlikova, M. & Upadhyaya, N.B. (2004). Origin of germ cells and formation of new primary follicles in adult human ovaries. Reprod. Biol. Endocrinol. 2, 20.Google Scholar
Buttino, I., Ianora, A., Carotenuto, Y., Zupo, V. & Miralto, A. (2003). Use of the confocal laser scanning microscope in studies on the developmental biology of marine crustaceans. Micros. Res. Tech. 60, 458–64.Google Scholar
Cao, L., Shitara, H., Horii, T. Nagao, Y., Imai, H., Abe, K., Hara, T., Hayashi, J. & Yonekawa, H. (2007). The mitochondrial bottleneck occurs without reduction of mtDNA content in female mouse germ cells. Nat. Genet. 39, 386–90.Google Scholar
Chang, P., Torres, J., Lewis, R. A. Mowry, K.L., Houliston, E. & King, M.L. (2004). Location of RNAs to the mitochondrial cloud in Xenopus oocytes through entrapment and association with endoplasmic reticulum. Mol. Biol. Cell. 15, 4669–81.Google Scholar
Costache, V., McDougall, A. & Dumollard, R. (2014). Cell cycle arrest and activation of development in marine invertebrate deuterostomes. Biochem. Biophys. Res. Commun. 450, 1175–81.Google Scholar
Coticchio, G., Dal Canto, M., Mignini Renzini, M., Guglielmo, M.C., Brambillasca, F., Turchi, D., Novara, P.V. & Fadini, R. (2015) Oocyte maturation: gamete-somatic cells interactions, meiotic resumption, cytoskeletal dynamics and cytoplasmic reorganization. Hum. Reprod. Update 21, 427–54.Google Scholar
Cuezva, J.M., Ostronoff, L.K., Ricart, J., López de Heredia, M., Di Liegro, C.M. & Izquierdo, J.M. (1997). Mitochondrial biogenesis in the liver during development and oncogenesis. J. Bioenerg. Biomembr. 29, 365−77.Google Scholar
Dalton, C.M. & Carroll, J. (2013). Biased inheritance of mitochondria during asymmetric cell division in the mouse oocyte. J. Cell Sci. 126, 2955–64.Google Scholar
de Paula, W.B., Agip, A.N., Missirlis, F., Ashworth, R., Vizcay-Barrena, G., Lucas, C.H. & Allen, J.F. (2013). Female and male gamete mitochondria are distinct and complementary in transcription, structure, and genome function. Genome Biol. Evol. 5, 1969–77.CrossRefGoogle ScholarPubMed
de Smedt, V., Szollosi, D. & Kloc, M. (2000). The balbiani body: asymmetry in the mammalian oocyte. Genesis 26, 208–12.Google Scholar
Di Liegro, C.M. & Rinaldi, A.M. (2007). Hsp56 mRNA in Paracentrotus lividus embryos binds to a mitochondrial protein. Cell Biol. Int. 31, 1331–5.Google Scholar
Di Liegro, C.M., Agnello, M., Casano, C., Roccheri, M.C., Gianguzza, F. & Rinaldi, A.M. (2008). Hsp56 protein and mRNA distribution in normal and stressed P. lividus embryos. Caryologia 61, 82–7.Google Scholar
Dumollard, R., Duchen, M. & Duchen, J. (2007). The role of mitochondrial function in the oocyte and embryo. Curr. Top. Dev. Biol. 77, 2149.Google Scholar
Enríquez, J.A., Fernández-Silva, P., Garrido-Pérez, N., López-Pérez, M.J., Pérez-Martos, A. & Montoya, J. (1999). Direct regulation of mitochondrial RNA synthesis by thyroid hormone. Mol. Cell Biol. 19, 657–70.Google Scholar
Fujiwara, A. & Yasumasu, I. (1997). Does the respiratory rate in sea urchin embryos increase during early development without proliferation of mitochondria? Dev. Growth Differ. 39, 179–89.Google Scholar
Gianguzza, F., Ragusa, M.A., Roccheri, M.C., Di Liegro, I. & Rinaldi, A.M. (2000). Isolation and characterization of a Paracentrotus lividus cDNA encoding a stress-inducible chaperonin. Cell Stress Chaperones 5, 87–9.Google Scholar
Giudice, G. (1985). The Sea Urchin Embryo. Springer-Verlag, Berlin, pp. 73–4.Google Scholar
Giudice, G., Sconzo, G., Bono, A. & Albanese, I. (1972). Studies on sea urchin oocytes. I. Purification and cell fractionation. Exp. Cell Res. 72, 90–4.CrossRefGoogle ScholarPubMed
