Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-10T13:36:02.423Z Has data issue: false hasContentIssue false
  • English
  • Français

In mouse oocytes the mitochondrion-originated germinal body-like structures accumulate mouse Vasa homologue (MVH) protein

Published online by Cambridge University Press:  29 April 2014

Arkadiy A. Reunov  and
Yulia A. Reunova
Arkadiy A. Reunov*
Affiliation:
Laboratory of Cell Differentiation, Paltchevsky st.-17, A.V. Zhirmunsky Institute of Marine Biology, Far East Branch of the Russian Academy of Sciences, 690041 Vladivostok, Russia.
Yulia A. Reunova
Affiliation:
A.V. Zhirmunsky Institute of Marine Biology FEB RAS, Laboratory of Cell Differentiation, Paltchevsky st.-17, Vladivostok 690041, Russia.
*
All correspondence to: A.A. Reunov, Laboratory of Cell Differentiation, Paltchevsky st.-17, A.V. Zhirmunsky Institute of Marine Biology, Far East Branch of the Russian Academy of Sciences, 690041 Vladivostok, Russia. Tel: +7 4232 311143. Fax: +7 4232 310900. e-mail: arkadiy_reunov@hotmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

Mouse Vasa homologue (MVH) antibodies were applied to mouse Graafian oocytes to clarify if mitochondrion-originated germinal body-like structures, described previously by conventional electron microscopy, were associated with the germ plasm. It was found that both the mitochondrion-like structures with cristae and the germinal body-like structures that lacked any signs of cristae were labelled specifically by the anti-MVH antibody. Moreover, some granules were MVH-positive ultrastructural hybrids of the mitochondria and germinal body-like structures, the presence of which clearly supported the idea of a mitochondrial origin for the germinal body-like structures. This finding is the first evidence that mitochondrion-originated germinal body-like granules represent mouse germ plasm.

Keywords

Germ plasmGerminal body-like structuresMouseMVH proteinOocytes
Type
Research Article
Information
Zygote , Volume 23 , Issue 4 , August 2015 , pp. 501 - 506
Copyright
Copyright © Cambridge University Press 2014 

