Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-17T19:48:11.979Z Has data issue: false hasContentIssue false
  • English
  • Français

Pre-meiotic transformation of germplasm-related structures during male gamete differentiation in Xenopus laevis

Published online by Cambridge University Press:  16 December 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: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

To highlight the ultrastructural features of transformation occurring with germplasm-related structures (GPRS), the spermatogenic cells of Xenopus laevis were studied by transmission electron microscopy and quantitative analysis. It was determined that in spermatogonia and spermatocytes, the compact germinal granules underwent fragmentation into particles comparable with inter-mitochondrial cement (IMC). Fragments of IMC agglutinated some cell mitochondria and resulted in the creation of mitochondrial clusters. Clustered mitochondria responded with loss of their membranes that occurred by the twisting of membranous protrusions around themselves until multi-layered membranes were formed. The mitochondrial affinity of multi-layered membranes was proven by an immunopositive test for mitochondrial dihydrolipoamide acetyltransferase. As a consequence of mitochondrial membrane twisting, the naked mitochondrial cores appeared and presumably underwent dispersion, which is the terminal stage of GPRS transformation. As no GPRS were observed in spermatids and sperm, it was assumed that these structures are functionally assigned to early stages of meiotic differentiation.

Keywords

Germinal granulesInter-mitochondrial cementMitochondriaSpermatogenesisXenopus laevis
Type
Research Article
Information
Zygote , Volume 24 , Issue 1 , February 2016 , pp. 42 - 47
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.Google Scholar
Amikura, R., Sato, K. & Kobayashi, S. (2005). Role of mitochondrial ribosome-dependent translation in germline formation in Drosophila embryos. Mech. Develop. 122, 1087–93.Google Scholar
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.Google Scholar
Chuma, S., Hosokawa, M., Tanaka, T. & Nakatsuji, N. (2009). Ultrastructural characterization of spermatogenesis and its evolutionary conservation in the germline: germinal granules in mammals. Mol. Cell. Endocrinol. 306, 17–23.Google Scholar
Denegre, J.M., Ludwig, E.R. & Mowry, K.L. (1997). Localized maternal proteins in Xenopus revealed by subtractive immunization. Dev. Biol. 192, 446–54.Google Scholar
Eddy, E.M. (1975). Germ plasm and the differentiation of the germ cell line. Int. Rev. Cytol. 43, 229–80.Google Scholar
Gur, Y. & Breitbart, H. (2006). Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes. Genes Dev. 20, 411–6.Google Scholar
Gur, Y. & Breitbart, H. (2008). Protein synthesis in sperm: dialog between mitochondria and cytoplasm. Mol. Cell. Endocrinol. 282, 45–55.Google Scholar
Hecht, N.B. (1998). Molecular mechanisms of male germ cell differentiation. BioAssay 20, 555–61.Google Scholar
Ikenishi, K. (1998). Germ plasm in Caenorhabditis elegans, Drosophila and Xenopus. Dev . Growth Differ. 40, 1–10.Google Scholar
Kalt, M.R. (1973). Ultrastructural observations on the germ line of Xenopus laevis. Z. Zellforsch. 138, 41–62.Google Scholar
Kerr, J.B. & Dixon, K.E. (1974). An ultrastructural study of germ plasm in spermatogenesis of Xenopus laevis . J. Embryol. Exp. Morph. 32, 573–92.Google Scholar
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.Google 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.Google Scholar
Mahowald, A.P. (1977). The germ plasm of Drosophila: An experimental system for the analysis of determination. Am. Zool. 17, 551–63.Google Scholar
Matova, N. & Cooley, L. (2001). Comparative aspects of animal oogenesis. Dev. Biol. 231, 291–320.Google Scholar
Reunov, A.A. (2006). Structures related to the germ plasm in mouse. Zygote 14, 231–8.Google Scholar
Reunov, A.A. (2013). Premeiotic transformation of germ plasm-related structures during the sea urchin spermatogenesis. Zygote 27, 95–101.Google Scholar
Reunov, A.A., Isaeva, V.V., Au, D.W.T. & Wu, R.S.S. (2000). Nuage constituents arising from mitochondria: is it possible? Dev. Growth Differ. 42, 139–43.Google Scholar
Saffman, E.E. & Lasko, P. (1999). Germline development in vertebrates and invertebrates. Cell Mol. Life Sci. 55, 1141–63.CrossRefGoogle ScholarPubMed
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.Google Scholar
Thomson, T. & Lasko, P. (2005). Tudor and its domains: germ cell formation from a Tudor perspective. Cell Res. 15, 281–91.Google Scholar
Villegas, J., Araya, P., Bustos-Obregon, E. & Burzio, L.O. (2002). Localization of the 16S mitochondrial rRNA in the nucleus of mammalian spermatogenic cells. Mol. Hum. Reprod. 8, 977–83.Google Scholar
Volodina, N., Denegre, J.M. & Mowry, K.L. (2003). Apparent mitochondrial asymmetry in Xenopus eggs. Dev. Dynam. 226, 654–62.Google Scholar