Goffart, S. & Wiesner, R.J. (2003). Regulation and co-ordination of nuclear gene expression during mitochondrial biogenesis. Exp. Physiol. 88, 3340.CrossRefGoogle ScholarPubMed
Hertzler, P.L. & Clark, W.H. Jr (1992). Cleavage and gastrulation in the shrimp Sicyonia ingentis: invagination is accompanied by oriented cell division. Development 116, 127–40.Google Scholar
Holy, J.M. (1999). Imaging sea urchin fertilization. In Methods in Molecular Biology, Confocal Microscopy Methods and Protocols (ed. Paddock, S.W.). Humana Press, Totowa: New Jersey, pp. 153–66.Google Scholar
Hood, D.A. (2001). Invited Review: Contractile activity-induced mitochondrial biogenesis in skeletal muscle. J. Appl. Physiol. 90, 1137–57.Google Scholar
Kiyomoto, M., Zito, F., Costa, C., Poma, V., Sciarrino, S. & Matranga, V. (2007). Skeletogenesis by transfected secondary mesenchyme cells is dependent on extracellular matrix-ectoderm interactions in Paracentrotus lividus sea urchin embryos. Dev. Growth Differ. 49, 731–41.CrossRefGoogle Scholar
Klingenspor, M., Ivemeyer, M., Wiesinger, H., Haas, K., Heldmaier, G. & Wiesner, R.J. (1996). Biogenesis of thermogenic mitochondria in brown adipose tissue of Djungarian hamsters during cold adaptation. Biochem. J. 316, 607–13.Google Scholar
Kloc, M. & Etkin, L.D. (1998). Apparent continuity between the messenger transport organizer and late RNA localization pathways during oogenesis in Xenopus . Mech. Dev. 73, 95106.Google Scholar
Kloc, M., Bilinski, S., Dougherty, M.T., Brey, E.M. & Etkin, L.D. (2004). Formation, architecture and polarity of female germline cyst in Xenopus . Dev. Biol. 266, 4361.Google Scholar
Kloc, M., Jaglarz, M., Dougherty, M., Stewart, M.D., Nel-Themaat, L. & Bilinski, S. (2008). Mouse early oocytes are transiently polar: three-dimensional and ultrastructural analysis. Exp. Cell Res. 314, 3245–54.Google Scholar
Knaut, H., Pelegri, F., Bohmann, K. & Nüsslein-Volhard, C. (2000). Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification. J. Cell Biol. 149, 875–88.Google Scholar
Kosaka, K., Kawakami, K., Sakamoto, H. & Inoue, K. (2007). Spatiotemporal localization of germ plasm RNAs during zebrafish oogenesis. Mech. Dev. 124, 279–89.Google Scholar
Matsumoto, L., Kasamatsu, H., Pikó, L. & Vinograd, J. (1974) Mitochondrial DNA replication in sea urchin oocytes. J. Cell Biol. 63, 146–59.Google Scholar
May-Panloup, P., Chretien, M.F., Malthiery, Y. & Reynier, P. (2007). Mitochondrial DNA in the oocyte and the developing embryo. Curr. Top. Dev. Biol. 77, 5183.CrossRefGoogle ScholarPubMed
Morici, G., Agnello, M., Spagnolo, F., Roccheri, M.C., Di Liegro, C.M. & Rinaldi, A.M. (2007). Confocal microscopy study of the distribution, content and activity of mitochondria during Paracentrotus lividus development. J. Microsc. 228, 165–73.Google Scholar
Nagata, T. (2006). Electron microscopic radioautographic study on protein synthesis in hepatocyte mitochondria of aging mice. Sci. World J. 15, 1583–98.Google Scholar
Nishi, Y., Takeshita, T., Stato, K. & Araki, T. (2003). Change of the mitochondrial distribution in mouse ooplasm during in vitro maturation. J. Nippon Med. Sch. 70, 408–15.Google Scholar
Pawley, J.B. (ed.) (1995). Handbook of Biological Confocal Microscopy, 2nd edn. Plenum Press: New York.CrossRefGoogle Scholar
Pedersen, H.S., Løvendahl, P., Larsen, K., Madsen, L.B. & Callesen, H. (2016). Porcine oocyte mtDNA copy number is high or low depending on the donor. Zygote 24, 617–23.Google Scholar
Pepling, M.E., Wilhelm, J.E., O'Hara, A.L., Gephardt, G.W. & Spradling, A.C. (2007). Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body. Proc. Natl. Acad. Sci. USA 104, 187–92.Google Scholar