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

Amikura, R., Kashikawa, M., Nakamura, A. & Kobayashi, S. (2001). Presence of mitochondria-type ribosomes outside mitochondria in germ plasm of Drosophila embryos. Proc. Natl. Acad. Sci. USA 98, 9133–8.CrossRefGoogle ScholarPubMed
Amikura, R., Sato, K. & Kobayashi, S. (2005). Role of mitochondrial ribosome-dependent translation in germline formation in Drosophila embryos. Mech. Dev. 122, 1087–93.CrossRefGoogle ScholarPubMed
Castrillon, D.H., Quade, B.J., Wang, T.Y., Quigley, C. & Crum, C.P. (2000). The human VASA gene is specifically expressed in the germ cell lineage. Proc. Natl. Acad. Sci. USA 97, 9585–90.CrossRefGoogle ScholarPubMed
Chang, P., Torres, J., Lewis, R.A., Mowry, K.L., Houliston, E. & King, M.L. (2004). Localization of RNAs to the mitochondrial cloud in Xenopus oocytes through entrapment and association with endoplasmic reticulum. Mol. Biol. Cell 15, 4669–81.CrossRefGoogle Scholar
Cox, R.T. & Spradling, A.C. (2003). A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development 130, 1579–90.CrossRefGoogle ScholarPubMed
Cuykendall, T.N. & Houston, D.W. (2010). Identification of germ plasm-associated transcripts by microarray analysis of Xenopus vegetal cortex RNA. Dev. Dyn. 239, 1838–48.CrossRefGoogle ScholarPubMed
Eddy, E.M. (1975). Germ plasm and the differentiation of the germ cell line. Int. Rev. Cytol. 43, 229–80.CrossRefGoogle ScholarPubMed
Eddy, E.M. & Hahnel, A.C. (1983). Establishment of the germ cell line in mammals. In Current Problems in Germ Cell Differentiation (eds McLaren, A. & Wylie, C.). Brit. Soc. Dev. Biol. Symp. 7, 41–69.Google Scholar
Edwards, R.G. & Beard, H.K. (1999). Hypothesis: sex determination and germline formation are committed at the pronucleate stage in mammalian embryos. Mol. Hum. Reprod. 5, 595–606.CrossRefGoogle ScholarPubMed
Ewen-Campen, B., Schwager, E.E. & Extavour, C.G.M. (2010).The molecular machinery of germ line specification. Mol. Reprod. Dev. 77, 3–18.CrossRefGoogle ScholarPubMed
Extavour, C.G. & Akam, M. 2003. Mechanisms of germ cell specification across the metazoans: epigenesist and preformation. Development 130, 5869–84.CrossRefGoogle Scholar
Hayashi, K., de Sousa Lopes, S.M. & Surani, M.A. (2007). Germ cell specification in mice. Science 316, 394–6.CrossRefGoogle ScholarPubMed
Hübner, K., Fuhrmann, G., Christenson, L.K., Kehler, J., Reinbold, R., De La Fuente, R., Wood, J., Strauss, J.F., Boiani, M. & Schöler, H.R. (2003). Derivation of oocytes from mouse embryonic stem cells. Science 300, 1251–6.CrossRefGoogle ScholarPubMed
Iida, T. & Kobayashi, S. (1998). Essential role of mitochondrially encoded large rRNA for germ-line formation in Drosophila embryos. Proc. Natl. Acad. Sci. USA 95, 11274–8.CrossRefGoogle ScholarPubMed
Ikenishi, K. (1998). Germ plasm in Caenorhabditis elegans, Drosophila and Xenopus. Dev. Growth Differ. 40, 1–10.CrossRefGoogle ScholarPubMed
King, M.L., Messitt, T. & Mowry, K. (2005). Putting RNAs in the right place at the right time: RNA localization in the frog oocyte. Biol. Cell 97, 19–33.CrossRefGoogle Scholar
Kloc, M., Bilinski, S., Chan, A.P. & Etkin, L.D. (2000). Mitochondrial ribosomal RNA in the germinal granules in Xenopus embryos revisited. Differentiation 67, 80–3.CrossRefGoogle Scholar
Kloc, M., Dougherty, M.T., Bilinski, S., Chan, A.P., Brey, E., King, M.L., Patrick, C.W. Jr & Etkin, L.D. (2002). Three-dimensional ultrastructural analysis of RNA distribution within germinal granules of Xenopus. Dev. Biol. 241, 79–93.CrossRefGoogle ScholarPubMed
Kloc, M., Bilinski, S. & Etkin, L.D. (2004). The Balbiani body and germ cell determinants: 150 years later. Curr. Top. Dev. Biol. 59, 1–36.CrossRefGoogle ScholarPubMed
Kobayashi, S., Amikura, R. & Okada, M. (1993). Presence of mitochondrial large ribosomal RNA outside mitochondria in germ plasm of Drosophila melanogaster. Science 260, 1521–4.CrossRefGoogle ScholarPubMed
Kobayashi, S., Amikura, R. & Okada, M. (1994). Localization of mitochondrial large rRNA in germinal granules and the consequent segregation of germ line. Int. J. Dev. Biol. 38, 193–9.Google ScholarPubMed
Kobayashi, S., Amikura, R. & Mukai, M. (1998). Localization of mitochondrial large ribosomal RNA in germ plasm of Xenopus embryos. Curr. Biol. 8, 1117–20.CrossRefGoogle ScholarPubMed
Mahowald, A.P. (1962). Fine structure of pole cells and polar granules in Drosophila melanogaster. J. Exp. Zool. 151, 201–5.CrossRefGoogle Scholar
Mahowald, A.P. (1977). The germ plasm of Drosophila: an experimental system for the analysis of determination. Am. Zool. 17, 551–63.CrossRefGoogle Scholar
Matova, N. & Cooley, L. (2001). Comparative aspects of animal oogenesis. Dev. Biol. 231, 291–320.CrossRefGoogle ScholarPubMed
Matsui, Y. & Okamura, D. (2005). Mechanisms of germ-cell specification in mouse embryos, BioEssays 27, 136–43.CrossRefGoogle ScholarPubMed
McLaren, A. (2003). Primordial germ cells in the mouse. Dev. Biol. 262, 1–15.CrossRefGoogle ScholarPubMed
Ninomiya, Y. & Ichinose, S. (2007). Subcellular distribution of mitochondrial ribosomal RNA in the mouse oocyte and zygote. PLoS One 2, e1241.CrossRefGoogle ScholarPubMed
Noce, T., Okamoto-Ito, S. & Tsunekawa, N. (2001). Vasa homolog genes in mammalian germ cell development. Cell Struct. Funct. 26, 131–6.CrossRefGoogle ScholarPubMed
Ogawa, M., Amikura, R., Akasaka, K., Kinoshita, T., Kobayashi, S. & Shimada, H. (1999). Asymmetrical distribution of mitochondrial rRNA into small micromeres of sea urchin embryos. Zool. Sci. (Tokyo) 16, 445–51.CrossRefGoogle Scholar
Onohara, Y., Fujiwara, T., Yasukochi, T., Himeno, M. & Yokota, S. (2010). Localization of mouse vasa homolog protein in chromatoid body and related nuage structures of mammalian spermatogenic cells during spermatogenesis. Histochem. Cell Biol. 33, 627–39.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Reunov, A.A. (2004). Is there a germ plasm in mouse oocytes? Zygote 12, 329–32.CrossRefGoogle Scholar
Reunov, A.A. (2006). Structures related to the germ plasm in mouse. Zygote 14, 231–8.CrossRefGoogle Scholar
Saffman, E.E. & Lasko, P. (1999). Germline development in vertebrates and invertebrates. Cell. Mol. Life Sci. 55, 1141–63.CrossRefGoogle ScholarPubMed
Seydoux, G. & Braun, R.E. (2006). Pathway to totipotency: lessons from germ cells. Cell 127, 891–904.CrossRefGoogle ScholarPubMed
Snow, M.H.L. & Monk, M. (1983). Emergence and migration of mouse primordial germ cells. In Current Problems in Germ Cell Differentiation (eds McLaren, A. & Wylie, C.C.), pp. 115–35. Cambridge: Cambridge University Press.Google Scholar
Strome, S. & Wood, W.B. (1982). Immunofluorescence visualization of germ-line specific granules cytoplasmic granules in embryos, larvae and adults of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 79, 1558–62.CrossRefGoogle ScholarPubMed
Strome, S. & Wood, W.B. (1983). Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell 35, 11–25.CrossRefGoogle ScholarPubMed
Thomson, T. & Lasko, P. (2005). Tudor and its domains: germ cell formation from a Tudor perspective. Cell Res. 15, 281–91.CrossRefGoogle ScholarPubMed
Toyooka, Y., Tsunekawa, N., Takahashi, Y., Matsui, Y., Satoh, M. & Noce, T. (2000). Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech. Dev. 93, 139–49.CrossRefGoogle ScholarPubMed
Watanabe, M., Itoh, K., Abe, K., Akizawa, T., Ikenishi, K. & Furusawa, M. (1992). Immuno- Localization of DEAD family proteins in germ line cells of Xenopus embryos. Dev. Growth Differ. 34, 223–31.CrossRefGoogle ScholarPubMed
Wilk, K., Bilinski, S., Dougherty, M.T. & Kloc, M. (2004). 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.CrossRefGoogle Scholar
Williamson, A. & Lehmann, R. (1996). Germ cell development in Drosophila. Annu. Rev. Cell Dev. Biol. 12, 365–91.CrossRefGoogle ScholarPubMed
Wolf, P.M., Priess, J. & Hirsh, D. (1983). Segregation of germline granules in early embryos of Caenorhabditis elegans. An electron microscopic analysis. J. Embryol. Exp. Morphol. 73, 297–306.Google ScholarPubMed
Yoshimizu, T., Obinata, M. & Matsui, Y. (2001). Stage-specific tissue and cell interactions play key roles in mouse germ cell specification. Development 128, 481–90.CrossRefGoogle ScholarPubMed