Perez, G.I., Trbovich, A.M., Gosgen, R.G. & Tilly, J.L. (2000). Mitochondria and the death of oocytes. Nature 403, 500–1.Google Scholar
Pollak, J.K. & Sutton, R. (1980). The transport and accumulation of adenine nucleotides during mitochondrial biogenesis. Biochem. J. 192, 7583.Google Scholar
Poulton, J. & Marchington, D.R. (2002). Segregation of mitochondrial DNA (mtDNA) in human oocytes and in animal models of mtDNA disease: clinical implications. Reproduction 123, 751−5.Google Scholar
Rinaldi, A.M., De Leo, G., Arzone, A., Salcher, I., Storace, A. & Mutolo, V. (1979a). Biochemical and electron microscopic evidence that cell nucleus negatively controls mitochondrial genomic activity in early sea urchin development. Proc. Natl. Acad. Sci. USA 76, 1916–20.CrossRefGoogle ScholarPubMed
Rinaldi, A.M., Salcher-Cillari, I. & Mutolo, V. (1979b). Mitochondrial division in not nucleated sea urchin eggs. Cell. Biol. Int. Rep. 3, 179–82.Google Scholar
Roccheri, M.C., Bosco, L., Ristuccia, M.E., Cascino, D., Giudice, G., Oliva, A.O. & Rinaldi, A.M. (1997). Sea urchin mitochondrial matrix contains a 56-kDa chaperonine-like protein. Biochem. Biophys. Res. Commun. 234, 646–50.Google Scholar
Roccheri, M.C., Patti, M., Agnello, M., Gianguzza, F., Carra, E. & Rinaldi, A.M. (2001). Localization of mitochondrial Hsp56 chaperonin during sea urchin development. Biochem. Biophys. Res. Commun. 287, 1093–8.Google Scholar
Schnapp, B.J., Arn, E.A., Deshler, J.O. & Highet, M.I. (1997). RNA localization in Xenopus oocytes. Semin. Cell. Dev. Biol. 8, 529–40.Google Scholar
Sieber, M.H., Thomsen, M.B. & Spradling, A.C. (2016). Electron transport chain remodeling by gsk3 during oogenesis connects nutrient state to reproduction. Cell 164, 420–32.CrossRefGoogle ScholarPubMed
Summers, R.G., Stricker, S.A. & Cameron, R.A. (1993). Applications of confocal microscopy to studies of sea urchin embryogenesis. In Methods in Cell Biology: Cell Biological Applications of Confocal Microscopy (ed. Matsumoto, B.). Academic Press, San Diego: California, USA pp. 266–86.Google Scholar
Sun, Q.Y., Wu, G. M., Lai, L. X. 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 depends on the stage of pre-ovulatory maturation. Theriogenology 61, 1675–89.Google Scholar
Van Blerkom, J. (2011). Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion 11, 797813.Google Scholar
Van Blerkom, J., Davis, P., Mathwig, V. & Alexander, S. (2002). Domains of high-polarized mitochondria may occur in mouse and human oocytes and early embryos. Hum. Reprod. 17, 393406.Google Scholar
Wessel, G.M., Berg, L. & Conner, S.D. (2004a). Cortical granule translocation is linked to meiotic maturation in the sea urchin oocyte. Development 129, 4315–25.Google Scholar
Wessel, G.M., Voronina, E. & Brooks, J.M. (2004b). Obtaining and handling echinoderm oocytes. Methods Cell Biol. 74, 87114.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
Yaffe, M.P. (1999). Dynamic mitochondria. Nat. Cell Biol. 1, E149–50.Google Scholar
Yakovlev, K.V. (2016). Localization of germ plasm-related structures during sea urchin oogenesis. Dev. Dynam. 245, 5666.Google Scholar
Yi, K., Rubinstein, B., Unruh, J.R., Guo, F., Slaughter, B.D. & Li, R. (2013). Sequential actin-based pushing forces drive meiosis I chromosome migration and symmetry breaking in oocytes. J. Cell Biol. 200, 567–76.Google Scholar
Zhang, W.H., Zhu, S.N., Lu, S.L., Huang, Y.L. & Zhao, P. (2000). Three-dimensional image of hepatocellular carcinoma under confocal laser scanning microscope. World J. Gastroenterol. 6, 344–7.CrossRefGoogle ScholarPubMed
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, 189201.Google Scholar